Surgical Neuroangiography: Vol. 3: Clinical and Interventional Aspects in Children (Surgical Neuroangiography)

Surgical Neuroangiography 3

The complete three-volume set consists of Volume 1

Clinical Vascular Anatomy and Variations Volume 2

Clinical and Endovascular Treatment Aspects in Adults Volume 3

Clinical and Interventional Aspects in Children

Surgical Neuroangiography

P. Lasjaunias K. G. ter Brugge A. Berenstein

3

Clinical and Interventional Aspects in Children

Second Edition With 865 Figures in 2277 Separate Illustrations and 102 Tables

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Pierre Lasjaunias, M.D., Ph.D. Professeur des Universités en Anatomie Chef de Service de Neuroradiologie Diagnostique et Thérapeutique Centre Hospitalier Universitaire de Bicêtre 78, rue du Général Leclerc, 94275 Le Kremlin Bicêtre, France Karel G. ter Brugge, M.D., FRCPC The David Braley and Nancy Gordon Chair in Interventional Neuroradiology University of Toronto Head, Division of Neuroradiology Toronto Western Hospital, UHN 399 Bathurst St., 3MCL – 434,Toronto, ON M5T 2S8, Canada Alejandro Berenstein, M.D. Professor of Radiology and Neurosurgery Albert Einstein School of Medicine, NY Director of the Hyman-Newman Institute of Neurology and Neurosurgery, and of The Center for Endovascular Surgery Roosevelt Hospital Medical Center 1000 10th Ave. 10 G, New York, NY 10019, USA

ISBN 10 3-540-41681-1 Springer Berlin Heidelberg New York ISBN 13 978-3-540-41681-4 Springer Berlin Heidelberg New York Library of Congress Control Number: 00049688 This work is subject to copyright. All rights reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilm or in any other way, and storage in databanks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September, 9, 1965, in its current version, and permission for use must always be obtained from Springer-Verlag.Violations are liable for prosecution under the German Copyright Law. Springer is a part of Springer Science+Business Media springer.com © Springer-Verlag Berlin Heidelberg 1997, 2006 The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and there forefree for general use. Productliability: The publisher cannot guarantee the accuracy of any information about dosage and application contained in this book. In every individual case the user must check such information by consulting the relevant literature. Editor: Dr. Ute Heilmann, Heidelberg Desk Editor: Dörthe Mennecke-Bühler, Heidelberg Production: LE-TeX Jelonek, Schmidt & Vöckler GbR, Leipzig Reproduction and Typesetting: AM-productions GmbH, Wiesloch Cover design: E. Kirchner, Heidelberg Printed on acid-free paper 21/3100/YL – 5 4 3 2 1 0

Preface to the Second Edition

This volume completes the 3-volume series of the second edition of “Surgical Neuroangiography”. In the first volume, functional vascular anatomy, collateral circulation and vascular variations affecting the brain and spinal cord were described in detail. The second volume dealt with neurovascular diseases in adults and their management by surgical neuroangiography. This third volume focuses on the management of vascular diseases affecting the brain, spinal cord, and head and neck areas in the pediatric age group. Twenty-seven years have elapsed since the original publication of the first part of volume 1,“The Craniofacial and Upper Cervical Arteries”, in 1979. Eighteen years later the first edition of the volume on “Vascular Diseases in Neonates, Infants and Children” was published, which documented our improved understanding and growing experience with the endovascular management of pediatric patients. Similar to our experience in adults, we were able to make significant discoveries in the pediatric population, allowing us to break down previously established obstacles, widen the scope of our specialty, and create new reference points. This in turn is likely to facilitate the evolution of new management strategies as it will stimulate the participation of experts with different clinical backgrounds. It took us 10 years to create the second edition of the 6 previously published books and convert them into 3 large volumes. These books are based on shared practices, thoughts, and doubts, rather than on a compromise between 3 different individuals. They demonstrate a common vision generated by 30 years of practice and commitment. Our different personal skills and knowledge were enhanced by the others’ visions and thoughts. These books are therefore not multi-author books but the reflection of 3 experiences integrated into a common larger one. Recognition of the specificities of pediatric diseases is particularly challenging. It reflects the degree of sophistication and maturation of a given society. The development of pediatric hospitals and pediatric neurosurgery in the second half of the twentieth century already signified this evolution. These 3 volumes are meant to constitute the theoretical background of modern management of neurovascular diseases in adults and children. Our desire to share and teach this experience started in the early 1980s with the New York University/Paris XI University joint courses, the ABC Courses that were started in Paris 15 years ago, and more recently the

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Perface

Toronto Course. Finally, this text corresponds to the Syllabus of the present Masters Degree in Neurovascular Diseases, jointly created by the Paris XI and Mahidol Universities, taught in Asia and open to students from all over the world. However, our task has not been finished yet. As new frontiers keep appearing, they allow new fields to be explored and new teaching challenges to be resolved. We believe that these 3 volumes will contribute to an improved understanding of neurovascular disorders and that they represent a solid foundation upon which the development of new approaches of treatment can be based. October 2006

Pierre Lasjaunias, Karel ter Brugge, Alex Berenstein

We wish to thank our colleagues from the pediatric ICUs, Pediatric Neurology, Neurosurgery and Maxillofacial Surgery, and their teams without whom we could not have accomplished this work. Our particular thanks go to: Prof. Denis De Victor Dr. Philippe Durand Dr. Laurent Chevret Prof. Marc Tardieu Prof. Pierre Landrieu Prof. Michel Zerah Prof. Marc Tadié Prof. Marie Paule Vazquez Prof. Dan Benhamou Prof. Jacques Duranteau Prof. Fred Epstein* (*deceased) Prof. Mark Persky Prof. Milton Waner Prof. Mark Kupersmith Dr. Peter Dirks Dr. Derek Armstrong Dr. Gabrielle deVeber

Preface to the First Edition

This volume on vascular diseases in neonates, infants and children represents the fruit of our labour and experience in interventional neuroradiology in children that started in 1975, and now accounting for 30% of the activity in our unit at Bicêtre in Paris. The competence and support of the anaesthesia, paediatric intensive care, and paediatric neurology departments in Bicêtre have been key factors in our development, and their specific contributions are included in these pages. Through collaboration, I have learned that “multidisciplinary approach” is not just a turn of phrase, but rather the way adults who respect one another share information, and I have also learned that children are not small adults. I am especially indebted to Karel ter Brugge, to whom I owe the development, in 1984, of my paediatric interventional practice. Over the past 15 years, beyond our friendship, our practical and academic collaboration has never ceased. It is reflected in this book: not only did Karel edit the whole of this work, he also wrote the core of the chapter on aneurysms (with Jehad Al-Watban) as well as the chapter on cerebral arterial ischaemia (with Guillaume Sebire). Throughout the years, encouragement from the neurosurgeons has been precious. I also particularly appreciate the continuous support of A. Raimondi, who in Child’s Nervous System provided us with a forum to publish our material. Because vascular diseases are rare in neonates, infants and children and geographically dispersed, the international neuroradiology network that we have created has been very beneficial. The greater part of the information used in this volume was contributed via this network. This is not, then, a multi-author book, but rather the result of observations converging at various intervention sites: Toronto (Karel ter Brugge), Lisbon (Augusto Goulao), London (Wendy Taylor), Berlin (Jörg Meisel and Christian Koch), Singapore (Robert Kwok), Riyadh (Jehad Al-Watban), Bangkok (Sirintara Pongpech and Suthisak Suthipongchai), Stockholm (Michael Soderman), Cape Town (Steve Beningfield), and Bicêtre, Paris (Georges Rodesch and Hortensia Alvarez). Is a book the best means of communicating or sharing experience? Textbooks are only seldom quoted and often hardly read. Until recently, a written work was a synonym for book, but nowadays it may also appear on the computer screen. Although it may seem archaic - technically speaking - when compared to electronic publications, a book appeals to more of the senses and its content is more likely to be remembered. It must, however, choose between having its own style, and thus being controversial, or becoming sterile, politically correct, and consensual. No

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doubt books of the latter kind will become an endangered species, for they lose the elements of human imperfection and coherence. Most of those we have trained at Bicêtre or elsewhere have contributed to our analysis of paediatric vascular pathologies, and their work has usually been published. All or part of this material has been grouped within the corresponding chapters: – Aneurysmal malformations of the vein of Galen: Ricardo GarciaMonaco (Buenos Aires), Hortensia Alvarez, Michel Zerah (Paris), Nadine Girard (Marseille), Soichi Inagawa (Hamamatsu), Jehad Al-Watban, Maria Moersdorf (Trier), and Dominique Fournier (Angers) – Pial arteriovenous malformations: Hortensia Alvarez, Yuo Iizuka (Tokyo), and Robert Willinsky (Toronto) – Dural arteriovenous shunts: Ronie Piske (Sao Paulo), Augusto Goulao, Jean de Villiers, Francis Hui (Singapore), Georges Magufis (Athens), Wendy Taylor, and Robert Kwok – Venous ischaemia: Michael Soderman – Venous malformations and abnormalities: R. Piske, Karel ter Brugge, Jörg Meisel, and Philippe Pruvost (Bicêtre) – Traumatisms and epistaxis: Suthisak Suthipongchai (Bangkok) and Hortensia Alvarez – Para-notochordal fistulas: Georges Rodesch and Marco Trosselo Pastore (Bologna) – Spinal cord: Georges Rodesch As for the chapters on maxillofacial malformations and facial haemangiomas, Patricia Burrows (currently in Boston) contributed an essential part of the content. In the last chapter, finally, we are privileged to be able to reproduce work of very high quality: a part of Jeanne-Claudie Larroche’s (Paris) foetal pathology atlas, meningeal spaces anatomy studied by Roy O. Weller (Southampton), meningeal vascularisation in the foetus by Claude Maillot and Pierre Kherli (Strasbourg), and a perinatal cerebral myelinisation MRI atlas by Nadine Girard. In agreement with Alex Berenstein, with whom all five volumes of Surgical Neuroangiography were published from 1986 to 1992, certain of the cases presented in volumes 2,3 and 5 have been used again here, completed by follow-up X-rays taken nearly 10 years after embolisation in some cases. Accent has been put on the clinical experience acquired. Whenever the benefit of therapeutic hindsight was pertinent and the number of patients sufficient, the resulting figures were given. As it was impossible for this work to be exhaustive, we do not make any such claims. More often than not, we present our cases in terms of global care, whether lesions were embolised or not. Arterial and venous ischaemia are thus discussed in this volume, too, to reflect their clinical significance in a practice such as ours.Technique has thus been relegated to a position of secondary importance, which justifies the title of this work. In Vascular Diseases in Neonates, Infants and Children, rarely is the disease itself presented but rather its consequences. The morphological approach in vascular pathology is actually blatantly inadequate. Our knowledge of vascular diseases today is about equivalent to that of infectious

Preface

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diseases at the end of the eighteenth century: an abscess or a pleural effusion could be drained, just as we can obstruct a vascular malformation or an aneurysm; however, the causes and remedies remain to be found for affected vessels just as infectious agents and antibiotics did for an abscess or pleurisy then. Notions far removed from the usual preoccupations of a diagnostic and therapeutic neuroradiologist have been introduced: for example, the postnatal nature (as opposed to the congenital nature) of cerebral arteriovenous malformations, angiogenesis, vascular disease genetics, apoptosis, and vascular remodelling. The complete excision of a vascular lesion in a child often proves to be very mutilating and the long-term burden of handicap and dependence too heavy to bear. Hence, our intuition that partial treatment is valid has been confirmed.Whereas initially it resulted from failure to do better, it is now a therapeutic goal in itself - and sometimes the only acceptable one. These disorders are not necessarily treated to obliterate the image of the vascular lesion, but rather to correct the underlying causes of failure of the natural repairing systems. Vascular remodelling and the restoration of normal maturation processes complement endovascular treatments. Many interpretations of the facts have been offered. They illustrate the logical decision-making pathway we had to construct so as to make sound and reproducible decisions. It is this logic that has cemented our experience and grounded our teaching. The logic we use, though it appears to many to be a working hypothesis, is necessary when communicating with parents and children. Trusting relationships with children differ from those which can be established with adults. Trust is not won with eloquence, false seduction or pontificating certitudes. It is not difficult to gain, but it is the result of a simple relationship, free of deception or worries. Children are not usually afraid and are actually extraordinarily brave, in the adult sense of the term. They do not love the doctor; they simply trust him. January 1997

Pierre Lasjaunias

To Dr. Yvette Viallard Physician in Yemen

Pour le sillon qu’elle a tracé.

Contents

1

Embryological and Anatomical Introduction . . . .

1

1.1

Preliminary Remarks . . . . . . . . . . . . . . . . . . . .

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1.2

Leptomeninges

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1.3 1.3.1 1.3.2 1.3.3 1.3.3.1 1.3.3.2

Subpial Space . . . . . . . . . . . Anatomy . . . . . . . . . . . . . . Relationships of the Subpial Space Pathology . . . . . . . . . . . . . Inflammation . . . . . . . . . . . Tumors . . . . . . . . . . . . . . .

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22 22 23 23 23 24

2

Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts . . . .

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2.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . .

28

2.2

From Adults to Children . . . . . . . . . . . . . . . . . .

28

Vascular Lesion Types and Disease Groups . . . . . . . . Nonproliferative Lesions . . . . . . . . . . . . . . . . . . Arteriovenous Lesions . . . . . . . . . . . . . . . . . . . Isolated Brain AVMs . . . . . . . . . . . . . . . . . . . . Cerebral Arteriovenous Fistulas . . . . . . . . . . . . . . Vein of Galen Aneurysmal Malformations . . . . . . . . Cerebrofacial Arteriovenous Metameric Syndromes . . . Dural Lesions . . . . . . . . . . . . . . . . . . . . . . . . Telangiectasias . . . . . . . . . . . . . . . . . . . . . . . The Blue Rubber-Bleb Nevus or Bean Syndrome . . . . . Venous Malformations (Cavernomas) . . . . . . . . . . Venous Angiomas or Developmental Venous Anomalies Cerebrofacial Venous Metameric Syndrome (Sturge-Weber Syndrome) . . . . . . . . . . . . . . . . . 2.3.1.12 Induced Pial Shunts . . . . . . . . . . . . . . . . . . . . . 2.3.1.13 Spinal Cord AVM . . . . . . . . . . . . . . . . . . . . . . 2.3.1.14 General Conclusions on Vascular Lesions . . . . . . . . . 2.3.2 Proliferative Lesions . . . . . . . . . . . . . . . . . . . . 2.3.2.1 PHACE or PHACES . . . . . . . . . . . . . . . . . . . . . 2.3.2.2 Diffuse Angiodysplasia . . . . . . . . . . . . . . . . . . .

31 34 34 35 39 39 39 41 41 41 44 45

2.3 2.3.1 2.3.1.1 2.3.1.2 2.3.1.3 2.3.1.4 2.3.1.5 2.3.1.6 2.3.1.7 2.3.1.8 2.3.1.9 2.3.1.10 2.3.1.11

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47 47 48 48 49 51 51

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2.4 2.4.1 2.4.2 2.4.3 2.4.4

Classification of CAVMs by Age Group Fetal Age . . . . . . . . . . . . . . . . Neonatal Age . . . . . . . . . . . . . Infancy . . . . . . . . . . . . . . . . . After 2 Years . . . . . . . . . . . . . .

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2.5 2.5.1 2.5.2 2.5.3

Classification by Symptom Group . Congestive Cardiac Manifestations Hydrodynamic Disorders . . . . . Melting-Brain Syndrome . . . . . .

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63 63 64 73

2.6

Clinical Evaluation Scores . . . . . . . . . . . . . . . . .

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2.7

Revised Concept of the Congenital Nature of Vascular Malformations . . . . . . . . . . . . . . . 2.7.1 Genetics . . . . . . . . . . . . . . . . . . . . . . . . . 2.7.1.1 Familial Hemiplegic Migraine . . . . . . . . . . . . . 2.7.1.2 Familial Cerebral Aneurysms . . . . . . . . . . . . . 2.7.1.3 PKD1 and Bourneville PDK1-PDK2 . . . . . . . . . . 2.7.1.4 Ehlers-Danlos Type IV . . . . . . . . . . . . . . . . . 2.7.1.5 Multiple Cutaneous Mucous Venous Malformations, Blue Rubber Bleb Nevus Syndrome . . . . . . . . . . 2.7.1.6 CADASIL . . . . . . . . . . . . . . . . . . . . . . . . . 2.7.1.7 Familial Paragangliomas . . . . . . . . . . . . . . . . 2.7.1.8 Familial Cavernomas . . . . . . . . . . . . . . . . . . 2.7.1.9 Neurofibromatosis-1 and Other Collagen Diseases . 2.7.1.10 Hemorrhagic Hereditary Telangiectasia or Rendu-Osler-Weber Disease . . . . . . . . . . . . 2.8

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2.8.4 2.8.5

Vascular Remodeling and the Congenital Nature of Arteriovenous Shunts . . . . . . . . . . . . . . . . . . Endothelium as a Sensor and Transducer of Signals . . . Endothelium-Specific Receptor-Coupled Event . . . . . Endothelium and Mediator-Effector Molecules Involved with Remodeling . . . . . . . . . . . . . . . . . . . . . . Role of Matrix Modulators in Vascular Remodeling . . . Clinical Implications of Vascular Remodeling . . . . . .

3

Vein of Galen Aneurysmal Malformation . . . . . . 105

3.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 106

3.2 3.2.1 3.2.2

Historical Landmarks . . . . . . . . . . . . . . . . . . . 107 Lesions . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107 Clinical Aspects . . . . . . . . . . . . . . . . . . . . . . . 107

3.3

Modern Concept of Vein of Galen Aneurysmal Malformation

2.8.1 2.8.2 2.8.3

93 94 95 95 95 95

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3.4

Vein of Galen Aneurysmal Dilatation . . . . . . . . . . . 112

3.5

Dural Arteriovenous Shunts with Aneurysmal Dilatation of the Vein of Galen

3.6

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Vein of Galen Varix . . . . . . . . . . . . . . . . . . . . . 117

Contents

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3.7

Vein of Galen Aneurysmal Malformation . . . . . . . . . 117

3.8

Natural History of Vein of Galen Aneurysmal Malformation

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3.9

Cardiac Manifestations . . . . . . . . . . . . . . . . . . . 143

3.10

Macrocrania and Hydrocephalus . . . . . . . . . . . . . 152

3.11

Late Natural History of Vein of Galen Aneurysmal Malformation with Patent Sinuses

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3.12

Dural Sinus Occlusion and Supratentorial Pial Congestion and Reflux . . . . . 167

3.13 3.13.1

Dural Sinus Thrombosis and Infratentorial Pial Reflux . 180 Spontaneous Thrombosis . . . . . . . . . . . . . . . . . 184

3.14 3.14.1 3.14.2 3.14.2.1 3.14.2.2 3.14.3

Objectives and Methods of Treatment General Remarks . . . . . . . . . . . Neonates . . . . . . . . . . . . . . . . Reducing Oxygen Consumption . . . Improving Oxygen Delivery . . . . . Infants and Children . . . . . . . . .

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191 191 191 197 197 200

3.15 3.15.1 3.15.2 3.15.3 3.15.4 3.15.5

Technical Management . . . . . . . . General Remarks . . . . . . . . . . . Follow-Up . . . . . . . . . . . . . . . Complications: Morbidity . . . . . . Overall Mortality . . . . . . . . . . . Neurological Outcome by Age Group

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203 203 205 210 220 221

3.16 3.16.1 3.16.2 3.16.3

Other Techniques . . . Surgery . . . . . . . . . Transvenous Treatment Radiosurgery . . . . .

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221 221 223 224

4

Cerebral Arteriovenous Fistulas . . . . . . . . . . . . 227

4.1

Definitions and Anatomic Spaces . . . . . . . . . . . . . 227

4.2 4.2.1 4.2.2

Angioarchitecture . . . . . . . . . . . . . . . . . . . . . . 228 Single CAVFs . . . . . . . . . . . . . . . . . . . . . . . . 228 Multiple CAVFs . . . . . . . . . . . . . . . . . . . . . . . 231

4.3 4.3.1 4.3.2

Associated Conditions . . . . . . . . . . . . . . . . . . . 236 Hereditary Hemorrhagic Telangiectasia . . . . . . . . . 236 Encephalocraniocutaneous Lipomatosis . . . . . . . . . 246

4.4 4.4.1

Presentation . . . . . . . . . . . . . . . . . . . . . . . . . 249 Natural History . . . . . . . . . . . . . . . . . . . . . . . 265

4.5

Management

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5

Cerebral Arteriovenous Malformations . . . . . . . 291

5.1

General Remarks . . . . . . . . . . . . . . . . . . . . . . 292

5.2 5.2.1

Angioarchitecture of Cerebral Arteriovenous Malformations . . . . . . . . . . . . . . . 298 Single Nidus Versus Multifocal Niduses . . . . . . . . . . 298

5.3

Conditions Associated with CAVMs . . . . . . . . . . . . 302

5.4 5.4.1 5.4.2 5.4.3 5.4.4 5.4.5

Conditions Mimicking CAVMs . . . . . False Pial Arteriovenous Malformations Perinidal Angiogenesis . . . . . . . . . Postischemic Luxury Perfusion . . . . Proliferative Angiopathy . . . . . . . . Induced Pial AV Shunts Secondary to Dural Sinus High-Flow Lesions . . .

5.5 5.5.1 5.5.2 5.5.3 5.5.4 5.5.5 5.5.6 5.5.7

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306 306 306 306 306

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Angioarchitectural Progression of CAVMs in Children Venous Angiopathy . . . . . . . . . . . . . . . . . . . Dural Sinus High Flow . . . . . . . . . . . . . . . . . Venous Ischemia and Thrombosis . . . . . . . . . . Venous Hemorrhage . . . . . . . . . . . . . . . . . . Venous Enlargement . . . . . . . . . . . . . . . . . . Arterial Angiopathy . . . . . . . . . . . . . . . . . . . Spontaneous Thrombosis of Arteriovenous Malformations . . . . . . . . . . .

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311 311 312 315 316 321 324

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5.6 5.6.1 5.6.2 5.6.3 5.6.3.1 5.6.3.2 5.6.4 5.6.5

Objectives of Treatment . . . . . . . . Complete Exclusion . . . . . . . . . . . Partial Treatment . . . . . . . . . . . . Neonates and Infants . . . . . . . . . . Hydrodynamic Disorders . . . . . . . Multiple Arteriovenous Malformations Children . . . . . . . . . . . . . . . . . Rebleeding . . . . . . . . . . . . . . . .

5.7 5.7.1 5.7.2 5.7.2.1 5.7.2.2

Technical Management General Remarks . . . Other Techniques . . . Surgery . . . . . . . . . Radiation Therapy . .

6

Cerebrofacial Arteriovenous Metameric Syndrome

6.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 359

6.2 6.2.1

Clinical Manifestations . . . . . . . . . . . . . . Retinal AVMs and AVMs Along the Optic Nerve and Chiasm . . . . . . . . . . . . . . . . . . . . Retinal AVMs . . . . . . . . . . . . . . . . . . . Optic Nerve and Chiasmatic AVMs . . . . . . .

6.2.1.1 6.2.1.2

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Contents

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6.2.2 6.2.3 6.2.4

Cerebral AVMs . . . . . . . . . . . . . . . . . . . . . . . 376 Facial AVMs, Nasal AVMs, and Mandibular AVMs . . . . 382 Investigation for CAMS Patients . . . . . . . . . . . . . . 384

6.3

CAMS and Angiogenic Activity

7

Dural Arteriovenous Shunts . . . . . . . . . . . . . . 389

7.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 389

7.2 7.2.1 7.2.2

Classification . . . . . . . . . . . . . . . . . . . . . . . . 390 Age Groups . . . . . . . . . . . . . . . . . . . . . . . . . 392 Disease Groups . . . . . . . . . . . . . . . . . . . . . . . 392

7.3 7.3.1 7.3.1.1 7.3.2

Dural Sinus Malformations . . . . . . DSM with Giant Pouches . . . . . . . . Fetal and Postnatal Changes of Sinuses DSM of the Jugular Bulb . . . . . . . .

7.4

Infantile Dural Arteriovenous Shunts (AVS) . . . . . . . 436

7.5

Adult Type of Dural Arteriovenous Shunts in Children

7.6 7.6.1 7.6.2

Other Dural Shunts . . . . . . . . . . . . . . Vein of Galen Aneurysmal Malformation . . Dural Supply to Pial Cerebral Arteriovenous Malformations . . . . . . . . . . . . . . . . Proliferative Angiopathic Disease . . . . . . Systemic Disorders . . . . . . . . . . . . . . Recurrence in Intradural AVS and Secondary Transdural Supply . . . . . .

7.6.3 7.6.4 7.6.5

. . . . . . . . . . . . . . 384

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

396 398 398 434

. 444

. . . . . . . 447 . . . . . . . 447 . . . . . . . 447 . . . . . . . 448 . . . . . . . 448 . . . . . . . 449

7.7

General Remarks on Treatment . . . . . . . . . . . . . . 451

8

Venous Anomalies and Malformations . . . . . . . . 455

8.1 8.1.1 8.1.2 8.1.3

Developmental Venous Anomalies Single Abnormalities . . . . . . . Associated Features . . . . . . . . Associated Cavernomas . . . . .

8.2

Segmental and Nonsegmental Cerebro-orbito-facial Venous Lesions Sturge-Weber Syndrome . . . . . . . From SWS to Cerebrofacial Venous Metameric Syndrome . . . . Orbitofacial Venous Lesions . . . . .

8.2.1 8.2.2 8.2.3

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

455 455 459 473

. . . . . . . . . . . 478 . . . . . . . . . . . 478 . . . . . . . . . . . 485 . . . . . . . . . . . 496

8.3

Complex Pseudo-metameric Cerebrofacial Venous Syndrome . . . . . . . . . . . . . . . . . . . . . . 499

8.4 8.4.1 8.4.2 8.4.3

Blue Rubber Bleb Nevus (Bean Syndrome) The Association of BRBN with DVA . . . . Cerebral Venous Malformations in BRBN BRBN and HHT1 . . . . . . . . . . . . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

503 504 507 507

XVI

Contents

9

Craniopagus and Cranial Midline Epidural Venous Anomalies . . . . . . . . . . . . . . . 509

9.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 509

9.2

Postulated Relationships Between the Superior Sagittal Sinus and Adjacent Structures . . . 511

9.3

Ladan and Laleh’s Angiographic Anatomy . . . . . . . . 521

9.4

Technical Remarks and Functional Testing . . . . . . . . 531

9.5

Discussion on Surgical Management . . . . . . . . . . . 534

10

Cerebral Venous Thrombosis . . . . . . . . . . . . . . 537

10.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 537

10.2

Pathophysiology and Risk Factors . . . . . . . . . . . . . 539

10.3

Imaging . . . . . . . . . . . . . . . . . . . . . . . . . . . 545

10.4

Symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . 547

10.5

Treatment . . . . . . . . . . . . . . . . . . . . . . . . . . 556

10.6

Outcome . . . . . . . . . . . . . . . . . . . . . . . . . . . 557

11

Hemangiomas . . . . . . . . . . . . . . . . . . . . . . . 559

11.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 560

11.2

Pathogenesis . . . . . . . . . . . . . . . . . . . . . . . . . 562

11.3

Histological Findings . . . . . . . . . . . . . . . . . . . . 563

11.4

Clinical Presentation of Hemangiomas . . . . . . . . . . 564

11.5

Diagnosis

11.6

Complications in Hemangiomas

11.7

Management of Hemangiomas

11.8 11.8.1 11.8.2 11.8.3 11.8.4 11.8.5

Pharmacological Therapy of Hemangiomas Corticosteroids . . . . . . . . . . . . . . . . Interferon-Alpha 2a . . . . . . . . . . . . . . Vincristine . . . . . . . . . . . . . . . . . . . Aminocaproic Acid . . . . . . . . . . . . . . Other Treatments . . . . . . . . . . . . . . .

11.9

Laser Treatment of Hemangiomas

11.10 11.10.1 11.10.2

Endovascular Treatment of Hemangiomas . . . . . . . . 580 Arterial Embolization . . . . . . . . . . . . . . . . . . . 580 Intralesional Embolization . . . . . . . . . . . . . . . . . 582

11.11

Noninvoluting Capillary Hemangiomas

11.12

Subglottic Hemangiomas . . . . . . . . . . . . . . . . . . 588

11.13

Periorbital Hemangiomas . . . . . . . . . . . . . . . . . 590

. . . . . . . . . . . . . . . . . . . . . . . . . . 570 . . . . . . . . . . . . . 574 . . . . . . . . . . . . . . 577 . . . . . .

. . . . . .

. . . . . .

. . . . . .

. . . . . .

. . . . . .

. . . . . .

578 578 579 579 579 579

. . . . . . . . . . . . 580

. . . . . . . . . 585

Contents XVII

11.14

Oral Hemangiomas . . . . . . . . . . . . . . . . . . . . . 592

11.15

Salivary Gland Hemangioma

11.16

Bone Hemangiomas

11.17

Associated Anomalies . . . . . . . . . . . . . . . . . . . . 598

11.18

Psychological Impact . . . . . . . . . . . . . . . . . . . . 598

11.19

Kaposiform Hemangioendothelioma and Consumption Coagulopathy, the Kasabach-Merritt Syndrome Phenomena

. . . . . . . . . . . . . . . 592

. . . . . . . . . . . . . . . . . . . . 595

. . . . . . 602

12

PHACES . . . . . . . . . . . . . . . . . . . . . . . . . . . 607

12.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 607

12.2 12.2.1 12.2.2 12.2.3 12.2.4 12.2.5 12.2.6 12.2.7

Clinical Aspects . . . . . . . . . . . . . . . Posterior Fossa Abnormalities . . . . . . . Hemangiomas . . . . . . . . . . . . . . . . Arterial Anomalies . . . . . . . . . . . . . Coarctation and Congenital Heart Disease Eye Abnormalities . . . . . . . . . . . . . Sternal Cleft . . . . . . . . . . . . . . . . . Stenotic Arterial Disease . . . . . . . . . .

12.3

PHACES, a Congenital Malformation and a Proliferative Disease . . . . . . . . . . . . . . . . . 631

13

Cervicofacial Vascular Malformations . . . . . . . . 633

13.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 634

13.2

Traditionally Postulated Embryogenesis . . . . . . . . . 638

13.3

Diagnostic and Pretherapeutic Evaluation . . . . . . . . 640

13.4

Clinical Diagnosis of a Vascular Malformation

13.5 13.5.1 13.5.1.1 13.5.1.2 13.5.2 13.5.2.1 13.5.2.2 13.5.3

Arteriovenous Shunts . . . . . . . Soft Tissue AVMs . . . . . . . . . Intramuscular AVMs . . . . . . . Cutaneous AVMs . . . . . . . . . Intra-osseous AVMs . . . . . . . Mandibular and Maxillary AVMs Signs and Symptoms . . . . . . . Metameric Cerebrofacial AVMs .

13.6

Intra-osseous Slow-Flow Malformations . . . . . . . . . 659

13.7

Arteriolar-Capillary Malformations

13.8

Capillary Venous Malformations

13.9

Venous Vascular Malformations . . . . . . . . . . . . . . 660

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

609 611 618 622 623 627 627 627

. . . . . 640 . . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

. . . . . . . .

641 643 643 644 646 646 651 657

. . . . . . . . . . . 659

. . . . . . . . . . . . . 659

XVIII Contents

13.10

Complex Cerebrofacial Venous Syndromes (CVMS or Sturge-Weber Syndrome) . . . . . . . . . . . . 670

13.11

Lymphatic Malformations . . . . . . . . . . . . . . . . . 670

13.12

Mixed Vascular Malformations . . . . . . . . . . . . . . 681

13.13

Multifocal AVMs . . . . . . . . . . . . . . . . . . . . . . . 681

13.14 13.14.1 13.14.2

False Maxillofacial Vascular Malformations . . . . . . . 681 Idiopathic Facial Vascular (Venous) Dilatations . . . . . 681 Facial Venous Dilatation Associated with Intracranial Vascular Lesions . . . . . . . . . . . . . 685

14

Parachordal Arteriovenous Fistulas (Extracranial and Extraspinal Arteriovenous Fistulas) . . . . . . . 687

14.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 687

14.2

Specific Clinical Features . . . . . . . . . . . . . . . . . . 689

14.3

Topographic Approach . . . . . . . . . . . . . . . . . . . 696

14.4 14.4.1 14.4.2

Branchial Arteriovenous Shunts . . . . . . . . . . . . . . 696 Maxillary Artery/Vein Arteriovenous Fistulas . . . . . . 697 Ascending Pharyngeal-Internal Jugular Arteriovenous Fistulas . . . . . . . . . . . . . . . . . . . 699

14.5

Vertebro-vertebral Arteriovenous Fistulas . . . . . . . . 700

14.6

Paraspinal Arteriovenous Fistulas

14.7

Technical Management of High-Flow Fistulas . . . . . . 719

15

Spinal Cord Arteriovenous Malformations . . . . . 721

15.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 721

15.2

Classification

15.3

Natural History and Clinical Aspects . . . . . . . . . . . 737

15.4

Neonatal and Infants . . . . . . . . . . . . . . . . . . . . 737

15.5

Children Over 2 Years of Age . . . . . . . . . . . . . . . . 743

15.6

Diagnosis

15.7

Angioarchitecture . . . . . . . . . . . . . . . . . . . . . . 750

15.8 15.8.1 15.8.2 15.8.3

Treatment . . . . . . . . . . . Therapeutic Abstention . . . Embolization . . . . . . . . . Results . . . . . . . . . . . . .

. . . . . . . . . . . . 714

. . . . . . . . . . . . . . . . . . . . . . . . 722

. . . . . . . . . . . . . . . . . . . . . . . . . . 750 . . . .

. . . .

. . . .

. . . .

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. . . .

. . . .

. . . .

758 758 759 761

Contents

XIX

16

Vascular Trauma and Epistaxis . . . . . . . . . . . . . 767

16.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 767

16.2

Traumatic Carotid-Cavernous Fistulas . . . . . . . . . . 768

16.3

Post-traumatic Sinus Thrombosis . . . . . . . . . . . . . 776

16.4

Traumatic Dissections

16.5

Intracranial Arterial Aneurysms

16.6

Iatrogenic Injury . . . . . . . . . . . . . . . . . . . . . . 780

16.7

Traumatic Insult of Vascular Malformation

16.8

Epistaxis . . . . . . . . . . . . . . . . . . . . . . . . . . . 785

16.9

Technical Remarks

17

Intracranial Aneurysms in Children . . . . . . . . . 789

17.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 789

17.2

Incidence . . . . . . . . . . . . . . . . . . . . . . . . . . . 793

17.3

Presentation . . . . . . . . . . . . . . . . . . . . . . . . . 795

17.4

Etiology

17.5

Traumatic Aneurysms

17.6

Infectious Aneurysms . . . . . . . . . . . . . . . . . . . . 803

17.7

Saccular Aneurysms

17.8

Dissecting Aneurysms

17.9

Location . . . . . . . . . . . . . . . . . . . . . . . . . . . 835

17.10

Therapeutic Strategies . . . . . . . . . . . . . . . . . . . 836

18

Arterial Ischemic Stroke . . . . . . . . . . . . . . . . . 851

18.1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 851

18.2

Epidemiology . . . . . . . . . . . . . . . . . . . . . . . . 852

18.3

Pathophysiology . . . . . . . . . . . . . . . . . . . . . . . 852

18.4

Clinical Presentation . . . . . . . . . . . . . . . . . . . . 853

18.5

Imaging of Arterial Stroke in Children . . . . . . . . . . 856

18.6

Outcome and Prognosis

18.7

Etiology

18.8

Cardiac Disorders . . . . . . . . . . . . . . . . . . . . . . 867

18.9

Acute Regressive Cerebral Arteriopathy

18.10

Dissections . . . . . . . . . . . . . . . . . . . . . . . . . . 878

18.11

Moyamoya Disease . . . . . . . . . . . . . . . . . . . . . 885

. . . . . . . . . . . . . . . . . . . 777 . . . . . . . . . . . . . 779 . . . . . . . 783

. . . . . . . . . . . . . . . . . . . . . 787

. . . . . . . . . . . . . . . . . . . . . . . . . . . 797 . . . . . . . . . . . . . . . . . . . 798 . . . . . . . . . . . . . . . . . . . . 813 . . . . . . . . . . . . . . . . . . . 823

. . . . . . . . . . . . . . . . . . 860

. . . . . . . . . . . . . . . . . . . . . . . . . . . 866 . . . . . . . . . 870

XX

Contents

18.12

Hematological Disorders and Coagulopathies . . . . . . 892

18.13

Metabolic Disorders

18.14

Proliferative Angiopathy . . . . . . . . . . . . . . . . . . 893

18.15

PHACE . . . . . . . . . . . . . . . . . . . . . . . . . . . . 899

18.16

Hereditary Hemorrhagic Telangiectasia, or Rendu-Osler-Weber Disease . . . . . . . . . . . . . . . 899

18.17

Spinal Cord Strokes . . . . . . . . . . . . . . . . . . . . . 899

18.18

Treatment and Management . . . . . . . . . . . . . . . . 905

19

References . . . . . . . . . . . . . . . . . . . . . . . . . 909 Subject Index

. . . . . . . . . . . . . . . . . . . . 893

. . . . . . . . . . . . . . . . . . . . . . . 967

1 Embryological and Anatomical Introduction

1.1

Preliminary Remarks 1

1.2

Leptomeninges 21

1.3 1.3.1 1.3.2 1.3.3 1.3.3.1 1.3.3.2

Subpial Space 22 Anatomy 22 Relationships of the Subpial Space 23 Pathology 23 Inflammation 23 Tumor 24

1.1 Preliminary Remarks In this section we have collected illustrations that are relevant to the basic principles described in the various chapters of this book. Vascularization of dural covers in the fetus, particularly the venouslike channels, points to the role that they may play before granulation maturation. This rich vascularization contrasts with the rarity of true dural arteriovenous malformation in clinical practice. On the other hand, it may also constitute a reservoir for the sometimes dramatic response of the dural covers to angiogenic stimulation (Figs. 1.1, 1.2). C. Larroche and N. Girard have allowed us to reproduce some of their work; we have used fetal brain sections published by Larroche in an atlas that is no longer in print (Figs. 1.3–1.8) and magnetic resonance imaging (MRI) evaluation by Girard of myelinization in the perinatal period (Figs. 1.9–1.18). These pictures are not intended to formally establish what constitutes a normal appearance, but rather to help visualize the path that the myelinization process follows in neonates and infants. The subpial space has been extensively studied by various authors. Weller (1992; Nicholas and Weller 1988) has contributed to the better understanding of both the anatomy and the role of the subpial space. The following text and images illustrate this particular meningeal space (Figs. 1.19–1.25). An understanding of meningeal relationships in terms of the biology of the barrier that they constitute should explain why hemorrhage in one space gives rise to a spasm, but a few millimeters after a transpial passage the same vessel does not show a spastic reaction to the same abluminal stimuli. On the venous side, in neonates subpial congestion gives rise to multiple trophic changes, which are very mild if the congestion occurs only in the subarachnoid space. The responses to inflammatory diseases certainly account for the transdural contributions and indicate that several cellular proliferative reactions can cross this barrier very easily.

2

1 Embryological and Anatomical Introduction

Fig. 1.1A–F. Anatomic preparation of neonatal dural coverings. A Axial section showing the occipital lobe, the falx cerebri and the striate sinus. Note the multiple vascular spaces contained in the torcular region. B Higher horizontal section above the torcular showing the parietal suture and the superior sagittal sinus. Note the bilobed appearance of the superior sagittal sinus (see the sinus malformations illustrated in Chap. 4). Many vascular channels can be seen within the dura. C Horizontal section showing the straight sinus and the tentorium at the torcular level. Highly vascularized dural spaces can still be seen. D Vertical section demonstrating the straight sinus and two additional venous channels in the falx. The arachnoid covers can be clearly seen. E Parasagittal section showing the lateral sinus and the marginal sinus at the lower edge of the occipital bone. The cerebellum and the tentorium are easily recognizable. F Vertical section demonstrating a superior sagittal sinus in its mid-third portion. Multiple venous channels are seen surrounding the sinus itself. The arachnoid and pia mater can be clearly seen. v, Vascular spaces. (Courtesy of P. Kherli and C. Maillot, unpublished data). E–F see p. 3

Preliminary Remarks

3

Fig. 1.1 (continued). E Parasagittal section showing the lateral sinus and the marginal sinus at the lower edge of the occipital bone. The cerebellum and the tentorium are easily recognizable. F Vertical section demonstrating a superior sagittal sinus in its mid-third portion. Multiple venous channels are seen surrounding the sinus itself. The arachnoid and pia mater can be clearly seen. v, Vascular spaces. (Courtesy of P. Kherli and C. Maillot, unpublished data)

4

1 Embryological and Anatomical Introduction

Fig. 1.2A, B. Injected newborn specimen. A Medial face of the dural tentorium, demonstrating the arterial capillary network and a converging drainage in a perforating vein, joining the external surface of the dura mater (arrows). B Arterial capillary network on the tentorium cerebelli. The arrow points to the free margin of the tentorium. (Courtesy of C. Maillot, unpublished data)

Preliminary Remarks

5

Fig. 1.3. Fronto-oblique section passing through the frontal lobe and the olfactory nerve, the optic and infundibula recesses, the pons and trigeminal nerve, and the large fourth ventricle in a 13-week-old fetus. (Reprinted from Fess-Higgins and Larroche 1987, with permission)

Fig. 1.4A–F. A 40-g fetus. A Horizontal section for a gestational age of 12–13 weeks. The germinal matrix is well demonstrated. The choroid plexus fills the lateral ventricle entirely. B On the frontal section, the choroid plexus of the third ventricle can be clearly seen. A corpus callosum has not developed yet. C Mid-sagittal view. 1, Corpus callosum; 2, fornix; 3, lamina comissuralis; 4, olfactory bulb; 5, infundibulum; 6, mesencephalic aqueduct; 7, quadrigeminal plate; 8, fourth ventricle; 9, cerebellum. D Superior view. 1, Longitudinal fissure of the cerebrum; 2, cerebellum; 3, fourth ventricle; 4, medulla oblongata; 5, medulla spinalis. E Basal view. 1, Olfactory bulb; 2, optic chiasm; 3, infundibulum; 4, lateral fossa; 5, transverse fissure of the cerebrum; 6, pons; 7, cerebellum; 8, medulla oblongata; 9, medulla spinalis. F Lateral view. 1, Lateral fossa; 2, cerebellum; 3, medulla oblongata; 4, medulla spinalis. (Reprinted from Fess-Higgins and Larroche 1987, with permission) C–F see p. 6

6

1 Embryological and Anatomical Introduction

Fig. 1.4 C–F (continued). C Mid-sagittal view. 1, Corpus callosum; 2, fornix; 3, lamina comissuralis; 4, olfactory bulb; 5, infundibulum; 6, mesencephalic aqueduct; 7, quadrigeminal plate; 8, fourth ventricle; 9, cerebellum. D Superior view. 1, Longitudinal fissure of the cerebrum; 2, cerebellum; 3, fourth ventricle; 4, medulla oblongata; 5, medulla spinalis. E Basal view. 1, Olfactory bulb; 2, optic chiasm; 3, infundibulum; 4, lateral fossa; 5, transverse fissure of the cerebrum; 6, pons; 7, cerebellum; 8, medulla oblongata; 9, medulla spinalis. F Lateral view. 1, Lateral fossa; 2, cerebellum; 3, medulla oblongata; 4, medulla spinalis. (Reprinted from Fess-Higgins and Larroche 1987, with permission)

Fig. 1.5. A Frontal section of a 280-g fetus, 19–20 weeks of gestation. The deep nuclei are clearly demonstrated, in particular the thalamic and amygdaloid complex. B The trigeminal matrix and cells that have migrated toward the cortical surface can be clearly seen. (Reprinted from Fess-Higgins and Larroche 1987, with permission)

Preliminary Remarks

7

Fig. 1.6. A Axial and B frontal section of a 1,140-g embryo, 28 weeks of gestation, showing the development of the corpus callosum and the cortical layers. The matrix cannot be seen very well. The choroid plexus is reduced in size. Note the subarachnoid and pial spaces filled with small vessels. (Reprinted from Fess-Higgins and Larroche 1987, with permission)

Fig. 1.7. Mid-sagittal section of a 2,600-g embryo, 36 weeks of gestation, showing the choroid fissure. The same aspect is demonstrated Fig. 1.8. (Reprinted from Fess-Higgins and Larroche 1987, with permission)

8

1 Embryological and Anatomical Introduction

Fig. 1.8. Frontal view of 2,510-g embryo, 37 weeks of gestation. (Reprinted from Fess-Higgins and Larroche 1987, with permission)

Fig. 1.9A–C. Axial T1-weighted images (T1WI) in a 23-week-old fetus. C Axial T2-weighted image (T2WI) in a 21-week-old fetus. A The brain is agyric and the sylvian fissures are wide open, as they should be at this stage. The lateral ventricles are large; this feature corresponds to the relative hydrocephalus of the fetus. The cortical ribbon has a high signal, as do the germinal matrix and the migrant cells, which results in a multilayered pattern. High signal intensity is observed in the basal ganglia, corresponding to the high cellularity. B This is also the case in the posterior part of the brain stem as a result of myelination. C The cortical ribbon has low signal intensity on T2WI. (Courtesy of N. Girard)

Preliminary Remarks

9

Fig. 1.10A–H. Coronal T1-weighted images (T1WI) in a 29-week-old fetus. T2-weighted images (T2WI) in a 28-week-old fetus in C axial and D sagittal planes. E, G Axial T1WI and F, H axial T2WI of a 28-week-old premature newborn. A, B The cortical ribbon can still be seen as high signal intensity, while the migrant cells are no longer as visible. A, C The ventricles are now thinner than in Fig. 1.9. C The cortical ribbon can be seen as low signal intensity that is well delineated from the white matter and the subarachnoid spaces, which appear as high signal intensity. Moreover, early gyration can be seen and is better depicted on T2WI. The brain stem appears as B high signal intensity on T1WI and D low signal intensity on T2WI secondary to the completion of myelination. In the 28-week-old premature newborn, the cortical ribbon shows G high signal intensity on T1WI and H low signal intensity on T2WI E–H see p. 10

10

1 Embryological and Anatomical Introduction

Fig. 1.10E–H (continued). The posterior part of the pons looks mature, displaying E a high signal intensity on TlWI and F low signal intensity on T2WI. The internal capsules do not yet show any process of myelination, since they demonstrate G low signal intensity on T1WI and H high signal intensity on T2WI. The white matter appears as lower signal intensity on T2WI than on prenatal study (probably because the sequence used is different). (Courtesy of N. Girard)

Preliminary Remarks

11

Fig. 1.11. A Axial T1-weighted image (T1WI) in a 31-week-old fetus. B Axial T2weighted image (T2WI) in a 32-week-old fetus. High signal intensity can be seen on T1WI in the posterior limb of the right internal capsule, corresponding to the myelination process. A The hemispheric parenchyma appears homogeneous on T1WI. B It is easily recognizable on T2WI as high signal intensity. Note that the pons demonstrates low signal intensity on T2WI secondary to maturation. (Courtesy of N. Girard)

Fig. 1.12A, B. Axial T1-weighted images (T1WI) in a 35-week-old fetus. The ventricles are almost invisible, as are the subarachnoid spaces. The cortical ribbon is not well delineated from the subarachnoid spaces and the white matter on T1WI. B The optic radiations display a high signal intensity (clearly seen on the left side). A The central area also has high signal intensity. These features correspond to the developing process of myelination, since the so-called myelination gliosis has high signal intensity on T1WI. (Courtesy of N. Girard)

12

1 Embryological and Anatomical Introduction

Fig. 1.13. A–C Legend see p. 13

Preliminary Remarks

13

▲

Fig. 1.14. A Coronal T1-weighted image (T1WI) and B axial T2-weighted image (T2WI) in a 1-month-old child. A The optic radiations are not yet myelinated, since they show myelination gliosis only on T1WI as high signal intensity. B They appear as high signal intensity on T2WI. (Courtesy of N. Girard)

Fig. 1.13. A–C Axial T1-weighted images (T1WI), D–F axial T2-weighted images (T2WI) and G–I axial proton density-weighted images (PDWI) in a 3-week-old newborn. The posterior part of the pons shows high signal intensity on C T1WI and low signal intensity on F T2WI and (I) PDWI, corresponding to the complete maturation of the sensory pathways of the pons. The central area appears as high signal intensity on A T1WI and as low signal intensity on D T2WI and G PDWI; this results from the complete maturation of the central area. B, E, H This feature is also observed in the occipital area. On the other hand, at this stage the internal capsules only show myelination gliosis on B T1WI as high signal intensity, since it appears as high signal intensity on E T2WI and H PDWI. The internal capsules are difficult to delineate on T1WI only, since the basal ganglia also display high signal intensity on T1WI. The immature white matter shows low signal intensity on A–C T1WI and high signal intensity on D–F T2WI and G–I PDWI. Note also that the basal ganglia demonstrate high signal intensity on B T1WI and low signal intensity on D T2WI and H PDWI. (Courtesy of N. Girard)

14

1 Embryological and Anatomical Introduction

Fig. 1.15. A Axial T2-weighted image (T2WI), B proton density-weighted image (PDWI), and c axial T1-weighted image (T1WI) in a 2.5-month-old child. (The child in C is a different one from the one in A, B.) Myelination begins in the posterior limb of the internal capsules as low signal intensity on A T2WI and B PDWI. The optic radiations are not myelinated, since they show high signal intensity on both A T2WI and C T1WI. The immature white matter still appears as low signal intensity on T1WI and as high signal intensity on T2WI. (Courtesy of N. Girard)

Fig. 1.16. A–C Axial T2-weighted images (T2WI), D lateral T1-weighted image (T1WI), and E sagittal T1WI in a 4-month-old child. High signal intensity is observed on T1WI in the semioval center, the central area, the internal capsule, and the optic radiations. The deep white matter displays a similar signal as the cortex on T1WI and no longer has the low signal intensity seen in neonates. A On T2WI, myelination begins in the semioval center. B, C The internal capsules are entirely myelinated, as are the optic radiations, since they show low signal intensity on T2WI. On the other hand, the deep white matter is still unmyelinated on T2WI. D, E see p. 15

Preliminary Remarks

15

Fig. 1.16 (continued). E The corpus callosum shows high signal intensity on TlWl. C However, myelination is not complete on T2WI. (Courtesy of N. Girard)

Fig. 1.17A–C. Axial T2-weighted images (T2WI) in an 8-month-old child. A Myelination is complete in the semioval center. B It is also complete in the corpus callosum. C The optic radiations show complete myelination in their lower portion. The upper part is not fully myelinated. Note at this stage that the hemispheric parenchyma appears homogeneous, but the subcortical white matter fibers are not yet myelinated. (Courtesy of N. Girard)

16

1 Embryological and Anatomical Introduction

Fig. 1.18. A–C Axial T1-weighted images (T1WI) and D–F axial T2-weighted images (T2WI) in a 19-month-old child. The pattern is similar to that found in adults. The deep white matter, including the subcortical fiber tracts, appears as high signal intensity on T1WI and as low signal intensity on T2WI. (Courtesy of N. Girard)

Preliminary Remarks

Fig. 1.19. Relationships of the subpial space. (From Weller 1994)

17

18

1 Embryological and Anatomical Introduction

Fig. 1.20. The subpial space (sps) of the human cerebral cortex. The pia mater is at the top, and an artery surrounded by two or three layers of smooth muscle cells is seen in the center. A thin layer of pial cells (PC) surrounds the artery, enclosing its perivascular space. The subpial space separates the artery from the glia limitans (gl). Transmission electron micrograph (TEM), ¥5,000. (Reproduced from Zhang et al. 1990, with permission)

Fig. 1.21. The subpial space (higher magnification than Fig. 1.20). The pia mater is at the top, and the glia limitans at the bottom. Within the subpial space is a thin-walled vein filled with erythrocytes. Collagen bundles (coll) are distributed through the subpial space and dissociated leptomeningeal cells are also seen. A thin basement membrane coats the astrocyte processes of the glia limitans. Transmission electron micrograph (TEM), ¥6,700. (Reproduced from Alcolado et al. 1988, with permission)

Preliminary Remarks

19

FFig. 1.22. Collagen bundles within the spinal subpial space. Scanning electron micrograph (SEM), ¥1,000

Fig. 1.23A, B. The subpial space (sps) in inflammation. A The subarachnoid space (top) is filled with macrophages and dead polymorphonuclear leukocytes. Three vessels in the subarachnoid space have expanded perivascular spaces surrounded by black-stained reticulin fibers. In the center, the subpial space is expanded by inflammatory cells. Surface of the cerebral cortex (bottom). B Inflammatory cells fill the subpial space, separating the pia mater (p) from the glia limitans (gl). An artery is seen entering the cerebral cortex. Light microscopy, reticulin stain, ¥470. (Reproduced with permission from Hutchings and Weller 1986)

20

1 Embryological and Anatomical Introduction

Fig. 1.24. Subpial space: inflammation. Inflammatory cells (P, polymorphonuclear leukocyte; L, lymphocyte; M, monocyte/macrophage) enter the subarachnoid space or the subpial space from the veins (right) and are then distributed into the perivascular spaces of meningeal vessels. There is little penetration into the perivascular spaces of the brain

Fig. 1.25. Subpial space: tumors. Leukemic or primary cerebral lymphoma cells (L) enter the subarachnoid and subpial spaces from the vessels and form a dense reticulin network. Cells penetrate the brain either by direct invasion or along perivascular spaces. Carcinoma (Ca) and malignant melanoma cells may remain in the subarachnoid space or they may penetrate the subpial spaces and pass along perivascular spaces into the central nervous system. Carcinoma cells may also penetrate directly through the glia limitans into the brain

Leptomeninges

21

1.2 Leptomeninges MRI with gadolinium enhancement (Bradley and Bydder 1990) has proved to be of great value in detecting the two major pathologies of the leptomeninges, i.e., inflammation and invasion by neoplastic cells (Weller 1990). Meningeal enhancement has been reported in a number of different conditions, including tuberculous meningitis (Kioumehr et al. 1994), Lyme disease (Demaerel 1994), and primary meningeal lymphoma (Berciano et al. 1996); MRI appears to be more suitable than computed tomography (CT) for the identification of leptomeningeal metastases, particularly in the spinal cord (Chamberlain et al. 1990). Leptomeninges cover the surface of the brain and spinal cord as well as the nerve roots and blood vessels within the subarachnoid space (Weller 1995). The outer, arachnoid mater, is composed of multiple layers of leptomeningeal cells, which form an impermeable barrier to cerebrospinal fluid (Alcolado et al. 1988). Separating the arachnoid and pia mater is the subarachnoid space containing cerebrospinal fluid and major arteries and veins supplying the central nervous system. Delicate ligaments and perforated sheets of leptomeninges traverse the subarachnoid space, forming compartments filled with cerebrospinal fluid. Sheet-like and filiform trabeculae traversing the subarachnoid space are composed of bundles of collagen fibers and a thin outer coating of leptomeningeal cells (Weller 1995; Alcolado et al. 1988; Hutchings and Weller 1986). Blood vessels within the subarachnoid space are suspended by such trabeculae, which have a structure similar to the major dorsal and ventral ligaments of the spinal cord and the dentate ligaments (Nicholas and Weller 1988). The pia mater (Alcolado et al. 1988) is a delicate sheet, often only one cell thick; it is in contact with the surface of the brain, spinal cord, and nerve roots. Pia follows the gyri and sulci of the cerebral hemispheres and the folia of the cerebellum and closely invests the surface of the spinal cord. It is separated from the surface of the brain by the subpial pace and, as it is reflected onto the surface of blood vessels in the subarachnoid space, pia mater separates the subpial space from the subarachnoid space. Individual cells of the pia mater are joined by desmosomes and gap junctions (Alcolaclo et al. 1988; Spray et al. 1991), and they form a designated interface between the cerebrospinal fluid of the subarachnoid space and the surface of the brain (Feuer 1991). The pia mater appears to act as an active barrier, and its cells actively pinocytose particulate matter and contain enzymes such as catechol-O-methyl transferase (Kaplan 1981) and glutamine synthetase (Feuer 1991), which degrade neurotransmitters. Growth factors such as transforming growth factor b (TGFb) have also been identified in leptomeningeal cells (Johnson et al. 1992).

22

1 Embryological and Anatomical Introduction

1.3 Subpial Space 1.3.1 Anatomy

The anatomy of the subpial space is summarized in Fig. 1.19. The subpial space is normally difficult to discern with light microscopy and was not well recognized as a separate compartment until ultrastructural studies (Huntchings 1986) confirmed that it was bound on one side by a complete sheet of pia mater and on the other by the glia limitans (Alcolado et al. 1988; Huntchings and Weller 1986; Zhang et al. 1990). As shown in Fig. 1.19, the pia mater is reflected onto the surface of arteries and veins in the subarachnoid space and coats collagenous trabeculae extending from the arachnoid to the pia mater. A sheath of pia mater cells extends from the deep aspect of the pia mater proper to accompany arteries into the brain, but this sheath is either incomplete or absent around veins (Zhang et al. 1990). The perivascular space formed by this tube-like insertion of pia mater appears to be a major pathway for the drainage of interstitial fluid from the brain into the perivascular spaces of the leptomeningeal arteries and thence into the subarachnoid space (Weller et al. 1992). With the barrier and enzymatic properties of the pia mater mentioned above, the sheath of pia mater may also form a regulatory interface separating blood vessels and their nerve supplies from the surrounding brain tissue. The glia limitans is composed of compacted astrocyte processes, often joined by gap junctions (Peters and Feldman 1976). A basement membrane coats the astrocytic component of the glia limitans and separates it from the small collagen fibers that form a web-like matrix on the surface of the brain. Over the surface of the cerebral hemispheres, the subpial space largely contains arterioles (Fig. 1.20), small veins (Fig. 1.21) and bundles of collagen of varying size, dissociated pia mater cells, and occasional inflammatory cells. Bundles of collagen fibers extend from the trabeculae that cross the subarachnoid space and expand in a fan-like manner into the subpial space (Fig. 1.19), apparently forming an anchor for the trabecula (Alcolado et al. 1988). Similar anchorage is seen in the arachnoid mater (Weller 1995; Alcolado et al. 1988). Arterioles within the subpial space are fine branches of the major arteries in the subarachnoid space. They have smooth muscle coats of varying thickness and an outer coating of leptomeningeal (pia mater) cells. Small veins in the subpial space, on the other hand, are larger in diameter and have thin walls with few smooth muscle cells and no outer coating of pia mater cells. The subpial space of the spinal cord contains a thicker layer of collagen bundles (Nicholas and Weller 1988), as seen in the scanning electron micrograph in Fig. 1.22. This thick layer of collagen is continuous with the dentate ligaments laterally and may play a role in stabilizing the cord (Nicholas and Weller 1988). The nerve supply of the leptomeninges and the vessels in the subpial space has been mainly investigated at the level of the spinal cord in experimental animals. Innervation of the pia and leptomeningeal ligaments by

Inflammation

23

small sensory fibers appears to be derived from ventral roots (Risling et al. 1994; Parke and Whalen 1993), although this origin is disputed (Karlsson and Hildebrand 1993). Over the surface of the cerebral cortex, some blood vessels may be supplied by branches from cortical neurons (McKenzie 1990). Small nerve branches consisting of myelinated and nonmyelinated fibers can be identified within the spinal leptomeninges of the spinal cord in humans (Nicholas and Weller, unpublished observations).

1.3.2 Relationships of the Subpial Space

Although the subpial space is separated from the subarachnoid space by the pia mater, it is continuous with the perivascular spaces of the central nervous system. A sheath of pia mater surrounds the arteries as they enter the brain and divides the periarterial space into two compartments (Fig. 1.19). It is probably the inner space between the pia mater sheath and the vessel that is the conduit for fluid drainage (Weller 1992), but which of these spaces should be called the Virchow Robin space is unclear. The relationships of the subpial space are particularly important when considering pathological reactions within the space.

1.3.3 Pathology 1.3.3.1 Inflammation

Inflammatory leptomeningitis may be due to a number of different types of organisms or may even be due to the escape into the cerebrospinal fluid of sterile inflammatory agents, such as cholesterol or keratin, from epidermoid cysts or craniopharyngiomas. A variety of blood-borne cells may be associated with inflammation of the leptomeninges, and the time course and nature of the inflammation depend upon the stimulating agent (Weller 1990). Pyogenic bacterial infections, such as streptococcal or staphylococcal leptomeningitis, result in exudation of large numbers of polymorphonuclear leukocytes into the subarachnoid and subpial spaces. In the later stages of infection, when the polymorphonuclear leukocytes have ingested bacteria and died, macrophages derived from blood monocytes (Fig. 1.23) replace and ingest the dead polymorphs, dead bacteria, fibrin, and tissue debris. Macrophages generally arrive 2–3 days after the initial infection. The pattern of inflammation in viral meningitis is mainly that of lymphocyte exudation into the subarachnoid and subpial spaces; in fungal and tuberculous infections, there is granulomatous inflammation in addition to lymphocyte infiltration, often with multinucleate macrophagederived giant cells and areas of caseation (Weller 1990). The time course and intensity of breakdown of the blood–brain barrier is different in each of these cases. In purulent leptomeningitis, significant alteration in the blood-brain barrier may only last for a few days to

24

1 Embryological and Anatomical Introduction

1 week before the barrier is restored. In more chronic infections, such as tuberculosis, disruption of the blood-brain barrier may last much longer. Inflammatory cells, polymorphonuclear leukocytes, monocytes, or lymphocytes pass from the blood into either the subarachnoid space or the subpial space through the walls of veins (Fig. 1.24). Although in the rest of the body most of the traffic of inflammatory cells is through the walls of postcapillary venules, they escape from large veins into the subarachnoid space. Traffic of inflammatory cells through the walls of smaller veins in the subpial space may be an important route for cells to enter both the subpial and the subarachnoid spaces. Figure 1.24 shows how inflammatory cells entering the subpial space may be distributed along perivascular spaces of arteries and veins in the subarachnoid space and penetrate the pia mater (Krahn 1981) to enter the subpial space. By expanding the subpial space, the relationships between the pia mater and the glia limitans become clearer by light microscopy, and the presence of a leptomeningeal sheath around blood vessels in the subarachnoid space is clearly demonstrated (Fig. 1.23). Although there is a connection between the subpial space and perivascular spaces within the brain, inflammatory cells rarely extend far into the perivascular spaces of the central nervous system. It appears that the pia mater is an effective barrier to the spread of bacteria into the subpial space. The pia mater also forms a barrier to the spread of red blood cells from the subarachnoid space, and blood does not usually penetrate the perivascular spaces of the brain following subarachnoid hemorrhage (Hutchings and Weller 1986). Hemorrhage does occur in the subpial space, particularly in infants (Friede 1972). Subpial hemorrhage can be distinguished from subarachnoid hemorrhage, since subpial hemorrhage usually remains closely confined and spreads in the subpial space into sulci rather than filling the sulci, as occurs in subarachnoid hemorrhage.

1.3.3.2 Tumor

Breakdown of the blood-brain barrier and gadolinium enhancement is well recognized in association with poorly differentiated glial tumors, such as glioblastoma multiforme and anaplastic astrocytoma, as is the absence of a blood-brain barrier in association with solid metastatic carcinomas and primary lymphomas in the nervous system (Bradley and Bydder 1990). Enhancement due to breakdown of the blood-brain barrier also occurs in carcinomatous, lymphomatous, and leukemic meningitis and is well demonstrated by MRI (Berciano et al. 1996; Chamberlain et al. 1990). Neoplastic cells enter the subarachnoid and subpial spaces by penetrating blood vessel walls. However, leukemic and lymphoma cells show a different pattern of invasion from carcinomas. Although leukemic involvement of the central nervous system is common, it is usually only primary lymphomas of the central nervous system that invade the parenchyma of the brain and spinal cord (Weller 1990; Berciano et al. 1996).

Tumor

25

Leukemic and lymphoma cells in the subarachnoid and subpial spaces induce the formation of a delicate network of reticulin (small collagen; Fig. 1.25). From the subpial space, cells penetrate the glia limitans and invade the surface of the brain or penetrate deeply into the parenchyma along perivascular spaces (Fig. 1.25). Carcinomas and malignant melanoma, on the other hand, invade the subarachnoid space but may be prevented either by the pia or the glia limitans from directly invading the brain. Some carcinomas remain almost totally confined to the subarachnoid space with minimal invasion of the brain, whereas other carcinomas and malignant melanomas enter the subpial space and penetrate deep into the brain along perivascular spaces (Fig. 1.25). Direct invasion through the glia limitans is also seen in some carcinomas. Such invasion may increase the thickness of the zone of blood–brain barrier breakdown and thus enhancement on MRI. The mechanisms of blood–brain barrier breakdown in carcinomatous meningitis are not entirely clear. Once the carcinoma has entered the subpial and arachnoid spaces, it appears that the tumor cells continue to influence the characteristics of blood vessels in the region, as with solid metastases. Carcinoma cells are known to produce growth factors (Wiestler 1994), which may modify the permeability characteristics of the brain vessels in the region of leptomeningeal metastases. The significance of the subpial space lies mainly in the blood vessels that traverse it, in its proximity to the surface of the brain and in its connections with the perivascular spaces of the central nervous system. For the most part, inflammatory cells entering the subpial space pass into the subarachnoid space rather than into the brain. In many cases of leptomeningitis, there is only a microglial reaction in the surface regions of the brain rather than direct invasion by inflammatory cells. The picture is rather different in carcinomatous or lymphomatous meningitis, in which invasion of the surface of the brain is as common as invasion of the perivascular spaces.

2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

2.1

Introduction 28

2.2

From Adults to Children 28

2.3 2.3.1 2.3.1.1 2.3.1.2 2.3.1.3 2.3.1.4 2.3.1.5 2.3.1.6 2.3.1.7 2.3.1.8 2.3.1.9 2.3.1.10 2.3.1.11 2.3.1.12 2.3.1.13 2.3.1.14 2.3.2 2.3.2.1 2.3.2.2

Vascular Lesion Types and Disease Groups 31 Nonproliferative Lesions 34 Arteriovenous Lesions 34 Isolated Brain AVMs 35 CAVFs 39 VGAMs 39 Cerebrofacial Arteriovenous Metameric Syndromes 39 Dural Lesions 41 Telangiectasias 41 The Blue Rubber-Bleb Nevus or Bean Syndrome 41 Venous Malformations (Cavernomas) 44 Venous Angiomas or Developmental Venous Anomalies 45 Cerebrofacial Venous Metameric Syndrome (Formerly Sturge-Weber Syndrome) 47 Induced Pial Shunts 47 Spinal Cord AVM 48 General Conclusions on Vascular Lesions 48 Proliferative Lesions 49 PHACE or PHACES 51 Diffuse Angiodysplasia 51

2.4 2.4.1 2.4.2 2.4.3 2.4.4

Classification of CAVMs by Age Group 56 Fetal Age 56 Neonatal Age 59 Infancy 59 After 2 Years 62

2.5 2.5.1 2.5.2 2.5.3

Classification by Symptom Group 63 Congestive Cardiac Manifestations 63 Hydrodynamic Disorders 64 Melting-Brain Syndrome 73

2.6

Clinical Evaluation Scores 77

2.7

Revised Concept of the Congenital Nature of Vascular Malformations 85 Genetics 85 Familial Hemiplegic Migraine 85 Familial Cerebral Aneurysms 86 PKD1 and Bourneville PDK1-PDK2 86 Ehlers-Danlos Type IV 87 Multiple Cutaneous Mucous Venous Malformations, Blue Rubber Bleb Nevus Syndrome 87 CADASIL 87 Familial Paragangliomas 87 Familial Cavernomas 87 Neurofibromatosis-1 and Other Collagen Diseases 88 Hemorrhagic Hereditary Telangiectasia or Rendu-Osler-Weber Disease 88

2.7.1 2.7.1.1 2.7.1.2 2.7.1.3 2.7.1.4 2.7.1.5 2.7.1.6 2.7.1.7 2.7.1.8 2.7.1.9 2.7.1.10

28 2.8 2.8.1 2.8.2 2.8.3 2.8.4 2.8.5

2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts Vascular Remodeling and the Congenital Nature of Arteriovenous Shunts 93 Endothelium as a Sensor and Transducer of Signals 94 Endothelium-Specific Receptor-Coupled Event 95 Endothelium and Mediator-Effector Molecules Involved with Remodeling 95 Role of Matrix Modulators in Vascular Remodeling 95 Clinical Implications of Vascular Remodeling 95

2.1 Introduction Since 1982, more than 3,000 patients with cerebral arteriovenous malformations (CAVMs) have been referred to the three authors, including 800 children under the age of 16 years. Our active involvement in the management of vein of Galen aneurysmal malformations (VGAMs) started in 1984; since then, 350 children with VGAMs have been seen by the group in Bicêtre Hospital alone, where it accounts for 50% of total pediatric intradural intracranial AVS patients. More than 25 new VGAM patients are now referred to us each year. Over the past 20 years, these centers combined have collected about 500 VGAMs. In comparison, the two historically important series describing the surgical management of this disease show referral patterns of roughly one new patient with VGAM per year: the Hospital for Sick Children in Toronto (29 patients over 30 years) and the Royal Alexandra Hospital in Sydney (13 patients in 10 years). It is also of interest to note that in these surgical series, VGAM represented 34% of all the CAVM managed in children. A survey on the European continent (Raimondi 1992) showed that in the year 1989 in a population of 530 million people, 189 surgical procedures were performed for vascular disease in children, i.e., about one procedure a year per 3 million people. Most active neurosurgical centers in Europe perform between 10 and 15 procedures for this disease in children, which in most cases consists of cavernoma removal. In our interventional centers, 100–170 pediatric neurovascular procedures are performed each year, mostly AVMs. The large number of patients seen does not reflect a true population profile with any epidemiological significance, but rather our status as a quaternary referral center for Europe and North America. In view of the distances involved, only the more complex cases tend to be referred while the simpler ones are more likely managed locally. Our current practice and management reflects both the improvement in fetal and neonatal diagnosis and care of children with neurovascular disease as well as the progressive shift toward endovascular management in the treatment of children with brain AVSs.

2.2 From Adults to Children Cerebral arteriovenous (AV) shunts have different characteristics in children than in adults. Children can have multifocal lesions, induced remote AV shunts (Garcia Monaco 1991c; Iizuka 1992), large venous ectasias, highflow lesions, and single hole arteriovenous fistulas (Weon et al. 2005; Yoshi-

From Adults to Children

29

da et al. 2004), venous thrombosis, brain atrophy, and systemic phenomena (Cronqvist 1972; Cumming 1980; Willinsky et al. 1990a). Conversely, highflow angiopathic changes are rare in children, as are flow-related arterial aneurysms (Lasjaunias 1988a), while proximal occlusive arteriopathy is more frequent. For this reason, management protocols derived from experience in adults should not be applied to the pediatric population. In particular, adult-based classifications and AVM grading according to the expected surgical outcome is particularly inappropriate in children, in whom (a) cerebral eloquence is difficult to assess, particularly in the first few years of life, (b) most lesions are fistulas or multifocal, (c) drainage usually affects the entire venous system, and (d) the potential for recovery is different. It is often believed that the adult type of classification and grading of AVMs indicates or in some way corresponds to the natural evolution of the lesion, and, although unintentionally, this has created a significant amount of misunderstanding and confusion.A difficult to operate AVM (i.e., a high-grade AVM) is not necessarily a dangerous one for the patient if not operated upon or more dangerous for the patient than a low-grade AVM. In addition to the conventional objectives, the decision-making process in children must take into consideration additional specific details pertaining to the veins and the myelinization process. Thereafter, staged partial treatment of progressive deficits associated with congested cerebral veins, poorly controlled seizures, hemorrhagic episodes with or without specific changes upstream or downstream from the AVM, or headaches in children without ventricular enlargement or macrocrania may all represent good indications for treatment. Neurocognitive evaluation is the key follow-up criterion in children even without deficits, hemorrhage, or seizures, as it helps in the assessment of treatment quality and success. Failure to obtain a normal maturation process may constitute a therapeutic failure if the optimum moment for intervention has been missed (therapeutic window). When discussing CAVMs or vascular diseases in children, one might wonder whether it represents an artificially created grouping. AVMs in children are primarily characterized by diagnostic and therapeutic difficulties specific to the population in which they occur. CAVM corresponds more to a clinical group than a nosological one. However, some rare lesions (see Chaps. 4, 7, 12, this volume) are exclusively encountered in children, mainly in neonates and infants. In addition, the anatomic and physiologic characteristics of the neonatal and infant brain and the immaturity of its systemic flexibility (hydrovenous) create a specific group of nonhemorrhagic symptoms and therapeutic challenges. This vulnerability means that the lesion rapidly becomes lethal or creates a disabling state, whereas a similar lesion in an adult might produce only few symptoms. The clinical characteristics of CAVMs in children are therefore related to the children themselves and their specific anatomy and physiology. Children are not small adults and the therapeutic challenges cannot be measured in terms of size of the target, but is related to our capability to understand the other structures and processes involving the brain and its vasculature and anticipate the potential interferences between the CAVM and the maturing brain. For a long time, vascular lesions in children were divided into nonproliferative and proliferative lesions. The former group comprises vascular

30

2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Scheme 2.1. Role of structural weaknesses in disease development

Scheme 2.2. Vascular diseases according to the arterio-veno-lymphatic tree

Vascular Lesion Types and Disease Groups

31

malformations, the latter hemangiomatous lesions. In fact, such a distinction, which was helpful during the past 20 years, has also greatly benefited from recent biological contributions as well as the recognition of shear stress mechanisms in vascular modeling and remodeling.Actually angiogenesis is involved in both so-called malformations and hemangiomas, but they are different in terms of trigger factor (agent), target, and timing (Schemes 2.1, 2.2).They will be discussed in the various chapters dealing with brain and maxillofacial AVMs and hemangiomas.

2.3 Vascular Lesion Types and Disease Groups Many and often confusing classifications have been proposed in the past. The role of coagulation disorders, systemic manifestations, topography, size, eloquence of the involved brain, and extrapolation from experience with adult lesions has led to emphasis being placed on many different aspects, which, in combination with technical advances, tended to focus on certain particular details rather than on an understanding of the problem as a whole. The assumption that AVMs are congenital, the rarity of the disease, the small number of patients in the clinical series reported, and the aggregation of various pathologies described in literature reviews further added to this confusion (Govaert 1993; Raimondi 1980; Edwards and Hoffman 1989). Basic classifications of vascular diseases use pathological, biological, and clinical data. For instance, one should now be able to distinguish AV shunts from venous lesions or malformations. Furthermore one should be able to recognize and differentiate venous variations from malformations. Similarly, one should not label an associated arterial variation or embryonic persistence a malformation when associated with a CAVM or a giant aneurysm. This distinction is not only of academic interest, but may also have clinical consequences. A true malformation is not an anatomic variant, and the isolated persistence of an embryonic disposition does not give a congenital character to a lesion even if in some cases it is a time marker of an embryonic event, which may not necessarily be related. When considering vascular lesions in children, one should keep in mind several keys to approaching the questions raised and understanding the clinical expression (phenotypes) of the various diseases involved. Even in an apparently single-disease category such as CAVMs, several entities must be distinguished as their predictable presentation or progression requires different management at different times. The generic name artificially regrouping different situations expresses the use of a single key (the arteriovenous shunt for example) where two or three would reveal the differences: single hole AVF (Yoshida 2004; Weon et al. 2005), familial disorder for HHT (Mahadevan 2004), metameric disease for CAMS (Bhattacharya et al. 2001), proliferative activity for proliferative angiopathy, PHACE (Bhattacharya et al. 2004), etc.

32

2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Table 2.1a. Vascular diseases, genetics: karyotypes Diseasea HHTb Cavernomas

MCMVM: BRBN (Bean syndrome) ED IV NF1 NF2 VHL Moyamoya Bourneville TSC1 TSC2 CADASIL FHM Paragangliomas Polycystic kidney disease a

b

Chromosome location Ch 9q33–34 endoglin Ch 12q Alk 1 Ch 7q21–22 CCM1 (KRIT1 is the mutated protein CCM1) Ch 7p13–15 (CCM2) Ch 3q25,2–27 (CCM3) Ch 9p Tie 2/Ch1 cutaneous Chromosome 2 Ch 17q22 Chromosome 22 Ch 3p25–26 Ch 17q25 Ch 3p24.2-p26 Ch 9q34 Ch 16p13 Ch 19q Ch 19 11q23 Ch 16p13.3 (PDK1) Ch 4 (PDK2)

The same effects are expected to follow functional blockade of a gene rather than single type of structural alteration in each patient: when the gene involves interactions (ligand), the mutations are multiple; when the gene makes a protein active, the mutations are often identical: lack of stage (protein or mRNA is missing), poor emission of signal or wrong destination (pigmentation), no reception of signal (ligand), insufficient message (too short, too few), hyperactive protein. Each family has its own mutation >100.

Table 2.1b. Vascular diseases, genetics: angiogenic activity Arterial angiogenesis VHL NF1 Moyamoya PHACE Proliferative angiopathy CAMS Primary arterial angiectasiaa Aneurysms

a

Not flow-induced.

Venous angiogenesis HHT BRBN Cavernomas CVMS

Primary venous angiectasiaa DSM DVAs Venous angiogenesis Lymphatic angiogenesis LM

Vascular Lesion Types and Disease Groups

Scheme 2.3. Timing of triggering events and phenotypic expressions

Scheme 2.4A. „Age“ of vascular lesions

33

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Scheme 2.4B. So-called congenital or malformative vs acquired neurovascular lesions

The following keys can be put forward:
Proliferative or nonproliferative lesion
Type of disorder (Table 2.1): – Monogenetic (surface protein dysfunction, improper collagen structure, extracellular matrix deficiency), progressive dysfunction (triggered structural defect or failed repair or inadequate maintenance systems), extrinsic and acquired damage (infectious, traumatic) (Scheme 2.1)
Location on the vessel tree: – From the arterial tree to the arterial capillary, venous junction venules, veins, sinuses, and lymphatics (Scheme 2.2)
Time of occurrence: – Germinal mutation transmitted, early somatic mutation, early stage metamerically arranged defect, fetal failed signaling, postnatal mutation, failed remodeling during vascular renewal (Scheme 2.3)
Time of revelation: – In utero, fetal period, neonatal, infancy prior to 2 years of age, 2–6 years, and after 6 years (Scheme 2.4)
Clinical evolution and natural history: – Permanent increase in flow, arterial occlusion, spontaneous thrombosis (see Chap. 7, this volume).
Secondary effects on the maturing or remaining vasculature:
High-flow angiopathy, jugular bulb maturation, cerebral vein opening into the cavernous sinus, pacchionian granulations development (see Chaps. 3, 5, this volume).

2.3.1 Nonproliferative Lesions 2.3.1.1 Arteriovenous Lesions

The AV lesions that can be encountered depend on the meningeal space from which they primarily develop: dural, pial, subarachnoid, or choroidal (Scheme 2.5). These locations give rise to several subtypes and may be unifocal, multifocal, hereditary, etc. (Scheme 2.6).

Isolated Brain AVMs

35

Scheme 2.5. Spaces hosting intracranial ateriovenous (AV) shunts. VGAM, vein of Galen aneurysmal malformation; AVM, arteriovenous malformation

Scheme 2.6. Subtypes of vascular lesions in children. AVM, arteriovenous malformation

2.3.1.2 Isolated Brain AVMs

Pial AV Shunt in Children Micro/Macro AVM Micro/Macro AVF Multifocal CAMS Familial Proliferative angiopathy Hemorrhagic angiopathy False and induced AV shunts

These can be small (micro-AVM; see Fig. 2.1) or large (macro-AVM; Fig. 2.2), and this distinction is of nosological interest, as the passage from one type to the other cannot be demonstrated. Of interest is the distinction between the nidus type (with an arteriolar network; Fig. 2.1) and the fistulous type (single or multiple large, direct AV communication; see Fig. 2.3). The former consists of a group of small AV shunts within a vascular meshwork within the nidus, while the latter is a direct opening of an artery or arteries into an unusually enlarged or giant draining vein, with or without outflow restriction. This distinction is a significant one, and in our opinion similar to what was said for micro- and macro-AVMs, there

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Fig. 2.1A, B. Typical aspect of a cortical micro-AVM revealed by an intralobar hematoma in a young boy

Fig. 2.2A, B. Medium-sized deep-seated AVM discovered incidentally in a young boy. Both lesions were treated successfully by embolization

is no transition from AVMs to AVFs or vice-versa. CAVMs can occur in the subpial space, where they can be superficial or deep, corticoventricular, or buried in the white matter; in this latter location they should be distinguished from hemorrhagic angiopathy (see below and Chap. 18, this volume) (Fig. 2.4). From their origin onwards, they contain no neurons or nerve fibers within their nidus, which had led some authors to describe pial AVM (PAVM) as extracerebral. This justifies the distinction of proliferative angiopathy as a distinct group of diseases (see below and Chap. 18, this volume). Fistulas are also subpial; they drain either immediately into subarachnoid vein(s) or within the subpial venous network. They are superficial at the cerebral cortex or the surface of the cord. They are not supplied by ventral longitudinal neural perforators.

Isolated Brain AVMs

37

Fig. 2.3. A, B A 7-day-old child presented with cardiac failure, for which a cerebral arteriovenous fistula (AVF) was diagnosed. There was a family history suggestive of HHT. The AVF was embolized at the age of 3 years. There was no focal melt in relation to the direct subarachnoid vein opening of this cortical fistula. C The child is neurologically normal at 12 years of age, the lesion is partially excluded, and there is no evidence of melting-brain syndrome

Fig. 2.4. A 5-year-old boy presenting with hemianopia in relation to a subcortical hemorrhage. B, C Angiography demonstrates a hemorrhagic angiopathy. D, E One year after radiation therapy, the lesion is no longer visible

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Fig. 2.5. A A male infant presented with macrocrania with vein of Galen aneurysmal malformation (VGAM) of the mural type. Untreated cardiac overload was also noted at that time. He was referred to us at the age of 3 years following an episode of generalized seizure. B Almost complete occlusion was obtained in one session. C, D A small remaining shunt was seen 2 years later (arrow, remaining venous drainage) and final spontaneous disappearance was verified. At the age of 8 years, the child’s score was 4 and he was not taking any antiepileptic medication

Cerebrofacial Arteriovenous Metameric Syndromes

39

2.3.1.3 CAVFs

We have treated cerebral arteriovenous fistulas in children in a separate chapter since they raise specific nosological clinical and therapeutic challenges (Yoshida et al. 2004; Weon et al. 2005). Their linkage with hereditary hemorrhagic telangiectasia is remarkable (see Chap. 4, this volume) (Mahadevan 2004). Drainage into subpial or subarachnoid veins is of paramount importance in this topography, particularly in neonates and infants (Fig. 2.3; see Sects. 2.4.2 and 2.4.3). Finally, there is no gender dominance in CAVM in children (see Chap. 5, this volume)

2.3.1.4 VGAMs

Galenic Vascular Lesions in Children Choroidal VGAM Mural VGAM VGAD Dural VGAV shunt Venous dilatation

VGAM is a unique, well-defined group of malformations that occur at the end of the embryonic period (Fig. 2.5). They constitute a separate group from other lesions such as CAVMs, and they are often called non-Galenvein AV malformations, particularly in neonates and infants. In the VGAM group, there is a 2–3:1 male predominance (see Chap. 3, this volume).

2.3.1.5 Cerebrofacial Arteriovenous Metameric Syndromes

The diagnosis of cerebrofacial arteriovenous metameric syndromes (CAMS) (Chap. 6, this volume) encompasses a spectrum of phenotypic expressions. Features of the syndrome as originally described and common to all cases include arteriovenous malformations of the brain and orbit (with retinal and/or retrobulbar lesions) (Bonnet-Dechaume-Blanc or Wyburn-Mason syndrome) and maxillofacial lesions. A portion of these patients will manifest the complete expression of the disease with additional high-flow arteriovenous malformations of the maxilla or

Fig. 2.6. Cerebrofacial vascular metameric syndromes. Three territories linking the brain to the face can be recognized. Depending upon the type of cell involved, arteriovenous (CAMS 1–3) or venolymphatic (CVMS 1–3) metameric syndromes are involved. At the first cervical segment, SAMS 1 (green arrow) (SAMS 1–31) is represented. (From Bhattacharya 2001)

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Fig. 2.7A–C. CAMS 2. A 4-yearold boy presented with a retinal AVM. A At that time, MR was normal. B, C Six years later, a diencephalic lesion associated with the previous lesion can be seen

mandibular regions. These represent distinct and additional life-threatening risks because of epistaxis or oral hemorrhage. We have suggested segmental patterns of involvement in what is likely to be a disease of the neural crest and/or adjacent cephalic mesoderm.A newly proposed rational classification reflects the putative, underlying disorder and calls for a new label: cerebrofacial arteriovenous metameric syndrome (CAMS) (Bhattacharya et al. 2001) (see Chap. 6) (Fig. 2.6). The various lesions associated with CAMS may reveal themselves over time in a consecutive fashion suggesting pseudo de novo lesions (Fig. 2.7).

The Blue Rubber-Bleb Nevus or Bean Syndrome

41

Fig. 2.8. In utero MR diagnosis of dural sinus malformation (DSM)

2.3.1.6 Dural Lesions

Dural AV Shunt in Children Sinus malformation High-flow lesions Multifocal „Adult“ types Post-traumatic

Dural lesions can be encountered at any age in children, but represent different disease entities. We will describe them in detail (see Chap. 7, this volume), since they can represent true malformations in very young children and secondary AV shunts in older patients. The former are encountered in neonates and infants and can be diagnosed in utero (Barbosa 2003) (Fig. 2.8). The latter are usually multifocal and contain large sinuses and high-velocity flow phenomena, but are originally associated with low pressure in the dural sinuses (Fig. 2.9). They become symptomatic during childhood and create remote manifestations on the dural sinuses as well as the cerebral cortex caused by the venous sump effect. Their treatment is particularly difficult. Different types of dural lesions are encountered with different frequency in various age groups (Scheme 1.3).

2.3.1.7 Telangiectasias

Telangiectasias are usually included in the malformation group and they are occasionally described in children at autopsy. They are likely to represent improper capillary remodeling (see Sect. 2.7.1). They can be secondary to local ischemia or hemorrhage, but are seldom the cause of it (Fig. 2.10).

2.3.1.8 The Blue Rubber-Bleb Nevus or Bean Syndrome

The blue rubber-bled nevus or bean syndrome (BRBN) can produce multiple types of central nervous system (CNS) involvement. These features consist of multiple VMs (venous malformations similar to large telangiectasias), DVAs (developmental venous anomalies) in supratentorial

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Fig. 2.9A–F. Legend see p. 43.

▲

The Blue Rubber-Bleb Nevus or Bean Syndrome

Fig. 2.9A–G. A 1-month-old boy presenting with progressive macrocrania and referred at the age of 2 years. A, B Computed tomography (CT), C magnetic resonance imaging (MRI), and D–F angiography demonstrate a typical multifocal dural arteriovenous lesion with venous restriction (jugular dysmaturation) at the base and tonsillar prolapse. G Note the flowrelated aneurysm on the AICA contribution (subarcuata artery)

Fig. 2.10A–C. MRI and angiographic aspect of an hemorrhagic micro-AVM or telangiectasia in a child presenting with a family history of HHT

43

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Fig. 2.11A, B. BRBN, blue rubber bled nevus.Association of intracerebral telangiectasia (A, B) and large cerebellar DVA, with capillarectasia (see Chap. 8, this volume). (From Chung 2003)

brain, cerebellum, and tectum mesencephali (Fig. 2.11). Since its first description by Bean there have been many cases of BRBN manifesting with gastrointestinal bleeding with or without associated hemorrhage. Cases with CNS involvement are rare; many of the reported descriptions are confusing with various terms used to describe them such as capillary venous malformation, hemangiomas, and vascular malformations. The association with DVAs was recognized in some cases but is likely underestimated because of the use of different nomenclature in the published cases. Although as in Chung’s case (2003) BRBN can be sporadic, its familial transmission is frequent and the link with HHT1 unlikely despite the involvement of the same chromosome (chromosome 9p) (Boon et al. 1994; Gallione et al. 1995; see Chap. 8, this volume).

2.3.1.9 Venous Malformations (Cavernomas)

Venous malformations are located outside the nervous tissue and therefore do not contain nervous or glial elements. They are referred to as being cavernous and can be isolated or multiple. In the latter case, they are often familial with autosomal dominant transmission. These lesions are malformations (Fig. 2.12) and can be found in autopsy series in any location within the intradural space (subarachnoid, subpial). They increase in size following intralesional hemorrhage. They occasionally have the appearance of a tumor (in particular in children) or a cyst, through confluence of recurrent hematomas. Patients most often present with a hemorrhagic episodes leading to acute symptoms (epilepsy, sudden headache, deficit, and very occasionally subarachnoid hemorrhage in the case of subpial location or intraventricular hemorrhage in subependymal le-

Venous Angiomas or Developmental Venous Anomalies

45

Fig. 2.12A, B. Multiple intradural intraneural and subarachnoid cavernomas in a young adult (familial case)

sions). Different from AVMs in HHT, new cavernomas may become apparent, as the disease is potentially multifocal with other microsatellite lesions still too small to be detected with imaging. Subsequent growth is secondary to intralesional hemorrhage, although these episodes may be subclinical (see Chap. 8, this volume). They can be associated with venous anomalies or other malformations such as dural sinus AV malformations (DSMs) (Fig. 2.13) and be induced by radiation therapy.

2.3.1.10 Venous Angiomas or Developmental Venous Anomalies

Venous angiomas or developmental venous anomalies (DVAs) are anatomic variations that can involve one or both hemispheres and be located infratentorially. They do not exist at the spinal cord level or where no secondary germinal matrix migration has occurred. Their symptomatic character is primarily dependent upon associated malformations (AV or cavernomatous). The lack of flexibility due to the extreme anatomic disposition of the venous drainage to the brain in the region may also produce ischemic episodes manifesting various levels of clinical severity. The venous channels are morphologically normal and drain normally functioning brain, although transit time through their venules is sometimes rapid and almost similar to that in a slow-flow AVM. Careful analysis of the venous anatomy always provides the necessary information to make the proper diagnosis. DVAs should therefore never be a target for treatment (see Chap. 8, this volume).

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Fig. 2.13. A, B A 6-month-old infant with right frontal cutaneous venous malformation, torcular DSM and posterior fossa DVA. C, D Eight months later, multiple cavernomas with intracerebral hemorrhagic changes are noted. Dramatic enlargement of the DSM and extension to the right transverse sinus can be seen. (From Mohamed et al. 2002)

Induced Pial Shunts

47

2.3.1.11 Cerebrofacial Venous Metameric Syndrome (Formerly Sturge-Weber Syndrome)

Cerebrofacial venous metameric syndrome (CVMS, formerly SturgeWeber Syndrome) consists of cutaneous, facial, port-wine stain (venular malformation), subcutaneous lymphatic malformations (with secondary maxillofacial bone and soft tissue hypertrophy), and cerebral, cortical vein thrombosis with cortical atrophy, secondary angiogenesis, and transhemispheric venous drainage, with or without choroid plexus hypertrophy (Fig. 2.14). The disease is not hereditary. In line with CAMS, Ramli (2003) suggested the name of cerebrofacial venous metameric syndrome (CVMS; see Chap. 8, this volume). In CVMS, a linkage between various craniofacial vascular disorders can be identified as related to the neural crest/mesodermic segmentation. Involvement of the maxillofacial and skull base bone, skin, subcutaneous tissue, and vessels are in the same metameric distribution. The facial involvement represents the distal destination of the migrating neural crest cells, contributing to the vascular network rather than the trigeminal dermatome. The cerebral abnormalities when present are also in the same metameric distribution.

2.3.1.12 Induced Pial Shunts

Induced pial shunts are unique in juvenile dural arteriovenous lesions and occur only in children. They develop with the sump effect from the abnormal dural sinus, retrograde to the cerebral vein, with subsequent pial AV shunt formation (Figs. 2.9, 2.15). This observation has been confirmed by sequential angiographs and spontaneous post-therapeutic regression of the induced AV shunts (see Chap. 7, this volume).

Fig. 2.14A, B. Cerebrofacial venous metameric syndrome CVMS Sturge-Weber (see Chap. 8, this volume). A CVMS 1, 2; B CVMS 2, 3. (From Ramli et al. 2003)

48

2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts Fig. 2.15. An 11-year-old girl, who had presented at the age of 2 with right proptosis related to an orbital hematoma. Angiography performed at that time failed to demonstrate any intracranial anomaly. Over a period of 10 years, she developed progressive right-sided hemiparesis, dysphasia, and ataxia. Although angiography had been normal at the age of 2 at the intracranial cavity, note the juvenile type of dural arteriovenous shunt and the remote cortical and basal pial arteriovenous communications (single and double arrows) induced by the lesion. (From Garcia-Monaco et al. 1991c)

2.3.1.13 Spinal Cord AVM

Spinal cord AVMs and spinal cord cavernous malformations present the same characteristics as those mentioned in the brain. Similar to the cranial region, spinal arteriovenous metameric syndromes (SAMS) are recognized, enriching the historical description of Cobb’s syndrome (see Chap. 15, this volume). Thirty-one segments to the spinal division allow for single or multimetameric syndromes (Matsumaru et al. 1999).

2.3.1.14 General Conclusions on Vascular Lesions

Vascular malformations are multifocal twice as often in children as in adults. This multifocal character has been underestimated in children due to poor-quality angiographic studies and lesions not being recognized on magnetic resonance imaging (MRI). Some can be truly multifocal with interposed normal tissue between two AV shunt niduses (Fig. 2.16) and separate or distinct draining veins. Others can be contiguous, simulating compartments within a single lesion. Proof of the presence of these compartments is sometimes hard to establish; however, they may represent individual therapeutic goals at the time of endovascular treatment. The most typical is probably CAMS syndrome, which encompasses vascular malformations in adjacent locations such as the optic nerve, diencephalon, and occipital cortex. These lesions may reveal sequentially over several years (as much as 20 years in the cases of Jiarakongmun et al. 2002), illustrating the effect of the surrounding relationships along the migration pathway on the impaired cells, each region compensating differently (and revealing differently) for the quiescent defect that originated from the early stages of metameric organization. Some associated lesions cannot be integrated into the CAMS scheme even though obviously linked (Fig. 2.17).

Proliferative Lesions

49

Fig. 2.16A, B. A 7-year-old boy presented with generalized seizures in relation to a brain AVM. Note the multifocality demonstrated at angiography

Within these multifocal lesions, some may be false AV shunts. Following hemorrhage or ischemia, the true lesion may induce angiogenesis (neoangiogenesis or capillarectasia) and early venous return. The final appearance is sometimes difficult to understand unless prior angiography had been performed. Interestingly, the number of thrombosed lesions also seems to be more frequent on follow-up of CAVMs in children.

2.3.2 Proliferative Lesions

Proliferative vascular lesions in children form a distinct group of disorders; the name „angioma“ is often given indiscriminately to all apparently congenital, nonischemic vascular lesions. The failure to differentiate between nonproliferative and proliferative lesions has been the source of misinterpretations and erroneous prediction of the course of the disease. The name „angioma“ (vascular growth) should be abandoned or reserved for hemangiomas, which are benign tumors of blood vessel origin in infants (see Chap. 11, this volume). Some hemangiomas can be seen intracranially but such localization is rare and usually associated with superficial hemangiomas (see Chap. 12, this volume). Infant hemangiomas appear to be rare in Asian populations. The older the child, the more likely the angioarchitecture of these vascular tumors will be of the cavernous type. Yet some of them keep a capillary angioarchitecture and are called NICH (noninvoluting capillary hemangiomas).

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Fig. 2.17A–D. A 6-year-old child presented with an external ear capillary lesion on the left side (A, B), associated with an ipsilateral intracranial cerebellar arteriovenous malformation (AVM) discovered incidentally (C, D). These findings suggest a CAMS 3 syndrome

Diffuse Angiodysplasia

51

2.3.2.1 PHACE or PHACES

These are acronyms for a syndrome of variable phenotypic expression comprising posterior fossa malformations, facial hemangiomas, arterial anomalies, coarctation and other cardiac disorders, eye abnormalities, and stenotic arterial disease; many of the elements of this disorder could reflect an underlying abnormality of cell proliferation and apoptosis (see Chap. 12, this volume) (Bhattacharya et al. 2001).

2.3.2.2 Diffuse Angiodysplasia

Diffuse angiodysplasia was reported in neonates by Hasper (1983) and Flower (1972): it is characterized by glomeruloid hypertrophy of perithelial and endothelial cells and can be associated with hydranencephaly and hydrocephalus. Schmitt (1984) reported possible cytomegalovirus transplacental transmission in one infant, while Flament-Durand (1981) identified an associated adenovirus type 4 infection. In children and young adults, proliferative and angioectatic diseases are frequently triggered by spontaneous or traumatic dissections, viral infections, immune phenomena, and other causes. Moyamoya disease, moyamoya-like syndromes, and proliferative angiopathy in children are the most typical disorders in this group (Figs. 2.18, 2.19). They combine neoangiogenesis (production of lumen) and angiectasia (production of vessel wall), which may be difficult to differentiate; however, in such instances there is a discrepancy between the apparent size of the nidus-like network of vessels and the draining veins that are often normal or slightly enlarged. In angiectasia, the architecture of the nidus is homogeneous and appears normal, while it is unpredictable in angiogenesis. The rapid venous filling is usually due to a faster capillary transit time and seldom caused by true AV shunts in capillarectasia (in some DVAs for example). The evolution of these proliferative diseases is unpredictable (see Chap. 18, this volume). Hemorrhagic angiopathy is another entity that we encounter in some rare cases of intracerebral hematomas in children. Most often after the age of 5 they correspond to a network of intracerebral subcortical arterioles with normal morphological and sequential venous drainage. They may rehemorrhage and can therefore be partially embolized when the area of weakness in the angioarchitecture can be identified; if it is not possible to identify such a target, one may consider radiosurgery. The response to radiation therapy is amazingly rapid and effective (Fig. 2.4). Even this approach to vascular lesions is too static, since not all malformations are seen at the same age and are invariably not seen at the beginning of their development. The age of a given lesion is therefore unknown (Scheme 2.4). They often represent significant anatomic differences and yet are usually discussed as a group, thereby creating confusing statistical population projections. They are thought to be congenital, which has never been proven, and are believed to be essentially stable in size. Our experience contradicts both statements. Over time, certain CAVMs may appear to increase in size, while others spontaneously thrombose without

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Fig. 2.18A–D. Legend see p. 53

▲

Diffuse Angiodysplasia

53

Fig. 2.18A–F. A 12-year-old boy presented at the age of 1 month with a generalized seizure. A–C MRI was performed. D–F A few months after additional seizures and transient right-sided deficit, angiography shows a stenotic disease of the ICA anterior division involving the A1 and M1 segments. There is intracerebral lenticulostriate angiectasia and angiogenesis corresponding to the first stage of moyamoya disease. The vertebral artery injection demonstrates the sparing of the posterior fossa arteries

symptoms. However, one never sees a micro-AVM becoming a large one or a nidus arranged AVM becoming a fistulous lesion. Whenever it is possible to compare high-quality angiographic studies 10 years apart, amazing changes in the vasculature can be observed. These changes are less spectacular in adults, where the vascular plasticity does not cover the same range of possibilities as in children and therefore does not show the same degree of variability. This introduces two new approaches to the problem of CAVMs in children: the aspect of age and symptoms vs the impact of vascular remodeling in the congenital concept of CAVM. The fact that the remodeling is the same during the perinatal period as in infants and children is probably only a gross approximation and not completely correct.

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Fig. 2.19A–D. Legend see pp. 56

Diffuse Angiodysplasia

Fig. 2.19E, F. Legend see p. 56

55

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Fig. 2.19A–G. A 15-year-old girl presenting with generalized seizures was diagnosed a proliferative angiopathy. A, B Note on the MRI section the amount of dilated vessel running at the surface of the cortex. C–F Angiographically, there are several cortical artery interruptions with local „explosive“ angiectasia. Diffuse supra- and infratentorial transdural supply at the base and the convexity testify to the active angiogenic activity of this disorder. G Despite medical treatment, the patient died 4 years after the diagnosis from major ischemic stroke

2.4 Classification of CAVMs by Age Group In caring for children over time, one must consider the different phases of their development. Depending on individual interests and experience, one may wish to emphasize age, symptoms, or various diseases. However, clinical practice forces us to constantly switch from one to the other to establish the most accurate prognosis. To illustrate these various methods and their contributions to decision making, we will consider them sequentially based on age group.

2.4.1 Fetal Age

Intrauterine antenatal ultrasound or MRI diagnosis of a large fetal intracranial mass as a pseudocystic, nonechogenic or poorly echogenic spherical image, depending on its topography, illustrates either a VGAM or a dural sinus malformation (DSM) (Fig. 2.20). In a few cases we made a prenatal diagnosis of CAVM (Scheme 2.7). Despite all the possible features associated with each type of lesion involved (see the corresponding chapters), we will concentrate on two abnormalities: macrocrania with or without encephalomalacia and cardiac tolerance (Scheme 2.8). With regard to the mother, there has not been any effect observed during pregnancy of a prenatal diagnosed intracranial AV shunt. We have not found any trigger responsible for the occurrence of such a shunt at that time. With regard to the fetal brain, macrocrania can be seen in both VGAM and DSM, but it has opposing prognostic values. In VGAM, macrocrania (in the absence of ventricular enlargement) is usually a benign obser-

Intracranial AV Shunt in Children Age Groups Fetuses Neonates (30 days) Infants (<2 years) Children (£15 years)

Fetal Age

Fig. 2.20. Prenatal diagnosis of vein of Galen. The baby presented at birth with mild cardiac overload and was treated within the therapeutic window at 5 months of age

Scheme 2.7. Frequency of the various types of intracranial arteriovenous (AV) shunts in children in relation to age (M months, Y years) at diagnosis. VGAM, vein of Galen aneurysmal malformation; AVM, arteriovenous malformation

57

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Scheme 2.8. Physiopathological mechanisms involved in the clinical presentation of intracranial vascular malformations and arteriovenous shunts in relation to age groups. VGAM, vein of Galen aneurysmal malformation

Table 2.2. Frequency of symptoms revealing vascular malformations or arteriovenous shunts in neonates

Systemic Hydrodynamic Convulsive Haemorrhagic Neurological

VGAM

Dural malformation

Pial AVM

+++ +++ – – –

+ +++ ++ +++ +

++ + +++ ++ ++

VGAM, vein of Galen aneurysmal malformation; AVM, arteriovenous malformation; +++, very frequent; ++, frequent; +, possible; –, not seen (or severe brain damage).

vation without a negative impact on the prognostic neonatal score (Table 2.2). In contrast, macrocrania in DSM indicates an already active sinus dysfunction with water and venous effect; if present, the prognosis, which is already not good, would become even worse (see Chap. 7, this volume). The only finding that has the same importance at that age of diagnosis, regardless of the type of AV shunt, is the presence of encephalomalacia. In fact, even with MRI, it is often difficult to be certain about the presence of brain damage in fetuses. This diagnosis is certainly of major importance, since in our management strategy this discovery may lead to therapeutic abortion. The presence of isolated cardiomegaly has no impact on prognosis. Experience with DSM is limited because of the rarity of the disease, but neonates with this malformation seldom present with major systemic symptoms in utero. On the other hand, cardiac failure in fetuses with VGAM is known to have a poor prognosis. This finding proved to be the only constant early predictive unfavorable factor in our series, resulting in a low neonatal score and consequently in treatment being withheld.

Frequency of Vascular Lesions Per Age Group In utero 1. Aneurysmal malformations of the vein of Galen 2. Dural sinus malformation 3. Pial arteriovenous shunt

Infancy

59

2.4.2 Neonatal Age Frequency of Vascular Lesions Per Age Group Neonates 1. Aneurysmal malformation of the vein of Galen 2. Dural sinus malformation 3. Pial arteriovenous shunt 4. Cavernoma 5. Arterial aneurysm

Not all lesions diagnosed (visible) in utero will become clinically eloquent at birth. When symptomatic, the clinical manifestations are usually the systemic effects of the high-flow lesion. Lack of treatment may rapidly lead to multiorgan failure and a cerebral melting process within days or weeks (see Sect. 2.5.3; Fig. 2.21). At that age, there is a fundamental difference between VGAM and non-Galenic AV malformations (pial). Early neurological symptoms in VGAM are of major negative prognostic value, to the extent that treatment may be withheld (Fig. 2.22). On the other hand, similar symptoms are an indication for emergency management in non-Galenic AVSs. In VGAM in neonates, neurological manifestations such as convulsions indicate the anoxic insult to the brain. VGAM drainage has no venodural resistance and immediately overloads the cardiac venous return, while it protects the cerebral hemodynamic circulation from retrograde pial vein congestion. VGAM venous outflow is craniofugal without direct interference with the pial veins, and such anoxic failure, when present, indicates rather diffuse and indirect brain damage. This effect has usually already started in utero. These symptoms are never isolated, but indicate the presence of a severe systemic syndrome, which, in turn, should lead to the decision not to treat. Conversely, a non-Galenic AV malformation in a patient presenting with a convulsive episode indicates focal, yet early damage in relation to subpial damage of the shunt. Ischemia of venous origin or focal hemorrhage (hemorrhagic infarct) is the most frequent cause suggested to explain the convulsion. It requires urgent treatment to avoid the melting-brain syndrome, which otherwise rapidly occurs in the following few weeks. In non-Galenic lesions, these neurological signs are not consistently associated with cardiac manifestations. The systemic symptoms in neonatally diagnosed CAVM are usually better tolerated than in VGAM, probably because the venodural junction is relatively preserved and protects the cardiac function. Hemorrhage in VGAM in this age group does not occur. A hemorrhagic episode or convulsion in a neonate should steer one away from the diagnosis of VGAM.

2.4.3 Infancy

Infancy is dominated by hydrovenous disorders. The water homeostatic system of neonates is still immature, which results in the venous system being responsible for the venous drainage and the intrinsic and extrinsic cerebral water dynamics. The granulations are not functional yet, and their maturation is likely to be delayed if increased pressure is present in the dural sinuses. Separation of the circuits between cerebrospinal fluid (CSF) from choroidal secretion and intrinsic water secreted by capillaries in the Virchow Robin spaces does not take place. A specific and complex gradient and equilibrium between the subpial and subependymal space develops; in addition to the physiological link existing between the ventricle and subarachnoid spaces, a rich venous network is present in the dura, adjacent to the future dural sinuses (see Chap. 7, this volume).

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Fig. 2.21. A A female neonate presented a generalized convulsive episode leading to MRI. The diagnosis made at that time was vein of Galen aneurysmal malformation (double arrows) although a lateralized pouch was seen (single arrow); because of the absence of systemic manifestations, the child was not treated. Two months later, the child developed progressive macrocrania and had repeated seizures. B CT demonstrated bilateral venous infarction with focal deep-seated frontal hemorrhages. The child was then treated successfully at another institution. One year later, the child became severely disabled. C MRI confirms complete exclusion of the malformation and irreversible brain damage

Infancy

61

Fig. 2.22. A Neonatal chest X-ray and B CT in a female neonate weighing 2,650 g and presenting with severe multiorgan failure and cerebral encephalomalacia. The neonatal score was 6. She died 24 h later

The signs of water retention start with macrocrania without ventriculomegaly. Clinical consequences are almost consistently neurocognitive delay with no direct relationship to the degree of the increase in head circumference. The link between the water disorders and the myelinization delay is of interest, but still speculative. With regard to the presence of macrocrania with an increase in intracranial pressure, it is thought not to be an indicator of negative outcome in infants with intracranial shunts, unless a DSM is diagnosed (see Chap. 7, this volume). If left untreated, this water dysfunction progressively leads to ventriculomegaly. In other situations when the suture enlargement is too slow or not possible, signs of transependymal resorption become evident. The loss of a functioning resorption gradient is then established, and true hydrocephalic manifestations will occur.Ventricular shunting at this time is associated with significant morbidity (see Chap. 3, this volume). This morbidity demonstrates a widespread lack of understanding of the physiology of the water equilibrium in infants and the various and progressive shifts that result in a very unstable situation. Venous changes have a direct impact at this age. Direct pial or subarachnoid congestion is noted in CAVMs, whereas they remain absent for a long time in VGAMs. In non-Galenic AVMs, local congestion rapidly leads to focal ischemia, as revealed by convulsions and later hemorrhage. Rarely do such infants present with progressive deficit, except for deep thalamic or basal ganglia lesions, which may be part of CAMS (cerebrofacial arteriovenous metameric syndrome). Recurrent and multifocal postischemic venous hemorrhagic infarcts in these CAVM patients are often remote from the AVM site. In VGAM, pial congestion is absent for a long time and depends on whether maturation of the venous drainage at

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

the skull base occurs (cavernous sinus capture; see Chap. 3, this volume). The dysmaturation and subsequent closure of the jugular foramen in VGAMs and in some CAVMs and in DSM patients is unlikely to be related to a high-flow venous angiopathy, and more likely to cause impaired postnatal development. The dominant vault enlargement in these children with macrocrania probably shows the usual active enlargement of the skull base caused by the growing brain; in addition, the specific growth patterns of the posterior fossa make it impossible for the jugular foramen to develop harmoniously. Regardless of the etiology involved, the restriction of cranial venous outlets produces retrograde diffuse venous congestion. A direct relationship between the demonstrated reflux and the cerebral damage then occurs. The deeper or more midline the retrograde congestion is expressed, the more diffuse the infarctions and hemorrhages. These rather acute or subacute failures can be expected in most cases. The slowly developing end result of hydrovenous dysfunction at the posterior fossa level will be progressive tonsillar prolapse (see Sect. 2.5.2). Its presence is an expression of the stage of the disorder rather than any specific etiology. We have encountered tonsillar prolapse every time that the above conditions were in effect. If such conditions are met in non-AV diseases, it is likely that the same response would occur. This prolapse is reversible for a long time with adequate treatment of the AV shunt, even in the presence of jugular bulb occlusion. As soon as this phase has passed or the prodromes of each situation have been identified and corrected, the evolution will be slower and with less rapid cerebral consequences. However, brain damage that has occurred in the meantime is less likely to be reversible and the outcome result is one of increased morbidity associated with decreased mortality. This supports the concept of a therapeutic window for intervention at the optimal moment, thereby permitting treatment to result in a normally developing child. MRI, which enables one to assess the brain tissue, the subarachnoid spaces, ventricular size, and the position of the tonsils, in combination with the head circumference and neurocognitive testing, provides the best information for follow-up. Stagnation of the head circumference or rapid closure of the sutures results in a disastrous situation and reveals the loss of brain substance through its incapacity to enlarge the skull by craniofugal pressure; melting-brain syndrome often follows such a phase, again indicating the vulnerability of the cerebral tissue at this age.

Frequency of Vascular Lesions Per Age Group Infants 1. Aneurysmal malformation of the vein of Galen 2. Dural sinus malformation 3. Pial arteriovenous shunt 4. Cavernoma 5. Arterial aneurysm

2.4.4 After 2 Years

Children that have not presented with systemic and hydrovenous disorders will reveal their vascular lesions with neurological symptoms. Cardiac failure does not occur for the first time at this age. Hydrodynamic disorders that were not present before and appear now are caused by mechanical compression of the intraventricular foramen or the foramen of Magendie. Direct compression of the mesencephalic aqueduct, although well known, is in fact extremely rare even in VGAM. Venous thrombosis may start to occur as part of the high-flow angiopathy phenomena (see

Frequency of Vascular Lesions Per Age Group Children 1. Pial arteriovenous malformation 2. Cavernoma 3. Arterial aneurysm 4. Dural arteriovenous shunt (juvenile type)

Congestive Cardiac Manifestations

63

Chaps. 5, 6, this volume). During the follow-up of children, very different issues are recognized. In particular, the hemorrhagic risks are more frequently discussed. Our experience clearly shows that, in the pediatric population during the first 2 years of life, physiological, anatomic, and pathophysiological considerations differ from those in older children. The endovascular technical discussions are trivial considerations when compared with these ongoing changes. At age 3–10 years, these challenges are easier to deal with, and after the age of 10, lesion management requires a more classical knowledge of lesion risk vs treatment risk and feasibility vs patient acceptance. The relationship with the patient changes significantly at this point, and this should never be underestimated, since it often constitutes a particular source of difficulties in the decision-making process at this age. The clinical interaction with young children and adolescents will be particularly challenging and entirely different from those in adults; information to parents also requires thorough knowledge of the consequences of the diseases involved rather than the techniques available.

2.5 Classification by Symptom Group Intracranial AV Shunt in Children Symptom Groups

Systemic manifestations, hydrovenous disorders with tonsillar prolapse, and the melting-brain syndromes are the most typical manifestations of CVAM in young children.

Systemic manifestations Hydrodynamic manifestations Cerebral manifestations

2.5.1 Congestive Cardiac Manifestations

Intracranial AV Shunt in Children In Utero Manifestations Cardiac overload Congestive cardiac failure (cp>200/mn, ventricular extrasystoles, tricuspid insufficiency) Macrocrania Ventriculomegaly Brain loss

High-output cardiac manifestations are the most frequent systemic manifestation encountered. Liver and renal insufficiency occurs secondary to congestive cardiac failure (CCF). Their extent should be carefully assessed in neonates before the therapeutic decision is made (see neonatal score in Sect. 2.6). Cerebral AV shunts are infrequent causes of CCF.When CCF is suspected following clinical examination including cranial auscultation, then confirmation can easily be obtained by transfontanel ultrasound (Pellegrino et al. 1987). Unfortunately, many of these infants are initially considered to have congenital heart disease (Cumming 1980; Long et al. 1974; Massey et al; 1982) and are sometimes subjected to cardiac catheterization (Long et al; 1974; Massey et al. 1982; Pellegrino et al. 1987). Cardiac manifestations secondary to intracranial cerebral AV shunts are extremely variable in extent and vary from severe heart failure with multiorgan failure resistant to medical treatment, to well-tolerated mild cardiac overload or incidental discovery of an enlarged cardiac silhouette. In the past, the prognosis of a newborn presenting with severe heart failure from a CAV shunt was poor, with a mortality rate of 100% (Hoffman et al. 1982; Johnston et al. 1987). However, in recent years, the use of endovascular therapy in newborns and infants has significantly changed this traditionally poor outcome in these patients (Garcia Monaco 1991a). Arterial embolization, although technically challenging in babies weighing only a

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few kilograms, can result in dramatic improvement of cardiac function (see Chaps. 3, 4). Among 600 referred cases (adults and children) with cerebrocranial vascular lesions, only 30 (5%) presented with cardiac symptoms (Garcia Monaco 1991a). However, when only the pediatric population was considered, this figure rose to 19%. Some types of isolated high-flow fistulas in children are surprisingly infrequently associated with cardiac manifestations (see Chap. 4). VGAMs, in contrast, are frequently associated with cardiac manifestations. They account for 73% of the population with CCF or cardiomegaly of cranial cause (Garcia Monaco 1991a). Cardiac angiography is not indicated and may result in transient or permanent impairment of the femoral vasculature. The cardiac manifestations are not specific in suggesting a cranial cause, but occur in the presence of right-to-left shunt, an atrial communication or patent ductus arteriosus (Cumming 1980; Maheut et al. 1987; Pellegrino et al. 1987), or ventricular septal defects. This persistence of a fetal type of circulation should not be regarded as a true cardiac anomaly, since it reflects right atrium volume and pressure overload. In Garcia Monaco’s series, severe heart failure in newborns was always secondary to an intracranial vascular lesion. However, in some instances management of a patent ductus arteriosus may have to be considered (Chevret 2002) prior to active treatment of the intracranial shunt itself. Besides VGAM, cerebral or dural AV shunts can also result in severe CCF (Chan and Weeks 1988; Albright et al. 1983). In addition, CAV shunts produce cardiac failure only at a very young age (1–19 days in Garcia Monaco’s series). The older the child, the lower the chances are of cardiac manifestations and the milder they will be. Mild heart failure or simple cardiomegaly is observed in infants whose chief complaints are macrocrania or other neurological manifestations. In these cases, the etiologic diagnosis occurs later, usually after 6 months of age. The prognosis of severe CCF of cranial origin in newborns or infants has traditionally been considered to be very poor, but this has improved significantly with modern endovascular techniques. Treatment of CCF with giant capillary hemangiomas of the face is different. Symptoms start with the proliferation phase of the lesion at 4–12 months of age. The objective here is to exclude the lesion from the general circulation and to gain time to allow spontaneous regression to occur (see Chap. 11, this volume).

Intracranial AV Shunt in Children Systemic Manifestations Cardiac failure Pulmonary hypertension Renal dysfunction Hepatic insufficiency Coagulation disorders

2.5.2 Hydrodynamic Disorders

A special relation between cerebral veins and water absorption has been suspected for a long time: The hypothesis that cerebrospinal fluid is absorbed by the Pacchionian granulations is instantly shattered by the fact that these structures only develop in time. They do not exist in infants and young children, nor do they exist in many animals. (Dandy 1929)

According to Le Gros Clark (1920) and Gomez et al. (1981), changes leading to the development of arachnoid villi and granulations are confined to the posterior half of the superior sagittal sinus; lacunas are present

Intracranial AV Shunt in Children Hydrodynamic Manifestations Macrocrania Ventriculomegaly Hydrocephaly Tonsillar prolapse Melting brain syndrome Hydromyelia

Hydrodynamic Disorders

65

during the 26th week, and by the 35th week typical arachnoid villi are seen. These increase in size and complexity during childhood. The first appearance of complex proliferations has been reported by the 18th month. However, both contributions do not provide information on the function of the developing arachnoid villi and granulations. More recently, Welch and Friedman described the flow patterns through the labyrinth of small tubes in monkey villi: the tubes are closed by high pressure in the venous sinus and opened by high CSF pressure. However, the CSF flow through human arachnoid granulations may not be as responsive to venous sinus pressure as in the animal villi (Upton and Weller 1985) The various steps and the schedule of this maturation are poorly understood. Only a few facts seem established or accepted, e.g., the development of the villi is not mechanically related to the formation of the subarachnoid space. Villi have been described in the lungs of South American Indians living at a high altitude; the presence of the villi was related to the permanent edema present in the interstitial tissue. The growth of the villi is linked to the superior sagittal sinus (SSS) development. For a long time, evidence of villi could only be found along the posterior half of the SSS. Although visible at neonatal and infant ages, villi and granulations do not show full complex development until infancy or early childhood. Although factors of functional maturation are unknown, relationships can be postulated between villi function and venous hemodynamics. The venous system continues developing during the first few months of life, and this venous hemodynamic maturation may play a significant role in villi development. In normal situations, specific features of cranial venosinus flow include pulsatility, negative pressure (sump effect), and absence of valves. In babies, Valsalva episodes are more frequent, which primarily increases venous pressure, but also suppresses the diastolic flow in the arteries to the brain. These observations led to the belief that most of the cerebral blood flow is, to a significant extent, sumped by the venous system rather than pushed as in any other part of the body (with the possible exception of the lungs). In abnormal conditions such as high-flow AV shunts, the sinusal negative pressure is diminished. The arterial steal phenomenon, noted in some rare cases, is associated with the disappearance of the arterial diastolic flow. If these changes are sufficient to create the link between villi and sinuses and their progressive postnatal maturation, then the question remains of where the water is reabsorbed in the meantime (Scheme 2.9). Again, certain facts should be recalled: (a) the lack of ependymal resistance to free exchange between the fluid in the extracellular space (ECS) and the CSF, and (b) the similar composition of ECS and CSF may have a direct bearing on the possibility that the parenchyma is the main source of nonchoroidal CSF formation responsible for up to 10%–20% of CSF production (McComb 1983). Since the venular endothelium is comparable to that of the capillary bed, the venular endothelial cells possess a comparable polarity and perhaps participate in the active regulation of the ECS and CSF environment. It has been suggested that the intraparenchymal vasculature is directly linked to the sequestration and removal of substances moving in and between the CSF and the ECS. Such a vascular uptake of CSF sub-

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Scheme 2.9. Cranial hydrodynamic circuits. CSF, cerebrospinal fluid

stances may have a significant role in the absorption of CSF and the maintenance of a homeostatic environment (Povlishock and Levine 1984). From our experience in vascular disorders in neonates and infants, we believe that, both normally and in the presence of an intracranial AV shunt, the intrinsic and CSF fluids are mainly reabsorbed into medullary veins of the brain and cerebellum. As soon as the conditions are met to recruit villi functions, a progressive shift will take place, separating the intrinsic system and the extrinsic types of resorption. Since all cerebral veins open into the torcula at birth, the system is obviously convergent and therefore poorly compliant in the case of early intracranial AV shunt; normal secondary capture of the middle cerebral veins by the cavernous sinus is the earliest diverging opportunity for venous drainage of the brain. Ophthalmic and facial veins as well as the pterygoid plexuses may become important associated venous (and water) pathways, despite their different hemodynamic regimen in the facial and external jugular veins. In high-flow AV shunts draining into the torcula, the facial veins have a comparatively lower pressure than the SSS; pulmonary hypertension, maturation of fetal circulation, and progressive skull base growth will all further increase the positive pressure changes in the sinuses. We therefore accept the observations that hydrodynamic disorders are usually absent in neonates and develop after a free interval in infants. Later on, the fusion of the sutures will contribute further to the advent of a poorly

Hydrodynamic Disorders

67

Fig. 2.23. A 12-year-old boy presented with a vein of Galen dilation due to a choroid plexus arteriovenous lesion. Following chronic venous sinus congestion, note the significant enlargement of the cranial bones

Scheme 2.10. Events likely to interfere with the hydrovenous maturation process

compliant hydrovenous system, in particular when the villi have not become functional. Diploic engorgement and bone thickening (Figs. 2.23) are associated with this search for collateral circulation into the subgaleal veins and cranial lymphatics (Scheme 2.10). The sequence of hydrodynamic impairment events may occur as follows in intracranial AV shunts: a stabilized shift in hydrovenous function with abnormal parameters creates macrocrania.A ventriculocortical gradient allows reabsorption of the secreted water as well as some transmeningeal passage in the dural venous network present at that age. Progressive failure in the medullary venous system, worsened by jugular stenosis that progressively accompanies the macrocrania, produces a loss in the ventriculocortical gradient and causes ventricular enlargement, hydrocephalus with raised intracranial pressure (ICP). Subependymal atrophy (with normal ICP) resulting in slowly progressive ventriculomegaly represents a different effect of the same constraints and failure.

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Fig. 2.24A–C. A female neonate presented with cardiac failure. A MRI performed at that time shows the small vein of Galen aneurysmal malformation. At 5 months, following progressive macrocrania, the child was shunted. She rapidly developed neurological problems in relation to a slit ventricle syndrome. B, C MRI performed at that time demonstrated the rapid tonsillar prolapse with the enlargement of all the perimesencephalic and pontine veins. D see p. 69

It points to the trophic role of the hydrovenous equilibrium in the interstitial space. At the hydrocephalic stage, ventricular shunting will reverse the necessary ventriculocortical gradient without treating the cause and often leaves residual ventriculomegaly through subependymal atrophy. Rapid disequilibrium provoked by the ventricular shunting may sometimes lead to slit ventricles (Fig. 2.24). These facts and speculative remarks derived from our experience require special comments for the posterior fossa. In intracranial AV shunts in neonates and infants, the usual posterior fossa drainage takes place through the petrosal vein and superior petrosal sinus toward the cavernous sinus or caudally to the jugular bulb or

Hydrodynamic Disorders

69

Fig. 2.24 (continued) D Emergency embolization resulted in an almost complete occlusion of the malformation, improvement of the tonsillar prolapse, and a decrease in the basal vein network. Clinically, the child improved significantly, but a mild deficit remained following the slit ventricle episode, as well as some degree of mental retardation. She is now 13 years old and has a score of 1

spinal cord veins (Scheme 2.11). Stenosis or thrombosis of the transverse, sigmoid sinus, jugular bulb, or jugular vein will lead to venous reflux into the cerebellar veins from the lateral sinuses or petrosal veins (Scheme 2.12). If at this time the cavernous sinus is not sufficiently developed, then there is insufficient venous outflow pathways for the posterior fossa, resulting in interference with the absorption of the cerebellar water. Hence there is accumulation of intrinsic fluids, leading to an increase in posterior fossa water contents with resultant tonsillar prolapse (Figs. 2.24–2.26).A normal or small fourth ventricle is noted.As the accumulation of brain water supratentorially results in macrocrania, the infratentorial venocongestive status depends on the available outlets and it manifests itself as tonsillar prolapse. Tonsillar prolapse expresses the combined impact of all the posterior fossa hydrodynamic disorders. It is primarily due to the particular physiology of CSF circulation in neonates and infants, but also the congestion of the cerebellar veins into the sinuses (initially patent) and the stiffness of the bony sutures. Secondarily, it is caused by the progressive occlusion of the jugular foramen, which increases the congestion and further delays granulation maturation. It is reversible through a decrease in the sinus venous hyperpressure if the available outlets are sufficient (Fig. 2.27). The fourth ventricle has a slit-like appearance rather than being small in relation to a presumed aqueduct compression by an ectatic venous pouch. Finally, caudal engorgement may involve the spinal ECS, leading to longitudinal cavitation or atrophy (Fig. 2.28). Such a situation is encountered in all types of intracranial AV shunts, VGAM, pial AV shunts, and DAV, provided that the appropriate sequence and timing of events are given.

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Scheme 2.11. (left) Neonatal cerebral venous drainage. At this age, venous drainage converges into superior and posterior sinuses. Posterior fossa drainage is via the mesencephalic vein and the superior petrosal sinus to the cavernous sinus and caudally to the jugular bulb. There is no cortical venous drainage to the cavernous sinus yet (hatched). Arrows indicate pathway flow Scheme 2.12. (right) Infant venous drainage and distal sigmoid venous occlusion (asterisk). With high pressure caused by the arteriovenous shunt in the sinus, flow of the cortical vein is forward into the cavernous sinus. Flow is reversed in the temporal vein as well as in the petrosal and cerebellar veins (hatched). Cavernous high flow via the inferior petrosal sinus to the jugular bulb occurs, as well as via the ophthalmic vein or the vein of the oval foramen. Posterior fossa drainage depends critically on the adequacy of the venous channel supratentorially, the cavernous sinus drainage, and the presence of the patent jugular vein distal to the occluded bulb (double arrow). If there is inadequate drainage, venous flow in the posterior fossa vein becomes stagnant and enlarges the cervical spine veins caudally

Fig. 2.25A, B. A male neonate presented with mild cardiac failure. He was referred at the age of 5 months, at which time he was found to have slight acquisition delay (score of 2). MRI demonstrated single-hole high-flow fistula in the prefrontal branch of the left middle cerebral artery. Note the moderate atrophy around the lesion and the tonsillar prolapse

Hydrodynamic Disorders

71

Fig. 2.26A–D. A male infant presented at the age of 6 months with epistaxis. Macrocrania was noted. He was referred at the age of 2 years with left-sided exophthalmos, intense facial collateral circulation and no neurocognitive delay. On MRI there is evidence of a small vein of Galen aneurysmal malformation with rerouting of the venous blood flow through the left superior petrosal sinus, cavernous sinus, and orbital vein. The tonsillar prolapse points to the posterior fossa hydrovenous disorders

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Fig. 2.27A, B. A young girl was referred to us at the age of 5 years with significant macrocrania already shunted. A MRI demonstrated tonsillar prolapse. B Following embolization, there is almost complete occlusion of the vein of Galen aneurysmal malformation with shrinkage of the ectatic pouch. Also note the hypersignal and the thickening of the cranial vault bones

Fig. 2.28A–C. A young adult male had had a torcular dural sinus malformation with macrocrania since infancy. After 10 years, the lesion is partially thrombosed; note a tonsillar prolapse, upper cervical spinal cord cavitation, and bone hypertrophy. Solid arrows, arterial supply (A), venous drainage (open arrows) (B), and partially thrombosed torcular herophili (arrows) (C). (From Apsimon et al. 1993)

Melting-Brain Syndrome

73

2.5.3 Melting-Brain Syndrome

Melting-brain syndrome consists in the rapid destruction of the brain, usually the white matter, with secondary ventricular enlargement. This phenomena is associated with severe neurological manifestations and no signs of increased intracranial pressure, although they are usually present before the morphological damage is seen. When brain suffering leads to trophic changes, these are usually bilateral and symmetrical; they correspond to a regional decrease in the cerebral blood flow caused by retrograde venous hyperpressure,leading to hydrovenous dysfunction.Arterial steal is not present or accessory in this syndrome.The local atrophy around a PAVM can be a focal expression of this phenomenon (Fig. 2.29). These findings are never encountered in adults. It illustrates the role played by the subpial and medullary veins in the maintenance and development of the white matter. It may not be seen in lesions that open without restriction into a subarachnoid venous outlet. We have observed it in neonates and young infants (up to 3 months of age) in all types of AV shunts: VGA, DSM, and PAVM. However, while the mechanism is the same, each lesion creates the condition (regional hydrovenous dysfunction) in a different fashion (Table 2.3).

Fig. 2.29A, B. A 10-year-old girl presented a cerebellar arteriovenous malformation revealed by a generalized seizure. Note the cerebellar atrophy detected at MRI examination. Clinically, she has mild cerebellar ataxia

Table 2.3. Melting-brain syndrome Etiology

Prenatal

Neonatal

Early infancy

Late infancy

VGAM DAVS PAVM

++a + –

+++ ++b 0

– +++ ++c

+ – +++

Cumulative negative factors include the following: no cavernous sinus opening of cerebral venous drainage; pial vein congestion, or decreased venous flow with hydrodynamic disorders; progressive sinus stenosis and secondary thrombosis; venodural sinus junction incompetence with or without raised intrasinusal pressure and pial vein reflux. VGAM, vein of Galen aneurysmal malformation; DAVS, dural arteriovenous shunt; PAVM, pial arteriovenous malformation; +++, very frequent; ++, frequent; +, possible; –, not seen. a Systemic mechanism. b Dural malformative mechanism. c Hydrovenous congestive mechanism.

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Fig. 2.30A–C. Legend see p. 75

▲

Melting-Brain Syndrome

Fig. 2.30A–H. A young boy presented at the age of 4 months with macrocrania. A–C At the age of 6 months, initial MRI (not shown) and angiogram confirmed the diagnosis of a small vermian arteriovenous malformation; retrograde congestion of the torcular in relation to bilateral stenosis of jugular bulbs had already occurred. The venous drainage of the carotid injection demonstrates the difficulty of drainage associated with restriction of the outlets. One month later, the child became comatose. D, E Angiography demonstrated a complete occlusion of the jugular bulbs. F–H Major melting-brain syndrome is seen in the frontal region. Note in this particular patient the small size of the lesion and the absence of arterial steal phenomenon. The child died soon after these examinations. (Courtesy of R. Piske)

75

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

In VGAM, the damage starts during fetal development in relation to the systemic failure; the combination of venous and arterial disorders may accelerate the melting phenomena. In DSM, the malformation of the sinus and the early occlusion of the few venous outlets available rapidly precipitate the central venous drainage. In CAVM, the phenomenon occurs late (at 7–8 months of age) and progressive spontaneous thrombosis of the venous drainage has to occur to provoke the syndrome in the absence of patent alternate pathways (Fig. 2.30). This mechanism is progressive and once it starts, it develops fairly rapidly, although it is slow enough to result in a loss of substance rather than a hemorrhagic infarct, which supports the role played by water in the maintenance of brain tissue. In some cases, following limited hemorrhagic infarct, progressive melting is noted despite treatment (Fig. 2.21). In this situation, the venous congestion has been partially or totally relieved, but the insult has remained irreversible. If the insult is even slower, calcifications will take place with a moderate tissue loss until a new equilibrium is found between the remaining brain substance, the available nutrition, and venous outflow. The different outcome in diffuse melting-brain syndrome and the regional type and local atrophy encountered in young children depends on the role played by subpial and subarachnoid venous drainage (Table 2.4). Subpial veins actually communicate with subependymal veins via the medullary veins located in the Virchow Robin spaces and are therefore capable of interfering with the water (intrinsic) equilibrium. In contrast, the subarachnoid veins directly travel in the pericerebral spaces with little impact on the intrinsic water physiology as long as the dural sinuses are sufficiently patent. Thus two high-flow lesions both apparently located on the surface of the brain may have different effects on the underlying cerebral tissue, depending on whether they open directly into subpial or subarachnoid outlets almost independently of the flow they carry. In neonates and infants, this equilibrium represents a highly sensitive system. Any shift in the hydrodynamics will have a regional effect, and any decrease in the ventriculocortical gradient will alter the growth of the corticosubcortical substance. Water retention is often noted before the obvious destructive phase of the brain: most melting-brain syndromes provoke macrocrania before the head circumference curve falls below normal values. The fear of being confronted with such a syndrome should prompt therapeutic attempts, provided that one is able to identify irreversible damage and predict the degree of residual disability if treatment succeeds in limiting damage (Fig. 2.22). Appropriate knowledge and understanding of the natural history and pathophysiology of VGAM, DSM, and CAVM disorders in neonates and infants is mandatory. The so-called melting of brain tissue may be an apoptotic phenomenon triggered by the hydrovenous disorders described above.

Intracranial AV Shunt in Children Cerebral Manifestations Venous congestion Venous ischemia Haemorrhagic infarct Melting brain syndrome Arterial steal

Intracranial AV Shunt in Children Neurological Symptoms Mental retardation Epilepsy Deficit Hypertony and abnormal movements Headaches

Clinical Evaluation Scores

77

Table 2.4. Systemic hydrovenous manifestations in arteriovenous shunts and their specific main venous drainage Manifestation

Drainage

Cardiac failure

Melting-brain syndrome

VGAM AVF pial AVM subpial Nidus or fistula Subpial AVF Epidural AVF

Choroidal vein Subarachnoid vein Subpial vein

+ + ±

+ – ++

Subarachnoid vein Epidural venous system

± ±

– ±

VGAM, vein of Galen aneurysmal malformation; AV, ateriovenous; AVF AV, fistula; AVM, AV malformation.

2.6 Clinical Evaluation Scores With the tendency to use sophisticated tools to approach brain function in children, combined with our lack of knowledge on the physiology and plasticity of the brain at this age, clinical evaluation represents one of the most important and difficult aspects of management in children. Perinatal and early childhood examinations are challenging for neurologists and even more so for neuroradiologists. With the quality of images obtained, a strict morphological result, elegantly photographed, is often felt to be eloquent enough. However, this satisfaction cannot be complete without appropriate clinical assessment and follow-up. This is the primary therapeutic goal and challenge for us: a child growing normally is more important than one that is morphologically cured but disabled. With the increasing role of neurological interventions in children and the full-time involvement of pediatric neurosurgeons, attention has been directed toward the peritherapeutic clinical follow-up, with an attempt to use reliable scores and evaluation scales. More recently, we have been contributing to pretherapeutic evaluation in neonates and follow-up in these children in order to anticipate early delays and identify reversible situations. This subsequently led us to the therapeutic window concept, in which early management is a complex technical challenge with few chances of a good clinical outcome (see Chap. 3, this volume), and late management, although easier, will not be able to correct irreversible functional damage (see Chap. 4, this volume). Three aspects of the classical clinical references available illustrate the difficulties we face in trying to compare our individual results: 1. The adult scores do not apply: Glasgow (initial and outcome) and Karnowski (Tables 2.5–2.7). 2. Pediatric scores are usually simple but do not take into consideration the vascular nature of the lesion, but rather the static analysis of a traumatic insult to an otherwise normal brain (Tables 2.8, 2.9; Seshia 1988;Yager 1990; Reilly-Simpson 1982, 1988; Raimondi 1984).

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Table 2.5. Adult Glasgow Coma Scale Score

Eye opening

Verbal response

Motor response

6 5 4 3 2 1

– – Spontaneous To speech To pain None

– Oriented Confused conversation Inappropriate words Incomprehensible words None

Carrying out commands Localization of pain Withdrawal from pain Abnormal flexion Extensor response None

World Federation of Neurological Societies grading is as follows: grade I, for a total Glasgow score of 15; grade II, for a total Glasgow score of 13/14 without deficit; grade III, for a total Glasgow score of 13/14 with deficit; grade IV, a Glasgow score of 7–12; grade V, a total Glasgow score of 3–6.

Table 2.6. Adult Glasgow Outcome Score Score

Outcome

5 4

Good recovery; full independent life with minimal neurological deficit Moderately disabled; neurological or intellectual impairment, but independent Severely disabled; conscious, but totally dependent on others Vegetative Death

3 2 1

Table 2.7. Karnovsky Scale Score

Patient’s condition

100 90 80 70 60 50 40 30 20 10 0

Normal, no complaints Normal activity, minor signs Normal activity with effort Can care for self, but unable to carry out normal activities or do active work Requires occasional assistance Requires considerable assistance and frequent medical care Disabled; requires special care and assistance Severely disabled; hospitalization necessary Very sick; hospitalization necessary Moribund Dead

Clinical Evaluation Scores

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Table 2.8. Modified Adelaide Pediatric Glasgow Coma Scale (Simpson et al. 1991) Score

Eye opening

Verbal response

Motor response

6 5 4

– – Spontaneous

Carrying out of commands Localization of pain Withdrawal from pain

3

To speech

2

To pain

1

None

– Oriented (smiles) Words (can be consoled when crying) Vocal sounds (inconsistent, consolable) Cries (not consolable, irritable, restless) None

Abnormal flexion to pain (decortication) Extension to pain (decerebration) None

Modified from the Children’s Coma Scale (CCS), derived from the Glasgow Comas Scale by Hahn (1988).

Table 2.9. Pediatric milestones (Adelaide Pediatric Coma Scale; Simpson et al. 1991)

Motor responsesa

Verbal responsesb

a b

Age

Response

Birth 12 weeks 20 weeks 26 weeks 32 weeks 48 weeks 52 weeks 18 months 2 years Birth 8 weeks 16 weeks 28 weeks 48 weeks 52 weeks 18 months 24 months 3 years 4 years 5 years

Spontaneous and reflex flexion and extension Selective movement of limb when pricked Voluntary grasp Voluntary transfer Gazes directly at limb when pricked Gives toy to examiner Localizes prick exactly Obeys simple orders Points to parts of the body Cries Vocalizes (chiefly vowels) Laughs, uses consonants Syllables (ba, da, ka, mu) One-word utterances with meaning Two- and three-word utterances with meaning Jargon, many intelligible words Spontaneous two- or three-word sentences Asks questions, uses pronouns Talks fluently, often fabricates or fantasizes Answers age questions correctly, knows name, draws man

Motor coma norms: flexion, 0–26 weeks; localization or pain, 6 months to 2 years; obeys orders after 2 years. Verbal coma norms: cries, 0–26 weeks; vocal sounds, 26–52 weeks; words, 1–5 years; oriented verbal response, after 5 years.

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3. Neonatal neurological assessment is a particularly difficult issue, with little attention paid to possible systemic manifestations (Duncan et al. 1981; Table 2.10). We therefore have had to develop several scores and have combined these in accordance with our personal experience since 1982: – A neonatal score, particularly oriented to choose the timing for embolization and predict the neurological outcome in severe systemic disorders. Most of these neonates have a limited neurological examination (Table 2.11). – An initial and outcome score for infants and older children, introducing developmental delays with focal neurological deficits and systemic cardiac manifestations. This gross categorization attempts to introduce the quality of a cognitive result, despite the neurologically normal examinations often reported (Table 2.12). – The Denver and Brunet Leisine test for neurocognitive evaluation was chosen by our pediatric neurology group, despite its imperfection, for its ease of use and acceptable quantification regardless of cultural differences (Schemes 2.13, 2.14). We have found these tools useful, not to give universal rules but rather to compare and rationalize our decisions over time. We have been able to assess the stability and accuracy of the criteria chosen to establish the therapeutic objectives.(Scheme 2.15; Fig. 2.30) Our experience has shown that these scores do not seem to apply only to Caucasians, but can be applied in many different cultures, and they appear to confirm that cultural differences in terms of life, death, and handicap are smaller among children than adults.

Table 2.10. Neonatal Coma Scale (Duncan 1981) Score

Response to bell

Response to light

Motor response

6

–

–

5 4 3 2 1

Facial and extremity movements Grimace, blink Increase in righting reaction Seizures/extensor posturing No response

– Blink, facial/extremity Blink Seizures/extensor posturing No response

Spontaneous periods of activity alternating with sleep Occasional spontaneous movements Extremity movementsa Grimace/facial movementsa Seizures/extensor posturinga No responsea

a

Response to sternal rub.

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Table 2.11. Bicêtre Neonatal Evaluation Score Pointsa

Cardiac function

Cerebral function

Respiratory function

Hepatic function

Renal function

5 4

Normal Overload, no medical treatment Failure: stable with medical treatment Failure: not stable with medical treatment Ventilation necessary

Normal Subclinical isolated EEG Abn’s Nonconvulsive intermittent neurologic signs Isolated convulsion

Normal Tachypnea, finishes bottle

– –

– –

No hepatomegaly, normal function

Normal

Hepatomegaly, normal function

Transient anuria

Permanent neurological signs

Moderate or transient hepatic insufficiency Abn coagulation, elevated enzymes

Unstable diuresis with treatment

Resistant to medical treatment

Tachypnea, does not finish bottle Assisted ventilation, normal saturation FIO2 <25% Assisted ventilation, normal saturation FIO2 >25% Assisted ventilation, desaturation

3

2

1

0

Seizures

Anuria

a

Maximal score: 5 (cardiac) + 5 (cerebral) + 5 (respiratory) + 3 (hepatic) + 3 (renal) = 21. Abn, abnormal; FIO2, inspirated fraction of oxygen.

Table 2.12. Bicêtre Admission and Outcome Scoresa (BAS and BOS) Score

Condition

5 4

Normal (N) Minimal non-neurological symptoms (MS), not treated and/or asymptomatic enlargement of the cardiac silhouette Transient neurological symptoms (TNS), not treated and/or asymptomatic cardiac overload with treatment Permanent minor neurological symptoms, mental retardation of up to 20%; nonpermanent neurological symptoms (MNS) with treatment; normal school with support and/or cardiac failure stabilized with treatment Severe neurological symptoms (SNS), mental retardation of more than 20%; specialized school and/ or cardiac failure unstable despite treatment Death (D)

3 2

1

0 a

Does not apply to neonates.

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Scheme 2.13. The Denver and Brunet Leisine test for neurocognitive evaluation

Clinical Evaluation Scores

Scheme 2.14. Percentage of children who passed the test in Scheme 2.13

Scheme 2.15. A Typical curve in a macrocranic female and response following transarterial embolization (E). Normal curves in (B) boys and (C) girls (see p. 71)

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Scheme 2.15. B,C

Familial Hemiplegic Migraine

85

2.7 Revised Concept of the Congenital Nature of Vascular Malformations With increasing knowledge on neural crest derivatives, it is clear that the homeobox-containing genes and endothelial cell physiology genetics in vascular diseases will provide the key to future understanding and management of vascular disorders. Clinical, surgical, and autopsy data have provided a great deal of information and probably have not reached their limits. However, they appear to be advancing too slowly for the questions raised today. Biology, genetics, and morphology are introducing time as a new dimension (the fourth dimension: time and duration) in our practice. Unfortunately, our culture and capacity of imagination are limited, since they do not evolve at the same speed as the advances currently underway.

2.7.1 Genetics Familial Diseases (seldom symptomatic at pediatric age) Arterial aneurysm (PKD, Chr16, Chr4, ... ) Pial arteriovenous shunts (HHT, Chr12, Chr9) Usually high-flow (multifocal AVFs) ED chr.2, NF1chr.17: „spontaneous“ AVFs, para chordal AVFs Cavernomas Chr7: often multiple in the brain and the cord BRBN Chr 1, Chr 9

Several diseases are known to be hereditary. Some have been related to a chromosome disorder, and others have been localized to a single gene (Table 2.1). In clinical practice, the quest for familial disease is imperative and yet seldom fruitful. Although little use can be made of such findings today, future gene therapy and genetic counseling will transform the prognosis of many of these diseases. Some genealogical trees are difficult to establish, and patient interviews may be misleading if precise inquiries are not undertaken in order to establish the reality of a hereditary disease. The possibility of including information pertaining to relatives or even requiring their presence for possible interview purposes should be strongly considered. We had such an opportunity with a family in which three male members of the same generation presented with neonatal or infantile hemiplegia (Scheme 2.16). The decoding process of the events described by the family members was particularly fruitful, and the exceptional character of the initial findings was not as unique as we initially thought. The following diseases were recently identified or are entering direct research programs (obviously many more are being considered for genetic research, but the following are often discussed in our daily practice).

2.7.1.1 Familial Hemiplegic Migraine

Familial hemiplegic migraine (chromosome 19; Joutel et al. 1993) is similar to cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) and consists of migraine attacks marked by the occurrence of a transient hemiplegia during the aura. The age of onset varies from 5 to 30 years, but it is predominant during youth.

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Scheme 2.16. Genealogical tree of a HHT family affected by neonatal/pediatric hemiplegia. Asterisks indicate patients seen as out-patients. PAVF, pulmonary arteriovenous fistula. The numbers are the ages of the family members(y, years; m, months) (see Fig. 18.1)

2.7.1.2 Familial Cerebral Aneurysms

In Finland, 10% of patients with ruptured aneurysms have a family history of aneurysmal subarachnoid hemorrhage (91 families with 203 arterial aneurysms). Of these, 54% are female and aged around 49 years. Middle cerebral arterial aneurysm was found in 47% of these patients (Ronkainen et al. 1993). A prospective study in healthy family members showed incidental arterial aneurysms in 12%. The chromosomes involved are not yet known (see Chap. 17, this volume).

2.7.1.3 PKD1 and Bourneville PDK1-PDK2

These are the two recognized genes of Polycystic kidney disease (PKD). They are located, respectively, on chromosome 16 (translocation that represents 85% of PKD cases, in the vicinity of the Bourneville disease), and on chromosome 4. PDK1 codes a polycystin membrane protein. With the advancement of molecular genetics, the deletion of the TSC2/PKD1 gene at chromosome 16p13.3 has been discovered to be responsible for the tuberous sclerosis complex sharing some of the clinical manifestations of autosomal dominant adult polycystic kidney disease such as multiple renal cysts and intracranial aneurysms (see Chap. 17, this volume).

Familial Cavernomas

87

2.7.1.4 Ehlers-Danlos Type IV

This belongs to the collagen diseases. Diagnosis is established on cultured fibroblasts that synthesize abnormal type III collagen. A mutation in the gene for the type III procollagen (COL 3A1) is the cause of the disease, which is transmitted as an autosomal dominant trait on chromosome 2. It is associated with arterial ruptures and aneurysms (see Chap. 17, this volume).

2.7.1.5 Multiple Cutaneous Mucous Venous Malformations, Blue Rubber Bleb Nevus Syndrome

The dominantly inherited gene lies within a 24-cM interval on chromosome 9p. The alpha and beta interferon gene cluster and the putative tumor suppressor genes MTS1 and MTS2 are also incorporated into this locus, chromosome 9p. A few cases of autosomal dominant inheritance have been reported, but most cases published are sporadic. BRBN is characterized by multiple cutaneous venous malformations in association with visceral lesions, most commonly affecting the gastrointestinal tract. Some case reports have demonstrated involvement of the central nervous system (see Chap. 8, this volume).

2.7.1.6 CADASIL

This disease (Tournier Lasserve 1993; chromosome 19q12) leads to dementia, but starts in early or mid-adulthood. There is no arterial hypertension, no atherosclerosis, and no amyloid angiopathy (see Chap. 18, this volume).

2.7.1.7 Familial Paragangliomas

This disease (Hentink 1992; chromosome 11q23ter) shows that clinical manifestations are determined by the sex of the transmitting parent. All affected individuals have inherited the mutated gene from their father. Expression of the phenotype is not observed in the offspring of an affected female until subsequent transmittance of the gene through a male carrier (see Chap. 4, Vol. 2).

2.7.1.8 Familial Cavernomas

Familial cavernomas are autosomal dominant, and the genetic localizations are on chromosome 7q21–22 CCM1 (KRIT1 is the mutated protein CCM1), 7p13–15 (CCM2), 3q25,2–27 (CCM3) (Günel 1995) (see Chap. 8, this volume).

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2.7.1.9 Neurofibromatosis-1 and Other Collagen Diseases

Only neurofibromatosis-1 (NF1) leads to vascular anomalies; known as peripheral neurofibromatosis, it is carried by chromosome 17 (17qll.2), and the gene was recently cloned. Vascular lesions will result from infiltration of the vessel wall, and are characterized by stenosis, occlusions, aneurysms, and fistulas by rupture of a weakened arterial wall. Meningoceles and dural ectasias are also noted. Renal stenosis is the most frequent vascular lesion, but is only associated with significant renovascular hypertension in less than 1% of cases (Pope et al. 1991; Schievink and Piepgras 1991) (see Vol. 2, Chap. 7). Neurofibromatosis-2 (NF2) is carried by chromosome 22 does not lead to vascular manifestations. In fact, familial diseases and genetic discussions tend to simplify to a mechanical sort of relationship a demonstrated gene alteration and a function or a disease. The phenotypic expression of HHT is very illustrative of this type of challenge.

2.7.1.10 Hemorrhagic Hereditary Telangiectasia or Rendu-Osler-Weber Disease

The clinical aspects of the disease (chromosome 9q33–34; Shovlin et al. 1994) will be discussed in Chaps. 4 and 5, this volume. However, the authors concluded that HHT is a heterogeneous disorder, which certainly fits with our observations. According to Shovlin, based on its map location (9q33–34) and expression in vascular tissues, type V collagen is a possible candidate gene for HHT. If a single genotype is considered, several mutations involving endoglin can be seen, one per family. Certain manifestations (head and neck vs digestive tract) are frequently seen within one family. Yet in the head and neck group of families, certain characteristics are not transmitted, in particular CAVM or CAVF. It seems, however, that AVFs are typical if not specific of AVSs in young children (Fig. 2.31). The AVSs in adults tend to be expressed through nidus arranged lesions (AVMs). Since there are several foci in both types, why would this occur?

▲

Fig. 2.31A–E. A 1-year-old boy with familial history of ROW disease was first admitted with disturbances of consciousness and intraventricular hemorrhage on CT (A). Angiography (B–D) revealed three AVMs, two in the right cerebellar lobe and one SCAVM at C2 and C3. The main cerebellar arteriovenous shunt (AVS), supplied by the right AICA, appeared with an ectatic venous drainage of the posterior fossa and venous pseudoaneurysm. The cord lesion seemed more nidus arranged. In HHT, the cerebral AV shunts (with the same apparent genotype) diagnosed in children vs those in adults are very different. They are likely to represent two morphological expressions of the same venous malformation triggered at different maturation stages or phases of the endothelial cell (re)generation cycle. For comparison (C, E), see experimental lesion in mice end +/- Toronto group

Hemorrhagic Hereditary Telangiectasia or Rendu-Osler-Weber Disease

Fig. 2.31A–E. Legend see p. 88

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Is there a different genotype? It is unlikely that the two genotypes presently known and the AVF trait are linked to one group of other phenotypic expressions.
Is there a different mutation? If one mutation is specific for a given family this trait would be more frequently expressed in that family in comparison with others with the same genotype.
Do all cells share the same defect because its expression is related to environmental conditions? These will either compensate or on the contrary betray the quiescent damage or dysfunction. The fact that the AVF is seen in babies points to the early timing of disclosure (or failure to compensate). The same genotype and mutation better compensated or triggered later will show itself later in older children. The fact that the architecture of the lesions (nidus) is different does not point to a specific genotype but rather to a difference in timing of the window of exposure (perinatal vs childhood). The power of interference of the endoglin deficiency varies with age, or an unknown associated failure of a compensatory system does not allow the vascular tree to pass this window of vulnerability (Mahadevan et al. 2004).
One can only be puzzled by the peculiarities of HHT: no new intradural shunts have been seen during patient follow-up; all lesions in a given place, whether AVFs or AVMs, appear at the same time. This is specific of the brain and spinal cord, as pulmonary AVFs do appear during follow-up. This favors a rather systemic type of secondary event in relation to the multifocality of the disease expression to support the simultaneous appearance of the AVFs and AVMs. It is unlikely that a focal event would impact simultaneously remote sites on different cerebral hemispheres, supra- and infratentorially or in the brain and spinal cord.
In contrast, the impact of the mutation on the vessel wall remodeling in other areas with different environments and life spans (maxillofacial) leads to progressive appearance of telangiectasias with age (they are absent in children when the disease may have already expressed with highflow multifocal CAVFs). This points to the potential role of the surroundings (brain or maxillofacial) with respect to vessel wall (vein) construction, renewal, and thus vulnerability. This compensatory role can protect, repair, or reveal an impaired structure (or cascade) and directly interfere with the disease expression according to place (Scheme 2.17) and age (Scheme 2.18). This links certain disease geotropism and age of onset.
The fact that an AVF reveals at perinatal age does not prove the overall systemic weakness of the fetus; it remains as a focal problem with good systemic compensatory resources; properly treated at the right time, such a situation will lead to normal neurocognitive development. Improperly treated or at the wrong time, the permanence of the induced hemodynamic conditions will rapidly compromise the maturing system and engender new disorders.
In other situations, the weakness that led to the AVF revelation impacted the rest of the maturing cascades, reducing the compensatory resources to inefficiency; at that stage, regardless of what will be done on the AVF, the entire body enters an irreversible disequilibrium. Between these extreme situations each neonate and infant reacts with its own systemic resources that is best appreciated with the neonatal score.

Hemorrhagic Hereditary Telangiectasia or Rendu-Osler-Weber Disease

91

Scheme 2.17. Underlying steps from genotypic to phenotypic expression in neural crest migration. ML, medial lateral; CC, craniocaudal; VD, ventrodorsal

The younger the child, the more dynamic and interrelated the developing organs and functions, and the more compliant and adaptable the child is as well. Looking at diseases as fixed targets requiring mechanical correction ignores the dynamic nature of the morphological growth of the perinatal phase. The risk is to overcorrect a situation. Interdependence between systems should be corrected to relieve the bulk of abnormal signals, allowing for spontaneous repair. Partial targeted embolization, staged procedures and proper timing are key issues in the management of such diseases at that age. In other situations, we tend to ignore the identity changes that tissues have undergone following maturation and integration to a given environment. In this later misconception all arteries or veins are postulated to be the same throughout the body and therefore have equal capacity to express a genetic disorder. Experience shows that although shared by all cells, genetic defects will express in some areas and will spare others. This segmental vulnerability is well illustrated in diseases that affect the arterial wall. For example, describing a distal, subpial MCA aneurysm as a „berry aneurysm of the distal branches of the MCA“ (Peters et al. 2001) is a misnomer since this denomination is traditionally used for subarachnoid aneurysms. The former ruptures and gives intracerebral hematoma and the latter a subarachnoid hemorrhage. Stressing the role played by the extravascular space certainly points to the fact that the subpial environment is significantly different from the subarachnoid environment in the generation of the aneurysm, its rupture, and the response to that rupture. The age of the lesion (how long has aneurysm been present unruptured) and the exact time(s) of rupture are both unknown. Using the STA or another, easy-to-access artery for structural comparison and extrapolation is probably incorrect. It mistakenly postulates that the arterial system is homogeneous and that vessels such as the middle

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Scheme 2.18A. Vascular vulnerability phenotypic expression: continuous variability

Scheme 2.18B. Vascular vulnerability phenotypic expression: uncertain variability

Vascular Remodeling and the Congenital Nature of Arteriovenous Shunts

93

cerebral artery (MCA) and superficial temporal artery (STA) can be compared. The segmental vulnerability will show that these vessels have significant phylogenetic, embryologic, and hemodynamic differences. The hemodynamics and shear stresses in both systems are different, with no diastolic flow occurring in the STA. In addition, the STA does not develop aneurysms, which is a characteristic of the external carotid biological evolution in comparison to the internal carotid branches. The few aneurysms described in the superficial temporal arterial system are seen following trauma or MCA–STA anastomoses, which introduces a diastolic flow in the external carotid artery (ECA) and subsequently in the STA. This certainly emphasizes the role played by the environment and that of the signals coming from a distal territory, the surrounding tissue in the regulation and expression of the various genes. One can also question the maturation over time of some genetic programs of modeling and remodeling of the brain vessels. The cell turnover and the repair capacities are unlikely to be continuous but rather spread over equal periods throughout life. Postnatal maturation presents additional challenges that one should foresee in interpreting gene expression disorders (Lasjaunias 2000).

2.8 Vascular Remodeling and the Congenital Nature of Arteriovenous Shunts The provocative statement made by Professor G. Yasargil in the 1980 s regarding the possible noncongenital origin of cerebral AVM was not fully accepted at that time, although some felt it might be correct. The role of the endothelial cell is becoming better understood, and experience gained in prenatal diagnosis and progressive treatment of these lesions gives further credibility to Yasargyl’s observation and allows a general hypothesis to be elaborated. In what is considered the normal vascular tree, continuous remodeling will take place. The emerging concept of vascular remodeling is as follows (Gibbons and Dzau 1994). The vessel wall is an active, integrated organ composed of endothelial, smooth-muscle, and fibroblast cells combined with each other in a complex autocrine–paracrine set of interactions. The vasculature is capable of sensing changes within its milieu, integrating these signals by intercellular communication, and changing itself through the local production of mediators that influence structure as well as function. Vascular remodeling is an active process of structural alteration that involves changes in at least four cellular processes – cell growth, cell death, cell migration, and production or degradation of extracellular matrix – and is dependent on a dynamic interaction between locally generated growth factors, vasoactive substances, and hemodynamic stimuli. Remodeling is usually an adaptive process that occurs in response to long-term changes in hemodynamic condition, but it may subsequently contribute to the pathophysiology of vascular diseases and circulatory disorders. The biological process of vascular remodeling may be divided into the following components: (a) the detection of signals due to changes in hemodynamic conditions and humoral factors (sensors);

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(b) the relay of signals within the cell and to adjacent cells (transducers); (c) the synthesis and release of activation of substances that influence cell growth, death, or migration or the composition of the extracellular matrix (mediators); and (d) the resulting structural changes in the vessel wall (both cellular and noncellular components). The endothelial surface is constantly exposed to humoral factors, inflammatory mediators, and physical forces. The endothelium is strategically located to serve as a sensory cell assessing hemodynamic and humoral signals, as well as an effector cell eliciting biological responses that may eventually affect the structure of the vessel.

2.8.1 Endothelium as a Sensor and Transducer of Signals

Hemodynamic stimuli involve, in essence, the vessel remodeling itself in response to long-term changes in flow such that the luminal diameter is reshaped to maintain a constant predetermined level of shear stress. The capacity of the endothelium to sense shear stress is therefore an important determinant of luminal diameter and overall vessel structure (Fig. 2.32). In vitro, increases in shear stress alter the balance of endothelial cellderived mediators involved in the regulation of vascular tone, hemostasis, vascular-cell growth, and matrix production. New evidence suggests that shear stress activates a genetic program that alters the balance of the mediators of remodeling by activating the transcription of genes for factors such as nitric oxide synthase, platelet-derived growth factor (PDGF), and transforming growth factor b1 (TGF-b1).

Fig. 2.32. Arterial adaptations to increased pressure and increased blood flow. (Berdeaux 1994, adapted from Langille 1993)

Clinical Implications of Vascular Remodeling

95

2.8.2 Endothelium-Specific Receptor-Coupled Event

Endothelial cells regulate vascular tone, hemostasis, inflammation, lipid metabolism, cell growth, cell migration, and interactions with the extracellular matrix through many receptor-mediated mechanisms. Similarly, the delicate balance between thrombosis and fibrinolysis involves specific endothelial-cell receptors for proteins involved in both enzymatic cascades.

2.8.3 Endothelium and Mediator-Effector Molecules Involved with Remodeling

Endothelial cells can participate directly in vascular remodeling by releasing or activating substances that influence the growth, death, and migration of cellular elements or the composition of the extracellular matrix. The contents of vessel walls may be determined by a balance between cell growth and programmed cell death, or apoptosis. In contrast to cell necrosis, apoptosis is a selective process of cell loss that occurs without evoking an inflammatory response.

2.8.4 Role of Matrix Modulators in Vascular Remodeling

The extracellular matrix is composed of the scaffolding elements of collagens (type I, III, IV, and IV) and elastin embedded in a mixture of glycoproteins (e.g., fibronectin) and proteoglycans (e.g., heparin sulphate).Vascular remodeling entails the reconstruction of the matrix scaffolding and therefore a process of active proteolysis and resynthesis of these proteins. The theme of homeostatic balance is again evident in that the proteolytic factors produced within the vasculature are counterbalanced by endogenous protease inhibitors. Alterations in the balance of factors modulating matrix composition appear to be important determinants of vessel architecture.

2.8.5 Clinical Implications of Vascular Remodeling

Vascular injury is induced by tissue ischemia resulting from occlusion of the vase vasorum and mechanical injury. Studies suggest that PDGF and TGF-b1 are involved in the neointimal proliferative response to surgical injury. The increased intraluminal pressure appears to result in thickening of the vessel wall. An imbalance between endogenous growth promotors and inhibitors may allow occlusion of vein grafts. Patients with saphenous vein grafts have impaired generation of nitric oxide by endothelial cells and increased angiotensin-converting enzyme activity. Thus, the adaptive response of vein grafts to surgical implantation into the arterial circulation involves a dynamic interplay among vasoactive substances, local growth factors, and hemodynamic stimuli.

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The possible closure of the ductus arteriosus can be induced either by the increased generation of local vasoconstrictors (e.g., endothelin) in response to increased oxygenation at the time of birth or by pharmacological blockade of endogenous vasodilators (e.g., prostacyclins by indomethacin). Hypertensive vessels in animals and in humans are characterized by a thickened media, a reduced lumen, and an increased extracellular matrix. Structural changes in hypertensive vessels are associated with increased expression of growth factors such as TGF-b1, local vasoactive substances such as angiotensin II, matrix proteins such as collagen and elastin, and matrix proteinaceous such as collagenase and elastase. These alterations predispose patients with hypertension to the sequelae of this disorder. Vascular remodeling also influences the natural history of atherosclerotic lesions. The endothelium appears to have a central role in this initiation of atherogenesis by regulating the infiltration of mononuclear cell and endothelial malfunction. We postulate that vascular stenosis increases shear stress and thereby induces an increase in the vessel radius to normalize shear stress, as described above in normal vessels. If this compensatory mechanism fails to keep pace with the growth of the plaque, the stenosis may lead to flow disturbances that further enhance the progression of the lesion and favor platelet aggregation and plaque rupture. Why does balloon angioplasty increase the luminal diameter in the vast majority of cases? Four factors determine the characteristics of flow after angioplasty: capacity of the regenerated endothelial surface to act as a transducer, the relative balance between cell growth and cell death, and the capacity of the remodeled matrix to contract and maintain the geometry of the vessel affected by the endovascular procedure. The resultant luminal diameter will depend on the net balance between factors promoting shear stress-induced expansion of the area of the lumen and the reparative response to injury that promotes restenosis due to the formation of neointima and matrix modulation. With time, the remodeling results in a gradual decrease in compliance, although it usually remains compatible with function. This results in a progressive morphological shift in the angioarchitectural features of the vascular anatomy. The normal endothelial cells adjacent to an AVM play a central role in the remodeling process, and their plasticity is a key factor in understanding the natural history of an AV shunt. It has been demonstrated that in the arterial wall proximal to an AV shunt, changes in pressure within the vessel result in a change in wall thickness (with release of local growth factors), while velocity changes result in lumen enlargement (preserving the wall thickness). The concept of secondary angiopathy related to chronic high flow (or flow changes beyond normal equilibrium) applies to a normally reacting vasculature that has been abnormally triggered by an AVM. This intraluminal trigger is a stress trigger, which can be related to flow, pressure, or other factors (Schemes 2.19a–c, 2.20).

Clinical Implications of Vascular Remodeling

Scheme 2.19A. Constitution of a quiescent AVM

Scheme 2.19B. Revelation of the dormant defect into an AVM

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2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Scheme 2.19C. Induced high-flow angiopathy

It may be postulated that, if triggering events were eradicated, highflow angiopathy would no longer develop or persist. This can be achieved by controlling the AV shunt and is well demonstrated by the disappearance of flow-related arterial aneurysms following successful treatment of a CAVM. This has served as a rationale to offer partial, targeted treatment for certain types of AVMs. Over time, the increased rigidity and fragility of this stressed vascular system becomes evident, when even partial and limited attempts to remediate the abnormal shunting zone lead to failure of the remaining normal vasculature, with early rupture and hemorrhage or ischemia as a result of intervention. These remarks point to the difference that should be made between primary lesion and secondary induced changes that are not part of the CAVM diseases, even if they represent its clinically eloquent part. Still, CAVM, even with variable high-flow angiopathic changes, is a heterogeneous group of abnormalities. With this apparent heterogeneity, some specific features are recognized in young children, including systemic manifestations, hydrodynamic disorders, and severe cerebral trophic changes. The specific morphological alterations encountered during the course of the disease in this age group are striking, as most of them are not observed in otherwise similar AVMs discovered in adults. If the lesions were present during the first few years of life– the time of specific vulnerability of the maturing brain– one would expect to find some degree of brain damage. It has become apparent that AVMs diagnosed in

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Scheme 2.20. Different phases necessary for the development of cerebral arteriovenous malformation (AVM). 1, Quiescent cellular dysfunction; 2, triggered susceptible cell; 3, active AV shunt developing stress trigger (ST) on the proximal and distal vasculature; 4, high-flow angiopathy with proximal arterial aneurysm, distal venous ectasia, and stenosis. RT, revealing trigger

adults are not present at birth, and if their initial course is clinically silent, the lesion was probably morphologically occult (Fig. 2.33). The term „malformation“ means failure to comply to a molded morphology or visible shape. Adding congenital to this denomination needs further explanation. The term „congenital“ means the period of the development that resides in the matrix. This does not mean embryology or genetics. Congenital in short means before birth. If we postulate that AVMs are the result of a congenital event, although occult, its expression will later become morphologically detectable. Its impact is primarily structural, cellular, linked somehow to vascular modeling and remodeling. The quiescent dysfunction that results (and persists over time) must involve the endothelial cells or any cell that interacts directly with its function (e.g., astrocytes, pial, ependymal). For this dysfunction to be eventually revealed as a morphological abnormality, a trigger factor is necessary. We call such postulated triggers revealing triggers (Schemes 2.21, 2.22).

100 2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

Fig. 2.33A–F. Legend see pp. 102

Clinical Implications of Vascular Remodeling

Fig. 2.33G–K. Legend see p. 102

101

102 2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts Fig. 2.33A–K. A 10-week-old boy admitted to the hospital was suspected of having meningitis. On admission he was noted to have on the lower right arm a 3¥4-cm capillary. On CT (not shown) of the skull, a dural arteriovenous fistula of the superior sagittal sinus (SSS) was noted. Electroencephalogram (EEG) showed a left parieto-occipital focal disorder detected in otherwise normal background activity. Antibiotics were given. A At 3 months, magnetic resonance angiography (MRA) confirmed the parieto-occipital, dural arteriovenous venous malformation of the superior sagittal sinus. B Cerebral angiography showed a dural arteriovenous shunt on the superior sagittal sinus. A small associated pial AVM was diagnosed draining into the SSS. C–E MRI shows the focal cerebral atrophy. F–G At the time of embolization of the dural arteriovenous shunt, an increase in the size of the pial parieto-occipital shunt vascular malformation was noted without parallel modification of the dural lesion. At 10 months, there was a slight statomotor developmental delay, possibly due to his environment. Physical examination showed facial venous circulation, especially under the right eyelid. At 15 months, the child had age-appropriate reactions and was in good general and nutritional condition; left-frontal and left-periorbital venous circulation had increased. H–K Follow-up MRI shows two de novo cavernomas, one in the brain stem and the other in the white matter below the enlarged pial shunt. Cerebral MRI of the mother revealed no AVM and no cavernoma

Scheme 2.21. Vascular malformation: target, timing, trigger

Scheme 2.22. Vascular malformation: target, timing, trigger (causative and revealing)

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These triggers may not be identifiable, but are likely to include mechanical, hormonal, pharmaceutical, hemodynamic, thermal, radiation, viral, infectious and metabolic triggers. The nature and timing of the revealing trigger (or triggers) and the nature and timing of the abnormally functioning endothelial cell (or cells) may result in the variety of AVMS that are now recognized (Table 2.1, Scheme 2.6). The developing central nervous system (CNS) is clearly more vulnerable than the mature one; if revealing triggers act during cell migration, myelinization or CSF physiology maturation, while the embryonic brain matures to a fetal one and then to a fully myelinated brain, or until the skull base has largely grown and sutures are fixed, the revealing trigger may affect the vascular target more severely (e.g.? widespread, multifocal). An AVM morphologically and clinically present early in life must have had a more severe initial abnormality to have been effectively triggered over such a short period of time. This suggests that most adult AV shunts are either not present in the child or, if a cellular dysfunction is present, it has not been triggered yet. Therefore, classifications of brain AVMs in fact describe different types of abnormalities that may reveal the underlying timing and/or nature of an initial event (Schemes 2.4, 2.20). For example, there are genetic „dysfunctions“ which lead to multiorgan, multifocal, polymorphic and inherited types of AV shunts: HHT disease, collagen disorders, NF1. An early dysfunction, when hox genes are operating and para-axial neural crest or mesodermic cell groups are still migrating and differentiating (see Chap. 6, this volume), may result later in CAMS, SAMS, or CVMS (Cobb-, Sturge-Weber- or Wyburn-Mason -type abnormalities). Macro-AVM, proliferative angiopathy, and micro-AVM are likely to result from an acquired nonreversible abnormal remodeling process. However, many multifocal AVMs encountered in children do not fall into any of the proposed categories, but rather express the overall cerebrovascular vulnerability to revealing triggers. The vulnerability of the vasculature actually changes throughout life from structural weakness to damaged function. The vessel wall considered then as an organ and not as a semi-passive wall can express a wide range of dysfunctions, many of which are repaired (Scheme 2.18). In our experience, two lesions mainly result from a prenatal revealing trigger. The first occurs at the end of the embryonic period and results in VGAM. The second occurs during the 4th–6th month and corresponds to DSM with AV shunts. Both revealing triggers are certainly different, although they still remain unknown.Although we recently discovered the presence of CAVFs in utero, this remains an exceptional occurrence and represents less then 1% of our total clinical CAVF/CAVM experience (see Chaps. 3, 5, 7, this volume). Some AV shunts may be the result of a remote abnormality (usually downstream and venous), and not the expression of an in situ abnormal cell function; such AV shunts are an upstream normal response to abnormal stress triggers. If the primary cause can be identified and corrected, this AV shunting will spontaneously regress. Unfortunately, in most cases the primary cause of such conditions is difficult to detect. The remote alteration of the vascular remodeling process can produce tertiary abnor-

104 2 Introduction and General Comments Regarding Pediatric Intracranial Arteriovenous Shunts

malities (nonmorphological, such as venous thrombosis and subsequent venous hypertension), which are often considered primary causes; thus the effect is mistaken for the cause and the disease history is read in reverse. Dural AV shunts probably belong to this type of process in which a remote anomaly engenders a proximal AV shunt. This response is potentially multifocal and (as yet) its actual location is unpredictable. It is possible that it develops in a region in which there is a locally increased sensitivity. The aim should be to treat the remote causal anomaly, if detectable, as well as the secondary irreversible undesirable effects. Some iatrogenic interference may actually exacerbate the situation rather than ameliorate it and may behave as a new trigger (therapeutic venous sinus occlusion). Venous approaches to dural AV shunts that achieve sinus occlusion can create new shunting zones away from the primary site. Some lesions result from both postulated processes, for example, the perinatally diagnosed CAVM and even VGAMs, which are triggered by the hemodynamic changes at birth. In this situation, these normal hemodynamic perinatal changes create natural stress triggers that reveal an underlying endothelial cell dysfunction. The neonatal AV shunt in turn engenders specific abnormal stress triggers on the rest of the vasculature; it then becomes a morphologically and eventually clinically detectable AVM. Some rare DSMs revealed at birth and triggered by the normal perinatal changes will continue growing and expressing additional associated lesions in an irrepressible fashion, rapidly leading to fatal outcome regardless of treatment (Fig. 2.13) (Mohamed et al. 2002). An acquired event (revealing trigger) might have the same consequences as the postulated congenital one described above, provided that it affects a target related to vascular remodeling for a certain length of time (extracellular matrix and cells). In these instances, the revealing triggers produce a lesion that mimics a congenital AVM. Vascular malformation is thus a very unsatisfactory term for the cerebral and even more so for the dural AV shunts found in the adult or pediatric populations. Unless we accept the concept of embryonic, fetal, postnatal, and acquired AV malformations, we should rather speak of pial or dural AV shunts. Finally, the AV lesions that most often develop during the embryonic period are VGAMs; some DSMs with secondary AV shunts develop during the fetal period. Nearly all the other intracranial AV lesions develop at the earliest during the perinatal period and most likely after infancy. Such remarks suggest that AVMs are in fact manifestations of various types of vascular failure of normal wall remodeling.

3 Vein of Galen Aneurysmal Malformation

3.1

Introduction 106

3.2 3.2.1 3.2.2

Historical Landmarks 107 Lesions 107 Clinical Aspects 107

3.3

Modern Concept of Vein of Galen Aneurysmal Malformation 109

3.4

Vein of Galen Aneurysmal Dilatation 112

3.5

Dural Arteriovenous Shunts with Aneurysmal Dilatation of the Vein of Galen 117

3.6

Vein of Galen Varix 117

3.7

Vein of Galen Aneurysmal Malformation 117

3.8

Natural History of Vein of Galen Aneurysmal Malformations 141

3.9

Cardiac Manifestations 143

3.10

Macrocrania and Hydrocephalus 152

3.11

Late Natural History of Vein of Galen Aneurysmal Malformation with Patent Sinuses 162

3.12

Dural Sinus Occlusion and Supratentorial Pial Congestion and Reflux 167

3.13 3.13.1

Dural Sinus Thrombosis and Infratentorial Pial Reflux 180 Spontaneous Thrombosis 184

3.14 3.14.1 3.14.2 3.14.2.1 3.14.2.2 3.14.3

Objectives and Methods of Treatment 191 General Remarks 191 Neonates 191 Reducing Oxygen Consumption 197 Improving Oxygen Delivery 197 Infants and Children 200

3.15 3.15.1 3.15.2 3.15.3 3.15.4 3.15.5

Technical Management 203 General Remarks 203 Follow-Up 205 Complications: Morbidity 210 Overall Mortality 220 Neurological Outcome by Age Group 221

3.16 3.16.1 3.16.2 3.16.3

Other Techniques 221 Surgery 221 Transvenous Treatment 223 Radiosurgery 224

106 3 Vein of Galen Aneurysmal Malformation

3.1 Introduction Over the past 10 years, written contributions on cerebral arteriovenous malformations (CAVMs) in children have evolved from anecdotal case reports to short series, offering a better understanding of the disease, the therapeutic strategies, and the results of various management strategies (Ventureyra and Herder 1987; Gerosa et al. 1981; Fong and Chan 1988; Hoffman et al. 1982; Johnston et al. 1987; Lasjaunias et al. 1995, 1996a; Maheut 1987; Mori et al. 1980; So 1978; Raimondi 1987; Seidenwurm et al. 1991). Historical contributions from the neurosurgical point of view have demonstrated limitations in the management of these difficult lesions and relinquished them to interventional neuroradiology. Generally speaking, a review of the literature pertaining to CAVM in the pediatric age group is difficult. The upper limit of the pediatric age group has varied between 15 and 20 years. Few reports have documented the management of AVMs that were not vein of Galen malformations in neonates and infants, or in antenatal series. To differentiate between cortical, deep, and infratentorial AVMs is technically of interest, but the topography is known to be the least important factor in the anticipated natural history (Berenstein 1983; Brown et al. 1988; Crawford et al. 1986; Ondra et al. 1990). Choroidal AVMs, which are rarely analyzed separately, are probably a distinct entity within the CAVMs (see Chap. 5, this volume). Most series are small and difficult to analyze since, for example, a distinction between vein of Galen aneurysmal malformation (VGAM) and CAVM is not always clearly made. Most recent reports no longer confuse VGAM and CAVM, but within the VGAM group, the vein of Galen aneurysmal dilatations (VGAD) (Lasjaunias et al. 1987b) and the true VGAMs are often not distinguished, particularly by those who still use Yasargil’s classification (Yasargil 1988). In large groups of nonoperated patients, information regarding outcome is often lacking. Partial surgical treatment with feeder ligation, while not promoted as such, is often performed. This type of intervention differs from partial embolization with bucrylate, and therefore comparing the two treatment strategies and their results is of little interest. Many of the cases included in the surgical series as children are in fact operated on in adulthood. Evidence of anatomic obliteration and clinical status is often difficult to assess, since few follow-up angiograms have been done and neurocognitive testing has rarely been carried out or reported. Patient selection has been insufficiently documented, and the associated management mortality varies from 0% to 35%, depending upon the aggressiveness of a given team in desperate situations. Technical morbidity/mortality is not distinguished from expected morbidity/mortality despite attempted treatment. This lack of precision tends to promote unnecessary hazardous procedures in potentially nonfatal situations. The same comments apply to reports of series of endovascular VGAM treatment that have appeared in the literature. While emphasizing mainly technical solutions, they often have failed to provide satisfactory mid-term results (Ciricillo et al. 1990; Dowd et al. 1990; King et al. 1989; Mickle and Quisling 1986). Mental retardation in these young children,

Clinical Aspects

107

while often present, is seldom mentioned or tested. Unnecessary premature interventions have also interfered with the quality of the results. To degrade the therapeutic challenge to a strictly morphological goal ignores fundamental aspects of neonatal and infant anatomy and fluid physiology (Andeweg 1989; Girard et al. 1994; Zerah et al. 1992). In fact, in certain reports anatomic exclusion of lesions is counted as technical success even if the child died shortly after treatment.

3.2 Historical Landmarks 3.2.1 Lesions

The first description of a possible VGM occurred in 1895 (Steinhel, cited by Dandy 1928); it was actually a CAVM of the diencephalon draining into a dilated vein of Galen. Today it would be described as a false vein of Galen malformation (Berenstein 1992a; Lasjaunias et al. 1987b). The first therapeutic attempts were recorded at the beginning of this century describing an infant who presented with intracranial hypertension and subsequently underwent bilateral internal carotid ligation. In 1946, Jeager reported bilateral arteriovenous (AV) communications draining into an aneurysmally dilated vein of Galen, and in 1949 Boldrey and Miller treated two similar patients with arterial ligation. Only the last case seems to correspond to a VGAM. Most authors have subsequently used the same generic name, VGAM, for very different entities. Failure to recognize the true nature of the lesion resulted in imprecise anatomic and natural history descriptions (Agee et al. 1969; Amacher et al. 1979; Gold 1946; Gold et al. 1964; Grossman et al. 1984; Horowitz et al. 1994; Martelli et al. 1980; Merland et al. 1987; Norman and Becker 1974; Stehbens et al. 1973; Watson et al. 1976; Yasargil et al. 1976). In fact, Litvak et al. in 1960, Raimondi in 1972, Clarisse et al. in 1978, and Diebler et al. in 1981 already suggested the possible existence of true and false vein of Galen malformations. Subsequent surgical series (Agee et al. 1969; Amacher and Shillito 1973; French and Peyton 1954; Gibson et al. 1959; Hoffman et al. 1982; Johnston et al. 1987; Massey et al. 1982; Menezes et al. 1981; Mickle and Quisling 1986, Mickle and Peters 1993; Raimondi 1987; Smith and Donat 1973) and endovascular series (Casasco et al. 1991; Ciricillo et al. 1990; Dowd et al. 1990; Mickle and Quisling 1986; Reichman et al. 1993) attempted to deal with this rare, and still poorly understood disease entity, often emphasizing the technical challenge related to the treatment, but failed to grasp the real nature of the disease.

3.2.2 Clinical Aspects

The link between the lesion and cardiac failure in neonates was noted by Pollock and Laslett in 1958, Claireaux and Newman in 1960, and Glatt and Rowe in 1960. Since that time, the relationship between intracranial AV lesions and, for instance, hydrodynamic disorders with ventricular enlargement, facial venous collateral circulation in infants, and epistaxis has been accepted. In 1964 in a review of 34 patients, Gold described three

108 3 Vein of Galen Aneurysmal Malformation

consecutive clinical stages: neonates with cardiac insufficiency, infants and young children with hydrocephaly and convulsions, and older children or adults with headaches and subarachnoid hemorrhage. In 1978, Amacher (1973) added a fourth group, which included neonates and infants with macrocephaly and minimal cardiac symptoms. Knudson and Alden (1979) reviewed all cases of cardiac failure secondary to AV shunt and noted that 64% were caused by VGAM. In fact, these contributions were inadvertently combining clinical sequelae created by both the natural evolution of the disease and their post-therapeutic modifications. In his excellent review, Johnston et al. (1987) exhaustively analyzed the clinical presentations of VGAM. In 82 infants, he found the following symptoms: CSF disorders, 70%; neurological deficits, 31%; and neurocognitive delay, 12%. In children 1–5 years of age, these symptoms occurred in 61%, 33%, and 5%, respectively. For comparison, in our series of neonates and infants in the same age group, more than 50% had neurocognitive delay and almost none had neurological manifestations unless they had been previously shunted. This apparent discrepancy in the clinical profile of our material emphasizes the variability in the way symptoms have been documented and interpreted by various specialists.We will, therefore, not use this type of approach in the analysis of the natural history. We favor the understanding of the various disease processes rather than the knowledge of the anticipated frequency of their occurrence.

Table 3.1. VGAM patients referred to Bicêtre per age group each year (1981–2002)

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109

The potential for prenatal diagnosis of VGAM has already been documented using noninvasive tools such as ultrasound, including color flow Doppler and magnetic resonance imaging (MRI) (Abbitt et al. 1990; Cubberlay et al. 1982; Heibel et al. 1993; Martinez-Lage et al. 1993; Saliba et al. 1987a; Sivakoff and Nouri 1982; Stockberger et al. 1993). From October 1984 to October 2002, 317 children with VGAM were studied in Bicêtre Hospital (Table 3.1). We consider this group of patients to be homogeneous, since the neuroradiological assessment, the technical principles involved, and the perioperative clinical management have been similar over the past 20 years and were carried out by the same group of physicians. The following observations were derived from this experience.

3.3 Modern Concept of Vein of Galen Aneurysmal Malformation Raybaud et al. (1989) was the first to recognize that the ectatic vein in VGAM was actually the median vein of the prosencephalon, the embryonic precursor of the vein of Galen itself. This was based on the choroidal nature of the arterial vascularization of this malformation (Figs. 3.1–3.3). A complete pathology specimen of a neonatal case of VGAM was carefully analyzed and illustrated by Landrieu in the late 1980 s (Fig. 3.4). We assessed the dural sinus abnormalities (Lasjaunias et al. 1987b) and persistent alternative embryonic routes of the deep venous drainage associated with this condition (Lasjaunias 1991). From then on, the vein of Galen malformation was recognized as an embryonic vascular malformation (as the timing for the causative trigger). It is a choroidal AV malformation (as a target for that causative trigger) (Fig. 3.4).

Fig. 3.1. Arterial supply to vein of Galen aneurysmal malformation (VGAM). All the various choroidal and subependymal arteries are represented. 1, Posterior callosal artery; 2, anterior choroidal artery; 3, posterolateral choroidal artery; 4, posteromedial choroidal artery; 5, circumferential artery (tectal) 6, subependymal artery; 7, hypothalamo-subependymal artery; 8, thalamostriate and subependymal artery

110 3 Vein of Galen Aneurysmal Malformation

Fig. 3.2A–D. Embryology of vein of Galen aneurysmal malformation (VGAM). View from above. A The vein primarily drains the choroidal afferents and secondarily collects the lenticulostriate afferents. B The final disposition of the normal vein of Galen is that of the deep venous confluent opening into the straight sinus. C In some instances, the median vein of the prosencephalon persists and bulges because of an arteriovenous shunt. The choroidal vein (single arrow) and thalamostriate vein (double arrow) then drain separately. D Very occasionally, the median vein of the prosencephalon retains its choroidal vein drainage, while the lenticulostriate venous system still opens in a separate fashion; in this instance, anastomoses may open with time with the inferior striate veins

Fig. 3.3. View from above of the choroidal fissure showing the triangular shape of the nidus in choroidal type of vein of Galen aneurysmal malformation (VGAM) (single arrow). The dilated median vein of the prosencephalon is seen posterior to the base of triangular shaped nidus (double arrow)

Modern Concept of Vein of Galen Aneurysmal Malformation

Fig. 3.4A–D. Legend see p. 112

111

112

3 Vein of Galen Aneurysmal Malformation

Fig. 3.4A–D. Neonatal specimen showing the choroidal type of VGAM opening into the median vein of the prosencephalon and secondarily into a falcine sinus. Postmortem study was obtained (courtesy of Prof. Landrieu). The general pathology showed no extracranial malformation. Neuropathological examination at autopsy showed that the cranium was unusually thick and the fontanelles appeared ossified. The brain weight was 220 g after fixation. There was a diffuse, symmetric atrophy of the cerebral mantle, and the ventricles were markedly dilated. The ependyma was thickened with the formation of numerous ependymal rosettes and astrocytic proliferation. The destruction of the cerebral mantle was either complete or characterized by a multicystic degeneration of the cortical zone invaded by macrophages. In the residual cortex, white matter, central grey nuclei, and subependymal zones, there were multiple malacic lesions from various ages and types: recent hemorrhagic infarcts; calcium deposits and incrustation of cellular process; nets of glial spumous cells; and pseudo-crystalline lipidic deposits. The periphery of these malacic lesions was frequently underlined by a slight astrocytic reaction. Diffuse subpial hemorrhagic necrosis and congestion of the subarachnoid vessels were prominent in the occipitotemporal areas, but vascular dilatation was also present, to a lesser extent, in all subarachnoid and parenchymal areas. The brain stem appeared malacic and edematous, without cavitation or glial reaction. The cerebellum was largely preserved, but focal depopulation of Purkinje cells and neurons of dentate nuclei is noticeable. The mesencephalic aqueduct appeared permeable, but could not be precisely measured. The vascular malformation was situated in the tectal area, in close connection with the posterior part of the circle of Willis. This malformation consisted of a large, entirely extracerebral cluster of intermingled vessels, closely associated with formations of mature choroid plexus. The small vessels displayed very irregular walls forming valvule-like folds, the media and the intima showing considerable variations in thickness. There was an internal elastic membrane showing sharp interruptions in those areas in which the dysplastic vessels shunt together or make shunts with venous-like branchs ending in the dilated Galen vein. The vascular cluster was nourished, through large shunts, by many arterial branches coming from the circle of Willis, especially from choroidal arteries. These nourishing arteries also appeared dysplasic with irregular walls. The dilated vein of Galen, 30 mm at its maximum diameter, was situated posterior to the bulk of the vascular malformation. Its wall, 500 mm thick, was made of a thin intima and of thick fibrous adventice. Many vascular fistulas appeared at the opening of the ampulla, in the lateral and anterior walls, measuring 200–500 mm. The dilated vein opened posteriorly into a patent falcorial sinus of normal histological structure. Comments: (A) the vascular malformation is entirely extracerebral, appears as a dysplastic process affecting the arteriovenous differentiation of the small choroidal vessels, resulting in the formation of numerous shunts, each of variable importance; (B) the hemodynamic and/or hydrodynamic consequences are largely prenatal, as shown by the pathology of the cerebral lesions

3.4 Vein of Galen Aneurysmal Dilatation Vein of Galen aneurysmal dilatations (VGADs) (Figs. 3.5–3.7) belong to the group of cerebral AVMs (CAVMs) draining into the deep venous system with an acquired ectatic dilatation of the vein of Galen confluence due to either stenosis at the venodural junction or thrombosis of the straight sinus. The dilated vein in this instance is the vein of Galen (great cerebral vein): it drains the AVM as well as normal brain tissue. The presence of reflux into the normal cerebral venous tributaries that open into the venous pouch indicates and confirms the presence of a matured Galenic confluent, the diagnosis of VGAD, and definitively excludes the

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113

Fig. 3.5. A Typical appearance of vein of VGAM with the choroidal supply to the dilated median vein of the prosencephalon. B Typical appearance of the choroidal supply to a choroidal arteriovenous malformation (AVM) associated with a dilated vein of Galen and reflux in the deep vein of the brain following straight sinus thrombosis

diagnosis of VGAM (Fig. 3.8). The evidence of primary opening of the shunt in a nonchoroidal vein, even without reflux, confirms the diagnosis of VAGD. In neonates and infants, the occurrence of VGAD is infrequent. However, 10 years ago 20% of children referred with the diagnosis of VGAM were actually VGAD patients. Today this confusion is much less frequent. VGADs are encountered in older children, corresponding in most cases to a deep-seated CAVM; they may show all the symptoms associated with this location and type of lesion. Tectal CAVM locations are those most closely resembling VGAMs; however, the transmesencephalic arteries will be seen at the time of angiography to be projecting below the P2 segment of the posterior cerebral artery, on the lateral projection of the vertebral injection and easily seen on axial MRI sections.

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3 Vein of Galen Aneurysmal Malformation

Fig. 3.6A, B. False VGAM diagnosed at the age of 6 months in a young boy presenting with a macrocrania. C Note the cingulate gyrus AVM draining into a posterior callosal vein and into a large vein of Galen

Subependymal arteries can be seen in VGAD in certain choroid plexus AVMs. Thalamoperforating arteries are also seen in VGADs of thalamic AVM origin. Proper analysis of the venous anatomy and clinical correlations will always enable one to differentiate the type of malformation involved. Characteristic symptoms are progressive neurological deficits associated with the mass effect and/or retrograde venous congestion, and hemorrhage of venous origin, either thalamic or subependymal. Epilepsy and other cortical manifestations are rare. Although theoreti-

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115

Fig. 3.7A–D. Typical aspect of a vein of Galen dilatation in a 2-year-old boy; note the opening of the left basal vein into the matured and dilated vein of Galen

cally possible, cardiac and hydrodynamic disorders are also rare. It is interesting to note that VGADs develop postnatally (no melting-brain syndrome despite pial veins reflux, no mental retardation, no jugular bulb dysmaturation), and lesions have usually already been present for a long time by the time they are diagnosed (acquired venous thrombosis, venous ectasia). Analysis of high-flow angiopathy changes in such patients will help in deciding on the best treatment strategy and its timing.

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3 Vein of Galen Aneurysmal Malformation

Fig. 3.8A–D. Typical aspect of a vein of Galen dilatation in a 10-year-old boy; note in addition to the opening of the right basal vein into the matured and dilated vein of Galen, the cerebral venous congestion of both supra- and infratentorial spaces

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3.5 Dural Arteriovenous Shunts with Aneurysmal Dilatation of the Vein of Galen Dural AV shunts (DAVSs) with aneurysmal dilatation of the vein of Galen were described in children by Fournier et al. in 1991; vein of Galen aneurysmal dilatation (VGAD) was secondary to a vermian AVM with dilatation of the Galen vein (thrombosis of the straight sinus). In a 2-year-old boy presenting with intraventricular hemorrhage, computed tomography (CT) and angiography demonstrated a small vermian cerebellar AVM with reflux in the Galen vein afferents. A mild macrocrania had been noted at 3 months but was not further investigated, and the child was shunted (ventricular-peritoneal). Following embolization of the AVM and subsequent surgical removal of the remainder of the lesion, a 6-month follow-up angiogram demonstrated a dural shunt remote from the surgical field. The AV shunts were located within the wall of the previously dilated Galen vein. Feeders corresponded to vasa vasorum of the normal Galen vein, thus contributing to a nidus type of network extending from the venous wall into the intraluminal clot partially filling the ectatic lumen. These lesions are usually seen in adults and probably reflect the longstanding presence of triggering factors and secondary changes before they become clinically evident (see Vol. 2).

3.6 Vein of Galen Varix Vein of Galen varices constitute a group of dilatations of the vein without the presence of an AV shunt. Two types have been encountered in children. The first are transient dilatations of the Galen vein in neonates presenting with cardiac failure of another origin. This dilatation persists for a few days after birth and then disappears on follow-up ultrasound studies. The dilatation does not lead to any symptoms and the disappearance parallels the cardiovascular improvement. The second type of vein of Galen varix occurs when hemispheric venous drainage of the brain converges toward the deep venous system. This condition does not always correspond to a postthrombotic collateral circulation, but sometimes to an obvious anomalous disposition of the overall venous system (complex DVA). It will not give any specific symptoms, but the lack of compliance of this type of venous drainage system over time may create venous insufficiency manifestations.

3.7 Vein of Galen Aneurysmal Malformation It is possible to distinguish the angioarchitectural differences between an AVM involving the vein of Galen forerunner, which we call VGAM, and an AVM with venous drainage into a dilated, but already formed vein of Galen, which will be called VGAD (Lasjaunias 1987b). The VGAM involves the choroidal fissure and extends from the interventricular foramen rostrally to the atrium laterally (Fig. 3.3).

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3 Vein of Galen Aneurysmal Malformation

Fig. 3.9. Schematic representation of VGAM illustrating in particular the choroidal supply as well as the limbic arterial arch. The subependymal and lamina terminalis supplies are not represented. (Courtesy of J. Bhattacharya)

The arterial supply usually involves all the choroidal arteries (Figs. 3.9, 3.10,), including subfornical and anterior choroidal contributions (Figs. 3.11, 3.12); it may also receive a significant contribution from the subependymal network originating from the posterior circle of Willis. These arteries should be differentiated from transmesencephalic arteries (their involvement, in fact, would exclude the diagnosis of VGAM and indicate a tectal location of the AVM). The subependymal arteries pierce the floor of the third ventricle and run subependymal to join the choroid fissure, where they contribute to the opacification of the lesion. Very rarely are thalamoperforating arteries recruited, and this occurrence is grossly overestimated in the literature (Fig. 3.11). Subependymal and transcerebral contributions appear accessory in the supply to the shunt, possibly created by the sump effect of the venous drainage. Their contribution can sometimes be used for an endovascular approach (Fig. 3.13), but they usually disappear following the proper occlusion of the most prominent shunts (see Fig. 3.14). The persistent limbic arterial arch (see Vol. 1, Chap. 6), which bridges the cortical branch of the anterior choroidal artery initially (Fig. 3.15) and the posterior cerebral artery (Fig. 3.16) secondarily with the pericallosal artery, is seen in nearly half of neonatal cases. It should be distinguished from subcallosal and subfornical supply to the choroidal shunts (Fig. 3.17). Its presence should be anticipated at the time of embolization into a lateral choroidal artery when it arises far distally along the posterior cerebral main stem. The limbic arterial arch on each side can anastomose and may even fuse on the midline in the supracallosal region (Figs. 3.18, 3.19). The circle(s) regress (mature) after obliteration of the VGAM by means of embolization (Fig. 3.17), leaving behind various anatomical dispositions where the posterior cerebral artery (PCA) supplies the ipsilateral or contralateral para central gyrus (Figs. 3.18, 3.19). Cerebellar arteries do not contribute to the supply of the VGAM, except

Vein of Galen Aneurysmal Malformation

Fig. 3.10A–C. Legend see p. 120

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Fig. 3.10A–E. Female neonates presenting with moderate cardiac overload. A, B Because of the MRI appearance with enlarged arteries within the capsular region, the diagnosis of vein of Galen was questioned. Angiography was performed (C), showing a significant intraparenchymal angiectasia joining the choroid fissure on the right side. Note supply to an arteriovenous fistula at the interventricular foramen. D, E angiographie and MRI demonstration of the subependymal artery in a retromammilar position

indirectly through their dural branches, which can be enlarged, as they may participate in the supply to the vasa vasorum at the venodural junction. Other dural contributions can be seen in true VGAM and may be located at a distance from the choroid fissure shunting zone. They often represent secondary dural AV shunts after sinus thrombosis (usually sigmoid; Fig. 3.53) or AV dural communications caused by the sump effect from an otherwise patent sinus [usually the superior sagittal sinus (SSS)]. In three premature babies who presented with severe cardiac failure, we encountered a rare arterial aspect resembling a moyamoya network (Fig. 3.20). In all three patients, the damage to the cerebral tissue appeared irreversible and the babies died during the next 48 h. This condition was the only one to resemble an early high-flow angiopathy type of response of the remaining vasculature to the shunt. Some rare stenoses are seen along the course of large choroidal feeders to mural types of VGAM (see below; see Fig. 3.56). Since they are located at the edge of the tentorium cerebelli, they are likely to express the mechanical effects of the ectasia by the stiff dural margin on the enlarged feeders. We suspect that a further slight increase in this pressure phenomenon (by ventricle enlargement) might lead to occlusion of the artery involved. Subsequent spontaneous thrombosis of the VGAM will occur if the number of compressed feeders to the lesion is limited, as in a mural type of VGAM.

Vein of Galen Aneurysmal Malformation

Fig. 3.11A–D. A 2-month-old girl presenting with cardiac overload equilibrated with medical treatment as well as macrocrania and already moderate ventricular dilatation. She presented with a generalized seizure and a mild motor deficit. When we saw her at 6 months of age, there was already a delay in neurological acquisitions. A, B Angiography and C, D MRI demonstrates an explosive transhemispheric network of vessels reaching the choroid fissure and opening into the vein of Galen malformation

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Fig. 3.12A, B. Two different VGAMs with an interventricular foramen arteriovenous fistula, associated with a more posteriorly located usual VGAM in a choroidal form

The nidus of the lesion is usually located in the midline and therefore receives a bilateral and symmetrical supply (Fig. 3.17). In certain instances, one side may be more prominent, and this will cause the dilated pouch to be shifted by the force of the jet of the fistula away from the prominent supply toward the opposite side (see Fig. 3.42). In general terms, two types of angioarchitecture are encountered: choroidal and mural. The former corresponds to a very primitive condition, with the contribution of all the choroidal arteries and an interposed network before opening into the large venous pouch (see Figs. 3.12, 3.16). This condition is encountered in most neonates with low clinical scores (see Sect. 3.8). The latter corresponds to direct AV fistulas within the wall of the median vein of the prosencephalon (see Figs. 3.17, 3.39). These fistulas can be single or (more often) multiple and either converge into a single venous chamber or into multiple venous lobulations located along the anterior aspect of the pouch or along the afferent choroidal veins of the fissure (Fig. 3.11). This mural form is often better tolerated and encountered in infants who do not develop cardiac symptoms and who have a better disease tolerance and feature higher clinical scores. Intermediate forms can occur, but their identification does not assist in the understanding of the disease, and they are only interesting from a technical and management point of view. So far, we have not seen a true VGAM associated with another type of AVM.

Vein of Galen Aneurysmal Malformation

Fig. 3.13A–F. Legend see p. 124

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Fig. 3.13A–G. A 3-year-old boy presented macrocrania at the age of 4 months. MRI (A, B), 3D angiography in superior (C) and lateral (D, E) views, demonstrating the recurrent artery from the ACA-A1 segment supply an interventricular foramen AV shunt associated with a choroidal VGAM (E). F, G MR follow-up following embolization of the Heubner as well as choroidal contributors to the lesions

Since the choroidal veins are the embryonic tributaries of the median vein, potentially fistulous communications can be located at some distance from the pouch (Figs. 3.10, 3.13). They usually occur at the level of the interventricular foramen, where they can recruit a specific perforating branch (Fig. 3.13) from the anterior communicating artery or the Heubner artery. Some multifocal AVSs can associate mural communications with an additional shunting zone at the rostral end of the choroid fissure (Fig. 3.10). In this case, a choroidal venous segment is seen prior to its opening into the ectatic vein. The venous drainage of the VGAM is, by definition, toward the dilated median vein of the prosencephalon, forerunner of the Galen vein, and no communication exists with the deep venous system of the brain nuclei. In VGAM patients, thalamostriate veins open into the posterior and inferior thalamic (diencephalic) veins, as occurs normally during the 3rd month in utero (Figs. 3.21, 3.22). They secondarily join the anterior confluence, a subtemporal vein, or (more often) the lateral mesencephalic vein to open into the superior petrosal sinus, demonstrating a typical epsilon shape on the lateral angiogram (see Figs. 3.23, 3.24). In older children, the choroidal veins opening into the VGAM may become visible; if restriction in the skull base outlet has occurred (see Fig. 3.25) subependymal-striate anastomoses may open and become visible on the venous phase of vertebral angiograms. These can be the cause of intraventricular hemorrhages following transvenous approaches. The remainder of the venous drainage is variable, with the straight sinus being absent in almost all cases. Falcine dural channel(s) drain the pouch toward the posterior third of the superior sagittal sinus, which also happens to be where granulations are expected to appear first (see Chap. 2, this volume). In most cases, restrictions at the venodural

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Fig. 3.14. A A 26-year-old woman with more than 20% mental retardation and right-sided hemiparesis showing VGAM revealed at the age of 5 months. Note the subependymal contribution to the anteriorly located shunting zone to the ectatic vein. B Immediately following embolization, there was still flow inside the lesion. C After spontaneous secondary thrombosis, the subependymal supply, although not embolized, regressed spontaneously

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Fig. 3.15. Typical limbic circle of the archaic type: anterior choroidal to anterior cerebral artery in a young girl presenting with a VGAM diagnosed in infancy with mild macrocrania

Fig. 3.16A, B. Three-dimensional aspect of a persistent limbic arch. A Lateral and slightly anterior oblique view. B Medial and slightly anterior oblique view. Note the choroidal and subependymal feeders

Vein of Galen Aneurysmal Malformation

Fig. 3.17. A,B Legend see p. 128

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Fig. 3.17. A An infant girl presented with macrocrania at the age of 6 months leading to the diagnosis of a large VGAM. She was referred at the age of 8 months. There is a posterior cerebral to anterior cerebral limbic system with a midline fusion phenomenon of the anterior cerebral artery. B Following embolization of the main feeders and despite persistence of minimal shunt at the end of the second embolization, spontaneous thrombosis occurred concomitantly with (C) the maturation of the limbic circle and shrinkage of the mass

junction or in the falx create upstream and downstream turbulence and significant dilatations (Fig. 3.25). Other embryonic sinuses persist, such as the occipital and marginal sinuses (Fig. 3.26), particularly in neonates. The appearance of the remainder of the venous system is difficult to predict, even though all cerebral veins converge at birth toward the posterior sinuses. A few months after birth, the cavernous sinus matures and is able to „capture“ the sylvian veins, offering the brain a potential drainage through the orbit, pterygoid plexus, or inferior petrosal sinus (Fig. 3.27). Drainage of the cerebral veins into unusual transcranial channels may take place, apparently without significant functional implications (Figs. 3.28, 3.29). The plasticity of the venous system in these instances is remarkable. Although the anatomic framework is exact and predictable, it is crucial to remember that it changes with spontaneous modification of the hemodynamics, the influence on growth and maturation induced by the disease and, eventually, the treatment undertaken. The timing of interference with this anatomic maturation continuum is as important as the extent of the corrections proposed. At this age, it is more important to restore normal growth conditions than a normal appearance, which is often the therapeutic goal in adults. Other midline malformations (clefts, sinus pericranii, coarctation) have been noted in some rare cases, although they rarely correspond to existing or potential syndromes (Fig. 3.30).

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Fig. 3.18. A, B Persisting limbic arch immediately after embolization. C–F Unilateral remodeling of the supply to the paracentral gyrus after completion of the VGAM occlusion

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Fig. 3.19A–F. A 13-year-old boy presented at the age of 5 years with macrocrania. Subcallosal anastomosis between right and left posterior cerebral arteries (PCAs) (A, B) is likely to correspond to an asymmetrical maturation of the limbic circle. Note the right A1 agenesis (C), and P2 on the left (D). Bilateral distribution of the left anterior cerebral artery (ACA) (E, F). These features point to the capacity of midline fusion in the limbic system as well as ACA remnants

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Fig. 3.20A–C. Premature girl presented with cardiac failure immediately after birth. Stabilization was obtained with medical treatment. At the age of 2 months, A MRI and B, C angiography were performed because of the failure to thrive and abnormal neurological findings. A focal infarct was noted on MRI corresponding to arterial occlusive disease associated with VGAM. This neonatal moyamoya-like condition is a contraindication for treatment when noted, as it adds arterial depravation to venous ischemic congestion

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Fig. 3.21A–D. Schematic representation of different types of deep venous drainage. A Usual disposition, B epsilon aspect noted in VGAM, C medial parietal opening of the internal cerebral vein, D associated transosseous drainage in the orbital region (see Fig. 3.29). (Courtesy of J. Bhattacharya)

Vein of Galen Aneurysmal Malformation

Fig. 3.22A, B. Typical venous pattern of the cerebral drainage in a previously embolized VGAM. Note the cortical anastomosis between the frontal and sylvian veins and the epsilon-shaped deep venous system bilaterally. B Incomplete capture of the sylvian vein on the left side and A its almost complete opening on the right side. Note also the superior and inferior petrosal sinuses that are clearly demonstrated on both sides

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Fig. 3.23A–C. Late venous phase of the carotid (A) and vertebral angiogram (B), 3D angiographic aspect (C). Epsilon-shaped deep venous drainage into the superior petrosal sinus via the lateral mesencephalic vein

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Fig. 3.24A–C. Typical aspect of the epsilon-shaped venous return in a 13-year-old patient with a completely excluded VGAM. Note the bilateral drainage of the supratentorial collectors into the lateral mesencephalic vein and petrous vein infratentorially. Occlusion of the right sigmoid sinus promoted the transcortical drainage into the deep venous system

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Fig. 3.25. A VGAM with bilateral sigmoid sinus occlusion secondary to jugular bulb dysmaturation. All possible supra- and infratentorial anastomotic channels are recruited to provide drainage. Subependymal anastomoses create a nidus-like network in the vicinity of the VGAM itself. B, C Oblique posterior and superior 3D views of the venous drainage

Vein of Galen Aneurysmal Malformation

Fig. 3.26A–E. A 12-month-old child presenting a VGAM with already existing venous outlet restrictions and reflux in sinuses and subependymal veins (A, B). C One year after partial embolization, although the child was normal, there was an increase in the pial reflux. D At short-term follow-up, there was spontaneous occlusion of the falcine outlets requiring rapid completion of the exclusion of the remaining shunts (E)

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Fig. 3.27. A A 6-year-old boy with choroidal VGAM diagnosed 1 year before with prominent facial veins and moderate macrocrania without neurological symptoms or retardation. B On the MRI, note the stigmata and the chronic venous sinus congestion, which over time created subependymal anastomoses. C, D The angiographic study demonstrates the subependymal inferior striate vein opening and its secondary opening into the cavernous sinus

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Fig. 3.28A, B. VGAM with restricted outlet and transcranial opening in the subgaleal veins

Fig. 3.29A–F. A 20-month-old boy presenting a supraorbital varix and a choroidal VGAM (A, B). C Bone X-rays suggested sinus pericranii confirmed on the venous phase of carotid angiography with basal and lateral views on venous 3D angiography (D–F). C–F see p. 140

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Fig. 3.29C–F. Legend see p. 139

Natural History of Vein of Galen Aneurysmal Malformations

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Fig. 3.30. Infant boys presenting with VGAM and maxillofacial midline disorders: A cleft palate; B tip-of-the-nose hemangioma

3.8 Natural History of Vein of Galen Aneurysmal Malformations Similar to other types of vein of Galen AV lesions, VGAMs are not hereditary. In our series, two cousins presented with vein of Galen-type AV shunts diagnosed at neonatal and infant age, but upon analysis they did not seem to represent true VGAMs. Neither in our series of children with hereditary hemorrhagic telangiectasia (HHT) disorder, nor in the group of adult patients with cerebral localizations of HHT was there a VGAM present. Boynton and Morgan (1973) reported a case of a neonate with a rapidly lethal vein of Galen AVM fed by posterior, anterior, and middle cerebral arteries and a family history of HHT. In 1987, Salazar reported a similar case, but from the description in both cases we doubt that the AVM was a true VGAM. Despite the male dominance in this type of AVM (it is the only arteriovenous malformation with a sex dominance), there is presently no convincing evidence to suggest a hereditary genetic influence on the development of VGAM (Scheme 3.1A). The natural history of VGAM is unclear from what is documented in the literature. In particular, since many classic descriptions were not actually VGAMs but were descriptions of VGADs, much of the so-called natural history of the surviving children was learned from babies who had undergone shunting procedures. The need for emergency treatment in many patients certainly represented an acceptable explanation for the delay in appreciating the associated negative effects of ventricular drainage on the neurological progression in these children. In particular, the onset of seizures traditionally described in the late phase of VGAMs reflects this progressions in babies who had been shunted. Most neurological symptoms and hemorrhages reported in the literature are in mistakenly diagnosed VGAMs or are the result of changes in angioarchitecture, which in turn alter the consequences of the initial lesion. All these

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Scheme 3.1A. Natural history of vein of Galen aneurysmal malformations

phases are predictable, and most prodromes are recognizable; early management does not necessarily mean emergency interventions. Finally, endovascular management of this population has given us a chance to observe the anatomic and clinical progression in nonsurgical circumstances. Several papers (Andeweg 1989; Del Bigio et al. 1985; Girard et al. 1992; Larroche 1977a; Le Gros Clark 1920; Quisling and Mickle 1989; Saliba et al. 1987b; Schroth and Klose 1992a; Seidenwurm et al. 1991; Weed 1923) provide crucial insights into the physiology and vasculature of the prenatal brain. They serve as a basis for us to better understand the original material that we were able to collect (Garcia-Monaco et al. 1991b; Girard et al. 1994; Lasjaunias et al. 1991b, 1995; Rodesch et al. 1994; Zerah et al. 1992) and to improve our interpretation of the literature. We have chosen a diagrammatic presentation of the natural history of VGAM to highlight the path followed by each individual case. Thus, once previous stages have been identified, the subsequent ones can be more easily anticipated. The therapeutic window outlines the optimal moment for the endovascular approach. this has become the objective of our decision as to therapeutic timing and points to the treatment and clinical goals to be targeted. We will concentrate only on the clinical aspect in this section and will consider the technical management and global results later. The reader is referred to Chap. 2 to gain a broader prospective with regard to the diagnostic challenge in the different age groups.

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3.9 Cardiac Manifestations Cardiac manifestations were reviewed for neonates (Garcia Monaco 1991b) and have been prenatally diagnosed in VGAMs (Rodesch et al. 1994). In contrast to the cardiac failure observed in large hemangiomas, where they occur in infancy at the proliferative stage of the disease, the congestive cardiac failure (CCF) in VGAMs can be present during the neonatal period (see Chap. 11, this volume) (Scheme 3.1B). In his series of 18 antenatally diagnosed VGAM patients, Rodesch noted that 17 were born with cardiac failure and only one without. During prenatal ultrasound examination, some cardiac enlargement was noted in four out of 17 patients. In all four of the patients in which this finding was demonstrated, the neonatal score was low (<8/21) either because of the significant peripheral effect of systemic failure or because of an already demonstrable encephalomalacia. Treatment was withheld in four patients and they soon died. The others were medically managed, carefully followed, and embolized between 2 and 13 months transarterially. A total of 30% of them had slight retardation (of less than 20%), which resolved in a few months after completion of embolization treatment. As far as the prognosis of an prenatally diagnosed VGAM is concerned, 22% of such babies have irreversible cerebral damage at birth and soon die; the remaining babies should undergo embolization at various times,

Scheme 3.1B. Systemic disorders

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Fig. 3.31A, B. Prenatal MR diagnosis of VGAM with enlarged ventricles mostly related to subependymal atrophy

depending on their individual response to medical treatment, and their late neurological outcome is excellent at 2-year follow-up. Therapeutic termination of pregnancy can be discussed in cases in which cardiac failure and or cerebral brain damage is noted in utero), while the presence of macrocrania in utero has no negative significance in our experience. It is of interest to note that, when comparing the series of prenatally diagnosed cases with our overall series of VGAMs, the amount of irreversible cerebral damage is the same (22% vs 25%), but the capacity to determine the correct therapeutic moment improves the neurological outcome (88% normal neurological examination in the prenatal group vs 78% in the entire series). In a twin pregnancy, the prenatal diagnosis of VGAM was made in one fetus, while no abnormality was present in the other baby. Prenatal diagnosis (Fig. 3.31) is not an indication for emergency embolization at neonatal age, but rather gives an opportunity to prepare the team that is to treat the child, monitor the degree of systemic disorders to be managed, and choose the best moment at which to handle them. Premature babies with VGAM are an additional challenge. In two patients, we performed angiography because of doubt regarding the nature of the lesion, the presence of a convulsion, the absence of encephalomalacia, and a score of 11 with an unstable CCF in both patients. A moyamoya type of network was noted in both in addition to typical features of true VGAM (Fig. 3.20). In such children, treatment should be withheld, since the neurological outcome no longer depends on the CCF and the VGAM, but is mainly related to diffuse arterial angiopathy. On the other hand, a premature 2-kg neonate, born at 36 weeks gestation and part of a twin pregnancy, presented with progressive CCF but otherwise good scores and was managed successfully with early arterial embolization and had a good neurological outcome. With regard to the spontaneous evolution of the CCF, the following observations can be made. After a brief period of stabilization, in most cases the CCF worsens during the first 3 days of life, then stabilizes again to then improve with appropriate medical management.

Cardiac Manifestations

Fig. 3.32A–E. Legend see p. 146

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Fig. 3.32. A–C MR and MRA with 3D reconstructions accurately demonstrating the cerebral condition, the lesion, and its feeders. Color Doppler ultrasound with morphological (D, E) and hemodynamic (F) analysis of a VGAM case

In none of the babies referred to us with the diagnosis of VGAM did cardiac failure develop de novo after the 2nd week of life. However, it can decompensate at 3 weeks or recur later following lung infections or other concurrent diseases. In infants, CCF never constitutes the presenting symptom, nor does it worsen at that age if already present. An increased cardiac index is often noted when the diagnosis of VGAM is made because of macrocrania. Cardiac manifestations have been reviewed for neonates (Garcia Monaco et al. 1991a; Chevret et al. 2002; Frawley et al. 2002) and the degree of failure is variable from one child to another, but seems to be independent of the characteristics of the shunt (Fig. 3.32). This is also noted in other neonatal CAVSs (Rodesch et al. 1994). Some obvious high-flow lesions are well tolerated, while conversely some apparently small ones may lead to multiorgan failure (Fig. 3.33). The intracranial hemodynamic parameters available do not provide us with any definitive information concerning the timing or even the end point of AV shunt correction. Some babies, while presenting with severe CCF and responding well to medical treatment, may already reveal CT evidence of venous infarction (Figs. 3.34, 3.35). Cerebral insult had presumably already started in utero. In one autopsy case of severe systemic failure with cerebral encephalomalacia, the cranial vault was already thick (8 mm) and the fontanelles closed (Landrieu, unpublished data; Figs. 3.4, 3.33), pointing to the early onset of melting-brain syndrome (see Chap. 2, this volume). Renal and hepatic damage may further aggravate CCF, and their function can be transiently impaired (oliguria, increase of enzymes) or become rapidly unstable despite intensive medical care. Ventilation, although important in stabilizing some life-threatening situations,

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Fig. 3.33A, B. A 2,650-g female neonate presented with severe cardiac failure. Head circumference was 31.5 cm and neonatal score 8. A Ultrasound and B CT examinations demonstrated diffuse brain damage; progression was rapidly fatal

Fig. 3.34. A Chest X-ray in a male neonate who presented with severe cardiac failure and a single convulsive episode. B, C Although the neonatal score is 13, CT demonstrates severe bilateral infarct with some degree of melting-brain syndrome already, indicating its onset in utero

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Fig. 3.35A–C. Male neonate weighing 3,200 g. Immediate cyanosis requiring intubation and ventilation with 100% O2. Under NO and dopamine, he had transient anuria and two convulsions. A–C CT performed the same day demonstrates periventricular encephalomalacia associated with neonatal calcification, particularly in the frontal region. Even though the score was 10, the child was not embolized. He had two additional generalized seizures and rapidly died

is often overused and may create additional difficulties when extubation is required once the decision is made not to embolize the child. The cause of CCF is not fully understood. In fetal life, the effects of heart rate on the combined ventricular output (CVO) (Rudolph 1976) suggest that the heart is functioning near its maximum performance (Marcelletti 1992). It seems that volume loading increases output to a limited extent. The fetal myocardium has less contractile tissue, as shown by its myofibrillar contents (Friedman 1993). Several major events change the fetal circulation at birth: (a) removal of the low-pressure circuit (placenta) from the systemic circulation, (b) reversal of the relative pressure between the right and the left atrium, leading to closure of the foramen ovale, (c) muscular contraction of the ductus arteriosus (its closure occurs 10–15 h after birth with a rise of PO2 the systemic level, but also neurological and vasoactive interferences), and (d) decrease in pulmonary vascular resistance. Transitional circulation takes place. This leads to change in cardiac output from 150 ml/min per kg in the fetus to 3–400 ml/min per kg postnatally. Since the reduced reserve for increased CVO is observed, the aug-

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mentation in output might be obtained from a transitory gain in cardiac contractility, which disappears after the 1st week (Marcelletti 1992). Temperature is also an important parameter at this age; it is maintained by peripheral vasoconstriction and secondary oxydation of triglycerides and free fatty acids. Further changes are seen during growth of the child. Our interventional strategy and medical support in neonatal CCF are in accordance with these physiological changes, and medical treatment is based more on diuretics and inotropic drugs than on the use of digitalis. CCF is mainly encountered in the choroidal forms of VGAMs, which are the most frequent AV shunts diagnosed at that age (cause or consequence?). Severe forms of CCF are associated with persistence of the fetal type of circulation. Septal communications and ductus arteriosus are often noted during cardiac ultrasound; they should not be considered as associated cardiac malformations, even if they increase the systemic insufficiency. Like most of the disorders encountered in these circumstances, they either disappear spontaneously or following endovascular management of the AV shunt itself. They should be followed with special attention if embolization is not to be done early, and they may induce a failure-to-thrive condition. In our series, two neonates presented with an associated cardiac malformation and an aortic coarctation for which they were first operated on; embolization was then carried out at the age of 1 and 2 months. Five and 10 years later, the children had satisfactory clinical progression and a score of 4. In two other patients, we decided to clip a ductus arteriosus before embolizing the VGAM in neonates with severe CCF and a score of 12. After VGAM is suspected by clinical examination, a pretherapeutic evaluation should be obtained, including the following information: (a) clinical evaluation of the baby and documentation of all the possible events that have occurred since birth (convulsions, for example, do not occur in VGAM at that age unless brain damage has already taken place); (b) evaluation of renal and liver function; (c) transfontanel ultrasound to evaluate possible encephalomalacia; (d) cardiac ultrasound to assess cardiac tolerance and to diagnose any associated cardiac malformation that might require specific treatment; (e) good-quality MRI to provide all the necessary morphological information regarding the lesions (the diagnosis of a CAVM at this age would have completely different therapeutic consequences) and the status of myelinization; (f) electroencephalogram (EEG) only if the baby is in an intensive care unit (ICU), intubated, and sedated. Angiography in the neonatal work-up is not indicated and not recommended; only if embolization is contemplated will the angiographic procedure be performed at the same time. All the information listed above is necessary to make management decisions. The baby’s weight and the head circumference constitute frequently omitted information that needs to be carefully documented and collected in the weeks that follow. The decisions made at this stage follow a strict protocol and involve many specialists. Neurological assessment is difficult in neonates and the presence of systemic disorders has prognostic implications, while cere-

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Table 3.2. Bicêtre Neonatal Evaluation Score Pointsa

Cardiac function

Cerebral function

Respiratory function

Hepatic function

Renal function

5 4

Normal Overload, no medical treatment Failure: stable with medical treatment

Normal Subclinical isolated EEG Abn’s Nonconvulsive intermittent neurologic signs Isolated convulsion

Normal Tachypnea, finishes bottle Tachypnea, does not finish bottle

– –

– –

No hepatomegaly, normal function

Normal

Assisted ventilation, normal saturation FIO2 <25% Assisted ventilation, normal saturation FIO2 >25% Assisted ventilation, desaturation

Hepatomegaly, normal function

Transient anuria

Moderate or transient hepatic insufficiency Abn coagulation, elevated enzymes

Unstable diuresis with treatment Anuria

3

2

1

0

Failure: not stable with medical treatment Ventilation necessary Resistant to medical treatment

Seizures

Permanent neurological signs

a

Maximal score: 5 (cardiac) + 5 (cerebral) + 5 (respiratory) + 3 (hepatic) + 3 (renal) = 21. Abn, abnormal; FIO2, inspired fraction of oxygen.

bral damage may go undetected on imaging, either because of the quality of the examination obtained or because of the early nature of changes present in the neonatal age group. We have designed a specific neonatal score that documents the significant non-neurological manifestations in this age group in addition to assessing the gross neurological status (see Table 3.2). A score of less than 8/21 results in a decision not to treat; a score of between 8 and 12/21 entails emergency endovascular intervention (Fig. 3.36); a score of more than 12/21 leads to the decision to manage with medical treatment as long as possible until the child is 5 months of age, providing there is no failure to thrive. At this time, a decision is made to proceed with endovascular treatment no matter what the symptoms are. In our experience, angiography and treatment at 5 months has shown to best balance the maximum efficacy of embolization against the minimum risk of cerebral maturation delay. The first few months of clinical assessment are crucial to be able to predict the future and neurological status of the child. The goal is to have a baby that is (a) stable on medication for cardiac insufficiency; (b) easier to manage from a technical point of view; (c) not showing significant developmental delay; (d) not developing a significant macrocrania. Pediatric follow-up criteria therefore include monthly head circumference, weight, and developmental assessment as well as MRI at 3-month intervals. Obviously, alteration in any of these parameters will prompt endovascular management. A postnatal decrease in the head circumference is probably the worst finding to be noted, since it indicates the loss of brain substance and early suture fusion. The next phase in the progression of the disease is marked by hydrovenous disorders (see Chap. 2, this volume).

Cardiac Manifestations

Fig. 3.36A–D. Prenatal diagnosis at 33 weeks of VGAM. A At day 1, there was rapid congestive cardiac failure, requiring intubation and assisted ventilation, moderate hepatic insufficiency, and normal renal function. B, C CT shows a normal brain. The neonatal score is 12. D The baby was therefore embolized as an emergency procedure on day 7. Subsequently, the child was extubated and the cardiac medication was significantly decreased. VGAM was completely excluded in a second session, and cardiac medication discontinued. At 9 months, complete occlusion was confirmed and the child’s score was 4

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3.10 Macrocrania and Hydrocephalus As opposed to CCF, hydrodynamic disorders can manifest themselves in fetuses, neonates, and infants (Scheme 3.1C). Choroidal and mural types almost equally give rise to these types of manifestations. They constitute the primary revealing factor at infant age if the diagnosis has not been made previously. They result from the abnormal hemodynamic conditions present at the torcular venous sinus confluence, the posterior convergence of the venous drainage of the brain, and the immaturity of the granulation system. For many years, and even now, the mechanical compression of the mesencephalic aqueduct was and is sometimes still considered to be the primary cause of the hydrodynamic disorders at this age. Actually, the aqueduct is patent in almost cases (Diebler et al. 1981; Zerah et al. 1992). Macrocrania, while resulting in an increasing head circumference, is associated with slightly enlarged ventricles and generous perivascular spaces (see Figs. 3.37, 3.38). The water dysfunction combines an intracerebral (intrinsic) retention with an increase in the cerebrospinal fluid (CSF) (extrinsic) volume. Both phenomena have little or no effect on the brain itself as long as the sutures enlarge, since they tend to continually adapt to intracranial pressure vs the resistance by the cranial vault. On the other hand, in VGAM in infants the lack of macrocrania is even more worrisome than its presence. The cerebrofugal medullary veins constitute a gradient that will induce absorption of most of the intracerebral water. If the sutures stop growing or if the medullary vein

Scheme 3.1C. Hydrodynamic disorders

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Fig. 3.37A, B. Young girl with VGAM diagnosed at 2 months due to macrocrania. The child was shunted, but the surgical diversion was unsuccessful. The child was referred at the age of 8 months with mild mental retardation. Complete occlusion was obtained in three sessions over 2 years. C, D Final MRI after occlusion of the VGAM shows complete shrinkage of the mass and absence of subependymal atrophy, despite the earlier (nonfunctioning) ventricular shunting

resorption decreases (or the pial vein pressure increases), or if for any other unknown reason the compliance of the venous system fails, hydrocephalus and intracranial hypertension occur. At infant age, persistence of the situation leads to clinical manifestations, e.g., irritability, alteration of the level of consciousness and neurological status, stagnation of the head circumference, a decrease in brain volume with enlargement of fluid spaces, and developmental delay. This means that, before ventricular enlargement occurs, intracranial pressure is not as high because of macrocrania, and therefore ventricular shunting

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Fig. 3.38. A Girl with macrocrania, with typical VGAM curve and her response following transarterial embolization (E)

is not indicated. Spontaneous stabilization of the enlarging head phenomena can occur with the cavernous sinus capture of the sylvian veins. A new low-pressure venous system offers an alternative pathway for water resorption and therefore improves the excessive hydration status of the cerebral tissue. The progression from macrocrania to hydrocephalus is therefore not inevitable. Ventricular shunting has long been performed and, while conceptually simple, does require special skill to ensure safe results (Fig. 3.39). Ventricular shunting in VGAM, however, carries an additional risk of morbidity (Fig. 3.40). As early as 1987, in their review of the literature from 1950 to 1985, Johnston et al. noted that, of 11 shunted infants (aged 1 month to 1 year), seven died and only one had no deficit. In an additional group of six shunted children (aged 1–5 years), only two had no deficit. In 1992, in the series of Zerah et al. (1984–1991), only one out of 17 infants (aged 1 month to 2 years) underwent an uneventful shunting procedure. The others had enlargement of the VGAM (n=7; Fig. 3.41), persistent seizures (n=3), subdural hematomas (n=6; Fig. 3.40), mechanical problems (n=3), slit ventricles (n=1; Fig. 3.42); none of the patients died. In VGAMs, the venous pressure is consistently increased and is often very high. Quisling (1989) reported that pressures were always above 30 cc H2O and, in another publication in 1986, pressures were above 50 cc H2O with a 1:5 ratio between intraventricular pressure (IVP) and superior sagittal sinus pressure (SSSP). The increased SSSP dramatically falls to almost 0 after successful embolization. The IVP to SSSP ratio explains why it is so difficult for the CSF to pass from the subarachnoid space into the dural sinus compartment.

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Fig. 3.39A–D. Female infant (A, B) with VGAM of the mural type diagnosed at 6 months with macrocrania. C, D In view of rapidly progressing hydrocephalus, the child was referred and embolized as an emergency procedure at 9 months. E–G see p. 156

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Fig. 3.39. (continued) E, F Complete occlusion was obtained at 1 year. G Four years later, shrinkage is complete. Note the mild subependymal atrophy.

Ventricular shunting does not deal with the problem created by the hydrodynamic disorders at the macrocrania phase, but only transiently and incompletely resolves an emergency situation at the ventricular level. It creates a cerebropetal flow along the medullary veins opposite to the natural and necessary cerebrofugal flow. The deficits, seizures, or hemorrhages seen following ventricular shunting have been so well accepted that they have even been considered as part of the natural history of VGAM. Endovascular management of the same situations today has shown that, even with a partial treatment of the AV shunt, these secondary symptoms do not occur unless additional factors intervene to change the angioarchitecture of the lesion (see Sect. 3.15). At the infant stage, careful monitoring of the development of macrocrania is recommended until the moment of endovascular treatment (at the latest at 5 months). If the increase in head circumference appears to be too rapid, or if there is preclinical MRI evidence of intraventricular hyperpressure, or if the clinical follow-up demonstrates a significant developmental delay, then urgent embolization should be carried out and ventricular shunting

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Fig. 3.40A, B. This young boy was diagnosed on day 16 with macrocrania and was then shunted; note the bilateral subdural sequelae following multiple ventricular shunting. He had severe mental retardation, multiple seizures, and motor deficit. At age 10, he was referred and was cured by one session of embolization. Although his gait dramatically improved, he still scores 1 because of his mental retardation and multiple deficits

avoided. The rapid deflation (reversal of overhydration) of the brain tissue after embolization is quite characteristic of the hydropic nature of the disorder (Fig. 3.37). In addition, cessation of the head circumference increase indicates the permanence of the result obtained. If the child, on the other hand, is referred too late with increased intracranial pressure that is already clinically detectable in addition to ventricular enlargement, embolization should be carried out first as an emergency procedure; however, clinical improvement will usually be insufficient even if the hemodynamic result proves to be spectacular, and a surgical ventricular drainage procedure (ventriculostomy or derivation) may have to be performed (Fig. 3.38). With this treatment sequence, the morbidity rate from the shunting procedure is lower. In our experience, following additional embolization and clamp testing, the ventricular drainage can often be removed in a few months. The reversed strategy, shunting first and then embolization, is the worst one for the child unless endovascular treatment is not available. Today endoscopic ventriculostomy seems to offer an acceptable alternative to the ventricular drainage after embolization in patients with already symptomatic hydrodynamic disorders if the base of the brain arteries and veins are not significantly enlarged at the level of the surgical opening. The overall stagnation at the mesencephalic aqueduct level observed on flow MRI sequences and the transfer to the cerebral ventricles with water congestion is then bypassed and it is likely to offer the skull base and spinal cord alternative resorption possibilities until the granulations mature. The morbidity of ventriculostomy is significantly lower than that of ventricular shunting.

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Fig. 3.41A–C. Prenatal diagnosis of VGAM. A Male neonate weighing 3,630 g at birth with a head circumference of 35 cm. Presented cardiac insufficiency responding to medical management. B Ventricular shunting was performed at 3 months of age. At the age of 6 months, MRI demonstrated a spectacular change in the size of the venous pouch as well as the torcular herophili. The child was referred for embolization at the age of 10 months. His lesion was completely excluded in two sessions 1 week apart. C Four years later, exclusion was confirmed, and complete shrinkage of the mass was obtained. Slight subependymal atrophy persists

Associated dysmaturation of the jugular bulb adds to the complexity of the situation and should be carefully assessed (see Sect. 3.12). Developmental delay is part of the natural history of untreated VGAM. Careful evaluation of neurocognitive performance shows that most children with macrocrania present some degree of mental retardation. In view of the poor prognosis of the disease, specialists and parents tend to accept as normal a child with mild retardation (up to 20% of normal for the chronological age). This level of delay allows the child to attend a normal school albeit with some support. To measure the neurocognitive

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Fig. 3.42A–C. Legend see p. 160

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Fig. 3.42A–E. Following ventricular shunting (A, B), a VGAM infant rapidly developed intracranial hypertension problems connected with (C–E) a slit ventricle phenomenon. At that time, no cortical veins were seen. C All drainage of the brain occurred via the veins of the base, posterior fossa, or spinal cord. Emergency embolization was performed at the age of 6 and 7 months, rapidly improving the clinical situation. Additional embolization at 2 and 3 years led to almost complete occlusion of the lesion. Seven years later, the child still has some motor sequelae from this acute intracranial hyperpressure episode; however, cognitive performance is satisfactory. Her score is 1

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status during follow-up, pediatric neurologists recommend the Denver test (Frankenburg et al. 1992) and the Brunet-Leisine test, which are easy and reproducible (see Chap. 2, this volume) for the purpose of therapeutic decision making. The developmental phenomenon is not one-dimensional. Development of different skills can be quite independent of other skills, and development of a single skill is usually influenced by multiple interactive factors. Development rates are determined by a variety of factors such as heredity, biological intactness, emotional health, as well as the physical and psychological environment. Deviation in development profiles is usually the result of multiple etiological factors. For instance, a child suffering from a hearing loss will have a different development profile than a child suffering from cerebral palsy or social depravation. One should interpret the developmental status of a child at one point in time with caution. It is more important to look at the rate of development over time and interpret the result together with what is known about the child’s background (see Chap. 2, this volume). Such tests are not meant to compare children, but are meant as an aid to follow a child’s ongoing development. The difference between the chronological age and the age apparent on testing is the basis for neurocognitive delay that we refer to in our scoring system. A 20% developmental delay is significant, but below 20% most children will catch up with continuation and eventually completion of endovascular treatment of the VGAM. Although there is no direct relationship between the degree of macrocrania and the severity of developmental delay (the head enlargement actually protects the brain), there is an obvious link between hydrodynamic disorders and the delay. Any event that creates a loss in compliance has an impact on brain maturation, e.g., intracranial hypertension, spontaneous decrease in the head circumference, or ventricular shunting. The specific evaluation score in VGAM neonates cannot be used for clinical follow-up in infants. We have chosen a more global clinical admission and outcome assessment. Although this type of quantification may lack certain details, it has been good enough to follow the progression in a given child. The use of these scores has helped us rationalize and compare our decisions and verify their stability over the past 20 years. Cardiac manifestations are differentiated into absent (5), asymptomatic cardiac enlargement (4), overload treated (3), failure stabilized (2), unstable failure (1). Macrocrania represents a non-neurological symptom, which is usually not treated and is assigned a score of 4. Children with a ventricular shunt who are neurologically asymptomatic or who have had an isolated seizure that is not treated have a score of 3. Children with seizures that are medically treated, or children with a delay of less than 20% have a score of 2.A unilateral hemianopsia, regardless of its cause, warrants a score of 2. Hemiparesis or monoparesis are serious neurological symptoms in infants and are assigned a score of 1 whatever the neurocognitive function (motor neurological deficit following ventricular shunting are included here).

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The next step is often marked by the effect of macrocrania on the skull base venous maturation. It should be considered in two parts, depending whether the sinuses have remained patent. Obviously no scoring is accurate in all situations and a new but persistent mild deficit in a 13-year-old child will not have the same meaning or prognosis as the same symptom in an 8-month-old infant without macrocrania.

3.11 Late Natural History of Vein of Galen Aneurysmal Malformation with Patent Sinuses This stage and its subsequent evolution can be described as chronic. All the possible acute damage has occurred by now. All manifestations clinically detected represent subacute and chronic manifestations of venous ischemia or brain loss due to the previous hydrodynamic disorders (Fig. 3.40). Seizures and mental retardation are the main symptoms seen if the correction of the AV shunt was not done in time, and they often occur in children who were referred late in the development of their disease or after ventricular shunting. Therefore, convulsions are not a necessary phase through which all VGAM patients pass, but rather indicate poor timing of treatment. Some patients with completely excluded VGAM and late cavernous sinus capture have developed pseudo-phlebitic appearance of the cortical veins. In some these cases, a seizure may reveal a focal cortical vein thrombosis requiring coagulation profile analyses and anticoagulation treatment (Scheme 2.1D).

Scheme 3.1D. Late neurological disorders

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Fig. 3.43A–D. Girl presenting with headaches at the age of 8 years; VGAM was diagnosed. A, B The lesion has a peculiar appearance with a reflux into choroidal veins (C, D). Note the unusual calcification in the putamina-caudate nuclei on both sides in association with more conventional types of subcortical calcifications

Some unusual endocrine manifestations have been reported, such as precocious puberty and failure to thrive. Pineal involvement and recruitment of the hypothalamohypophyseal portal system may constitute elegant explanations for the few cases quoted. However, they do not provide an explanation for all the apparently similar situations in which this endocrine dysfunction does not occur. Cerebral morphological sequelae express themselves in calcifications (Fig. 3.43), subependymal atrophy (pseudo-ventriculomegaly; Fig. 3.44),

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Fig. 3.44. A 4-year-old child was referred because of a neurological deficit and seizure in a neglected VGAM. The child presented with transient and recurrent motor hemiplegia on the left side. MRI demonstrated VGAM with significant bilateral calcifications in the subcortical region, but also in the putamina-caudate region, indicating transcerebral venous collateral circulation in the brain

and eventually the stigmata of previous acute accidents with cortical and subcortical atrophy (Fig. 3.45). It should be noted that in VGAM with patent sinuses, as opposed to cerebral AVMs, local or regional melting-brain phenomena are not encountered, since pial and therefore subpial reflux do not occur. The insult to the brain is therefore a slow and permanent one, as testified by the calcifications. There are different types: mural in the lesion itself where the calcifications are secondary to its partial or complete thrombosis; at the subcortical in the white matter, they reflect deep hydrovenous watershed failure. The latter occurs when the compliance of the medullary veins loses its ventriculocortical gradient and its activity is shifted from the subpial level to the medullary level (when pressure in the subarachnoid veins increases progressively following closure of the sutures). These calcifications are usually bilateral and symmetrical, located preferentially in the frontal region. The occipital lobe region is often affected earlier and may undergo subependymal atrophy with subsequent focal occipital horn enlargement and a thin splenium of the corpus callosum (Fig. 3.45). They may be asymmetrically located, mostly in unilaterally shunted children and often on the side opposite the shunt. These calcifications are not caused by a so-called cerebral arterial steal (Yu et al. 1987). Any transient episode of hydrocephalus may give rise to such calcifications, since it expresses the loss of compliance in the fragile hydrovenous system functioning in infants. A third type of calcification is located in the striatum and in the caudate and putamen bilaterally and symmetrically. These calcifications express subacute ischemia in the region of the prominent transcerebral collateral circulation system for the telencephalic veins. Striate vein congestion occurs after the cortical veins can no longer drain the cerebral white substance or when the persisting thalamic pathways (mainly diencephalic and rarely telencephalic) are overloaded with the drainage of the parieto-occipital regions. The calcifications indicate both

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Fig. 3.45A–B. Infant girl diagnosed as having VGAM because of macrocrania and prominent facial veins. The child received stereotactic radiosurgery at 10 months. Because of the failure to obtain a satisfactory result, the patient was referred to us at the age of 3.5 years with mild mental retardation. A CT shows diffuse bilateral and symmetric white matter calcifications and B a mural type of VGAM. C see p. 166

the mechanism and the specific vulnerability of this area at the infant stage. The clinical manifestations do not parallel the intensity of these calcifications. Some of them demonstrated during infancy after a brief episode of increased intracranial pressure may be absent on follow-up CT. Therefore, although indicative of a previous ischemic insult, the calcifications do not have a predictive value for neurological outcome in a treated VGAM. They rarely produce abnormal movement disorders that are most often seen with more posteriorly located damage. Subependymal atrophy is primarily seen in the occipital regions as a spontaneous progression of VGAM (see Fig. 3.46). It may be dramatic and

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Fig. 3.45. (continued) C The child was later embolized and her VGAM completely occluded in one session

Fig. 3.46A, B. MR studies 3 weeks apart showing the rapid changes occurring at the occipital horns of the lateral ventricles

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seems to be at least partially related to corpus callosum postnatal developmental delay. This atrophy remains reversible for a long time, with parallel growth of the splenium and a decrease in size of the occipital horn. Children that have undergone ventricular shunting do not show equal capacities for this correction and keep large ventricles at low pressure and a thin corpus callosum. Calcifications do not reflect an progressive process, but are rather scarring of past long-lasting insults. It seems that the degree of clinical sequelae depends on the severity of the brain insult over time and the rapidity with which appropriate correction of the disorders took place. This highlights the inability of imaging modalities to appreciate the true substrate of the neurological handicap. Focal evidence of iatrogenic hemorrhagic or acute hydrocephalus is infrequent, and their incidence should further diminish with the increased use of early endovascular management of macrocrania. Cerebral angiography may provide crucial information, as it demonstrates that, in the absence of pial reflux and in the absence of late venous thrombosis, hemorrhage does not occur. Exceptional association with subependymal cavernomas has been seen without introducing a new nosological entity. The rarity of such association does not justify a specific screening. It is important to realize that the clinical outcome of children with patent sinus outlets is relatively good compared to those with secondary occluded sinuses. This is probably the most clinically relevant observation to be derived from angioarchitecture analysis in infancy.

3.12 Dural Sinus Occlusion and Supratentorial Pial Congestion and Reflux Dural sinus occlusion and supratentorial pial congestion and reflux correspond to a dysmaturation of the jugular bulbs. The persistent medial occipital and marginal sinuses with VGAM flow seem to delay transverse sinus development. Most of the efferent torcular flow seems directed medially and does not trigger the sigmoid sinuses that remain distally thin.When finally the medial occipital and marginal sinuses disappear, the sigmoid sinuses will have fully occluded distally. The extracranial jugular veins are still patent and receive the inferior petrosal sinus (Fig. 3.47) (Scheme 3.1E). This progression of the VGAM is a very common one, although seldom recognized as the reason for a significantly different clinical outcome. The cause of the thrombosis is unknown, even if we acknowledge the influence of abnormal skull base growth maturation caused by macrocrania as opposed to a venous high-flow angiopathy. Thrombosis is one of hallmarks of AVM in children as compared to those in adults. Thrombosis is usually progressive and may develop slowly and without symptoms over a long period of time. In one neonate, a mild CCF was noted at the age of 10 days; which was well tolerated and therefore left untreated. MRI done at 2 months of age when the child presented with a slight macrocrania demonstrated a sinus thrombosis and a cerebellar area of hemorrhagic infarction (see Fig. 3.41). Although the infant had been asymptomatic, the fear of an impending acute event prompted angiography and embolization at that

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Fig. 3.47. A A 15-month-old boy presented with a mural VGAM with cardiac insufficiency and macrocrania. Tonsillar prolapse and ventricle dilatation resulted from jugular bulb occlusion. There was no mental retardation in relation with good cavernous drainage and inferior petrosal sinus drainage. Note the rarefaction of the temporal veins in relation to the sigmoid sinus thrombosis.VGAM diagnosed with macrocrania; the child was surgically shunted. He was referred at 12 months with severe mental retardation. Jugular foramen narrowing is present; however, no pial venous reflux is seen. B Collateral circulation uses posterior fossa venous outlets. Note in particular the perimesencephalic and peripontine vein outlining brain stem structures

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Scheme 3.1E. Pial reflux

time. The sinuses proved to have reopened, and embolization was carried out and repeated over time. At 4 years, the child was neurologically normal, had a score of 4 and has never had a further episode related to venous impairment. In some cases, time-of-flight magnetic resonance venography (MRV) may not show the jugular bulb stenosis or occlusion, mainly because of flow artifact or insufficient attention being paid to such features, but MRI with contrast enhancement should be able to reliably assess the status of the dural sinuses. Angiography demonstrates the secondary nature of the process and its effect on cerebral circulation. The development of a jugular bulb stenosis protects the heart but exposes the brain. Not only does it interfere with water resorption, but it also creates congestion within the cerebral veins.All symptoms will depend on the timing between the upstream effects of the stenosis and the capture of the sylvian veins by the cavernous sinus. The overall prognosis of an untreated VGAM is therefore largely dependent on the patency of the jugular bulbs. The more restricted the venous outlets, the less compliant the system. In the presence of moderate jugular bulb stenosis and capture of the cerebral veins by the cavernous sinus outlets, macrocrania and developmental delay may stabilize, as long as the stenosis does not progress further. The veins of the foramen ovale will be recruited, and in other situations the ophthalmic veins will reroute the brain drainage toward the facial veins (Fig. 3.48). This development facilitates the facial veins becoming collaterals in infants; they are not present at neonatal age, as the redistribution and capture of veins has not yet occurred. Under these circumstances, the combination of a VGAM and

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Fig. 3.48. A Female neonate diagnosed as having VGAM due to severe cardiac overload. Embolization had to be performed at 2 months of age. At 8 months of age, progressive macrocrania and facial circulation appeared, and cardiac overload had resumed. Note the facial circulation at 12 months. B Six years later, the lesion was completely occluded. The child was normal at 13 years of follow-up

prominent facial veins is a good indicator relief of cerebral venous hyperpressure in the absence of sigmoid sinus occlusion. If the jugular bulb stenosis is more severe or if a unilateral sigmoid sinus thrombosis has occurred, the VGAM and the brain may drain into the same cavernous sinus outlets (see Fig. 3.49). The VGAM will drain via the recently captured sylvian vein, and the brain via the superior petrosal sinus. If the transcranial openings are sufficiently patent, then the indirect effect of congestion is apparent on angiography as a phlebitic type of appearance of the cortical veins (Fig. 3.50). Despite this feature, clinical tolerance is still good. Epistaxis related to nasal vein congestion may occur, indicating increased flow through the ophthalmic vein (rather than an alternative hydrovenous pathway along the olfactory tract). Depending on the patency of the inferior petrosal sinus beyond the jugular occlusion, the cerebral pial congestion may exist without reflux. The long-term result is a chronic ischemic phenomenon with delayed calcifications and the peculiar appearance of the cortical veins. Conversely, if the superior-to-inferior petrosal sinus collateral bypass is not sufficiently patent, a longer collateral circuit for the VGAM drainage is necessary. Pial

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Fig. 3.49A–E. Legend see p. 172

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Fig. 3.49. A, B An 8-year-old boy referred to us because of VGAM and significant facial collateral circulation with bilateral proptosis. C, D Angiography demonstrated a choroidal type of VGAM with bilateral occlusion of the sigmoid sinus. Reflux from the superior sagittal sinus into the cortical veins joins the cavernous sinus bilaterally and subsequently the ophthalmic veins. Several transarterial embolization procedures were performed. A significant decrease in the flow to the malformation led to a dramatic improvement in the facial circulation. e In order to completely occlude the lesion, a transtorcular approach with balloon occlusion of the exit to the vein of Galen was used. Following successful placement of the balloon, the child had focal subependymal vein hemorrhage with a thalamocapsular hematoma, leading to rightsided hemiplegia. Progressive improvement occurred with incomplete recovery before discharge. F–I Late follow-up images demonstrated complete occlusion of the lesion. At 19 years of age, the child still presents with residual right-sided deficit

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Fig. 3.50. A, B Cerebral venous drainage remodeling. Neonate male presented with mild cardiac insufficiency and secondary macrocrania from a prenatally diagnosed choroidal VGAM. Embolized at 6 months, he was clinically normal 7 years later. Bilateral cavernous sinus drainage and the phlebitic aspect of the cortical veins despite complete exclusion of a VGAM was noted. He presented a seizure at the age of 8 years in relation to a cortical ischemic venous event. Three-dimensional views of pseudophlebitic venous cortical network (C, D)

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Fig. 3.51A, B. Typical aspect of papilledema on MRI T2 sequence in a case of VGAM with severe hydrodynamic disorders

venous reflux is then demonstrated, and macrocrania may progress to hydrocephalus and acute focal or diffuse damage may occur (Fig. 3.51): seizures, deficit, and hemorrhage. Under these circumstances, emergency endovascular management should aim to balance the flow of the AV shunt to the capacity of the posterior outlets and functionally split the VGAM drainage from the normal cerebral one. Unfortunately, this situation is a transient stage, and its progression to completion of the jugular bulb occlusion will occur if treatment is not undertaken immediately. The worsening of macrocrania at that stage enhances the triggers for further occlusion. The results of such urgent embolization should be rapidly clinically detectable and recognizable by the progressive disappearance of the facial venous collateral circulation and the normal neurological status (Fig. 3.48). The situation is particularly unstable if the occlusion has occurred and is bilateral, even if it has been present for a few years. The clinical tolerance is dependent on the capacity of the alternative outlets to drain the VGAM and the brain. These pathways always exist in infancy or childhood; otherwise the condition would be rapidly fatal, similar to neonatal dural sinus malformations (see Chap. 7, this volume). The risk of hemorrhage and venous infarction is high, as there is significant pial reflux and the VGAM has become an AVM draining into the pial venous system (Fig. 3.49). However, if the occlusion has not developed too quickly, the child may grow without acute hydrovenous failure and with progressive adaptation of the various collateral pathways. As the venous system compliance is reduced, transient neurological episodes (seizures or deficits) may express this fragile equilibrium of the venous drainage of the brain (Fig. 3.52). The neurological prognosis is still excellent if the treatment is started before the onset of acute symptoms. The hemodynamic goal might then be complete exclusion of the VGAM from the cerebral circulation.

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Fig. 3.52A–C. Legend see pp. 177

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Fig. 3.52D,E. Legend see p. 177

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Fig. 3.52. A An 8-month-old boy. VGAM was diagnosed due to rapidly progressing macrocrania. Angiography demonstrated a small choroidal type of lesion with patent jugular foramen at 9 months. He was embolized 5 months and 1 year later. Although he showed no delay in neurological aquisition, at the age of 3 years he had several attacks of right-sided hemiplegia lasting for several hours and resolving spontaneously. B, C Although partial stenosis had previously been seen, follow-up angiography demonstrated bilateral occlusion of jugular bulbs, retrograde opacification of the superior petrosal sinus, and pial reflux in the temporal vein and posterior fossa bilaterally. D, E Emergency embolization was performed, and the malformation was completely occluded. Two years later, the child was clinically normal. Note the spectacular stagnation of the veins (F) before treatment and their correction on the follow-up angiogram after embolization (G)

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Fig. 3.53. A A 10-year-old boy with MRI evidence of long-term effect of bilateral sigmoid sinus thrombosis with congestion of sinuses and intracranial veins. Note the spectacular bone hypertrophy corresponding to the recruitment of the transcranial venolymphatic outlets. B, C Note the dural sinus shunt on the torcular and the sigmoid sinus. Following complete embolization of the remaining malformation, the dural shunts disappeared. D Different child with prenatal diagnosis of VGAM. The child presented at birth with cardiac overload responding to medical treatment. Instability in the response led to embolization at 22 days of age. Note the spectacular transdural supply to the lesion

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Fig. 3.54. A, B A baby boy diagnosed at the age of 1 year with macrocrania associated with a small VGAM. Ventricular shunting was performed, and progressive spontaneous thrombosis of the jugular bulbs was demonstrated. Neurological deficits following ventricular shunting were found, as were seizures and mental retardation. The child was referred to us at the age of 2 years and embolized. A deficit remains and the child has a score of 1 at age 5. He also shows some psychotic behavior. C Note on MRI the various transcerebral collateral circulations bridging the cortical system to the deep venous system. Striate vein collateral circulation calcification of the region is clearly demonstrated. D see p. 180

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Fig. 3.54. (continued) D There is bilateral occlusion of the sigmoid sinuses

Dural AV shunts may develop within the thrombosed portion of the sinus (Figs. 3.53, 3.54). In our series, they caused no specific clinical symptoms. They disappeared following complete obliteration of the VGAM. The condition of bilateral jugular bulb occlusion and pial venous reflux may exist for a few years, and some children with undiag-nosed VGAM may present late with intracerebral hematomas, or subdural or subarachnoid hemorrhagic events. These are rare examples of hemorrhages seen in children or young adults with true VGAM. It is of interest to note that, after approximately 5 years of age, only subacute or chronic symptoms tend to occur, as well as sequelae of already preexisting dysfunction. Failure to thrive, bone hypertrophy, mental retardation, cerebral calcifications, and some psychiatric syndromes can be noted in older children or young adults. Once the optimal therapeutic window has been missed, these symptoms can no longer be reversed, even if the lesion is obliterated.

3.13 Dural Sinus Thrombosis and Infratentorial Pial Reflux The infratentorial consequence of the sinus occlusion is tonsillar prolapse (see Chap. 1, this volume; Fig. 3.55). It is secondary to the cerebellar pial congestion and only appears in its presence. It may disappear with correction of the AV shunt, provided that the prolapse has not existed for a long time (Fig. 3.56). It does not create any specific symptoms at this age. The long-term effects of this condition are unknown, since it is likely that most children that present with this complication of jugular bulb stenosis are in the worst natural history group; however, a case of a torcular dural sinus malformation in a child with a tonsillar prolapse revealed the presence of

Dural Sinus Thrombosis and Infratentorial Pial Reflux

181

Fig. 3.55A–D. A 2-year-old boy presented with a VGAM with macrocrania. The child was referred to us at the age of 7 years. He already had severe mental retardation. A Initial angiography demonstrated a choroidal type of VGAM. B Consecutive angiography (during embolization sessions) demonstrated the progressive occlusion of the jugular bulbs with the reflux into the cortical veins and progressive cerebral congestion. The child was embolized twice with significant improvement in clinical status. At 10 years of age, he still had a score of 1. C, D Note the tonsillar prolapse and the perimedullary veins on angiography

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Fig. 3.56A–D. Legend see p. 183

Dural Sinus Thrombosis and Infratentorial Pial Reflux

183

Fig. 3.56A–G. Neonatal diagnosis of VGAM. A male neonate weighting 3,310 g presented with cardiac failure responding to medical treatment. He was referred to us at 3 months. A–D He had a mural type of VGAM. Some jugular stenosis can already be seen. D, E He developed progressive occlusion of the remainder of the jugular foramen as well as asymptomatic tonsillar prolapse. F, G Embolization led to complete occlusion of the malformation. At that time, some degree of reopening of one sigmoid sinus was noted. Six years later, MRI showed complete occlusion of the lesion. There is partial shrinkage of the mass and resolution of the tonsillar prolapse

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Fig. 3.57A, B. Unusual severe supratentorial melting-brain syndrome predominantly affecting the occipital lobes and tonsillar prolapse. Both express the hydrovenous constraints exerted and their morphological consequences (A, B)

syringomyelia on 10-year follow-up (Apsimon 1993; see Fig. 2.28). It is most important to understand that the prolapse is not related to global intracranial hypertension, even if the mechanism that creates it is also able to produce supratentorial hydrodynamic failure (Fig. 3.57). Therefore, evidencing a prolapse does not indicate emergency ventricular shunting, but rather embolization to diminish the relative importance of the VGAM drainage in the overall venous pathways. In fact, progressive ventricular enlargement is usually not associated with tonsillar prolapse. In addition, this anomaly does not occur at the neonatal age (see Chap. 2, this volume); it is not related to the volume of the VGAM ectasia (Fig. 3.58; see also Fig. 3.59), but to the venous changes that have occurred over time and to their effect on water dynamics. It also does not represent an associated Chiari-1 malformation. On the contrary, some secondary or associated Chiari-1 malformations might very well have the same physiopathological explanation as some skull base craniostenoses. The significance of tonsillar prolapse in VGAM is the same as in CAVMs or dural AV shunts (see Chaps. 4, 5, 7, this volume) and develop in the same age group. Jugular bulb occlusion occurring after the age of 5 years would not have the same hydrovenous consequences as those described above. Yet congestion of posterior fossa veins will lead to brain dysfunction and/or hemorrhages supporting an active endovascular approach (Fig. 3.60) (Scheme 3.1F).

3.13.1 Spontaneous Thrombosis

Spontaneous thrombosis of the VGAM is rare (Fig. 3.61). In our experience, 2.5% of patients showed spontaneous thrombosis, but only half of them are neurologically normal, which is less than what proper treat-

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185

Fig. 3.58A–C. A 6-month-old boy with VGAM diagnosed because of macrocrania. A He was shunted at the age of 8 months, with a significant increase in the vein of Galen size. The patient was referred to us at the age of 10 months. B The malformation was excluded in one session. One year later, a follow-up angiogram confirmed complete occlusion of the lesion and MRI demonstrated shrinkage of the mass. C Note the persisting subependymal atrophy and the absence of tonsillar prolapse despite the size of the supratentorial ectasia prior to its embolization

ment can now accomplish. In addition, this thrombosis is mostly unpredictable, although the tentorial edge compression of the arterial feeders together with the secondary intraluminal thrombosis in the stenosed draining veins might be an indication of such a development. In any event, this thrombosis tends to occur late, when cerebral damage may already be irreversible. It is possible to make a retrospective diagnosis of a completely excluded VGAM by recognition of the persistent embryonic arrangement of the deep cerebral veins. Spontaneous thrombosis should not be considered as a favorable outcome, and expecting it to occur is not a therapeutic strategy and now constitutes an unacceptable choice.

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Fig. 3.59A–C. Legend see p. 187

Spontaneous Thrombosis

Fig. 3.59. A Male infant with a VGAM presented with significant macrocrania. Ventricular shunting was performed shortly after diagnosis. Facial collateral circulation and moderate mental retardation were observed. The child was referred to us at the age of 2 years. Embolization of the malformation was performed in one session. B, C Immediately after embolization, a significant reduction in the flow was noted, with whirling phenomena inside the pouch and complete stagnation. D–F Following embolization, he was kept asleep for 1 day. It took him 5 days to wake up. Note the fluid level within the pouch. F Complete shrinkage of the mass was observed at 1-year follow-up. At the age of 13, the child had a score of 5

187

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Fig. 3.60A–D. Legend see p. 189

Spontaneous Thrombosis

189

Fig. 3.60. A, B A child who was a few months old with a well-tolerated VGAM was referred to radiation therapy and lost for follow-up. He was referred to us at the age of 10 years with rapidly progressive brain stem symptoms related to venous congestion secondary to outlet restrictions (C, D). Angiographic aspects (E, F)

Neonate

Infant

Child <5 Years

Child >5 Years

Congestive cardiac failure

Multiorgan failure Encephalomalacia

Macrocrania hydrocephalus Hydrodynamic disorders

Dural venous thrombosis (sigmoid s., jugular bulb Decrease in head circumference

Neurocognitive delay

Infratentorial pial reflux and congestion

Subependymal atrophy (pseudo ventriculomegaly) calcifications (chronic venous ischaemia)

Tonsillar prolapse Optimal therapeutic window

Hydromyelia or syringomyelia F

Scheme 3.1F. Infratentorial disorders

Convulsions Neurological deficits Cerebro-meningeal haemorrhages

Epilepsy Neurological deficits

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Fig. 3.61. A–B „Spontaneous“ occlusion of VGAM revealed by macrocrania with ventriculomegaly shunted at 7 months of age. C, D Follow-up angiography performed at 1 year demonstrates complete occlusion of the VGAM with calcification of the wall of the pouch. The deep venous drainage pattern of the brain confirms the diagnosis. Arrows, deep venous drainage, and arrowhead, torcular stump, in D

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191

3.14 Objectives and Methods of Treatment 3.14.1 General Remarks

The aim is for a child to develop normally without neurological sequelae. To achieve this, normal cerebral development does not require, in all cases or at all times, rapid morphological disappearance of the AV shunt or rapid shrinkage of the ectasia. However, disappearance of the ectasia over time will result from a successful transarterial approach. We have never observed regrowth of a shrunken VGAM. To reach the objectives mentioned above, similar to other teams (Berenstein 1992; Seindenwurm et al. 1991), we favor transarterial embolization using the femoral approach with glue (N-butyl cyanoacrylate, NBCA) as the primary embolic agent. This method has proven reliable and predictable results. The perioperative technical aspects and results will be discussed below (see also Vol. 2, Chap. 14). We have chosen not to use coils, balloons, or particles as first-line agents, as they are inappropriate materials for the treatment of these high-flow lesions. We cannot comment on the transvenous approach, which has not yet been reported to provide reliable benefit as a primary form of treatment in children as compared to the transarterial approach. The available results regarding the long-term neurological outcome (Mickle and Quisling 1986; Mickle and Peters 1993) and the unpublished morbidity and mortality rates with the transtorcular and transjugular venous approaches confirm the doubts expressed in the mid 1980 s when this technique was first introduced. In any case, the treatment goal being good clinical outcome, our discussion will be based on the results observed from the consistent management of 300 VGAM patients during the past 20 years.

3.14.2 Neonates

The idea that a neonate with severe multiorgan failure would do well if the VGAM were to be excluded is wrong; there is evidence in the literature that in neonates following properly performed emergency embolization, the neurological outcome was disastrous, despite apparently normal pretherapeutic brain imaging (ultrasound or CT). This emphasizes the importance of a thorough analysis in order to best predict the degree of cerebral tissue impairment not evident on diagnostic imaging. We are very aware of the difficulty of making these observations and decisions, and this is actually the basis and purpose of the VGAM neonatal score. The relationship with the parents and fair information on the disease and results of the therapeutic team are crucial in the decision-making process. Thus we do not perform embolization in a neonate with evidence of severe cerebral damage (25/140 neonates) or severe multiorgan failure (score of less than 8, 17/140 neonates) in whom embolization would only be a technical challenge without any hope of acceptable clinical benefit. This was the case in 17% of the patients referred to us with VGAM, representing 42 out of 140 neonates (30%). This group thus forms the most seriously ill group with a high spontaneous mortality rate.

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Prenatal diagnosis is not by itself an indication to perform early delivery, interruption of pregnancy, or caesarian section at term. Few prenatal manifestations have thus far shown prognostic value that are today an indication for abortion (3/93): in utero cardiac failure and cerebral damage. In both in utero instances, these findings are associated with severe irreversible multiorgan failure at birth. Cardiac manifestations have been reviewed for neonates (Garcia Monaco 1991b; Chevret et al. 2002; Frawley et al. 2002) and for prenataly diagnosed VGAMs (Rodesch et al. 1994). Over 140 neonates (including the prenatally diagnosed cases referred) only 23 (among the 95 cases that were felt to likely have an acceptable neurological prognosis) needed to be embolized at neonatal age. Yet half of these patients died despite treatment. The role of the pediatric intensive care physician is crucial in the neonatal age management of VGAMs. We rely heavily on their analysis of the controllability of the various disorders and their therapeutic choices. The following information will be useful in the management strategy (Chevret et al. 2002):
Clinical evaluation of the baby and documentation of all the possible events that have occured since birth (convulsions, for example, do not occur in VGAM at this age unless brain damage has already taken place)
Evaluation of renal and liver function
Transfontanellar ultrasound
Evaluate for possible encephalomalacia
Research cerebral arterial flow reversal
Cardiac ultrasound to evaluate hemodynamic status: (Fig. 3.62) – Right and left end diastolic diameters – Left ventricular shortening – Stroke volume – Left ventricular output – Systolic arterial pressure – Research of patent ductus arteriosus and foramen ovale – Ductal flow if present – Search for descending aortic flow reversal – Shape of the interventricular septum – Search for associated cardiac malformation that might require specific treatment
Good-quality MRI to provide all necessary morphological information regarding the lesions and the status of the brain tissue
Electroencephalogram to evaluate neurologic maturation and eliminate seizures Cerebral AV shunts result in a hemodynamic hyperkinetic state characterized by a high cardiac output and a decrease in vascular systemic resistances. The hemodynamic consequences are of variable intensity, ranging from mild cardiac overload to cardiogenic shock. AV fistulas lead to an increase in venous return and subsequent right heart overload. The result is right heart dilatation, pulmonary arterial hypertension and increased pulmonary blood flow. The resultant greater pulmonary venous return to the left heart increases left ventricular diastolic volume, which

Neonates

193

Fig. 3.62A–D. Cardiac ultrasound evaluation. A Right cardiac failure with rightchamber dilatations; B dilated pulmonary arteries; C,D see p. 194

may be further increased by a possible persistent arterial duct. The consequence of the increased left ventricular preload is an increase in stroke volume and stroke work. Excessive stroke work results in increased myocardial oxygen requirements. Coronary perfusion to the left ventricle occurs mainly during diastole and depends on the systemic arterial intramyocardial diastolic pressure difference as well as the duration of diastole. Therefore, a reduction in arterial diastolic pressure (as observed in AV shunt), an increase in end diastolic pressure (due to increased preload), and a reduction in diastolic period (due to tachycardia) are all detrimental to myocardial perfusion, and hence oxygen delivery, and may precipitate left ventricular failure. Thus, even if only the right ventricle

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Fig. 3.62. (continued) C suprasystemic arterial pulmonary hypertension with tricuspid regurgitation; D type 3 interventricular septum pattern

fails initially, biventricular failure frequently follows depending on the size of the left to right shunt. Several mechanisms are involved in the attempt to maintain myocardial performance, normal systemic output, and adequate tissue oxygenation in the event of cerebral AV fistulas. One of them is increased catecholamine release. As a result, there are increases in heart rate and in the force of contraction of the myocardium. It should be noted that catecholamine release also has a detrimental effect on heart work by increasing left ventricular afterload. In the neonatal period, such compensatory mechanisms are limited, because the sympathetic nervous system is immature at birth and because myocardial reserves are limited. The limitation in myocardial reserves is anatomic and functional.

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195

The neonatal heart contains a high proportion of noncontractile fibers. Moreover, all functional cardiac reserves are mobilized to deal with adaptation to extrauterine life, and the resting cardiac output required to provide oxygen to the tissues is at its maximum level. Consequently, the heart is limited in its reserve capabilities and cannot cope with the extra work imposed by the fistula. These factors explain the rapid progression toward cardiogenic shock observed in neonates with high-flow fistulas. Furthermore, the transition from a fetal circulatory pattern to an adult circulatory pattern is complex, and both pulmonary and systemic circulations remain highly unstable during the 1st week after birth. This can explain a persistent transitional circulation with shunts through the ductus arteriosus and the oval foramen and a pulmonary hypertension, which worsen the systolic and diastolic wall stress. Pulmonary edema is linked to high pulmonary blood flow and to left ventricular failure. Pulmonary edema creates a reduction in distal ventilation. Consequently, arterial oxygen content and therefore also oxygen delivery decrease, leading to the shock. Right heart failure secondary to increased venous return creates congestion in the suprahepatic veins and secondary retrograde congestion in the centrolobular region of the liver. In patients in whom cardiogenic shock supervenes, reduction in hepatic arterial blood flow may precipitate centrolobular necrosis. These are the regions that are most sensitive to ischemia, but in the majority of cases the double vascular supply to the liver (portal vein and hepatic artery) protects the liver from ischemia, and hepatic dysfunction is only reflected in mild biological changes. A reduction in cardiac output and mean arterial blood pressure can reduce the glomerular perfusion pressure. This may cause oliguria or anuria and activation of the renin-angiotensin system. This situation worsens the working conditions of the heart. The renin-angiotensin system activation increases left ventricular afterload by vasoconstriction and the preload of the right ventricle by increased circulation volume and increased sodium and water reabsorption (through associated secondary hyperaldosteronism). Thus diuretics play a critical role in management. The role of the atrial natriuretic factor has not been documented in this situation, but from experimental studies we have seen that it is probable that its influence is modest. There is often aortic and middle cerebral steal of the diastolic flow assessed by echo Doppler. This steal usually has no consequences on whole brain maturation, which is more dependent on hydrocephalus and heart failure. The clinical presentation depends on the size of the left-to-right shunt and tolerance. If the shunt is not large, cardiovascular manifestations are usually mild. Major symptoms are sweating, feeding difficulties, and poor weight gain. Major signs are continuous murmur with a dancing carotid pulse and distended jugular veins. There is tachycardia, and the peripheral pulses are also bounding. Systolic arterial pressure is normal, but diastolic pressure is low. The liver is always enlarged. Patients with cardiogenic shock present with respiratory distress, pallor, and often coma. All pulses except the carotid pulses are feeble. Systemic arterial blood pressure has a tendency to drop. The capillary refilling time is prolonged to over 3 s. Pulmonary edema is indicated by respiratory distress, tachyp-

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nea, and rales on auscultation of the lungs. The patient is oliguric or anuretic, and metabolic and lactic acidosis are present. Chest radiography demonstrates cardiomegaly, especially of the right heart. The superior vena cava is generally markedly dilated, and there may be signs of pulmonary edema. Electrocardiographic evidence of atrial and ventricular hypertrophy depends on the duration and magnitude of the shunt and the degree of heart failure. Echocardiography is the best method of assessing the cardiac consequences of the fistula; it demonstrates right ventricular dilatation. The distensibility and compliance of the right ventricular wall are compromised. The left ventricle is hyperkinetic with a shortening fraction of greater than 40%, a normal shortening fraction indicating a left ventricle failure. Echocardiography and Doppler ultrasound can measure pulmonary hypertension, ejection fraction, stroke volume and cardiac output and can detect a tricuspid insufficiency. Echocardiography is also useful for the diagnosis of persistent ductus arteriosus or a cardiac malformation, which must be corrected before any decision is made concerning endovascular treatment of the AV shunt itself (Tables 3.3, 3.4; Chevret et al. 2002). The aims of symptomatic therapy are to improve oxygen delivery to the tissues and decrease tissue oxygen consumption. If cardiac failure cannot be controlled by these measures, embolization of the AV shunt should be considered.

Table 3.3. Cardiac parameters before the first endovascular embolization of the VGAM Ultrasound parameters

Death (n=12)

Survivalb (n=12)

P

PDA (right-to-left shunting, %) LVEDD (mm) LVSF (%) RVEDD (mm) SIV pattern 1 /2 / 3 (n)a Cardiac output (ml:min.kg–1) Systemic arterial pulmonary pressure (mmHg) Suprasystemic arterial pulmonary pressure (%) Descending aortic diastolic reverse flow (n)a

10 (83.3%)

4 (33%)

0.003

20 (10–23) 47 (30–55) 16 (11–25) 0 /2 /8 395.5(265–650)

20 (15–27) 39.5 (31–53) 15.5 (8–18) 4/3/2 325.5 (224–500)

0.23 0.68 0.82 0.005 0.29

67.5 (44–85)

65 (40–90)

0.19

70%

20%

0.031

8

1

0.0007

LVSF, left ventricular shortening fraction; LVEDD, left ventricular end-diastolic diameter; RVEDD, right ventricular end-diastolic diameter; SIV, interventricular septum; PDA, patent ductus arteriosus; VGAM vein of Galen aneurysmal malformation.aMissing data in three survival and two dead infants. b Missing data in four survival and two dead infants.

Improving Oxygen Delivery

197

Table 3.4. Clinical characteristics of newborns with VGAM and severe cardiac failure (Chevret 2002)a, b n Sex ratio F (%) Gestational age (weeks) Birth weight (percentile) Head circumference (>95th percentiles) VGAM diagnosis (days of life) CCF diagnosis (days of life) MV onset (days of life) Bicêtre PICU admission (days of life) Inotropic drugs use Endovascular treatment Yes First session (days) Neurological outcome Developmental delay Epilepsy

All 24

Death 12

Survival 12

P

37.5 40 (36–42.7) 75th 50% 2.5 (0–15) 1.5 (0–14) 3 (0–19) 12 (0–25) 54%

42 40 (36.7–41) 75th 50% 1.5 (0–15) 2 (0–14) 2.5 (1–19) 12 (2–22) 100%

33.3 39 (36–42.7) 75th 50% 3 (0–8) 1 (0–5) 3 (0–17) 11.5 (0–25) 8.3%

1 0.58 1 1 0.1 0.2 0.47 0.56 <0.0001

75% 21 (7–38)

50% 20 (11–29)

100% 26 (7–38)

0.014 0.68

66.7% 27.3%

VGAM, vein of Galen malformation; MV, mechanical ventilation; CCF, clinical cardiac failure; PICU, pediatric intensive care unit. a Results are expressed as percentage or median (range) as appropriate. b Fischer’s exact test and Wilcoxon rank sum test are used for statistical analysis.

3.14.2.1 Reducing Oxygen Consumption

In patients with severe distress, tracheal intubation and mechanical ventilation reduce oxygen consumption and improve myocardial performance by limiting right heart overload. Oxygen consumption can also be reduced by providing good external warmth for small infants and by prescribing bed rest and sedation.

3.14.2.2 Improving Oxygen Delivery

Oxygen transport is determined by three factors: arterial oxygen saturation, hemoglobin concentration, and cardiac output. Measures that improve the patient’s effective ventilation, arterial oxygen saturation, and hematocrit should therefore be the first steps taken to treat patients with heart failure. Endotracheal intubation and adjustments of fractional inspired oxygen concentration on mechanical ventilation are often necessary to obtain an adequate arterial saturation. The goal is to obtain an arterial saturation equal to 100%. Hemoglobin concentration should be maintained between 10 and 12 g/dl, and the hematocrit level at about 30%. A higher concentration of hemoglobin may induce blood hyperviscosity and hence a decrease in oxygen transport. Since cardiac output is determined by preload, afterload, contractility, and heart rate, effective drug therapy influences one of these factors.

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Diuretics are the first step for reducing preload. They are given to eliminate excess salt and water and to prevent their reaccumulation. Furosemide is the most powerful agent (2–4 mg/kg per day in four IV injections or orally). Diuresis is often more rapid and effective if the drug is given intravenously. This diuretic tends to eliminate potassium; thus serum potassium must be measured periodically and potassium supplements may be needed. One alternative to the use of diuretics is to attempt to restrict sodium and fluid intake. Water intake may be reduced to 60%–80% of maintenance levels. Cardiac output can be improved by increasing cardiac contractility with inotropic agents. Digoxin is the main agent used for increasing myocardial contractility. However, its use in hyperkinetic states due to AV fistulas remains controversial: pretreatment myocardial function indices may already be above normal, and there is no clear evidence that their further increase has any clinical benefit. Theoretically, when left ventricular dysfunction from chronic volume overload occurs, digoxin should be beneficial. Digoxin also slows conduction, thus beneficially lowering ventricular rates and improving myocardial perfusion. The oral loading dose of digoxin is 30 mg/kg in newborns, and the maintenance dose is 10 mg/kg per day. In situations of severely compromised cardiac output, catecholamines are powerful boosters of myocardial contractility. Dobutamine and dopamine can be used. These agents should be administered under close supervision, optimally with monitoring of arterial pressure, central venous pressure, heart rate, and urinary output. Dobutamine is less chronotropic and arrhythmogenic than dopamine, and it may have a more direct effect on enhancement of coronary flow. These drugs can be used in concert with other agents, such as afterload-reduction drugs. Amrinone, an inhibitor of myocardial cyclic adenine monophosphate (cAMP) phosphodiesterase activity, is the most recent drug proposed in cardiogenic failure without drop of systemic arterial pressure. This drug has the combined effects of inotropic support and peripheral vasodilation. However, pediatric experience is limited. Cardiac output can also be improved by decreasing ventricular afterload. However, vasodilators should be used with caution, because vasodilation can produce severe hypotension, decrease coronary perfusion, and cause myocardial ischemia. Vasodilators are obviously contraindicated if systemic arterial pressure is low. For chronic vasodilation, an angiotensin-converting enzyme inhibitor can be used (0.1–0.4 mg enalapril/kg per day in one or two doses; 0.1 mg captopril/kg per day in one or two doses with a progressive increase to 2 mg/kg per day). When sodium is depleted secondary to initial measures, it is important to start with low doses, monitoring for a possible drop in arterial blood pressure. Part of this neonatal VGAM group with CCF is identified as carrying harmful manifestations such as suprasystemic pulmonary hypertension resistant to NO (Chevret et al. 2002). This group was not identified 10 years ago and this raises the possible deleterious side effects of active ICU management and oxygen therapy on postnatal lung vascular maturation (pericytic vascular coverage). There is now experimental evidence to suggest that increased pulmonary blood flow and pulmonary hypertension can alter normal post-

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natal vascular remodeling, preventing a fall in pulmonary vascular resistance, even once the cause of pulmonary overflow is removed (Reddy 1995; Jouannic 2003). A recent fetal model with high pulmonary blood flow, obtained by aortopulmonary shunt placement, provided for an alteration of the endothelin cascade by earlier upregulation of gene expression, contributing to vascular remodeling and enhancement of pulmonary vascular reactivity (Black 2000). In severe situations with mechanical ventilation and a high level of pulmonary hypertension, fine evaluation of hemodynamic parameters (see Sect. 3.15) should be decisive so as to provide the best medical treatment associated with diuretics and fluid restriction:
Reopen ductus arteriosus with prostaglandin E1, alprostadil (ProstineVR“) (in case of closed ductus arteriosus with dilatation of right chambers)
Use other inotropic agents: amrinone (with vasodilatation effect benefit to pulmonary pressure), dobutamine or dopamine.
Agents used in pulmonary hypertension (PHT) of other diseases: nitric oxide (NO)or prostacycline. The indication to reopen is typically in VGAM neonate with CCF associated with iso or suprasystemic PHT. Alprostadil is used in perfusion and starts at 0.1 g/kg per min until response is obtained then doses will decreased until 0.01 g/kg per min to find the smallest efficient dosage. The main secondary effects are tachycardia fever, apneas, and cutaneous flush. Alprostadil is used to temporarily relieve the right ventricle, in order to fully evaluate the consequences of the CCF and to decide on whether early endovascular management is needed. Two-thirds of neonates referred could be treated in infancy; if we add the patients who were diagnosed at that age, three-quarters of VGAM babies could be treated at the time of the optimal therapeutic window. In neonates, the immediate goal is to not only to restore a satisfactory systemic physiology and to gain time (Abbit et al. 1990; Garcia Monaco 1991a; Gomez et al. 1963; Norman and Becker 1974), but also to recreate the conditions enabling postmaturation of the various vascular systems. It is apparent that the VGAM neonatal score used during the first few days of life varies from one day to the next depending on the response to medical treatment. Failure to observe a response to ICU management (or stagnation) leads to early embolization at neonatal age. The end point of partial embolization is usually the reduction by one-third to one-half of the AV shunt for a significant systemic impact. This is still very subjective; however, we use endovascular or follow-up hemodynamic tools that allow these changes induced by embolization to be quantified (Moersdorf and Lasjaunias 1996). Immediate clinical evaluation with cardiac ultrasound demonstrates the response to the embolization and the possible need to repeat the intervention. Waiting till the 5th month of age to perform the first diagnostic and therapeutic angiogram is the optimal timing whenever feasible. If the parameters that have been chosen during that period are not reached, then the date of this session is brought forward. In some small VGAMs, unusually severe CCF or PHT may be noted. Lack of response to drugs must lead to a careful search for an associated cardiac malformation, primary pul-

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monary disease, or an undesired persistent ductus arteriosus. The latter should regress rapidly and spontaneously; if this is not noted and before embolization, thorascopic clipping should be discussed. A high-quality cardiac ultrasound study can show the role played by the present fetal circulation in persistent CCF. The physiopathology of such CCF, mimicking fetal persistant circulation in its most severe forms, is better known.

3.14.3 Infants and Children

In infants and children, the immediate goal is to preserve the hydrovenous equilibrium and normal development and at the same time to exclude the lesion. Our concern in patients of this age is to anticipate the natural history in order to avoid ventricular shunting (Andeweg 1989; Del Bigio et al. 1985; Sainte Rose et al. 1984; Zerah et al. 1992; Girard et al. 1994; Gibson et al. 1959). Understanding the mechanisms of clinical expression (Scheme 3.1A–F) and their reversibility with appropriate treatment is the basis for a coherent management policy for this disorder. The concept of a therapeutic window derived from this understanding helps us optimize treatment management and timing (Fig. 3.63). Premature attempts to exclude an asymptomatic lesion or taking significant technical risks to exclude, in a single session, a VGAM that presents no immediate cerebral danger and can be eradicated in two or three sessions should not be encouraged. Conversely, a decision not to treat on the assumption that an asymptomatic lesion is well tolerated is certainly naive and dangerous. At this age, reliance on the parameters and scores presented above is recommended. Pediatric neurologists will provide all the necessary information on the progression of the child and the need to improve the capacity for normal development. In the series used in this chapter, the treatment was declined in 9 out of 125 young infants and 3 out of 52 older children who presented severe brain damage. In others, referred late with already permanently impaired functions or severe developmental delays, treatment attempted to improve the quality of life. Under these circumstances, endovascular treatment has also proven to achieve satisfactory results, even with incomplete exclusion of the lesion. Endovascular endpoints will be directed to the draining pattern of the brain dependent upon the presence and degree of cavernous sinus capture, jugular bulb maturation, parietal convexity sump effect, venous stagnation from sinus congestion, pial reflux, superior petrosal to lateral mesencephalic reflux and posterior fossa venous congestion, subependymal veins reflux, etc. Although the volume of the ectatic vein does not seem to be mechanically responsible for brain stem compression, shrinkage of the pouch is always a welcome reward for an effective transarterial embolization. As mentioned in the analysis of the natural history, the fact that a given VGAM has transformed into a VGAM draining into pial veins necessitates complete exclusion, as a formal goal, in order to eliminate the risk of hemorrhage. In this situation, the strategy and timing may be similar to that in any nonruptured, deep-seated lesion in which embolization and combined approaches can be contemplated.

Infants and Children

201

Fig. 3.63A–F. Prenatal diagnosis of VGAM at 34 weeks of gestation. The baby was born by caesarian section weighing 3,300 g and was macrocephalic with a head circumference of 36 cm (more than 2 SD). Cardiac failure responded to medication, with a neonatal score at 16. A Because of the instability of the response to medical treatment and the severity of the macrocrania, embolization was performed at 3 months and 4 months. B Complete occlusion of the malformation was achieved. C–F One year later, complete occlusion was confirmed, but the child had severe mental retardation, indicating underestimated consequences of the early hydrovenous disorders despite the absence of true hydrocephalus. Note the pseudo-phlebitic appearance of the cortical cerebral veins bilaterally. D–E see p. 202

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Fig. 3.63D–F. Legend see p. 201

General Remarks

203

3.15 Technical Management 3.15.1 General Remarks

We favor the transarterial femoral approach to deliver glue in situ as the first treatment modality in every case. In some rare cases, we have had to perform the femoral puncture with the help of Doppler ultrasound. The smallest baby that was embolized weighed 2.0 kg. No cut-down has been necessary in our experience. We try to obtain complete exclusion in the lowest number of sessions, but this desire is primarily guided by the clinical stability observed in the infant. On one occasion, we failed to embolize a young infant as we did not achieve a safe catheter a safe position and he died shortly thereafter. An average of 2.4 sessions per child is needed to obtain the expected therapeutic goal. The venous route was used in 5% of cases when it became impossible to achieve effective embolization via the arterial route or to specifically disconnect a sinus reflux in order to protect the brain. In each case, the child was in a clinical condition that required immediate treatment; no deliberate attempt was made to completely exclude the VGAM drainage considering the hemorrhagic risk related to the sudden congestion of nonvisualized subependymal anastomoses. The largest arterial contributors to the lesion should be embolized first. The microcatheters to be used are a combination of flow-guided and over-the-wire devices, their size depends upon the flow of the feeders to be excluded and the agent selected. In high-flow lesions, one of us (PL) uses the Baltacci P1,8 (Balt Extrusion, Montmorency, France) specially designed for high-flow lesions in babies. This microcatheter is used directly through the 4-F sheath, without a guiding catheter; therefore, no co-axial system is used in 90% of neonatal or infant cases. Catheterization is usually rapid, since these devices can straighten the vertebral and internal carotid cervical skull base kinks. Microcatheters that are too soft are often unstable during fast injection of pure glue, while the over-the-wire microcatheters tend to be stiff or kink in these loopy vessels. The occlusion of the VGAM can often be obtained in one or two sessions; however, the purpose is not the fastest time to obtain 100% exclusion of the lesion but rather the safest reduction that guarantees normal cerebral maturation and neurocognitive development (Table 3.5). Whenever the occlusion of the malformation of the Galen vein is complete or almost complete, we recommend keeping neonates and infants under general anesthesia for the next 24 h in the ICU. This protocol has been used since the beginning of our experience in order to avoid the unnecessary agitation of a baby awakening. Babies are woken up the following day. There are no specific postoperative measures taken in the management of most of these patients, except for in the situation mentioned above; in particular, no heparin or steroids are utilized; blood pressure is kept at a normal level while the child is asleep in the ICU. Endovascular treatment sessions are arranged every 3–6 months depending on the clinical status and response to the embolization.
Femoral punctures should be avoided in the ICU as should scalp or jugular venous lines.

204

3 Vein of Galen Aneurysmal Malformation

Table 3.5. Bicêtre Admission and Outcome Scorea Score

Condition

5 4

Normal (N) Minimal non-neurological symptoms (MS), not treated and/or asymptomatic enlargement of the cardiac silhouette Transient neurological symptoms (TNS), not treated and/or asymptomatic cardiac overload with treatment Permanent minor neurological symptoms (MNS), mental retardation of up to 20%; nonpermanent neurological symptoms with treatment; normal school with support and/or cardiac failure stabilized with treatment Severe neurological symptoms, mental retardation of more than 20% (SNS); specialized school and/ or cardiac failure unstable despite treatment Death (D)

3 2

1 0 a

Does not apply to neonates.

The technical aspects of VGAM embolization at Bicêtre Hospital are summarized below:
General anesthesia
Femoral puncture 20-gauge Teflon needle. In tiny patients, arterial access may be a significant obstacle, which may require catheterization of the umbilical artery shortly after birth (Berenstein et al. 1997) or the assistance of Doppler ultrasound to localize and cannulate the femoral artery
A 4-F sheath (Terumo), 6 ml contrast/kg pure contrast for runs, diluted at 50% for fluoroscopic control)
A4-F thin wall guiding catheter, if necessary
Pure NBCA + tantalum powder + Lipiodol (for slow-flow shunts)
Intraoperative blood pressure 70 mm systolic or lower if possible at the time of high-flow fistula embolization
One to three angiographic runs in neonates 3 ml/s, for a total of 6 ml (vertebral Towne’s projection or biplane when possible, followed by lateral view of both internal carotid arteries, ICA). If one posterior cerebral artery is not seen on the first run, choose the corresponding ICA side on the second run, and the opposite one for expected cerebral venous information
No additional arterial line
No heparin is used
Alternate femoral puncture side at each session
Usual length of procedure is 45 min, maximum length of procedure, 2h
Recovery room (a few hours)
Pediatric ICU (24 h GA) if the occlusion incomplete or almost complete (secondary thrombosis expected)
No induced low blood pressure, but controlled blood pressure (nicardipine if high blood pressure)
Pediatric neurology ward

Follow-Up

205

3.15.2 Follow-Up

From our experience with the use of bucrylate in CAVM patients, we consider results to be stable at 6 months to 1 year following the final embolization. We have not observed revascularization at later follow-up when angiographic evaluation at 6 months to 1 year was completely normal. When slight hyperemia is demonstrated at 6 months, even without evidence of AV shunting, another follow-up angiogram is taken 1 and 2 years later. Presently, we do not rely on the immediate postembolization angiographic appearance. Magnetic resonance angiography (MRA) is likely to satisfactorily document the stability of a complete occlusion. During follow-up, all children are clinically evaluated by the referring physicians or the pediatric neurologists. Clinical assessment is based on neurocognitive examination. After treatment is completed, children are followed up with a clinical examination every year and MRI every 2 years (Fig. 3.64). This management has created a population of children that did not exist 20 years ago. This ongoing clinical follow-up is therefore mandatory; in the pediatric population, therapeutic success can only be truly evaluated when brain maturation is complete and functionally evaluated over time. Our series of 317 VGAM patients (Table 3.6) include the cases referred and those for whom embolization was not indicated to overcome the clinical situation or predictable outcome (Tables 3.7, 3.8) Total exclusion of a VGAM is a clear and simple observation, as demonstrated by a repeated negative angiogram (Fig. 3.64). Total or nearly total obliteration of the lesion is already obtained in 55% of the children who were embolized and alive (Tables 3.9, 3.10), which means that a significant number of children do not have an eradicated VGAM. In 97% of the patients in whom the treatment of the lesion was considered complete, total exclusion of the shunt was obtained and confirmed. In only 3% was the exclusion incomplete, but the persisting remaining shunt is less of a risk in comparison to the technical difficulty in completely obliterating it. In many instances, complete disappearance is not achieved at the end of embolization, and some slow flow inside the lesion can still be demonstrated (Fig. 3.65). We have never seen any rupture of the VGAM under these circumstances. Among the children partially treated, with the exception of the complications described below, none developed any permanent neurological symptoms that they did not have before, e.g., seizure, deficit, and hemorrhage. As will be seen with CAVFs and CAVms, staging and progressive exclusions of the active portions of the lesion make it possible to follow over time incompletely embolized lesions until complete exclusion is deemed feasible and necessary; the presence of subependymal supply is not a contraindication to embolization as soon as they have shown no regression following the highest flow shunts (Figs. 3.66, 3.67). Among the goals to reach is the presence of a faint subependymal reflux in an incompletely excluded lesion. Spontaneous thrombosis of the pouch could lead to hemorrhagic risk in the thalamic region (similar to what is observed following transvenous approach and packing of the venous ectasia distal to these anastomoses) (Fig. 3.68). Partial targeted sessions or deposition should be directed to the control of this reflux (Fig. 3.69).

206

3 Vein of Galen Aneurysmal Malformation

Fig. 3.64A–C. Legend see p. 207

Follow-Up

207

Fig. 3.64A–F. Male neonate presenting with cardiac failure and rapidly progressing macrocrania initially related to a small VGAM. A Following ventricular shunting, the size of the lesion dramatically increased. The child came to us at 10 months of age and mild mental retardation was noted. Tonsillar prolapse was also noted. B–D In two sessions of embolization, 1 week apart, complete occlusion of the shunt was achieved. One year later, complete occlusion was confirmed. E The supply from the basilar tip branches and, in particular, the choroidal and subependymal arteries regressed spontaneously. F At 8 years of follow-up, the child had a score of 5

Table 3.6. VGAM: patients (1981–2002)

Fetus Neonates (<1 month) Infants (>1 month <2 years) Children (2–16 years) Total

Age at diagnosis

Age at first consultation

93 (29.3%) 119 (37.5%) 82 (25.9%) 23 (7.3%) 317

18 (5.7%) 122 (38.5%) 125 (39.4%) 52 (16.4%) 317

Table 3.7. VGAM therapeutic decision and proposed treatment

Neonates Infants Children Total Total (%) a

Embolization

Abstention

Lost to follow-up

Total

88 (5)a 103 (8) 42 (4) 233 (17) 73.5%

45 16 6 67 21.1%

7 6 4 17 5.4%

140 125 52 317

Numbers in parentheses denote embolization done elsewhere.

208

3 Vein of Galen Aneurysmal Malformation

Table 3.8. Reasons for therapeutic abstention Neonates

Infants

Therapeutic abstention Encephalomalacia NN score <8a Therapeutic interruption of pregnancy a

45 25 (56%) 17 (38%) 3 (6%)

Children

Therapeutic abstention Encephalomalacia Technical failure Spontaneous occlusion

16 9 (56%) 1 (6%) 6 (38%)

Therapeutic abstention Bicêtre Admission Score 1 Surgery Spontaneous occlusion

Score 8: four patients; score 7: six patients; score 6: three patients; score 5: four patients.

Table 3.9. VGAM therapeutic results 1981–2002: patients referred for management

Neonates Infants Children Total a

Total

Death

Alive

23 153 40 216

12 11 – 23

11 142 40 193a

Seven patients with angiography without embolization and five patients with angiography and spontaneous occlusion.

Table 3.10. VGAM therapeutic results 1981–2002: morphological results (surviving children)a 100% 95% 90% ±50% <50% Total a

82 8 16 75 12 193

55% of patients have a 90%–100% occlusion; 38.5% of patients have a 50%–90% occlusion; 6.2% of patients have a <50% occlusion.

6 3 (50%) 1 (17%) 2 (33%)

Follow-Up

209

Fig. 3.65A–E. A Male infant presented with macrocrania at the end of neonatal age. He was referred for consultation at 10 months. He had a score of 4 at that time. B, C The lesion was embolized in two sessions.An immediate response of the head circumference was observed; however, a minimal shunt was still seen on the wall of the VGAM. C Note the presence of nonocclusive glue inside the sigmoid sinus. D, E Finally, 2 years after the last embolization, the shunt finally disappeared, both sigmoid sinuses opened in patent jugular bulbs. E see p. 210

210

3 Vein of Galen Aneurysmal Malformation

Fig. 3.65E. Legend see p. 209

3.15.3 Complications: Morbidity

There are non-neurological complications related to the embolization procedure and the technical difficulty of injecting pure NBCA glue in 6.7% of cases. On three occasions, a drop of glue caused an asymptomatic partial occlusion of the internal iliac artery during removal of the catheter. In all patients, follow-up showed progressive reconstitution of the vessel lumen; in one additional patient, the catheter became glued in place, resulting in a homonymous hemianopsia from which he recovered at 3 years of follow-up. In this situation, the catheter should be cut as short as possible at the femoral entrance and be pushed forward to float in the aorta. The catheter rapidly became extraluminal and incorporated in the vessel wall (Fig. 3.70). It has not led to any thrombotic or embolic manifestations in our experience, nor has it required preventive anticoagulation treatment. In an additional patient, a drop of glue remained at the tip of the catheter and could not be passed through the sheath (Fig. 3.71). Despite the small size of the drop, it occluded the distal aorta of a 4.6-kg baby girl. The microcatheter tip and its attached glue were pushed into a standby position in the suprarenal aorta. Immediate surgery by transperitoneal approach to the aortic bifurcation was performed. After gentle pulling on the catheter to bring the tip and the glue droplet under direct visual control, a small aortotomy was done; the microcatheter was cut and its tip removed directly (Fig. 3.72). After completion of the direct surgery, the sheath was removed and the postoperative course was uneventful. The aorta and the femoral artery demonstrated no detectable anomaly at angiographic follow-up performed during a

Complications: Morbidity

211

Fig. 3.66A–C. Subependymal arterial supply and venous anastomoses (A) rapidly remodeling after a single subependymal arterial glue deposit (B, C)

212

3 Vein of Galen Aneurysmal Malformation

Fig. 3.67A–F. Presence of a rich perimesencephalic network (A–C) that did not compromise a satisfactory glue embolization, leading to complete exclusion of the lesion (D–F)

Complications: Morbidity

Fig. 3.68A–G. Legend see pp. 215

213

214

3 Vein of Galen Aneurysmal Malformation

Fig. 3.68H–K. Legend see p. 215

Complications: Morbidity

215

Fig. 3.68A–N. A 4-month-old child presenting with a well-tolerated VGAM (A–C) was partially embolized in two sessions over 2 years with nearly complete exclusion but closure of the falcine sinus and faint subependymal reflux (D–G). Nearly 2 years later, he presented a sudden intrathalamocapsular and ventricular hemorrhage. H–K The angiogram demonstrated an angiogenic colonization of the thrombosed venous pouch generating an increased flow into the subependymal vein anastomoses and their remote rupture away from the VGAM. L–N Further embolization aimed to reduce the angiogenic field further

216

3 Vein of Galen Aneurysmal Malformation

Fig. 3.69.A, B. A 7-month-old infant with a well-tolerated VGAM and an early subependymal venous reflux. The objective of the preventive treatment was first to make the reflux disappear. Follow-up angiogram 3 months after the first session of embolization (C)

Complications: Morbidity

217

Fig. 3.70.A, B. Catheter glued in place and hanging in the aorta. C, D Follow-up angiogram during an additional session 10 years later. The catheter is now extravascular and the vertebral artery is patent, allowing for a further microcatheter approach

Fig. 3.71A, B. Droplet of glue remaining at the tip of the catheter when pulled detached in the internal iliac artery to preserve the lower limb arterial patency

218

3 Vein of Galen Aneurysmal Malformation

Fig. 3.72. Extremity of a Sensé microcatheter with a drop of glue that was too big to be withdrawn through the 4F sheath by the femoral approach. This 4,600-g baby had to be operated on. The catheter tip was cut and removed from the abdominal aorta following direct aortotomy. Clinical and morphological follow-up 7 years later showed excellent results. Scale is in centimeters

new session of embolization of the VGAM. This is to emphasize the need for a proper pediatric environment when endovascular specialists perform these procedures on babies in an adult hospital (Table 3.11). We have experienced no limb vascular complications as a result of repeated arterial punctures in VGAM patients except in the following case. In a 3-kg neonate with severe CCF with aortic diastolic steal and poor peripheral circulation in which the diagnosis of VGAM was uncertain, we encountered a persistent femoral artery spasm while pulling the 4-F sheath. As we had decided against treatment, the baby died of systemic failure 2 days later with an associated severe distal ischemia in his lower limb. We have had few venous passages of fragmented glue cast (less than 3%) into the sinuses or further distally; the use of low blood pressure during glue injection helps in keeping these figures low. However, in case of bilateral jugular bulb occlusion, a converging and restricted venous drainage of the VGAM and the brain, any glue passage into the venous outlet will produce an immediate postembolization hemorrhagic venous infarction (Fig. 3.73). If the glue remains in the sinuses, further occlusion of the shunt must be obtained to avoid the effect of rerouting of the VGAM flow into the pial venous system. Remodeling over time usually shows satisfactory recruitment of collateral venous channels. Heparin in these cases will be needed to preserve the remaining lumen if iatrogenic occlusion is incomplete to allow for that remodeling to take place. In this same group of treated patients, 2% developed permanent neurological disability. Children treated by the transvenous route after failure to achieve further embolization by the transarterial approach are at risk of intracerebral hemorrhage within a few hours after embolization. This occurs when the

Complications: Morbidity

219

Table 3.11. VGAM Therapeutic results 1981–2002a: complications in the patients receiving embolization (193 surviving children) Transient neurological complications Permanent neurological complications Non-neurological complications Hemorrhage after embolization a

Fig. 3.73. A A 6-month-old boy in whom macrocrania revealed a VGAM. Progressive occlusion in the jugular bulb produced a significant congestion on the cerebral veins. The superior petrosal sinus on the left side drained the malformation into the ophthalmic vein. Prior to admission, the child presented with a generalized seizure that required antiepileptic medication. He had proptosis on the left side and facial collateral circulation, but had a score of 4. He was embolized three times with significant improvement in the facial circulation. B, C Following erratic venous embolic material during the final session, a large lethal venous infarct in the left hemisphere resulted from the occlusion of the ipsilateral cavernous sinus, and immediate extension to all its converging venous afferents

3 4 13 11

1.55% 2% 6.7% 5.7%

Death: 23/216 patients (10.6%); angiography no embolization = 4 (one technical failure, three angiograms only); after embolization = 14 (death related to embolization); between sessions = 4; after embolization and surgery = 1.

220

3 Vein of Galen Aneurysmal Malformation

occlusion of the venous outlet to the pouch is complete and the remaining flow into the VGAM insufficiently reduced toward subependymal anastomoses. Hemorrhages have been reported in the literature but they refer to unrecognized VGAD treated with the transvenous approach. A total of 5.7% of hemorrhages (including the ones mentioned in Sect. 3.12) have been noted mostly caused by arterial perforation in the vicinity of the shunt with small arterial feeders and using a microguidewire. Immediate gluing of that feeder led mostly to minor and transient manifestations. We have never seen the so-called perfusion break-through phenomenon in the many acute closures of high-flow fistulas that we have performed (see Chap. 4, this volume), nor have we seen a VGAM increase in size following thrombosis, as our experience has shown that shrinkage of the mass occurs rapidly after significant transarterial embolization. Furthermore, we have not observed in any patients a consumption of coagulation factors type of syndrome induced by thrombosis in the large venous pouches. In one patient, a giant VGAM progressively thrombosed after embolization, and the infant awoke a few days after sedation was discontinued. All clinical and EEG parameters corresponded to those of a sleeping child, and it was demonstrated that the pouch behaved like a reservoir and was still releasing drugs. The child woke up 5 days after embolization with his VGAM completely excluded and had a score of 5 at the age of 13.

3.15.4 Overall Mortality

In our series, and after applying our selection criteria, treatment was withheld in 18% of children. The mortality rate in our group of embolized children was 10.6% (23/216 patients). Many of these were early cases which today would be scored below 8 and would thus be included into the nontreatment group. They belong to the „death despite treatment group“ at the beginning of our experience or to the newly recognized group of irreversible suprasystemic pulmonary hypertension resistant to NO. The proportion of patients with a rapidly fatal form still remains lower than the quoted mortality rate in comparable series with different selection criteria or different therapeutic techniques (Casasco et al. 1991; Ciricillo et al. 1990; Dowd et al. 1990; Merland et al. 1987; Mickle and Peters 1993; Hoffman et al. 1982; Johnston et al. 1987; Raimondi 1987; Yasargil et al. 1976). In most cases where fatal outcome occurred even though the individual procedures were successful, the timing and sequence of the interventions resulted in the accumulation of secondary effects eventually causing death. Sudden death occurred in one infant, probably due to transtentorial herniation, following ventricular shunting in the presence of bilateral subdural effusions. Complete embolization of a large VGAM was performed 3 days later. The baby was not kept asleep and was sent back to the ward, where he remained clinically intact till he collapsed 24 days after embolization. The overall management (decision not to treat and treatment-related) of VGAM in our series carried a 23.7% mortality rate.

Surgery

221

Table 3.12. Therapeutic results in the VGAM patients receiving embolization 1981–2002

Neurologically normal, BOS 3, 4, 5 Moderate mental retardation (BOS 2) Severe mental retardation (BOS 1) Death despite or because of embolization

Neonates

Infants

36.4% 54.5% 9.1% 52%

78.9% 11.3% 9.8% 7.2%

(4/11) (6/11) (1/11) (12/23)

Children (112/142) (16/142) (14/142) (11/153)

67.5% 20% 12.5% 0%

(27/40) (8/40) (5/40) (0/40)

Total 74% (143/193) 15.6% (30/193) 10.4% (20/193) 10.6% (23/216)

3.15.5 Neurological Outcome by Age Group

With regard to the age at diagnosis, we identified four groups of children: fetuses, neonates, infants (up to the age of 2 years), and children. These groups are used as a point of reference and are matched with the date of first referral and the date of first embolization. These different dates are important, since they outline the delay between diagnosis and endovascular possibilities, the role of decisions made prior to the intervention itself and the neurological outcome resulting from this management. The neurological outcome in the surviving group shows 74% neurologically normal children (Table 3.12). Among the 20 out of 193 (10.8%) children with a severe neurological or cognitive handicap, some were already in an irreversible state when referred to us but for others we failed to anticipate a poor outcome.

3.16 Other Techniques 3.16.1 Surgery

The framework of the anatomic and clinical features of this disorder explains the improvement in the overall outcome. Even if the duration of follow-up was not long enough, it is important to try to assess which of the many techniques or decisions made has resulted in real progress. Up to 1997, we found 354 cases of VGAM in the literature, which proved to be difficult to compare since most of them emphasized the technical challenges or the grave prognostic outcome of the lesion (Table 3.13). The majority of surgical treatments reported are only partial, with ligature often far from the point of the fistula, while others were excisions of already thrombosed lesions (Beltramello 1991; Lazar 1974). Above all, ventricular shunting must be viewed with suspicion; while it alleviates acute hydrocephalus, it carries a high morbidity rate and may worsen the neurological outcome. Taking Johnson’s review of 1987 as a reference (Table 3.14), the results of surgery in VGAM management are very poor, with 38%–91% mortality in the overall group and 33%–77% mortality in the operated group. Normal children represented only 4%–32% of the overall group, depending on the age group. These results are certainly quite different from the results published in over 120 cases managed by transarterial embolization, with a 26% overall mortality and 78% of the children having a normal neurological status on follow-up (Mickle and Quisling 1986; Mickle and Peters 1993).

? National review 1979–1986

?

1977–1988

1950–1990

15 years 28 months

7 years

1 month

3 years

12 years

18 years

20 years

Merland et al. 1987

Ciricillo et al. 1990

Casasco et al. 1991

Mickle 1991 (transtorcular embolization) Wisoff et al. 1990 (Berenstein) Total

1988–1990

1978–1989

1950–1985

1975–1985

Study period

20 years

10 months

Upper age limit

Johnston et al. 1987 (includes Hoffman’s series) Yasargil 1988 Maheut et al. 1987

Johnston et al. 1987 (personal series)

Authors

357

33

26

7

14

6

14 53

191

218

33

24

7

13

6

14 26

89

6

(N)

(N) 13

VGAM treated

Patients

70

17

5

5

1

–

9 3

27

3

32

52

21

71

8

–

64 12

30

50

43

5

13

0

0

–

– 5

19

2

20

15

54

0

0

–

– 19

21

33

Patients treated by direct approach Neurologically Neurologically normal abnormal (N) (%) (N) (%)

84

6

6

0

7

3

5 18

38

1

(N)

38

18

25

0

54

50

36 69

43

17

(%)

Operative mortality

Table 3.13. Review of the literature on treatment of vein of Galen aneurysmal malformations (Lasjaunias et al. 1996a)

Another patient died 2 years after embolization with balloons and particles The normal patient with total exclusion embolization with particles; no follow-up angiography Surgery alone, embolization alone or combined; no follow-up angiography Two infants had ventriculoperitoneal shunts inserted; one survived with a mild deficit, the other died suddenly Includes surgery and embolization; five late deaths not included Eighteen treated patients suffered late death or were not accounted for; impossible to assess the amount of stable complete exclusion

One patient died 3 months after total obliteration, not considered as operative death. Two patients had embolization intraoperatively Result unknown in five cases

Remarks

222 3 Vein of Galen Aneurysmal Malformation

Transvenous Treatment

223

Table 3.14. Neurosurgical management of vein of Galen aneurysmal malformations in the period 1950–1985 (Johnston et al. 1987) Treatment

Patients

Death

(n)

(%)

(n)

74

Neonatesa No treatment or medical 52 treatment only Surgery (palliative or direct) 18 Total 70 Infants (1–12 months)b No treatment or medical 17 treatment only Surgery (palliative or direct) 52 Total 69 Children (1–5 years)c No treatment or medical 7 treatment only Surgery (palliative or direct) 27 Total 34 a b c

No deficit

(%)

Lost to follow-up (n) (%)

50

96

1

2

1

2

26 100

14 64

77 91

0 1

0 1

2 3

11 4

25

10

59

–

–

5

30

75 100

20 30

38 43

1 1

2 1

15 20

29 29

21

4

57

1

14

1

14

79 100

9 13

33 38

2 3

7 9

10 11

37 32

(n) (%)

Two neonates had a deficit. Eighteen infants had a deficit. Seven children had a deficit.

3.16.2 Transvenous Treatment

Transvenous treatment of a VGAM can be achieved by percutaneous transfemoral or transtorcular access, the latter via surgical exposure of the torcular or ultrasound-guided percutaneous penetration of the overlying dura with a needle (Lylyk et al. 1993; Mitchell et al. 2001) A reduction in arteriovenous shunting is achieved by packing the venous pouch with a variety of materials including coils (Borthne 1997; Lylyk et al. 1993), nylon (Borthne 1997), and balloons (Lylyk et al. 1993), often requiring several sessions to achieve a satisfactory response (Mickle 1991). The extent of embolization can be monitored during the procedure by injection of contrast transarterially or directly into the pouch, or alternatively by measurement of intra-aneurysmal pressure (Casasco et al. 1991). One can also consider use of the venous route to perform dural sinus angioplasty and stenting to target progressive sigmoid/jugular occlusion and severe intracranial venous hypertension in cases where other endovascular solutions are not achievable (Brew et al. 2001). The longterm durability of dural sinus stenting is unknown at this point. While the venous approach may be appealing because of its lesser technical challenge compared to transarterial treatment, the reported experience is shorter, long-term neurological outcome is less clear, and there are several potential unique problems associated with it. The diagnosis of VGAM must be unequivocal prior to embarking on transvenous packing, since the treatment is contraindicated in VGAD patients due to the disastrous consequences of occluding the venous outlet without ad-

224

3 Vein of Galen Aneurysmal Malformation

dressing the associated pial AVM (Lasjaunias 1987b; terBrugge 2001). Even with true VGAMs, sudden closure of the venous end (sometimes without precise control of placement of the embolic material) may put the patient at risk of venous infarction or hemorrhage. Perforation of the venous pouch with the guiding catheter has lead to fatal intracranial hemorrhage in a number of cases (Lylyk et al. 1997). Lastly, severe consumptive coagulopathy has been reported following transvenous treatment (Rosenberg and Nazar 1991; Charafeddine et al. 1999). A number of centers utilize a combination of transarterial and transvenous therapy, tailoring the technique according to the local confidence in use of each approach, the angioarchitecture of the lesion, and the response to prior attempts at treatment.

3.16.3 Radiosurgery

In our series, four children had radiotherapy (Al Watban et al. 1995), three before they had been referred to us. In all three patients, a linear accelerator had been used with no effect on the lesion; these three patients were subsequently cured by embolization. The other patient completed treatment with a combination of Knife radiotherapy following embolization of 80% of the lesion (Figs. 3.45, 3.60).

Case 1. A baby girl born at term by vaginal delivery had a head circumference at birth of 39 cm. No systemic manifestations were detected. At 3 months of age, the parents noted the appearance of a facial venous network that increased slightly with age. At 7 months, the head circumference was 49 cm (more than +2 SD). A CT scan was performed and detected a VGAM associated with a dilatation of the lateral ventricles.A cerebral angiogram confirmed this diagnosis, and when the infant was 8 months old, she underwent stereotactic radiosurgery (25 Gy). The follow-up examinations, performed up to the 33rd month of age, revealed no change in the lesion itself. Even though the neurocognitive status of the child was considered normal, her facial veins had not regressed and her head circumference had continued to increase (58 cm; + 4 SD). The child was then referred to our team for endovascular treatment of the lesion. Angiography performed at that time revealed a mural form of VGAM with four shunting zones and venous outlets characterized by a thrombosis of the right sigmoid sinus. Despite this constraint on the cortical veins, the brain drained satisfactorily anteriorly through the cavernous sinus into the superior ophthalmic veins, explaining the lack of clinical symptoms and the dilatation of the facial veins. Four arterial pedicles were embolized with glue in two therapeutic sessions over a 4month period, leading to complete exclusion of the malformation. Neurocognitive examinations (Denver and Brunet-Leizine test) confirmed that the child was normal, and the head circumference showed no further increase.

Radiosurgery

225

Case 2. This baby girl was born 5 days after term with a birth weight of about 3 kg. At 3 months of age, she was suspected of having macrocephaly, and prominent facial veins were noted. A CT scan performed at that age revealed VGAM and ventricular dilatation, for which a ventriculoperitoneal shunt was placed when the child was 4 months old. The baby underwent angiography when she was 10 months old in order to confirm the diagnosis of VGAM prior to radiosurgery, which was performed at that time (25 Gy, 50% isodose, single 8-mm collimator). Regular follow-ups were obtained, including physical examinations and CT scans. The clinical report mentioned a „general and locomotor delay“ that was suspected at 18 months of age; radiological examination showed no change in the size of the ventricles and the VGAM. Two years after radiosurgery, follow-up angiography was performed and confirmed a persistent and unchanged AV malformation. The child was referred to our group when she was 3.5 years old. On admission, her head circumference was within normal limits (49 cm), and the child was normal from a neurocognitive point of view. Total cure of her malformation was obtained in two sessions of embolizations 6 months apart (five pedicles occluded). Follow-up neurological examinations have remained normal (Fig. 3.45).

Case 3. A baby girl (normal pregnancy and vaginal delivery) presented at birth with a head circumference at the upper limit of the normal (38 cm). Macrocrania developed and prominent facial veins were detected at 3 months of age. There was no heart failure. A CT scan indicated a VGAM, which was confirmed by cerebral angiography. In order to treat this malformation, the 9-month-old girl underwent radiosurgery (20 Gy to the 50% isodose curve, 14-mm collimator). About 6 months after treatment, the patient had a further CT because of episodes of head banging and screaming. Multiple subcortical and basal ganglia calcifications were noted at this time, with the development of a cerebral atrophy.At 19 months of age, her head circumference was 52.7 cm (1.7 cm above the 98th percentile), and she was considered neurologically normal except for a mild motor delay. At 22 months, her head circumference was 53.2 cm, and she „tended towards tip-toe walking.“ The prominent facial veins were still present, as was the cranial bruit. Follow-up angiography performed 23 months after radiosurgery revealed „some reduction in the size of the VGAM, thrombosis of one previously feeding pedicle and a thrombosis of both sigmoido-jugular pathways“. A reflux in supratentorial and posterior fossa veins was noted at that time. The child was then considered for endovascular treatment and sent to our unit. On admission, she was considered slightly retarded (2.5 years neurological age, 3 years of chronological age). Transarterial embolization was performed with glue through the posteromedial choroidal artery, and total occlusion of the VGAM was obtained in one therapeutic session. The child’s neurological status, although showing some improvement, remained abnormal and delayed at fine motor control. The head circumference has stabilized.

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3 Vein of Galen Aneurysmal Malformation

In the search for minimally invasive techniques to cure difficult or unreachable vascular malformations of the brain, radiosurgery has become a reliable therapeutic alternative, even in the pediatric population (Steinberg et al. 1990; Steiner et al. 1989; Altschuler et al. 1989; Colombo et al. 1989; Fabrikant et al. 1989; Loeffler et al. 1990). The main problem in applying this technique in VGAM is the vulnerability of the brain in children and the time needed for progressive endarteritis to completely occlude the malformative shunt. During this delay, the hemodynamic and hydrodynamic effects, either on the supratentorial (Zerah et al. 1992) or infratentorial (Girard et al. 1994) spaces created by the VGAM with the concurrent maturing and developing brain, can induce irreversible damage and neurocognitive delay. This retardation is one of the most challenging problems and is often overlooked and rarely reported in the literature. It was present in nearly all the infants referred to us, even though they were considered neurologically normal. To avoid irreversible delay, we believe that one should not wait 2 years in any of these cases to obtain occlusion of the shunt. Although theoretically effective, we believe that there is no indication for radiosurgery as the first modality in treatment in VGAM. In a combined approach, radiosurgery is a powerful tool that can be used as soon as most of the lesion has been controlled in terms of size and analyzed in terms of future neurological risks. The time allotted for treatment depends on the hydrovenous status. As a general policy, we do not recommend radiosurgery in children unless a complete morphological result has to be obtained and if other techniques cannot be used. Indications are thus rare and are discussed on an individual basis, and in our experience as late as possible in the child’s development.

4 Cerebral Arteriovenous Fistulas

4.1

Definitions and Anatomic Spaces 227

4.2 4.2.1 4.2.2

Angioarchitecture 228 Single CAVFs 228 Multiple CAVFs 231

4.3 4.3.1 4.3.2

Associated Conditions 236 Hereditary Hemorrhagic Telangiectasia 236 Encephalocraniocutaneous Lipomatosis 246

4.4 4.4.1

Presentation 249 Natural History 265

4.5

Management 270

4.1 Definitions and Anatomic Spaces Cerebral arteriovenous fistula (CAVF) is the name we have assigned to direct communication between a pial artery and a cerebral vein, without an intervening nidus and located in the subpial meningeal space. This newly distinguished subtype of intradural AVS is necessary because it corresponds to an architecture that engenders specific symptoms, occurs in a special age group, constitutes the phenotype of a well-defined disease, and requires a specific therapeutic technical approach. The location of the arteriovenous fistula (AVF) in the subpial meningeal space separates it from the two other main groups of shunts: the subarachnoid (vein of Galen) and the dural fistulas. Brain AVMs, pial AVMs, cerebral AVMs or non-Galenic cerebral arteriovenous malformations (CAVMs) all refer to the same entity, i.e., arteriovenous communications in the subpial compartment of the central nervous tissue. We distinguish these single-hole communications from the nidus type of angioarchitecture present in CAVMs. CAVFs have a presentation and a natural history that is different from CAVMs and will therefore require different management strategies. The subpial meningeal space is common to all regions of the central nervous system (CNS) and links spinal cord AVFs (SCAVFs) with CAVFs as part of the subpial fistulas group, at least for those that are ventrally located. As the AV shunt is located in the subpial space, its drainage pattern may have an impact on the venous drainage of the regional brain parenchyma, which will then have a secondary hemodynamic impact on the fistula. The longer the subpial segment of the draining vein to the lesion, the higher its chances of interfering with regional circulation of the brain parenchyma,

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until it joins a significant outlet that takes it across the subarachnoid space to the dural sinuses and away from the regional brain vasculature. Along the length of its subpial segment, the venous channel draining the fistula receives drainage from normal venules participating both in blood drainage and CSF homeostasis of normal brain, which are at a lower pressure and therefore unable to function properly, with a high chance of inducing regional ischemia, which will result in atrophic changes and progressive melting-brain syndrome. Conversely, if the drainage of a lesion is at or near the subarachnoid level, and the subarachnoid transit distance is short, as it tends to be in most CAVFs, the subpial venous congestion will be reduced, and the chances for regional atrophic changes and meltingbrain syndrome are therefore reduced. Premedullary posterior fossa AVFs that arise from the distal vertebral arteries or the basilar trunk also tend to fall into this category and have surprisingly few neurological symptoms. Some high-flow lesions encountered in infants may lead to macrocrania without cortical atrophy (as long as the dural sinuses are patent). This occurs when the increased venous pressure resulting from the AV shunt is exerted at the dural sinus level, compromising its function to absorb CSF. In the absence of active resistance or occlusion at the venodural junction where the draining vein opens, the brain remains protected. Regardless of the AVF size, jugular vein occlusion in an initially subarachnoid draining lesion will create not only a severe intradural water disorder, but also rapid venous ischemia, infarction, and hemorrhage in any area of the brain. The associated neurological symptoms at that time will have no relationship with the topography of the AV shunt itself, since they are often remote from its location, potentially bilateral, and multifocal. It is likely that the cerebral venous drainage in the lateral sinuses, the cavernous sinus capture of the sylvian cortical veins, and the comparatively lower pressures in the sinuses offer enough venous pathways for the intrinsic water to exit. Failure of the hydrodynamic equilibrium then becomes unlikely. In comparison with VGAM, ischemic episodes occur after head enlargement, before the development of hydrocephalus. Venous congestion and reflux decreases tissue perfusion faster than the changes in cerebral blood flow through a moderate increase in intracranial pressure that accompanies macrocrania. Considering all the possible negative effects of high-flow lesions on the growing and maturing brain, it is difficult to believe that all lesions encountered in adults were present at birth (see Chap. 2, this volume).

4.2 Angioarchitecture 4.2.1 Single CAVFs

CAVFs are direct communications between the arterial and venous system with an abrupt transition from the arterial feeder(s) to the draining vein and an absence of the plexiform nidus as seen in the classic cerebral AVMs. While the arterial feeders, which participate in this direct communication, may be single (Fig. 4.1) or multiple (Fig. 4.2), they will all converge on a single venous channel. The AVFs are always superficial and cortical

Single CAVFs

229

Fig. 4.1A, B. Anterior-posterior (AP) views of vertebral angiogram (A) and selective superior cerebellar angiogram (B) in a 4-month-old girl demonstrate arteriovenous fistula (AVF) supplied by single artery and draining into single vein with abrupt lumen enlargement at the site of the fistula (arrow)

in location and can be supra- or infratentorial. CAVFs make up a significant proportion of the total number of CAVMs, in particular in the pediatric age group. Among 303 pediatric CAVM patients, there were 52 patients (17%) with CAVFs in the Bicêtre Hospital series (Weon et al. 2005; Yoshida et al. 2004). They can arise from any artery of the brain, and while generalized, arterial enlargement of the feeding artery or arteries is common in highflow lesions, we have thus far never seen the development of focal arterial ectasia (aneurysm) in neonates, infants, or young children with CAVFs. This differs from the adult situation where upstream aneurysms are not uncommon, indicating that the progression toward the presence of arterial focal ectasia apparently requires significant time (see Vol. 2, Chap. 1). Arterial or venous pseudo-aneurysms do occur and denote the location of a previous hemorrhage similar to that seen in CAVMs in adults (see Chap. 5, this volume). The transition from artery to vein in CAVFs is recognizable by an abrupt increase in caliber of the AV channel. Further downstream, dramatic caliber changes are often seen on the venous side of the fistula (Figs. 4.1, 4.2). The absence of arterial aneurysms and the presence of marked venous ectasias are characteristic for CAVFs in the pediatric age group. Pediatric AVFs were associated with large or giant venous pouches in up to 88% of cases in the Bicêtre series of 41 patients with 43 supratentorial AVFs and stenosis of the vein draining the AVF was present in 42% (Weon et al. 2005). Venous pouches are very frequent in children, since thrombosis and high flow are often present. They are characteristic of AVFs seen in HHT children. These pouches behave like any large pulsatile mass and may have neurological manifestations, although the ability of the infant’s head

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Fig. 4.2A–D. Legend see p. 231

▲

Multiple CAVFs

231

Fig. 4.2A–F. A 9-month-old boy presented with increasing head circumference and mild developmental delay. MRI in coronal (A) and sagittal (B) views demonstrates large area of flow void along medial aspect of left temporal occipital lobe. Vertebral angiogram at 12 months of age in AP (C, D) and lateral (E, F) views demonstrates AVF fed by several branches of the left posterior cerebral artery all converging in to a single draining vein, which was dramatically enlarged, causing mass effect

to enlarge often allows giant pouches to be diagnosed with almost no mass-related symptoms (Fig. 4.2). These huge pouches are therefore rarely directly responsible for symptoms in children as the adjacent brain is apparently capable of adapting to them. Neurological deficits and seizure activity may occur in relationship to these pouches in some patients, and in our experience, this is nearly always associated with a spontaneous partial thrombosis of the pouch. MRI at this point demonstrates an area of increased signal in the brain surrounding the pouch (Berenstein 1992a; Lee and terBrugge 2003). It is of interest to note that the thrombosis of similar pouches induced by embolization does not produce the same perilesional changes, nor does it produce deficit or seizures, as it also closes or reduces the flow through the AVF. These pouches can increase in size over time subsequent to the development of restriction of the downstream outlets.

4.2.2 Multiple CAVFs

AVFs can be single or multifocal if each fistulous communication harbors a distinctly separate vein draining each fistulous point (Fig. 4.3). Multiplicity is a common feature of CAVFs in the pediatric age group and should raise the suspicion of associated or systemic conditions (see Sect. 4.3.1) (Fig. 4.4).

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Fig. 4.3A–D. Legend see p. 233

▲

Multiple CAVFs

233

Fig. 4.3A–H. A 23-month-old boy initially presented with a generalized seizure at the age of 1 year and subsequently developed headaches and left-sided weakness. T2 W MRI axial views (A, B) demonstrated multiple tortuous signal voids along the lateral aspect of the right temporal lobe, which was atrophic and showed increased signal of white matter. Angiography of right internal carotid artery on lateral views (C, D) and left vertebral artery in AP (E) and lateral (F) views demonstrated seven arteriovenous fistulas, each draining into separate dilated veins. G, H At 15 months of follow-up, the morphological result was satisfactory but the child was severely handicapped

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Fig. 4.4A, B. CAVF in a young adult. Note the flow-related aneurysm at the basilar tip

Table 4.1. Incidence of CAVFs in children in comparison to overall intradural AVM cases from Weon et al. 2005 and Yoshida et al. 2004): 52 CAVF children for 80 AVFs

Total AV shunts referred (all ages) Total AV shunts in children (<16) Non-Galenic AVSs in children Posterior fossa AVMs in children Posterior fossa AVFs/posterior fossa AVMs in children Posterior fossa AVFs/AVFs in children Supratentorial AVMs in children Supratentorial AVFs/supratentorial AVMs in children Supratentorial AVFs/AVFs in children Posterior fossa + supratentorial AVFs/AVFs in children

Number

%

52/1565 52/620 52/303 47/303 11/47 11/52 256/303 38/256 38/52 3/52

0.33% 0.84% 17.2% 15.5% 23.4% 21.1% 84.5% 14.8% 73.1% 0.06%

CAVF, cerebral arteriovenous fistula; AVS, arteriovenous shunt; AVM, arteriovenous malformation.

Series and case reports of multifocal lesions and unusual associations have been published (Reddy 1987; Rodesch et al. 1988; Schlater 1980; Smith et al. 1981; Willinsky et al. 1990a; Tamaki et al. 1971; Tada et al. 1986; Zellem and Buchheit 1985; Hoffman et al. 1976). Among 52 pediatric patients with AVFs, 23 (45%) had multiple AVFs ranging from one to seven per patient; three patients had both supra- and infratentorial locations of the AVFs and one patient also had a spinal cord location in Yoshida’s series (Yoshida et al. 2004; Weon et al. 2005). The number of multifocal lesions in children, in our experience, is twice that of adults (17.2% vs 9%). Any variation of AV shunt can occur in the same patient, but we often find the same type of architecture in all sites in the same individual, i.e., multiple fistulas or multiple niduses. Tables 4.1–4.3 summarize the characteristics of pediatric CAVFs in Weon and Yoshida’s experiments.

Multiple CAVFs

235

Table 4.2a. Angioarchitectural features (supratentorial CAVFs) (Weon et al. 2005) Angioarchitecture

No. of cases (%)

Venous ectasia Pial venous stenosis or thrombosis Dural sinus stenosis or thrombosis Pial venous reflux Angiogenesis Transdural supply Arterial stenosis False venous aneurysm Flow-related arterial aneurysm

36 (87.8%) 17 (41.5%) 9 (21.9%) 5 (12.2%) 5 (12.2%) 5 (12.2%) 3 (7.3%) 2 (4.9%) 2 (4.9%)

Table 4.2b. Angiographic features (infratentorial CAVFs) (Yoshida et al. 2004) Angioarchitecture

No. of cases (%)

Venous ectasia Pial venous congestion Dural sinus thrombosis Pial venous stenosis Dural sinus stenosis False venous aneurysms Arterial stenosis Angiogenesis Arterial aneurysms Transdural supply Transependymal supply Pial venous thrombosis Multiple fistulae

13 6a 6a 4 3 2 1 1 0 0 0 0 5

a

(93%) (46%) (46%) (31%) (23%) (15%) ( 8%) ( 8%)

(38%)

Two presented with hemorrhage.

Table 4.3. Topography of the supratentorial AVFsa (Weon et al. 2005)

Single (24/24 cases) Multiple (39/17 cases) Total (63b, c/41 cases) a b c

Frontal lobe

Temporal lobe

Occipital lobe

Parietal lobe

16 (25.4%) 7a (11.1%) 23 (36.5%)

7 (11.1%) 15a (23.8%) 22 (35.4%)

1 (1.6%) 9 (14.3%) 10 (15.9%)

8a (12.7%) 8 (12.7%)

Three cases had an additional associated infratentorial AVF not included in this total number. One had two additional parietal AVFs; one had an additional temporal AVF, and one had additional frontal AVF. There were two multiple lesions associating large AVFs with separate or closely related micro-AVMs. These micro-AVMs are not included in this total number.

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4.3 Associated Conditions 4.3.1 Hereditary Hemorrhagic Telangiectasia

Hereditary hemorrhagic telangiectasia (HHT) (previously called RenduOsler-Weber Disease) is a rare autosomal disorder, characterized by multiple mucocutaneous and visceral telangiectasias (Fig. 4.5), giving rise to hemorrhagic complications in adulthood (MacAllister et al. 1994). Although autosomal dominant (chromosome 9q33-q34, long arm, the locus is named HHT1, a second genotype is located on chromosome 12q), HHT exhibits a cellular recessive pathology and requires inactivation of the normal allele as the initiating event in the formation of a vascular lesion.Alternatively, the initiating event in the formation of a vascular lesion might be damage to the vessel wall with associated failure to remodel normally.

Fig. 4.5A–C. Usual appearance of skin lesions in hereditary hemorrhagic telangiectasia (HHT)

Hereditary Hemorrhagic Telangiectasia

237

Fig. 4.6. A Diagrammatic representation of the progression of HHT in a given patient, which shows the acute changes observed following hormonal events. B Similar approach for a patient with slowly progressive worsening of symptoms not obviously related to hormonal events. Note the repeated embolization sessions needed in this particular case. M, packing; R, radiation; C, electrocoagulation; T, transfusion; D, dermoplasty; E, embolization. Stage 1: episodic but spontaneously resolved bleeding requiring no specific treatment and often neglected by the patient. Stage 2: periodic bleeding sometimes following mechanical trauma (sneezing, blowing nose) requiring no more than one hospitalization per year and/or one blood transfusion, permitting normal professional life. Stage 3: frequent spontaneous bleeding requiring multiple hospitalizations and transfusions per year with incapacitation

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4 Cerebral Arteriovenous Fistulas

Recent careful epidemiological studies in France, Denmark, and Japan, however, have revealed an incidence of 1 in 5,000–10,000 (Bideau et al. 1989; Kjeldsen et al. 1999; Dakeishi et al. 2002). The incidence was previously reported at 1 or 2 in 100,000 (Guttmacher et al. 1995). Three mutations altering the synthesis of endoglin have been found in affected individuals, one substitution (CÆG: TAG code) and two deletions (nucleotide 882 and nucleotide 1553). Endoglin is a homodimeric integral membrane glycoprotein expressed on human endothelial cells of capillaries, arterioles, and venules. The earliest event in the formation of telangiectasias appears to be dilatation of postcapillary venules. Endothelial cells lacking endoglin respond poorly to transforming growth factor-b1 (TGF-b1) and form abnormal vessels, particularly in response to injury. Endoglin is the most abundant TGF-b-binding protein. TGF-b in vivo is a potent angiogenic factor and a mediator of vascular remodeling, as it controls extracellular matrix production by endothelial cells, smooth muscle cells, and pericytes. TGF-b is the prototype of a family of at least 25 growth factors that regulate growth, differentiation, motility, tissue remodeling, normal repair, and programmed cell death in many cell types. The locus heterogeneity in this disorder may be due to mutations within other members of the TGF-b receptor complex or other endothelial cell components of the TGF-b signal transduction pathway. One could question whether the deficiency or immaturity of a similar protein fraction in non-HHT patients could cause the same type of AVM. We have never observed a new CNS AVF in follow-up of HHT patients and have rarely seen high-flow AVFs in adult HHT patients. This suggests that the inherited protein deficiency expresses itself only in AVF at an early age and differently later due to the various maturation processes involved and compensatory mechanisms. Recurrent epistaxis, hemoptysis, melena, and genital bleeding are not uncommon manifestations in adults with HHT, but are rare in children (Aasar 1991; Boynton and Morgan 1973; Lasjaunias 1987; Willinsky et al. 1990a; Mahadevan et al. 2004b). Mucocutaneous telangiectasias and visceral hemorrhagic complications are unusual in children; cerebral or spinal AVM may be the sole manifestation of HHT at this age. Our observations correlate well with the literature, in which telangiectasias and mucosal hemorrhagic complications increase in frequency with age in patients with HHT (Fig. 4.6) (Table 4.4). In HHT patients, CNS AV malTable 4.4. HHT criteria (Mahadevan et al. 2004b)

Epistaxis FH of epistaxis Cutaneous lesions F/H of cutaneous angioma Hepatic lesion Gastric lesion Pulmonary lesion Family history of HHT (F/H) FH, family history.

Adult

Children

Total

10 (90.9%) 8 (72.7%) 8 (72.7%) 2 (18.2%) 1 (9.1%) 5 (45.5%) 5 (45.5%) 11 (100%)

13 (56.5%) 17 (73.9%) 6 (26.1%) 5 (21.7%) 1 (4.3%) 0 (0%) 3 (13.0%) 18 (78.3%)

23 (67.6%) 25 (73.5%) 14 (41.2%) 6 (17.7%) 2 (5.9%) 5 (14.7%) 8 (23.5%) 29 (85.3%)

Hereditary Hemorrhagic Telangiectasia

239

Fig. 4.7A–D. A 3-year-old child presented with a generalized seizure. A family history of epistaxis suggested the diagnosis of HHT. Internal carotid (A, B) and selective anterior cerebral angiogram (C) on lateral views demonstrated single-hole AVF with drainage toward the inferior sagittal sinus. Vertebral angiogram on AP view (D) disclosed a second AVF at the posterior fossa level

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formations conform to the usual AVF and AVM types (Boynton and Morgan 1973; Reddy 1987; Roman et al. 1978) and should be distinguished from telangiectasias. This suggests that AVMs represent either an associated lesion or the early expression of the capillary-remodeling disorder in HHT. AVMs of the CNS are present in approximately 8% of patients with HHT (Reddy 1987). Multiplicity increases this likelihood significantly and Willinsky et al. (1990a) reported that 28% of patients with multiple CNS AV malformations had HHT (Fig. 4.7). Identification of multiple CAVMs should therefore lead one to suspect the possibility of HHT disorder. Garcia Monaco et al. (1995) reported five cases in which a CAVF was the initial manifestation of HHT disorder among 120 children with CAVMs. None of the children had mucocutaneous telangiectasias at clinical examination, but all of them had a strong family history of HHT. None of the children complained of a subjective bruit (pulsatile tinnitus), although an objective cranial bruit was perceived by auscultation in three of them, suggesting that the AVF was present at birth or shortly thereafter. In two patients, the main symptoms were related to AVF rupture, but in three patients venous ischemic and congestive manifestations were found. All patients seen with HHT had one or several single-hole AVFs with a large venous ectasia; two of them also had a small nidus type of lesion demonstrated during the four-vessel work-up. No patients showed focal melting-brain syndrome, indicating the rapid subarachnoid drainage of the AVF and suggesting an explanation for the consistency of the venous pouches reported. More recently, Mahadevan et al. (2004b) reviewed the Bicêtre experience and noted that among 620 children with CAVM there were 23 (3.7%) patients with HHT disorder (Table 4.5). Significant differences in the

Table 4.5. CAVM population reviewed (Mahadevan et al. 2004b)

Total CAVM Total CAVM in adults Non-Galenic CAVM in children Total SCAVM

Number

No. and % of HHT

1,566 946 303 194

34 (2.2%) 11 (1.2%) 23 (7.6%) 5 (2.6%)

SCAVM Spinal cord arteries venous malformation. Table 4.6. Presenting symptom that led to diagnosis (Mahadevan et al. 2004b)

Epilepsy Headache Deficit without ICH Cardiac Insufficiency Deficit with ICH Macrocrania Incidental/prenatal Total number of cases

Adult

Pediatric

Total

2 (18.2%) 2 (18.2%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 7 (63.6%) 11 (32.4%)

4 (17.4%) 3 (13.0%) 4 (17.4%) 4 (17.4%) 3 (13.0%) 3 (13.0%) 2 (8.7%) 23 (67.6%)

6 (17.6%) 5 (14.7%) 4 (11.8%) 4 (11.8%) 3 (8.8%) 3 (8.8%) 9 (26.5%) 34 (100%)

ICH, intracerebral hemorrhage.

Hereditary Hemorrhagic Telangiectasia

241

Table 4.7. Angioarchitecture in HHT-related CAVM (Mahadevan et al. 2004b)

Venous ectasia and giant pouch AVF Multiplicity Nidus Stenosis of pial venous supply Micro-AVM Distal arterial aneurysm Transdural venous supply Reflux venous pial Stenosis of dural venous supply Dural venous thrombosis Angiogenesis Angiectasia Total number of cases

Adult

Pediatric

Total

2 (18.2%) 2 (18.2%) 5 (45.5%) 9 (81.8%) 1 (9.1%) 3 (27.3%) 1 (9.1%) 0 (0%) 0 (0%) 1 (9.1%) 0 (0%) 0 (0%) 0 (0%) 11 (32.4%)

21 (91.3%) 16 (69.6%) 11 (47.8%) 7 (30.4%) 7 (30.4%) 3 (13.0%) 5 (21.7%) 6 (26.1%) 6 (27.3%) 4 (17.4%) 4 (17.4%) 3 (13.0%) 3 (13.0%) 23 (67.6%)

23 (67.6%) 18 (52.9%) 16 (47.1%) 16 (47.1%) 8 (23.5%) 6 (17.6%) 6 (17.6%) 6 (17.6%) 6 (17.6%) 5 (14.7%) 4 (11.8%) 3 (8.8%) 3 (8.8%) 34 (100%)

HHT, hereditary hemorrhagic telangiectasia; AVF, arteriovenous fistula; AVM, arteriovenous malformation.

Scheme 4.1. HHT phenotype per age group (log of the age). (Krings et al. 2004)

clinical presentation of CAVMs in pediatric patients with HHT vs those in adults were also noted. In children, in addition to congestive cardiac failure and macrocrania, neurological deficits without hemorrhage were a frequent presentation (Table 4.6). Almost 70% of the CAVMs in our pediatric HHT population were of the fistula type (CAVF) compared to 18% in the adult HHT population (Table 4.7). Krings et al. (2005b), reviewing the neurovascular phenotypes of HHT per age group in 50 cases with 75 separate lesions, found a significant difference between the types in children and in adults.
Thirty-four cerebral AV fistulae were found in 20 patients. The mean age was 3.0 years; all patients but two were less than 6 years old.

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Seven spinal cord AVMs that were all of the fistulous type were found in seven patients harboring this disease were between 1 month and 6 years of age, with a mean age of 2.2 years.
Sixteen nidus-type AVMs were found in 16 patients whose age ranged from 6 to 60 years (mean, 23.1)
Eighteen micro-AVMs (nidus size under 1 cm) were present in 11 patients (Fig. 4.6). Patient age ranged from 6 to 59 years (mean, 31.8 years). The disease displays an age-related expression, with manifestations developing throughout life and varying between affected individuals, even individuals from the same family. While AVFs were present almost exclusively in the age group of young children under 6 years of age, AVMs were present predominantly in the population of adolescents and young adults, whereas micro-AVMs were present in adults (Scheme 4.1).

Fig. 4.8A–D. A 5-year-old girl presented with sudden onset of headaches showed on enhanced CT (A) evidence of bilateral occipital enhancing vascular lesions. Over the next few days, a partial visual field defect developed and repeat enhanced CT scan (B) showed evidence compatible with partial thrombosis of the vascular channel on the right side. MRI T2 W (C, D) showed increased signal changes within the adjacent brain parenchyma (arrow). E–J see pp. 243,244

Hereditary Hemorrhagic Telangiectasia

243

Fig. 4.8E–H. (continued) Vertebral angiograms in AP view prior to (E) and 10 years following transarterial embolization with glue of bilateral occipital lobe AVFs (F) demonstrate long-term stability after embolization. The suspicion of HHT was confirmed. Right internal carotid angiograms in AP view at presentation (G) and10 years after embolization of bilateral B-AVFs (H) demonstrate a persistent cortical microAVM (arrows), which had remained asymptomatic and could not be seen on MRI examination (I, J). I,J see p. 244

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Fig. 4.8I,J. Legend see p. 243

Moreover, 25% of single AVF and 50% of the multifocal AVFs in children occur in HHT family patients (Weon et al. 2005; Yoshida et al. 2004; Krings et al. 2005a), indicating that AVF might be included in the known diagnostic criteria of HHT. While symptoms may be specifically related to one of the AVFs, complete angiography may disclose additional lesions, some of which may not be visible on MRI examination (Fig. 4.8). This raises questions on the indications and timing of noninvasive screening of the CNS in young patients with a family history of HHT. It is our opinion that such screening should be proposed before 2 years of age and should be repeated after age 6 years. Screening children who have proven HHT but are not symptomatic in terms of the CNS is appropriate at any time, but if negative no repeat screening appears to be necessary, as under such circumstances no new CAVFs are expected to become apparent. Although it has not been our practice in managing HHT children with proven CAVFs to screen the spinal cord with MRI, we would recommend it now, given that these multifocal localizations can coincide (Fig. 4.9). In view of our satisfactory results with management of AVFs in the pediatric population and their unfavorable natural history, we favor the treatment of incidentally discovered AVFs in HHT patients. However, this may not apply to micro-CAVMs in HHT children, as their natural history appears to be very benign (Matsubara et al. 2000; Mahadevan et al. 2004b) (Fig. 4.8), and we would manage those conservatively unless they appear easy to reach by the endovascular approach.

Hereditary Hemorrhagic Telangiectasia

245

Fig. 4.9A–G. Various aspects of HHT phenotypes in the pediatric population. A, B 1year-old boy with familial history of HHT presented with ruptured right cerebellar hemisphere (three locations, arrows) associated with a lesion that quickly ruptured at the upper cervical cord level. C, D A 6-year-old boy with ruptured mesencephalic micro- or small AVM. E–G see p. 246

246

4 Cerebral Arteriovenous Fistulas

Fig. 4.9. (continued) E–G A 12-year-old boy with intracerebral AVM reaching the floor of the IVth ventricle

4.3.2 Encephalocraniocutaneous Lipomatosis

Batista et al. (2002) reported a child with encephalocraniocutaneous lipomatosis (ECCL) associated with posterior fossa AVFs. The child had two high-flow fistulas, one supratentorial and one infratentorial, with additional nonvascular intracranial malformations (lipoma, arachnoids cysts, and cortex dysplasia) (Fig. 4.10). Manifestations of this rare syndrome are shown in Table 4.8.

Hereditary Hemorrhagic Telangiectasia

247

Fig. 4.10A–H. Axial T1 W image (A) shows right-sided paracavernous lipoma (arrow) accompanying the trigeminal nerve. Coronal T2 W images (B, C) show bilateral arachnoid cysts (black arrows) as well as a perimesencephalic venous pouch (white arrow). Lateral angiogram of left internal cerebral artery (LICA) (D) shows a pial AVF (arrow) supplied by middle temporal artery and draining into a Labbé vein and transverse sinus posteriorly. Vertebral angiogram, lateral (E) and AP (F) views and 3D angiogram (G) show a pial AVF (white arrow) supplied by a short circumferential artery from a basilar tip and draining into a ectatic tegmental vein that runs supratentorially toward the transverse sinus; there is a pial venous reflux to the sagittal superior sinus and posterior fossa. The basilar tip AVF was treated first by placing coils loosely in the venous pouch creating a basket and occluding the AVF with two small coils as shown on the 3D angiogram (H). I–M. see p. 248

248

4 Cerebral Arteriovenous Fistulas

Fig. 4.10I–M. (continued) Superselective angiogram in lateral view (I) of he left temporal branch prior to embolization shows cortical AVF, which was then treated by selective injection of pure glue at the fistula, as demonstrated by the cast of glue (J) (arrow). Angiographic follow-up 2 months later of the LICA in lateral view (K) shows complete occlusion of the temporal fistula and vertebral angiogram (L, M) in lateral view shows persistent occlusion of basilar tip AVF

Table 4.8. Encephalocraniocutaneous lipomatosis (from Batista et al. 2002) Subcutaneous soft tumors of the cranium and face consistent with: Lipomas Alopecia and ocular lesions Eyelid defects Epibulbar dermoids Ipsilateral brain malformations: Arachnoids cysts Brain atrophy Changeable degree of enlargement of the ventricular system Mental retardation appears variable intracranial (cisternal) lipoma is uncommon

Presentation

249

4.4 Presentation CAVFs in the pediatric population in our experience present slightly differently depending on their supra- or infratentorial location, presumably related to their different venous drainage characteristics. The symptomatic supratentorial-located AVFs tend to present at an earlier age than the symptomatic infratentorial locations (Tables 4.9, 4.10). While in utero demonstration in our experience has occurred with both supra- and infratentorial locations, symptomatic AVFs at neonatal and infant age are more likely to be supratentorial (Fig. 4.11). In the same series of 52 pediatric patients with CAVFs, there were 41 with supratentorial single-hole cerebral AVFs, with a total of 63 AVFs. The male:female ratio was 28:13 and the mean age at presentation was 24 months. The most common presenting symptoms leading to diagnosis were cardiac insufficiency (31.7%) (Figs. 4.12, 4.13), epilepsy (24.4%), and macrocrania (14.6%) (Figs. 4.14, 4.15) (Tables 4.11, 4.12). About half of the seizures were associated with a hemorrhagic episode. Hemorrhagic onset was found in seven cases. The location of the hemorrhage was intracerebral hemorrhage (ICH) in three cases, combined ICH and intraventricular hemorrhage (IVH) in three, and combined ICH, IVH, and subarachnoid hemorrhage (SAH) in one case. Six patients developed their neurological deficit as the result of intracranial hemorrhage. Nonhemorrhagic neurological symptoms or progressive neurological deficits are infrequent presentations of CAVFs (Figs. 4.16, 4.17).

Table 4.9. Age at diagnosis, referral and first treatment (Weon et al. 2005), Supratentorial AVFs Age

First symptom

First consultation

First embolization

0–30 days 1 month–2 years 2 years–15 years Total

21 (52.5%)a 9 (21.9%) 11 (26.8%) 41 (100%)

9 (21.9%) 21 (52.5%) 11 (26.8%) 41 (100%)

4 (11.3%) 18 (51.4%) 12 (34.3%) 35 (100%)b

a b

Four cases of prenatal diagnosis are included. Six cases were not treated.

Table 4.10. Age at presentation and at diagnosis in 14 children (Yoshida et al. 2004), Infratentorial AVFs Age group

Clinical presentation

Diagnosis

Neonatal Infantile Childhood

1a (7%) 7 (50%) 6 (43%)

0 8 (57%) 6 (43%)

a

Symptoms related to cardiopulmonary malformations.

250

4 Cerebral Arteriovenous Fistulas Fig. 4.11A–E. Prenatal diagnosis of intracranial AVS was made on color flow Doppler ultrasound (A) at 37 weeks gestation. Left carotid angiography in lateral view (B, C) demonstrated two frontal interhemispheric AVFs (arrows) supplied by the anterior cerebral arterial system. Elective embolizations of the AVFs were done with glue at 2 and 11 months of age, resulting in complete exclusion of the lesions, as shown on the postembolization internal carotid angiogram on lateral views (D, E) with normal development of the child for age

Presentation

251

Fig. 4.12. A three-day-old neonate presented with moderate heart failure. Two separate AVFs were shown on internal carotid angiogram in AP (A) and lateral (B) views. One was fed by the middle cerebral artery (long arrow) and the other by the anterior choroidal artery (short arrow). The 3D angiograms before (C) and after embolization (D) of the choroidal fistula with coils showed complete exclusion (arrow). The middle cerebral artery fistula is being progressively occluded with coils (E, F). E,F see p. 252

252

4 Cerebral Arteriovenous Fistulas

Fig. 4.12E,F. Legend see p. 251

▲

Fig. 4.13A, B. A premature baby boy presented with neonatal respiratory distress. The child was intubated and ventilated for 7 days. At 4 months, he developed cardiac failure with hepatomegaly and splenomegaly initially felt to be related to a portocaval fistula. Transfontanel ultrasound revealed an enlargement of the subarachnoid spaces and a pulsatile mass in front of the genu of the corpus callosum. Head circumference rapidly increased. MRI T1Win sagittal views (A, B) and internal carotid (C) and selective anterior cerebral angiography (D) in lateral views revealed an arteriovenous fistula fed by a cingular branch of the anterior cerebral artery (arrow). Embolization eradicated most of the lesion and resulted in improved cardiac status. Note the residual intravascular angiogenesis (E, F). C–F see p. 253

Presentation

Fig. 4.13E,F. Legend see p. 252

253

254

4 Cerebral Arteriovenous Fistulas Fig. 4.14A–E. A 13-month-old child presented with macrocrania related to a left frontal AVF. Postcontrastenhanced MRI T1 W mid-sagittal image (A) and lateral view internal carotid angiogram (B) show an arteriovenous fistula fed by left anterior cerebral artery draining toward the superior sagittal sinus with venous ectasia. On the 1-year follow-up, carotid angiogram in lateral view (C), the AVF is proven to be completely obliterated following two sessions of embolization with glue. The head circumference normalized after embolization therapy, which resulted in decreased dural sinus pressures and remodeling of the dural sinuses as shown on the venous phase of the carotid angiogram in AP views prior to embolization (D) and on 1-year follow-up (E)

Presentation

255

Fig. 4.15A–D. A 6-year old boy presented with headache and macrocrania at age 5 years. MRI on axial (A) and sagittal view (B) demonstrated hydrocephalus related to a huge ectatic vein at the level of the posterior fossa. Vertebral angiography on lateral (C) and AP view (D) demonstrated right cerebellum AVF, fed by the right posterior inferior cerebellar artery (PICA), draining into the vein of Galen. Note the straight sinus occlusion and the major supratentorial venous congestion. E–H see p. 256

256

4 Cerebral Arteriovenous Fistulas

Fig. 4.15E–H. (continued) Selective PICA angiogram in lateral view (E) embolization of the fistula was performed with pure glue (F). At 6 weeks of follow-up, vertebral angiography in lateral (G) and AP view (H) showed complete cure and already satisfactory vascular remodeling. One year later, he was neurologically normal and his macrocrania stabilized

Presentation

257

Table 4.11. Revealing symptoms and symptoms at admission in patients with supratentorial CAVFs (41 patients) (Weon et al. 2005) Revealing symptoms

No. of patients

Symptoms at admission

No. of patients

Cardiac insufficiency Epilepsya Macrocrania Headache Neurological deficitb Growth retardation Prenatal diagnosisc

13 (31.7%) 10 (24.4%) 6 (14.6%) 4 (9.8%) 3 (7.3%) 1 (2.4%) 4 (9.8%)

Cardiac insufficiency Neurologic deficit Macrocrania Epilepsy Growth retardation Headache Epistaxis Exophthalmos

19 (46.3%) 14 (34.1%) 13 (31.7%) 12 (29.3%) 6 (14.6%) 3 (7.3%) 2 (4.9%) 1 (2.4%)

Total

41 (100%)

a b c

Five patients had their epilepsy associated with intracerebral, intraventricular, and/or subarachnoid hemorrhage. One patient had transient facial palsy, another had visual loss, the remaining had progressive hemiparesis. Two of them were diagnosed as cerebral AVFs and two as vein of Galen aneurysmal malformation. At birth three of them had heart failure; one was asymptomatic.

Table 4.12. Clinical features at presentation and on admission (one patient may have multiple abnormalities) (14 patients) (Yoshida et al. 2004), infratentorial AVFs Clinical features

Patients (%) At presentation On admission

Macrocrania Headache Neurological deficit from hemorrhage Neurological deficit without hemorrhagea Cardiac overload Cerebellar symptom Retardation Incidental Epilepsy

4 (28%) 3 (22%) 3 (22%) 2 (14%) 2 (14%) 0 0 0

a

Brain-stem deficit.

5 (36%) 5 (36%) 6 (43%) 4 (28%) 2 (14%) 3 (22%) 1 (7%) 1 (7%)

258

4 Cerebral Arteriovenous Fistulas

Fig. 4.16A–D. A 19-month-old boy presented with a mild, slowly progressive motor deficit on the right side for more than 1 year. MRI T2 W in coronal (A) and T1 W on sagittal (B) views demonstrated multiple large areas of flow void along the ventral aspect of the brainstem and the left lateral aspect, significantly displacing the brainstem and cerebellar structures. Vertebral angiogram in lateral (C) and AP (D) views showed three separate AVFs (white arrows) fed by distal circumferential branches of the vertebral arteries and draining into three large venous pouches, which in turn drained upward toward the perimesencephalic venous system. E–I see p. 259

Presentation

259

Fig. 4.16E–I. (continued) Staged embolization of the AVFs was performed, resulting in near complete thrombosis of the venous pouches and diminished mass effect, as shown on the MRI T2 W in coronal (E, F) and T1 W on sagittal (F) views obtained at 2.5 years of age. Follow-up vertebral angiogram (G, I) demonstrates obliteration of most AVFs and minimal flow in the third. Additional endovascular treatment will be explored while the neurologically is nearly normal now

260

4 Cerebral Arteriovenous Fistulas

Fig. 4.17A–D. Legend see p. 261

▲

Presentation

261

Fig. 4.17A–F. A 3-month-old baby presented with two convulsions and a mild postictal right-sided deficit. T1 W MRI in sagittal views (A, B) demonstrated multiple flow voids along the medial aspect left frontal-parietal cortex (arrow, A) and evidence of hemorrhagic infarction deep within the left frontal lobe (arrow, B). A LIC angiogram in lateral view (C) showed two distinct high-flow shunting zones (arrowheads, asterisks) as well as a third slow-flow shunt (arrow). Delayed venous opacification of the left frontal lobe is noted on the lateral view LIC (D). Embolization was done a few days later and completed in three further sessions. Two and a half years later, the lesion is almost completely occluded, as shown on the LIC angiogram in lateral views (E, F). The neurocognitive evaluation was normal at that time and the right-sided deficit had almost disappeared

In the Bicêtre series, the symptoms tended to progress fairly quickly, requiring investigation and hospitalization. The most frequent clinical symptoms noted at admission were cardiac insufficiency (46.3%), neurological deficit (34.1%), macrocrania (31.7%), and epilepsy (29.3%) (Tables 4.8, 4.12).Among the 52 pediatric patients with CAVFs, there were 14 with posterior fossa AVFs (Figs. 4.18, 4.19). In this series, the diagnosis was not made at prenatal or neonatal age. Eight cases (8/14, 57%) were diagnosed in infancy and six out of 14 (43%) in children under 12 years of age. The mean age at diagnosis was 3.5 years. The male:female ratio was 9:5 (Table 4.10). Revealing symptoms were macrocrania (28%), hemorrhage (22%), headache (22%), nonhemorrhagic neurological deficit (14%), and cardiac overload (14%) (Table 4.12).

262

4 Cerebral Arteriovenous Fistulas

Fig. 4.18A–D. A 6-year-old boy presented with grade II subarachnoid hemorrhage without focal neurological deficit. The T1 W MRI axial view (A) revealed a large flow void along the lateral aspect of the right cerebellar hemisphere. Vertebral angiogram in lateral view demonstrated an AVF from the right PICA, which was embolized with glue in one session with excellent outcome, as shown on follow-up vertebral angiogram in lateral views (C, D)

Presentation

Fig. 4.19A–E. Legend see p. 264

263

264

4 Cerebral Arteriovenous Fistulas

Fig. 4.19A–G. An 11-year-old girl with a family history of HHT suffered from occasional epistaxis and migraines. Neurological examination revealed moderate left spasticity and nystagmus. Cranial auscultation revealed a systolic bruit that was not perceived by the patient. T1 W MRI in sagittal view (A) showed a large flow void along the posterior aspect of the left cerebellum and a small rounded flow void (arrows) near the vein of Galen region. Vertebral angiogram, lateral views (B–D), demonstrate a large AVF arising from the posterior inferior cerebellar artery (arrow, B). Embolization with glue resulted in complete occlusion of the lesion, as shown on the follow-up MRI T1 W sagittal view (E) performed several weeks later, demonstrating increased signal within the previous venous pouch (asterisk, E). Postembolization right (F) and left vertebral (G) angiograms in AP views confirmed closure of the AVF. The child has become neurologically normal on follow-up

Natural History

265

4.4.1 Natural History

The natural history of CAVF after presentation remains mostly speculative, as in our experience we have rarely found such a lesion in a neonate or infant– incidentally or with minor symptoms– that we were able to follow and that continued to be well tolerated without treatment. On the other hand, in particular with posterior fossa locations and depending on the age at diagnosis, their tolerance in young children can be surprising, when one considers their size and flow. As was mentioned in Chap. 2 of this volume, this would suggest a spectrum of natural history rather then a single one. In other words, the natural history after presentation is likely determined by the individual host response to the presence of the AVF, systemically (heart, liver, kidney, etc.), regionally (brain, dural sinus, CSF, etc.), and the decompensation that may occur at the level of the AVF itself (hemorrhage, etc.). The in utero demonstration of CAVF is rare and by itself does not have any clinical implications. Noninvasive imaging by ultrasound or MRI may, however, demonstrate evidence in utero or at neonatal age of regional, hemispheric, or diffuse cerebral malacia. Such findings in our experience are not reversible, despite curative treatment, and in fact are a contraindication to active treatment when extensive encephalomalacia is present, as the natural history under those circumstances is extremely poor (Figs. 4.20–4.23). The reason for the comparatively low frequency of CAVFs in adults would suggest either their early expression, their spontaneous (asymptomatic) thrombosis, the early progression toward symptomatology, or even incompatibility with survival. From our combined experience, there is little evidence to suggest the occurrence of spontaneous asymptomatic thrombosis and we therefore favor the postulate that CAVFs have a natural history that is highly age- and host-specific and unlikely to be tolerated for a long time.

Fig. 4.20A, B. T2 W MRI in coronal (A) and sagittal (B) views in a 2-week-old girl demonstrates right-sided cingular gyrus AVF draining into the deep venous system and associated with hemispheric atrophy

266

4 Cerebral Arteriovenous Fistulas Fig. 4.21A–C. A baby girl presenting as a neonate with acute heart failure related to a CAVF. Digitalis and diuretic treatment was given and improved the clinical situation. Ultrasound, computed tomography, and angiography (not shown) led to diagnosis of a sylvian AVF, and embolization was attempted three times at another institution. Because of these technical difficulties, the child was transferred at 1 year of age to our institution. Heart failure was under control but developmental delay of about 3 months had occurred as well as a right hemiparesis. MRI was performed (A) and showed hemispheric atrophy. LICA angiogram in lateral views (B, C) demonstrated high-flow AVF from left MCA with venous congestion affecting the left hemisphere. An endovascular procedure was performed with difficulty and partially occluded the shunt. The remaining lesion was subsequently surgically resected but the child died shortly afterward

Natural History

Fig. 4.22A–C. Prenatal diagnosis. Neonate presented in acute heart failure, which was difficult to manage, as well as macrocrania and an intracranial bruit. There was systemic manifestation of hepatic and renal failure. CT revealed large, intracerebral venous pouches associated with ventricular dilatation and subcortical leukoencephalomalacia. The child was in severe neurological distress. The true nature (pial or dural) of the lesion could not be assessed. The baby died rapidly

267

268

4 Cerebral Arteriovenous Fistulas

Fig. 4.23A–F. Legend see p. 269

▲

Natural History

269

Fig. 4.23A–K. Color flow Doppler examination (A) demonstrated evidence of large AV shunt at posterior fossa level at 36 weeks gestation in utero. MRI examination at 5 days of age showed, on sagittal (B) and axial views (C, D), evidence of a very large flow void at lower aspect posterior fossa as well as second lesion along right sylvian region. Cerebral atrophy was already present at that time, while the child clinically was in moderate to severe heart failure. Vertebral angiogram demonstrated in AP views (E, F) evidence of large AVF fed by right PICA. Selective PICA angiogram in AP (G) and lateral (H) views confirmed AVF prior to obliteration with coils (long arrow), as shown on postembolization vertebral angiograms in AP (I) and lateral (J) views. Additionally, a small AVF was shown fed by the right MCA (small arrow). Follow-up MRI 1 week later in axial view (K) demonstrates closure of the AVFs as well as progressive cerebral atrophy. The baby progressively clinically worsened and died 1 week later

270

4 Cerebral Arteriovenous Fistulas

4.5 Management The indications, the time, and the method of treatment chosen for management of CAVFs depend on a variety of factors such as the age at presentation, presenting symptoms, the status of the brain, and the status of the other organs. Treatment may be contraindicated because of already existing severe brain damage: melting brain syndrome (cortical or subependymal) and/or diffuse parenchymal calcifications (Fig. 4.23). These can be noted either at the time of diagnosis or can develop rapidly between the initial consultation and the actual admission of the child for treatment. This was the case in 7% of patients with supratentorial CAVFs (Weon et al. 2005). Treatment objectives in neonates and infants are the same as in VGAM; however, the insult to the cerebral tissue is more rapid, as the drainage occurs to subpial veins in most instances. Because of the poor neurological prognosis, one should attempt to achieve total occlusion or a significant reduction of the shunting through the AVF (more than 75%) more rapidly (Figs. 4.24–4.26). Early management is dictated by the danger of brain impairment, and less so by the congestive heart failure, which is usually mild. Patients should be evaluated clinically, by noninvasive imaging, in order to assess the degree of interference between the AVF and the brain tissue. Angiography is done with intent to treat, planning the first embolization session, almost regardless of the existing symptoms. If congestive heart failure is severe, the prognosis is extremely poor, since it combines both systemic and subpial effects. Possible hydrodynamic disorders should be managed early through reduction or occlusion

Fig. 4.24A, B. Legend see p. 271

▲

Management

271

Fig. 4.24A–F. A male neonate presenting in moderate to severe cardiac failure showed on vertebral angiogram on lateral (A) and AP (B) views a high-flow AVF fed by the superior cerebellar artery, which was embolized with glue when the baby was 23 days old. The child became clinically asymptomatic and follow-up vertebral angiogram in lateral (C) and AP (D) views at 1 year and vertebral angiogram in lateral views at 3 years of age (D, E) demonstrated progressive thrombosis of the AVF. The child was clinically normal at that time and remains so at 2 years follow-up

272

4 Cerebral Arteriovenous Fistulas

Fig. 4.25A–D. A 20-month-old boy presenting at 3 days of age with cardiac failure that was controlled medically with digitalis and diuretics. Ultrasound and MRI of the brain (not shown) suggested a temporal AV shunt. This diagnosis was confirmed on left ICA angiogram on lateral view (A) and vertebral angiogram lateral view (B). Embolization was started at 3 months of age when the child was referred to us, and after the third session the lesion was almost completely excluded from the circulation. Long-term follow-up internal carotid angiogram in lateral view (C) and vertebral angiogram on lateral view (D) demonstrated permanent occlusion of the AVF

Management

273

Fig. 4.26A–D. Neonate presented at birth with acute heart failure. There was a family history of HHT. CT examination (A, B) demonstrated large vascular structure within the sylvian fissure on the right side, which at carotid angiography on AP (C) and lateral (D) views proved to be the venous pouch associated with a AVF. Embolization with glue resulted in greatly diminished flow through the lesion, as shown on carotid angiogram in lateral views before (E) and immediately after embolization (F). The child no longer has heart failure, E,F see p. 274

274

4 Cerebral Arteriovenous Fistulas

Fig. 4.26E,F. Legend see p. 273

of the AV shunts (Figs. 4.27, 4.28) unless noninvasive imaging already shows evidence of irreversible diffuse brain damage. Convulsion is a major symptom and should indicate the need for rapid treatment, even if the convulsion remains isolated and without permanent effect. Although pial lesions in infancy present features that simulate the VGAM pattern, symptoms are significantly different, rarely causing hydrodynamic disorders, but frequently focal neurological symptoms (Fig. 4.29) and hemorrhage. CAVF rapidly produces local brain atrophy (focal melting-brain syndrome) and not diffuse macrocrania with bilateral brain damage, in contrast to VGAM. This atrophy represents the subacute local effect of abnormal hydrodynamics induced by surrounding pial venous congestion. Dural sinus hyperpressure (Quisling and Mickle 1989; Zerah et al. 1992) can induce reversible tonsillar prolapse (Girard et al. 1994), which expresses the posterior fossa hydrovenous disorders (Andeweg 1989). Special attention must be paid to the venous drainage of the brain at each session in order to follow the maturation of the various outlets and their patency. Therapeutic decision-making is usually complex in children with multiple AV shunts and should be approached on an individual basis (Iizuka et al. 1992; Willinsky et al. 1990a,Yoshida et al. 2004; Weon et al. 2005). The clinical history in combination with the MRI, computed tomography (CT), and angiographic findings, help determine which lesion or lesions cause symptoms and therefore need prompt treatment. At the neonatal age, the most prominent shunt should be attacked first, as well as the one that gives rise to the most prominent pial congestion, in order to obtain systemic relief and brain drainage improvement, or if the presentation is a hemorrhage, the lesion that produced the bleed must be treated first.

▲

Management

275

Fig. 4.27A–D. Neonate presented at birth with heart failure (A) and progressive macrocrania. An intracranial bruit was heard at auscultation (B). Tonsillar prolapse was noted on MRI T1 W sagittal view (C). Carotid angiogram on lateral view (D) prior to staged embolizations with glue demonstrated a frontal AVF draining into the ectatic sylvian and subtemporal veins (short arrows). E–G see p. 276

276

4 Cerebral Arteriovenous Fistulas

Fig. 4.27E–G. (continued) At 9 years of follow-up, carotid angiogram on lateral (E, F) and AP (G) views demonstrated near complete obliteration of the AVF (long arrow) with incomplete remodeling of the middle cerebral artery trunk (short arrow)

Management

277

Fig. 4.28A–D. AP views of vertebral artery (A, B) in a 4-month-old girl demonstrate single-hole AVF. Embolization with pure glue obliterated the AVF, as confirmed by postembolization vertebral angiogram on lateral views (C, D) (same case as Fig. 4.1)

278

4 Cerebral Arteriovenous Fistulas

Fig. 4.29A–D. A 3-year-old girl presented with severe headache and multiple neurological deficits (right IIIrd nerve palsy, left facial weakness, and left motor weakness of the leg). MRI T2 W in sagittal view (A) and MRA (B) showed a large flow void at the interpeduncular cistern level. V-P shunt was performed because of acute ventricular enlargement. Three weeks later vertebral angiography in AP view (C, D) demonstrated an AVF, fed from the right superior cerebellar artery (SCA) and draining into the vein of Galen. E–L see p. 279

Management

279

Fig. 4.29E–I. (continued) The feeder was thought to be too short to allow for a safe injection of glue without risk of reflux into the parent arterial trunk, and coils were placed in the fistula, reducing the flow by 90%, as shown on selective superior cerebellar (E) and postembolization vertebral angiogram (F). Follow-up MRI T1 W sagittal (G), axial (H), and MRA (I) showed complete closure of the lesion. Resolution of the neurological deficit occurred over the next few months and complete clinical recovery was noted at 1 year of follow-up

280

4 Cerebral Arteriovenous Fistulas

Regarding the management of asymptomatic CAVFs, the therapeutic decision is controversial. it has been suggested that no treatment and simply follow-up is a reasonable option in asymptomatic patients. In contrast, we recommend the active treatment to close the AVF because of the poorer prognosis of conservatively managed patients. Based on our experience and the high mortality of untreated patients reported in the literature (Nelson et al. 1992; five deaths in eight patients who were conservatively managed), we highly recommend active intervention. Treatment options to achieve this goal are embolization or open surgery (Nelson et al. 1992; Tada et al. 1986) (Table 4.13); there is a very limited role for radiosurgery in older children. Both surgery and embolization have proven equally effective in the cure of CAVF. However, we prefer the endovascular approach, since it avoids craniotomy with its concurrent morbidity and reduces the hospitalization time. In 11% of cases, treatment of the supratentorial CAVFs was performed within the first 30 days of life, 51% within the first 2 years, and the remainder between 2 and 15 years of life (Weon et al. 2005). This was significantly earlier than the infratentorial CAVFs, which had a median age of 3.5 years (range 5 months to 12 years) when first treated. While open surgery has been performed to obliterate these lesions (Carillo et al. 1984; Barnwell et al. 1990; Aoki et al. 1991; Nelson et al. 1992; Kikuchi et al. 1994; Talamonti 1997), the method of choice over the past two decades has become the endovascular approach. The maturation of this technique in dedicated pediatric neuroendovascular centers has allowed for safe and targeted embolization of these CAVFs. Similar to the

Table 4.13. Selected literature on supratentorial AVFs in children (Weon et al. 2005) Author

Age of reported cases

No. of AVFs Treatment modalities

Clinical outcome

Mortality

Carrillo et al. 1984 Vinuela et al. 1987 Barnwell et al. 1990 Aoki et al. 1991

4 years

1

Surgery

Good

0%

12–15 years

2

Good

0%

3–7 years

3

Combined (1 case), conservative (1 case) Surgery, combined

Good

0%

1 year

1

Surgery

Good

0%

Nelson et al. 1992

1 day–-19 years

13

7 and 16 years

2

8 months

1

Surgery

7/11 complete exclusion 1 excellent, 1 unknown Normal

7.8%

Kikuchi et al. 1994 Talamonti 1997 Weon et al. 2005

Endovascular (9 cases), surgery (1 case), combined (1 case), conservative (2 cases) Surgery (2 cases)

£15 years

63 AVFs in 41 patients

Endovascular (34 cases), endovascular + radiotherapy (1 case)

88.6% good

5.6%

?

Remarks

1 case of HHT1 Minimal leg weakness

HHT1

0% 11 cases of HHT1 (25%)

Management

281

experience gained with vein of Galen malformation, we have seen the benefit of the progressive staged obliteration of these lesions, allowing the vasculature and the maturing brain to adapt to the new hemodynamic circumstances. In the Bicêtre series, 48 of 49 pediatric patients with CAVFs were treated by embolization alone and one with embolization and radiosurgery; 91% of the supratentorial CAVFs were treated with glue alone, 6% with a combination of coils and glue, and 3% with coils alone. A single embolization session was performed in 34%, two or three sessions in 49%, and four or five sessions in six cases (17%). These data were approximately the same for the endovascular approach to posterior fossa CAVFs: 79% were treated with glue alone, 14% with a combination of coils and glue, and 7% with coils alone. Although it is known that an AVF can be cured if the occlusion is achieved distal to the last normal arterial branch and proximal to the first normal opening vein, this is often more simply achieved by the transarterial approach. No retrograde transvenous approaches were performed. It is not our intention to describe the techniques used in detail, as its practice takes time and requires appropriate guidance (see Vol. 2.2, Chap. 14 for various techniques of high-flow fistula occlusions). It should be clearly understood that injections into high-flow fistulas with pure glue require experience. While the endovascular occlusion of a single channel representing the AVF is in most cases technically feasible and safe, many of the AVFs actually have multiple arterial feeders converging on to a single draining vein and closure of such angioarchitecture may benefit from a staged or a multidisciplinary approach in order to achieve the desired clinical outcome at the lowest risk. The results of endovascular or surgical therapy needs to be assessed with the clinical outcome in mind. Curative treatment performed without recognizing that it is contraindicated will necessarily lead to poor clinical outcome (Fig. 4.23). On the other hand, partial and staged treatment that is well targeted and performed for the proper reasons may result in stabilization of the hemodynamic equilibrium with clear improvement over the anticipated natural history. Following endovascular management of the supratentorial CAVFs, 89% were asymptomatic, improved, or clinically stabilized in Weon’s series; 74.3% of the patients were neurologically normal and 14.3% continued to have minor neurological symptoms, which were unchanged from their status at the time of the original referral. Treatment was considered complete following a maximum of three embolization sessions in 78% of patients, which also included the treatment of multifocal lesions. The average number of sessions was 2.3 per child, with each intervention lasting between 30 and 90 min per session. Follow-up since the last intervention ranges from 6 months to 7 years (mean, 4.2 years). Complications of endovascular therapy of high-flow AVFs might be related to the inadvertent distal embolization of the embolic material (glue or coils) or the proximal occlusion of the parent vasculature (Fig. 4.30). Proper analysis of the angioarchitecture and the choice and sequence of the embolic materials to be used will avoid many of these pitfalls.

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Fig. 4.30A–D. A neonate female presented with moderate to severe heart failure and showed at MRI T2 W coronal (A) and sagittal (B) views to have prominent flow voids along high-convexity left hemisphere (long arrow) and near the vein of Galen region (short arrow). Left ICA angiogram on AP view (C) and oblique view (D) demonstrated a high-flow AVF (short arrow) arising from the left posterior cerebral artery and draining toward the vein of Galen as well as a second AVF (long arrow) fed by the left middle cerebral artery. Staged embolizations were performed at 2 weeks and 2 months of age, and a neurological deficit occurred following inadvertent deposition of a small droplet of glue into the M1 segment upon withdrawal of the microcatheter following embolization of the MCA AVF. E–I see p. 283

Management

Fig. 4.30E–I. (continued) Postembolization carotid angiogram in lateral view (E) demonstrated near complete occlusion of the PCA AVF, while CT scan (F, G) showed evidence of embolic material within the MCA trunk (long arrow) and early ischemia (short arrow). Eighteen months later after a mild transient hemiparesis, the child was neurologically normal, the MCA was fully patent, and the left parietal AVF was occluded. The large posterior AVF has significantly decreased its flow, as shown by the dramatic change of the vein of Galen size; however, spectacular angiectasia has taken place in the vicinity of the previous fistulous point (H, I)

283

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Fig. 4.31A–C. A 10-year-old boy with a family history of HHT was known to have a history of intermittent epistaxis. He then presented with a generalized seizure caused by an intracranial hemorrhage. T1 W MRI sagittal view (A) revealed prominent flow voids along the medial aspect of the posterior left frontal lobe cortex as well as along the right parietal lobe region adjacent to the recent hemorrhage, as shown on T2 W axial view (B). Left ICA angiogram on lateral view (C) showed a parasagittal AVF fed by the anterior cerebral system. A–C see p. 285

Management

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Fig. 4.31D,E. (continued) The RIC angiogram on lateral views (D, E) showed a right parietal AVF, confirming the multiplicity of the AVFs. Fatal hemorrhage occurred several months after staged partial embolizations

In Yoshida’s series, there was no significant morbidity and no mortality immediately related to the endovascular procedures in the 23 AVFs treated at the posterior fossa level. However, two patients developed a transient and one patient a permanent neurological deficit among 35 patients treated for supratentorial CAVFs. Delayed hemorrhage occurred in two patients who were undergoing staged endovascular treatment several months after partial treatment (Figs. 4.31, 4.32). Staging is therefore an important element of our ability to anticipate the natural history of these lesions, their multifocal character, or the impossibility of further embolizing a lesion located in an eloquent area, potential limiting factors. Thorough knowledge of the brain maturation processes, as well as the arterial and venous anatomy, are necessary to properly apply the agents or combinations of agents available today in a timely manner. The transarterial route still remains the optimal approach at this time in our experience. Yet several cases have had their venous sector embolized through the arterial feeders (Figs. 4.33, 4.34).

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Fig. 4.32A–F. Legend see p. 287

▲

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Fig. 4.32A–H. Fig. 4.32A–H. A 20-month old baby presented with macrocrania and arymptomatic moderate cardiomegaly Sine age of 12 month. MRI (A,B) and angiography (C,D,E) demonstrate two AVFs in the porterior fona. Four senious and 6 arterial feeders reduced the lesions by over 50% as seen on angiography (F). A significant amount of glue was delivered (G). The treatment was spread over 2 years period. After the last MRI (H) he was well and scheduled for further session 6 month later. He died suddenly from brain strem hemorrhage while diving in a swimming pool.

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Fig. 4.33A–G. A 3-year-old boy presented with speech difficulties. Axial MRI (A) angiogram showed a high-flow fistula with short feeders in an eloquent area (B–D). The embolization was therefore performed with coils transarterially in one session into the venous chamber of the fistula. At 6 months, the nearly complete exclusion immediately after coil deposit was completed (E–G). The child is neurologically normal

Management

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Fig. 4.34A–E. A 4-year-old child presenting with single hole AVF on the frontal lobe (A, B). The short arterial feeder to the fistula’s chamber led to the use of coils deposited on the venous side after transarterial catheterization across the fistula. Follow-up angiogram 5 months after the treatment (C, D); the child is clinically normal

5 Cerebral Arteriovenous Malformations

5.1

General Remarks 292

5.2 5.2.1

Angioarchitecture of Cerebral Arteriovenous Malformations 298 Single Nidus Versus Multifocal Niduses 298

5.3

Conditions Associated with CAVMs 302

5.4 5.4.1

Conditions Mimicking CAVMs 306 False Pial Arteriovenous Malformations Including Proliferative Angiopathies 306 Perinidal Angiogenesis 306 Postischemic Luxury Perfusion 306 Proliferative Angiopathy 306 Induced Pial AV Shunts Secondary to Dural Sinus High-Flow Lesions 309

5.4.2 5.4.3 5.4.4 5.4.5 5.5 5.5.1 5.5.2 5.5.3 5.5.4 5.5.5 5.5.6 5.5.7

Angioarchitectural Progression of CAVMs in Children 311 Venous Angiopathy 311 Dural Sinus High Flow 312 Venous Ischemia and Thrombosis 315 Venous Hemorrhage 316 Venous Enlargement 321 Arterial Angiopathy 324 Spontaneous Thrombosis of Arteriovenous Malformations 330

5.6 5.6.1 5.6.2 5.6.3 5.6.3.1 5.6.3.2 5.6.4 5.6.5

Objectives of Treatment 330 Complete Exclusion 330 Partial Treatment 336 Neonates and Infants 340 Hydrodynamic Disorders 341 Multiple Arteriovenous Malformations 342 Children 342 Rebleeding 344

5.7 5.7.1 5.7.2 5.7.2.1 5.7.2.2

Technical Management 345 General Remarks 345 Other Techniques 345 Surgery 345 Radiation Therapy 352

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5.1 General Remarks Cerebral arteriovenous malformation (CAVM) is the name we assign to a direct communication from an artery to a vein through an intervening “nidus” which is located in the subpial meningeal space. Brain AVM, pial AVM, cerebral AVM, or non-Galenic CAVM all refer to the same entity: arteriovenous communications in the subpial compartment of the central nervous tissue. Although in the past we have discussed the nidus and fistula types of lesions together (Lasjaunias 1997), we have now elected to distinguish these two types of angioarchitecture (see Chap. 4, this volume). CAVMs appear to have a presentation and a natural history that is different from CAVFs and will therefore require different management strategies. The location of CAVMs in the subpial meningeal space separates them clearly from dural and subarachnoid shunts (dural malformations, vein of Galen malformations). Since there is an anatomic continuum between the subpial and the subependymal sectors along the interstitial and perivascular space (Virchow Robin spaces), CAVMs can be superficial, subcortical, deep, or subependymal without this constituting a formal difference. The same applies to cerebellar or brain stem locations. AVMs are randomly distributed in the CNS, and various sites appear (in terms of frequency and epidemiology) according to the respective proportion of the regional mass tissue from which they develop as compared to the rest of the CNS. Posterior fossa AVMs are not less frequent than hemispheric AVMs, but simply reflect the ratio between the mass of infratentorial and supratentorial tissue. The nidus can vary in type and size. CAVMs are often associated with some degree of angiogenesis (Fig. 5.1) or angiectasia (Fig. 5.2). The latter should be recognized and separated, as it occurs in normal adjacent territories. These niduses can be deeply buried or superficially located. In our experience, since nearly all fistulas and high-flow lesions of the brain are superficial in location, CAVMs in children are more common in deep locations at the time of presentation. This observation enforces the role played by the venodural junction in determining the flow in a given type of shunting zone and its subsequent angioarchitecture. The significance of the size of the nidus vs the expected type of presentation or natural history is likely to be different in children and adults. In children, similar to adults, hemorrhagic events can be caused by a microAVM (Fig. 5.3). This presentation is more likely to occur in older children, as hemorrhagic events in neonates and infants are more likely caused by venous infarction. Discovery of a micro-AVM in a young child is infrequent before the age of 6 years. Most AVMs are of the macro-AVM type and most often deeply seated. The therapeutic decision to treat depends on one’s ability to understand the effect time has on the vasculature in order to appreciate both the aggressiveness of a lesion and the weakness of the host, which will determine their natural history. At a given moment, one should be able to identify the natural history and the specific background of an individual, which in turn indicates the type of risks he or she is exposed to.

General Remarks

Fig. 5.1A,B. A 7-year-old girl suffering from daily migraines associated with generalized seizures that were well controlled by antiepileptic therapy. Her neurological examination was normal. No visual field troubles were detected (A). Following proximal embolization, note the intense angiectasia (B). C,D see p. 394

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Fig. 5.1C,D. (continued) The child was operated upon successfully (C, D)

General Remarks

295

Fig. 5.2A, B. Young female presenting right-sided vascular malformation of the frontal region. Note the significant stenotic phenomena observed at the circle of Willis (A, B). Angiectasia as well as some arterial dilatation can be seen. Transdural supply from the ethmoidal artery also contributes to the revascularization of the frontal lobe

The eloquence of the tissue in the vicinity of the AVM is an additional source of confusion. While important at the time of a surgical approach, the concept of eloquence should not imply the type of clinical manifestations through which an AVM reveals or expresses itself. The precision with which a given technique can reach the lesion will determine the importance of the neighboring tissue. If a certain treatment technique remains inside a given extracerebral space (subpial and endovascular) without enlarging it and remains within the lesion, then the induced effects will be hemodynamically based and not mechanically related. The second consequence of the eloquence of a brain AVM is that, in order to fully appreciate the effects of a given treatment, how the disorder is expressed should be understood. Experience in children has shown that the clinical expression of CAVMs is related to the remote impact of the AV

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Fig. 5.3. A 9-year-old boy presenting with a large frontoparietal hematoma associated with a microlesion (arrow)

shunt on the hemo- and hydrodynamic equilibrium. In addition, cerebral eloquence has a different significance in a maturing brain in an infant, and it is therefore improper to apply the adult experience with functional cerebral mapping or scoring to children. The size is mostly a surgically emphasized aspect of the nidus, which does not have any formal predictive value as far as the natural history is concerned, since diffuse niduses can be well tolerated and a small vermian lesion may produce a rapidly lethal melting-brain syndrome (Fig. 2.30). In addition, determining the size at a given moment is to take a snapshot picture of a biologically active entity in an attempt to transform it into a fixed target. There are three frequently held misconceptions: (1) all CAVMs are present at birth and their symptoms occur randomly, (2) all individuals have the same biology and therefore react or fail to react in a similar fashion, based on the time elapsed and statistical formulas, and (3) the vascular system remains the same (with the same compliance) throughout aging (Fig. 5.4). The venous drainage pattern of an AVM will influence the surrounding brain area that may eventually suffer hemodynamic consequences. If the vein draining the lesion is subpial for a long segment, its chances of interfering with brain drainage are maximal until it joins a significant outlet that takes it across the subarachnoid space to the dural sinuses away from the brain vasculature. However, during its subpial portion, the venous channel is in direct connection with the venules participating in both arterial drainage and water homeostasis (Fig. 5.5). This subpial course can be particularly long. Some convexity AVMs have a draining vein that courses toward the superior sagittal sinus (SSS), but instead of opening into it, it suddenly turns in a different direction, causing congestion of multiple cortical veins before finally draining into the SSS using a remote cortical venous outlet. The opacified cortical veins may have some seg-

General Remarks

297

Fig. 5.4A–F. A 9-year-old child presenting a posterior fossa malformation discovered incidentally due to facial cosmetic problems. The lesion resembles proliferative angiopathy within the right cerebellar hemisphere (C–F). MRI performed 8 years before shows almost no abnormality in the same region (A, B)

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Fig. 5.5. The venous angioarchitecture comprises variations, collateral venous circulation, thrombosis, stenosis and kinking, false aneurysm, as well as sump effects with induced arteriovenous shunts. This part is particularly rich in children since it carries specific aspects never encountered in adults, i.e., hydrovenous disorders. 1, Venous drainage; 2, venous pouch; 3, venous reflux; 4, dural opening; 5, cortical reflux; 6, subpial reflux; 7, medullary and 8, subcortical reflux; 9, secondary pial reflux

mental stenosis, which corresponds to extrinsic arterial compression in the subpial space at the cortex. The subpial congestion is maximal locally, although it can extend to impact an entire hemisphere. Its interference with the local trophicity is maximal in neonates and infants. The specific appearance of the melting-brain syndrome at the neonate and infant ages in CVAMs is directly related to this anatomic characteristic. Conversely, if the drainage of a lesion is immediately subarachnoid, provided that the subarachnoid transit distance is short, the subpial venous congestion will be reduced, as well as the chances of melting-brain syndrome and local atrophic changes. Venous reflux decreases tissue perfusion faster than the changes in cerebral blood flow through a moderate increase in intracranial pressure that accompanies macrocrania.

5.2 Angioarchitecture of Cerebral Arteriovenous Malformations 5.2.1 Single Nidus Versus Multifocal Niduses

In children, even more so than in adults, it is important to recognize the existence of multifocal CAVMs (Figs. 5.6, 5.7). Series and case reports of multifocal lesions and unusual associations have been published (Reddy 1987; Rodesch et al. 1988; Schlater 1980; Smith 1982; Willinsky et al. 1990a; Parkinson 1977; Stone 1980; Tamaki et al. 1971; Tada et al. 1986; Zelam and Buchheit 1985; Hanieh et al. 1981; Hash 1975; Hoffman et al. 1976). The number of multifocal lesions in children, in our experience,

Single Nidus Versus Multifocal Niduses

299

Fig. 5.6A–D. Various types of multifocal arteriovenous malformations (AVMs) (from Garcia Monaco 1991c). A Multifocal arteriovenous malformation; B compartmentalized malformation without separate venous drainage; C separate nidus with distinct venous drainage; D induced pial shunt in infantile type of dural arteriovenous shunts

Fig. 5.7. A 14-year-old girl suffering from seizures not controlled by medical therapy. She had four arteriovenous malformations in the left temporal region, the left prefrontal region, the right middle temporal lobe, and the right rolandic region

is twice that of adults (17.2% vs 9%). The various characteristics of every type of AV shunt can occur, but more often we find the same type of angioarchitecture in all sites in the same individual, i.e., multiple fistulas or multiple niduses. The lesions usually involve both hemispheres (Fig. 5.7) and may be located supra- and infratentorially. The reason for the comparatively low frequency of multiple AV shunts in adults remains unclear but some AVMs in multifocal pediatric cases thrombose spontaneously (Fig. 5.8). The fact that an AVM becomes evident in children (Table 5.1) (see Chap. 2, this volume) indicates an earlier

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Fig. 5.8A–E. A 10-year-old boy complaining of ophthalmic migraines associated with a right hemianopsia since the age of 6 years. CT shows a brain stem AVM (A) seen on angiography with two additional locations (B, C). At follow-up, note the progressive thrombosis of two of them (D, E). He died 4 years later from sudden intracranial hemorrhage. D,E see p. 301

Single Nidus Versus Multifocal Niduses

301

Fig. 5.8D,E. Legend see p. 300

disruption of the equilibrium of the vascular system created by a given revealing trigger; this may indicate an age-related or an individual-specific weakness rather than a focal weakness. In children, the trigger may be exerted randomly, as shown by the distribution of the AVMs, and the weakness can potentially be diffuse; hence AVMs are potentially multifocal. In adults, the compliance of the system and the maturation of the vascular remodeling interferes with the occurrence of multiple locations, either because local vasculature failure becomes the predominant condition or because vascular healing takes place over time and is associated with a course remaining totally subclinical. Table 5.1. Pial (non-Galenic) AVMs: age at first diagnosis Age

n

Prenatal Neonatal Infancy Childhood (<16 years) Adults Total

3 17 39 244 946 1,248

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5.3 Conditions Associated with CAVMs Some specific syndromes can be identified in CAVMs in children and have now been recognized as the expression of the origins of the cerebral and facial vasculature: the cerebrofacial arteriovenous metameric syndromes (CAMS) (see Chap. 6, this volume). Others include genetically based disorders. There are thus far no convincing reports of familial occurrence of CAVM. CAVMS in HHT children have several specific aspects in angioarchitecture that may distinguish them from the sporadic forms, as discussed in Chap. 4 of this volume. While the hallmark of the angioarchitecture in younger HHT patients is fistula communication, venous ectasias, and their multiplicity, the nidal type of configuration tends to occur in older children after the age of 5 or 6 years. Nidus types are seen in adolescents and younger children and microlesions in young adults (Krings et al. 2005b). It is interesting to note that no new lesions have been seen in the follow-up of these patients, nor have telangiectasias been demonstrated in the brain or spinal cord despite the name of the disease. The association of a CAVM and a separate intracranial dural high-flow AVS is rare but has occurred in two children in our series (Fig. 5.9). The entity of CAVMs induced by high-flow DAVSs will be discussed later on in Sect. 5.1.4.5. Diseases involving collagen abnormalities have been associated with cerebral AV shunts. Neurofibromatosis-1 (NF1) (Fig. 5.10) and ElhersDanlos syndrome have been reported in patients with CAVM, but the brain location is not specific and the relationship between these arterial wall diseases and the advent of an AV shunt phenotype is unclear. CAVM in young patients can also be associated with other vascular anomalies such as cavernomas and developmental venous anomalies (DVAs) (Fig. 5.11). This association is not common and the coexistence of these entities needs to be carefully assessed with respect to the perceived cause of symptoms and proposed treatment strategies. For instance, a CAVM draining into a DVA is likely to be more clinically eloquent, and at the same time will be associated with a higher risk of treatment-related complications if the DVA is not preserved for drainage of the adjacent normal brain (see Chap. 8, this volume).

Conditions Associated with CAVMs

303

Fig. 5.9A–D. A 27-year-old female had become symptomatic at age 13 with dyspnea, and at that time 15 pulmonary arteriovenous shunts (AVSs) were diagnosed and subsequently treated by embolization. Recent CT investigation for headaches (not shown) suggested posterior fossa AVM. Lateral views of the external (A) and internal carotid angiogram (B) demonstrated a dural AVF along the anterior aspect of the middle cranial fossa (arrows), while the vertebral angiogram in lateral view (C) demonstrated a small AVM adjacent to the inferior aspect of the fourth ventricle (arrow). Examination of the right hand (D) revealed typical changes involving the nailbeds compatible with longstanding cyanosis as well as a post-traumatic AVS involving the dorsal aspect of the right hand in this patient with proven HHT

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Fig. 5.10A–E. A 13-year-old boy suffering from repeated intracranial hemorrhage resulting in permanent moderate hemiparesis, seizures, and headaches. Family history was suggestive of NF1 (A–E)

Conditions Associated with CAVMs

Fig. 5.11A–C. A young adult presenting with a sudden intracerebral hemorrhage with no previous personal history, resulting in a residual left-sided hemiplegia. Note the typical DVA appearance (A, B). Elective embolization of the fistula was achieved (C)

305

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5.4 Conditions Mimicking CAVMs 5.4.1 False Pial Arteriovenous Malformations Including Proliferative Angiopathies

False pial arteriovenous malformations (PAVMs) demonstrate early venous return associated with some types of nidus appearance. Some are easy to identify, usually because of the clinical history or in some circumstances because of their angioarchitectural appearance. Some angiogenic networks may give rise to a hemorrhagic event, and because of their AVM resemblance, they are referred for endovascular treatment.

5.4.2 Perinidal Angiogenesis

Perinidal angiogenesis can occur is some patients with PAVMs. These perinidal angiogenic areas may make the nidus appear to be enlarged. The difficulty is that if an AVM (nidus) develops (see Chaps. 2 and 6, this volume), it expresses the activity of a given growth factor or factors to achieve an aberrant remodeling program. Since the nidus does not seem to grow under the same conditions and the same pattern as the secondary angiogenesis, it suggests that either the growth factors are different or the receptors have changed or both (Figs. 5.12, 5.13).

5.4.3 Postischemic Luxury Perfusion

Postischemic luxury perfusion occurring in the subacute phase following cerebral infarction may mimic at angiography the appearance of a diffuse type of AVM nidus. Clinical presentation and the normal-size feeding arteries and draining veins will distinguish these two conditions. Conversely, deeply located true AVMs with a small, early draining vein may sometimes have a similar angiographic appearance as postischemic luxury perfusion, except that the revealing symptom will usually be a hemorrhagic episode, which may recur. These ischemic lesions should obviously not be surgically removed or treated by embolization or radiosurgery.

5.4.4 Proliferative Angiopathy

Proliferative angiopathy also belongs to this group, as it combines a diffuse vascular network with moderately enlarged veins not dissimilar to what would be seen in a true AVM. Patients usually do not present with an acute neurological deficit or hemorrhage but more commonly with epileptic syndromes, headaches, and progressive neurological deficits (Fig. 5.14).Angiogenesis is confirmed by transdural supply demonstrated bilaterally, anywhere on the cortex and sometimes infra- and supratentorially. Segmental stenosis of the middle or anterior cerebral arteries can be seen during follow-up. The angiopathy is often mistaken for moy-

Proliferative Angiopathy

307

Fig. 5.12A–E. A 15-year-old girl presenting with a sudden right hemiplegia due to intracerebral and intraventricular hemorrhage. The first angiographic diagnosis, although not typical, was AVM (A–C). She was treated conservatively; she hemorrhaged again a few months later (D, E), which corresponded to typical hemorrhagic angiopathy

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Fig. 5.13A–F. Legend see p. 309

Induced Pial AV Shunts Secondary to Dural Sinus High-Flow Lesions

309

amoya disease (Fig. 5.2) when bilateral and the posterior circulation is spared. However, the pattern of capillary ectasia, the rapid venous filling, and the type of dural angiogenesis is different. This angiopathy is most commonly encountered in Caucasian females (3:1). This group is similar to some of the cases that Chin et al. (1992) described as diffuse nidus AVMs. In his series, six out of 12 patients were children. This entity will be seen with the ischemic diseases in Chap. 18.

5.4.5 Induced Pial AV Shunts Secondary to Dural Sinus High-Flow Lesions

▲

The next group includes induced pial AV shunts secondary to dural sinus high-flow lesions (see Chap. 7, this volume). This group is particular, as these shunts develop over time, usually years, and do not seem to produce any specific symptoms, despite their obvious progression over time (Fig. 5.15). Some regress after partial occlusion of the prominent primary shunts on the sinus wall. Their own natural history is not known, but the persistence of the primary dural shunt seems sufficient to make them more active and create flow-related arterial aneurysms or induce additional lesions. This actually shows how a lesion that is essentially the same will eventually appear worse by the induced effect on a previously normal portion of the vasculature. The secondary occurrence of these pial shunts shows the efficacy of the venous sump effect in creating these lesions upstream and involving the cerebral veins. It seems that the early maturation of the vascular system introduces the low-pressure regimen of the jugular system. Its role in arterial diastolic flow appearance is likely to be important, as shown by its rapid disappearance during crying or other Valsalva maneuvers in babies. The increase in diastolic fraction in CAVM points to the loss of resistance at the capillary level, but also suggests the loss of resistance at the venodural junction; in addition, the loss of normal autoregulation at the shunt site may later involve additional vasculature. This raises the question of whether the failure of the venodural junction to establish an early resistance in otherwise normal dural sinuses might not, through the sump effect, trigger the development of certain superficial AVFs that open directly into the superior sagittal sinus. Some of them, although showing highflow characteristics, are amazingly well tolerated and without any cardiac overload.

Fig. 5.13. A, B A 6-year-old boy presented with a sudden left-sided hemiplegia caused by a ruptured mesencephalie AVM with a cranially located intracerebral hematoma. Angiography demonstrates the small nidus and what seems to be a false sac annexed on the single venous drainage (C, D). Six months later, there was evidence of angiogenesis into the previous hematoma, resulting in a slight enlargement of the draining vein (E, F)

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Fig. 5.14A–E. MRI with coronal (A) and axial (B) views demonstrates typical appearance of abnormal vasculature interspersed with brain parenchyma involving the left parietal lobe, which is of slightly increased signal on T2WI during investigation of a young female with seizure disorder dating from age 15. Angiography of the left internal carotid artery in lateral (C) and frontal (D) views demonstrates a proliferative angiopathy with slow shunting into normal-sized draining veins, while external carotid angiogram in frontal view (E) shows transdural supply to the same lesion

Venous Angiopathy

311

Fig. 5.15A, B. An 11-year-old girl who had presented at the age of 2 years with right proptosis related to an orbital hematoma. Angiography performed at that time failed to demonstrate any intracranial anomaly. Over a period of 10 years, she developed progressive right-sided hemiparesis, dysphasia, and ataxia related to a juvenile type of dural arteriovenous shunt. Although angiography had been normal at the age of 2 at the intracranial cavity, note the remote pial arteriovenous communications induced by the lesion. (From Garcia-Monaco et al. 1991c)

5.5 Angioarchitectural Progression of CAVMs in Children In all AVMs, there are changes that occur in the angioarchitecture of the lesion as time passes, and this is even more apparent in children. Knowledge and understanding of these changes correlate with the natural course of the disease and its symptomatology constitutes a guideline to be used in treatment planning. Similar to VGAMs, or CAVMs in adults, we link the course of the disease to various angioarchitectural characteristics.

5.5.1 Venous Angiopathy

The abnormalities of the venous system are a prominent feature of childhood AVMs (Scheme 5.1A). They can be very obvious and possibly be related to an acute event. They should always be scrutinized with special care, as they are the most active part of an AVM. It is probable that all symptoms before the age of 3 years are venous in origin and it is only much later that some of the more common types of high-flow angiopathy of arterial origin are seen. We have divided the venous features into four main groups that can be differentiated as distinct problems.

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Scheme 5.1a. Venous high-flow angiopathy in cerebral arteriovenous malformations (AVM) in children. AV shunt, arteriovenous shunt. Asterisk, Water retention is found in infants

5.5.2 Dural Sinus High Flow

Similar clinical and imaging findings that occur in primary high-flow dural AVSs, can also be encountered in high-flow pial lesions (Fig. 5.16), provided that the same dural conditions are present (Scheme 5.1B). These hydrodynamic disorders are specific to very young children, prior to the maturation of the Pacchionian granulations. All the events described in infancy involving hydrodynamic failure (see Chaps. 2 and 3, this volume) can occur, including tonsillar prolapse, hydrocephalus, and melting-brain syndrome as soon as venous ischemia starts to develop (see Chap. 2, this volume). Rapid brain destruction can be observed, but this occurs most rapidly at the end of the neonatal period (Fig. 5.17). Careful attention should therefore be paid to any early warning symptoms. Convulsion, which in CAVM indicates a local insult, should lead to urgent management, regardless of the good clinical tolerance. Multiple convulsive episodes often accompany obvious cerebral damage and indicate a melting-brain phenomenon; morphological exclusion of the lesion at this stage will not prevent severe disability.

5.5.2 Dural Sinus High Flow

313

Fig. 5.16A, B. Neonate presenting at birth with acute cardiac failure. Loud intracranial bruit could be heard. Angiography demonstrates a large posterior fossa AVM

Scheme 5.1b. Venous high-flow angiopathy in cerebral arteriovenous malformations (AVM) in children. AV shunt, arteriovenous shunt. Asterisk, Water retention is found in infants.

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Fig. 5.17A–D. Neonate presenting with moderate to severe heart failure demonstrates on nonenhanced CT (A) and enhanced CT (B) severe focal cortical atrophy involving the left temporal/occipital/parietal lobe with abnormal enhancement caused by cerebral arteriovenous malformation (CAVM). One year later following partial embolization that corrected the congestive heart failure (CHF), MRI T1W1 (C, D) showed severe focal cerebral atrophy as well as diffuse ventricular enlargement. The child had persistent neurological deficits and developmental delay

Venous Ischemia and Thrombosis

315

5.5.3 Venous Ischemia and Thrombosis

All possible degrees of venous ischemia can be observed with the severest expression resulting in melting-brain syndrome, which occurs at the end of the neonatal period and during infancy. Subacute brain loss can often be noted in retrospect, as focal ischemia in infants may produce seizures or deficits that can remain limited or can regress if the lesion is quickly managed or if the venous impairment is limited or compensated (Fig. 5.18). The new equilibrium that results from progressive changes in the venous drainage or from successive adaptations to subacute episodes may eventually fail. Under such circumstances, usually in early childhood, hemorrhagic venous infarction will occur. The related deficit depends on the extent of the hemorrhagic infarct, but regression is seldom complete because of the underlying ischemia. Depending on where the thrombosis is located, the infarction may be closely related to the malformation and may eventually lead to its spontaneous exclusion. Infarction may be multifocal, remote, and bilateral if the thrombosis affects the dural sinuses (Scheme 5.1C).

Fig. 5.18A, B. A young girl presented at the age of 9 years with generalized seizures, cerebellar syndrome, and nystagmus. Slight exophthalmia was also detected. Note the focal atrophy

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Scheme 5.1c. Venous high-flow angiopathy in cerebral arteriovenous malformations (AVM) in children. AV shunt, arteriovenous shunt. Asterisk, Water retention is found in infants

5.5.4 Venous Hemorrhage

Venous thrombosis or any other obstacle may also lead to venous rupture, which may be located at some distance from the nidus. In such cases, a false aneurysm of venous origin can sometimes be demonstrated. When extravascular blood is shown, it can point to the exact site of the rupture (Figs. 5.19–5.21). The size of the hematoma is unpredictable, and there is no relationship between the size of the hematoma and the size of the AVM. Since the rupture is venous, in our experience, subarachnoid bleeding under these circumstances is rarely seen alone and subdural hemorrhage can be seen, particularly in infants. The course of such false aneurysms usually involves their partial integration into the venous drainage of the malformation. The hemorrhage usually provokes an isolated seizure, and its repetition can be indicative of an early recurrence, which is not rare in early childhood. The deficit caused by the hematoma tends to resolve without residual neurological impairment. Some permanent sequelae may be seen in very eloquent areas in older children (Scheme 5.1D).

Venous Hemorrhage

317

Fig. 5.19A–D. Neonate presented at the age of 3 days right partial sensory-motor epilepsy. MR examination disclosed a rolandic region arteriovenous malformation that was confirmed by angiography (A, B). An embolization was planned but before the procedure could be performed, the child had an intracranial hemorrhage due to rupture of the lesion (C, D)

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Fig. 5.20A–D. A 9-year-old girl presented with intracerebral hemorrhage and neurological deficit. On MRI T2W1 axial (A) and coronal view (B), it was demonstrated that she had increased signal surrounding a well-defined area of mixed signal (arrows), which at left internal carotid angiography frontal views (C, D) proved to be caused by venous pseudoaneurysm (arrow)

Venous Hemorrhage

319

Fig. 5.21A–D. Unenhanced CT (A, B) demonstrates evidence of recent right cerebellar hemorrhage with defined area of slightly lower hyperdensity (arrow) in a 5-yearold girl. MRI at that time demonstrated the same lesion on T2WI (C) to have a mixed signal but showed homogeneous enhancement (arrow) with contrast (D). E,F see p. 320

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Fig. 5.21E,F. (continued) Vertebral angiogram in frontal views (E, F) showed this lesion to be venous pseudoaneurysm (arrows)

Scheme 5.1d. Venous high-flow angiopathy in cerebral arteriovenous malformations (AVM) in children. AV shunt, arteriovenous shunt. Asterisk, Water retention is found in infants

Venous Enlargement

321

5.5.5 Venous Enlargement

Venous pouches are very frequent in children, since thrombosis and high flow are often present. They are characteristic of CAVFs seen in HHT children (see Chap. 4, this volume). These pouches behave like any large pulsatile mass and may have neurological manifestations, although the ability of the infant’s head to enlarge often allows giant pouches to be diagnosed with almost no mass-related symptoms. Adaptation of the adjacent brain makes these huge pouches rarely directly responsible for symptoms in children. Some subtle deficits can be noted, as well as seizure activity. In our experience, the latter is nearly always associated with a spontaneous partial thrombosis of the pouch. MRI at this point demonstrates an area of signal hyperintensity in the brain surrounding the pouch (Berenstein 1992a). It is of interest to note that the thrombosis of similar pouches induced by embolization does not produce the same perilesional changes, nor does it produce deficit or seizures. Increasing size of these pouches can be observed over time subsequent to the development of restriction of the downstream outlets; it can be difficult to distinguish a giant arterial pouch from a giant venous pouch when located within a nidus (Fig. 5.22). Spontaneous thrombosis of a false sac and the secondary possibilities of angiogenesis within the thrombosed pouch should not be underestimated and therefore followed up (Fig. 5.13; Scheme 5.1E).

Scheme 5.1e. Venous high-flow angiopathy in cerebral arteriovenous malformations (AVM) in children. AV shunt, arteriovenous shunt. Asterisk, Water retention is found in infants

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Fig. 5.22A–D. A, B Right internal carotid artery (RICA) demonstrated slow-flow AVM (arrow, A) draining into a cortical vein (arrows, B) and no filling of the giant distal arterial aneurysm or venous pouch. C, D Three weeks later, the child presented a 2-h episode of transient weakness and numbness involving the left side of his body as well as slurred speech and incapacitating headaches (enhancing portion of the venous ectasia; arrow, D). E–I see pp. 323, 324

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323

Fig. 5.22E–H. (continued) E, F MRI T2 W showed evidence of flow artifact (arrow) as well as slight edema posterior to the giant distal arterial aneurysm or venous pouch. G, H Angiogram at that time demonstrated partial re-opacification of the previously thrombosed giant distal arterial aneurysm or venous pouch (arrow, G), apparently causing worsening clinical symptoms. There is also residual AVM nidus draining into a separate cortical vein (arrows, H). I see p. 324

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Fig. 5.22. (continued) I Obliteration of the entry (arrow) into the giant distal arterial aneurysm or venous pouch resulted in dramatic reversal of clinical symptoms

5.5.6 Arterial Angiopathy

Arterial changes are sometimes observed in older children and rarely in neonates or infants. Localized stenotic or diffuse stenotic changes in our series occurred only after many years (Scheme 5.2A–C). They require a certain degree of angiogenesis, as indicated by the occurrence of a dramatic transdural supply. They have minimal symptoms in comparison to the vascularization status, again indicating the unique level of tolerance of the cerebral tissue in childhood. This contrasts with the obvious vulnerability in the first few years of life. The subclinical course of CAVMs in children comes at the expense of compliance, and as soon as the system fails, the overall equilibrium is difficult to restore. In our experience, headaches in children are often associated with arterial stenosis and rarely with an increase in intracranial pressure. There is no relationship between the transdural supply and headaches. These headaches often indicate a pseudo-migrainous course (Fig. 5.1). As a result of this proximal arterial angiopathy, the brain tissue surrounding the CAVM may produce seizures or deficits. These are usually progressive and while they can be stabilized they are rarely fully reversible, as the subischemic state of arterial origin will not be improved by partial or total exclusion of the lesion. Diffuse arterial involvement is rare and in older children may produce moyamoya phenomena associated with true CAVM (Garcia Monaco et al. 1991c). Arterial enlargement (Scheme 5.2D) can theoretically cause compression, but we have never observed this phenomenon in this age group. We do not believe that it constitutes a morphological goal for partial treatment. Mural (wall) abnormalities are the most important angioarchitectural artery-related characteristic; however, they are extremely rare in children (Scheme 5.2E). Flow-related aneurysms are thought to be caused by the

Arterial Angiopathy

325

Scheme 5.2a. Arterial high-flow angiopathy in cerebral arteriovenous malformations (AVM) in children

Scheme 5.2b. Arterial high-flow angiopathy in cerebral arteriovenous malformations (AVM) in children

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Scheme 5.2c. Arterial high-flow angiopathy in cerebral arteriovenous malformations (AVM) in children

Scheme 5.2d. Arterial high-flow angiopathy in cerebral arteriovenous malformations (AVM) in children

Arterial Angiopathy

327

Scheme 5.2e. Arterial high-flow angiopathy in cerebral arteriovenous malformations (AVM) in children

increased shear forces established on the endothelial cells proximal to an AV shunt, but the time required to overcome the remodeling capabilities of the vessel wall is long, and the individual host response capabilities make this development highly unpredictable (Fig. 5.23). Flow-related aneurysms should be distinguished from extradural and distal internal carotid aneurysms. The latter are exceptional in this age group and even more so in association with a CAVM. Distally or intranidally located arterial pouches are less rare in older children. In our strategy, they will lead to the same therapeutic decisions as in adults. The clinical symptoms that express this type of arterial wall abnormality relate to hemorrhagic events. False arterial aneurysms are very rare in children (Fig. 5.24) and indicate again that most bleeding episodes are due to abnormalities involving the venous system. We know the extent to which high-flow angiopathy can modify the angioarchitecture of a given AVM. Angiogenesis following hemorrhage or ischemia and angiectasia following local arterial steal phenomena as well as stenosis and enlargement of the venous sector following outlet restriction can all be causes of enlargement of an AVM (Fig. 5.21). All types of AVM have a different significance. The differences in the physiology of the various endothelial cells with regard to their resistance or weakness to the AVM triggers makes the natural history of the disease depend on the weakest part and therefore may differ from one AVM to the next. What causes regression is also obscure, and even while thrombosis can be an ongoing process in a CAVM, most AVMs do not thrombose. Associ-

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Fig. 5.23A–C. Young girl, seen for the first time in consultation at 9 years of age, who had suffered a first intracerebral hemorrhage at 2 months of age. This had been reported to be a brain AVM but no treatment was given at that time. At 9 years, she presented a new hemorrhage with a transitory left hemianopsia. Note the intranidal aneurysm (arrow, A) embolized as the priority target (arrow, B, C)

Arterial Angiopathy

329

Fig. 5.24A–D. A 1-year-old child first presented intracerebral hemorrhage opening into the right ventricle requiring subsequent surgical ventricular shunting. There were two recurrent hemorrhagic episodes 5 and 8 days later (A–C). Angiography demonstrates partial thrombosis of the draining vein in a small lenticulostriate AVM with venous false aneurysm. Complete cure by endovascular approach was obtained in one session (D)

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ated hemorrhage or stimulation of healing processes can also induce the thrombosis of a previously demonstrated AVM (Fig. 5.8). Even a stable situation is only a rough appreciation of a slowly evolving process that is beyond our abilities to discriminate. Finally, if certain good reasons can be identified to explain a given outcome (growth, stability, regression), then explaining why this does not occur in other similar cases remains a challenge. Growth through neighboring angiopathic changes and scarring phenomena following acute extravascular events are distinct ways that will modify the CAVM architecture over time.

5.5.7 Spontaneous Thrombosis of Arteriovenous Malformations

Spontaneous thrombosis is a rare progression in CAVM in children, although it has been reported. We have seen several cases of multifocal AVMs in which one shunt was no longer demonstrated as the result of spontaneous thrombosis, while the other remained patent. We have never observed complete and stable occlusion of an isolated non-Galenic AVM. Thrombosis is often seen in large lesions and large venous pouches. Thrombosis of AVMs in children has been proposed to explain the lower proportion of multiple AVMs in adults. As mentioned above, thrombosis is either the expression of the capacity of the endothelial cells to repair or, in contrast, of the endothelium not being able to preserve the normal platelet–vessel wall relationships. When looking at the perilesional extravascular changes associated with spontaneous thrombosis, it is likely that abluminal phenomena interfere as well in the exclusion of some CAVMs. In addition, the concentric nature of some vascular proliferations points to the possible occlusive arterial role played in such rare favorable progression of CAVMs. It is likely, however, that single-hole AVFs are more likely to thrombose than nidus-arranged lesions.

5.6 Objectives of Treatment 5.6.1 Complete Exclusion

Ever since AV shunts were first recognized, the aim to eradicate the lesion has been the only satisfactory goal. This strategy was based on pathological information that tends to demonstrate fixed changes. While complete elimination of a pediatric CAVM is an acceptable goal, it should be considered in the context of the anticipated natural history of the CAVM in a particular child vs the risk of treatment. If the risk of total obliteration is below the estimated natural risk, total elimination of the lesion should be pursued (Figs. 5.25–5.27).Our capacity to exclude AVMs completely has increased,in particular for small lesions that present with intracerebral hematomas (Figs. 5.25, 5.27). However, for more than 25 years, our interventional neuroradiological experience has demonstrated the presence of vascular compliance and adaptability. Progress in biology has also shown that remodeling represents the reconstructive capacity of the vascular system. The recognition of high-flow angiopathy has revealed the participation of the remain-

Complete Exclusion

331

Fig. 5.25A–D. A 12-year-old child presented with sudden headaches due to intracerebral hemorrhage. A, B Angiography demonstrates a micro-AVM. C–E Distal catheterization with a 1.2 microcatheter was achieved, which made it possible to exclude the lesion completely. E see p. 332

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Fig. 5.25E. Legend see p. 331

ing vasculature in the clinical expression of a given lesion. In addition, the importance of the parallel maturation of the surrounding brain in children created the concept of optimal therapeutic timing. Finally, the fact that lesions may not be present at birth certainly further questions the desire to obtain eradication of the AV shunt as the only guarantee of a return to a normal state and protection over time. Such an approach in children is not based on any evidence and on the contrary has often resulted in improper treatment decisions, particularly in young children. The preeminence of the technical challenge to erase any risk and the consequent aggressiveness of the treatment performed has obscured the fact that it might not always be needed immediately and might perhaps be more safely achieved later. Several years ago, staged treatment procedures entered the interventional arena. This represented a progression from palliative to secondarily completed surgery and subsequently to planned staged procedures. Little attention was paid to the recovery of the vascular system, and the challenge to achieve total eradication precluded recognition of the reconstructive results obtained. Interventional neuroradiological experience with CAVM management has demonstrated the validity of the following concepts:
There is more than a semantic difference between staged, partial, and palliative treatment.
The desire to rapidly obtain a complete exclusion of the AVM is often a compulsory objective, which may indicate a failure of analysis to understand and predict the spontaneous outcome in a given patient.
Incomplete exclusion does not mean the absence of treatment.
Postsurgical remnants do not have the same significance as partially embolized lesions.

Complete Exclusion

333

Fig. 5.26A–D. A 14-year-old boy presenting with a brutal left hemiplegia associated with IVth nerve palsy and Parinaud syndrome. CT and MRI (A, B) disclosed a right quadrigeminal hematoma. Although the images are suggestive of cavernoma, the axial cut demonstrates a small network on the tegmental portion of the mesencephalon. Selective arteriography demonstrates an arteriovenous malformation (C, D). E–G see p. 334

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Fig. 5.26E–G. (continued) Selective injection into the feeder allowed glue deposition (E). Postembolization follow-up after a few months demonstrates complete stable occlusion of this mesencephalic AVM (F, G)

Complete Exclusion

335

Fig. 5.27. A, B A 6-year-old child presenting with an intracerebral hematoma resulting in an incomplete hemiparesis. B–D Following embolization in one session, the entire lesion was excluded. Clinical recovery has started


The endovascular approach to CAVMs provides a wider range of options, both in the degree of completeness and the timing of treatment, and more so than any other traditional treatment modality.
The complete disappearance of a lesion at imaging follow-up is reliable.
Total stable exclusion of an AVM does not require secondary removal for preventive purposes.
Embolization is a generic name that encompasses many different practices, objectives, and results.

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5.6.2 Partial Treatment

In our practice, the goal of treatment in children has become the preservation of normal neurocognitive maturation as well stable protection from acute episodes. In most instances, the morphological goal can be superimposed on the clinical goal. In babies, however, as seen in VGAM, these objectives can be separate in time or even contradictory, if the attempt to obtain a cure compromises neurological outcome. Staged treatment is the planning of steps to reach a more favorable situation and to achieve an exclusion with lower morbidity than if it was accomplished in a single session. Palliative treatment is an incomplete exclusion of a lesion in order to stabilize a critical situation. Partial targeted treatment is an incomplete exclusion motivated by a clinical concern requiring improvement and directed toward a specific portion of the lesion when complete exclusion cannot be offered with an acceptable level of risk. It has a clinical objective and, in contrast to the palliative objective, its results are morphologically and clinically identifiable and can therefore be evaluated (Fig. 5.28). A certain group of patients have not yet completed the embolization treatment, making up a new population of patients who did not exist as such in the past. Some are still under treatment (staged), and one may ask why the treatment is not continued more rapidly. The decision to stage a procedure carries some significant advantages, particularly in children, where the length of the procedure is limited by puncture time or fluid volumes. In addition, with the hemodynamic triggers being modified, the correction of some disorders induces a normal, although delayed maturation. In this group, the problem is the time between two consecutive sessions. There is no definitive optimal schedule; however, with experience each interventional neuroradiologist knows whether a better technical result can be achieved by waiting for a few weeks or months. This strategy will permit a rearrangement of the remaining anatomy, and some areas of induced angiogenesis may regress, whereas some smaller feeders may enlarge, permitting easier catheterization. This will have to be balanced with the hemodynamic changes induced by embolization and hemodynamic needs, to ensure a proper or preserved maturation process. There are a number of patients who cannot be cured even with the current treatment options and capabilities, either because the lesion cannot be reached or because the disease is multifocal. In this subgroup, treatment is partial and is repeated in time with long intervals between sessions. We do not perform palliative embolization in children with AVM. The aim of partial treatment is to eliminate dangerous portions of the AVM (intranidal aneurysms, false aneurysms seen following a hemorrhagic episode, and venous ectasias [Figs. 5.24, 5.28]) or its effects on the adjacent brain (venous congestion, venous thrombosis) or to reduce seizure activity, progressive deficits, or headaches (Figs. 5.29, 5.30). In some instances, this targeted embolization deals with a dangerous part of the lesion prior to the irradiation of the remainder, to avoid repeated hemorrhage during the 2-year interval and to reduce the size of the target further (Figs. 5.33, 5.34). In our experience, partial targeted embolization

Partial Treatment

337

Fig. 5.28. A, B An 8-year-old boy presented with sudden intracerebral hematoma resulting in right-sided hemiparesis and hemianopia. C, D The presence of an intranidal aneurysm prompted partial targeted embolization prior to discussing further management. Clinical recovery is incomplete

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Fig. 5.29. A–C A 5-year-old child had had a progressive motor deficit in relation to large multifocal AVMs located in the brain stem since the age of 2 years. Following four distal glue deposits in three sessions (D–F), although the angiographic changes were not spectacular, the clinical improvement was dramatic

Partial Treatment

Fig. 5.30A–E. Legend see p. 340

339

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Fig. 5.30. A, C Deep-seated AVM located in the head of the caudate nucleus and revealed with an intraventricle hemorrhage (A frontal, B early, and C late lateral views). D Distal selective catheterization of the Heubner artery allowed the embolization, thus disconnecting 90% of the lesion (E–G)

is an acceptable therapeutic objective only if a complete cure cannot be obtained at a satisfactory level of risk and if the procedure is performed with a permanent agent, such as NBCA. This means that we aim to obtain – by endovascular or other techniques – total exclusion if a good neurological outcome can be guaranteed. The fact that most lesions in patients referred to us are large or multifocal explains the small number of complete cures in our series.

5.6.3 Neonates and Infants

Treatment objectives in this age group are the same as in VGAM; however, the insult to the cerebral tissue is more rapid, as the venous drainage is usually impaired, and collateral venous circulation is compromised, using as alternative drainage toward subpial veins in most instances. The poor neurological prognosis forces us to try to achieve a significant reduction of the shunting more rapidly. Early management is, therefore, not so much motivated by the CCF, which is usually mild to moderate, but by the possibility of ensuing irreversible cerebral damage. The patients should be evaluated without angiography in order to assess the degree of interference between the AVM and the brain tissue, while rapidly scheduling the first embolization session, almost regardless of the existing symptoms. If the CCF is severe, the prognosis is extremely poor, since it combines both systemic and subpial effects (Fig. 5.17).

5.6.3.1 Hydrodynamic Disorders

341

Table 5.2. Pial AVMs in children (<16 years): clinical presentation in neonates Cardial overload Hemorrhage Incidental

50% 37.5% 12%

Table 5.3. Pial AVMs in children (<16 years): clinical presentation in infants Hemorrhage Macrocrania Cardiac overload Deficit Epilepsy Incidental

30% 26.6% 23.3% 6.6% 6.6% 6.6%

Convulsion is a major symptom and should point to the need for rapid treatment, even if the convulsion remains isolated and without permanent clinical effect (Tables 5.2, 5.3). In the series of Rodesch et al. (1995a), CAVSs had a poorer prognosis than VGAMs when the onset of symptoms was at neonatal and infant age. Sixteen neonates or infants were embolized as the primary modality of treatment and four of these eventually died. One died due to multiorgan failure, one following a complementary surgical approach, one from hemorrhage after incomplete treatment (three sessions) for a multifocal perimesencephalic AVM, and one from a posterior fossa hemorrhage despite complete occlusion of the AVM. Eight out of 12 had a normal neurological status (scores of 5, 4, or 3), and the remaining four had a score of 2. Eight patients had surgical resection of their CAVS as the first (and only) treatment modality; seven of them were older than 2 years of age at the time of surgery. All patients had their AVM removed and all are still alive; two out of eight have moderate permanent neurological deficits.

5.6.3.1 Hydrodynamic Disorders

Possible hydrodynamic disorders should be managed early through reduction or occlusion of the AV shunt. Even if pial lesions in infancy present features that simulate the VGAM pattern, symptoms are significantly different, rarely causing hydrodynamic disorders, but frequently focal neurological symptoms and hemorrhage. CAVMs rapidly produce local brain atrophy (focal melting-brain syndrome) (Fig. 5.17). This atrophy represents the subacute local effect of abnormal hydrodynamics induced by surrounding pial venous congestion. Dural sinus hyperpressure (Quisling and Mickle 1989; Zerah et al. 1992) can induce reversible tonsillar prolapse (Girard et al. 1994), which expresses the posterior fossa hydrovenous disorders (Andeweg 1989). Special attention must be paid to the venous drainage of the brain at each session in order to follow the maturation of the various outlets and their patency.

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5.6.3.2 Multiple Arteriovenous Malformations

Therapeutic decision-making is usually complex in children with multiple AV shunts and should be approached on an individual basis (Iizuka et al. 1992; Willinsky et al. 1990a). At neonatal age, the most prominent shunt should be attacked first, as well as the shunt that gives rise to the most prominent pial congestion, in order to obtain systemic relief and brain drainage improvement.

5.6.4 Children

The clinical history in combination with the MRI and angiographic findings help determine which lesion or lesions cause symptoms and therefore need prompt treatment (Tables 5.4–5.8). For CAVMs other than the AVF and multiple AV shunts, the rules of management are similar to those in adults (see Berenstein 1992a). When reading the literature, it seems that the expected bleeding rate reduction is the only indicator for successful treatment. It is our experience that CAVMs do not bleed more frequently in children than in adults, while on the other hand cerebral damage and the ongoing risk of seizures constitute a major restriction for schoolchildren and adolescents.

Table 5.4. Pial AVMs in children (<16 years): clinical presentation in children Hemorrhage Epilepsy Deficit Headaches Incidental Cardiac overload Mental retardation Macrocrania Other

50% 16.6% 15% 7.7% 3.3% 2.2% 1.6% 1.1% 2.2%

Table 5.5. Cerebral arteriovenous malformations in children (<15 years) in Japan, 1986–1988 (Tamaki 1992) Patients Neonatal hemorrhages CAVM (all pial) Idiopathic Coagulation disorders Ruptured aneurysms Tumor Occlusive disease Total

(n)

(%)

432 125 101 61 27 13 10 769

56.2 16.3 13.2 7.9 3.5 1.6 1.3 100

Children

343

Table 5.6. Classification of seizures I

II

III IV

Generalized seizures Bilaterally symmetric and without focal clinical onset Tonicoclonic seizures (grand mal) Isolated tonic or clonic seizures Bilateral myoclonus Infantile spasms Atonic or astatic seizures (infants and children) Absences Simple (petit mal) Complex (with various symptoms) Myoclonic Tonic, atonic With automatisms With autonomic (visceral) symptoms Partial seizures (seizures beginning locally) Simple seizures, generally without loss of consciousness Complex seizures with loss of consciousness Partial seizures with secondary generalizations Unilateral seizures (infancy) concerning only one cerebral hemisphere

Table 5.7. Various types of partial seizures Type of seizure Simple seizures Motor seizures Dysarthria, jacksonian seizures Non-jacksonian seizures Adversive seizures Masticatory seizures Sensory seizures Somatosensory seizures Visual seizures Auditory seizures Olfactory seizures Gustatory seizures Vertiginous seizures Abdominal pain Vocal Phonatory seizures

Site

Prerolandic gyrus Frontal cortex Amygdaloid nucleus Postrolandic gyrus Occipital or temporal cortex Temporal cortex Mesial temporal cortex Insular cortex

Inferior rolandic cortex or supplementary motor cortex Posterior temporal or inferior frontal cortex

Aphasic seizures Complex seizures Psychomotor automatisms Temporal cortex Psychosensory automatisms Intellectual seizures (dreamy states, depersonalization) Affective seizures (joy, sadness, fear, hunger, déjà vu impression)

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Table 5.8. Hemorrhagic episode in cerebral arteriovenous malformations in children and adults (Celli et al. 1984)

Frequency Mortality Coma Immediate morbidity Ventricular hemorrhage

Children (%)

Adults (%)

55–77 7–13 23–31 78–89 56

37–41 3–10 11–17 50–53 40

These symptoms will interfere with the future quality of life to a great extent and are not as such fully appreciated by the Glasgow Outcome Score. Failure to thrive, mental retardation, physical atrophy, and facial collateral circulation all reflect irreversible changes that have been the result of active treatment. It has not been our experience that symptoms worsen at the time of puberty. Headaches may sometimes start at that time, but either they reveal an already large lesion or this is a retrospective finding in an incidentally discovered AVM at adult age.

5.6.5 Rebleeding

Rebleeding occurrence is an important point, since the delay between embolization sessions can be variable. During a 12-year period, the rebleed rate in embolized pediatric CAVMs seems to be low, except in large deeply located lesions that were poorly controlled. This empirical statement also illustrates the fact that hemorrhagic episodes are often difficult to identify in the past history of children. The information from the literature is also difficult to interpret. For example, Hladky (1994) reported that a hemorrhage occurred at the former AVM site in 5.7% of CAVM patients believed to have been successfully treated surgically. In our series of CAVM patients waiting for embolization, three children bled and one rebled. One of the former three suffered delayed hemorrhage 1 month before his scheduled first session of embolization. Two of the three patients (one with a diencephalic AVM and one with a mesencephalic AVM) bled between the third and fourth sessions. The first of them, who was initially not operable, was subsequently successfully operated on and had a moderate residual sensory motor deficit; the second had a nonoperable AVM and died from the hemorrhage. The fourth patient died from a recurrent hemorrhage 5 years after the first bleeding episode and 1 year following the embolization session, in which incomplete occlusion had been achieved. Our group had felt that the therapeutic risks involved in completing the treatment by any method were too high.

Surgery

345

5.7 Technical Management 5.7.1 General Remarks

When discussing partial or complete endovascular exclusion in CAVM patients, we are referring to transarterial embolization with glue. From published and unpublished experience in CAVM in children,coils,particles,balloons, cocktails, threads, collagen mixture, and other methods have shown no reliable and predictable results, even if they were useful in some isolated situations, nor are they safer. In our experience, they have never constituted an improved embolic agent to reach the therapeutic goal, nor are they a satisfactory alternative as a primary embolic agent. It must be emphasized that frequent changes in the type of embolic material used have been a significant hindrance for many teams in their attempts to increase their technical experience and develop a reliable follow-up with a given agent. Our technique is the same as the one described in Chap. 3 of this volume. Complete exclusion,if it can be obtained,is the goal (Figs. 5.30,5.31),but can not be achieved as frequently as in VGAMs. Even if endovascular management is the primary choice, complementary treatment is usually planned (see Sect. 5.3.2). The basic technical challenge consists in occluding the arterial part of the nidus with the immediate portion of the draining vein in AVFs. The entire nidus demonstrated may not have to be occluded, as secondary regression of other supplies can sometimes be seen in young children. Superselective injections are rarely helpful in making this decision. The dangers related to the venous passage of glue and possible subsequent hemorrhage depends on the converging or diverging position of the venous outlets. Multiplicity of the nidal veins and the length of the course in the subpial compartment indicate the distal point of possible venous occlusion. In addition, one should never forget that children with CAVMs, in particular those who are known to have HHT disorder, also need management of their associated vascular disease, such as the pulmonary AVSs, which can be a major cause of neurological sequelae (Fig. 5.32).

5.7.2 Other Techniques 5.7.2.1 Surgery

Interpretation of published results is very difficult, since the age limits include children up to 20 years. In our review of several series between 1941 and 1990, 80% of children were operated on and approximately 65% had complete exclusion of their lesion. In a more recent review (Hladky 1994) of 62 cases admitted between 1975 and 1992, 75% eventually had complete exclusion of their malformation with a very good neurological outcome. This is superior to all previously published management data: a mortality rate of 7.6% and a recurrence rate of 5.6% was reported. Epilepsy occurred in 14.8% of patients after surgery, although it was not present prior to surgery; it was felt that it was an acceptable drawback. Reviewing the latest series, the mortality rate in nonoperated patients varies from 20% to 57%. These numbers are particularly high considering that there were few young children in these series (Table 5.9).

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Fig. 5.31A–C. A 14-year-old girl presenting with sudden headaches with a moderate right upper limb deficit. CT (A) revealed a subcortical parietorolandic hematoma.Angiography disclosed a parietal arteriovenous malformation (B). We decided to follow up the patient after resolution of the hematic collection in order to better visualize the malformation and to attempt the endovascular approach during the same session. This was done 2 months later. The lesion was embolized with glue (C), resulting in the total elimination of the nidus

Surgery

347

Fig. 5.32A–D. This 23-month-old girl presented with congestive heart failure (IVC, pulmonary stenosis), mental retardation on the Denver score (<20%), and progressive left hemiparesis, leading to the diagnosis of PF AVFs. MRI (A, B) and angiography (C, D) demonstrated three AVFs in the right parietal temporal cortex and brain stem. The brain stem lesion was of the AVF type, fed from the basilar tip. She had no significant family history, but was highly suspected of having HHT1 on the basis of multifocality and fistulous architecture. The fistulas were embolized in three sessions, four feeders were occluded with N-Butyl CyanoAcrylate (NBCA), and the fistulas were reduced to 50% over a 1-year period (E–I). Another session was proposed 1 year later, but her family refused further treatment. The child unfortunately had an ischemic stroke related to a pulmonary AVF and died 14 months after the last embolization, confirming the diagnostic suspicion of HHT1. E–I see p. 348

348

5 Cerebral Arteriovenous Malformations

Fig. 5.32E–I. Legend see p. 347

1968–1985

1941–1989

16 17

16

18 15 15 ? 15

16 15

17

16

18

18

20

Gerosa et al. 1981 Eiras et al. 1987

Fong and Chan 1988

Amacher et al. 1979 Celli et al. 1984 Yasargil 1988 Martin 1989 Mori et al. 1980

Mazza et al. 1983 Lapras et al. 1990

Humphreys 1989

Partington et al. 1989

Garza-Mercado et al. 1987 Malik et al. 1991

Laine et al. 1981

1950–1980

1985–1988

1954–1986

1971–1982 ?

? 1951–1980 ? ? ?

1971–1987

1954–1979 1975–1985

Upper Study age period limit (years)

Authors

20

46

19

12

100

24 65

20 19 60 35 28

39

20

27

12

12

72

18 62

20 11 60 35 18

27

38 14

(n)

(n) 56 17

Operations for CAVM/VGAM

Patients

12

23

3

11

43

15 26

15 6 54 30 –

23

17 9

60

85

25

92

60

83 42

75 55 90 86 –

85

45 64

Neurologically normal (n) (%)

4

2

4

1

23

1 25

1 5 6 1 –

3

6 2

20

7

33

8

32

6 40

5 45 10 3 –

11

16 14

Neurologically abnormal (n) (%)

Patients with total exclusion

Table 5.9. Review of the literature on surgical treatment of pial arteriovenous malformations (Lasjaunias et al. 1995)

4

2

4

0

6

2 6

0 0 0 1 3

1

3 0

(n)

20

7

33

0

8

11 10

0 0 0 3 17

4

8 0

(%)

Operative mortality

Over 19 patients below 16 years; only four were cured and neurologically normal out of seven surgically treated

Total actually 65, but two had VP shunts only and one had embolization (excluded) Figures vary in text; 74 patients but only 72 accounted for; 54 removals of AVM; no distinction made between TE and PE; all cases taken to be TE Stereotactic surgery; includes cavernoma and venous angioma

Ages not stated Some discrepancy between tables and text

Partial treatments included Partial treatments not included No distinction made between TE and PE; all cases taken to be TE

Remarks

Surgery 349

19

18

Nelson et al. 1992 alone or combined Ventureyra and Herder 1987

1941–1990

?

636

23

13

15

(n) 25

Patients

7 9

388

10 11 18

510

66

50

64

70

7

(n) 25

89

3

–

0

17

16

–

–

Neurologically abnormal (n) (%) 2 8

Patients with total exclusion Neurologically normal (n) (%) 23 92

Operations for CAVM/VGAM

39

3

1

3

(n) 0

8

16

9

30

(%) 0

Operative mortality

22% Of lesions were occult; full activity is counted as normal; in this group some children had had lobectomy or chronic epilepsy 112 counted as TE and neuro logically normal

No distinction made between TE and PE; all cases taken to be TE Computation of percentage not accurate Surgery alone, embolization

Remarks

AVM, arteriovenous malformation; CAVM, cerebral AVM; VGAM, vein of Galen aneurysmal malformation; TE, total exclusion; PE partial, exclusion; VP, ventriculoperitoneal shunt.

15–20

1975–1985

15

Suarez and Viano 1989

Total

1978–1990

19

Tamaki et al. 1991

1970–1990

Upper Study age period limit (years)

Authors

Table 5.9. (continued)

350 5 Cerebral Arteriovenous Malformations

▲

Fig. 5.33A–F. A 10-year-old female presented with intracerebral hemorrhage and neurological deficit. The left internal carotid angiogram frontal view (A) and lateral view (B) showed that she had a moderate-sized medial left frontal parietal AVM, which was embolized to reduce the size, as shown on the follow-up angiogram, frontal (C) and lateral (D) views, which was then radiated. One year after radiosurgery, she had a second hemorrhage resulting again in neurological deficit. She underwent surgical removal of the AVM, as shown on follow-up angiogram, frontal (E) and lateral (F) views. She has made near complete recovery

Surgery

Fig. 5.33A–F. Legend see p. 350

351

352

5 Cerebral Arteriovenous Malformations

Combined approaches, including presurgical embolization, will depend on the availability of expertise in a given institution (Fig. 5.33). The number of postoperative epilepsy cases is high and could possibly be reduced with presurgical embolization. An obvious indication for surgery is still the removal of large hematomas with an unstable clinical status or a lesion that cannot be reached by catheterization. Obviously, technical skills vary between individuals performing the embolization, as they do from one surgeon to another. In young patients, we favor the combination of embolization plus surgery, as the vulnerability to radiation is high in children.

5.7.2.2 Radiation Therapy

There are few reports of radiotherapy in this age group (Shin et al. 2002; Smyth et al. 2002).We have used radiation in combination with embolization after control of demonstrated weak portions of the lesions in a few cases (Figs. 5.28, 5.34) and exceptionally as the primary form of treatment (Fig. 5.35). Its indications in this age group are certainly limited. Among such indications, we have to consider are the nonfeasibility of other techniques, the maturation stage of the brain, and the risks associated with conservative treatment. We tend to discuss radiation therapy in adolescents rather than young children in view of the risk involved on a maturing brain (Table 5.10). Some lesions such as hemorrhagic angiopathy, mimicking CAVM and presenting with subcortical hemorrhage, should be irradiated following angiography and possible targeted embolization (Fig. 5.36). On the other hand, proliferative angiopathies and most CAMSs should not be treated with radiation (Fig. 5.37), as eloquent brain is intermingled with the vascular spaces (see Chaps. 6 and 18, this volume).

Radiation Therapy

Fig. 5.34. A, B Typical partial targeted embolization directed to a false aneurysm at the acute stage in a ruptured brain AVM. C Angiogram after embolization. Secondary management can then be discussed, whether conservative or radiation therapy

353

354

5 Cerebral Arteriovenous Malformations

Fig. 5.35A–D. A 9-year-old girl presented with small left thalamic and intraventricular hemorrhage and made a full neurological recovery. Left internal carotid angiogram in lateral (A) and frontal (B) views demonstrated small AVM within the medial aspect of the thalamus. Stereotactic radiosurgery was performed and 2 years later the follow-up angiogram in lateral (C) and frontal (D) views demonstrated obliteration of the AVM. E,F see p. 355

Radiation Therapy

355

Fig. 5.35EF. (continued) MRI prior to (E) and 2 years after radiosurgery (F) also shows the impact of radiosurgery

Table 5.10. Review of the literature on radiotherapy of pial arteriovenous malformations Authors

Upper age limit (years)

Study period

Patients

Total exclusion NeuroNeuro logically logically normal abnormal (n) (%) (n)

Operative mortality (%)

Remarks

(n)

Operations for CAVM/ VGAM (n)

In another 11 patients, no angiography was performed One patient not yet scheduled for angiography In six patients, no angiography was performed 18 Patients with no FU angiography

Altschuler et al. 1989

18

1987–1988

18

18

–

3

17

0

Loeffler et al. 1990

15

1986–1988

5

5

–

3

60

0

Colombo et al. 1989

18

1984–1989

24

24

–

11

46

0

1984–1989

47

47

–

17

60

0

Total

AVM, arteriovenous malformations; CAVM, cerebral AVM; VGAM, vein of Galen aneurysmal malformation; FU, followup.

356

5 Cerebral Arteriovenous Malformations Fig. 5.36A–E. A 10-year-old girl with sudden headaches with aphasia and right-sided hemiplegia. A CT shows a subcortical hematoma. The hematoma was removed surgically, resulting in good clinical recovery: slight underuse of her right upper limb was noted, but right-handed writing remains. B, D CT and angiography suggest hemorrhagic angiopathy, with typical subcortical nidus and small draining vein. Partial targeted embolization on the medial aspect of the nidus was done. Radiotherapy was organized 2 months later and 12-month follow-up angiogram failed to demonstrate any residual lesion (D, E)

Radiation Therapy

Fig. 5.37A–B. A 10-year-old boy presented when 7 years old with a subarachnoid hemorrhage attributable to a ruptured arteriovenous malformation located on the internal face of the frontal lobe under the rostrum of the corpus callosum beneath the lamina terminalis (A, B). C,D see p. 358

357

358

5 Cerebral Arteriovenous Malformations

Fig. 5.37C,D. (continued) No endovascular approach could be performed because of the multiple small vessels vascularizing the lesion. The patient was scheduled for radiotherapy. Two years after the radiosurgery (linear accelorator, Lineac), the patient underwent a new angiographic follow-up that demonstrated the complete exclusion of the arteriovenous malformation (C, D). Six months after the radiosurgery, the patient presented right blindness with no intracranial hypertension, from which he has not recovered

6 Cerebrofacial Arteriovenous Metameric Syndrome

6.1

Introduction 359

6.2 6.2.1 6.2.1.1 6.2.1.2 6.2.2 6.2.3 6.2.4

Clinical Manifestations 374 Retinal AVMs and AVMs Along the Optic Nerve and Chiasm 374 Retinal AVMs 374 Optic Nerve and Chiasmatic AVMs 376 Cerebral AVMs 376 Facial AVMs, Nasal AVMs, and Mandibular AVMs 382 Investigation for CAMS Patients 384

6.3

CAMS and Angiogenic Activity 384

6.1 Introduction As already stressed in the previous chapters, the generic name CAVM encompasses various entities that, although treated with the same tools, are completely different disorders. The target and the timing of the primary impact are likely to provide some insight into the understanding of what were believed to be random associations of multiple AVMs. The historical descriptions of cerebrofacial-associated lesions have resulted in the identification of classic syndromes: Wyburn-Mason, Bonnet-DechaumeBlanc, Sturge-Weber, all of them involving the orbit (Fig. 6.1). The condition of retinal arteriovenous malformation was first described by Magnus in 1874 and was long regarded as a mere ophthalmological curiosity. In 1932,Yates and Payne described a patient with retinal and cerebral AVMs, but based on a single patient could not identify a syndrome. An association between arteriovenous malformations of the face, retina, and brain was first recognized by Bonnet, Dechaume, and Blanc, in Lyon, France, who reported two cases in 1937. Six years later, at Queen Square in London, Wyburn-Mason reviewed all cases previously described and added nine further examples in a detailed study. The association of retinal, facial, and cerebral vascular malformations became known as Bonnet-Dechaume-Blanc syndrome in France and continental Europe, and as the Wyburn-Mason syndrome in the English literature. The degree of expression of the syndromes’ components varies, both clinically and morphologically. Thus the most fully expressed cases have maxillofacial AVMs, in addition to the orbital and intracranial lesions, and are susceptible to life-threatening epistaxis or gingival bleeding in addition to the risks of blindness or cerebral hemorrhage. Some confusion has existed regarding the use of the two names, the term “Bonnet-

360

6 Cerebrofacial Arteriovenous Metameric Syndrome

Fig. 6.1. Schematic drawing showing potential zones of involvement: I, facial; II, orbital; III, cerebral. Locations of lesions within zones: 1, cutaneous; 2, maxillofacial; 3, retina; 4, optic nerve; 5, hypothalamus/chiasm/ hypophysis; 6, thalamus; 7, occipital lobe; 8, midbrain; 9, cerebellum. (From Bhattacharya et al. 2001)

Dechaume-Blanc” sometimes being preferred for the more extreme end of the disease spectrum, which includes high-flow maxillofacial AVMs. Careful reading of the original articles, however, confirms that both syndrome descriptions referred to the same condition. The two eponyms of the syndrome can thus be used interchangeably. The syndrome is usually classified together with the neurocutaneous syndromes or phakomatoses (neurofibromatosis, Divry-van Bogaert syndrome, Sneddon syndrome, or tuberous sclerosis). This classification, however, tells us more about our inclination to classify than about the nature of the condition itself, the various phakomatoses being of very different morphology and etiology. Unlike neurofibromatosis or tuberous sclerosis, an inherited basis for CAMS has never been described. This does not exclude this possibility, but the absence of a family history with similar AVMs makes a lesion arising downstream from a germ-line disorder more likely. Although a very rare condition, it still offers insight into the development of AVMs in general and the underlying segmental structure of the developing vasculature of the brain and face. Few descriptions of the syndrome were made with full access to modern imaging techniques. Moreover, other than the original descriptions (of nine and two cases) and two other reports of three and two cases, all the remaining descriptions were based on single case reports. In reviewing our series of 15 cases, Bhattacharya et al. (2001) derived new diagnostic criteria as an aid to diagnosis. Underlying patterns of involvement reflecting the segmental nature of the cerebrofacial structures were found, supporting a disorder of neural crest development (Fig. 6.2). When comparing our findings with previously published cases, we propose a new rationale for the classification of the syndromes.

Introduction

361

Fig. 6.2A, B. Schematic aspect of cephalic ectomesoderm. Migrating cells: phenotypic acquisition. A Neural crest vascular components: during their migrating process, a progressive modification occurs until the cell line becomes committed to a certain cell type. The same applies to cephalic mesodermic cells; even though they originate from regionalized mesoderm, endothelial cells acquire phenotypic specificity during their migration. B Process by which migrating cells acquire (selection) a place and a role by establishing a relationship with the environment. ML, medial/lateral; CC, cranio/caudal; VD, ventral/dorsal

The segmentation, under the control of the hox genes, of the rhombencephalon into rhombomeres (Orr 1887) and forebrain anlage into prosomeres (Lumsden 1989) has been substantiated in birds, mice, and other animals and extrapolated to humans (Puelles and Rubinstein 1993). Following Le Douarin’s (1997) introduction of the quail-chick chimera system in 1969, which provides a system for labeling cells in avian embryos and then following their migration to their definitive sites, studies revealed the metameric nature of brain and craniofacial structures deriving mainly from the neural crest and plate. The initial process of vessel formation in the embryo, known as

362

6 Cerebrofacial Arteriovenous Metameric Syndrome

vasculogenesis, involves differentiation and sprouting of mesodermderived endothelial cells to form the primitive capillary network, which is then extended and remodeled by angiogenesis (Le Douarin et al. 1997). These primary capillary vessels become progressively ensheathed by differentiating smooth muscle cells. It is now recognized that while head and neck endothelial cells, as elsewhere, derive from mesoderm, the tunica media of these vessels differentiates from neural crest cells (NCCs) (Risau 1997), which stream into the developing head and pharyngeal arches. Hox gene-encoded positional information in the crest cells is known to be involved in patterning of the pharyngeal arches and is most likely involved in determining NCC distribution among the arch-derived arteries as well. The work of Couly and Le Douarin has further shown that the neural crest and mesodermal cells originating from a given transverse (metameric) level of the embryo finally occupy the same territory in the head, and that these embryonic tissues are regionalized in various areas devoted to providing blood vessels to specific regions of the face and brain (Couly et al. 1995), (Etchevers et al 2001). Fate maps of the cells occupying these regions of the neural plate, crest, and cephalic mesoderm, in these avian experiments, reveals striking similarities to the distribution of lesions encountered in the human Wyburn-Mason syndrome: for example, the region of the anterior lip of the neural plate contains the anlage of the hypothalamus (closely related to the adenohypophysis) and the skin of the future nasal region. Similarly, ablation experiments of the anterior rhombencephalic neural crest are associated with absence of development of the mandible. A somatic mutation developing in the region of the neural crest or adjacent cephalic mesoderm prior to migration could be expected to produce malformations with a segmental distribution in a similar fashion to Cobb’s syndrome in the spine (metameric AVMs of the spinal cord and cutaneous involvement of the related dermatome: SAMS (see Vol. 2, Chaps. 11 and 15, this volume). We have proposed the name cerebrofacial arteriovenous metameric syndrome (CAMS) for this condition (Bhattacharya et al. 2001). We identified subgroups of patients within a spectrum of segmental craniofacial AVMs (Table 6.1). This disease spectrum finds its origin related to the neurosensorial placodes, as schematically illustrated in Fig. 6.3.
CAMS 1: A midline prosencephalic (olfactory) group with involvement of hypothalamus (hypophysis) and nose (Fig. 6.4).
CAMS 2: A lateral prosencephalic (optic) group with involvement of optic nerve, retina, parietal temporal occipital lobes, thalamus, and maxilla (Fig. 6.5).
The mesencephalic crest does not appear to reach facial expression and lesions here would not be expected to result in a cerebrofacial syndrome.
CAMS 3: A rhombencephalic (otic) group, with involvement of cerebellum, pons, petrous bone, and mandible (Fig. 6.6).

Introduction

363

Table 6.1. Proposed scheme of transitory topographic distribution of vascular lesions in CAMS 1–2, CAMS 3, and SAMS 1–31 (Wong et al. 2003) Metameric Type / Territories involved

CAMS 1, 2

CAMS 3

SAMS 1–31

CNS AVMs

S/pial S/arach

+ + At least VIIIth nerve

+ + Radicular nerves

PNS

–

+ – Only Ist and IInd nerves are involved, but they are subpial + If Ist and IInd nerve are excluded – + Nose, maxillae, ethmoid, and sphenoid + +

+ At least VIIIth nerve

Spinal nerves

Dura Bone

Muscles Skin

– +

+ +

– + Mandible, petrous and basiocciput + +

Vertebrae and ribs

CNS, central nervous system; PNS, peripheral nervous system; S/arach, subarachnoid compartment; –, not present; +, present.

Fig. 6.3. Schematic representation of the cerebrofacial arteriovenous metameric syndromes (CAMS). (From Bhattacharya et al. 2001). The proposed metameric disease groups (CAMS 1–3) are shown by their main areas of involvement. Note also from the drawing that the upper cervical Cobb syndrome simply represents the caudal extension of the same disease spectrum: SAMS (spinal arteriovenous metameric syndrome) 1

A more extensive insult would be expected to overlap territories, producing a complete prosencephalic phenotype (CAMS 1+2) (Fig. 6.7) or bilateral involvement (CAMS 2) (Fig. 6.8). Of course, the disease spectrum could be incomplete, either because some cells are spared or because they have not been triggered to reveal the disease. The insult producing the underlying lesion would have to develop before the migration occurs and thus before the 4th week of development. This supports the concept that sporadic brain AVMs could have a similar early initiating cause, but which may not be morphologically revealed for several years (Lasjaunias 1997).

364

6 Cerebrofacial Arteriovenous Metameric Syndrome

Fig. 6.4. A CAMS 1. This 49-year-old man was admitted to his referring hospital with severe epistaxis. He had been noted at birth to have an angioma of the nose, which had enlarged gradually in recent years (B). He was otherwise well, with normal vision and retinoscopy. He was referred for embolization of this lesion. External carotid angiography demonstrated a midline nasal and alar AVM (C) fed by both facial arteries. Internal carotid angiography revealed an additional AVM of the floor of the third ventricle involving the optic chiasm and hypothalamus (D, E)

Introduction

365

Fig. 6.5A–D. A 12-year-old boy presented with headaches and sensitive seizures in the left superior limb treated by Depakine. He suffered from a right amblyopia associated with slight exophthalmos and retinal vascular malformation. Progressively, a left hemiparesis and quadranopsia appeared. CT, MRI, and angiography (A, B) revealed a CAMS 2 with three locations: opticoretinal, thalamostriate, and calcarine. The child was embolized in 1987 and following the procedure he did not suffer any headaches and recovered from his hemiparesis. After 1 year, however, the symptomatology recurred but no further endovascular treatment was proposed because of poor access to the lesion

366

6 Cerebrofacial Arteriovenous Metameric Syndrome

Fig. 6.6A–E. Legend see p. 367

▲

Introduction

367

Fig. 6.6A–H. A CAMS 3. A young girl presenting with mild oral bleedings in relation with a loose tooth overlying a mandibular AVM (B, C). As a systematic screening, the angiogram (D–F) revealed the posterior fossa-associated lesion. Note on the MRI the involvement of the brain tissue as well as the subarachnoid space and temporal bone (G, H)

368

6 Cerebrofacial Arteriovenous Metameric Syndrome

Fig. 6.7A–D. CAMS 1, 2 (A). This 28-year-old man was originally found to have a retinal arteriovenous at the age of 7 years. CT and MRI studies reportedly showed an arteriovenous malformation involving the left optic nerve, chiasm, and thalamus. A diagnosis was made of a retinocephalic vascular malformation syndrome: Wyburn-Mason or Bonnet-DechaumeBlanc. In 1990, he noticed a small red spot on the tip of his nose, which was diagnosed as an angioma (B). Cerebral angiography delineated the elongated AVM nidus in the midline (C, D). E–G see p. 369

Introduction

Fig. 6.7E–G. (continued) Injections of the external carotid arteries show two AVMs: one involving the palate and the other the nose, fed by branches of the maxillary and facial arteries (E, F). In addition, a large aneurysm is present at the terminal internal maxillary artery and two further aneurysms cluster together in the facial artery in the submandibular region. Embolization of the nasal lesion prior to plastic surgery was done (G)

369

370

6 Cerebrofacial Arteriovenous Metameric Syndrome

Fig. 6.8A–E. Bilateral CAMS 2 (A). An 8-year-old boy presenting high facial edema with venous dilatation and proptosis. Right-sided deafness and decrease in visual acuity of the right eye. A few months before, progressive appearance of right-sided hemiparesis. MRI (B) and angiography (C–E) demonstrate typical CAMS 2 type of arteriovenous malformation. Note the typical aspect of the lesion on the right side and the small size of the early draining veins. In addition, there is an usual bilateral thalamic location. It should be noted that despite the extension of the apparent nidus, the symptoms were moderate

Introduction

371

In the series of Willinsky et al. (1990a) of 213 patients with multifocal vascular malformations, there was a single CAMS case, while in the Scottish Intracranial Vascular Malformations Study, a true population-based epidemiological study, in the first 2 years, only one case among 100 brain AVMs was encountered (Bhattacharya, unpublished data). Bhattacharya et al. (2001) reported a series of 15 cases. There were eight male and seven female patients. The age range at presentation was 4–49 years (mean age, 18 years) and 11 of the 15 were 16 years of age or under. The age of presentation of these patients is clearly much younger than is seen with sporadic AVMs.As an aid to diagnosis, we divide the potential areas of involvement into three axial zones (brain, orbit, and face) and propose the criteria that lesions must be present in at least two of these zones for the diagnosis to be made and then the craniocaudal type of CAMS established. All but one of the 15 patients had orbital involvement, while a cutaneous discoloration was only recorded in four cases. Thus the most frequent patterns of involvement were optic nerve (13/15), retina (11/15), thalamus (9/15), and chiasm/hypothalamus (9/15). In our series, there was no definite involvement of the midbrain, and it is possible that previous reports such as Wyburn-Mason’s confused prominent mesencephalic draining veins for nidus, suggesting that this was a common site of involvement. Indeed, the nidus concept of AVMs was not recognized until 1971, and then initially only in spinal cord lesions (Doppman 1971). There were also no cases of cerebellar involvement. Typical features of CAMS 2 (Wyburn-Mason or Bonnet-Dechaume-Blanc syndrome), are the association of a high-flow arteriovenous malformation of the face with retinal and brain AVMs. In its most complete prosencephalic form (CAMS 1, 2), AVMs can extend forward, continuously, from the occipital lobes and thalamus via the hypothalamus, optic chiasm, and optic nerve to the retina; however, they seem to spare the sphenoid and ethmoid bones (Fig. 6.5). Previous reports have described a range of abnormalities from this phenotypic spectrum, mostly stressing the unilateral cerebral involvement. In CAMS 2, bilateral orbital involvement is rare (Kim et al. 1998a). Retinal involvement is also not universal (Brown et al. 1973). Theron et al. (1974) found that among 25 cases (including their three new ones), four with retinal lesions had no clinical evidence at presentation of a cerebral AVM, and the extent of facial involvement was not always apparent clinically. Retinal AVM is often the earliest manifestation of a CAMS 2 (Fig. 6.9), and in two cases, follow-up showed secondary expression of the syndrome 6 years later, while the full extent of the spectrum was revealed over a 28-year period in another case (Fig. 6.7) (Jiarakongmun et al. 2002). Anticipation of the other locations can be discussed when isolated retinal, hypothalamic, or optic nerve AVM is diagnosed (Fig. 6.10). However, it is intriguing to note that vision tends to be preserved for a long time despite extensive involvement of the visual pathways.

372

6 Cerebrofacial Arteriovenous Metameric Syndrome

Fig. 6.9A–C. CAMS 2 revealed over 6 years. A A 4-year-old boy with only retinal AVM. B, C Six years later a diencephalic AVM is visible

CAMS 3 has been very infrequently described and involves the midbrain, cerebellum, petrous bone, and mandible (Theron et al. 1974; Fischgold et al. 1952; Tamaki et al. 1971; Wong et al. 2003; Haw et al. 2003). CAMS 3 is located in a strategic position at the crossroads of the complex cephalic segmental arrangements and the relatively simplified spinal metamers, and it may therefore bear transitional characteristics with features shared by either end of the spectrum. In the review of spinal arteriovenous malformations syndromes (SAMSs), Matsumaru et al. (1999) showed that vertebral lesions and radicular lesions occur in 42% and 21% of cases, respectively. It appears that in SAMS, there is a high propensity

Introduction

373

Fig. 6.10A, B. Isolated optic nerve AVM. Is it an isolated lesion or the early expression of a CAMS2? (Courtesy of M. Mursdorf)

of lesions in sclerotomal mesenchymal aggregates around the notochord underlying the developing spinal cord. The lesion in the petrous bone in one of our cases showed that a similar phenotype can be exhibited in CAMS 3. On the other hand, the main targets for osseous involvement of CAMS 1, 2 are the maxillary structures, with apparent sparing of the corresponding skull base (ethmoid and sphenoid). The rostral part of the notochord reveals many peculiarities in comparison to the trunk mesoderm, including a wide variation in the relationship of notochord with prechordal mesoderm in different species (Barteczko and Jacob 1999). During development of the cranial base, primordial cartilage develops from mesenchymal cell aggregates, which extend cephalad. The otic capsules, destined to develop into petromastoid temporal bones, are located directly lateral to the parachordal cartilage, which are the precursors for the future basiocciput. The parachordal cartilage intimately surrounds the rostral end of the notochord (Sperber 1989). In comparison, the prechordal mesenchymal centers for the facial skeleton are more distal and cephalic to the rostral notochord. The rare skull base involvement in CAMS 1, 2 might possibly be explained by the relatively remote location of prechordal mesenchymal centers in comparison with the otic capsules and the parachordal cartilage with respect to the notochord. The presence of an AVM surrounding the left vestibulocochlear nerve (subarachnoid location) in one of our patients sheds light on the transitional nature of CAMS 3. In CAMS 1, 2 patients, previous reports mentioned only the optic nerve as the “cranial nerve” being affected. It is important to note that the retina and optic nerve are direct extensions of the forebrain, projecting directly from the optic vesicle. This significantly differs from other cranial nerves, which basically are peripheral nerves link-

374

6 Cerebrofacial Arteriovenous Metameric Syndrome

ing the central nervous system to the peripheral tissues. The lesions involving the retina, optic nerve, and chiasm, in cases of CAMS 1, 2, should therefore be regarded fundamentally as pial AVMs. On the contrary, a significantly higher proportion of cases of SAMS (21% from Matsumaru’s series) have lesions along radicular nerves within the subarachnoid space, reflecting a basic difference in selection of compartmental location. The cause of such diversity is not understood, but this may be related to the different influences of abluminal and intraluminal factors at the spinal vs the cranial levels or the difference in their embryonic origin. The topography of vascular malformations of CAMS 1, 2 appears to follow the same rule governing the location of sporadic AVMs, in that nidi of the AVMs reside only within the subpial compartment, with the subarachnoid space spared. The occurrence of subarachnoidal AVMs in CAMS 3 possibly suggests a transitory process toward the spinal distribution (Wong et al. 2003).

6.2 Clinical Manifestations The commonest presenting symptom is visual deterioration (reduced acuity or field). This is sometimes detected several years before further neurological symptoms lead to more detailed investigations (CT, MRI), confirming the presence of a retinal AVM but also revealing an associated brain AVM. Epistaxis is encountered in patients in whom the presenting cause is the associated high-flow maxillofacial AVM. In the Bhattacharya et al. (2001) series, 25% of the patients suffered from a intracranial hemorrhage (at 4, 6, 23, and 49 years of age) related to their brain AVM, and none of the brain AVMs was considered curable. It is important to note that only one-third of the patients were recorded as having any facial involvement (although this was a retrospective study, and such involvement could have been overlooked or not recorded). There is no evidence to suggest an inherited basis of CAMS and there are also no reports in the literature of brain or orbital AVMs occurring among family members of CAMS patients. It has been intriguing, however, to find other cerebrofacial vascular lesions in close relatives in two out of our 15 patients with CAMS.

6.2.1 Retinal AVMs and AVMs Along the Optic Nerve and Chiasm 6.2.1.1 Retinal AVMs

Retinal AVMs are present in most CAMS patients, but there are some reported cases without retinal involvement (Bhattachaya et al. 2001; Ponce et al. 2001; Maeda et al. 1992) (Table 6.2). Jiarakongmun et al. (2002) found among 14 CAMS 2 cases, nine patients with retinal AVMs, and suggested screening including ophthalmologic examination with visual field testing, visual acuity, and fluorescein angiography for patients suspected of having CAMS.

6 12 7

M

M

M

F

NA

F

F

F

F

F

F M

F

Jiarakongmun et al. 2003; case II

Jiarakongmun et al. 2003; case III Muthukumar and Sundaralingam (1998) Yasuhara et al. (1999)

Gibo et al. (1989)

Tost et al. (1996)

Maeda et al. (1992)

Daenis and Appen (1984)

Hopen et al. (1983)

Kikuchi et al. (1988)

Fujita et al. (1989) Schlieter et al. (1976)

Lalonde et al. (1979)

16

5 39

7

56

14

5

6

NA

4

28

M

Jiarakongmun et al. 2003; case I

Age (years)

Sex

Reference

Retina

Retina and optic nerve Optic nerve Retina

Optic nerve and chiasm

Optic nerve and chiasm

Retina

Retina

Retina, optic nerve, left orbit Optic chiasm

Retinal

Retina

Optic nerve, retina (diagnosed at 7 years) Left optic nerve

Impaired visual acuity

Left eye blindness Impaired visual acuity Impaired visual acuity Strabismus, impaired visual acuity Impaired visual acuity, optic atrophy Progressive chiasmal syndrome Proptosis, injected eye Proptosis Impaired visual acuity

Right eye blindness Blindness

None

Impaired visual acuity

Hemiparesis, hemiaNone nopia, speech disability None None

None

None

None

Yes Yes

None

Severe oral bleeding None

None

None

None

Symptoms

None

None

None

None

None

Cheek nevus, None (present at 1 year) None None

Hemifacial AVMs

Left maxilla

Left submaxilla

None

None

Nose tip (diagnosed at 18 years) None

None

None

None

None

None

None

None

None

Headache, right hemiparesis, hemianopsia Progressive neurological deficit None

None

Present

Facial vascular lesion

Yes

Yes

None

None

Yes (2 years later)

None

Yes, lesion progress in size Yes

Yes (1 year later) Yes

Yes (diagnosed at 15 years) Yes

Symptoms

Present

Present

Symptoms

Intracranial vascular malformations

Visual pathway presentation

Table 6.2. Cerebrofacial arteriovenous metameric syndrome II (CAMS 2) with visual tract involvement (Jiarakongmun et al. 2002)

Retinal AVMs 375

376

6 Cerebrofacial Arteriovenous Metameric Syndrome

Progressive visual loss, including decreased visual acuity and visual field defects, appears to be the earliest presenting symptom of CAMS 2 disease, which tends to occur several years prior to the discovery of the retinal lesions. Bhattacharya et al. (2001) showed 60% cases of CAMS patients presented with visual symptoms at a mean age of 18 years. The retinal arteriovenous malformation or arteriovenous communications of the retina (AVCR), or so-called racemose hemangioma in the ophthalmological literature, is probably a misnomer because it does not show proliferative or tumor behavior. According to Archer’s classification, grade III AVCR is the most severe form and is often linked with an intracranial lesion or CAMS (Meinhold 1996). Retinal AVMs or AVCR, are usually considered to be stable retinal lesions, despite progression of the coexisting intracranial AVMs (Yasuhara et al. 1999). Clinical presentations of this lesion include loss of vision due to intraretinal macular hemorrhage, central and peripheral retinal vein occlusion, and vitreous hemorrhage, or even gradual reduction of vision due to neovascular glaucoma in association with changes in the retinal AVMs and retinal and choroidal ischemia (Effron et al. 1985).

6.2.1.2 Optic Nerve and Chiasmatic AVMs

Optic nerve and chiasmatic AVMs are also hallmark findings in CAMS. They often appear to be clinically silent, eventually resulting in a slowly progressive functional deficit. The presenting symptoms include decreased visual acuity and field defects or blindness from optic nerve atrophy, and progressive dysfunction of the optic pathways. Exophthalmos is a rare presenting symptom in CAMS, with optic nerve AVMs and intraorbital congestion resulting in mass effect, as reported by Fujita et al. (1989), Muthukumar and Sundaralingam (1998), and in one of the cases of Jiarakongmun et al. (2002) (Fig. 6.8). Exophthalmos could also result from an enlarged ophthalmic vein, which may drain normal brain tissue or cerebral AVMs related to increased intracranial venous pressure caused by venous occlusion of draining intracranial veins. Treatment of these orbital lesions remains a challenge because of the complex anatomic and hemorrhagic characteristics of the malformation. Attempts to treat these patients with combined surgery and careful preoperative embolization are not without risk (Goldberg et al. 1993).

6.2.2 Cerebral AVMs

Considered as a metameric lesion, intracranial AVMs in CAMS are one of the most common findings in such patients. We found cerebral AVMs in three-quarters of our cases. The cerebral AVMs in CAMS may involve in continuity the optic chiasm, hypothalamus, thalamus, the cortex around a calcarine fissure or the cerebellum, depending on the subtype of CAMS (1, 2, or 3). Infrequently they present as multiple scattered lesions in the same segmental distribution. The corpus callosum or the olfactory region belong to CAMS 1 arrangement and should be associated with midline frontonasal vascular malformations (Figs. 6.11, 6.12).

Cerebral AVMs

377

Fig. 6.11A–C. Young CAMS 1 patient presenting with a midline frontal AVM mostly supplied by the ophthalmic terminal branches (A). In addition, the angiographic exploration disclose a holocallosal AVM with an intrasplenial aneurysm representing a priority target for a partial embolization (B, C). (Courtesy of G. Caldas)

Considering the angioarchitecture of cerebral AVMs in CAMS, we observed that there were certain findings in cerebral AVMs in CAMS, which tend to differ from sporadic AVMs. In particular, the AVM nidus in CAMS patients is usually described as a cluster or group of small vascular networks with intervening normal brain tissue and optic pathways and some degree of angiogenesis. Transdural arterial supply was present in some cases (Fig. 6.13). There are no reported cases of intradural high-flow arteriovenous fistulas (AVFs) or related findings of high-flow shunts such as dysplastic flow-related arterial aneurysms or hugely dilated draining veins, as we often seen in hereditary hemorrhagic telangiectasia (RenduOsler-Weber disease). Progressive development and enlargement of cerebral AVMs is one of the special observations in CAMS (Figs. 6.7, 6.13, 6.14) Yasuhara et al. (1999) also reported similar observations with a progressive increase in size and flow of the cerebral AVM with worsening neurological deficit.

378

6 Cerebrofacial Arteriovenous Metameric Syndrome

Fig. 6.12A–C. A 12-year-old girl with a nasal AVM and recurrent severe epistaxis; presence of an associated olfactory AVM (CAMS 1) (A, B). The severity of the epistaxis led to nose resection (C)

These findings suggest that AVMs in CAMS are not static processes within the segment that carry the embryonic defect. Multifocality and the continued progression of the expression of the disease are characteristic of cerebral AVMs in CAMS, with lesions along the visual pathways. Usually lesions are located in one hemisphere, but there are some reports of bilateral involvement. Angiogenesis crossing the midline could be related to ischemia of the midline structures from chiasmatic or hypothalamic AVMs; however, bilateral neural crest migration exists (as seen with mirror aneurysms) and may not be restricted to one side but expressed in separate but adjacent segments. Despite the common occurrence of cerebral AVMs in CAMS, they are usually clinically silent or asymptomatic at the time of discovery. They rarely present with acute neurological symptoms caused by intracerebral or subarachnoid hemorrhage (Bhattachaya et al. 2001), but rather reveal with progressive neurological deterioration without evidence of intracranial bleeding (Jiarakongmun et al. 2002).

Cerebral AVMs

Fig. 6.13A–F. Legend see p. 380

379

380

6 Cerebrofacial Arteriovenous Metameric Syndrome

Fig. 6.13A–J. CAMS 2. Angiogenic activity over 8 years. A–C The child is 4 years old; D–F the child is 6 years old; G–I, the child at 9 years of age. Note the increase in flow, leading to aneurysm formation, but also transdural supply (J)

▲

Fig. 6.14A–F. A 3.5-year-old girl presented with what was diagnosed as hemorrhagic stroke (A, B). The angiogram failed to show anything but a faint local hyperemia. Three years later, worsening of the aspect and the diagnosis of AVM is observed (C, D). Another 3 years later, the lesion continued to increase in size and there was hyperemia of the optic nerve (E, F). Is this a CAMS 2 appearing?

Cerebral AVMs

Fig. 6.14A–F. Legend see p. 382

381

382

6 Cerebrofacial Arteriovenous Metameric Syndrome

Because of their rarity, we probably discover CNS symptoms mostly after the patients have already presented to the referring specialist with other symptoms. This may have led to an overestimation of the incidence of neurological events in CAMS disease. Therapeutic management of the cerebral AVMs and AVMs along the optic pathways related to CAMS is particularly challenging. We would suggest targeted embolization in an attempt to exclude weak angioarchitectural structures or to reduce the AVS in the least eloquent areas in symptomatic patients who are clinically significantly affected.

6.2.3 Facial AVMs, Nasal AVMs, and Mandibular AVMs

Facial AVMs and mandibular AVMs are hallmark locations of CAM disease. The full spectrum of the syndrome was present in one-third of the cases in the review of Jiarakongmun et al. review (2002). Bhattacharya et al. (2001) noted that four out of 15 had a facial AVM in his series. The presence of the facial vascular lesion can be difficult to recognize or clinically silent, sometimes representing a small stable red spot or angioma since infancy or the early childhood period. Then an unknown trigger occurs promoting growth of the lesion with revealing symptoms such as bleeding of the gums or mass effect resulting in facial asymmetry, often during adolescence. The angioarchitecture of facial or mandibular AVMs in CAMS look similar to sporadic cases. They usually present as an arteriovenous fistula or nidus-type arteriovenous malformation with intranidal fistulas. Large proximal arterial aneurysms were noted in our series despite relatively slow flow or small facial or mandibular AVMs (Fig. 6.7). It should be pointed out that sporadic isolated maxillary or mandibular AVMs are not associated with external carotid artery aneurysms regardless of their flow. It is therefore apparent that facial AVMs and intracranial AVMs in CAMS patients are different in terms of angioarchitecture and natural history from sporadic counterparts. In the case of the Jiarakongmun et al. (2002) case, a proximal unruptured arterial aneurysm in the sphenopalatine fossa far away from distal nasal AVMs prompted preventative treatment to reduce the risk of severe epistaxis. Maxillary or mandibular AVMs with intraosseous venous lakes or pouches are also at risk of gum bleeding and severe hemorrhages after tooth extraction (Fig. 6.15). Hemorrhage associated with facial and mandibular AVMs was the revealing symptom in one of our cases, and in most series the posterior fossa lesions were identified only after screening (Wong et al. 2003; Haw et al. 2003; Yasuhara et al. 1999) (Fig. 6.6).

Facial AVMs, Nasal AVMs, and Mandibular AVMs

383

Fig. 6.15A–D. CAMS 2. A 9-year-old girl presented with the onset of right-sided hemiparesis. Investigations revealed an intraventricular hemorrhage arising from an AVM of the left basal ganglia (A). She was reviewed annually and a recent decline in visual acuity was detected in the left eye together with an inferior quadrantanopia of the right visual field. Significant maxillary involvement with bone hypotrophy (B, C) and rapid expansion over 2 years of the extracranial location led to embolization with glue to prevent epistaxis (D). The maxillofacial lesion was considered to present the most immediate danger, with the possibility of life-threatening hemorrhage at the loss of her molar baby teeth

384

6 Cerebrofacial Arteriovenous Metameric Syndrome

6.2.4 Investigation for CAMS Patients

Proper investigations for patients suspected of having CAMS will vary depending on the clinical manifestation associated with the revealing lesion. The patients suspected of having CAMS 1 who present with hypothalamic AVMs should be investigated in detail for nasal AVMs and olfactory or corpus callosum AVMs by physical examination and detailed MRI examination. For CAMS 2, patients who present with diencephalic lesions such as chiasmatic or optic nerve AVMs with progressive visual loss should be investigated for maxillary lesions including AVMs or dysplastic aneurysms involving the external carotid system to prevent life-threatening epistaxis from an aneurysm of this type. For CAMS 3, patients presenting with cerebellar AVMs should be investigated for mandibular lesions such as high-flow AVMs, which could lead to severe bleeding after tooth extraction in the adolescent. Conversely, patients presenting with facial vascular lesions with characteristic high-flow AVFs or dysplastic aneurysms in the nasal maxillary or mandibular areas should be investigated for possible coexisting asymptomatic intracranial AVMs.

6.3 CAMS and Angiogenic Activity Facial involvement varies from a faint cutaneous discoloration caused by a venous malformation to the full-fledged maxillofacial or mandibular AVM, which may present with life-threatening hemorrhage in addition to severe cosmetic and psychological problems (Gibo et al. 1989) (Figs. 6.7, 6.12, 6.15). Preventive treatment of such lesions is recommended. The angioarchitecture of facial or mandibular AVMs in CAMS is not significantly different from the sporadic cases. They can either present as an arteriovenous fistula or as an nidus-type of arteriovenous malformation. An interesting finding is the presence of arterial aneurysms (Fig. 6.7) arising from external carotid artery branches. Since the flow in the AVM is not very high and the external carotid system (facial and maxillary arteries) is involved, the dysplastic (angiogenic or proliferative) origin of these aneurysms is supported, similar to what can be seen in PHACES syndrome (see Chap. 12, this volume) (Table 6.3). Unlike CAVMs where angiogenesis is not seen unless special traumatic, hemodynamic, ischemic, or other triggers interfere, the way CAMSs present and evolve over the years is peculiar. In particular, there is an obvious increase in AVM size in the maxillofacial region, de novo locations in the brain, or apparent extension of previously demonstrated ones. While a single sporadic CAVMs related to a late causative trigger does not become larger (all the cells involved show their common impairment), CAMSs, on the other hand, since they are generated by an earlier causative trigger (involving groups of migrating and nonmigrating cells), maintain their capacity over the years to reveal their full extent through a pseudogrowth or proliferation.

CAMS and Angiogenic Activity

385

Table 6.3. Postulated relation between metameric syndromes and neural crest/mesoderm contribution, lymphatic to arterial impact, and proliferative behavior

Mirror aneurysmb PHACESb CAMS 1, 2b CAMS 3b CVMS 1–3b SAMS 1–31

Lymphatica malformation

PWSa

Cartilage bonea

Membrane bonea

AV shunta

Angiogenesisa

Arterial aneurysma

– – – – + +

– – – – + +

– – – + + +

– – + + + +

– – + + – +

– + + + – +

+ + + + – +

a

From less angiogenic to more angiogenic (from left to right). Neural crest and mesoderm to mesoderm alone; craniocaudal (from up to down). PWS: Port wine Stain.

b

Obviously the facial AVMs and intracranial AVMs in CAMS patients are different in terms of angioarchitecture and natural history (Jiarakongmun et al. 2002) from sporadic AVMs. The different expression of the disease and the various locations are the result of the relationship established by the cells during their migration. Although belonging to the AVM group of disorders, the successive development of the lesions, their being intermingled with normal tissue, and the presence of dysplastic aneurysms suggest a malformative target closer to the arterial side than usually associated with CAVMs (see Chap. 2, this volume), and an early causative timing impacting the still poorly differentiated arteriovenous structures. The resulting phenotypes will combine AVS characteristics with arterial ones such as preserved active angiogenesis and aneurysmal development. Slightly more proximal on the vascular tree to be developed, one would place the PHACE syndrome with the combination of various proliferative properties and fewer AV malformative features (Scheme 6.1). More distally on the tree, one would expect CVMS (Ramli et al. 2003) or Sturge-Weber syndrome, which associates venolymphatic malformations without angiogenesis and aneurysm. All these syndromes share the migrating pattern of the neural crest and cephalic mesoderm along their three main paths. Multiple hemangiomas can also be analyzed with this geographical distribution in mind (Waner et al. 2003) (see Chap. 8, this volume) (Fig. 6.16). SAMS 1–31 belong to the same group; however, the peculiar nature of the vessel’s embryological origin make them combine several types of expression from arteriovenous to purely venous; yet they keep some degree of angiogenic potential with nidus growth and aneurysm formations (Figs. 6.17, 6.18).

386

6 Cerebrofacial Arteriovenous Metameric Syndrome

Scheme 6.1. Vascular diseases according to the arterio-veno-lymphatic tree

Fig. 6.16. The nonrandom distribution of facial hemangiomas. Based on their clinical photographs, 232 of the hemangiomas were mapped on a facial schema. The 55 diffuse hemangiomas showed a segmental tissue distribution and thus were designated as frontonasal (27%), maxillary (35%), or mandibular (38%). Note the three territories found by Waner, although he did not refer to the geotropism identified in the CAMS. The identical mapping point to the reality of these boundaries not only for malformative vascular lesions but also for proliferative lesions. (From Waner et al. 2003)

CAMS and Angiogenic Activity

387

Fig. 6.17. A SAMS 1/2. Typical aspect of the same segmental logic applied to the first segment caudal to the third cranial territory (B, C)

388

6 Cerebrofacial Arteriovenous Metameric Syndrome

Fig. 6.18A–D. A 26-year-old patient who presented with a chiasmatic syndrome and a cleft palate. Axial CT (A). Note the contrast-enhanced lesion of the area of the anterior commissure. Note the hyperemic cleft margins (arrowheads). B Selective injection of the ipsilateral facial artery. Note the hyperemic cleft margins (arrowheads). The upper lip also has a hyperemic zone (arrow). Note the medial branch to the inferior labial arcade (curved arrow). C, D Internal carotid injection shows an subcallosal suprachiasmatic lesion (arrowhead), suggesting associated AVM. The topography of both midline lesions may correspond to a CAMS 1-like syndrome

7 Dural Arteriovenous Shunts

7.1

Introduction 389

7.2 7.2.1 7.2.2

Classifications 390 Age Groups 392 Disease Groups 392

7.3 7.3.1 7.3.1.1 7.3.2

Dural Sinus Malformations 396 DSM with Giant Pouches 398 Fetal and Postnatal Changes of Sinuses 398 DSM of the Jugular Bulb 434

7.4

Infantile Dural Arteriovenous Shunts (AVS) 436

7.5

Adult Type of Dural Arteriovenous Shunts in Children 444

7.6 7.6.1 7.6.2 7.6.3 7.6.4 7.6.5

Other Dural Shunts 447 Vein of Galen Aneurysmal Malformation 447 Dural Supply to Pial Cerebral Arteriovenous Malformations 447 Proliferative Angiopathic Disease 448 Systemic Disorders 448 Recurrence in Intradural AVS and Secondary Transdural Supply 449

7.7

General Remarks on Treatment 451

7.1 Introduction Few reports have addressed the entity of dural arteriovenous shunts (DAVS) in the pediatric age group (Albright et al. 1983; Garcia-Monaco 1991c; Morita et al. 1995; Kincaid et al. 2001; Barbosa et al. 2003). These authors reviewed mostly the English literature on the subject and some reports included individual therapeutic attempts or described pediatric cases as part of an adult series. Discussion in the past tended to focus on the issue of the congenital vs. acquired character of the disease, and many authors referred to the same classic observations. Only rarely were pediatric examples used to help understand this disease as it affected children. In contrast, it has been a frequent presumption that certain adult circumstances likely also apply to children. Similarly, authors have tried to recognize in pediatric cases an adult pattern to justify the use of more familiar management strategies or tools. Application of technical experience in adults to the pediatric practice have ignored the specificities of this population and delayed appropriate steps that need to be taken toward understanding and treatment.

390

7 Dural Arteriovenous Shunts

7.2 Classifications Many DAVS classifications are available in the literature. Several of those classifications are being used in the endovascular community but none applies directly to the pediatric age group. Pediatric DAVSs are themselves evolutive and in addition develop on an evolving (maturing) vascular system. Understanding the mechanisms for symptoms and the chronology of events is more relevant in the management of pediatric DAVSs then memorizing classifications that are not applicable. It was Castaigne et al. (1976) who stressed the role of the pial venous drainage in understanding the pathophysiology of neurological symptoms in adult patients with DAVS. Since then, few reports have added to this fundamental contribution, until recently the analysis of the natural history of DAVS in adults has been described (Davies et al. 1996, 1997a, b; Satomi et al. 2002; van Dijk et al. 2002). DAVSs involving the superior sagittal sinus (SSS) and posterior sinusal confluents are often lumped together with cavernous plexus and anterior cranial fossa locations, yet they differ anatomically, histologically, physiologically, and are also likely to be biologically different and should therefore not be reported as a homogeneous group. Attention paid to the flow direction in the venous outlets has outlined various types of anatomic arrangements. Clearly, the only important predictive feature for future neurological manifestations in adults is the presence or absence of cerebral venous reflux at a given moment. Such basic observations would apply to pediatric cases provided that the maturation of the venous system had been achieved; however, in children neurological symptoms can also occur without pial venous reflux. Therefore, the understanding of how the brain and DAVS interact in children cannot be learned only from the analysis of the lesion itself but requires that the specifics (maturation, etc.) of the cerebral vasculature at that moment in time be scrutinized and analyzed. In children, any intracranial AVS may create a shift in the vascular maturation processes, resulting in a shift for that individual’s final vascular equilibrium. The shift may not compromise the physiological needs on a short-term basis but can weaken the individual vascular system, making it vulnerable or less flexible to various triggers, whether they be hemodynamic, immune, hormonal, or others. Arteriovenous shunts involving the dura and the epidural space, i.e., the different diseases that can be labeled, although improperly, pediatric DAV shunts, include the following:
Dural sinus malformations (DSMs)
Nontraumatic infantile DAVS
Nontraumatic adult type of DAVS (osteodural, sinusal-dural, duralsubdural)
Traumatic epidural AV communications
Induced DAVS (associated with cerebral AV malformations, sinusal high-velocity flow conditions, proliferative angiopathic diseases) Their causes and the degree of interference with the rest of the vascular system will be different, as the biological profile and reactivity are different in each of these situations.

Classifications

A. a1 a2 a3 a4 a5 a6 a7 a8 a9 a10 a11 a12 a13 a14 a15 a16 a17 ab8 ab9

Opthalmic Artery Intraorbital portion 1 Intraorbital portion 2 Intraorbital portion 3 Lateral muscular artery Lateral ciliary artery Central retinal artery Medial ciliary artery Supra orbital artery Lacrymal artery Recurrent tentorial artery Deep recurrent ophthalmic artery Recurrent meningeal artery Meningo ophthalmic artery Posterior ethmoidal artery Anterior ethmoidal artery Anterior falcine artery Jugum sphenoidale branch Anterior frontal meningeal Anterior frontal meningeal

C. c1 c2 c3 c4 c5 c6 c7 c8 c9 c10

Ascending Pharyngeal Artery Jugular branch Hypoglossal branch Clival branch Inferior petrosal branch Cerebello pontine angle branch Midline anastomosis Odontoid arterial arch system Foramen magnum branch Carotid branch Cerebellar fossa branch

D. d1 d2 d3 d4

Ascending Pharyngeal Artery Mastoid branch Cerebellar fossa branch Torcular branch Cerebello pontine angle branch

E. e1 e2 e3 e4 e5 e6 e7 e8 e9 e10 e11 e12

Internal Carotid Artery Meningo hypophyseal trunk Infero lateral trunk (I.L.T.) Antero medial branch (I.L.T.) Antero lateral branch (I.L.T.) Posterior branch (I.L.T.) Recurrent artery of the froamen lacerum Marginal tentorial artery Lateral clival artery (medial branch) Lateral clival artery (lateral branch) Postero inferior hypophyseal artery Medial clival artery Capsular artery

F. f1 f2 f3 f4

Vertebral Artery Artery of the falx cerebelli Posterior meningeal artery Cerebellar fossa branch Subarcuata artery

391

B. b1 b2 b3 b4 b5 b6 b7 b8 b9 b10 b11

Middle Meningeal Artery Cavernous branch Petrous branch Basal tentorial branch Posterior fossa branch Petro squamosal branch Parieto occipital branch Middle cranial fossa branch Sphenoidal branch Frontal branch Tentorial branch Cavernous branch of the accessory meningeal artery ba9 Meningo lacrymal artery

Fig. 7.1. Schematic representation of the arteries to the skull base and adjacent dura

392

7 Dural Arteriovenous Shunts

Following the identification and localization of the site of the shunt, the origin of the feeders and the venous drainage need to be identified (Fig. 7.1). Regardless of the population, there will be a clear difference between the dural sinus type of AVS at the vault and the epidural AV communications at the parasellar region. Similarities exist between the cavernous plexus and the spinal venous network, but not between the true cranial dural sinuses and the epidural venous spinal spaces. The skull base and its venous relationships can be followed caudally toward the sacral region because of their similar relationships. The cavernous region, however, does not drain brain tissue at birth and therefore an early lesion of the infantile type in the parasellar region will not have the same cerebral consequences as a similar one at the spinal level, where radicular veins already open into the epidural space. A malformation of the cavernous plexus is hard to conceive and indeed has never been described. Conversely, the malformation of the sinuses or conjoined sinuses in conjoined twins will illustrate this difference (see Chap. 9, this volume). The infantile AV shunt constitutes a separate group of lesions that will be discussed as such.

7.2.1 Age Groups

Within the pediatric population in general, neonates and infants constitute a special subgroup as their vascular system continues to mature. They are sensitive (exposed) to certain triggers that make them present with specific symptoms that do not occur in older children or adults (see Chap. 2, this volume). In particular, systemic manifestations and hydrodynamic disorders may occur with a natural progression, sometimes independent of the disease itself and remaining characteristics of the age group. Macrocrania and its progression following jugular occlusion, and thrombosis of slow-flowing dural pouches are examples of this specificity. The disease by itself is reported (Morita et al. 1995) to have a mortality rate of 38% in the pediatric age group and the mortality rate increases to 67% in the neonatal subgroup.

7.2.2 Disease Groups

Each of the three disease groups we will describe herein refers to features other than strictly the age of onset or the age of main clinical expression, since all types can be seen during the first few weeks of life. Some neonatal types may in fact not be revealed until infancy and others can be diagnosed in utero. The three types are: 1. Dural sinus malformation (DSM) (Fig. 7.2), in which the AVS shunts are secondary and usually accessory to the sinus malformation. 2. Infantile DAVS, often multifocal, without sinus malformation, although with large sinuses and sometimes secondary jugular occlusion (Fig. 7.3).

Disease Groups

393

Fig. 7.2A–D. Prenatal diagnosis of an intracranial cyst in a child presenting with polypnea, aged 2 months (the child could not finish his bottle). A MRI and angiography (B, C) performed at 3 months demonstrated a large dural sinus malformation on the midline. Dural and scalp arterial supply converged at the bregma suture. The cerebral medullary veins appeared to be congested. There was no evidence of cavernous sinus capture. There was no cardiac failure (D). Partial embolization was performed and led to a transient improvement; 10 days later, the child presented with convulsions and an intracranial hemorrhage

394

7 Dural Arteriovenous Shunts

Fig. 7.3A–E. An 11-year-old child presented with a right-sided exophthalmos, intracranial bruit, and vertigo. A CT shows an extensive enlargement of the skull base sinus from the orbit to the torcular. B–E Angiography demonstrated a high-flow shunting zone extending from the cavernous sinus region to the jugular bulb along the superior petrosal sinus, lateral sinus, and sigmoid sinus. All possible feeders to the region contributed to the supply of this shunting zone

Disease Groups

395

Fig. 7.4A–C. A 10-year-old child presented with ophthalmocavernous manifestations with proptosis and cranial nerve palsy. A Arterial feeders arose from the internal carotid and maxillary arteries. There was no evidence of cortical or inferior petrosal sinus drainage. B, C Manual compression of the ophthalmic vein at the medial canthus produced complete stagnation of the contrast medium within the sinus. Six months later, complete occlusion was noted and the symptoms had disappeared; there was no recurrence during 3 years of follow-up

3. An adult form of DAVS of the cavernous plexus (Fig. 7.4) or sigmoid sinus, in which the sinuses are normally small and sometimes partially thrombosed and can be secondary to another local event (thrombosis). The angiographic appearance of the three types is very different, as is their clinical history. In certain cases, the significance of neurological symptoms (cranial nerves) is different, although they may appear to look the same (arterial steal, mechanical compression by venous ectasias, inflammatory reaction around thrombosis, associated arteritis, venous congestion).

396

7 Dural Arteriovenous Shunts

7.3 Dural Sinus Malformations This disease group includes (Scheme 7.1):
DSMs with giant pouches or lakes and mural AV shunting involving the adjacent posterior sinuses. Partial thrombosis of the sinus may occur and can also be observed in utero (Fig. 7.5).
DSMs of the jugular bulb, with otherwise normal sinuses, appear as a sigmoid sinus-jugular bulb diaphragm and are associated with a petromastoid-sigmoid sinus high-flow AVF that is usually of the single-hole type.

Scheme 7.1. Natural history of dural sinus malformation with dural arteriovenous (DAV) shunts. ICP, intracranial pressure. During the fetal phase, dural sinus ballooning occurs at 4–6 months retrograde from the jugular bulb to the superior sagittal sinus

7.3 Dural Sinus Malformations

Fig. 7.5A–F. Legend see p. 398

397

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Fig. 7.5A–H. Prenatal aspects on MRI. A, B Giant DSM, B, C in utero diagnosis of epidural hematoma where it corresponds to an already partially thrombosed DSM. E, F Similar case in a neonate; G, H partially thrombosed lesion in an infant. (Courtesy of A. Goulao)

7.3.1 DSM with Giant Pouches 7.3.1.1 Fetal and Postnatal Changes of Sinuses

“Somewhat uneven ballooning of the transverse sinuses” (described by Masaki 1959, cited by Okudera et al. 1996) was observed in the roentgenograms of the fetuses from the latter half of the 4th to the 7th month. After 20 weeks, the inner caliber of the transverse sinuses gradually becomes even. From birth to the age of 1 year, the inner diameter of the transverse sinus decreases somewhat and after 1 year of age, the sinus will have developed the adult configuration. When we measured the inner diameters of the dural sinuses on roentgenograms of the injected fetal brains, we found that the inner diameters of the sigmoid sinuses remained relatively constant and small, ranging in size from only 1 to 2 mm. Up to the 6th fetal month, the course of the sinuses differs from that in the adult in following a gentle convex curve medially, on the Towne view. After the 6th fetal month, the sigmoid sinuses follow a gentle convex curve laterally. At this age, the course of the sinuses approaches that of adults. The inner diameter of the jugular sinus increases by only 1 mm from the 3rd to the 7th fetal months and is extremely small in caliber (1–2 mm on average). After birth, it rapidly

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399

Fig. 7.6. A MR at 5 months with a well-tolerated DSM. B,C In 7 months, explosive progression with suspected dural sinus proliferation, venous infarction, and hemorrhagic de novo cavernomas

enlarges, forming a bulb-like configuration at 2 years; this is the formation of the (high) jugular bulb. During the period when the jugular sinus is small and poorly developed, the transverse sinus is markedly enlarged (ballooning), acting as a reservoir for the increased amount of stagnant venous blood coming from (mostly the convexity of) the cerebrum and cerebellum. Overflow of the venous blood flow from the transverse sinuses is manifested by the development, enlargement, and engorgement of the emissary veins (the occipital sinuses, the marginal sinus, and the internal vertebral and paravertebral venous plexuses). The formation of the (high) jugular bulbs takes place after birth (clearly visible in the angiograms taken 2 years after birth) and is likely related to hemodynamic factors, resulting from a change from the fetal lying down position to the postnatal “erect posture” (Okudera et al. 1996). Thus the posterior sinus DSMs have been thought to correspond to an abnormal perinatal persistence of sinus ballooning. However, this does not explain why the so-called normal ballooning is not seen routinely in the prenatal period in normal cases. Cases of DSM are by definition associated with the uncontrolled development of posterior sinuses, including transverse, sigmoid sinus, and/or confluence of sinuses. Hence, DSM is a disease of the sinus development instead of the embryological nondevelopment. This accounts for the progression of the disease with sinus wall overgrowth, abnormal development of epidural confluence of venous spaces leading to segmental giant lakes, followed by secondary thrombosis of the spaces and subsequent remodeling if the venous drainage of the brain can be rerouted. In some cases, the DSM ongoing increase in size is associated with the appearance of hemorrhagic cavernomas (Mohamed et al. 2002) (Fig. 7.6). Associations with sinus pericranii, ipsilateral lymphovenous maxillofacial abnormalities, hemangiomas, or cleft palate testify for a more complex disorder and suggest a cerebrofacial venous segmental distribution. No known hereditary vascular disease, such as HHT, is associated with DSM. There is also no family history of DSM in our group of patients.

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Associated slow-flow multiple AV shunts are consistently noted within the wall of the malformed dural sinus, adding to the venous congestion of the brain resulting from the frequently associated outlet restrictions, since the brain has to drain through the diseased sinus. These additional constraints for normal brain venous drainage persist until the cavernous capture of the sylvian veins provides an alternate outlet toward the ophthalmic veins, inferior petrosal sinus into the jugular bulb, or directly into the pterygoid venous plexuses. Early and rapid spontaneous thrombosis within the DSM lake and postnatal dysmaturation of the jugular outlets further compromise cerebral venous drainage and subsequently lead to acute hydrocephalus, venous infarction and lethal intraparenchymal hemorrhage. As long as the venous outlets are patent, the clinical manifestations remain contained and restricted to related hydrodynamic symptoms (macrocrania). The DSMs away from the torcular herophili have a better chance of favorable outcome, as there will be at least one normal sinus for the brain to drain. However, it is important to have the ipsilateral cerebral hemisphere drain into an alternate pathway either by cavernous capture or by a persistent medial occipital sinus bypassing the thrombosed distal sigmoid sinus into the ipsilateral jugular vein or into the contralateral sinus via the SSS. Drainage of the posterior fossa is always difficult to demonstrate and is a significant risk if thrombosis of the poorly anastomosing midline veins occurs. The presence of cerebellar DVAs will add further to that risk by making the system convergent, which normally is divergent toward the petrous vein, the basal veins, and the cervical spine veins. Barbosa et al. (2003) reported on 30 patients with DSM seen in Bicêtre Hospital from 1985 to July 2003 (Table 7.1). DSM accounted for 57.7% of the DAVS in children. The three classic age groups are used to date the clinical onset: neonates (from birth to 30 days), infants (1–24 months) children (2–15 years). The clinical and neurological statuses of the patients were determined by pediatric neurologists and assessment included the Brunet-Leizine and Denver neurocognitive tests. Infants were scored at admission and on follow-up using the Bicêtre scoring system (See Chap. 2, this volume). A male dominance was noted (2:1). The oldest patient at the time of diagnosis was 2 years of age and the mean age was 5 months in this series. The mean age at first consultation was 7 months for a maximum at 4 years. Eight (26.7%) patients were diagnosed prenatally during routine ultrasound; half had the torcula type of DSMs and for these the M:F ratio was 1:1. Six patients (75.0%) had a favorable outcome and two (25.0%) had an unfavorable outcome, one of which presented with brain damage. Early postnatal symptoms can be cardiac failure (usually mild and infrequent), coagulation disorders (consumption syndromes), moderately increased intracranial pressure (with irritability, macrocrania, neurocognitive delay, and seizures) occurring in young infants. The most frequent clinical presentation (76.7%) was macrocrania. Seizures, psychomotor delay, and intracranial hemorrhage (ICH) were noted in 23.3%. The latter

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Table 7.1. Clinical manifestationsa (Barbosa et al. 2003) Clinical features

%

Macrocrania Seizures Psychomotor delay Intracranial hemorrhage Brain damage Hydrocephalus Congestive cardiac failure Bruit cranial Facial veins dilatation Intracranial hypertension

23/30 (76.7%) 7/30 (23.3%) 7/30 (23.3%) 8/30 (26.7%) 6/30 (20.0%) 8/30 (26.7%) 6/30 (20.0%) 5/30 (16.7%) 3/30 (10.0%) 3/30 (10.0%)

a

Children may have more than one.

was due to either venous infarcts or cavernomas in certain cases associated with underlying DVAs (Fig. 7.7). Brain damage was noted in 20% and hydrocephalus in 24% (Table 7.1). The other clinical presentations were cranial bruit, facial vein dilatation, and intracranial hypertension (ICT), the latter being associated with macrocrania. Few cases were diagnosed almost incidentally because of scalp hemangiomatous lesions or other midline vascular abnormalities. Most of the lumps noted were located at the vertex at the junction with the lambdoid suture, some of them representing a sinus pericranii equivalent (with a patent yet malformed sinus) (Figs. 7.8–7.11). MRI should be obtained whenever possible in these patients, as it demonstrates best the dural sinus anomaly and its draining pattern, as well as the status of the underlying brain. Other tools to analyze the hemodynamics in these lesions have so far not provided additional information leading to a better understanding, nor have they helped in the decision-making process. Angiography and embolization, if deemed necessary, should be performed during the same session, as most of the features encountered will be predictable. In neonates and infants in the absence of congestive cardiac failure (CCF), satisfactory imaging of the cerebral drainage of the brain must be obtained by selectively injecting the internal carotid artery rather than global injections that confuse drainage of the lesion with drainage of the brain. Precise venous analysis is more important than knowing the actual arterial supply to the mural AVS. It determines the importance, the speed, and the area where the endovascular approach should be targeted as well as the timing of the sessions.

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Fig. 7.7A–D. Legend see p. 403

▲

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403

Fig. 7.7A–F. A 5-year-old boy who presented with a failure to thrive, an objective intense bruit of which he did not complain, moderate macrocephaly, dyspnea with effort, and poor school performance. A Chest X-ray shows moderate enlargement of the cardiac silhouette. B Intravenous digital angiography demonstrates a large supratentorial venous lake derived from the left lateral sinus. C Coronal enhanced CT. Selective injections in the left internal carotid (D) and maxillary artery (E) demonstrate the multiple feeders to the pouch (supratentorial) (arrow and double arrow); infratentorial, transosseous, and vessels on the right side supplied the lesion (not shown). The shunt was well controlled by incomplete embolization and the systemic effects of the shunt on growth and school performance abated within 1 year. F Follow-up showed a moderate decrease in the size of the venous mass and the presence of an underlying cerebellar DVA

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Fig. 7.8A–C. A 6-month-old girl presenting with a calvarial hemangioma (A). MR and angio-MR demonstrated an underlying DSM as well as a possible communication between both lesions (B, C). D,E see p. 405

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405

Fig. 7.8. (continued) A 6-month-old girl presenting with a calvarial hemangioma (A). MR and angio-MR demonstrated an underlying DSM as well as a possible communication between both lesions (B, C). Angiography confirmed the DSM and showed the so-called hemangioma to correspond to an emissary venous communication for the superior sagittal sinus mimicking a sinus pericranii (D, E)

Among the six patients with brain damage, five died and one was lost to follow-up. The cause of death was ICH in two, IVH in one, and uncontrollable high ICT with tonsillar prolapse in the remaining two. In four patients who presented without brain damage, diagnostic angiography showed no cavernous capture with involvement of torcular; the progression was poor in three (two died) and good in one. The patient with good progression did not have satisfactory delayed venous phase imaging to evaluate the cavernous capture; however, alternate pathways were likely sufficient. In this group of patients, the absence of cavernous capture and the involvement of torcular gave rise to an unfavorable neurological progression related to spontaneous thrombosis of the torcular. Under these circumstances, timely diagnosis and treatment is crucial, in order to avoid early torcular thrombosis before the cavernous sinus capture occurs.

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▲

Fig. 7.9A–D. Large middle cranial fossa (epi)dural sinus malformation following the path of the embryonic tentorial sinus. The lesion was incidentally discovered in view of hemangiomatous lesions on the ipsilateral face and skull (E). Spontaneous thrombosis occurred without significant clinical expression (F–I). However, careful analysis of the cerebral venous drainage showed severe pseudo-phlebitic remodeling (J, K), constituting a potential risk for seizures in the future. F–K see p. 407

Fetal and Postnatal Changes of Sinuses

Fig. 7.9F–K. Legend see p. 406

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Fig. 7.10A–D. A 2-year-old child (A) presenting with ipsilateral DSM (B, C) and facial soft tissue lesion much larger than the small AVM demonstrated on the angiogram (D)

Seven patients presented without brain damage, with partial or no cavernous capture, and the DSM was located some distance from the torcular. The follow-up showed six patients with good progression (six cured) and one with poor progression. The patient with the poor progression showed a progressive increase in the size of her malformation for 9 months and later died from intracranial hemorrhage due to associated cavernomas. Another patient presented without brain damage, bilateral cavernous capture, jugular bulb dysmaturation, but no pial, straight sinus, or SSS reflux. This patient had his mural AVS embolized with good progression in time. Five patients presented without brain damage, bilateral cavernous capture, jugular bulb dysmaturation and reflux into pial veins, straight sinus, or SSS. These patients were embolized transarterially for their arteriovenous shunt (AVS) and transvenously by coils to disconnect the pial vein openings. Four patients had good subsequent progression. One of them had stable progression for 18 months and later presented with an intraventricular hemorrhage due to persisting pial reflux.

Fetal and Postnatal Changes of Sinuses

Fig. 7.11A–C. A 3-month-old child presenting with macrocrania and a subgaleal mass. Clinical examination demonstrated a large pulsatile mass and intracranial bruit. Angio-MRI showed a large, partially thrombosed superior sagittal sinus, torcular, and straight sinus DSM. There was a large meningeal supply converging to the various pouches

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Fig. 7.12A–C. A 4-month-old boy presenting with an intracranial bruit. MRI performed at 7 months of age showed a complex malformation of the superior sagittal sinus initially demonstrated with a decrease in the intralesional flow and a partial thrombosis (A). No therapeutic decision was taken. The child presented at 8 months with a bilateral venous infarction with hemorrhage and ventricular rupture (B, C)

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Fig. 7.13A, B. Neonatal diagnosis of lateralized DSM preserving part of the torcular and one lateral and sigmoid sinus. Symptoms included intracranial bruit and macrocrania. A coagulation disorder (Kasabach-Meritt-like syndrome) was noted in this particular patient. Lymphatic malformation of the cranial cervical region was also diagnosed. (Courtesy of G. Wilms)

The other patients with better progression had lateralization of the DSM or a location away from the torcular on the SSS, allowing the brain to drain through the contralateral sinus or via the Labbé veins downstream from the DSM. In three patients from this group, a spontaneous cure with remodeling of the sinuses was observed. The clinical problem created by the dural sinus malformation is determining to which extent the venous outlets of the brain have been diminished and the additional overload into the sinus by the AVS. The endothelial properties of the malformed portion of the dural sinuses are also altered. Spontaneous thrombosis is common and spreads rapidly in certain forms (midline giant lakes associated with DVAs opening into the malformed sinus; Fig. 7.12). It may lead to complete occlusion of all venous outlets and sometimes coagulation factor consumption syndromes (Fig. 7.13). Bilateral venous infarctions are usually seen when spontaneous occlusion of the entire pouch occurs and can sometimes be promoted by endovascular embolization of the associated AVS. In one case, a venous stroke was demonstrated unilaterally on MRI but was still clinically asymptomatic (Fig. 7.12). In other situations, the available venous outlets remain sufficient for a while, and the manifestations will mostly be subacute, associated with convulsive episodes or focal intracerebral (Fig. 7.14) or subdural hemorrhages. If the lesion is still not recognized and properly managed

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Fig. 7.14A–C. Neonatal diagnosis of dural arteriovenous shunt in which MRI suggested A torcular and B left-sided DSM. Macrocrania and ventricular dilatation led to ventricular shunting. C At 7 months, the child presented with a large, right-sided hematoma. Note the secondary thrombosis with tonsillar prolapse and a slow-flow signal in the midline and left-sided sinus

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413

Fig. 7.15A–D. A 1-month-old boy presenting with mild cardiac overload that was not treated and progressive macrocrania with a large ventricle. Magnetic resonance imaging (A) and angiography (B, C) confirmed the DSM with bilateral thrombosis of the sigmoid sinus. Persistence of occipital and marginal sinus offered insufficient venous outlet. Note the melting-brain syndrome (D)

at this already eloquent phase, then melting-brain syndrome will eventually occur (Fig. 7.15), usually remote from the DSM site, where the venous constraints are maximum (see Chap. 2, this volume). These lesions are often seen in utero, and therefore early correction of the AVS and preservation of the remaining venous outlets seems to be a logical immediate goal. Yet similar to VGAMs and CAVMs, early delivery is not recommended, as we will then face an even more immature vascular system in a patient who needs emergency treatment. It appears that the

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therapeutic window following the first symptoms for these technically challenging lesions is quite narrow. In some instances, the delay between the first symptom and referral is such that irreversible brain damage has already occurred. In others, the impact of the malformation is such that the thrombosis has compromised the only remaining cerebral drainage. In these situations, regardless of the techniques available, the child will develop cerebral hemorrhagic infarction. In some of the less extensive forms of the malformation, we have successfully occluded the associated AVS in an emergency procedure, despite minimal or even absent symptoms (Fig. 7.16). Heparin treatment following the AVS occlusion has been used to keep the only patent jugular vein open. In other cases, the demonstration of alternative draining pathways for the brain may allow the transvenous exclusion of the venous lake or in such rare and favorable situations, the AVS and the DSM lake may thrombose spontaneously (Fig. 7.17). These children grow normally and have a normal neurocognitive status for their age. The key angioarchitectural features that will influence the natural history and therefore prompt immediate endovascular preventive or corrective measures are the following (Barbosa et al. 2003) (Scheme 7.2):
DSM involving the torcular: noted in 14 patients (46.6%) (Table 7.2; Figs. 7.16–7.19; Scheme 7.3).
Pial, straight, and superior sagittal sinus reflux: present in 15 patients (50.0%) (Table 7.3; Scheme 7.4).
Dysmaturation of the jugular bulb (postnatal occlusion of the jugular bulb and retrograde thrombosis of the sigmoid sinus) demonstrated in 16 patients (56.0%) (Table 7.4); persistence of a medial occipital sinus by-passing the occluded jugular bulb must be looked for (Schemes 7.5, 7.6).
Total bilateral cavernous sinus capture (drainage of deep and superficial sylvian veins in the cavernous plexus) seen in 14 patients (46.7%).
Partial cavernous sinus capture present in eight patients (26.7%).
No cavernous sinus capture was noted in eight patients (26.7%) (Table 7.5). The treatment includes endovascular techniques (transarterial or transvenous), often associated with medical management with heparin. The choice of embolization material is either glue or coils and in some cases both. Some neonates or young infants are not embolized due to either preexisting brain damage or a low Bicêtre admission score at the time of consultation. The therapeutic options depend on the individual case’s angioarchitecture and state of the maturation or dysmaturation process. When there is partial or no cavernous capture and no pial reflux, there is an option of treating with heparin and embolizing the shunts with glue, with the expectation that cavernous capture will take place with minimal or no consequences for the hydrovenous equilibrium of the maturing brain and granulations. If there is significant AV shunting causing pial reflux or adding to restricted outlets, embolization is necessary to prevent venous hypertension and cerebral ischemic damage. The goal is to reduce to pial reflux, realizing that the shunts may preserve the patency of the sinuses. If the dural AVSs are completely

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415

Fig. 7.16A–H. Neonatal diagnosis of left-sided capillary hemangioma of the face. A, B Clinical examination led to diagnosis of large dural malformation involving the left sigmoid and lateral sinus and reaching the left side of the torcular. C, D A highflow fistula into the sinus from the middle meningeal artery was embolized at 6 months. Considering the already existing venous restriction (tonsillar prolapse), the contralateral jugular vein narrowing, and the restriction in the cortical vein drainage, the child was treated with low-molecular-weight heparin for 5 months. At 16 months of follow-up, the hemangioma was stable, the occlusion of the fistula was confirmed, and the child was normal on neurocognitive evaluation. Left-sided hyperemia persisted, corresponding to a large hemangiomatous phenomenon with no dural sinus communication, but the tonsillar prolapse subsided (E, F). G, H Associated cutaneous lesions. E–H see p. 416

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Fig. 7.16E–H. Legend see see p. 415

Fetal and Postnatal Changes of Sinuses

417

Fig. 7.17A–C. A 2-month-old boy presented with macrocrania. A, B Early MRI already demonstrated tonsillar prolapse related to posterior fossa venous congestion secondary to superior sagittal sinus dural malformation, partially thrombosed, but remote from the torcular. Conservative treatment was chosen. Spontaneous thrombosis of the lesion occurred 12 months later and produced a significant reduction in the size of the lesion. C The superior sagittal sinus distal to the lesion reduced in size. The torcular remained patent, as did the sigmoid sinus bilaterally. The tonsillar prolapse resolved

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Scheme 7.2. Effect of the spontaneous or induced thrombosis of dural sinus malformation according to type and occurrence of maturation processes

Table 7.2. Location of the dural sinus malformation (Barbosa et al. 2003)

Favorable progression Unfavorable progression No follow-up Total no. of patients

Torcular involvement

No torcular involvement

4 (28.6%) 10 (71.4%) 0 14 (46.6%)

13 (81.25%) 2 (12.5%) 1 (6.3%) 16 (53.3%)

Fetal and Postnatal Changes of Sinuses

Fig. 7.18A–F. Legend see p. 420

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Fig. 7.18A–I. At the age of 9 and 11 months, this child was medically treated for leftsided seizures. At 1.5 years, the child sustained a cranial trauma and was submitted to surgery for drainage of a right temporo-occipital subdural hematoma. A–C Digital subtraction angiography (DSA) showed a dural arteriovenous fistula (DAVF) in the left sigmoid/transversus sinus. D Angiography and embolization using the venous approach; E–G 4.35 m of 38 guidewire was delivered into the left lateral and sigmoid sinus. H–I Six months later, angiographic control showed no arteriovenous (AV) shunts. The child is currently still well and without complications. Note the patency of one sinus and the quality of central drainage (Courtesy of R. Piske)

Fetal and Postnatal Changes of Sinuses

421

Fig. 7.19A–C. A 1-month-old girl presented with a generalized seizure and macrocrania. A MRI shows mild ventriculomegaly with large subarachnoid spaces. There was evidence of a right-sided subdural hematoma. B Angiography demonstrated lateralized dural sinus malformation with a venous lake and adjacent arteriovenous shunting. C Several patent venous outlets remained; however, minimal tonsillar prolapse was already evident. The baby was partially embolized and low-molecular heparin was administered

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Scheme 7.3. Effect of cavernous capture

Table 7.3. Analysis of pial, straight sinus, or SSS reflux (Barbosa et al. 2003)

Favorable progression Unfavorable progression No follow-up Total no. of patients

Reflux

No reflux

6 (40.0%) 8 (53.3%) 1 (6.7%) 15 (50.0%)

11 (73.3%) 4 (26.7%) 0 15 (50.0%)

Fetal and Postnatal Changes of Sinuses

Scheme 7.4. Effect of jugular bulb dysmaturation

Table 7.4. Analysis of jugular bulb dysmaturation

Favorable progression Unfavorable progression No follow-up Total no. of patients

Jugular bulb dysmaturation

No jugular bulb dysmaturation

6 (37.5%) 9 (56.3%) 1 (6.25%) 16 (53.3%)

11 (78.6%) 3 (21.4%) 0 14 (46.7%)

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Scheme 7.5. Effect of pial vein reflux with thrombosis

occluded, then the sinuses will likely also thrombose, resulting in the absence of outlets for the brain leading to poor outcome. The posterior fossa drainage and deep cerebral structures must be carefully analyzed. Associated deep DVAs are not rare, adding further to the clinical eloquence when involved by the reflux and to the extent of the infarction if thrombosis is to occur. The endovascular interventions include embolization of high-flow AVFs with glue (Figs. 7.20, 7.21), exclusion of converging DAVS into venous spaces by transvenous deposition of coils and separation of the DSM venous drainage from the normal brain drainage with coils (Fig. 7.22). Most techniques were combined, staged, and highly targeted. There has been no attempt to perform a surgical dural sinus bypass in our experience. Stenting of a highly symptomatic narrowed jugular bulb following thrombosis of the contralateral transverse sinus resulted in excellent immediate result but secondarily, stent stenosis and thromboses occurred, which was eventually resistant to several repeated angioplasties and anticoagulation therapy (Vilela et al. 2001).

Fetal and Postnatal Changes of Sinuses

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Scheme 7.6. Effect of pial vein reflux without thrombosis

Table 7.5. Analysis of cavernous capture

Favorable progression Unfavorable progression Lost to follow-up Total no. of patients

Total cavernous capture

Partial cavernous capture

No cavernous capture

10 (71.4%) 3 (21.4%) 1 (7.1%) 14 (46.7%)

5 (62.5%) 3 (37.5%) 0 8 (26.7%)

2 (25.0%) 6 (75.0%) 0 8 (26.7%)

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▲

Fig. 7.20A–I. A 6-month-old boy presented a torcular DSM (A) with a significant single AVF along the falx cerebelli (B, C). Selective embolization and glue deposition (D, E) allowed the previously dilated torcular (F) to shrink and remodel (G). Angiography confirms the quality of the venous remodeling (H, I). E–I see p. 427

Fetal and Postnatal Changes of Sinuses

Fig. 7.20A–I. Legend see p. 426

427

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Fig. 7.21A–F. Legend see p. 429

▲

Fetal and Postnatal Changes of Sinuses

429

Fig. 7.21A–H. A 6-month-old boy with lateralized DSM along the embryonic tentorial sinus (A–D). The lesion is partially thrombosed yet embolization with glue was performed in two sessions. Eight months later, the lesion was completely excluded and the remodeling completed (E–H)

In Barbosa’s series (Barbosa et al. 2003), the clinical progression of 14 (52%) conservatively treated patients was good in five out of 14 cases (35.7%) where favorable outcome was anticipated without treatment (four patients with spontaneous thrombosis) (Figs. 7.23, 7.24; Table 7.6). The progression was poor in nine of 14 cases (64.3%) where no acceptable therapeutic goal could be set and all patients died. Sixteen (53.3%) patients were embolized, 12 of 16 (75%) with glue via the transarterial approach; four of 16 (25%) were treated with glue and coils via the transarterial and transvenous approaches in the same or separate sessions. There was no morbidity or mortality related to the procedures themselves. Excluding the one patient lost to follow-up, the post-therapeutic follow-up period ranged from 3 to 84 months, with a mean follow-up of 3.6 years. The clinical progression of 16 embolized patients was good in 12 of 16 (75.0%) with eight of 12 (66.7%) cured, and was poor in three of 16 (18.8%) cases, as all patients died despite embolization. The analyses of the final clinical results are shown in Table 7.7. The initial score had been good (score, 3–5) in only 12 (50.0%). Good outcome scores were noted in 17 of 19 (89.5%) of the surviving children. Favorable clinical progression with morphologic exclusion was noted in 10 of 17 (58.8%) and conversely 11 of 12 (90.0%) with unfavorable progression died.

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Fig. 7.22A–F. Legend see p. 431

▲

Fetal and Postnatal Changes of Sinuses

431

Fig. 7.22A–H. A 1-year-old girl presenting with DSM with reflux into the straight sinus in relation to a bilateral dysmaturation of the jugular bulbs. Although the lesion is located at the torcular (A), the presence of a bilateral cavernous capture allowed for separation of the DSM circulation and that of the normal brain (B, C) prior to embolization. Five years later, the brain was draining normally (D, E); a posterior fossa DVA (F, G) drained into the superior petrosal sinus on the left. The lesion was nearly completely excluded but no longer presented a risk (H). Nine years after the venous separation, the child was normal

Table 7.6. Clinical progression of patients

Favorable progression Unfavorable progression Lost to follow-up Total no. of patients

Embolized

Not embolized

12 (75.0%) 3 (18.8%) 1 (6.3%) 16 (53.3%)

5 (35.7%) 9 (64.3%) 0 14 (46.7%)

Table 7.7. Overall results Clinical situation

No. of patients

Favorable clinical progression Favorable clinical progression with morphological exclusion Unfavorable clinical progression Unfavorable clinical progression with death No follow-up

17/29 (58.6%) 10/17 (58.8%) 12/29 (41.4%) 11/12 (90.9%) 1/30 (3.3%)

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Fig. 7.23A–D. This infant is a neurologically healthy 37-week-old, 2,900-g, megaloencephalic, 37-cm head circumference female with no dysmorphic features. There is a generous dilatation at the posterior part of the sagittal sinus at the point where it meets with the transverse and straight sinuses. The dilatation is to the right of the midline without causing any hydrocephalus. Doppler revealed venous low flow into the defect. The diagnosis of DSM was made (A, B). Six months later, the normally developing lesion has thrombosed completely; despite large pericerebral spaces, the venous remodeling is normal (C, D)

Fetal and Postnatal Changes of Sinuses

Fig. 7.24A–E. A child a few days old with MR and MRA evidence of DSM (A–C). Angiographic evaluation shortly after failed to demonstrate residual AVS; venous remodeling is the only stigmata of the previously demonstrated DSM (D, E)

433

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7.3.2 DSM of the Jugular Bulb

There are some minor sigmoid sinus–jugular bulb junction malformations that are seen at a slightly later age than the major ones illustrated in the previous section. We consider them as belonging to the malformation group in view of the diaphragm-like obstacle present at the level of the jugular foramen. We postulate that the abnormal onset occurs late in the maturation of the high jugular bulb and after the marginal sinus thromboses. The development of the AVF from the mastoid branch of the occipital artery and the subsequent high-flow angiopathic changes appear to be secondary phenomena (Okudera et al. 1996). They are often asymptomatic and most of the time discovered incidentally because a pulsatile bruit is heard by the parents, the child’s teacher, or the pediatrician. The child does not complain of the bruit as it is part of his a normal acoustic environment. Silence secondary to the successful occlusion of the lesion may create a disturbance in the child’s attitude. Appropriate explanation and preparation of the child and parents is recommended. Conservative treatment is probably acceptable if alternative pathways are present early enough to offer the brain the hydrovenous equilibrium it needs for proper morphological and neurocognitive maturation. Yet the presence of a craniopetal reflux into the lateral sinus and toward the opposite side suggests a probable future risk for venous congestion (Fig. 7.25). Evidence of a pial venous reflux, even in asymptomatic patients, represents an indication for endovascular treatment (Fig. 7.26). These well-tolerated malformations have an excellent outcome following endovascular management.

▲

Fig. 7.25. A 15-month-old boy presented with progressive macrocrania for several months. The parents found a pulsatile right retroauricular mass. Physical examination showed a normally growing child with mild macrocrania. The anterior fontanelle was soft. Clinically, there was no tachycardia and there were no signs of heart failure. Developmentally, he had normal milestones. Angiography shows single AVF of the sigmoid sinus with jugular diaphragm (A, B). Selective catheterization and glue embolization of the occipital supply allowed complete exclusion of the lesion (C, D). Note the normal drainage of the brain (E) and the disappearance of the meningeal supply, although not embolized (F). (Kwong 2001)

DSM of the Jugular Bulb

Fig. 7.25. Legend see p. 434

435

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Fig. 7.26A, B. Male infant presenting at 7 months of age with macrocrania due to subdural hygroma. During shunt placement for drainage, large malformed vessels were seen. At the age of 2 years, facial collateral circulation was seen around the eyes and face bilaterally; a loud bruit was heard over the right suboccipital area. A, B Angiographic study showed a dural arteriovenous shunt with malformed sinus and pial reflux. At the age of 2 and 3 years, the child was embolized completely. At the age of 4, he was clinically normal and started preschool

7.4 Infantile Dural Arteriovenous Shunts (AVS) Infantile DAVSs are the most frequent type of pediatric DAVs in the literature. They are dural high-flow AVSs seen at various pediatric ages, often multifocal, with sinuses that are patent for a long time and the occurrence of induced pial AV shunts (Table 7.8). The difficulty in this disease entity is that the effects of high-flow angiopathy are usually not recognized as such. Some cases, although different in appearance, are in fact two stages of the same disease; conversely, two lesions that look the same and therefore are classified similarly may in fact be separate and different entities. Depending on the age at onset of the lesion, the symptoms will be different. Neonatal or infant onset is marked by CCF manifestations, which are rare and infrequently require emergency management. In most instances, the CCF is mild and discovered retrospectively because of an enlarged cardiac silhouette.As all the sinus outlets are still patent at this age, there are no neurological manifestations. Management of the CCF can be similar to that of VGAM, and neonatal scores can be applied when necessary. The dural sinus high flow is often associated with low venous sinus pressure because of the high velocity, and secondary hydrovenous complications are less frequent than one would expect. The drainage will be craniofugal for a long time, usually unilateral without contralateral dural sinus drainage reflux, despite the associated high flow. The hydrodynam-

Infantile Dural Arteriovenous Shunts (AVS)

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Table 7.8. Comparative anatomical and clinical features in neonatal and infantile dural vascular lesions

Etiopathogenesis Angioarchitecture

Progression Clinical progression Initial Secondary With treatment Name of lesion

Neonates and infants

Infants and children

Sinus malformation Unifocal giant pouches; spontaneous dural venous thrombosis; small, slow-flow shunts Acute

Secondary development triggered Multifocal; large sinuses without lakes; possible jugular bulb occlusion; induced pial AV shunts; high flow, high velocity Subacute or regressive manifestations

Systemic, convulsive Venous reflux, infarct/hemorrhage

Macrocrania Mental retardation/progressive neurological deficit, depending on secondary sinus occlusion

Unfavorable; depends on the degree of sinus malformation Dural sinus malformation with AV shunt

Infantile dural AV shunt

AV, arteriovenous.

ic disorders do not interfere with brain maturation to the same degree as they do in VGAMs at the same age, and mental retardation remains moderate. This explains why most of these lesions are diagnosed in children rather than during the first 2 years of life. Some of them seem to be secondary to a head trauma or facial or orbital surgery. Following a free interval of several years, the DAVS becomes symptomatic, since it is located some distance from the trauma or the surgical field. Two types of progression can be seen: persistent high flow and progressive outlet restrictions. The persistence of the high flow, but with low pressure in the large sinuses, creates several remarkable phenomena (Scheme 7.7). The first is the development of induced corticopial AVSs (Figs. 7.3, 7.27) with opening of the cortical draining veins into the abnormal sinus. The dural sinus sump effect creates a remote venous steal upstream; it is not symptomatic as such, but probably produces some degree of white matter venous ischemia over time. The natural history of these pial AVSs is not known and some will regress following occlusion of the primary dural AV shunt. The persistence of the latter is, however, sufficient to provoke the enlargement of these pial lesions over time and even some flow-related aneurysmal ectasias proximal to the pial AVS on their arterial feeders as well as the meningeal arteries (Fig. 7.28). Partial, targeted treatment of these pial AV communications may give the impression of improved security, without formal evidence of a preventive clinical effect. The risk of these induced micro-AVSs is unknown, and the rationale to treat them is extrapolated from our experience with pial cerebral AVMs (CAVMs). The second characteristic of this type of progression is the development of multifocality, the opening of different zones of AV shunting along the dural sinuses. They may be at the skull base unilaterally, but may also be located supra- or infratentorially (Fig. 7.29). This type of progression should be differentiated from converging bilateral supra- and infratentorial dural supply to a single arteriovenous zone. With such features, these

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Scheme 7.7. Natural history of infantile dural arteriovenous shunts (DAVS). In the literature, neonatal onset and the neonatal type are often confused. Neonatal onset is rare: 20 cases of neonatal onset have been published, and all types of dural AV shunts (malformation, infantile, adult) can be seen. DAVS accounts for 10% of all intracranial shunts in children

lesions express a strong angiogenic activity mostly on the venous side, with de novo AVS and shear stress-induced dural arterial aneurysms. Converging supply, while very common in children, is not specific for this age group, but rather represents the normal dural capillary angioarchitecture and its rapid local angioectatic response to the de novo AVS. The unfavorable influence of multifocality in this infantile type of DAVS depends on its overall impact of the total sump phenomena and the relative venous ischemia without reflux that progressively develops. With time, moderate macrocrania and mental retardation will be noted, while cranial nerve deficits are often the initial symptom. Alternative pathways through the cavernous sinus also produce corresponding proptosis, extraocular motor nerve palsies, and facial vein enlargement. The recruitment of all sinuses precludes their endovascular sacrifice; arterial embolization is always partial, and the disease’s progression in several foci is responsible for recurrences. These do not occur through reopening of proximally or insufficiently occluded portions, but following the development of new shunting zones in the vicinity of the ones embolized a few months after the last treatment. The second type of progression is more typical in this age group and is associated with a relatively higher dural sinus pressure. Subsequent to macrocrania, unilateral or bilateral jugular bulb stenosis and occlusion will (a) increase hydrodynamic manifestations, (b) provoke bilateral pial

Infantile Dural Arteriovenous Shunts (AVS)

439

Fig. 7.27A–F. Juvenile dural AVS. An 11-year-old girl with progressive hemiplegia on the left side with diplopia and severe headaches. Proptosis, intracranial bruit, and cerebellar syndrome were also noted. A Angiography demonstrated a high-flow arteriovenous shunt extending to the sinuses bilaterally, predominantly on the right side. In addition, there was B extension in the superior petrosal sinus and C a direct fistula on the sigmoid sinus. C–E Remote pial shunts were seen on the surface of the cerebellum (arrow in D) and supratentorial structures. Several embolizations with partial control of the shunting zone at the dural level improved the child’s condition. However, symptoms always recurred 3–8 months following each session. F The child eventually died with a posterior fossa syndrome at the age of 16 years. E,F see p. 440

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Fig. 7.27E,F. Legend see p. 439

venous congestion, and (c) rapidly lead to pial reflux, in addition to all the chronic effects of hydrovenous venous hyperpressure (Vilela et al. 2001). At this point, all the classical manifestations described in Chap. 2 of this volume may be encountered, including tonsillar prolapse (Figs. 7.15, 7.16, 7.27) and eventually syringomyelia (Fig. 2.28; Apsimon 1993). Neurological symptoms are either related to congestion without reflux and lead to seizures and transient deficit or mental retardation, depending on the degree of cavernous sinus capture, or to pial reflux with venous hemorrhage, seizures, and progressive deficits. Treatment of these forms seems easier, and progression to multifocality is rarely observed, suggesting that high velocity is the dominant trigger for this particular feature of progression. The sinuses remain large, despite the reduction in their outlets. In this type of DAVS, computed tomography (CT) does not give

Infantile Dural Arteriovenous Shunts (AVS)

441

Fig. 7.28A–C. Juvenile dural AVS. A young boy presenting in early infancy with macrocrania and ventriculomegaly that led to ventricular shunting. He was referred to us at the age 12 with an intracranial hematoma. Angiography demonstrated a complex dural arteriovenous shunting zone involving several sinuses. A–C Later, angiography showed dysplasic changes and all possible dural branches supplying the various sinuses converging to the surgical field. Note the aneurysms on the dural arteries. Following partial embolization, some of these dysplastic changes were augmented, despite significant reduction in the flow of the lesion and clinical improvement. Multiple embolization procedures were performed with transient improvement. He died at the age of 17 from irreversible posterior fossa syndrome without hemorrhage

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Fig. 7.29A–F. A 14-year-old boy with superior sagittal sinus lesion. Note the aneurysms on the middle meningeal artery (A, B); the cavernous capture ensures a satisfactory alternate drainage to the brain veins (C, D). There are some remote, induced cortical AVSs bilaterally (E, F)

Infantile Dural Arteriovenous Shunts (AVS)

Fig. 7.30A–F. Legend see p. 444

443

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Fig. 7.30A–G. A 7-year-old girl presented with cervical pulsatile mass in relation to a dilated jugular vein. Mild headaches were noted at that time. Arterial and venous ligations are done at the neck level. Three years later, she was referred to us with macrocrania at 4 standard deviations. The skull base lesion was transformed as was its drainage, both retrograde with pial reflux and extracranial bypassing the ligation via the inferior petrosal sinus (A–C). Progressive exclusion of the reflux by venous disconnections and arterial embolization made it possible to fill the sigmoid sinus stump with coils (D–G)

enough information, particularly in infants in whom white matter maturation needs to be assessed and followed. The patency of the jugular bulbs and sinuses can be well demonstrated.Angiography is currently the only way to explore these lesions and to collect the necessary diagnostic and prognostic information for treatment planning. Incomplete surgery and neck or remote ligations have deleterious effects (Fig. 7.30). The scores presented in Chap. 2 of this volume are applicable to this pathology. The natural history of these lesions is consistently poor in our experience, with few cases of survival at young adult age despite repeated embolization sessions.

7.5 Adult Type of Dural Arteriovenous Shunts in Children The adult type of dural AVSs in children tends to develop within the sinus wall or the ventral epidural space (Table 7.9). Of the possible causative triggers, thrombosis is certainly the one most clearly recognized. Trauma of various origins may also create secondary dural shunts that are obviously different from the traumatic injuries leading to an AVF (see Chap. 16, this volume). We already referred to the shunts remote from the area of direct trauma or at a distance from a surgical field in cases of postoperative DAVSs.With this type of etiology, the time elapsed between the trauma and the diagnosis of the dural shunt can be as long as several years. These posttraumatic or postsurgical lesions are notably different from those described with the infantile type of DAVSs. The latter show an unsuppressed persistent angiogenic activity, whereas the former are a focal angiogenic wound healing phenomenon. This so-called adult type of DAVS may be encountered in young children. Several cases of neonatal cavernous plexus fistulas have been reported with successful embolization with Gelfoam (absorbable gelatin sponge; Ahn 1983) or coils (Konishi et al. 1990) or even with spontaneous regression (Vinuela et al. 1984; Yamamoto et al. 1995). Although these lesions are managed in a similar fashion to the adult lesions, the treatment should be as conservative as possible.

Adult Type of Dural Arteriovenous Shunt in Children

445

Table 7.9. Dural sinus malformations and arteriovenous shunts

Prognosis High flow, high velocity Sinus thrombosis (induced or spontaneous) Hydrodynamic disorders Neurological symptoms Bruit Sinus pouches Induced pial AV shunts Transdural (pial) supply Multifocal dural lesions Intracranial hemorrhage Seizures Bone thickening

Dural sinus malformations

Infantile type

Adult type

Poor + +++

Poor +++ +

++ (Macrocrania) + (Pial congestion) Incidental ++ – – – + (Venous infarction without pial reflux) – –

++ (Macrocrania) + (Pial congestion) + + + ++ ++ + (If sinus occlusion and pial reflux + (Calcifications) + (If sinus thrombosis)

Often excellent – + (Psychiatric manifestations) ± (Papilledema) + (If pial reflux) ± – – + (With thrombosis) + (Poorer prognosis) + (If pial reflux) hemorrhagic venous infarcts + (If pial reflux) –

+++, Very frequent; ++, frequent; +, possible; –, not seen.

The long-term follow-up of DAVS treated with sacrifice of sinuses has shown that, in some cases, a new DAVS develops in a previously normal region. It is therefore strongly recommended to avoid the sacrifice of a sinus that is still patent for the purpose of treatment of a dural lesion that does not present any neurological danger for the child. Post-thrombotic changes determine the possible risk for neurological symptoms; this is a rare transformation in adults and has never been seen in children for this type of DAVS. It is suggested that they are secondary to endovascular treatment, as demonstrated in adults (Satomi et al. 2002). The favorable spontaneous thrombotic occurrence of the shunt itself in the adult type of DAVS seems to be a classic phenomenon. The symptoms in children are probably more rapidly eloquent than in adults, where the progression has been silent for a long time. In the pediatric population, sigmoid sinus DAVSs are rare; cavernous sinus sites are the most frequently reported, and multifocality has not been described (Figs. 7.4, 7.31). Extrasinusal DAVS (dural-subdural, osteodural) have not been encountered. The presence of an intracranial bruit is rarely spontaneously mentioned by the child, despite the fistulous nature of the disease. The frequency of cavernous sinus lesions draining anteriorly may not even cause an objective bruit. A subjective complaint of bruit would certainly confirm the recent character of its change (or occurrence). Difficulties at school are sometimes the only symptom that allows us to trace the onset of the acoustic interference. The presence of a bruit and the CT or MRI evidence of the lesion establishes the diagnosis, but they are not sufficient to provide all the necessary pretherapeutic information;

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Fig. 7.31A–D. A 4-year-old boy presenting with a spontaneous mid-cranial fossa fistula involving the middle meningeal artery and draining into the ipsilateral ophthalmic vein (A). Clinical manifestations were those of the usual type of cavernous sinus draining lesion with exophthalmos and cranial nerve palsy. B Embolization was performed in the same session. C, D Diagnostic angiography was performed and complete occlusion of the lesion was obtained. Following embolization, after 3 years of follow-up, the initial symptoms have completely disappeared

in particular, the cerebral venous drainage must be thoroughly analyzed, which requires angiographic assessment. Most of the feeders can be predicted, but the development of potential alternative pathways should be demonstrated and their compliance evaluated. Angiography is still the only way to assess the information needed for proper treatment planning.

Dural Supply to Pial Cerebral Arteriovenous Malformations

447

7.6 Other Dural Shunts In this section we have regrouped diseases as well as the normal responses of the meninges as a differential type of diagnosis, but also to illustrate the variety of triggers that can create dural AV shunts. Careful analysis will assist in differentiating between the transdural resupply to normal brain, clot colonization with angiogenesis, and the dural location of general disorders.

7.6.1 Vein of Galen Aneurysmal Malformation

Dural shunts have been seen in four different instances in children presenting with VGAM: 1. Following thrombosis of the sigmoid sinuses upstream from a jugular bulb occlusion (Fig. 3.53) 2. Following a direct, surgical, incomplete approach to the VGAM 3. In premature babies with severe arterial occlusion of the cerebral arteries 4. Remote from the lesion, transiently in the superior sagittal sinus (Fig. 3.53) Although they complicate the angioarchitecture of the VGAM disease, they are in fact not disease-related, but correspond to a predictable response by the sinus wall or meningeal arteries to certain specific triggers. Blood clot represents a stimulus to angiogenesis, and cerebral ischemia is also an active trigger to the development of these DAVS (see Chaps. 3–5, this volume). Surgery is an additional factor that may induce some of these responses. These shunts are asymptomatic, and many of them are actually vascular compensating mechanisms; they need to be preserved and should not be treated. We have not observed direct dural supply to the venous pouch in a genuine VGAM; however, enlargement of dural arteries at the falx–tentorial junction can be identified in some children, indicating the effect of high flow over time, as in any dural sinus. The dural involvement described above in VGAM is different from the vein of Galen DAVS described by Fournier et al. (1991). Clearly, this significant difference points to the nature of the two veins involved: the medial vein of the prosencephalon (choroidal collector vein bringing the plexus to the primitive sinus across the subarachnoid space) and the true vein of Galen (a dural sinus bulging into the subarachnoid space to collect cerebral venous blood). Classifying a VGAM as a DAVS is therefore erroneous.

7.6.2 Dural Supply to Pial Cerebral Arteriovenous Malformations

In CAVMs, dural communication can occur in children. This feature is part of the arterial angiopathy response of late development compared to the venous response. Three situations can create dural contribution to the CAVM or to the adjacent brain, and sometimes to both (see Chap. 5, this volume).

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1. Thrombosis may give rise to dural or transdural supply and eventually AV shunting. It should be remembered that, with the exception of the true vein of Galen, no intradural vein has vasa vasorum. Therefore, only associated sinus thrombosis or vein of Galen dilatation can give rise to an intraluminal angiogenesis draining into the remaining patent portion of the otherwise thrombosed channel. 2. In the pial vasculature, high-flow angiopathy is known to produce adventitial angiogenesis. This is different again from the previous DAVSs associated with CAVMs. However, the transdural supply to CAVM directly and/or to the adjacent cerebral arteries certainly requires this adventitial angiogenesis. Local ischemia and superficial bleeding episodes are well-known triggering factors for such a dural contribution. 3. Surgery to the lesion or removal of a hematoma establishes pathways for new vessels across meningeal compartments. Cutaneous supply through burr holes is frequently seen in older patients with CAVMs. However, there is rarely supply to the brain associated with previous ventricular shunting. Since the burr holes in this situation are remote from the CAVM location, local effects of the surgical angiogenic triggers and the specific sensitivity of the CAVM region to such stimulation can be postulated.

7.6.3 Proliferative Angiopathic Disease

Dural contribution in proliferative groups of angiopathy can be spectacular. It corresponds to an alternative supply and should be preserved as such. Surgical approaches to proliferative angiopathy and moyamoya disease tend to use the same capacity of the dural arterial network to take on the supply of the incapacitated cerebral vasculature. It is difficult to know in these cases whether this response is the result of the normal explosive angiogenic factors of the disease itself or the normal response to a particular trigger. What looks like a disease in fact preserves neurological function and makes therapeutic decisions difficult. We believe that it corresponds to an uncontrolled response to a nonproportional ischemic trigger (see Chap. 18, this volume).

7.6.4 Systemic Disorders

Several systemic diseases are known to give rise to various types of AVS in adults. These findings are exceptional in young children, in particular at the dural level. Large vessels are likely to be involved in these sites rather than meningeal arteries. Single-hole multifocal AVFs in HHT (hereditary hemorrhagic telangiectasia or Rendu-Osler-Weber) disease and vertebro-vertebral fistulas have been reported in children and young adults. Multifocal CAVMs in neurofibromatosis-1 (NF1) can also be seen.

Recurrence in Intradural AVS and Secondary Transdural Supply

449

7.6.5 Recurrence in Intradural AVS and Secondary Transdural Supply

Incomplete and proximal embolization triggers angiectasia and regional collateral circulation. It may end up creating an area of shunting larger than the primary nidus if in addition some degree of local ischemia has resulted from the proximal occlusion. The greater the iatrogenic ischemia, either direct or secondary to a blood flow rerouting after embolization, the higher the chances of producing a transdural contribution. However, this transdural supply has to be understood as the normal response to an abnormal demand. It may look poorly adapted, with direct contribution in the area of the shunt or remote in a healthy region. Any intravascular clotting or extravascular blood triggers angiogenesis as a normal response aiming to digest the blood products. Yet in some instances, this phenomenon escapes control and seems to remain rather than being transient. There are probably situations where inflammatory reactions induced by emboli (or other foreign bodies) may further trigger this cascade (Figs. 4.13, 5.13, 5.22, 7.32). Such changes must correspond to a distorted recruitment or response of the angiogenic capacities in relation to the vascular malformation as the source of abnormal signals. The focal, local, or regional characteristics of the response as well as its duration are unpredictable; they seem more exaggerated in children than in adults. The recruitment of the AVM draining vein for the recurrence (whether hemorrhage or intervention) confirms the focal character of the phenomenon and the persistence of the lesion rather than a hyperemic scarring reaction. As most AVMs do reveal, they go through an angiogenic phase at this time– unrepressed, unnecessary abnormal production– yet this event is self-limiting in time, since a nidus does not grow except in the situations mentioned above and with high-flow angiopathic changes (Chap. 5, this volume). It seems that the older (on an embryological time scale) the causative event, the higher the chances of seeing new AVMs appear or an AVM nidus expand as in CAMS (Figs. 6.13, 6.15); full involvement of a given cephalic segment may express over 28 years (Fig. 6.7). From empirical observations, such angiogenic responses are linked to the arterial capillary side and will be encountered in special lesions such as PHACE, proliferative angiopathy, CAMS and some special conventional AVMs (Table 6.3) (Scheme 6.1). Such observations further support the fact that hemodynamics generate multiple signals and triggers to complex biological cascades and homeostatic systems. The concept of compliance of the host to an AVM (that we introduced nearly 20 years ago) as the key factor to anticipate the natural history and response to treatment is still valid. AVM approaches (classifications, hemodynamics, etc.) should not be overestimated in comparison to host parameters to overcome the effects of the malformation considered as a biological disease (abnormal signal emission). A special type of recurrence is related to the vein of Galen structure: the only intradural vein to have vasa vasorum. This feature can lead to a very particular type of post-therapeutic recurrence remote from the site of the initial AVM. This event has not been observed again; it combined several regional triggers to a partially clotted ectatic vein of Galen (Fig. 7.32).

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Fig. 7.32A–F. Legend see p. 451

▲

General Remarks on Treatment

451

Fig. 7.32A–F. Cerebellar AVM (A, B) cured by embolization and surgery. The followup angiogram 6 months later showed a newly developed AV shunt in the lumen of the partially thrombosed vein of Galen (C–E). Retrograde catheterization of the vein of Galen allowed the placement of a few coils and promoted complete exclusion of the shunting zone (F)

7.7 General Remarks on Treatment The diagnosis of a DAVS in a child leads to different diagnostic and treatment strategies depending on the age and type of lesion involved. Some general precautions should be kept in mind. In neonates, invasive studies are warranted when therapeutic management is urgently required. Multiple noninvasive examinations are often unnecessary for the proper decision-making process. At all ages, primary assessment of the situation is best achieved by good clinical examination and high-quality MRI. Proper visualization of the skull base should be obtained (including sagittal, coronal, and axial imaging) to demonstrate the posterior fossa venous outlets. It is only in exceptional cases that MRI and clinical information does not enable us to make the diagnosis of DAVS in the pediatric population. Angiography is a pretherapeutic examination. The place that Doppler ultrasound and endoluminal hemodynamic monitoring may have in the management of these lesions has not yet been clarified. The immediate prognosis is not related to flow characteristics, and treatment evaluation and follow-up cannot reliably depend on results of flow studies. Follow-up evaluation will, therefore, be based on MRI (with contrast enhancement) and less often angiography aiming to evaluate the venous drainage of the growing brain. The goal of treatment in each type of DAVS is difficult to establish, as patency of the sinuses must be preserved in most cases, since their thrombosis can produce extensive venous cerebral infarction. Transarterial embolization is, in our experience, the optimal approach to these lesions. The use of liquid agents such as N-butyl cyanoacrylate (NBCA) constitutes the only guarantee that partial or complete occlusion will remain stable. The recanalization observed with other agents is unacceptable in such children, for whom the therapeutic window for intervention is short. In addition, recanalization in children is sometimes more difficult to manage than the primary architecture. Arterial coils tend to produce proximal occlusion and collateral circulation that is often unreachable, necessitating secondary complex and hazardous management. An attempt to be definitive is particularly crucial in this group of diseases, and careful diagnosis and treatment planning is essential. Partial targeted treatment can be proposed in order to remove the risk of focal brain damage using a transarterial or transvenous approach to close the pial venous reflux (coil occlusion of the Labbé vein opening into the sigmoid sinus or in the straight sinus to stop reflux into the area) (Figs. 7.22, 7.31). This type of venous rearrangement must be preceded to some extent by AVS reduction by arterial embolization.

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Transvenous embolization of cavernous sinus lesions can be discussed in some cases; however, considering the quality of the results obtained by the arterial route and the need to use an arterial approach even in preparation for the transvenous approach, makes us favor the arterial route as the primary approach in children. The transvenous approach through the femoral vein or after direct approach to the sinus can be proposed if the analysis of the cerebral venous drainage has been done correctly (Fig. 7.18). It is unlikely that immediate complete exclusion of the DAVS is necessary in all cases. The long-term result of transvenous stent placement in order to preserve brain venous drainage in the presence of progressive jugular stenosis is still unsatisfactory despite its temporary early benefit (Vilela et al. 2001). In our experience, surgical management of such situations is required in exceptional cases, for example to remove spontaneous hematomas that are poorly tolerated. Ventricular shunting carries the same hazards as mentioned in Chap. 3 of this volume; and anticipation of ventricular enlargement should lead to early endovascular treatment to eliminate the risk of active hydrocephalus. We tend to use heparin for 1 week and low-molecular-weight heparin for 8 weeks until the next angiographic follow-up in order to preserve the patency of a (partially) malformed sinus. In some instances, the treatment is decided even before angiography has been performed. Progression is satisfactory if the exclusion of the initial AVS and malformed lakes results in remodeled patent cerebral venous pathways. The tools now available allow us to treat almost any type of circulation shunt to reduce or exclude it completely. The size and weight of patients are only relative limiting factors for any team accustomed to performing endovascular procedures in neonates and infants. The major problem is actually not a technical one, but a conceptional one. As seen for VGAMs, prediction of the natural history and anticipation of the next pathophysiological stage in a given patient constitute the ultimate goal for the specialist involved in the management of such different entities. The world (published) experience for such diseases (21 cases prior to 1995; Morita et al. 1995) shows the confusion that can result from reviewing a succession of anecdotal successful or failed management strategies. In such meta-analyses, reference to various hypotheses that mix incompatible analyses in an attempt to be consensual adds further to the mystery and fatalism accompanying dural vascular lesions in children. Reference to adult DAVS and inclusion of VGAM in this group is a dangerous academic exercise if they form the basis for heroic or inappropriate therapeutic management strategies. One can even question the academic value of a successful treatment based on the wrong concept and the result of an incomplete analysis. Over the past 18 years, we have been consulted in 52 cases of DAVS in children. The distribution in each group does not reflect the true occurrence of the disease, but rather our specific interest and referral patterns. The outcome of pediatric DAVS management even by experienced teams is still far from satisfactory.

General Remarks on Treatment7.3 Dural Sinus Malformations

453

However, our recent capacity to separate the different forms of progression of the disease in children with DAVS is helping us with their management in a dramatic fashion. The diagnostic tools (scores), clinical understanding, and therapeutic window concept developed in VGAM and CAVM patients are also applicable to pediatric DAVSs, as the mechanisms of clinical eloquence and progression are similar in the same age groups, regardless of etiology (see Chap. 2, this volume). The evidence that some of these DAVS are lethal 10 years after onset indicates the caution with which we must approach our decisions. The results of longterm follow-up should discourage unrealistically optimistic case reports advocating novel aggressive endovascular approaches.

8 Venous Anomalies and Malformations

8.1 8.1.1 8.1.2 8.1.3

Developmental Venous Anomalies 455 Single Abnormalities 455 Associated Features 459 Associated Cavernomas 473

8.2 8.2.1 8.2.2 8.2.3

Segmental and Nonsegmental Cerebro-orbito-facial Venous Lesions 478 Sturge-Weber Syndrome 478 From SWS to Cerebrofacial Venous Metameric Syndrome 485 Orbitofacial Venous Lesions 496

8.3

Complex Pseudo-metameric Cerebrofacial Venous Syndrome 499

8.4 8.4.1 8.4.2 8.4.3

Blue Rubber Bleb Nevus (Bean Syndrome) 503 The Association of BRBN with DVA 504 Cerebral Venous Malformations in BRBN 507 BRBN and HHT1 507

8.1 Developmental Venous Anomalies Developmental venous anomalies (DVA), the so-called venous angiomas, have baffled clinicians for many years (see Vol. 1, Chap. 7). Courville (1963) suggested that they constituted a “compensatory venous drainage” in the cortex, in what he described as a malformation. This compensatory system does not demonstrate increased incidence of rupture and is an adequate drainage mechanism. Courville made the same observation regarding the deep venous system and subependymal collectors, and his precise descriptions discuss the characteristic features of DVA, which, although rare, should therefore not be considered as vascular malformations. In the subsequent literature, most of the confusion arose from the misnomer and improper use of the term “angiomas” as a synonym for both arterial and venous malformations.

8.1.1 Single Abnormalities

DVAs must be considered as nonpathological normal venous pattern; therefore the term “developmental venous anomaly” (DVAs) was introduced (Lasjaunias et al. 1986a). The deep and superficial types of DVA (Valavanis et al. 1983) constitute the limits of variability of the transcerebral venous system (Saito and Kobayashi1981; Senegor 1983; Lasjaunias et al. 1986a; Jimenez et al. 1989; Rothfus et al. 1984). The deep varieties of DVAs drain the normal subcortical areas of the superficial medullary veins into the deep venous collectors (Fig. 8.1). The superficial group of DVAs occur in the super-

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Fig. 8.1. Typical appearance of deep-seated developmental venous anomaly (DVA) draining most of the cortical veins of the right hemisphere

Fig. 8.2. Typical appearance of the cortical drainage of the subependymal region of the left frontal horn. Angiography is not needed to confirm the diagnosis in such a typical situation

ficial medullary veins, which drain the deeper medullary regions into the cortical veins (Fig. 8.2). In both cases, visualization of the medullary venous system is not pathological, despite being unusual. This arrangement is compatible with the normal functioning of the area, as shown by the fortuitous manner in which most are discovered, i.e., in anatomic dissections or as incidental findings during CT, MRI, and angiography.

Single Abnormalities

457

According to other theories, an early (in utero) acquired venular occlusion, or regression, maintains the intrinsic venous anastomoses within the white matter; the DVA expresses an early collateral adaptation, but develops on a preexisting venous system that has been transformed. Both theories seem valid, but most DVAs are not associated with any sort of neural tissue damage or dysfunction. Thus the venous system remains adequate and the causal disorder, if it exists, is functionally negligible. It can hardly be imagined that a significant venous disorder (such as thrombosis) at an early stage of development would not be associated with some tissue abnormality (see melting-brain syndrome; see Chap. 2, this volume). To further exclude DVA from the group of malformations, it should be remembered that DVAs do not exist in the diencephalon, brain stem, or spinal cord, and they are only encountered where tectum derivatives exist (rhombencephalic, mesencephalic, telencephalic; Lasjaunias 1990; Berenstein 1992; Vol. 1). In children, in particular, thrombotic episodes may lead to DVA-like patterns, but DVAs can easily be distinguished from collateral circulations in the central nervous system (CNS) and venous system (see below). Although the former recruit pathways that have the greatest potential for enlargement and produce DVA-like patterns, they are never similar enough to cause misdiagnosis. The venous collectors of the DVAs follow a transcerebral course that can be demonstrated by CT or MRI examinations (Augustyn et al. 1985; Olson et al. 1984). Some DVAs are not detected with CT (Koussa et al. 1985) or MRI, but they are not angiographically occult. DVAs are opacified at the usual venous phase of angiography. Certain sites in the frontal or parietal regions show some capillary phase staining, which is sometimes wrongly considered to be abnormal (Hirata 1988; Simard et al. 1986; Lasjaunias and Berenstein 1990). These DVAs represent the sum of both the significant venular convergence (which is specific to DVAs) and the usual early drainage of the frontoparietal brain compared to the remaining brain. The analysis of intracerebral hemorrhage caused by a DVA in autopsy series shows a very low tendency to bleed when compared with true cerebral vascular malformations (arterial, capillary, arteriovenous, or cavernomas; Berenstein 1992). The discovery of a DVA during the investigation of a cerebral hemorrhage should raise the question of their etiological relationship (Gomori et al. 1986). DVAs undergo changes common to the aging process of the entire venous system. As an extreme anatomic variation, a DVA has a reduced flexibility (adaptability) that may lead to various venous ischemic manifestations (Figs. 8.3–8.5), including the following clinical symptoms:







Seizures Transient neurological deficit Headaches Macrocrania Mental retardation Cosmetic problems

These early ischemic signs (Berenstein and Lasjaunias 1992a; Burke et al. 1984; Kutscher et al. 1987; Pelez et al. 1983) may secondarily transform into hemorrhagic infarction (Fig. 8.3). This is an additional mechanism

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Fig. 8.3A–F. Legend see p. 459

▲

Associated Features

459

Fig. 8.3A–H. A 7-year-old child presented with an acute cerebellar syndrome in relation to an intraparenchymatous hematoma (A, B). Angiography demonstrated a focal AVF opening in a large DVA (C, D). Selective catheterization of the fistulous point allowed its elective embolization (E–H)

for the association of DVA and cerebral hemorrhage. This discussion is typical of the adult population, but does not constitute a common problem in pediatric practice. Bouchacourt et al. (1978) reported a well-documented case of thrombosis of a DVA that produced extensive venous hemispheric ischemia in a 37-year-old woman. Although the patient later (while under anticoagulation therapy) had a proximal iliofemoral venous thrombosis, the coagulation factor profile was not analyzed. Thus, despite all the clinical suspicions, DVA should be accepted as representing normal structures and should be treated neither by surgery nor by radiation. During a hemorrhagic episode, a cavernous malformation or other associated vascular malformation should be searched for and the DVA respected and preserved because of its role in draining normal brain tissue, even if its appearance is particularly unusual (Fig. 8.37). In case of an intracerebral hematoma associated with a large area of surrounding hypersignal on MR, a possible intra-DVA arteriovenous shunt should be looked for, in particular when investigations demonstrate no evidence of associated ruptured cavernoma or venous thrombosis.

8.1.2 Associated Features

DVAs may also be associated with tumors and other tumoral masses (Beers et al. 1984). Handa et al. (1984) reported a case of a deep DVA with an intracranial varix, discovered following a head injury. The varix seemed to result from an associated anomaly of the venodural junction, producing a secondary upstream ectasia of the venous collector of the DVA (Meyer et al. 1983; Handa et al. 1984).

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Fig. 8.4A–D. A young child presenting with a ruptured temporal DVA (A, B) associated with an upper parietofrontal AVM that has also produced an intracerebral hematoma (C, D). E–G Angiographic aspect of both unrelated lesions. E-G see p. 461

Associated Features

Fig. 8.4E–G. (continued) E–G Angiographic aspect of both unrelated lesions

461

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▲

Fig. 8.5A–C. A young child presenting with a focal melting-brain syndrome in relation to a DVA with no evidence of associated AVM. (A–D). E–G see p 463.

Associated Features

Fig. 8.5E–G. Legend see p. 462

463

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Fig. 8.6A–C. A 5-year-old boy presenting with a vascular lesion located on the midline and associated orbital phlebolith. Diagnosis of sinus pericranii was easily made. Note the association between transcranial drainage with a large bony defect (arrow) as well as an associated developmental venous anomaly (DVA). Despite the cosmetic problem, there was no neurocognitive problem. A Plain frontal skull X-ray. B, C Internal carotid angiogram in lateral early and late phases. Associated frontal DVA draining into a hemispheric vein (open arrow). Note the hyperemic aspect of the frontal parenchyma. A large pouch (arrows) is progressively filled and bulges subcutaneously after producing a well-circumscribed bony defect

Associated Features

465

Scheme 8.1. Vascular diseases according to the arterio-veno-lymphatic tree

Two associations are encountered in children: maxillofacial vascular malformations, in particular those of the venous (Boukobza et al. 1996) and lymphatic type (Figs. 8.32, 8.36), dural sinus malformations (see Chap. 7, this volume, and Scheme 8.1), multiple mucocutaneous venous malformations (MMCVM, or blue rubber bleb nevi or Bean syndrome), and cerebral cortical malformations (Barkovich 1988). Associated features of DVA in children include the following:










Maxillofacial venous malformations Maxillofacial lymphatic malformation Sinus pericranii Schizencephaly Pachygyria Microgyria Cavernomas Dural sinus malformation Multiple mucocutaneous venous malformations

What might cause a DVA to develop occurs at the embryonic stage and seems topographically unrelated to the type and segmental distribution of maxillofacial malformations. The association seems totally fortuitous and the DVA is rather considered as a time marker for the malformation with which it is associated. Both DVA and a sinus pericranii can be simultaneously present (Figs. 8.6–8.10). The diagnosis is discussed in the presence of a midline frontal varix; pretherapeutic evaluation must determine whether the varix communicates with the sinus and whether it drains any normal brain. The presence of a midline-located varix on the face does justify the search for an anomalous cerebral drainage prior to any removal or occlusion. The presence of a neurological symptom in the clinical history of a facial vascular malformation, regardless of its type, certainly requires intracranial screening; however, the discovery of a DVA should not be considered as the appropriate explanation for the neurological manifestations noted.

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Fig. 8.7A–C. A 28-year-old female patient complaining of cosmetic problems related to a subcutaneous midline varix of the forehead (A). The plastic surgeon prior to surgery requested an angiogram. B, C Left and right venous phases of the respective internal carotid angiograms demonstrate complex nonmalformative venous anomalies. The varix was identified as a sinus pericranii draining part of the right cerebral hemisphere. Treatment of this varix was not and should not be undertaken. Note the specific involvement of the striate system

Associated Features

467

Fig. 8.8. A A 7-year-old girl presenting with a large frontal varix. Following repeated attempts to correct the lesion surgically (without angiographic study), cheloid scar and bone hypertrophy were observed, together with a parallel increase in the soft, nonpulsatile expansile frontal varix. B MRI disclosed a small communication with the superior sagittal sinus. C Following direct puncture into the sinus pericranii, catheterization of the small transosseous venous communication was achieved and occluded with coils. Subsequent surgery allowed removal of the varix. At 15 years of follow-up, the lesions at the nose persist (D)

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Fig. 8.9A–C. Unusual type of lateral sinus pericranii. Note the converging pattern of the deep venous system in the inferior striate vein (A). Secondary drainage runs on the orbital roof and fills a midline-located varix (B, C). (Courtesy of P. Burrows)

The association with cortical migration anomalies was stressed by Barkovich (1988). It is not rare but seldom proven, as angiographic studies have only rarely been performed in such patients. The presence of various types of focal cortical sulcation and cellular migration anomalies (nonlissencephalic dysplasias or those of the pachygyric (Figs. 8.11, 8.12) or polymicrogyric (Fig. 8.13) type, as well as schizencephalic clefts (Fig. 8.14)), suggests the multiple opportunities for DVAs to develop during embryogenesis. It points to the role played by the transcerebral venous system in the cortical migration process. This does not mean that the venous anomaly is responsible for the cortical changes, but illustrates the close relation in topography and time between the venous maturation process (from the striatal veins and transhemispheric balance set-up) and the cell migration from the germinal matrix.

Associated Features

469

Fig. 8.10A–J. A 28-year-old female patient who presented, approximately 15 years ago, with a soft tissue mass in the right forehead and over the orbit. There were some prominent “veins” in the forehead. There was no change during pregnancy and/or during her menstrual cycles. The lesion has significantly increased in size in more recent months. The lesion is more prominent with Valsalva maneuvers. Physical examination demonstrates some pinkish discoloration in the skin. MRI (A, B) demonstrates a lesion with an extension from the diplopic space into the dura. The MRI confirms the intraorbital prominence of vascular structures (C–E). There are associated DVAs in the RT basal ganglia and RT cerebellum. Angiography shows the complex venous lesions involving the orbit, associated with several DVAs and a large frontal varix (F–H). The external carotid artery opacifies the frontal venous varix via an inflammatory type of capillaries. (I, J)The lesion is considered to be typically venous despite these minute AV shuntings. E–J see p. 470

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Fig. 8.10E–J. Legend see p. 469

Associated Features

Fig. 8.11A–C. A 7-year-old child presenting with seizures and a moderate, right-sided deficit due to neonatal hemiparesis. A, B Angiography demonstrated several cortical venous anomalies. C CT demonstrates pachygyria at the level of one of the venous dispositions

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Fig. 8.12A–D. A 4-month-old child presenting with convulsions and neurocognitive delay (actual age, 4 years; tested age, 2.5 years). At the age of 4 months, the child fell from a height of 3 m. Twenty days later, he had a partial convulsive crisis. He has been receiving antiepileptic treatment since then. A, B Note the peculiar dysplastic aspect of the frontoparietal veins on the right side. C, D MRI and CT also suggest some degree of frontal pachygyria

Associated Cavernomas

473

Fig. 8.13. A, B A young child presenting with an usual midline cortical vein with an overall appearance compatible with a diagnosis of complex developmental venous anomaly (DVA) of the entire hemisphere. C Among other findings, note the polymicrogyria at the level of the venous anomaly

8.1.3 Associated Cavernomas

The possible association of DVAs in adults with cavernous malformations has suggested the malformative nature of DVA: the cavernous malformation creates the need for an anatomic adaptation at the venular level and induces the DVA pattern that corresponds to an associated malformation. We certainly do not share this analysis; in practice, most DVAs in children are not associated with cavernous malformations. Cavernous malformations alone do exist in children and can produce hemorrhage (often intraventricular) or seizures (Figs. 8.15, 8.16); they are very rarely associated with a DVA. Kutscher et al. (1987) reported a 3.5-year-old child who presented with a posterior fossa hematoma and a DVA. The blood clot was removed at surgery, along with a lesion that showed evidence of recent and old

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Fig. 8.14A, B. An 8-year-old boy with a neonatal monoparesis. Convulsions developed during infancy. There is a moderate lower left limb hypotrophy. A Note the schizencephalic cleft with B the peculiar appearance of the veins on both lips

Fig. 8.15A, B. A 12-year-old boy presenting with a single partial motor seizure. Small subcortical cavernoma clearly seen on CT and MRI with evidence of old hemorrhage

Associated Cavernomas

475

Fig. 8.16A, B. An 8-year-old girl with a sudden onset of headaches. Large, deepseated cavernoma A before and B after surgical removal

hemorrhage.After surgery, the DVA was still present; a cavernous malformation was probably associated with the DVA, since the latter does not usually present with features of old hemorrhage. It can be postulated that the particular hemodynamic conditions created by the DVA (among other possible factors with supposedly normal venous anatomy) are capable of triggering an underlying defect and reveal it as a cavernoma over time. The potentially multifocal character of the disease (Fig. 8.17) and the familial possibilities associated with the genetic site on chromosome 7q11.2-q21 (Günel 1995) are illustrated by cases seen in the pediatric population at the brain and cord level. The revealing trigger is still unknown in these patients. Subependymal locations causing intraventricular hemorrhage are not rare. Large lesions can be seen in children. In adults, the association of a DVA and an intracerebral hematoma is almost always related to one or multiple cavernous malformations (Figs. 8.18, 8.19; Odom et al. 1961; Roda et al. 1988; Numaguchi et al. 1982). The association of DVA with an arteriovenous malformation (AVM) (Fig. 8.4) is a rare occurrence, which when present in the same area, creates a difficult therapeutic challenge (see Chap. 5, this volume).

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Fig. 8.17A–C. A 2-year-old girl presenting with generalized seizures. Multifocal cavernomas with an intralesional hematoma in the frontal lobe are seen on A CT and B, C MRI. Secondary familial investigations suggested multifocal familial cerebral cavernomatous malformations

Associated Cavernomas

477

Fig. 8.18A, B. Asymptomatic appearance of cavernoma (A, B) in a young child also presenting a dural AVS and a pial nidus

Fig. 8.19A–B. Legend see p. 478

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Fig. 8.19A–C. A young adult presenting with multiple images of venous origin over time. A Note the medial frontal developmental venous anomaly (DVA) on one side. B, C There is an associated cavernoma in the vicinity of the DVA. There is some degree of atrophy around the DVA–cavernoma region

8.2 Segmental and Nonsegmental Cerebro-orbito-facial Venous Lesions 8.2.1 Sturge-Weber Syndrome

In the past few years, the classic presentations of the various phacomatosis or neural crest disorders have been revisited. These classic syndromes can no longer be discussed without taking into consideration recent genetical or biological contributions (Henkemeyer et al. 1995; Eerola et al. 2003). Signaling mechanisms and postmigration changes must be recognized prior to any potential therapeutic application (preventive, conservative, or reconstructive) of the mutations encountered. Many of the latest discoveries offer updated classifications with modern nosological discussions and ultimately therapeutic opportunities. Our purpose is to contribute to the metameric approach of some venous cerebrofacial vascular syndromes in an attempt to overcome the therapeutic challenge. In 1860, Schirmer described the coexistence of port-wine stains and buphthalmus. Nineteen years later, Sturge (1879) reported a case that had an extensive port-wine stain of the right face and head with a right-sided buphthalmus, as well as a seizure attack. He also found a vascular malformation involving the ipsilateral brain. Cushing (1906) pointed out the tendency of the port-wine stains to follow the distribution of branches of the trigeminal nerve, yet Alexander and Norman (1960) did not support this relation. The atrophy of the affected cerebral hemisphere was first suggested by Weber in 1922 using X-ray examinations of the skull. In 1936, Bergstrand et al. illustrated the pathological characteristics, the clinical manifestations, as well as surgical indications and coined the currently accepted eponym Sturge-Weber disease in 1935. Port-wine stains are localized dermal venular malformations, which affect 0.3% of the general population at birth (Jacobs and Walton 1976).

Sturge-Weber Syndrome

479

Fig. 8.20A–D. An 11-year-old girl presenting with a rightsided port-wine stain and first convulsion at the age of 5 years. Sturge-Weber syndrome was diagnosed. Since then, she has had episodes of intense right-sided headaches with no evidence of intracranial hemorrhage. MRI findings are typical of Sturge-Weber syndrome with transcortical venous drainage and moderate frontal bone hypertrophy

Although they may occur anywhere, the face and neck represent the most frequent locations (Knudsen and Alden 1979).The progression of these skin lesions is not clear. They usually remain stable. These discolorations have to be distinguished within the birthmark group, which have an even higher incidence (30% of newborns) and from the skin discoloration of subcutaneous hemangiomas. According to Wisnicki, roughly 1%–2% of port-wine stains will be part of the Sturge Weber syndrome (Stevenson et al. 1974). This “encephalotrigeminal angiomatosis is a nonfamilial disease with a skin discoloration (port wine) in the V1 territory associated with a calcified leptomeningeal venous malformation of the ipsilateral supratentorial hemisphere” (Andre 1973). Symptoms appear before the 2nd year of life and include the cosmetic and neurological problems, related to subjacent cerebral atrophy leading to epilepsy, deficits, and mental retardation (Fig. 8.20). The lesions do not bleed except when they involve the oral cavity or the pharynx. They in turn need to be differentiated from the

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Fig. 8.21A, B. Maxillofacial port-wine stain. No venous abnormality could be found on the intracranial studies in both patients. The degree of pigmentation does not parallel the clinical tolerance or extension of the disease spectrum

gingivitis related to antiepileptic medications. Glaucoma occurs in onethird of patients with Sturge-Weber syndrome due to the presence of a retinal (most likely choroid) vascular malformation of the venous type. This facial vascular malformation is usually unilateral, but it can involve the midline and is reported to extend to the chest, trunk, and limbs in some cases (Figs. 8.21, 8.22). In exceptional cases they can be bilateral. They are often associated with progressive thickening of the skin and subcutaneous layers as well as facial capillary-venous malformations with subjacent lymphatic malformation. In such cases, overgrowth of the underlying facial skeletal structure is demonstrated, which often results in facial asymmetry and dental malocclusion (Figs. 8.23, 8.24). Port-wine stains usually remain stable and do not bleed. They are usually not associated with DVAs. While most port-wine stains are isolated vascular abnormalities, they may be associated with an underlying vascular malformation or a more complex dysmorphogenesis. Similar to the PWS, the venolymphatic malformations can involve the midline and have been reported to extend to the chest, trunk, and limbs in some series. Portwine stains over the spine may be associated with underlying spinal dysraphism or myelomeric AVMs (see below and Chap. 15, this volume). Their incidence is unclear and ranges from 1:5,000 to 1:10,000 births and are without gender dominance. About one-third of the patients with Sturge-Weber Syndrome (SWS) have ocular and/or orbital abnormalities: choroid venous malformation, congenital glaucoma with enlargement of the globe (buphthalmus), optic

Sturge-Weber Syndrome

481

Fig. 8.22A, B. Diffuse bilateral port-wine stain associated with right-sided CVMS 2

disc colobomas, and cataract. Intracranial manifestations are generally not present in patients with port-wine stains confined to the lower and mid face area. In fact, associated intracranial vascular abnormalities in SWS consist of cortical venous thrombosis with capillary venous proliferation and enlargement of the transmedullary collateral venous drainage with or without choroid plexus hypertrophy (Fig. 8.25). Typical CT or MRI findings include gyral enhancement with enlargement and enhancement of the ipsilateral choroid plexus. Occlusion of venules at the level of the brain with early failure of the venous drainage produces cortical calcifications at the primary site of ischemia and secondarily melting-brain syndrome, brain atrophy, which points to the precocity of the ischemic process, resulting in seizure, focal neurological deficits, and mental retardation. This collateral pattern in particular cannot be confused with a DVA, although it recruits transmedullary veins. Associated choroid plexus hypertrophy is unlikely to be related to the collateral circulation development, but rather to the choroid vein impact of the same venous disease during embryology. A case of Sturge-Weber syndrome diagnosed in a neonate on the basis of a characteristic port-wine stain was not initially associated with any acute neurologic findings. MR images obtained when the infant was 3 months of age showed a typical pial vascular dysplasia, as well as prominent hypotrophy of the ipsilateral hemisphere. Areas suggesting the pres-

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Fig. 8.23A–C. Bony involvement in a CVMS 2. The maxillary hypertrophy (A, B) has induced an abnormal growth of the ipsilateral mandible (C)

ence of developmental dysplasia of the cerebral mantel were found in association with the typical pial vascular abnormality. The prenatal effect of Sturge-Weber disease on normal brain development is best evaluated with improved cerebral imaging shortly after birth (Portilla et al. 2002). On early MR images, the brain parenchyma usually has normal myelination or slight hypermyelination in the centrum semiovale on the side involved. According to single photon emission CT (SPECT) results, cerebral blood flow is increased during the early asymptomatic period, whereas hypoperfusion and cerebral atrophy develop after the first hemiconvulsive episode or after the 1st year of life in children who do not have epileptic degradation (Pinton et al. 1997). Thus, venous stasis and recurrent episodes of venular thrombosis are presumably the main factors re-

Sturge-Weber Syndrome

483

Fig. 8.24A–C. Typical MR aspect of CVM 2 with cortical hypotrophy (A), choroidal enlargement, and enhancing cortex (B). Note the bone hypertrophy as well as the enlargement of transmedullary veins (C). (Courtesy of J.F. Meder)

sponsible both for neurologic deterioration and postnatal hemispheric atrophy (Carlos-Garcia et al. 1981). In the case reported by Portilla et al. (2002), clinical presentation and MR imaging findings suggested that the hemispheric lesions developed during the intrauterine period. In many instances, pachygyria, a macroscopic feature frequently associated with microscopic polymicrogyria or polymicrogyria visible on MR images (as in Portilla’s case), has been shown to result from microvascular disturbances (Levine et al. 1974; Barkovich et al. 1992). A plausible explanation for the present finding is that an abnormal venous drainage from the growing cortex may result in cortical rearrangements that eventually arrest hemispheric development.

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Fig. 8.25A–D. A 19-month-old boy presenting a generalized seizure with a persistent postictal hemiparesis. MRI (A, B) and angiography performed at the age of 5 years show a typical aspect of transcortical bilateral collateral circulation involving the striate veins bilaterally as well as the transcallosal vein on the right side (C, D). This pattern is clearly different from the DVA aspect; it suggests a secondary response to cortical vein occlusion without dural sinus impairment. Note the symmetry of the images. This aspect is compatible with the early (subclinical) appearance of cerebral location of CVMS type of disease without port-wine stain

From SWS to Cerebrofacial Venous Metameric Syndrome

485

Although hemispheric disease in SWS is frequently complicated by severe, sometimes intractable epilepsy that starts in infancy (Arzimanoglou and Aicardi 1992), in Portilla’s case there were no seizures or paroxysmal anomalies, as assessed with electroencephalography, during 2 years of follow-up, despite the presence of severe cortical anomalies. Presumably, the degree of cortical maturation necessary for neuronal firing and epileptic initiation might be less easily achieved in certain early developmental lesions than in postnatal degenerative changes. Cerebral imaging has become the usual practice in children with a port-wine stain, but the timing and techniques that can provide the most useful information on the neurologic prognosis remain a matter of debate (Campistol et al. 1999).

8.2.2 From SWS to Cerebrofacial Venous Metameric Syndrome

The venous abnormalities that affect the central nervous system as well as the face involve segmentally related territories (Couly et al. 1995; see Chaps. 2 and 6, this volume; Scheme 8.2). The SWS is expressed differently in the face and brain because of the phenotypic cell identity acquired during mesenchymatous migration (from neural crest and cephalic mesoderm). The final vascular abluminal differences, the exposure to different postnatal triggers, and a vulnerability at different moments lead

Scheme 8.2. Pattern of migrating neural crest cells and types of cerebrofacial venous metameric syndromes (CVMS 1–3)

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Fig. 8.26. Typical aspect of CVMS 1+2

to different remodeling dysfunctions and thus phenotypic expressions despite common impairment. The pharynx, the floor of the mouth and tongue, including the lower lip and chin, differ in that they are probably related developmentally to another organ system (the pharyngeal digestive tract) and therefore are not involved in these malformations. Thus, the venous malformations observed in SWS could be regarded as cerebrofacial venous metameric syndrome (CVMS) (Ramli et al. 2003; Luo et al. 2003). It may in some patients involve two or three consecutive metamers and be more or less complete in all tissues derived at a given level. SWS corresponds to a rostral cephalic mesoderm and neural crest (medial and lateral) disorder that respectively give rise to the endothelial cells and media of the nasofrontal and telencephalic derivatives (Couly et al. 1995).
Firstly, at the level of medial prosencephalic group (olfactory) with involvement of forehead and nose (CVMS 1) (Fig. 8.26)
Secondly, a lateral prosencephalic group (optic), with involvement of the occipital lobe, the eye, cheek, and maxilla (CVMS 2) (Fig. 8.27)
The third one, at the rhombencephalon (otic), would involve the cerebellum, lower face, and mandible (CVMS 3) (Fig. 8.28) According to this grouping, we can see that the port-wine stain is not along the trigeminal nerve territory distribution, but it is a mesodermneural crest region segmentation. Therefore in CVMS 1+2, a full prosen-

From SWS to Cerebrofacial Venous Metameric Syndrome

487

Fig. 8.27. Typical aspect of CVMS 2

cephalic impairment (the typical form of SWS), the lesion affects the orbit and maxillofacial region (Fig. 8.26), while CVMS 3 is considered as a rare form, and the port-wine stain is localized at the mandible with bear-shaped discoloration (Fig. 8.28) (Ramli et al. 2003; Luo et al. 2003) The full CVMS includes:
Port-wine stains in one or several facial segments related to the migration of vascular cells from the mesoderm and neural crest
Lymphangiomatous malformation of the cheek area (Fig. 8.29)
Maxillofacial (malar, frontal, or maxilla) and skull base (ethmoid, sphenoid petrous) hypertrophy (Fig. 8.30)
Pial cortical vein occlusions (supra- or infratentorial) with collateral circulation rather than venous remodeling (different from DVAs) Although the complete form can be encountered, the incomplete spectrum corresponding to the same cranial segmental disorder is much more frequent. In that regard, the association of cheek lymphatic malformation, second prosencephalic vascular territory port-wine stain and maxillary bone hypertrophy, without orbital or cerebral involvement, is suggestive of CVMS 2. There are certainly differences between CVMS (Ramli et al. 2003), CAMS (Bhattacharya et al. 2001), PHACES (Bhattacharya et al. 2003), SAMS (Matsumaru et al. 1999), and mirror aneurysms (Campos et al. 1998) beyond their segmental distribution patterns. If CVMSs are at the

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Fig. 8.28. Typical aspect of bilateral CVMS 2+3

Fig. 8.29A, B. Typical aspect of CVMS 2 (A) with maxillary hypertrophy (B)

From SWS to Cerebrofacial Venous Metameric Syndrome

Fig. 8.30A–F. Legend see p. 490

489

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8 Venous Anomalies and Malformations

Fig. 8.30. Bony and cerebral changes in a complete form of CVMS 2 (A). Note the short anterior floor on the cranial base and the atrophy and calcification of the right temporal lobe. B Same patient. The higher section demonstrates the significant frontal bone hypertrophy and calcification of the left occipital pole. C Same patient. Note the sphenoid bone hypertrophy and the asymmetry of the pneumatization of the ethmoid bone. D, E Hypertrophied maxillary bone (D) in a CVMS 2 patient (see Fig. 8.29) induced a mandible dysmorphism (E). Direct maxillary and mandible involvement (F, G) in a CVMS 2+3 patient (Fig. 8.28)

venous (venolymphatic) end of the arteriovenous tree (target), then mirror aneurysms are at the opposite arterial end of it. It is interesting to note that PHACES, which is arterial-capillary, is often associated with arterial aneurysms. CAMS, which is more on the venous side, can exceptionally be associated with external carotid arterial aneurysms. At the cranial level, there is an overlap between the various types of metameric syndromes (see Table 8.1). Considering the timing (embryonic 4th–5th week) for the generation of a metameric syndrome, one has to realize that arteries and veins are not identified by flow characteristics at that time but by molecular properties. If a trigger operating at that specific time is selective enough, then it will produce one type of the metameric syndrome; if less selective it will give slightly overlapping phenotypes. If the timing of the insult is late during migration it may involve part of the cell groups generated while the migration occurs, thus giving an incomplete spectrum within a given segmental syndrome. It should be noted that the skull base bones are not involved in CAMS 1 or 2, whereas they can be in CVMS 1 or 2. Of interest is also that CAMS 3 may involve the petrous bone, as does the SAMS 1–31 with the basioccipital, and the vertebral body with the more caudal bones, making CAMS 3 the craniocaudal transitional pattern between CAMS and SAMS patterns (Wong et al. 2003). This transition suggests a distinct vulnerability between notochordal and prechordal derivatives, and it emphasizes the role played by the neural crest in addition to the mesoderm in the vasculogenesis in the (prechordal) cephalic region, whereas the mesoderm alone ensures the vasculogenesis at the (notochordal) spinal level.

From SWS to Cerebrofacial Venous Metameric Syndrome

491

Table 8.1. Postulated relation between metameric syndromes and neural crest/mesoderm contribution, lymphatic to arterial impact, and proliferative behavior

Mirror aneurysmb PHACESb CAMS 1–2b CAMS 3b CVMS 1–3b SAMS 1–31b a b

Lymphatica malformation

PWSa

Cartilage bonea

Membrane bonea

AV shunta

Angiogenesisa

Arterial aneurysma

– – – – + +

– – – – + +

– – – + + +

– – + + + +

– – + + – +

– + + + – +

+ + + + – +

From less angiogenic to more angiogenic. Neural crest and mesoderm to mesoderm alone; craniocaudal.

At the cranial level, port-wine stains are not associated with intracranial AVMs, as if the trigger’s target for CVMS was located too far toward the lymphatic end of the vascular tree; thus the overlap between CVMS and CAMS is minimal. It should be noted that CAMS includes retinal AVMs, whereas CVMSs are associated with choroid malformations involving the same second cephalic segment. CAMSs and CVMSs are well differentiated cranially (perhaps because of the contribution of the neural crest) but not very well at the spinal level (where the neural crest does not contribute directly to vasculogenesis), as seen with Klippel-Trenaunay syndromes (venolymphatic) associated with spinal cord AA and AVMs, Parkes-Weber syndromes, or port-wine stains with typical SAMSs (see Vol. 2, Chap 11 and Chap. 15, this volume). Concerning ventricular choroid plexus hypertrophy, while speculative it is likely to represent the phenotypic expression of the same disorder that impacts the subpial cortical veins, and those that colonize the branchial arches to provide the venolymphatic structures. The concept of the choroidal plexus veins being a specific target is supported by the VGAM group, as the pial AVFs and AVMs identify the subpial venous system, and the dural sinus malformations the dorsal epidural venous system. The role of the VEGF family is highly probable, in particular VEGF C and D in the venous and lymphatic vasculogenesis and angiogenesis. Their role is slightly delayed in comparison to VEGF A and B involvement in the arterial vasculogenesis and angiogenesis. The link between the bone morphologic growth factor and angiogenesis involves sequentially the cartilage (mesoderm), the neural crest, and then the skeletal system. The bone involvement in segmental syndromes is assumed to be related to their lymphatic invasion, or the bone impact of potent vascular growth factor disorder; conversely Klippel-Trenaunay and Sturge-Weber could almost be considered as bone diseases with the vascular expression of a bone-related growth factor. There is a recent study that demonstrates that tissues from affected areas are genetically mosaic in selected patients with CVMS (Mahbubul 2002). However, further chromosomal studies are needed in a larger study population to ascertain whether these chromosomal alterations play an important role in the etiology and progression of CVMS.

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8 Venous Anomalies and Malformations

In our experience, angiography fails to demonstrate hypervascularization in these lesions. Bone hypertrophy, as mentioned above, should be related to the venular type of malformation, which is also responsible for the leptomeningeal lesions and the port-wine stain. Faint capillary stain can be seen when hypertrophied tissue is injected or when post-traumatic lesions have developed in an underlying port-wine stain. The venolymphatic abnormalities are likely to be responsible for the bone hypertrophy. Therefore, all the lesions observed are linked to the same embryonic stage of maturation of the vascular system in which venous and lymphatic malformations are formed (or programmed). Therapeutic angiography in these cases has been carried out when facial reconstruction for cosmetic purposes was indicated. Usually, the maxilla and cheek deformities will induce so many disturbances in the maxillofacial growth that the plastic and reconstructive surgeon may feel obliged to perform osteotomies and debulking surgery of the cheek masses. Presurgical angiography and embolization with particles of some post-traumatic high-flow lesions will devascularize the operative field, reducing the perioperative blood loss at the time of these difficult bone reconstructions. Other cerebrofacial metameric syndromes illustrate either the direct relationships between the neural tissue and the neural crest at a specific level, or the gap (by lack of fusion or excess of apoptosis) that may exist between two consecutive levels. Tessier (1976) in his classifications found 14 meridians to represent the most critical areas in the upper and lower frontomaxillary region. Some vascular malformations of the face may behave like clefts and receive unusual blood supply from rare arterial variations (see Chap. 6, this volume). Other venolymphatic malformations are associated to complex intracranial DVAs involving the supra- and infratentorial cranial fossa (Figs. 8.31–8.33).

From SWS to Cerebrofacial Venous Metameric Syndrome

Fig. 8.31A,B. Typical angiographic findings of a (CVMS 2) Sturge-Weber syndrome; (A) early and (B) late phase of the internal carotid angiogram. Note the absence of arterial or capillary lesions. C,D see p. 494

493

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8 Venous Anomalies and Malformations

Fig. 8.31C,D. (continued) The venous system is abnormal and the drainage occurs late during the series. Early (C) and late (D) phases of the vertebral angiogram in the same patient with CVMS 2+3. Note the aspect of the cortical cerebellar veins

From SWS to Cerebrofacial Venous Metameric Syndrome

495

Fig. 8.32A–F. A 15-year-old boy presenting with a giant lymphatic malformation of the right side of the face. In addition to this particular malformation, there were multiple developmental venous anomalies (DVAs) involving the supratentorial and infratentorial cerebral structures bilaterally. A, B Complex intracerebral DVA associated with facial lymphangioma. C–F Note the striate territory of the basal vein before it crosses the midline immediately at the level of the posterior communicating vein (curved arrow). The superior striate veins are clearly seen (1) joining the thalamostriate system, whereas the inferior striate veins (2) converge toward the right-sided large basal vein (3). The latter opens into an infratentorial type of great cerebral vein (4). 5, Lateral atrial vein draining subcortical territory; 6, vein of the superior peduncle draining the paraventricular territories of the fourth ventricle and an anterior left hemispheric territory. The open arrow points to the left insular vein draining into a large basal vein (arrow). The patient was neurologically intact with no objective deficit and no neuropsychological defect. He had no neurocognitive delay; on the contrary, he was quite successful at school. E,F see p. 496

496

8 Venous Anomalies and Malformations

Fig. 8.32E,F. Legend see p. 495

8.2.3 Orbitofacial Venous Lesions

Orbitofacial venous malformations are rare; they associate ipsilateral and communicating venous malformations of the orbit and orbital rim and face. They are located intraconical and seem to involve the extraocular muscles. The extension of the venous lesion includes the eye lid, the medial canthus, and the adjacent forehead. The lesion communicates with the cavernous plexus posteriorly and the facial veins anteriorly. Valsalva maneuvers produce exophthalmos that becomes painful over time. When lying flat, patients often complain of retro-orbital pain. Bone destruction can be seen in these situations. At rest, in supine position the chronic increase in venous pressure, albeit intermittent, has created a secondary orbit enlargement leading to enophthalmos (Fig. 8.34). Deconstructive treatments are difficult to perform as the drainage of the eye and optic nerve cannot be secured. Partial surgery with disappointing longterm results has been performed to overcome the pain symptoms. Focal posterior opening into the cavernous plexus has been performed in an attempt to decrease the effects of Valsalva maneuvers. The result has been subjectively excellent with significant reduction in pain; reports on the long-term effect are still lacking (Fig. 8.10).

Orbitofacial Venous Lesions

Fig. 8.33A–C. A young child presenting with left-sided fronto-orbital lymphatic malformation associated with multiple venous anomalies involving the frontotemporal region. Note the peculiar venous lake located in the greater wing of the spheroid bone

497

498

8 Venous Anomalies and Malformations

▲

Fig. 8.34A–G. A young girl presented at birth with a small red spot on the left eyelid that regressed by the age of 3 months. At 15 months, exophthalmos with bluish lower inferior eyelid on the left were noted. There was no pain, no visual problem, and no diplopia. Symptoms increased in Valsalva and appeared without hyperemia, with enophthalmos at rest (A). Numerous phleboliths in the masseteric and pterygoid regions (B, C). Possible lymphatic component. Orbitofrontal venous malformation (D, E). The venous lesion predominantly involves the inferior ophthalmic vein (E–G). D–G see p. 499

Complex Pseudo-metameric Cerebrofacial Venous Syndrome

499

Fig. 8.34D–G. Legend see p. 498

8.3 Complex Pseudo-metameric Cerebrofacial Venous Syndrome Dural sinus malformations (DSMs) in children generally occur at neonatal or early infancy age (see Chap. 7, this volume). DSMs can be diagnosed in utero and correspond to an abnormal fetal development of the posterior sinuses. Anatomically, two types of DSM can be seen and the most complex cases involve the confluence of sinuses with giant dural sinus pouches with very-slow-flow mural AV shunts. Partial thrombosis of the sinus may occur. Enlargement (or ballooning) of the transverse sinus is a normal phase of sinus development, during the 4th–6th gestational months (Okudera et al. 1996).An unknown trigger has been postulated to cause the persistence or the delay of the ballooning of the transverse

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8 Venous Anomalies and Malformations

and/or posterior part of the superior sagittal sinus (SSS). Important prognostic factors are the degree of lateralization (transverse, sigmoid sinus, jugular bulb) or mid-line location (torcular SSS), magnitude of the dural pouch, and thrombosis. Spontaneous thrombosis of the pouch and outlets further compromise cerebral venous drainage and subsequently lead to venous infarction and parenchymatous hemorrhage. As long as the venous outlets are patent, the clinical manifestations remain subacute. Yet growth of the lesion(s) is seen in some cases as well as the appearance of de novo cavernomas (Mohamed et al. 2002) (Fig. 8.35). Such associations and progressions are not seen with the other type of sinus malformation: jugular bulb malformation with otherwise normal sinuses. The malformation in the latter situation corresponds to a unilateral postnatal dysmaturation of the high jugular bulb, with occlusion of the sigmoid sinus; the normal postnatal regression of the marginal and medial occipital sinuses usually occurs. DSM can be seen with DVAs in few cases. Unlike in adults, most DVAs in children are not associated with cavernous malformations. However, in cases of DVA with cavernous malformation, it is postulated that the association may be due to the peculiar hemodynamic conditions created by the DVA, which is capable of triggering an underlying defect revealing the cavernoma over time. The secondary appearance of multiple cavernomas usually occurs in familial cavernous malformation and has been linked with a genetic site on chromosome 7q11.2-q21 (Günel 1995). DSM can actually be associated with various maxillofacial vascular malformations yet ipsilateral to the epidural malformation and thus is potentially segmental-related (Fig. 8.36) (see Chap. 7, this volume). Mohamed et al. (2002) described an unusual presentation of a complex cerebrofacial vascular syndrome involving a DSM (demonstrating dramatic postnatal enlargement) in association with a developmental venous anomaly, cavernous malformations, and a facial venous malformation. This child presented initially in the 1st month of life with a right facial hemangioma and an asymptomatic midline DSM involving the torcular and the posterior part of the superior sagittal sinus detected on MRI. Her situation gradually worsened with enlargement of the sinus malformation (at age 3 months) involving the right transverse sinus with partial thrombosis in the torcular and SSS. The angiogram revealed a complex DVA draining normal brain of the right cerebral hemisphere into the deep cerebral veins. These venous collectors converged toward the vein of Galen (a high-pressure system in this child), excluding the cortical system and the basal vein, which normally could provide alternate collateral draining venous pathways that could help to bypass the malformed torcular. The facial hemangioma first noticed in this infant was actually a superficial venous malformation under the bluish skin enhanced by Valsalva maneuvers. Her condition became further complicated by multiple cavernous malformations, which, while initially single, were clinically silent and demonstrated on an earlier MRI (1st month). She underwent embolization in two sessions in an attempt to reduce venous hypertension. MRI after embolization revealed multiple enlarged cavernomas that had bled in the right periventricular region. The unen-

Complex Pseudo-metameric Cerebrofacial Venous Syndrome

501

Fig. 8.35A–D. A 1-month-old baby with right frontal cutaneous venous malformation and torcular DSM (A, B). Slight delay at 5 months. In 7 months, she developed a giant dural sinus lake and several hemorrhagic cavernomas (C, D)

hanced brain CT demonstrated diffuse subcortical calcification in the right parieto-occipital region, indicating chronic venous congestion in the brain. Deterioration in the form of focal melting-brain syndrome occurred rapidly and she died 8 months after the diagnosis. In another case report, Janz et al. (1998) documented multiple cavernomas in an infant initially presenting with multiple AV shunts: dural and then pial AVM. The unusual combination of disorders in Mohamed’s case could be fortuitous. Yet their ipsilateral arrangement raises questions and hypotheses. The complex disease entity demonstrated in this infant (Table 8.2), appears to be a spectrum of phenotypic expressions of a single (yet early) embryonic disorder (venous target). The dural sinus malformation, facial venous malformation, DVA, and cavernous malformation on

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8 Venous Anomalies and Malformations

Fig. 8.36A–D. Associated dural sinus malformation, venolymphatic facial malformation, and AV shunt (A, B). Note the bilateral thalamic and right occipital DVAs (C, D)

the right side seem to be in a segmental distribution; her posterior fossa was normal. We must therefore postulate that the dural sinus development was also subsegmented in order to explain for the sparing of the most caudal cranial metamer. Or could this presentation be an incomplete presentation of a wider spectrum still resulting from a single focal target impact? The various disorders (face, DVA, cavernoma, and dural sinus malformation) could testify for the existence of an event at one point in time, several targets, not generation-related, all simultaneously involved signaling system impairment. The areas involved are those that are vulnerable at that very moment. The diseases expressed, although not anatomically related, were damaged simultaneously in time.

Blue Rubber Bleb Nevus (Bean Syndrome)

503

Table 8.2. Cerebro-dural-facial venous disease associations in children (Mohamed et al. 2002) Lesion / Reference

DSM

Janz et al. 1998 Bhattacharya et al. 2001 Pascual-Castroviejo et al. 1996 Lasjaunias et al. 1986a

DAVS

+

Cavernous malformation

+ +

DVA

+ + + +

Facial lymphatic or venous malformation

+ + +

Chung 2003 Fig. 8.36 Mohamed et al. 2002

+ +

+ +

+

+ + +

+ +

Sinus pericranii

BRBN

+ + + + +

+

DSM, dural sinus malformation; DAVS, dural arteriovenous shunt; DVA, developmental venous anomaly; BRBN, blue rubber bleb nevus.

These two hypotheses illustrate the role played by the target and timing in the production of congenital malformations (see Chap. 2, this volume). The actual genesis of this complex cerebrofacial vascular syndrome in this infant is still uncertain, though the second hypothesis could be the more likely explanation.

8.4 Blue Rubber Bleb Nevus (Bean Syndrome) The etiologic classifications of cerebral venous malformations can be grossly categorized into four groups (Table 8.3) based on the supposed timing of the causative defect (see Chap. 2, this volume):





Inherited germinal mutations (familial multiple cavernomas, etc.) Somatic mutations (sporadic BRBN, etc.) Metameric diseases (CVMS, etc.) Late altered venous modeling and remodeling processes (port-wine stains, single cavernoma, etc.)

In the group of genetic diseases, some are hereditary (familial) while others are not, indicating a nontransmittable single somatic mutation. Few genetically based diseases have been related to a chromosome disorder and some have already been localized to a single gene. The usual occurrence of BRBN is sporadic and is believed to result from somatic cellular mutations. However, some familial forms of BRBN with an autosomal dominant trait have been reported in the literature with involvement of chromosome 9. In the family of Boon et al. (1994) and Gallione et al. (1995), the disorder they reported was identical to BRBN. Similar to their cases, they pointed out that the family originally described by Bean also had gastrointestinal bleeding from vascular lesions. They suggested that the chromosomal loci of BRBN in family members having an autosomal dominant trait manifests as multiple cutaneous and mucosal venous malformations (MCMVM).

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8 Venous Anomalies and Malformations

Table 8.3. The postulated venous disorders producing cerebral vascular malformations (Chung 2003) Primary disorders

Illustrative type

Gross characteristics

Genetic, Familial

Familial cavernomas BRBN HHT1 BRBN HHT1 CVMS CAMS Cavernoma VGAM, DSM, AVM

Multifocal (chromosome 7) Multifocal (chromosome 9p) Multifocal (chromosome 9q) Multifocal Multifocal Cerebrofacial segmental distribution Cerebrofacial segmental distribution Single or multiple

Genetic, sporadic nonfamilial Metameric Posterior neural crest-mesoderm migration defect

BRBN, blue rubber bleb nevus syndrome; AVM, arteriovenous malformation; CVMS, cerebrofacial venous metameric syndrome; CAMS, cerebrofacial arteriovenous metameric syndrome; VGAM, vein of Galen aneurysmal malformation; DSM, dural sinus malformation; HHT1, hereditary hemorrhagic telangiectasia.

The dominantly inherited gene lies within a 24-cM interval on chromosome 9p, defined by the markers D9S157 and D9S163. The alpha and beta interferon gene cluster and the putative tumor suppressor genes MTS1 and MTS2 are also incorporated into this locus, chromosome 9p. Further characterization of the gene responsible for this inherited form of BRBN should be done for better understanding the mechanisms involved in these various venous lesions. The multifocal nature of BRBN lesions is suggestive of a random impairment, although it is an early prenatal genetic defect from a single somatic mutation at the time of susceptibility. The genetic target seems to be active during a short period of time: during vasculogenesis as well as the early (prenatal) active angiogenic phases of vascular remodeling. These speculative observations are based on the fact that the postnatal genetic susceptibility of endothelial cells, particularly in the brain, makes endothelial cell clonal mutations unlikely in comparison to the instability of tumoral cells.

8.4.1 The Association of BRBN with DVA

The association of DVA in BRBN is a relatively well-known phenomenon, especially presented with multiplicity in some case reports (Sherry et al. 1984; Osborn 1994). The previous reports of BRBN did not clearly describe the DVAs; however, a retrospective review of the illustrations show their frequency. In Chung’s case (2003), there are large deep bilateral cerebellar DVAs with intense capillary stains and rapid capillary transit (Fig. 8.37). Waybright et al. (1978) describes a dilated vein of Galen, but retrospective analysis shows a venous disposition similar to a DVA. Review of previous literature (Table 8.4) found that multiple cerebral venous malformations in corticoventricular disposition correspond in almost all cases to DVAs draining into deep venous collectors (Kunishige et al. 1997; Waybright et al. 1978; Chung et al. 2003; Osborn 1994).

The Association of BRBN with DVA

505

Fig. 8.37A–I. Blue rubber bleb nevus with cutaneous features (A–C) associated with a giant cerebellar DVA (D–G) and large deep-seated telangiectasia (H, I)

Partial seizures

Complex partial seizures, myoclonic seizure No neurologic symptoms Growing forehead mass Ataxia, dementia

Ataxia, ophthalmoplegia, palatal myoclonus

Headache, focal seizure, hemianopsia, monoparesis, ataxia N/E

Ataxic gait, nystagmus, intermittent vertigo, chronic headache

Kim 2000 (11 months/F)

Eiris-Punal et al. 2002 (5 months/M)

Kunishige 1997 et al. (16 years/F) Sherry et al. 1984 (6 months/M) Vig 2002 (82 years/M)

Satya-Murti et al. 1986 (19 years/M)

Waybright et al. 1978 (19 years/M)

Chung 2003 (21 years/M)

MRI, angiography

MRI

CT, angiography (N/E), autopsy

+; Supratentorial, cerebellum, cerebral VM, circumscribed, diffuse

N/E

No; single lesion, VARIX +; supratentorial, cerebellum, cavernomas (?, N/E) +; supratentorial cerebellum, (phleboliths), cerebral VM circumscribed, diffuse +; Supratentorial, cerebellum, telangiectasias (?,N/E)

CT, angiography MRI CT, angiography

No; single lesion, N/E

+; Supratentorial, cerebral VM, circumscribed, diffuse +; supratentorial, cerebral VM

Multiplicity and types of cerebral lesions

MRI, CT

MRI

MRI, MRA

Imaging

Corticoventricular

Corticoventricular

Corticoventricular

+; Multiple (?), thrombosed aneurysm of Galen +; Multiple, Sinus pericranii +; Multiple

No; N/E

No; N/E

Corticoventricular Cortical, corticoventricular

+; Sinus pericranii

No; dilated vein of Galen

+ (?); Anomalous venous sinus No

Associated DVAs

Cortical

Cortical

Cortical, corticoventricular Cortical, corticoventricular

Topography

VM, venous malformation; DVAs, developmental venous anomalies; MRI, magnetic resonance imaging; MRA, magnetic resonance angiography; CT, computed tomography, N/E not explored.

Osborn 1994 (N/E)

Clinical

Reference(age/sex)

Table 8.4. Intracranial manifestations in BRBN (revisited from the literature) for cerebral venous malformations and associated DVAs (Chung 2003)

506 8 Venous Anomalies and Malformations

BRBN and HHT1

507

8.4.2 Cerebral Venous Malformations in BRBN

The venous malformations in BRBN show the typical appearance of capillary ectatic changes with stagnant vascular pooling. The radiologic findings of cerebral VM also demonstrate its own histopathologic architecture. The cross-sectional imaging studies of cerebral VM in BRBN demonstrate multiple enhancing circumscribed or diffuse masses (SatyaMurti et al. 1986; Kim 2000). The identification of DVAs, cavernomas, telangiectasias, AVMs, and VMs as distinct entities should be done to improve the accuracy of the descriptions of cerebral lesions when assessing the angiographic and radiological aspects in individual BRBN cases with cerebral involvements. The cavernomas are angiographically occult. The AVMs show AV shunts with enlarged feeders and draining veins rarely associated with DVAs and even less frequently draining into DVAs. Telangiectasias are vascular malformations of the venules, depicted as dilated medullary capillary or venous structures and often form a mass-like appearance. Angiographic findings need to be read with precision to separate all these entities.

8.4.3 BRBN and HHT1

There was a single report (Rosenblum et al. 1978) that suggested that there might be an overlap between BRBN and HHT disease when comparing their pathology, implying more phenotypic expressions than those previously recognized in the literature. Hemorrhagic hereditary telangiectasias (HHT), or Rendu-Osler-Weber disease (ROW), is an autosomal dominant disease with two to three genotypes. HHT1 (endoglinlinked), which has several mutations altering the synthesis of endoglin, has been found in affected individuals (McAllister et al. 1994). The chromosomal locus in the hereditary form of BRBN is located on chromosome 9p, while the site of HHT1 mutation involves chromosome 9q. Yet HHT1 is not particularly associated with DVAs, and AV shunts or fistulas are not noted in BRBN. Finally, in the few cases of craniopagus that have been reviewed, no mention was made of any possible associated DVA, even though an obvious venous communication was present (Wolpert, in Newton and Potts 1974; Osborn 1980). The demonstration of the dural and venous connections is of paramount importance prior to the separation of these children (see Chap. 9, this volume).

9 Craniopagus and Cranial Midline Epidural Venous Anomalies

9.1

Introduction 509

9.2

Postulated Relationships Between the Superior Sagittal Sinus and Adjacent Structures 511

9.3

Ladan and Laleh’s Angiographic Anatomy 521

9.4

Technical Remarks and Functional Testing 531

9.5

Discussion on Surgical Management 534

9.1 Introduction Craniopagus twins are the rarest form of twinning of the human organism. These twins can be joined at the vertex, at the side, or at the forehead (O’Connell 1976; Winston 1987). Twins attached at the vertex are the most commonly seen. Such twins may face in opposite directions or the same direction, or can be slightly rotated one to the other. The major surgical consideration when separating twins that are joined at the vertex relates to the separation of the typically conjoined sagittal sinus. The separation of conjoined craniopagus twins is an exacting neurosurgical procedure requiring a multidisciplinary team for success. The assistance of craniofacial surgeons who can insert tissue expanders into the subcutaneous tissues of the scalp so that the scalp wounds can be closed after separation without requiring skin grafts has been described (Shively et al. 1985). The craniofacial surgeons assist with the harvesting of autogenous split-thickness bone grafts, which were fashioned and rigidly fixated with titanium microplates and screws. In an effort to separate twins’ cerebral circulations prior to surgery, interventional neuroradiological approaches are needed. We feel strongly that such new and emerging technology should be considered in all future separations of craniopagus twins. For that reason we have elected to present our experience in participating in separating child and adult conjoined twins. Spitz described the presence of marble statues 17 cm in length called the Double Goddess, dated 6,000 BC and displayed in the museum of Anatolian civilization in Ankara in Turkey (Spitz and Kiely 2003). Even if craniopagus twins are considered to be a malformed individual, they are actually a situation somewhere between normal (within normal range) and abnormal (pathological). Fusion of the embryos alters the developing messages, but as seen with Ladan and Laleh (Singapore twins operat-

510

9 Craniopagus and Cranial Midline Epidural Venous Anomalies

Fig. 9.1. Schematic representation by Winston (1987) of the four types of relationships in craniopagus

ed on in 2003), this is not incompatible with normal future development. The anatomy is difficult to understand rather than pathological. The purpose of the following discussion is to speculate on the alterations in the embryological signaling aspects in order to understand the dural sinus dispositions in relation to each twin. Classic embryonic theories support a fusion hypothesis of two embryos at an early stage (3rd or 4th week after fertilization). Looking at 500 conjoined twins, Spencer pointed out that craniopagus twins are seldom attached in the same area of the skull (Spencer 1992). It was Winston in 1987 who stressed the importance of venous drainage in craniopagus twins prior to surgery and the value of angiography in the assessment of the anatomic disposition (Winston 1987; Winston et al. 1987). However, exhaustive investigation by angiography is difficult to perform, particularly in the first few years of life, and this limits its quality and usefulness. In 1976, O’Connell drew attention to the importance of the venous confluence and its complexity, particularly in the occipital region (O’Connell 1976). Yang and Xu, in 2002, presented a case of craniopagus twins with a conjoined sinus in relation to a converging disposition of the falx cerebelli on the midline of the conjoined twins and there was apparently no medial portion of the tentorium (Yang and Xu 2002). Winston’s or Spencer’s description of the sharing of the meningeal coverings in craniopagus takes into consideration the dural coverage of the convexity but does not sufficiently cover the midline location, particularly the position of the falx cerebri (Fig. 9.1). The last type he describes with the ring sinus seems to suggest the linkage of one arm of the ring to one twin’s falx, while the remaining limb of the ring belongs to the other twin’s falx. In type B, the meninges are shared; however, it can hardly contain a sinus in such a remote position from the bone. The persistence of only one layer of dura is likely to exclude the presence of enough epidural space to create the development of a sinus lumen.

Postulated Relationships Between the Superior Sagittal Sinus and Adjacent Structures

511

In 1987, Winston recalled in his classification that conjoined twins have also been observed in fish, amphibians and reptiles, and some other animals closer to humans (Chai and Crary 1971). The references unfortunately relate to a mesoderm layer that would separate the cutaneous cover from the neuroectoderm in the cranial region. In fact, the intracranial dura mater as well as the osseous elements of the cranial vault are all derived from the neural crest as well as the leptomeninges.

9.2 Postulated Relationships Between the Superior Sagittal Sinus and Adjacent Structures As shown by Kehrli in 1999, the superior sagittal sinus goes through a plexus stage during embryonic and fetal life (Fig. 9.2). These plexuses, by confluence of their lumens, will evolve to become the single space that is known and described in adults. The epidural space therefore resembles a conjunctive tissue that serves as an interface between bone and arachnoid (Fig. 9.3). Within this space (interperiosteal-arachnoidal), several layers become individualized, leaving room for penetrating veins from the telencephalon ventrally and superficial osseous veins dorsally to develop and converge. The deepest portion of this periosteal-arachnoidal space will become the dura as we know it. The interface between the arachnoid and the epidural space is important, as it links this space to the cerebral veins during embryonic and fetal development and postnatally with the development of the granulations. Their late maturation is related to calvarial suture fusion as well as the infant attaining a standing position and later on to walking. It is remarkable to note that in most anatomical and pathophysiology discussions of craniopagus twins, there are few references to CSF absorption despite the reported variations in venous sinus disposition. In his PhD dissertation, Kehrli draws attention to the various modalities of development of the superior sagittal sinus and the rapid convergence of the cerebral veins that contribute to their constitution. This is expressed during the first 6 weeks of life by generation of numerous epidural plexuses.At this stage, most of the neural tube drainage seems to have a ventral-lateral direction. It is around the 8th week of development that the superior sagittal sinus becomes easily recognizable and enlarges in the craniocaudal region. At the beginning of the fetal period, the torcular region has a perisinusal space within the epidural space that is occupied by an extremely rich vascular plexus. Initially it drains the bony portion of the region (the squamous portion of the occipital bone) before later becoming the torcula confluence that is so developed in neonates (Lasjaunias et al. 2005). If one considers the development of the epidural space at the spinal and cephalic levels, the ventral region is colonized by a rich venous plexus to drain the red cells produced in the spongy bone derived from the notochord. In the cranial region, cephalization leads to secondary migration of the neural tube to produce cortex in the prosencephalic, mesencephalic, and rhombencephalic vesicles. This differentiation secondary to the primary development of the neural tube is mirrored by the changes in the venous drainage that are ventrally orientated in the beginning and secon-

512

9 Craniopagus and Cranial Midline Epidural Venous Anomalies

Fig. 9.2. A Frontal section of the human embryo at 11 weeks; B frontal section of human fetus at 27 weeks; C schematic representation of venous confluence at the superior sagittal sinus. 1, Subcutaneous vein; 2, meningeal vein; 3, epidural vein; 4, cerebral vein; 5, perisinusal venous space; 6, diploic vein; 7, superior sagittal sinus; 8, inferior sagittal sinus. (Courtesy of C. Maillot and P. Kehrli)

darily cortically and dorsally orientated. It appears that the midline signal for each cerebral vesicle will impact on the meningeal development, and timing seems to be clearly related to these secondary migration waves with sequenced development within the epidural space at the level of the prosencephalic, mesencephalic, and rhombencephalic vesicles. Rapidly, these signals associated with the cerebral veins opening in the preexisting epidural plexus lead to the development of the superior sagittal sinus and torcular confluence. This is in contrast to development caudal to the foramen magnum where there is normal formation of the ventral plexuses in relation to the neural tube and the ventral interperiosteal-meningeal space. Consequently, it indicates that dural sinus malformations can impact the dorsal development exclusively at the cranial level (Table 9.1).

Postulated Relationships Between the Superior Sagittal Sinus and Adjacent Structures

Fig. 9.3. Schematic representation of the interperiostoleptomeningeal space. Epidural space from Kehrli (1999): two different functionally related layers, one to the vault, the other to the cerebral leptomeninges and the cortex. The epidural space is an active interface between the cranial vault and the underlying cortex covered with leptomeninges. 1, Periostal layer; 2,dural layer; 3, dural limiting cells; 4, arachnoidal limiting cells; 5, dura mater; 6, arachnoid; 7, pia mater

Table 9.1. Comparison between dorsal and ventral venous derivatives Epidural sinuses

Epidural venous plexus

Membranous-dural tissue Cartilaginous-dural tissue Neural crest origin Mesoderm origin Evolved plexiform state Maintained plexiform state Water resorption Red blood cell circulation Dorsal (cortical) drainage Ventral (spinal cord-type) drainage Not segmented Segmented Supratentorial-specific Notochord-specific (clival-sacral) Intracranial Craniospinal Midline (falx) dorsal signals Midline ventral signals Dural sinus malformation No plexus malformation Craniopagus and fused sinus Alobar holoprosencephaly Junctional system: petrous pyramid and basioccipital System of the dorsal prosencephalic Primitive relation between the ventral migrations and midline telencephalic neural tube and the notochord: (mesencephalic, rhombencephalic?) spinal segments, myelencephalon, signals metencephalon, mesencephalon, diencephalon

513

514

9 Craniopagus and Cranial Midline Epidural Venous Anomalies

Developmentally there is a close relationship in the cranial region between the ectoderm and its secondary epidermal and bony derivatives with regard to the development of the dorsal aspect of the neural tube. Simultaneously and as a mirror relationship, one can link the ventral development to the notochord and the future skull base. A certain number of growth factors, as well as transcription and signaling factors are specific for both regions and intervene in the multiplication of cells as well as their differentiation and their migration (Fig. 9.4). In a recent review article, Hemmati-Brivanlou (2000) showed the importance of signals from the notochord to the floor of the neural tube and from the ectoderm to the dorsal part of the same neural tube. These signals are active following successive waves, creating various craniocaudal gradients as well as dorsal-ventral ones and even right-to-left gradients. The notochord or axial mesoderm is the source of the ventral signals leading to the development of motor neurons and interneurons, which are ventrally located. The prominent signal is sonic hedgehog (SHH). The fate of the dorsally located neural tube is independent of the signals that come from the axial mesoderm. If the signals coming from the notochord are blocked or if the notochord is eliminated, the neural tube dorsally keeps on becoming dorsal. Various factors belonging to the Wnt family are particularly expressed on the midline of the dorsal neural tube (Wnt 7b, Wnt 1, and Wnt 3a). The BMP/GDF (bone morphological proteins) are members of the TGFb family that interact with Wnt in building up the various profiles of the dorsal neural tube and determine the temporal sequence of events interfering or intervening at that level. Finally, TGF and other growth factors have a direct role in the persistence of the dorsal cellular fate. Some are preferentially expressed in the dorsal location. Their invalidation induces defects in the facial parts of the skeleton in relation to the disappearance of cranial derivatives of the neural crest in certain animals. The first neuralizing signal would induce a neural future from the ectoderm and impose the most anterior encephalic modeling at the same time. A second signal would have no neuralization activity but would act over the first signal to add new fates in a more posterior location (mesencephalon, rhombencephalon, and spinal cord). The source of signals is proposed in two hypotheses suggested by Doniach with the existence of longitudinal signaling systems as well as ventral-dorsal located systems arising from the axial mesoderm (Doniach 1993). The neural tube is therefore divided into several molecular territories and gradients. The interperiosteal-dural space must therefore be considered as a space rather than layers interposed between the bone and the leptomeninges covering the brain. Within that space, dorsally, following late signals in relation to the brain midline, venules will converge to constitute the primary superior sagittal sinus, which will rapidly capture the veins of the cortex (Fig. 9.2). It is during fetal development that the confluence of all the midline-located sinusal and perisinusal lumens will lead to the development of the superior sagittal sinus as well as the torcular and lateral sinuses (Fig. 9.5). Finally, the bone and the brain

Postulated Relationships Between the Superior Sagittal Sinus and Adjacent Structures

515

Fig. 9.4A, B. Schematic representation of dorsal and ventral signaling in the human embryo. B Hemispheric development with appearance of the superior sagittal sinus on the midline as well as the corpus callosum. SHH, sonic hedgehog; BMP, bone morphological protein; GDF, growth differentiation factor

with the interposed dura seem to trap the future superior sagittal sinus in the midline. Secondarily the development of the granulations (which are specific to the cephalic region) will complete the complexity of the system. On a schematic representation of the superior sagittal sinus, one can find the superior sagittal sinus, the falx cerebri, and the corpus callosum in the midline on the sagittal plane at the level of the interparietal suture (Fig. 9.4). If any change comes to intervene at the level of each of these landmarks of the midline, one can establish a hierarchy among them. In particular, it does not seem that the bone signal of the midline determines the position of the superior sagittal sinus but rather the falx cerebri between the two hemispheres of the brain (Fig. 9.6). This suggests the preeminence of the telencephalic signal. In congenital absence of the falx, as seen in a PHACES case (which includes various types of midline disorder), the SSS is flat (Fig. 9.7) and there is arterial and venous communications between both cerebral hemispheres through a shared leptomeningeal space. In craniopagus (Fig. 9.8), an axial schematic representation shows how the separated falx anteriorly could induce two distinct superior sagittal sinuses; the part located more posteriorly would only lead to a conjoined sinus if the convergence of the falx or falces coincides with the conjoined skull boundary (Fig. 9.9). Interposition of dural coverings or interperiosto-leptomeningeal space between the telencephalic vesicles derived from different prosencephalic vesicles does not seem to lead to the constitu-

516

9 Craniopagus and Cranial Midline Epidural Venous Anomalies

Fig. 9.5. A Schematic representation of the variation of the posterior fossa sinuses: 1, superior sagittal sinus; 2, torcular; 3, transverse sinus; 4, sigmoid sinus; 5, jugular bulb; 6, medial occipital sinus; 7, marginal sinus; EMV, emissary vein. This disposition can exist in adults (B). In children, the medial occipital sinus (open arrow) and the marginal sinuses (arrows) are common. This disposition is constantly encountered in neonates and demonstrates the size of the epidural space at that age (C)

Postulated Relationships Between the Superior Sagittal Sinus and Adjacent Structures

517

Fig. 9.6A, B. Perinatal atrophy: evidence on MRI of lateralized shift of the superior sagittal sinus remote from the interparietal suture. Note in addition the widening of the vault associated with poor telencephalic signal

tion of a sinus as shown; in other words in does not create a midline signal unless both midline signals meet on the conjoined line. One can derive from this observation that if the bone is necessary for the development of the sinus, the midline of the telencephalic vesicles derived from the same prosencephalon is compulsory. The absence of a superior sagittal sinus (M. Catala, personal communication; Probst 1979) in alobar holoprosencephaly supports this hypothesis (Fig. 9.10). Anencephaly is not associated with any telencephalic development nor with the vault or any type of sinus, whereas skull base development, venous plexuses, and emissary veins are preserved in all craniopagus, holoprosencephaly, as well as anencephalic individuals.

518

9 Craniopagus and Cranial Midline Epidural Venous Anomalies

▲

Fig. 9.7A–J. Typical PHACE syndrome with facial hemangioma (A), sternal defect posterior fossa malformation. B–F In addition, there is an unusual midline defect: agenesis of the falx. G–J The leptomeninges are common both supra- and infratentorially; subarachnoid arteries and veins cross the midline, the sinuses are flat off the midline. E–I see p. 519

Postulated Relationships Between the Superior Sagittal Sinus and Adjacent Structures

Fig. 9.7E–J. Legend see p. 518

519

520

9 Craniopagus and Cranial Midline Epidural Venous Anomalies

Fig. 9.8A, B. Craniopagus: both brains give rise to two separate superior sagittal sinuses. A On the midline, the anastomotic vein allows communication between both sinuses. 4, Falx cerebri. On the boundary zone, dura mater is represented. B When both falx cerebri (4) converge, conjoined superior sagittal sinus becomes possible

Fig. 9.9A, B. Convergence of both falcine signals on the midline allow for conjoined sinus (A). Anterior divergence induces separate sinuses (B)

Ladan and Laleh’s Angiographic Anatomy

521

Fig. 9.10. Alobar holoprosencephaly. Note the absence of falx and superior sagittal sinus. (Courtesy of M. Catala)

9.3 Ladan and Laleh’s Angiographic Anatomy The angiographic protocol used aimed to precisely define the morphology of arteries and veins on both sides as well as the functional efficacy of the postulated surgical rerouting of the dural sinuses (Table 9.2; Fig. 9.11). Absence of dural coverings on the frontier zones intracranially favors interindividual venous drainage, as seen in patients Laleh and Ladan (Fig. 9.12). In their case, the venous drainage of the superficial sylvian vein of Laden’s left hemisphere opened into Laleh’s right Breschet and cavernous sinuses. Similarly, the common temporal pole gyri led to interindividual temporal lobe arterial anastomoses between both MCAs (Fig. 9.12). Arterial connections are found in very few cases (seven in Winston’s 1987 review). A ring sinus was not observed in their case since that would relate to a vertex adherence. However, one limb of the ring has to correspond to one twin’s falx signal, whereas the other limb of the ring has to be related to the other twin’s falx sinus. It is difficult to imagine that both falx cerebri are located on the midline away from the periosteum and orthogonal to the frontier zone. Analysis of the dural disposition supratentorially in Laleh and Laden is quite clear as an indicator of the disposition of the sinuses. The lateral skull adhesion allowed convergence posteriorly of both falces on the junction line and therefore constitution of a conjoined superior sagittal sinus (Fig. 9.13). More cranially, the diverging position of both skulls led to the divergence of falx subsequent to individualization of the superior sagittal sinus for each twin. The bony midline at that location did not coincide with a brain midline signal and therefore did not lead to the development of a single sinus arrangement. The venous disposition in Laleh and Laden (Fig. 9.14) is therefore very illustrative of the position of the falx as drawn in Fig. 9.15 (Lasjaunias et al. 2004).

VA

ACA PCA

MCA

ICA

IJV

Thyroidal/laryngeal EJV

Occipital Facial

– –

Carotid bifurcation Distal ECA

Ladan left

Low <2 cm mandible ±1.3 mm No superficial temporal Small middle deep temporal Small middle meningeal; anastomosis on the lesser wing with opposite side, Deep course of IMA – ±1 mm complete – ±1.3 mm Faciolingual trunk Short facial distal ending in the alar branch – ±0.6 mm Not explored Large faciolingual venous trunk Small, but present Large jugular bulb, large Possible condyloid vein neck vein ±1.2 cm. with post JV Balloon was occlusive, possible condyloid vein Usual Small incomplete cervical OPH artery, usual position loop OPH artery, usual position Usual type Anastomosis across the junction with Laleh’s right MCA at the temporal pole level Preferential flow from Laleh’s to Ladan’s MCA No opacification of Laleh’s MCA through Ladan’s injections Good single trunk on each side and patent AComA From ICA Minute branch from basilar (small temporo-occipital lobe) Small. Faint opacification Dominant, nearly no left PCA of micro L.PCA

Ladan right

Vessel

Table 9.2. Anatomical analysis of the venous disposition

Usual type

Usual, OPH artery, usual position

Large

– Not explored

– –

– –

Laleh left

Good single trunk on each side and patent AComA Small branch from basilar From ICA (small temporo-occipital lobe) Large Dominant

Straight cervical course OPH artery, usual position OPH artery, usual position Anastomosis across the junction with Ladan’s left MCA at the temporal pole level Preferential flow from Laleh’s to Ladan’s MCA

Largest outlet >1.5 cm balloon was not occlusive

±0.6 mm No special afferent seen

±1.3 mm ±1.3 mm Faciolingual trunk Short facial distal

Low <2 cm mandible ±1.3 mm No superficial temporal No deep temporal Small MMA; anastomosis on the lesser wing with opposite side

Laleh right

522 9 Craniopagus and Cranial Midline Epidural Venous Anomalies

Half-spheric cerebellar vein opening into a tentorial sinus joining the proximal right transverse Superficial sylvian vein drainage by one collector into a single spheric parietal sinus then directly into the right cavernous sinus Secondary drainage into pterygoid plexus and IPS into small right jugular bulb Spheric parietal sinus drainage into the right. cavernous sinus. No deep sylvian vein seen Opening into pterygoid plexus and IPS into small right jugular bulb Large opening into right distal transverse sinus Large opening into specific SSS

Cerebellar veins

Frontoparietal veins

Labbé vein

Cavernous sinus

Sphenoparietal sinus

Ladan right

Vessel

Table 9.2. (continued)

Opening into specific SSS Small orbitofrontal vein draining across into Laleh’s right spheric parietal sinus

Absent (microtemporal lobe)

No

Superficial sylvian vein drainage by three collectors into a single spheric parietal sinus across the junction into Laleh’s right spheric parietal sinus and then directly into Laleh’s right cavernous sinus

Large vermian vein opening into proximal right transverse sinus

Ladan left

Opening into specific SSS

Absent (microtemporal lobe)

Large collector for sphenoparietal sinus, secondary opening into ipsilateral large pterygoid venous plexus via vein of foramen ovale

Superficial sylvian vein drainage by one or two collectors into a single spheric parietal sinus then directly into the right cavernous sinus

Large inferior mid vermian vein opening into cerebellar falx (occipital sinus) and ipsilateral left transverse

Laleh right

Large, opening into the ipsilateral transverse sinus Opening into specific SSS

Small cavernous sinus and drainage into pterygoid plexus and IPS into small left IJV Deep sylvian vein afferent

Superficial sylvian vein drainage by two or three collectors into a single spheric parietal sinus then directly into a paracavernous sinus and in the left pterygoid plexus

Two half-spheric cerebellar spheric veins opening into proximal left transverse

Laleh left

Ladan and Laleh’s Angiographic Anatomy 523

524

9 Craniopagus and Cranial Midline Epidural Venous Anomalies

Fig. 9.11A–D. Laleh and Ladan (A), craniopagus twins, and various presurgical 3D models (B–D)

Ladan and Laleh’s Angiographic Anatomy

525

Fig. 9.12A–D. Temporal shared gyrus led to vascular sharing (A).Venous drainage from one twin to the other in the frontal temporal region (B) and temporal arterial anastomosis between both middle cerebral arteries (C, D)

526

9 Craniopagus and Cranial Midline Epidural Venous Anomalies

Fig. 9.13A–C. MRI and MRA demonstrating the separate hemisphere and falx anteriorly (A, B). Posteriorly the falx convergence allowed the sinus to become conjoined (C)

The greatest difficulty arose at the infratentorial level, since in Laleh and Ladan, the infratorcular midline sinus structure could not correspond to a medially located interhemispheric cerebellar signal, but rather a petrous bone adherence. The conjoined sinus had to correspond at that time to a sigmoid and lateral sinus fusion rather than a medial occipital sinus sitting on the midline. The close relationship between both posterior fossa led to persistence of large communicating epidural venous lakes. These remnants of the medial occipital sinus and marginal sinuses in each twin can be observed in normal individuals (Fig. 9.16) and neonatal malformations (Fig. 9.17). Sinus malformations actually develop preferentially at this level, testifying to this confluence as well as to the proliferative activity of the interperiosteal leptomeningeal dural space of the occipital squamous portion in comparison to that of superior sagittal sinus in the interparietal

Ladan and Laleh’s Angiographic Anatomy

527

Fig. 9.14A–C. Selective injection of the left Ladan’s (A) and right Laleh’s (B) carotid with balloon redistribution of some of the outlets in order to visualize the venous anatomy (C)

or frontal region (Barbosa et al. 2003) (see Chap. 7, this volume) (Fig. 9.18). The most important risks therefore involved the difficulty in properly exploring these spaces and the epidural lakes located on the cranial midline and frontier zone between the twins’ heads. In Laleh and Ladan, although suspected, these lakes were underestimated preoperatively. Our capacity to understand what creates the persistence, development, or the regression of this sinus differentiation is crucial to surgical planning.

528

9 Craniopagus and Cranial Midline Epidural Venous Anomalies

Fig. 9.15A, B. Schematic representation of the demonstrated anatomy (A). Note that the lower portion of the conjoined sinus below the torcular corresponds in fact to the transverse and sigmoid sinuses (B)

Fig. 9.16A, B. Venous phase of a carotid angiogram showing the persistence of a medial occipital sinus corresponding to the posterior fossa equivalent of the superior sagittal sinus with regard to the role played by the supra- and infratentorial falces

Ladan and Laleh’s Angiographic Anatomy

529

Fig. 9.17A–D. Dural sinus malformation with dysmaturation of the jugular bulb on the right and left side. MRI (A–D) demonstrates the large epidural lakes sitting on the posterior fossa midline and the foramen magnum

530

9 Craniopagus and Cranial Midline Epidural Venous Anomalies

Fig. 9.18A–D. A boy presented at birth with facial hemangiomas in the second and third cephalic segments (A). A few months later, epidural hemangiomatous vascular spaces extending over the left cranial fossa from the temporal pole to the torcular were demonstrated (B–D). The lesion was incidentally discovered

Technical Remarks and Functional Testing

531

9.4 Technical Remarks and Functional Testing The management of another set of conjoined twins by the Toronto team was chosen to introduce the role of surgical neuroangiography in the overall management strategy. The craniopagus twins were referred to a Toronto neurosurgical unit from Pakistan (Rutka et al. 2004). They were part of a triplet pregnancy with the third child being born completely normal. The conjoined twins were 3 years old at the time of referral, and were a vertex craniopagus rotated 30° one to the other (Fig. 9.19). Tissue expanders were placed subcutaneously and expanded gradually over several weeks prior to surgery. Although they were outwardly healthy, while awaiting surgery, twin A developed cardiomegaly and twin B developed acute renal failure. Accordingly, the team was mobilized to work quickly and efficaciously to prevent one or the other of the twins from being medically unfit to undergo surgery. The twins were investigated using CT, MRI, and angiography to determine their mode of attachment and shared cerebral structures. Three-dimensional reconstructive CT scans showed the mode by which their cranial vaults were connected. MRI scans revealed how the twins’ brains were related to each other. A common dural shelf was seen to separate the brains of the two twins along half of their plane of attachment. Along the other half, the brains of the two twins were found to interdigitate across an undulating layer of leptomeninges. The MRI, MRA, and MRV suggested a common or shared sagittal sinus. Cerebral angiography demonstrated the passage of middle cerebral arterial vessels from twin A to twin B (Fig. 9.19). Twin A possessed the dominant superior sagittal sinus that was circular in its midportion and shared by twin B. Interventional neuroradiology was utilized in an attempt to disconnect the cerebral circulations of the two twins. The distal branches of the MCA from twin A that were feeding twin B were cannulated and then embolized. A partial separation of the twins’ arterial circulation was thus achieved. The shared sagittal sinus was partially occluded with coils to diminish the cross-flow return. There were no neurological consequences of the arterial or venous embolization in either twin. Progressive renal failure in twin B prompted renal transplantation of a normal kidney from twin A to twin B prior to separation. Following renal transplantation from twin A to twin B, the twins were prepared for surgery. The scalp incision was then made, the tissue expanders removed and a craniotomy was performed. The dominant sagittal sinus of twin A was then identified proximal to its circular sinus formation. The dural venous channel from twin B to the superior sagittal sinus of twin A was thus also found.At this time, the dural venous outflow from twin B to the dominant superior sagittal sinus of twin A was identified. Complete separation of the twins’ brains came after sectioning twin B’s falx below the level of the dominant superior sagittal sinus of twin A. Both twins survived the separation; however, twin B was slow to awaken. Postoperative imaging studies revealed a deep intracerebral hematoma in the right basal ganglia and thalamus, which was followed conservatively. She required prolonged postoperative intubation and ventilatory support. Obstructive

532

9 Craniopagus and Cranial Midline Epidural Venous Anomalies

Fig. 9.19A–D Legend see p.533

▲

Technical Remarks and Functional Testing

533

Fig. 9.19A–I. Preoperative photograph of craniopagus twins A (top) and B (bottom), aged 3 years, from Pakistan. The twins are joined at the vertex and rotated 30° one to the other. A CT scan with three-dimensional reconstruction showing the relationship of the cranial vaults of the two twins. B MRI scan, sagittal (top, twin A) and coronal (bottom, twin B) views. The interdigitation of the parietal lobes is appreciated on one side. A dural shelf separating the two twins can be seen on the other side. Minimal shared cerebral tissue was observed (arrow). The MRI suggested a shared common sagittal sinus. C–G Cerebral angiography of craniopagus twins. Left, early venous phase; right, arterial phase. “Left” refers to the side of the internal carotid of the bottom baby, early and late phases (C–E); “right” refers to the internal carotid of the bottom baby in early (F) and late (G) phase. H, I Postseparation CT shows the intracerebral hematoma. Postembolization and surgical separation: venous hemorrhagic infarction occurred with progressive neurological deficit and death of one of the children. I see p. 534

534

9 Craniopagus and Cranial Midline Epidural Venous Anomalies

Fig. 9.19A–I. Legend see p. 533

hydrocephalus developed after 2 weeks, and a ventriculoperitoneal shunt was placed. One month after separation, twin B suffered from acute pneumonia, fever, and sepsis from which she did not recover. She died 32 days after separation. Twin A leads a normal life with her family in Pakistan without neurological deficit.

9.5 Discussion on Surgical Management There have been several previous reports in the literature regarding the separation of craniopagus twins (Baldwin 1965; Bucholz et al. 1987; Campbell et al. 2002; Drummond et al. 1990; Gaist et al. 1987; Gaist and Rutka 1997; O’Connell 1976; Pertuiset 1989; Winston 1987). Successful separation of both twins with minimum morbidity is rarely accomplished (Gaist et al. 1987; Villarejo et al. 1981). Ethical decisions abound regarding whether such separation should take place. In the case of the twins presented here and treated at The Hospital for Sick Children in Toronto, progressive medical deterioration of both twins prior to surgery prompted neurosurgical separation in an attempt to save the lives of one or both twins. Prior to the separation of these twins, a detailed neuroradiological map was obtained through three-dimensional CT reconstruction, MRI, and cerebral angiography. The data from CT and MRI were captured and transferred to a neuronavigational workstation in the hope of utilizing this device at the time of separation. To our knowledge, this is the first report of the use of neuronavigation in the separation of craniopagus twins. In this particular case, neuronavigation was useful in the early identification of the shared superior sagittal sinus of the two twins. We also elected to attempt to detach the cerebral circulations joining the twins using endovascular strategies. While we were successful on the arterial side of the cerebral circulations, we could not successfully separate the twins at the level of the shared superior sagittal sinus using endovascular techniques. However, as has been reported with the separation of

Discussion on Surgical Management

535

the Baragwanath craniopagus twins in which chronic occlusion of the superior sagittal sinus was accomplished by means of an externally applied vascular clamp (Drummond et al. 1990), we believe that the strategy of slowly occluding the shared superior sagittal sinus of craniopagus twins using endovascular techniques holds great promise for future separations. Since the sacrificing of joined cerebral venous sinuses in craniopagus twins is the operative event that is typically associated with the major morbidity and mortality of the procedure, attempts to chronically occlude such shared sinuses, and yet maintain neurological function, would be a most welcome strategy. Advances in neuroendovascular techniques will undoubtedly lead to greater success in terms of applications to craniopagus twins in the future. Other strategies that have been reported and that facilitate wound closures following separation of craniopagus twins include the use of tissue expanders and the use of autologous split thickness cranioplasties with rigid titanium microplate and screw fixation for reconstruction of the cranial vaults. Because of the rare nature of craniopagus twins, and because of their unique cranial, cerebral, and vascular relationships from one to another, it is unlikely that one strategy can be applied to all craniopagus separations. However, we firmly believe that the approach we have utilized here will be of value to future teams wishing to conduct similar separations.

10 Cerebral Venous Thrombosis

10.1

Introduction 537

10.2

Pathophysiology and Risk Factors 539

10.3

Imaging 545

10.4

Symptoms 547

10.5

Treatment 556

10.6

Outcome 557

10.1 Introduction Venous thrombosis is not a common topic discussed in interventional neuroradiology, although we have referred to it several times in the various chapters of this volume, as a mechanism suspected or confirmed of being responsible for various episodes in the natural history of vein of Galen aneurysmal malformation (VGAM), cerebral arteriovenous malformation (CAVM), dural arteriovenous shunt (DAVS), dural sinus malformation (DSM), and even maxillofacial AVM. Age creates its own symptomatology or natural history, as water-related manifestations rapidly occur with sagittal sinus impairment. Maturation of the granulations, closure of the fontanelles, jugular bulb maturation, and the converging nature of the venous outlets into the torcular are obvious postnatal changes and anatomic weaknesses in this age group (Fig. 10.1, Scheme 10.1). Cerebral venous thrombosis (CVT) in children is a rare disorder but one that is increasingly diagnosed because of greater clinical awareness, improved noninvasive imaging techniques, and the survival of children with previously lethal diseases that confer a predisposition to CVT. Cerebral venous thrombosis usually involves the cerebral venous sinuses such as the sagittal and transverse sinuses but may involve the deep venous system or the cerebral cortical veins in isolation or as part of a diffuse thrombotic process. The earliest description of CVT in children was by Bailey and Hass in 1937. It is estimated that CVT constitutes 25% of ischemic cerebral vascular disease in children, with an annual incidence between 0.29 and 0.67 cases per 100,000 children (deVeber et al. 2001; Carvalho and Garg 2002). Fortythree percent of children with CVT were neonates and 54% were less than 1 year old in a prospectively collected pediatric Canadian stroke registry (deVeber et al. 2001), while in a smaller series of 31 pediatric patients with CVT, 61.2% were neonates, with a median age of 14 days (Carvalho et al. 2001).

538

10 Cerebral Venous Thrombosis

Fig. 10.1A–D. A 1-week-old neonate presented with left-sided convulsions without loss of consciousness. Cranial ultrasound revealed intracerebral hemorrhage on the right side and suspected a deep-seated arteriovenous malformation. A CT showed thrombosis of the torcular extending into the superior sagittal and straight sinus. MRI (B–D) demonstrated recent thrombosis of the deep venous system, the vein of Galen and straight sinus as well as the superior sagittal sinus associated with intraventricular hemorrhage

Pathophysiology and Risk Factors

539

Scheme 10.1. Sigmoid sinus thrombosis in neonates and infants (unilateral sinus thrombosis syndrome)

10.2 Pathophysiology and Risk Factors Thrombosis of the venous system can occur because of venous stasis, prothrombotic states, involvement of the vessel wall, and endovascular deposition of embolic materials. The slower blood flow, in particular in the recumbent position, favors the formation and propagation of thrombus in the venous system (Table 10.1). CVT may be associated with a variety of local or systemic conditions, and after extensive explorations, less then 5% of children with CVT reveal no predisposing risk factor (deVeber et al. 2001). Risk factors for CVT are therefore frequently present and tend to be related to age. Acute systemic illnesses were present in 84% of neonates, the most frequent illnesses being perinatal complications such as hypoxia at birth and dehydration. Head and neck disorders were more common in non-neonates, the majority being infections, while chronic systemic diseases were also more common in non-neonates (deVeber et al. 2001). In neonates, thalamic hemorrhage is thought to be caused by thrombosis of the central veins and the straight sinus (Fig. 10.1), perhaps induced by dehydration (Elhers 1936; Roland et al. 1990). In infancy and childhood, mastoiditis may cause transverse and sigmoid sinus thrombosis (Byers 1933). There is also an association between DST and generalized infection, such as a common cold, as well as with trauma and dehydration (Byers 1933; Taha et al. 1993).A hypercoagulable state, whether acquired or inherited, is important in the pathogenesis of CVT in children. Patients with a malignant tumor such as non-Hodgkin lymphoma, leukemia, and neuroblastoma, may have a variety of coagulation abnormalities leading to a prothrombotic state. Chemotherapy may also be associated with CVT. Tests for prothrombotic disorders have revealed abnormalities in more than 30% of children, including the presence of anticardiolipin antibodies, decreased levels of protein C, antithrombin, protein S, fibrinogen,

540

10 Cerebral Venous Thrombosis

Table 10.1. Clinical manifestations of unilateral dural sinus thrombosis in children Symptom

Underlying mechanism

Bruit Seizures Neurological deficit Intracerebral hemorrhage Subdural hematoma Facial veins Macrocrania Persistent open sutures Tonsillar prolapse Mental retardation Papilledema Optic atrophy

Patent venous sinus turbulence Venous ischemia, hemorrhage Venous ischemia, hematoma Hemorrhagic infarct – Cavernous plexus collateral circulation Water retention – Posterior fossa water retention Cerebral dysmaturation Intracranial hypertension Chronic intracranial hypertension

plasminogen, and the presence of lupus anticoagulant, factor V Leiden, and the prothrombin-gene mutations. The deficiencies of antithrombin, protein C and protein S were in many cases caused by an acquired disorder such as liver disease, nephrotic syndrome, or disseminated intravascular coagulation (deVeber et al. 2001). The impact of factor V Leiden mutation in children with CVT seems to be highest in newborns and young infants, reflecting the different physiology of hemostasis, with proportionately lower levels of protein C and protein S frequently observed in this age group (Carvalho et al. 2001). Malformations of the sinuses (Chap. 4, this volume) or arteriovenous shunts (Chaps. 2 and 3, this volume) may be seen before or at the time of the thrombotic episode. The causative responsibility that the occlusion plays in the appearance of the shunt is discussed in the chapters devoted to each of these pathologies. These malformations can be combined with a coagulation disorder, as in a recent VGAM patient in our series who presented with a thrombophlebitic episode supposedly unrelated to the completely treated arteriovenous shunt, for which a factor V Leiden genetic deficit was confirmed. DSMs during infancy are also known to produce extensive thrombosis of the epidural lakes. This phenomenon can sometimes be present in utero and lead to the mistaken diagnosis of epidural hematoma (see Chap. 7, this volume). Such disorders at these moments point to the specificity of the venous endothelium and/or hemostatic cascade on the venous side at certain ages. The venous ischemic changes observed in neonates and infants with intracranial AV shunts is responsible for the so-called melting-brain syndrome (see Chap. 2, this volume) (Fig. 10.2). Chronic ischemic changes will induce cerebral calcifications, either cortical or subcortical, in the hemispheric white matter (Fig. 10.2). Another child presented a few years after complete exclusion of his VGAM focal seizures related to parietal lobe cortical venous thrombosis. Soderman et al. (1996) reported on a patient with DST of the straight and left transverse sinus who was treated with ventricular drainage and direct infusion of fibrinolytic substance into the thrombus. The patient had anticardiolipin antibodies, which interfered with the activated prothrombin time and led to insufficient heparin levels (Fig. 10.3).

Pathophysiology and Risk Factors

541

Fig 10.2A–F. Various aspects of venous damage to the brain in nannies with intradural AVMs leading to focal or diffuse melting-brain syndrome. E,F see p. 542

542

10 Cerebral Venous Thrombosis

Fig 10.2E,F. Legend see p. 541

Pathophysiology and Risk Factors

Fig. 10.3A–F. Legend see p. 544

543

544

10 Cerebral Venous Thrombosis

Fig. 10.3A–H. Thrombosis of the straight sinus and the left transverse sinus in an 11year-old boy with a history of minor head trauma followed by unrelated infection of the upper airways. The patient presented with severe impressive and expressive dysphasia and stupor close to coma. He was treated with intraventricular shunting and in situ fibrinolysis as well as intravenous heparin. Antibodies against cardiolipins were abundant. Despite successful local thrombolysis, the patient suffered repeated thrombosis of the left transverse sinus and late thrombosis of the jugular vein. He recovered completely and was treated with oral anticoagulants for 1 year after the episode. A, B MRI on the day of admission. Note bilateral thalamic edema with compression of the third ventricle and widening of the lateral ventricles. Edema and hemorrhages in the left temporal lobe. C Magnetic resonance angiography (MRA) on the day of admission showed the absence of flow in central veins and straight sinus. D Sinography before thrombolysis with injection into the right transverse sinus showing contrast medium around the thrombus. E Sinography after thrombolysis and balloon thrombectomy. Injection into the right transverse sinus showing contrast medium in the sinus around the remainder of the thrombus. Posteroanterior view. Note the flow over the midline into the contralateral sinus and reflux into cortical veins. F, G MRA immediately after thrombolysis demonstrated reconstitution of some flow in the left sigmoid sinus, increased flow in the right transverse sinus, and diminished flow in the left transverse sinus close to the torcular. H MRI 7 months after the incident. Small remaining hypointense areas in thalami. In the left temporal lobe, there were small remnants of previous hemorrhages, but no other changes. (Soderman et al. 1996)

Imaging

545

10.3 Imaging Widespread availability of power Doppler ultrasound, contrast-enhanced CT, and MRI has resulted in increased and earlier diagnosis of CVT in children; conventional angiography is currently rarely used to make this diagnosis (Macchi 1986; Sze et al. 1988; Rippe et al. 1990, Anxionnat et al. 1994; Lee and ter Brugge 2002; Fig. 10.1, Table 10.2). The degree of clinical suspicion, the quality of the examination and the radiological interpretative skills all influence the accuracy of these imaging studies. In each situation and depending on local circumstances, one may favor one modality over another, with the accuracy for detection of dural sinus thrombosis being nearly equal for all modalities in centers of imaging excellence, with MRI being the most sensitive. Detection of cortical vein thrombosis without dural sinus thrombosis either requires detailed MRI examination with special sequences or careful selective cerebral angiography (Fig. 10.4). Conventional cerebral angiography will be able to document the extension of the lesion and the quality of the venous collateral pathways. In a cohort of 160 pediatric patients with CVT, the location of the thrombosis was superficial in 86% and deep in 38%, with no significant differences between neonates and non-neonates (deVeber et al. 2001). Multiple sinuses were involved in 49%, while the lateral sinus was more frequently involved in non-neonates (60%) than in neonates (39%). Cerebral parenchymal infarcts were present in 41%, which were hemorrhagic in more than 75%. Extraparenchymal hemorrhage was documented in 9%.

Table 10.2. Characteristic high-field MRI findings in the progression of venous thrombosis (Macchi 1986)

Initial

Intermediate

Late

Description of findings

Appearance of thrombosis

Absence of flow void; possible collateral venous channels on T1W1 No demonstrable flow with peripheral hyperintensity first observed on T1W1 and then on T2W1; hyperintensity progresses to fill the vessel lumen likely to correspond to the thrombus Beginning of recanalization of the vessel

Vessel appears isointense on T1W1and hypointense on T2W1 High intensity first on T1W1, then also T2W1

Flow void in recanalized venous channels

T1W1, T1-weighted images; T2W1, T2-weighted images.

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10 Cerebral Venous Thrombosis

Fig 10.4A–E. A 4-year-old child presented with generalized seizures and persisting headaches. A–C Typical CT and MRI aspect of cortical vein occlusion. D–E Focal parietooccipital vein occlusion with patent adjacent sinuses

Symptoms

547

10.4 Symptoms The presenting clinical features of CVT in children are age-dependent and can vary from minimal and nonspecific symptoms such as decreased oral intake and irritability to more ominous signs such as lethargy and coma. Seizures, fever, lethargy, or irritability and respiratory distress are common signs of CVT in neonates. Older children commonly present with fever and lethargy often associated with the classic signs of intracranial hypertension such as vomiting, headaches, papilledema, and abducens nerve palsy (Carvalho et al. 2001). In the Canadian pediatric cohort with CVT, 58% of the children had seizures, 76% had diffuse neurological signs, and 42% had focal neurological deficits (deVeber et al. 2001). If the DST develops slowly, the patient may only have signs of chronic outflow obstruction, such as macrocrania, bruit, or enlarged facial veins (Pruvost et al. 1989; Fig. 10.3). Progressive lateral or sigmoid sinus thrombosis may result in benign intracranial hypertension (Greer 1967; Roland et al. 1990), macrocrania with facial collateral venous circulation (Pruvost et al. 1989), or optic atrophy (Figs. 10.5, 10.6). The initial symptoms of pseudo-tumor cerebri syndrome (Lessel 1992) in older children and adolescents are typically headaches, sometimes accompanied by nausea and vomiting. However, young children may present with irritability rather than headaches. Some children are asymptomatic, their papilledema discovered at a routine school eye examination. Pseudo-tumor cerebri can also be manifest in infants as somnolence or apathy. Ataxia and dizziness are early symptoms in some childhood cases. The ataxia is intermittent. Neck, shoulder, or back pain may occur. Seizures and possibly ictal twitching of one hand have been reported. Paresthesias, facial numbness, tinnitus, and limb numbness have also been described. The onset of the process – its acute extension vs its slowly progressive development, which enabled the collateral venous system to develop – may give rise to different syndromes (Fig. 10.7). In some instances, although the dural sinuses are patent, the cerebral venous pattern at angiography suggests thrombosis of the cerebral veins (Fig. 10.8). In CVMS (Sturge-Weber disease), occlusion of the cortical veins is well recognized and an important part of the disorder (Fig. 10.9; see also Chap. 8, this volume). It is often impossible to assess whether the cerebral vein thrombosis is isolated or secondary to a (spontaneously recanalized) sinus thrombosis or transdural vein thrombosis. We have seen sinuses spontaneously reopened in infants with VGAM (see Chap. 3, this volume). Craniostenosis, like other skull-base diseases, can produce occlusion of the basal sinuses and therefore a CVT syndrome. However, when bilateral, it rapidly leads to hydrodynamic disorders rather than a venous ischemic syndrome to the brain. Transcranial outlets are recruited to bypass the obstacles. The scalp and facial veins then drain the normal brain and should therefore be preserved during surgery (Fig. 10.10).

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10 Cerebral Venous Thrombosis

Fig. 10.5. A A 4-year-old boy presenting with macrocrania (>4 SD), intracranial pulsatile bruit, and prominent nonpulsatile facial veins. Angiography demonstrated B a right-sided lateral and sigmoid sinus thrombosis (arrow) with C, D transcranial and transorbital collateral circulation. There was no particular arterial anomaly and no arteriovenous shunt. The bruit was related to turbulence inside the jugular bulb. Eight years later, the child was normal, and no treatment was prescribed

Symptoms

549

Fig. 10.6A–E. A 5-year-old boy presented with significant macrocrania (>5 SD). A The skull sutures were still open. B There was right-sided sigmoid sinus occlusion and bilateral chronic papilledema with beginning bilateral optic atrophy without a significant decrease in vision. Neurocognitive evaluation was normal. There was a loud bruit at the level of the left jugular vein. C–E Angiography demonstrated a delay in the contrast transit time through the capillaries of the brain. The cerebral veins had a pseudo-phlebitic appearance. There was no evidence of cavernous sinus opening of the cerebral veins. The right lateral sinus was not seen. This syndrome is typical of unilateral sinus occlusion. E see p. 550

550

10 Cerebral Venous Thrombosis

Fig. 10.6E. Legend see p. 549

▲

Fig. 10.7A–F. A 9-year-old child presented after a seizure with bilateral permanent visual impairment, as well as some transient postictal motor deficit. A–C The diagnosis of osteopetrosis was well established from the bone and chest radiographies. Failure to thrive and exophthalmos were associated clinical findings. D Bilateral occlusion of the jugular bulbs was demonstrated at angiography. Venous collateral circulation used the mastoid emissary vein and the ophthalmic venous system. C–F see pp. 551, 552

Symptoms

Fig. 10.7C,D. Legend see p. 550

551

552

10 Cerebral Venous Thrombosis

Fig. 10.7E,F. (continued) E–F Severe carotid stenosis at the skull base was documented

Fig. 10.8A–B. Legend see p. 553

▲

Symptoms

553

Fig. 10.8A–F. A 19-month-old boy presented after a generalized seizure with a persistent postictal hemiparesis. A, B MRI and C, D angiography performed at the age of 5 years showed a typical transcortical bilateral collateral circulation appearance involving the striate veins bilaterally and the transcallosal vein on the right side. This pattern is clearly different from the appearance of developmental venous anomaly (DVA) and suggests a secondary response to cortical vein occlusion without dural sinus impairment. E, F Note the symmetry of the images. This appearance is compatible with a diagnosis of early (subclinical cerebral location of CVMS (SturgeWeber disease) without a port-wine stain

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10 Cerebral Venous Thrombosis

Fig. 10.9. A–D Typical MRI appearance of unilateral cerebral and bone lesion in CVMS (Sturge-Weber disease). E,F see p. 555

Symptoms

Fig. 10.9. (continued) E, F Rare posterior fossa CVMS3 (Sturge-Weber disease) appearance shown at vertebral angiography.

555

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Fig 10.10A, B. Bilateral jugular bulb occlusion in a child with Apert syndrome. Collateral circulation through superior sagittal sinus emissary veins mimic a sinus pericranii

10.5 Treatment General medical care and neurologic supportive care is the mainstay of treatment. Adequate hydration is critical and aggressive antiepileptic and antibiotic therapy should be used when appropriate. The usual treatment of acute CVT in adults involves early intervention in the process by means of anticoagulation therapy (Bousser et al. 1985; Einhaupl 1991; De Bruyn and Stam 1999; Table 10.3). There is, however, limited data regarding the efficacy and safety of systemic anticoagulation and fibrinolysis in pediatric patients with CVT. A pilot study involving 30 children with CVT, with a median age of 6 years, where ten patients were given standard heparin and 12 children low-molecular-weight heparin (LMWH), it was demonstrated that anticoagulant therapy and in particular LMWH was safe and may have a role in the management of children with CVT (deVeber et al. 1998). In a Canadian cohort of pediatric patients with CVT, 53% received antithrombotic therapy, which represented 36% of the neonates and 66% of the non-neonates. Most children were treated for a 3-month period and none of these died or had neurological deterioration because of hemorrhagic complications. Seventy-four percent of the neonates required anticonvulsant therapy as compared to 42% of the non-neonates with CVT (deVeber et al. 2001). The role of surgery is by and large limited to mastoidectomy and shunt placement.

Outcome

557

Table 10.3. Standardized dosages in thrombotic therapy of children (Evans and Wilmott 1992) Drug

Dosage

Urokinase rt-PA

4,400 IU/kg as loading over 10 min followed by 4,400 IU/kg per hour 0.1–0.5 mg/kg per hour (for up to 3 days)

rt-PA, recombinant tissue-type plasminogen activator.

The role of fibrinolytic therapy by the retrograde transvenous approach used in adults who are not responding to anticoagulant therapy (Tsai et al. 1992; Svendsen 1993; Horowitz 1994; Lee and Ter Brugge 2002) is still extremely rarely performed in the pediatric population with CVT.

10.6 Outcome The outcome of pediatric patients with acute CVT is highly variable, and reports in the literature are often of limited value because of the small number of patients receiving adequate follow-up assessments (Carvalho et al. 2001). A cohort of 143 children in which neurological outcome after CVT could be assessed with a mean follow-up of 1.6 years included 61 neonates and 82 non-neonates. Of these, 54% were neurologically normal at follow-up, 38% had neurological deficits, and 8% had died, with half of the deaths being directly related to CVT (deVeber et al. 2001). Predictors for adverse neurological outcome were seizures at presentation for nonneonates and the presence of infarcts in neonates and non-neonates. Thirteen percent of children had symptomatic recurrent thrombosis. The long-term neurological of sinovenous thrombosis in children is still unclear, but the best available estimate suggests that after a mean of 2 years, approximately 75% of neonates and 50% of non-neonates will be neurologically normal (Shevell et al. 1989; Barron et al. 1992; deVeber et al. 2000). It is not currently possible to predict which patients will recover with the best medical therapy and it seems reasonable to assume that the poorer the patient’s condition, the worse the prognosis will be and therefore a more active therapy (anticoagulation) involving some degree of risk will be warranted. It also seems reasonable to use an aggressive form of treatment (retrograde transvenous fibrinolytic therapy) in those children whose condition declines despite adequate anticoagulation therapy.

11 Hemangiomas

11.1

Introduction 560

11.2

Pathogenesis 562

11.3

Histological Findings 563

11.4

Clinical Presentation of Hemangiomas 564

11.5

Diagnosis 570

11.6

Complications in Hemangiomas 574

11.7

Management of Hemangiomas 577

11.8 11.8.1 11.8.2 11.8.3 11.8.4 11.8.5

Pharmacological Therapy of Hemangiomas 578 Corticosteroids 578 Interferon-Alpha 2a 579 Vincristine 579 Aminocaproic Acid 579 Other Treatments 579

11.9

Laser Treatment of Hemangiomas 580

11.10 Endovascular Treatment of Hemangiomas 580 11.10.1 Arterial Embolization 580 11.10.2 Intralesional Embolization 582 11.11

Noninvoluting Capillary Hemangiomas 585

11.12

Subglottic Hemangiomas 588

11.13

Periorbital Hemangiomas 590

11.14

Oral Hemangiomas 592

11.15

Salivary Gland Hemangioma 592

11.16

Bone Hemangioma 595

11.17

Associated Anomalies 598

11.18

Psychological Impact 598

11.19

Kaposiform Hemangioendothelioma and Consumption Coagulopathy, the Kasabach-Merritt Syndrome Phenomena 602

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11 Hemangiomas

11.1 Introduction Hemangiomas are the most frequent vascular lesion specific to the pediatric population. Despite their benign nature, they can cause significant morbidity and even mortality if not properly recognized and treated. Over the past 20 years, the management of pediatric vascular disorders has emerged as a unique, truly interdisciplinary specialization in medicine. Advances in the biological characterization of vascular lesions have led to a reformulation of their classification. The landmark work of Mulliken and Glowacki in 1982 provided the basis for these changes (Table 11.1). Mulliken and Glowacki’s classification used tissue culture, histochemical, and electron microscopic studies, and were able to distinguish vascular lesions on the basis of endothelial behavior. They basically divided vascular lesions into two groups: hemangiomas and vascular malformations. They demonstrated that hemangiomas show endothelial hyperplasia, with an elevated mast cell population in the basement membrane, leading to a rapid proliferative phase and then to a stable plateau phase followed by an involution phase. This differs from vascular malformations, i.e., defective vessel remodeling without evidence of cellular proliferation, although an active role is played by certain growth factors. Histological findings in vascular malformations relate to the channel abnormalities present; the endothelium may show qualitative changes without evidence of increased cell turnover. Differences in hemangiomas and vascular malformations, the two major categories of lesions, are supported by clinical, histological, and histochemical analysis, as well as by characteristic imaging findings (Merland et al. 1980; Lasjaunias and Berenstein 1987; Enjolras and Mulliken 1993;

Table 11.1. Craniofacial vascular lesions (modified from Mulliken and Glowacki 1982, reprinted from Lasjaunias and Berenstein 1987)

Mast cells per high-power field (microscope) Factor VIII antigen Tissue culture In vitro angiogenesis Capillary formation Cell culture Clot culture Present at birth (%) Female:male ratio Vascular walls Cellular stroma

Hemangiomas

Vascular malformations

25

0.8

+ Easy Yes

+ Almost possible No

1–2 months 5 days 30 5:1 Thick basement membranes +

No No 90 1:1 Thin basement membranes –

Introduction

561

Finn et al. 1983; Mulliken and Glowacki 1982: Mulliken and Young 1988; Takahashi et al. 1994, North et al. 2000). This classification also permits a clinicopathologic differentiation, which can be translated into their clinical presentation and natural history. An important addition to our understanding of the proliferation phenomenon is the recent identification of various cellular markers in proliferating hemangiomas, including proliferating cell nuclear antigen (PCNA), type IV collagenase, vascular endothelial growth factor, basic fibroblast growth factor (bFGF), E-selectin, and urokinase (Takahashi et al. 1994). These markers are absent in vascular malformations. Hemangiomas overexpress the angiogenic proteins bFGF and vascular endothelial growth factor (VEGF) during the proliferating phase, and preliminary data indicate that the diagnosis of hemangioma can be supported, and the results of therapy monitored, by measuring bFGF levels in the urine (Takahashi et al. 1994). Cellular proliferation in hemangiomas is inhibited by interferon-a- (Ezekowitz et al. 1992; see Chap. 13, this volume). In 2000, North (North et al. 2000, 2001a) made the observation that hemangiomas were always positive for a specific immunohistochemical marker, not linked to mitotic activity, which reliably distinguishes endothelial cells of juvenile hemangiomas at all stages of their progression, in both the proliferative phase and the involution phase. The infantile hemangiomas display positive immunoreactivity for GLUT 1, mersin, Lewis Y (LeY) antigen, and Fc gamma receptor II (FcgRII), all placenta-associated antigens that are only found in the endothelium at sites of blood tissue barriers such as neural tissue (blood–brain barrier, BBB) and placenta but not seen in any other vascular tissue from tumors, malformations, or granulations (North et al. 2000; Waner 2001). A still underestimated factor in these complex lesions is their physiology and hemodynamics, which is infrequently noted, despite the specimen, or portion of the lesion obtained for histological or immunochemical studies that may not reflect all the various components of the lesion and do not take into consideration the type of flow present and its role in the overall pathology and its clinicopathologic implications. In 1993, Jackson et al. proposed a newer clinical classification system to assist in the selection of appropriate treatment (Jackson et al. 1993). They divided vascular malformations into low flow and high flow based on angiography, indicating the speed of flow through the lesion and the rate of shunting between the arterial and venous components. Even in Jackson’s classification there is no mention of the time when the site or target within the vascular system was affected or the triggering factor or factors that revealed the abnormality (see Chap. 2, this volume). In addition to previous classifications, our observations, based on clinical and angiographic experience over 25 years, with hemangiomas and vascular malformations suggest that they can be further subdivided according to the morphology of the abnormal channels present and their effect on the angioarchitecture at the time of angiographic analysis (see Chaps. 6, 12, 13, this volume). In malformations, the abnormality at the time of presentation, or discovery, may show a direct involvement of the vessel wall, it may involve a single vascular tissue site (arterial, capillary, venular, venous, or lymphat-

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11 Hemangiomas

ic), or it may affect more than one site. The changes seen at a given moment associate the primary dysmorphogenesis (vulnerable target) and the secondary response to changes occurring upstream: endothelial proliferation and/or muscular migration and secondary high-flow angiopathy (Pile-Spellman et al. 1986) and angiogenesis due to collateral circulation (Folkman and D’Amore 1996), thrombosis, ischemia, etc. These changes may result in downstream events (venous dilatation secondary to outflow restriction and subsequent kinking, resulting in further aggravated outflow, i.e., thrombosis, edema, etc. The classification that we have used in the past is similar to that of Mulliken and Glowacki (1982). Under a generic name of vascular anomalies, two types of lesions will be differentiated: vascular tumors and vascular malformations (Table 11.1). The PHACE syndrome and other complex vascular anomalies (CAMS, CVMS) (see Chaps. 6 and 12, this volume) will be presented as separate groups. Our experience with vascular lesions has shown that a clear distinction between malformations and neoplasms is not always possible and overlapping conditions are becoming apparent. The concept of angiogenesis has left the restricted frame of “neovascularization” to describe vessel wall cellular activity. It includes angioectatic changes, as seen in collateral circulation, to true vessel sprouting to fulfill hemodynamic or metabolic needs. With this restriction in mind, the management strategies that we propose for vascular malformations and hemangiomas depend on their location within the body. Each territory carries specific therapeutic risks that affect the choice between conservative management, the search for a palliative treatment to stabilize the lesion, i.e., close the high-flow shunt, treat a complication of the lesion’s progression, devascularize prior to surgery, and complete cure. The understanding of vascular lesions and progress in their treatment is one of the most rapidly changing areas in medicine. Therefore, the possibility that therapeutic techniques may be improved in the future dictates against the use of unnecessary, potentially mutilating procedures, unless life- or function-threatening situations are present.

11.2 Pathogenesis In understanding vascular lesions, their origin, time of occurrence, and the causes of their expression are all important elements. There are three cardinal factors that influence vascular lesions:
The target, the site of the vascular tree that is involved (arterial capillary, venular, or lymphatic).
The time related to a vulnerable window where a specific site or multiple sites are more exposed to becoming triggered.
The triggers will create and later reveal the damage in the target (see Chap. 2, this volume). These causative and revealing triggers may not be identifiable; the latter are likely to include mechanical, hormonal, pharmaceutical, hemodynamic, thermal, radiation, viral, infective, and metabolic agents or events.

Histological Findings

563

The trigger or triggers that reveal the vessel wall defect or create the dysfunction are probably active during specific time windows of vulnerability, expressing the maturation of various synergetic and antagonist systems. The same trigger on the same target may engender a hemangiomatous response at 2 months of age and no detectable abnormality in a 5-year-old child. Of course, the concept of target in early developmental times must be understood in vessel wall forerunners. Cavernous hemangiomas of adults are also tumors that have evolved by cellular proliferation. However, their clinical behavior and histological appearance are quite different from that of infantile hemangiomas. They often contain evidence of thrombosis in the vascular lumen. Central nervous system cavernous hemangiomas are misnomers, since they are venous malformations without proliferative activity and harbor a vascular malformation profile (see Chap. 8, this volume, and Vol. 2, Chap. 2). The hemangiomas of interest to us are the capillary hemangiomas, which are seen in infants in most cases. Cavernous hemangiomas of the liver or orbit occur in older children. Their biological tumor and clinical character is likely to be different from the capillary hemangiomas, and their treatment strategies and technique unrelated to those discussed here.

11.3 Histological Findings Histological findings in hemangiomas include plump, rapidly dividing endothelial cells with lumina of varying sizes, pericytes, and multilaminated basement membranes. During involution, mitotic activity decreases, mast cells appear and subsequently disappear, and endothelial cells drop out and are replaced progressively by deposits of perivascular and intralobular fibrous and adipose tissue. The diagnosis of hemangioma is usually easy and based on the clinical evaluation, sometimes supplemented by imaging. The most conclusive way to differentiate hemangiomas from all other types of vascular lesions is to note that hemangiomas are always positive for specific immunohistochemical markers, which reliably distinguishes endothelial cells of juvenile hemangiomas at all stages of their progression. Although not proven, it has been postulated that this immunophenotypic pattern and that hemangiomas present in the perinatal period are suggestive that hemangiomas may represent systemic metastasis from placental cells, or from angioblasts aberrantly switched toward the placental endothelium phenotype, either by somatic mutation or abnormal local inductive influences (North et al. 2000, 2001b). A more attractive theory may be that the apparent random distribution of hemangiomas is not truly random (Waner et al. 2003), but that the more frequent distribution in the head and neck and in the back of the torso and other locations seems to correlate with early cells of common origin, such as neural crest and/or dorsal mesoderm cells, and therefore with potentially similar vulnerability. During the perinatal period, the placenta releases regulators of angiogenesis. One such factor is Flt-1 (sFlt-1), a potent inhibitor of angiogenesis present in placenta and amniotic fluid that helps

564

11 Hemangiomas

to regulate angiogenesis and is found at a high concentration toward the end of gestation (Clark et al. 1998; North et al. 2002). One may postulate that in the immediate perinatal period, if no longer under the regulation of such angiogenesis inhibitors a single target (80% are single hemangiomas) or multiple targets (20% are multiple hemangiomas) results in unrepressed proliferation or “hemangiogenesis.” Recently, Boye et al. (2001), based on X-chromosome inactivation studies, reported that endothelial cells of hemangiomas are clonal. Blei et al. (1998) and Walter et al. (1999) reported the rare association of familial occurrences. Hemangiomas may involute by progressive cellular death (apoptosis) and dropout. On histologic examination, involuting hemangiomas of childhood consist of masses of endothelial cells with or without vascular lumens. The stimulus for involution is unknown. Possible mechanisms include occlusion of the vascular bed by endothelial cell proliferation or induced by humoral factors.What we see histologically as the lesion involutes is a lack of thrombosis or infarction. Potentially involuting hemangiomas of childhood have characteristic angiographic features that are similar to other benign tumors. They include mass effect, an organized pattern of arterial supply from adjacent arteries, drainage into dilated superficial veins that empty into normal veins, and a parenchymal stain that is often lobulated (Fig. 11.24). Increased circulation time may be present. Noninvoluting cavernous hemangiomas of adults typically appear as nonvascular masses on angiography, although some parenchymal blush and filling of vascular spaces may occur in the late venous phase if sufficient contrast material is injected. They grow like tumors and should not be considered as vascular malformations.

11.4 Clinical Presentation of Hemangiomas Hemangiomas are the most common tumors of infancy, appearing in as many as 10%–12% of children under 1 year of age. They are seen in up to 23% of preterm infants weighing less than 1,000 g (Amir et al. 1986). There is a tenfold higher incidence of hemangiomas in children of mothers who underwent chorionic-villus sampling (Burton et al. 1995). They are seen in the skin of 4%–10% of Caucasian newborns, and less frequently noted in dark-skinned infants (Jacobs and Walton 1976) and in Asians (Hidano and Nakajima 1972). There is a 3–5:1 female to male predominance. Most hemangiomas appear in the first 6 weeks of life. The head and neck region is most frequently involved (60% of cases), followed by the trunk (25%) and the extremities (15% of cases). Hemangiomas occur as an isolated lesion in 80% of cases, whereas in 20% they are multifocal. There is a high incidence of involvement of the liver, gastrointestinal track, or lungs in patients with multiple cutaneous lesions (Hochman 2001). Central nervous system involvement is rare, usually associated with the disseminated form, and is often lethal (Bar-Sever 1994).

Clinical Presentation of Hemangiomas1

Fig. 11.1A–C. Left facio-orbital hemangioma, showing natural proliferation and involution with residual amblyopia. A Newborn girl showing a faint macular stain of the left cheek and lower eyelid. B A few weeks later, the lesion has grown significantly and ulcerated. C At 3 years of age, the lesion had almost entirely involuted, leaving behind cutaneous scarring (secondary to the ulceration), fibrofatty residual, and amblyopia secondary to early visual obstruction

565

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11 Hemangiomas

As for the location of hemangiomas, their distribution is not random (Waner and al. 2003). In their review of 205 children with hemangiomas of the head and neck, Waner et al. described two patterns of tumor growth: the more prevalent focal mass (177 lesions, 76.3%) and the diffuse plaque-like lesions (55 lesions, 23.7%). The focal hemangiomas were mapped to 22 sites of occurrence, all near lines of mesenchymal or mesenchymal-ectodermal embryonic fusion. The most frequent location in the focal hemangiomas was at the level of the mid-cheek, followed by the lateral upper lip and the upper eyelid. The diffuse hemangiomas showed a more segmental distribution and were designated as frontonasal (15 lesions, 27%), maxillary (19 lesions, 35%), and mandibular (21 lesions, 38%). Ulceration was three times more common in patients with diffuse hemangiomas than in patients with focal hemangiomas. Airway obstruction was characteristic of diffuse mandibular hemangiomas, whereas in our experience subglottic hemangiomas have all been single and can probably be explained by personal referral pattern bias. This geographic distribution of hemangiomas in the face is similar to that previously described by Etchevers et al. (2001) for the origin of vascular structures at the face, and Bhattacharya et al. (2004)for the CAMS. Hemangiomas are seen at birth in 30% of newborns, appearing as a small pale or erythematous macula, red spot, ecchymotic-like patch, or telangiectasia. After birth, the lesion grows and if superficial, it will appear more as a bright red, slightly raised, noncompressible plaque lesion (Fig. 11.1). Deeper lesions involving the deep dermis or subcutaneous location may have minimal, blush-like discoloration, or no skin involvement, and will be noted only when they produce sufficient contour asymmetry and therefore tend to present several months later (Fig. 11.2). Hemangiomas without skin involvement can be differentiated from malformations, because of their rapid proliferation, which is faster than the normal growth of the patient. Hemangiomas are characterized by a rapid growth or proliferative phase that may last up to 18 months, at which point they reach a plateau. During this time, there is a marked hypercellularity with increased endothelial turnover, accompanied by mast cell infiltration and proliferation. After this proliferative phase, hemangiomas will grow in proportion to the child for some time. The first sign of the next phase is usually marked by a change from the bright reddish, purplish, or crimson color of the cutaneous involvement to a grayish, patchy less tense vascular soft tissue, with decreased or absent pulsations (Figs. 11.3, 11.4). Nearly all hemangiomas will go through a spontaneous involuting phase (Fig. 11.3). Not infrequently, there may be areas of ulceration and or necrosis with patchy healing (Fig. 11.5). By 5 years of age, 50% of hemangiomas will have achieved complete involution and 70% by 7 years of age, with the remaining children showing continued improvement until ages 10–12 years (Bingham 1979) (Figs. 11.2, 11.3). In approximately half of children, the skin at that time will appear normal, whereas in the other half some type of residual lesion is seen, ranging from a telangiectasia and discoloration to a fatty fibrous replacement with excess tissue (Fig. 11.5).

Clinical Presentation of Hemangiomas1

567

Fig. 11.2. A Spontaneous involution of a deep lip hemangioma in a 6-month-old girl. Note the bluish discoloration that occurred at 6 months, during the peak proliferation phase. B Eighteen years later, the result is satisfactory. Note the normal nasal development

More recently, there have been reports of prenatal diagnosis of in utero (Fig. 11.6) or congenital hemangiomas that are already fully grown at the time of birth (Enjorlas et al. 2001). Among these congenital hemangiomas there are two subgroups: firstly, a rapidly involuting (rapidly involuting capillary hemangioma, RICH) type that will usually regress by 1 year of age (Boon et al. 1996), and secondly a noninvoluting type that may have high flow and may be confused with an AVM (Enjolras et al. 2001) (noninvoluting capillary hemangioma, NICH).

568

11 Hemangiomas

Fig. 11.3A–D. Sequential pictures of a spontaneous progression of a capillary diffuse bilateral hemangioma in the bear distribution, the pictures cover a period of 5 years

Clinical Presentation of Hemangiomas1

569

Fig. 11.4. A 9-month-girl with a healed ulceration in the involution phase. Note the grayish areas in the lower portion, and the darker areas above the healed ulceration. Her monozygotic twin had no lesions

Fig. 11.5. Fatty fibrous replacement with excess tissue can be seen after involution, with a crepe-like laxity and discoloration, and the deformity of the lower ear lobe

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11 Hemangiomas

Fig. 11.6A–C. Prenatal diagnosis ot temporal hemangioma (A, B). Aspect at 1 month (C)

11.5 Diagnosis Superficial hemangiomas are clinically easy to diagnose because of the characteristic red, raised, strawberry-like appearance. The lesions are warm and soft to the touch and may be pulsatile with an audible bruit. Deep lesions with intact overlying skin may be more difficult to diagnose. The skin color may appear blue due to the presence of dilated draining veins beneath the skin (Fig. 11.2). Other characteristic physical features include a pale halo around the lesion and superficial telangiectasias. A history of rapid postnatal growth followed by stabilization and involu-

Diagnosis

571

Fig. 11.7. Bilateral facial hemangioma. MRI in T1; contrast-enhanced coronal images demonstrated uniformly enhancing facial masses with dilated feeding and draining vessels

tion is helpful in making the diagnosis (Figs. 11.1–11.3). Involution is often heralded by a whitening of the surface of the lesion. Involuting lesions have a soft, fatty consistency. In large lesions in young infants, swelling can be seen, particularly if the hemangioma has large draining veins. Such an increase in size during crying episodes can easily be differentiated from localized swelling due to a venous malformation. In some scalp locations associated with bone defect or over a bony suture, pulsatility and a transient increase in size during crying episodes may be noted (Martinez-Perez et al. 1995). While most hemangiomas can be diagnosed clinically, deep lesions may require imaging, especially to rule out soft tissue malignancies and vascular malformations. The hallmark of hemangioma on imaging is the combination of a homogeneous solid parenchymal mass lesion with evidence of increased vascularity, and less frequent high-flow vascular supply and drainage. Ultrasound scanning with Doppler imaging demonstrates the solid parenchymal component, with dilated vessels inside and around the lesion. Doppler assessment of the vessels indicates high flow with decreased arterial resistance and increased venous velocity consistent with micro-shunting. With involution, the vessels become smaller and the Doppler flow more normal. This examination is unnecessary in most situations. MRI demonstrates lobulated parenchymal mass lesions with dilated feeding arteries and draining veins both within and around the lesion (Baker et al. 1993; George et al. 1991; Meyer et al. 1991). Hemangiomas are iso- or hypointense on T1-weighted sequences and moderately hyperintense on T2-weighted sequences (Fig. 11.7). They enhance uniformly in the proliferating phase. There is no bone hypertrophy in capillary hemangioma in infants. Angiography is not needed for

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11 Hemangiomas

Fig. 11.8A–D. A 3-month-old girl presenting with orbital, labial, cheek, and parotid hemangiomas. A Early and B late phase of maxillary angiography showed the vascular supply and the multilobulated capillary blush of the hemangiomas (asterisks). C Early and D late phase of internal carotid angiography showed the main vascular supply of the orbital hemangioma through branches of the ophthalmic artery. (From Garcia-Monaco et al. 1993)

Diagnosis

573

Fig. 11.9. A Neonatal mass growing in the cheek. The mass corresponded to an ectopic choroid plexus. It is of interest to recall (Couly et al. 1995) that the endothelial cells of the choroid plexus (B) are derived from the same mesodermic region as the facial ones (see for comparison Fig. 11.21)

diagnosis; when performed at the time of a planned endovascular session, angiography demonstrates dilated feeding arteries, organized gland-like arterial angioarchitecture with a dense parenchymal blush, and drainage into dilated adjacent veins (Burrows et al. 1983) (Fig. 11.8). Venous filling may be very rapid, indicating arteriovenous shunting, although no arteriovenous fistulas exist. It may sometimes be difficult to distinguish hemangioma from hypervascular soft-tissue tumors, which tend to have less well-defined margins and irregular vessels with signs of encasement and neovascularity. Once in our experience a lesion clinically mimicked a neonatal form of hemangioma and turned out to be an ectopic choroid plexus located within the soft tissues of the cheek completely distinct from the cranial cavity (Fig. 11.9).

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11 Hemangiomas

11.6 Complications in Hemangiomas Approximately 20% of hemangiomas are associated with symptoms that may require treatment (Lasjaunias and Berenstein 1987; Enjolras et al. 1990). It has been estimated that 1% of hemangiomas are truly lifethreatening. Dermatologic complications manifest as hypertrophy of the epidermis and subcutaneous tissues can result in ulceration and are seen in up to 5% of hemangiomas (Margileth and Museles 1965). Secondary infection and bleeding may be seen, prior to or during the period of ulceration. Ulcerations and bleeding are seldom significant. These complications are also known to speed up regression of the proliferative phenomenon. The cutaneous extension of capillary hemangiomas leaves a very visible skin scar, even after complete regression (Fig. 11.5). This is significantly different from a strictly subcutaneous or a deep-seated lesion. Ulcerations may be destructive and may result in destruction of facial features, frequently seen in the tip of the nose (Cyrano’s hemangiomas) (Fig. 11.10) and in the lip (Fig. 11.10), requiring early intervention (Waner and Suen 1999b). Additional complications can occur, including congestive heart failure (CHF), primarily seen in hepatic or pelvic lesions (Boon et al. 1996a; Martinez-Perez et al. 1995), and are seldom seen in head and neck lesions (Fig. 11.11).

Fig. 11.10A, B. Ulcerations may be destructive and may result in destruction of facial features, frequently seen in the tip of the nose (A) or in the lip (B)

Complications in Hemangiomas

575

Fig. 11.11. A A 3-month-old baby girl with a rapidly growing hemangioma associated with congestive cardiac failure. B Rapid shrinkage of the mass and stabilization of the systemic manifestations was obtained following arterial embolization with particles. Several sessions were needed to fully overcome the clinical problems caused by the lesion

Hemorrhages are usually limited unless they are associated with a hemangioendothelioma with a consumption coagulopathy and will be discussed in Sect. 11.19. In rare cases, there may be significant and difficult-to-control bleeding without coagulopathy, which is mechanical in nature, such as in the folds of a rapidly proliferating lesion (Fig. 11.12). Focal mass effect may be important in periorbital, nose, mouth, and airway locations (Fig. 11.11). This may have immediate consequences, such as compromise to vital functions, or delayed consequences, which may result in either functional (blindness or various optical abnormalities) or dysmorphic symptoms (induced mandibular growth alteration, and in the nose, lip, or ear lobe).

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11 Hemangiomas

Fig. 11.12A–D. Hemangioma in the proliferative phase, with difficult-to-control bleeding at the tissue folds. B, C Left external carotid artery (ECA) before particle embolization. D Clinical picture immediately after the embolization. Note the significant bluish discoloration

Management of Hemangiomas

577

11.7 Management of Hemangiomas Indications for the active management of hemangioma include:









Cardiac failure Coagulation disorder Palpebral occlusion Tip of the nose location Orbital deformity Oral mass effect and mandible growth impairment Subglottic location Steroid resistance, dependence, or intolerance

The scar resulting from active treatment should always be smaller or better tolerated than the sequelae following spontaneous involution without such intervention. Thus the therapeutic challenge in most hemangiomas should not be centered on heroic procedures to be used in rare cases, but rather on the anticipation of the soft and skin tissue residual fibrofatty mass that might remain and may require correction. Newer trends with early interventions to reduce psychological impact must be applied judiciously (Waner and Suen 1999c). To gain the trust of children, some basic rules should be followed: 1. One should always aim to prevent pain in children. 2. The child should not be surprised by sudden actions. 3. He or she (and not only the parents) must be informed directly of what is going to be done and what is expected. 4. One should always tell the child the truth, as they may need to undergo multiple procedures, and their cooperation is essential. Provided that these rules are followed, a positive relationship can be established directly, regardless of any cultural differences. Patience is often necessary to balance the pressure exerted by the environment, and several consultations may be needed to establish direct contact with the child. Because most hemangiomas in the head and neck will invariably involute, observation is recommended in the vast majority of cases. However, certain indications call for actively treating patients. Massive deforming lesions and ulcerating, infected, hemorrhaging lesions warrant early aggressive treatment. Because hemangiomas located on the nasal tip and ear have a high risk of perichondral involvement and are notoriously slow to regress, early treatment is recommended to avoid deformities that will be more difficult to manage later. Other critical locations mandating early treatment include the lip, eyelid, and subglottis to avoid possible short- or long-term severe functional problems such as airway obstruction and blindness. The predictable difference in clinical behavior in the two major categories of vascular lesions, hemangiomas and vascular malformations, dictate entirely different therapeutic approaches (see Chap. 13, this volume).

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11 Hemangiomas

11.8

Pharmacological Therapy of Hemangiomas

11.8.1

Corticosteroids

Zarem and Edgerton’s discovery of the effect of oral corticosteroids on hemangiomas in 1967 was fortuitous (Zarem and Edgerton 1967; Edgerton 1976). These researchers observed resolution of a facial hemangioma after administering systemic corticosteroid for the treatment of hemangioma-associated thrombocytopenia. Reports of successful response to systemic corticosteroid treatment vary from 30% (Barthoshesky et al. 1978; Brown et al. 1972; Haik et al. 1979) to 93% (Waner and Suen 1999c). Steroids are mainly effective in the early, active proliferating phase that occurs in the first 6–8 months of a child’s life. Waner and Suen have recommended a relatively high dose starting regimen: prednisone or prednisolone, 5 mg/kg body weight, as one morning dose. Appropriate gastritis prophylaxis is added. If no response is seen after the 1st week on this protocol, alternative management should be implemented. If the lesion responds by complete cessation of growth or even reduction in size, the full dose should be continued for 2 or 3 weeks.We usually start with prednisone or prednisolone of 2–3 mg/kg body weight per day for 4–6 weeks, followed by tapering of the dose over 2–3 months. Systemic corticosteroids are considered by some to be the standard treatment for vision-threatening hemangiomas. All routes of administration have been implemented. The definitive mechanism of action is not clear, but proposed explanations include sensitization of the hemangiomatous vasculature to circulating endogenous vasoconstrictors (Edgerton 1976). Sasaki and colleagues (1984) described the influence of corticosteroids on hormone receptors in hemangiomas. Folkman and co-workers (1983) reported that cortisone inhibited angiogenesis in the presence of heparin. In an effort to overcome the systemic side effects or the risk of intralesional injections, clobetasol cream, a potent topical steroid, is used. Topical and intralesional injections of corticosteroids will be discussed in the treatment of periorbital hemangiomas in Sect. 11.13. Potential known complications of corticosteroid therapy include immunosuppression with increased frequency of childhood infections (Gunn 1981). Cushingoid changes, failure to thrive, increased appetite, and irritability are all reversible (Sadan and Wolach 1996). Systemic or local steroid treatment with the exception of Kasabach-Merritt syndrome (Brown et al. 1972) is not always effective in capillary hemangiomas (Haik et al. 1979) and some rebound growth may be observed after discontinuation (Lasser and Stein 1973). However, it may take 1 or 2 weeks to observe a response, with a too rapid involution with necrosis and ulceration leading to considerable problems of reconstruction.

Other Treatments

579

11.8.2 Interferon-Alpha 2a

Interferon-alpha 2a was originally developed as an antiviral agent, was noted to have an unexpected improvement of Kaposi’s sarcoma (a vascular tumor) during treatment trials in patients with the acquired immunodeficiency syndrome. Further studies revealed that interferon inhibits the advancement of capillary endothelium in vitro and angiogenesis in mice. Subsequent to these discoveries, the role of interferon in treating life-threatening hemangiomas has been under controversy with limited acceptability (Scheepers and Ouaba 1995; Garza et al. 2001). There have been some important side effects after interferon therapy, which include elevation of liver enzymes, low-grade fever, and irreversible neurotoxicity (Egbert and Nelson 1997), including an unacceptably high incidence (approximately 20%–25%) of severe spastic diplegia, presenting sometimes months after treatment with interferon and usually irreversible. Therefore, with the exception of severe, bilateral visionthreatening hemangiomas or those with intracranial extension or lifethreatening lesions that fail to respond to steroid treatment without a good surgical or endovascular option, the present recommendation appears to be to avoid interferon altogether.

11.8.3 Vincristine

Vincristine has been shown to be effective for refractory cases of hemangioma, and will be discussed in Sect. 11.19. Due to serious and sometimes delayed neurological complications, this therapy is no longer recommended in management of hemangiomas.

11.8.4 Aminocaproic Acid

Aminocaproic acid has been used in some patients, but is also not an innocuous drug (Neidhart and Roach 1982), and it is reserved for cases with consumption coagulopathy (see Sect. 11.19).

11.8.5 Other Treatments

Hemangiomas are at least theoretically responsive to radiation therapy, but this modality is not currently considered acceptable due to its longterm side effects (malignancy, regional growth impairment, and scarring). Streptokinase, heparin, and aspirin have all been used with mixed results.

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11 Hemangiomas

11.9 Laser Treatment of Hemangiomas Almost all forms of medical lasers available have been used to treat hemangiomas. In superficial telangiectasias associated with a regressing hemangioma, pulse dye photocoagulation should be used with caution to avoid any cutaneous scarring (Mulliken 1991). Nd:YAG laser results have been more dramatic but are associated with a much higher rate of complications, including delayed healing and permanent scarring. Carbon dioxide laser is more efficacious as an incisional and coagulating tool as opposed to an ablative instrument (Kom 1989). Waner and Suen (1999c) reported promising results using carbon dioxide laser for resurfacing of atrophic changes of involutional hemangiomas. The flashlamp-pumped dye laser (also called pulsed-dye laser or tunable dye laser) first reported by Geronimus and Ashinoff (Geronimus and Ashinoff 1991; Warner et al. 1994, Waner and Suen 1999c) for treatment of hemangiomas is now regarded as the laser of choice. Its wavelength can be modified. To best treat hemangiomas, the wavelength should be set between 585 and 600 nm (yellow light). A longer wavelength will result in deeper penetration, but this carries with it an increased risk of hypopigmentation. Pulse duration is another critical factor in the use of this type of laser. A longer exposure time will address larger vessels but at the same time increase thermal damage to surrounding tissue. In Geronimus and Ashinoff ’s series (Geronimus and Ashinoff 1991), there were no cases of ulceration, hypopigmentation, or scarring, but there was only a modest reduction in the size of all hemangiomas treated. They proposed that earlier treatment, when the lesion is smaller and thinner, may result in a better outcome.

11.10 Endovascular Treatment of Hemangiomas 11.10.1 Arterial Embolization

Arterial embolization employing microparticles or fluid agents such as N-butyl cyanoacrylate (NBCA) can produce significant ischemia and necrosis within the tumor. It is indicated in the treatment of life-threatening hemangioma, where drug treatment has failed or where mass reduction is rapidly required, prior to the anticipated response to medical therapy in patients with Kasabach-Merritt Syndrome (KMS) (Fig. 11.13) or cardiac failure (Fig. 11.11). Embolization of at least 70% of the arterial supply is necessary to produce a significant clinical response (Lasjaunias and Berenstein 1987; Burrows et al. 1987; Burrows and Fellows 1995; Konior et al. 1988). The result may be transient, requiring repeated embolizations, sometimes because of the improper choice of embolic agent, proximal embolic deposition, or persistent proliferation from a nonembolized portion of the lesion. A variety of embolic agents have been used, but superselective catheterization with small (2–3F or 4F) coaxial

Arterial Embolization

581

Fig. 11.13A–C. Kaposiform hemangioendothelioma with a severe consumption coagulopathy (KMS). At 3 months of age, the tumor had grown, platelets were in the 25,000 range, and systemic high-dose steroids failed. At 8 months of age, following radiotherapy, the lesion had ulceration necrosis, infection, and platelets in the 9,000 range (A). Aggressive three-staged embolizations with NBCA permitted platelets to be raised to 180,000, allowing resection (B). Note the tumor specimen (C)

catheters and embolization with polyvinyl alcohol (PVA) particles (50–150 mm, mixed with Gelfoam powder or soaked in ethanol), followed by Gelfoam strips, is the preferred technique. If embolization has been successful, then no swelling occurs, hemorrhages stop, and the cutaneous discoloration typically becomes immediately darker. The mass rapidly decreases in size (in 2–4 days), then stabilizes and likely follows a spontaneous, favorable regression course (Fig. 11.12). The goals of embolization based on the clinical situation and response to drug therapy determine the aggressiveness of the procedure and the need for additional procedures; embolization may also be combined with surgical excision.

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11 Hemangiomas

Embolization may produce several side effects: pain is usually absent, but it may be noted if normal tissues have been embolized together with the hemangioma. Iatrogenic postischemic superficial ulceration is rare, but predictable if Gelfoam powder is used and selectivity toward a skin extension is significant. It may require local antiseptic treatment or antibiotics, with recovery in a few weeks, and may actually accelerate involution. Fever of non-infectious origin may be noted without skin ulceration but with extensive necrosis of a large mass. This may persist for 2–3 weeks in patients with large hemangiomas that are extensively embolized. Anastomoses with the intracranial circulation are widely open in babies and children. The hypervascularity produces a sump effect toward the hemangioma, maintaining a craniofugal flow toward the lesion, which makes these anastomoses invisible during the pre-embolization work-up in the external carotid branches. As the embolization progresses and the flow in the lesion diminishes, a reversal of flow through the anastomosis can occur; therefore continuous fluoroscopic monitoring and follow-up angiography are done to demonstrate their presence (See Vol. 2, Chap. 14). Volume overload in children with large hemangiomas represents a technical challenge, as it requires multiple arterial feeder embolizations and many particle injections with contrast material in order to evaluate the potential anastomosis with the internal carotid or vertebral arteries. Even when dealing with infants weighing over 5 kg, it is necessary to be very careful with the number of injections during embolization in order to avoid the use of large amounts of contrast material. A separate supply from multiple sources constitutes a frequent challenge, as numerous selective catheterizations of various branches are necessary, each of them contributing only a small amount to the overall supply. Multiple sessions are often necessary in such circumstances and staging the procedure will permit a larger contrast material load.

11.10.2 Intralesional Embolization

Direct percutaneous puncture embolization under fluoroscopic monitoring can be done with ethanol (Fig. 11.14) or glue, alone or in combination with transarterial embolization (Fig. 11.14). Although better penetration can usually be achieved by direct percutaneous puncture, caution is important, mostly when using cytotoxic liquids such as alcohol, and one must ensure the intravascular position into the minute channels of the vascular bed of these proliferative lesions. In most instances, injections involve the interstitial space instead of the vascular bed, but this approach should be reserved for urgent cases in which patients fail to respond to medical therapy, surgery is thought to be a poor choice, and arterial embolization treatment is unsuccessful (Fig. 11.15).

Intralesional Embolization

Fig. 11.14. A A 7-month-old girl with a right lower lip and commissural hemangioma with a typical appearance and course. There was also a deeper component with some prominent veins in the skin, present since birth and prior to the proliferation of both lesions. B Two years later, there was involution of the lip lesion, and stabilization of the deep lesion (noninvoluting capillary hemangioma, NICH), the mass is rubbery, warm, and pulsatile. C Lateral, distal facial catheterization for transarterial embolization with particles in 50% alcohol; very distal catheterization was mandatory. D Direct intralesional angiogram prior to 98% ethanol injection. For alcohol to be safely injected, an intralesional intravascular location is mandatory. E Five years later, after transarterial and intralesional embolization, and laser treatment of the skin lesion

583

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11 Hemangiomas

Fig. 11.15A–D. Hemangioendothelioma presenting with a consumption coagulopathy (Kasabach-Meritt syndrome). A Frontal and B lateral digital subtraction angiography (DSA) of the right external carotid artery demonstrates a fine tumor hypervascularity. C Transarterial catheterization of a masseteric branch (arrow). D N-butyl cyanoacrylate (NBCA) cast after the first transarterial embolization following direct puncture and acrylic injections. E see p. 585

Noninvoluting Capillary Hemangiomas

585

Fig. 11.15E. (continued) E Frontal plain images show the final cast obtained. Note the improved opacification of the tumor vasculature by direct puncture, and the penetration of the acrylic in to the lesion’s angioarchitecture

11.11 Noninvoluting Capillary Hemangiomas We have managed several patients with noninvoluting lesions, associated with a cutaneous spider telangiectasia present since birth and a deeper lesion that grows, proliferates, and reaches a maximum, and then remains at that size without subsequent involution. The lesions are firm, rubbery, warm, with prominent pulsations, and present even with a bruit. At angiography, they are hypervascular, relatively well circumscribed, with rapid filling of venous drainage, secondary to the hypervascularity, but with no true fistulas, and they respond very well to endovascular embolization (Fig. 11.16). In one of our patients, an additional superficial lesion typical of a hemangioma involving the lower lip was also present, which behaved as a typical hemangioma, whereas the deep lesion did not: it increased in size over the first 2 years, stabilized, and was treated by transarterial and intralesional embolization (Fig. 11.14). In lesions that are hypervascular and do not flatten or disappear after embolization, surgery may obtain excellent results (Fig. 11.17). These groups of lesions are special in that clinically they behave as transitional lesions somewhere between hemangioma and malformation. At birth, a telangiectasia is already present, followed by a period of growth or proliferation and at 2–3 years the lesion stabilizes, but fails to involute (Fig. 11.16). These lesions remain high-flow lesions and then behave as malformations of a capillary type.

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Fig. 11.16A–F. Legend see p. 587

▲

Noninvoluting Capillary Hemangiomas

587

Fig. 11.16A–G. Noninvoluting hemangioma (NICH). This girl was born with a reddish telangiectasia (A). B Proliferation was noted within months and persisted unchanged 2 years later. C Mid-arterial angiogram shows a relatively well circumscribed hypervascular tumor blush. Note the prominent venous drainage, without AV fistulization. D Lateral injection of the transverse facial artery, opacifying all but the more anterior portion of the lesion supplied by the facial artery. E Distal ECA and F facial artery after embolization with microparticles in a 50% ethanol suspension. G There was a very fast shrinkage of the deep portion of the lesion after embolization. The cutaneous telangiectasia was treated with laser photocoagulation

Fig. 11.17A, B. A 3-year-old girl with a noninvoluting lesion (A) underwent intralesional Gelfoam powder and ethanol embolization, with initially a good result, recurrence, and then underwent surgical excision (B)

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11.12 Subglottic Hemangiomas A small percentage of head and neck hemangiomas involve the airway, with the subglottic area being the most common site. They become symptomatic relatively early, often in the first 4–8 weeks of life, and usually present with persistent croup-like symptoms and biphasic stridor (Hochman et al. 1999). Approximately 50% of patients with subglottic hemangioma will have an associated cutaneous lesion. The diagnosis is based on the appearance of a vascular lesion in the subglottic area on endoscopy (Sie and Tampakopoulou 2000). Subglottic hemangiomas follow a similar clinical history to other hemangiomas. In this subglottic location, they are constantly or exclusively fed by the inferior thyroidal artery. In spite of their small size and despite the natural history for complete regression, these lesions can cause asphyxia and require emergency therapy to prevent airway obstruction. If life-threatening symptoms occur, they will warrant early treatment. Ablation with the CO2 laser is the preferred method of treatment. Bommel reviewed 26 cases and found associated additional hemangiomas in 60% and one patient had Sturge-Weber syndrome. In 1979, Ohi presented the clinical profile of these lesions (Table 11.2). Corticosteroid therapy is usually the first treatment used. However, 35% did not respond to corticosteroids (Bommel). In total, 60% of the patients required intubation and radioactive phosphorus (450 rads). One child required 2 months of intubation, and only ten cures were observed after one application of phosphorus.As mentioned by Bommel, the therapeutic goal is to gain time since hemangiomas always regress.

In our experience, embolization has proven to be rapidly effective to alleviate the obstructive symptomatology of the hemangioma. In two cases (6- and 7-kg infants), immediate discontinuation of the corticosteroid therapy was achieved and extubation was possible immediately after embolization. One patient required corticosteroid therapy and antibiotics for a few days after a throat infection 4 months after the embolization. In each case, the procedure was easy and expeditious, and only a single artery had to be embolized (the inferior thyroidal artery) with PVA particles (140 mm in size) (Fig. 11.18). As a strategy, we think that each time an infant has to be intubated or corticosteroid therapy needs to be increased or repeated (corticosteroid resistance, corticosteroid dependence), and if CO2 laser fails, embolization should be performed. The present developments in pediatric laryngology and in particularly the introduction of single-stage laryngotracheoplasty (SS-LTR) have proven to be a very good treatment for symptomatic subglottic hemangiomas (Abbeele et al. 1999). Although there is some morbidity with SS-LTR, the authors conclude that open laryngeal surgery remains a reliable and valid method for managing symptomatic subglottic hemangiomas when laser and other methods of therapy have failed. We feel that a properly performed embolization and 3 days’ hospitalization must be balanced against these risks.

Subglottic Hemangiomas

589

Table 11.2. Symptoms of subglottic hemangiomas (Ohi 1979) Patients Total patients with symptoms Stridor Dyspnea Retractions Wheezing Cyanosis Eating problems and weight loss Hoarseness Tachypnea Cardiac arrhythmia Not stated

(n)

(%)

85 72 37 29 16 14 10 8 2 1 19

100 84.7 43.5 34.1 18.8 16.5 11.8 9.4 2.3 1.2 22

Fig. 11.18A, B. A 5-month-old girl with a symptomatic subglottic hemangioma. Steroid therapy and intubation failed to stabilize the symptoms. A Right and B left inferior thyroid angiography prior to embolization of the subglottic hemangioma (arrow). Note the normal blush of the thyroid gland (T). Embolization with particles resolved the dyspnea and laryngeal stridor. The baby was extubated and no further treatment was needed

590

11 Hemangiomas

11.13 Periorbital Hemangiomas Periorbital and upper eyelid hemangiomas may interfere with visual stimulation and amblyopia can occur relatively rapidly, which will require rapid intervention to preserve future vision (Fig. 11.1; see Chap. 12, this volume). Late sequelae of orbital hemangiomas are orbital cavity enlargement, which is well demonstrated on 3D CT studies (Fig. 11.24). In their series of periocular hemangiomas (orbit, eyelid, and ocular adnexa), Haik and colleagues (1979) found a predominance of upper eyelid involvement, with 75% showing orbital signs. Shields et al. (1986), in a series of 250 consecutive orbital biopsy in children younger than 18 years of age, found that hemangiomas accounted for 4% of all orbital lesions. A pale halo, an area of erythema, or a cluster of telangiectatic vessels characterizes the initial presentation of a cutaneous hemangioma a few weeks after birth. This may be confused with the so-called salmon patch (stork bite, angel kiss) that occurs in as many as 40% of newborns and that most often disappears by the end of the 1st year of life. In those children in whom it does not fully disappear, the lesion becomes apparent after exertion or stress and is easily differentiated from other lesions (Pratt 1953). Thompson (1979) considers that blindness will follow 1 week of occlusion of the upper eyelid in infants. Pasyk et al. (1984) could not preserve vision in one of her nine patients with two sessions of steroid treatments, although the hemangioma seemed to respond to treatment. In fact, visual acuity is extremely difficult to assess in infants; therefore, the decision has to be made on clinical grounds. Ophthalmic complications such as astigmatism result from direct globe deformity by an adjacent expanding mass. Treatment in this instance is controversial, because the induced refractive error has been observed to persist beyond the resolution of the occlusive-compressive mass (Robb 1977). Occlusion of the visual axis is a consequence of a rapidly growing mass that causes mechanical ptosis. Strabismus is due to the mechanical effect on an extraocular muscle or its motor nerve. Corneal exposure is secondary to axial globe displacement by an orbital mass. Other potential orbital complications requiring intervention include compressive optic neuropathy and orbital-palpebral bony asymmetry (Garza et al. 2001). Corticosteroids have become the treatment of choice for lesions compromising vision, with the fastest response produced by intralesional injections. In an effort to overcome the systemic side effects or the risk of intralesional injections, clobetasol cream, a potent topical steroid, was used in two separate studies (Elsas and Lewis 1994; Cruz et al. 1995). The results revealed a measurable decrease in the size of the lesions that was, nonetheless, insufficient to prevent amblyogenic astigmatism.

Periorbital Hemangiomas

591

Fig. 11.19A, B. Eyelid hemangioma treated early with intralesional steroid injections, resulting in normal vision

Kushner (1982) first reported the use of intralesional steroids for periocular hemangiomas. He recommended a combination of betamethasone and triamcinolone to provide both rapid action (betamethasone) and a long-term effect (triamcinolone). Currently, the most widely used combination is 3–5 mg/kg bw triamcinolone and 0.5–1.0 mg/kg bw betamethasone. The injections should be given separately via different syringes into the bulk of the lesion, to prevent the formation of solid precipitates (Kushner 1985). The effects are usually dramatic (Fig. 11.19), although sometimes additional injections are required. It is interesting that Zadok and associates (1996) reported regression of a distant hemangioma after local steroid injection. Current consensus suggests that the steroid effect is purely systemic, with no specific local effect based on regional injection. Reported complications vary from growth retardation with adrenal suppression (Weiss 1989) to bilateral retinal embolization (Ruttum et al. 1993). Other less dramatic but significant complications are subcutaneous linear fat atrophy at the site of injection (Townshend and Buckley 1990), eyelid depigmentation (Cogen and Elsas 1989), and necrosis (Sutula and Glover 1987). The effect of interferon on vision-threatening hemangiomas was studied by Hastings et al. (1997). A dramatic reduction in hemangioma volume, allowing eyelid opening, was seen after 6 weeks of treatment. However, five of the 15 children enrolled were reported to have residual amblyopia. From this observation, it appears that interferon is highly

592

11 Hemangiomas

effective but unfortunately too slow in clearing the visual axis to prevent amblyopia in one-third of cases. Under certain favorable circumstances, particularly with upper lateral eyelid locations, embolization with particles can be very efficient in reducing size, mostly if complete or nearly complete embolization of the nidus can be achieved (Fig. 11.24). At present, however, a direct intralesional steroid is the preferred treatment. Embolization and/or surgical excision may be an appropriate treatment for eyelid hemangioma not responsive to steroids (Deans et al. 1992). The capacity to safely catheterize and embolize distally the ophthalmic artery branches beyond the retinal supply offers new possibilities (Alvarez et al. 1990).

11.14 Oral Hemangiomas Oral hemangiomas rarely involve the bone, but may produce progressive osseous deformity and spontaneous hemorrhage; surgical treatment may become necessary in combination with embolization (Fig. 11.20). Softtissue hemangiomas of the cheek are usually well tolerated; embolization can sometimes be used to speed up involution and to avoid any impact on teeth eruption (Fig. 11.21), mandibular growth, or psychological development. Tongue capillary hemangiomas are also rare in this age group (Fig. 11.22).

11.15 Salivary Gland Hemangioma Parotid gland hemangiomas are the most common type of tumor of the parotid gland in children (Wisnicki 1984). The facial nerve itself is usually not involved, but facial asymmetry may be noted following rapid growth of the lesion. These hemangiomas have the same potential for involution as other proliferative lesions of the same type. However, other vascular masses in the same location, which become manifest later in young adults (capillary vascular malformations), do not regress and may require invasive treatment (Hidano and Nakajima 1972). Hemangiomas may be bilateral in this location (Fig. 11.7). Skin involvement can be treated by limited superficial surgical resection respecting the VIIth nerve and aiming to prepare easily correctable sequelae after regression, while obtaining a good cosmetic result by the decompressing effect of this type of pre-auricular skin resection.

Salivary Gland Hemangioma

593

Fig. 11.20A–D. A 6-month-old child presenting with a (potentially involuting) hemangioma of the mandible. A CT showed the intramandibular lesion. B Following embolization, intraosseous curettage was achieved C with preservation of the mandibular cortex. Pinna indicated for orientation (open arrow). D Follow-up examination 8 months later showed normalization of mandibular size and normal tooth eruption (arrow) from the segment of the mandible previously involved with the hemangioma

594

11 Hemangiomas

Fig. 11.21. A Capillary hemangioma of the cheek in a 6-month-old child. A–C Angiographic appearance of the facial artery. Internal maxillary arteries. Note the sharp margin between the two compartments of the lesion (arrowheads) and the rapid venous shunting (curved arrow). D, E Follow-up angiograms 1 year later when the mass was compromising tooth eruption. Note the intralesional changes associated with the disappearance of the arteriovenous shunts within the tumor; at this point periodic swelling led us to embolize with particles. F, G see p. 595l

Bone Hemangioma

595

Fig. 11.21. (continued) F, G Follow-up angiogram 1 year later shows disappearance of the capillary blush. This angiographic improvement correlates with the clinical decrease of the mass. This result was still stable after 5 years follow-up, and there are no tooth eruption problems

11.16 Bone Hemangioma Bone hemangiomas are extremely rare in the pediatric population (Fig. 11.20).Vascular tumors of the maxillo-facial bones in adults account for less than 1% of all osseous neoplasms (Dorfman 1971). In the jaw, they behave like slowly growing benign tumors and usually occur in females (female:male ratio 2:1) in the second decade of life (two-thirds of the patients reported by Batsakis 1979). Bony hemangioma are usually of the capillary type and are highly vascularized, although some may not be visualized during angiographic studies (cavernous or fibrous type (Fig. 11.23). Hemangio-pericytomas and malignant vascular tumors are also extremely rare in the facial skeleton and usually result from the bony invasion of adjacent soft tissue lesions. In each case, there are few specific clinical or radiological findings to confirm the nature of these rare lesions.

596

11 Hemangiomas

Fig. 11.22A, B. Tongue hemangioma. Angiogram of the lingual artery shows the tumor blush with no fistulas prior to embolization

Bone Hemangioma Fig. 11.23A–C. A 3-year-old boy with ptosis and VIth nerve palsy. Surgery was performed and incomplete. The diagnosis of bone hemangioma was made. Four years later, headaches and extraocular nerve palsy led to angiography. B, C Middle meningeal supply with typical aspect of cavernous type of epidural hemangioma. D, E A similar case with intraosseous proliferation (D) and angiographic appearance (E)

597

598

11 Hemangiomas

11.17 Associated Anomalies Hemangiomas can be associated with midline anomalies, including supra-abdominal, mid-abdominal raphe, cleft sternum, sacral and genito-urinary defects, spinal dysraphism, and Dandy-Walker cysts (see Chap. 12, this volume). In addition, vascular anomalies have been described in patients with hemangioma of the head and neck and include right-sided aortic arch, coarctation of the aorta, and abnormal aortic arch branching. Additional intracranial arterial anomalies are seen in large lesions such as persistent trigeminal artery, unilateral or bilateral internal carotid agenesis, or absent vertebral vessels (Burns et al. 1991; Goh and Lo 1993; Lasjaunias and Berenstein 1987; Mizuno et al. 1982; Murotani and Hiramoto 1985; Pascual-Castroviejo 1985; Schneeweiss et al. 1982; Bhattacharya et al. 2003). Many of these malformations or anomalies are associated with proliferative hemangiomas. They are a remarkable illustration of the intricated issues related to proliferation and malformation in terms of angiogenesis. Associated intradural hemangiomas can be seen. Their progression parallels that of facial location. The PHACE syndrome corresponds to these unusual associations, which are often underestimated at the time of diagnosis (Fig. 11.24).

11.18 Psychological Impact The psychological impact of cosmetic impairment in infants is still difficult to assess. Some slowly regressive hemangiomas in young children who enter school may sometimes require early treatment in order to accomplish a more rapid improvement by embolization or surgery. Lip involvement is sometimes the source of such problems. Parents often find it difficult to believe that spontaneous regression will occur in large lesions (Figs. 11.3, 11.25); we recommend that photographs be used to illustrate such regression in order to help them share the therapeutic decision and to accept the child’s problem as transient. Plastic surgery in the pediatric maxillo-facial population is recent; however, analysis of the cosmetic suffering in a child varies according to the child’s age. Before the age of 4 years, most problems are often related to the parents, as the child cannot truly differentiate between his or her appearance in relation to the malformation. Between the ages of 5 and 8, children can be placed in front of a mirror and recognize their image, but seldom point to the major area of cosmetic concern. On the other hand, parents looking at their

▲

Fig. 11.24A–F. A 3-month-old girl presenting with a capillary hemangioma of the eyelid and parotid region. A Due to the eye occlusion, and to prevent amblyopia, angiography and embolization with PVA particles were carried out. B Late phase of the distal external carotid artery angiogram. Note the multilobulated capillary blush and the venous shunt draining into the ophthalmic vein. C Carotid angiogram shows persistence of the ventral embryonic ophthalmic artery. Right-sided aorta (D). Note the late orbit enlargement at the age of 8 years (E). Follow-up picture at 12 years of age following surgical reconstruction (F)

Psychological Impact

599

600

11 Hemangiomas

Fig. 11.25A–D. Highly proliferative hemangioma at 1 month (A) and at 6 months (B). Regression was then noted. Aspect at 2 years (C) and 6 years (D) without treatment

children in the mirror find the situation worse than when they look at them directly, as they see a reverse image that is both familiar and yet different, unusual and strange. It is difficult to ask children of that age if they would like to be treated at this moment or when they are older. It is only around 8–10 years of age that the notion of time is sufficiently developed that it can be used. School landmarks can also be used if the child has

Psychological Impact

601

Fig. 11.26A–D. Highly proliferative hemangioma at 1 month (A), at 5 months (B), and at 9 months (C, D). E, F see p. 602

been at school long enough. After 11–15 years of age, skin scarring is often significant; surgeons tend to avoid surgery in this age group or use hidden approaches (intraoral or in-hair locations) (M.P. Vasquez 1995, personal communication). With the development of increased expertise, Waner and co-workers (1999) have advocated early intervention with surgery, laser, intralesional laser and embolization in selected cases, even in the proliferative stage, to prevent disfiguration or subsequent mutilating interventions. Some proliferative activities are beyond what one would consider as benign (Fig. 11.26).

602

11 Hemangiomas

Fig. 11.26E,F. (continued) CT aspect at 9 months (E, F)

11.19 Kaposiform Hemangioendothelioma and Consumption Coagulopathy, the Kasabach-Merritt Syndrome Phenomena A consumption coagulopathy, characterized by thrombocytopenia originally believed to be a capillary hemangioma, was first described by Kasabach and Meritt in 1940. Blix and Aas (1961) and Larsen et al. (1987) described associated fibrinopenia and accelerated fibrinolytic activity. In 1997, Enjolras’s group (Enjolras et al. 1997) and the Sarker team reported that the primary lesion is a rare, locally aggressive vascular tumor kaposiform hemangioendothelioma or a tufted angioma that is potentially lethal in up to 30% of patients (Esterly 1996). The tumors have a predilection for the upper trunk, pelvis, retroperitoneum, thigh, and extremities, but can be seen in the head and neck. On inspection, they are warm, firm indurated purpuric lesions (Figs. 11.3, 11.27, 11.28). There is no gender dominance. These tumors tend to proliferate longer than typical hemangiomas. Coagulation studies in patients with this disease frequently reveal profound thrombocytopenia, microangiopathic hemolytic anemia, and a profile similar to that of disseminated intravascular coagulation (DIC; Inceman and Tangun 1969; Adams 2001).

Kaposiform Hemangioendothelioma and Consumption Coagulopathy

603

Fig. 11.27. Kaposiform hemangioendothelioma of the chest wall with severe KasabachMeritt phenomena, treated by embolization

131I-fibrinogen

or 51Cr-labeled platelets injected in some of these patients (Straub et al. 1972; Brizel and Raccuglia 1965; Warrel and Sanford 1985) have been reported to accumulate within the tumor and indicate localized clotting and fibrinolysis within the lesion rather than disseminated intravascular coagulation, secondary to localized consumption of platelets and clotting factors within the tumor. The process that is responsible for the coagulopathy is still not clear; various theories have been put forward, including a deficiency of the production of prostacyclin by the endothelial cells and adhesion of thrombin to these cells. Alternatively, neoplastic endothelium within the lesion may initiate contact activation of the intrinsic coagulation pathway (Awbrey et al. 1979). Interaction between thrombo-modulin and protein C (Owen 1981) or secretion of plasminogen activator might allow the formation of platelet fibrin thrombi (Loskutoff and Edgington 1977). Stasis of blood in the lesion may lead to an accumulation of activated coagulation factors and increased local fibrinolysis. Coagulation in the lesion might then become auto-catalytic, resulting in thrombocytopenia and depletion of coagulation factors.

The syndrome usually occurs in children. In some patients, the coagulopathy is mild and does not affect survival, but in others it is more severe, and in the absence of treatment may result in death.

604

11 Hemangiomas

Fig. 11.28A–D. Kaposiform hemangioendothelioma of the neck and upper chest wall with severe Kasabach-Meritt syndrome, responding to Vincristine. Note the rapid spontaneous progression (A) in 4 days (B) following vincristine rapid involution, 3 days later (C), and 10 days after the previous picture (D)

Kaposiform Hemangioendothelioma and Consumption Coagulopathy

605

The imaging findings of hemangioendothelioma in patients with Kasabach–Merritt syndrome may be confusing. These lesions tend to appear as diffuse, infiltrating lesions, often without a discrete mass effect. Dilated feeding and draining vessels are, however, usually visible. Bone erosion can be seen in infiltrative lesions with KMS, suggesting a paraneoplastic coagulopathy, while in some of these forms pre-biopsy embolization has been proposed. In other cases, biopsy is not needed and is dangerous. In cases of severe thrombocytopenia, transfusions may actually aggravate the coagulopathy, and even have the tumor grow (Adams 2001). Complete eradication of the hemangioma by surgery or radiation has been reported to eliminate the coagulopathy (Shim 1969; Hill 1962). Neidhart and Roach in 1982 and Warrell and Sandford in 1985 reported the control of this coagulopathy with aminocaproic acid alone or in conjunction with cryoprecipitate in extensive nonsurgical lesions. Although successful in controlling the consumption coagulopathy, the treatment required very high doses over a long period of time and has been associated with episodes of acute thrombosis at sites distant from the tumor, which required temporary suspension of treatment. In addition, minor paresthesias of the lower extremities were noted in Warrell’s patients (Warrell and Sandford 1985). It is agreed that the first line of treatment is high-dose corticosteroids; interferon has not been effective. An antifibrinolytic agent such as aminocaproic acid alone, or in combination with antiplatelet agents such as aspirin or dipyridamidole, have been tried with variable results. If these regimens do not respond the next level is chemotherapeutic regimes with agents such as vincristine and actinomycin. Radiation treatment has been used by Neidhart and Roach (1982) and Warrell and Sandford (1985) (Fig. 11.13), but we have serious reservations as to its effectiveness and its safety when used in infants. In our experience, tumor resection is the best treatment (Shim 1969; Hill 1962). However, the coagulopathy makes surgery hazardous or impossible in infants and children even in circumscribed lesions.Aggressive embolization under those circumstances has proven to be effective in raising platelet count (at least temporarily), reducing vascularity within the tumor, and permitting surgery in selected cases (Fig. 11.13). Embolization in diffuse nonsurgical lesions has a synergistic effect with medical therapy (Figs. 11.15, 11.29). Embolization is best performed with liquid agents such as transarterial acrylic (NBCA) alone or supplemented with direct intralesional embolization also with NBCA (Figs. 11.13, 11.15) or ethanol (Fig. 11.15).

606

11 Hemangiomas

Fig. 11.29. A, B A 4-month-old baby presenting with an infiltrative hemangioendothelioma of the right cervical region with severe Kasabach-Meritt syndrome. Note the infiltrative nature of the mass. The CT is characteristic. C The vascularization is tumor blush-like

12 PHACES

12.1

Introduction 607

12.2 12.2.1 12.2.2 12.2.3 12.2.4 12.2.5 12.2.6 12.2.7

Clinical Aspects 609 Posterior Fossa Abnormalities 611 Hemangiomas 618 Arterial Anomalies 622 Coarctation and Congenital Heart Disease 623 Eye Abnormalities 627 Sternal Cleft 627 Stenotic Arterial Disease 627

12.3

PHACES, a Congenital Malformation and a Proliferative Disease 631

12.1 Introduction The association of cervicofacial hemangiomas with vascular and nonvascular intracranial malformations was first recognized by Pascual-Castroviejo in 1978, and the alternative name of cutaneous hemangioma-vascular complex syndrome was subsequently proposed (Pascual-Castroviejo et al. 1996). In 1996, Frieden et al. proposed the acronym “PHACE” for a neurocutaneous syndrome, of which the major features were Posterior fossa malformations, Hemangiomas, Arterial anomalies, Coarctation of the aorta and cardiac defects, and Eye abnormalities. A growing list of complex syndromes link disorders of the brain, meninges, or cerebral vessels with cutaneous and craniofacial lesions. These so-called neurocutaneous syndromes have been a source of fascination to a wide range of specialties, from dermatology to the clinical neurosciences to pediatrics and genetics. Some of these conditions are further associated with congenital heart disease. Advances in developmental biology over the last quarter of the twentieth century have suggested the neural crest as a common link between the various components of many of these syndromes, similar to the CAMS (Bhattacharya et al. 2001) (see Chap. 6, this volume), SAMS (Matsumaru et al. 1999), and CVMS (Ramli et al. 2003; Luo et al. 2003). Hemangiomas are recognized as the most common benign tumors of infancy (see Chap. 11, this volume) and seem to be the unifying feature in the spectrum of lesions constituting the PHACE syndrome. Many previous reports have acknowledged the association of cervicofacial hemangiomas with vascular anomalies and congenital heart disease (Pascual-Castroviejo 1978; Mizuno et al. 1982), and hemangiomas have also been associated with Dandy-Walker syndrome (Hirsch 1984) (Tables 12.1, 12.2).

608

12 PHACES

Table 12.1. Facial anomalies associated with Dandy-Walker syndrome Authors

Facial angiomas M F

Cleft palates

Ocular malformations

Macroglossia

Facial dysmorphia

Hart et al. 1972 March and Chalkey 1974 Chemke et al. 1975

0 0 0

0 0 0

2 0 0

0 0 0

0 0 0

Carmel et al. 1977 Stoeter and Marquardt 1978 Pascual-Castroviejo 1978 Bruyere et al. 1980

1 1 1 0

0 0 0 0

0 0 0 1

0 Scleroma Cataract, coloboma, retinal dysgenesis Microphthalmia 0 0 0

1 0 0 0

0

Tal et al. 1980 Sawaya and McLaurin 1981 Hirsch et al. 1984

0 3 3

0 1 1

2 2 0

0 0 Coloboma, embryotoxon

Atresia of the ear

0 0 0

0

Table 12.2. Cardiovascular malformations associated with Dandy-Walker syndrome Authors

Septal defect

Ductus arteriosus

Cerebral artery malformations

Coarctation of aorta

Dextrocardia

Molland and Purcell 1975 Huong et al. 1975 Pascual-Castroviejo 1978 Bruyere et al. 1980 Tal et al. 1981 Olson et al. 1981 Sawaya and McLaurin 1981 Hirsch et al. 1984

0 3 0 1 1 2 1 0

0 0 0 1 0 0 1 1

0 0 1 0 0 0 0 0

1 0 0 0 0 0 0 0

0 0 0 0 0 0 0 1

Burrows et al. (1998) further noted a stenotic disorder of the intracranial arteries resembling moyamoya disease in some of their infants, and the sometimes associated sternal cleft feature has prompted the appellation “PHACES syndrome.” We believe this disorder constitutes a spectrum of phenotypic expression (Rossi et al. 2001; Bhattacharya et al. 2004). The neural crest has been implicated in the pathogenesis of the PHACES syndrome (Goh 1993), although the involvement of the cerebellum, which is not a neural crest structure, has not been clarified (Rossi et al. 2001). It is important to recall, however, the reciprocal influences of the neural crest and adjacent cephalic mesoderm (which are similarly regionalized) and the trophic influence of the meninges on underlying neural structures (Etchevers et al. 1999, 2001) (Fig. 12.1).

Clinical Aspects

609

Fig. 12.1A, B. Neural crest derivative at the aorta (A) and vascular mapping in the cephalic region (B) in birds. (From Etchevers 2001)

12.2 Clinical Aspects As with any complex syndrome that has many associated lesions and incomplete phenotypic expressions, knowing exactly which patients to include or exclude can be problematic. While diagnostic criteria can assist in identifying patients, unfortunately the criteria have yet to be defined for the PHACES syndrome. PHACES is usually considered to be a neurocutaneous syndrome or phakomatosis but with uncommonly protean manifestations. All previous studies have stressed the phenotypic heterogeneity of the syndrome and absence of one or more components (Metry et al. 2001; Rossi et al. 2001; Bhattacharya et al. 2004) (Table 12.3). It involves mostly Caucasian infant females and depending on the areas clinically involved, the children consult very different specialists for diagnosis. The clinical picture and progression depend on the completeness of the spectrum as well as the response to medical and surgical treatments and corrections. The progression of the occlusive arterial disease is not known; its prognosis is likely to be reserved if one considers the involvement of the distal cortical arteries and external carotid branches (although these are less important) in the most severe forms, thus limiting the possibilities of distal revascularization.

610

12 PHACES

Table 12.3. Spectrum of lesions in PHACES syndrome (Bhattacharya 2004) Post. fossa Dandy-Walker

CB hypoplasia

CB cortical dysgenesis Arachnoid cyst

Hemangioma Large plaquelike multiple dermatoma Orbital extension common Lateralized Bilateral

Small focal

Arterial anomaly

Coarctation/ heart lesion

ICA agenesis/ hypoplasia Segmental agenesis ICA Prox origin of ICA Dysplastic fusiform MCA/ICA/ ECA aneurysms Aberrant origin MCA Dysplastic ophthalmic artery VA agenesis/ hypoplasia Aberrant SCA Trigeminal artery Pro-atlantal artery

Eye lesion

Sternal lesion

Stenotic arterial

Coarct

Choroidal HM

Sternal clefting

Occlusive intracranial artery

Arch atresia

Cryptophthalmos

Supra-abdo raphe

Subarachnoid and cortical

Right-sided arch Patent ductus

Colobomas Posterior embryotoxon

Tricuspid atresia VSD

Microphthalmos Strabismus

Partial anomaly venous return Tetralogy of Fallot

Optic nerve hypoplasia

Collateral vessels Infarcts

Progressive disease Occlusive extracranial artery

Glaucoma

CB, cerebellar; A, artery; ICA, internal carotid artery; MCA, middle cerebral artery; ECA, external carotid artery; VA, vertebral artery; SCA, subclavian artery; VSD, ventricular septal defect; HM, hemangioma; Rt, right.

Bhattacharya et al. (2004) reviewed six patients with definite PHACES syndrome (Table 12.4). Two additional patients were included, as they manifested a partial expression of PHACES. In all six of these, the lesion was lateralized, usually on the left side, and involved the maxillofacial region. In two patients, there was parotid or oral involvement. Metry et al. (2001) reviewed 130 cases and stated that in 43% of cases the lesions were on the left side, 29% on the right, and in 23% of cases the lesions were bilateral.

Posterior Fossa Abnormalities

611

Table 12.4. Clinical and imaging features of six patients with definite PHACES syndrome and two further patients (7 and 8) with possible partial phenotypic expression (Bhattacharya 2004) n° Age/ sex

Clinical features

Postfossa

Hemangioma

Arterial anomalies

Coarct- Eye ation

Stenotic disease

Imaging

1 2

4 years/F 3 months/M

– HM

+ –

A, CT A, MRI

ICA, TGA, –

– +

HM HM

+ –

A, MRI A

5

3 months/M

+

HM

–

CT

9m/F

DW, HM DW

Right SCA

6

Left orbit mass back Left facial mass

–

–

HM

–

MRI

7 8

14 years/F 14 years/M

H/a Aphasia, PND, hemiplegia

– –

Max Face, lip, left orbit Eyelid Left face, orbit, parotid Left orbit, parotid, back Left max, lip, eyelid – –

+ –

6 months/F 1 month/F

– DW, left CB – –

VBA, ICA, ECA ICA, ECA, SpA

3 4

H/a PND Left facial mass, seizure PND, chorea, h/a Left facial mass

VA, ICA, PICA ICA, MCA ans

– –

– ¥

+ +

A, MRI A

H/a, headache; PND, progressive neurological deficit; Max, maxillary; VBA, vertebrobasilar arteries; SpA, spinal artery; TGA, trigeminal artery; SCA, subclavian artery; ans, aneurysms; CM, cerebellar malformation; DW, Dandy-Walker; HM, hemangioma; A, arteriography.

Unlike in CAMS 3 (Wong et al. 2003) or CVMS (Ramli et al. 2003), there was no recognizable association between cerebellar abnormalities and lower face lesions. Orbital involvement (eyelid or intraorbital extension) by the hemangioma was encountered in five out of six patients, while no other eye lesions were described. Cardiac and associated abnormalities were encountered in four patients: coarctation in three and a right-sided aortic arch in one. Posterior fossa malformations were seen in three out of six. Two out of six patients had occlusive arterial disease, with some presenting at rather older ages: up to 4 years in the main group. If patients 7 and 8 do indeed have a partial PHACES syndrome, the age range for occlusive disease would extend to 14 years.

12.2.1 Posterior Fossa Abnormalities

Developmental abnormalities of the cerebellum ranging from classic Dandy-Walker (DW) malformations to cerebellar hypoplasia and arachnoid cysts or cortical dysgenesis have been associated with cutaneous hemangiomas in many reports (Table 12.1; Figs. 12.2, 12.3, 12.5, 12.6, 12.8). In 1996, Frieden et al. presented two new patients with PHACES syndrome and reviewed findings in 41 previous cases. Posterior fossa malformations were present in 74% of them. Other series have found posterior fossa abnormalities in closer to 50%: Burrows et al. (1998) reported cerebellar abnormalities in three of eight patients while Pascual-Castroviejo found these abnormalities in eight of 17 patients (Pascual-Castro-

612

12 PHACES

Fig. 12.2A–C. An infant girl, 9 months of age, presented with A large, left-sided facial hemangioma associated with B, C a Dandy-Walker cyst. T2-weighted MRI. The left cerebellar hemisphere is more hypoplastic than the right. Note left frontal hemangioma. (Courtesy of S. Pongpech)

viejo et al. 1996). In Bhattacharya’s series (Bhattacharya et al. 2004), three out of six had evidence of cerebellar abnormalities. Approximately 10% of cases in reported series of Dandy-Walker malformation are associated with capillary hemangiomas. It is notable that in the Dandy-Walker malformation, overall there is no significant gender difference (Hirsch et al. 1984; Golden et al. 1997). In the subgroup of DW patients with hemangiomas, however, there is a strong female predominance, similar to that encountered in PHACES syndrome (up to 8:1) (Hirsch et al. 1984). This raises the intriguing possibility that up to 10% of all patients with DW malformation may actually have unrecognized PHACES syndrome. It also demonstrates an unexplained female dominance in these early active benign proliferative diseases (hemangiomas, PHACES, and DW with he-

Posterior Fossa Abnormalities

Fig. 12.3A–C. A 3-month-old girl (A) with orbital hemangioma on the left; contrast-enhanced CT. B Left frontal hemangioma with intraorbital extension and ipsilateral cerebellar hemisphere hypoplasia (C). Note the left cerebellopontine angle enhancing mass, demonstrating an intracranial hemangioma

613

614

12 PHACES

Fig. 12.4A–C. Young infant with PHACE syndrome (A) with bilateral carotid agenesis (B, C). The vertebral artery is the only supply to the intracranial brain. Note the basilar artery origin of the ophthalmic artery (arrowheads). Posterior communicating arteries (arrow, double arrow)

Posterior Fossa Abnormalities

615

Fig. 12.5A–D. A 3-month-old boy presented with capillary hemangiomas of the face and one convulsion episode. MRIs (A–C) demonstrate the hemangiomas as well as the posterior fossa malformation. Angiography disclosed several variations and abnormalities (D): cervical ICA agenesis, intratympanic course, stapedial artery persistence, and fusiform intrapetrous aneurysm

616

12 PHACES

Fig. 12.6A–F. Legend see p. 617

▲

Posterior Fossa Abnormalities

617

Fig. 12.6A–L. In a 3-month-old girl with facial hemangioma (A), right-sided aorta (B), MRI (C, D) demonstrates the extent of the lesion in the face as well as the associated posterior fossa malformation. On the angiogram, there is dolichocervical ICA (E), cervical and petrous agenesis of the left ICA, and dolichohypoglossal persistence (F, G). Three years later, the hemangiomas have partially but significantly regressed (H). Four years later, the brain is normal, as is the child clinically (I). Angiogram shows progression although asymptomatic stenoses both on the right ICA (J, K) and on the left ICA (and actually the MCA) (L). Some degree of stenosis is noted on the hypoglossal artery. K,L see p. 618

618

12 PHACES

Fig. 12.6K,L. Legend see p. 617

mangiomas), even though they may correspond to the same spectrum entity. This is in contrast with most other complex vascular diseases that are less proliferative or nonproliferative in early childhood, which tend to show a male dominance (arterial aneurysms, DSM, VGAM). One of our cases also had an agenesis of the falx (Figs. 12.8, 9.7). The causes of the Dandy-Walker complex are poorly understood, with several competing theories offering possible explanations (Golden et al. 1987) and a variety of timings suggested for the provoking insult. In one of Frieden’s cases, ultrasound examination at 12 weeks’ gestation demonstrated the posterior fossa cyst, confirming the development of this component of the syndrome before the end of the first trimester. The cerebellar vermis is known to develop between weeks 5 and 15 (Altman et al. 1992), which would be consistent with an earlier onset of the syndrome. The first trimester (approximately 4th–12th weeks) is probably the most likely time for development of posterior fossa cystic malformations.Yet at least initially, normal cerebellar development is suggested in most instances by the normal bony posterior fossa (Figs. 12.2, 12.8), as cerebellar growth will promote posterior fossa bone growth (in particular the occipital squamous portions). Secondary cerebellar dystrophic alterations may then follow focal hydrovenous disorders related to (malformative) meningeal dysfunction (early melting-brain syndrome or absence of signal with abnormal apoptotic response; see Chap. 2, this volume) (Etchevers et al. 1999).

12.2.2 Hemangiomas

Hemangiomas are benign tumors demonstrating unsuppressed proliferation of capillary endothelial cells and typically develop in the neonatal period (see Chap. 11, this volume). They are common lesions occurring in up to 12% of Caucasian infants and rarely have any associated systemic

Hemangiomas

Fig. 12.7A–F. Legend see p. 620

619

620

12 PHACES

▲

Fig. 12.7A–K. A 6-month-old girl (A) presented with right-sided fronto-orbital hemangioma and progressive neurological deficit, chorea, and headaches. Imaging findings were 50% stenosis of the left supraclinoid ICA, occlusion of the left anterior cerebral artery (ACA),A1 segment (B, C), occlusion of the right ICA bifurcation (D, E), and occlusion of the distal basilar artery (F, G). An extensive network of collateral vessels was noted. Several arterial anomalies were identified. There was a segmental agenesis of the right ICA and a right persisting trigeminal artery. The external carotid system via the skull base contributed to the supply of the ACA territories bilaterally (H–K). J–K. see p. 621

Hemangiomas

621

Fig. 12.7J,K. Legend see p. 620

abnormalities. Pathologically, the hemangiomas in PHACES syndrome are no different from sporadic cases. Strikingly, in PHACES-associated hemangiomas, there is a 9:1 female:male ratio as compared to the 4:1 sex ratio for sporadic cases. Preponderance of hemangiomas among female patients was observed to be more pronounced for diffuse hemangiomas than for focal hemangiomas in this study (by a factor of nearly 2) (Waner et al. 2003). The hemangiomas are typically bulky, plaque-like lesions involving several cervicofacial segments, but without respecting their boundaries (Bhattacharya et al. 2001; Wong et al. 2003; Ramli et al. 2003; Luo et al. 2003). Waner et al. (2003), on the other hand, noted that all of the focal lesions in his series of non-PHACEs facial hemangiomas mapped to regions in close proximity to lines of fusion between mesenchymal growth centers or between the latter and facial ectoderm (see Fig. 6.16). Very small cutaneous hemangiomas have been described (Rossi et al. 2001); hence the cutaneous manifestations could be absent or could regress spontaneously without ever having been recognized or reported. They can also be associated with intracranial subarachnoid locations (Rossi et al. 2001). They will then be located on the same side and show parallel changes in size, and the progression of both is most often benign, requiring no specific treatment.(Fig. 12.3).

622

12 PHACES

Children with proliferating hemangiomas (similar to moyamoya disease) are known to have raised levels of several vascular growth factors, including vascular endothelial growth factor (VEGF) and basic fibroblast growth factor (bFGF) (Takahashi et al. 1994). In vitro studies show that bFgF stimulates endothelial cell hyperplasia and proliferation of vascular smooth muscle cells. Burrow et al. (1998) speculated that effects of these vascular growth factors could link the hemangiomas with the arterial occlusive disease (see Chap. 11, this volume).

12.2.3 Arterial Anomalies

The variety and extent of the vascular anomalies associated with this syndrome are remarkable (Figs. 12.4–12.8, 11.24.). Pascual-Castroviejo et al. (1996) described two patterns of abnormalities associated with facial hemangiomas: 1. Persistent embryonic arteries, e.g., trigeminal artery (Fig. 12.7), which is ipsilateral to the hemangioma, to which we can add hypoglossal (Fig. 12.6), pro-atlantal (Fig. 12.8), stapedial (Fig. 12.5), and ventral ophthalmic (Fig. 11.23). 2. Agenesis of major arteries, e.g., internal carotid or vertebral arteries (Figs. 12.4–12.6, 12.8). It is equally remarkable that these variations are all arterial. There are no venous malformations or dural vascular lesions, and no arteriovenous shunting has been identified in the PHACES syndrome. AVMs are believed to be lesions of venous origin (Lasjaunias and Berenstein 1997) and this further supports the notion that the vascular component (target) of the syndrome is purely arterial and therefore likely to be associated with angiogenic activities (Chaps. 2 and 6, this volume). The presence of arterial aneurysms further supports this speculation (Figs. 12.5, 12.8). The question of the timing of the causative trigger of this syndrome has not been answered. The trigeminal artery develops at 3.5 weeks and its involution accompanies the formation of the basilar artery at between 5 and 5.5 weeks. Therefore, one would expect an event causing persistence of this vessel to occur before about 5 weeks. The internal carotid artery (of which there are also frequently anomalies in PHACES) develops around 3.5 weeks. The carotid and facial vasculature develop jointly from cephalic mesoderm and neural crest, although the spinal vasculature develops from the mesoderm exclusively; the vertebrobasilar system is likely to be mostly mesodermal in origin, with little or no neural crest contribution (Wong 2003). The vertebrobasilar system in avian species receives no contribution from the neural crest (Etchevers et al. 2001), yet the posterior fossa supply is ensured by the posterior division of the ICA (see Vol. 1) and the occipital artery (the remnant of the proatlantal artery). The posterior fossa vascularization probably shares some of the carotids’ embryonic neural crest components.

Coarctation and Congenital Heart Disease

623

The differences in vessel wall vulnerability and involvement in various syndromes (moyamoya, CVMS, and CAMS) probably account for this limited contribution of the neural crest to the vertebrobasilar system in humans. Persistence of the branchial arteries and the absence of development of the internal carotid and/or vertebral arteries is not pathological by itself. According to Kier (1974), transitory fetal vessels such as the trigeminal artery appear within the first 8 weeks of fetal life and last no longer than 7–10 days. The vascular patterning follows sequential signaling to program, according to the phylogenetic options, resulting in the normal dispositions in humans. This development requires both proliferation and apoptotic cascades, as expressed in fusion and regression processes of multiple arterial channels in the head and neck region (see Vol. 1, Chap. 4). Lack of correct information (or information at the wrong moment) will lead to inappropriate regressions and peculiar variations. It remains a mystery as to why the arterial system should be so vulnerable in the PHACE syndrome and with such an early impact, while, conversely, the underlying abnormalities appear to be the venous capillaries and veins in CAMS and CVMS, respectively (see Chaps. 6 and 8, this volume). In the mirror type of aneurysms (Campos 1998), similar to familial aneurysms (as well as nonfamilial aneurysms), associated persistence of embryonic vessels is often noted, but rarely is there evidence of arterial agenesis (Mazighi 2002, see Vol. 2). In contrast to the arterial system, there are no known embryonic venous pathways, but while DVAs are not an embryonic pattern per se, they are likely to stem from the same time marker for venous lesions as the arterial variations do for aneurysms or the PHACES syndrome. The moment when a vessel develops is not a firm time window of vulnerability to create a lesion, but it may mark a progressive shift or delay in the sequence of signaling prolonging the system’s exposure to triggers and therefore to future disease(s). A distinction should be made between a persistent embryonic artery, an agenetic carotid segment, a regressed vertebral artery, and a progressive occlusion of cervical or intradural vessels, as they all correspond to very different processes and have different time implications (see Vol. 1, Chap. 5). They should therefore not be listed together and be credited as a single event.

12.2.4 Coarctation and Congenital Heart Disease

Schneeweiss et al. in 1982 described the association between aortic coarctation (Fig. 12.8) and facial hemangiomas. Among 68 children with coarctation, he found four with cutaneous hemangiomas. This occurrence of cardiac disease in conjunction with facial lesions raises the possibility of involvement of the neural crest in the PHACE syndrome (Fig. 12.1). Certainly, lower rhombencephalic crest cells contribute to the

624

12 PHACES

▲

Fig. 12.8A–J. Girl presenting with a left-sided hemangioma soon after birth (A). In addition, an aortic coarctation (B), posterior fossa malformation (C), and sternal agenesis were noted (D). At 4 years of age, she developed headaches and a progressive neurocognitive deficit. At 11 years, angiography revealed occlusion of the right internal carotid artery (ICA) bifurcation and narrowing of the left ICA. Moyamoya-type collateral vessels were found in the basal ganglia regions bilaterally and there was further supply to the brain from acquired transdural collaterals (E, F). Worsening of symptoms prompted a new MR (G, H) and angiographic evaluation. In addition to these acquired lesions, the left ICA and ascending pharyngeal artery shared a common trunk and there was a type-1 pro-atlantal artery. The left ICA showed segmental agenesis (aberrant course) with a fusiform aneurysm in the temporal portion of the ascending pharyngeal artery. Both distal vertebral arteries were hypoplastic, supply to the basilar system coming mainly from the pro-atlantal artery (see also Fig. 9.7 for falx agenesis). E–O see pp. 625, 626

Coarctation and Congenital Heart Disease

Fig. 12.8E–J. Legend see p. 624

625

626

12 PHACES

Fig. 12.8 (continued) Subischemic state of the brain led to burr hole surgery (L), similar to moyamoya treatment. Follow-up 2 years later (M–O) shows the triggered angiogenesis supplying the left hemisphere. The patient partially improved clinically

Stenotic Arterial Disease

627

heart and tunica media of the aortic arch, just as crest cells from more cranial levels contribute to the development of the great vessels and the carotid arteries (Etchevers et al. 2001). Right-sided aortas were also encountered in our series of PHACE cases (Figs. 12.4, 11.23).

12.2.5 Eye Abnormalities

Ophthalmological abnormalities have been described in approximately one-third of the cases in the literature (Coats et al. 1999). These include choroidal and other orbital hemangiomas, cryptophthalmos, colobomas, posterior embryotoxon, microphthalmos, optic nerve hypoplasia, and glaucoma. Exophthalmos, optic atrophy, and strabismus are probably secondary phenomena. The orbital skeleton, as well as the connective tissue of the orbit, sclera, and cornea are all of neural crest origin derived mostly from the mesencephalic crest, as established from studies in species with tectal vision.

12.2.6 Sternal Cleft

In reviewing the literature of 43 patients who were identified as having PHACE syndrome, Frieden et al. (1996) found three patients with ventral developmental defects (Fig. 12.8). Both sternal clefts and supra-abdominal raphes were encountered. This feature seems rarer than the arterial stenotic disease discussed below and the S in the extended acronym PHACES probably should more appropriately refer to arterial stenosis.

12.2.7 Stenotic Arterial Disease

The description by Burrows et al. (1998) of progressive arterial occlusive disease together with the four cases in Bhattacharya’s series (2004) illustrate the susceptibility of the large- and medium-caliber arteries in the PHACE syndrome very well. The addition of S for stenotic arterial disease makes the acronym PHACES quite appropriate. In Burrows’s series, the onset of occlusive disease was between birth and 18 months of age. This correlates with the timing of the proliferative phase of the associated hemangiomas (see above for discussion of the possible effects of vascular growth factors and Chap. 11, this volume). However, Bhattacharya’s patients’ presentation was much later: from 4 to 14 years of age, by which time involution of the hemangiomas is long past. The stenotic lesions are mostly located at the anterior division of the ICA or the M1 segment (Figs. 12.7, 12.8), as they are in children with other vascular diseases (see Chap. 18, this volume). Intradural extracerebral pial collateral circulation is predominantly recruited; we have not observed true moyamoya phenomena or significant transdural supply. The lesions are usually unilateral and can involve P1. Cortical arteries on the supratentorial vascular bed can be involved (Fig. 12.8). The unsuppressed vessel wall proliferation (angiogenesis) rapidly leads to centripetal narrowing of the lumen and to

628

12 PHACES

Fig. 12.9A–C. A 14-month-old girl with interventricular communication operated on at 3 months of age. MRI for hemangioma in the occipital region and ipsilateral orbit found several asymptomatic vascular anomalies: peculiar dolicho-P1 segment of the posterior cerebral artery (A), dolichocervical internal carotid (B), and stenotic distal internal carotid artery (C). D–F see p. 629

Stenotic Arterial Disease

Fig. 12.9 (continued) Three-dimensional pictures (D–F)

629

630

12 PHACES

collateral angiectasia and some neovascularization. The occlusive phenomena may not stabilize at the same time as the hemangiomas involute, and this can in turn lead to neurological manifestations. Treatment includes antiplatelet therapy and surgical cortical stimulation of angiogenesis (Fig. 12.8). The timing of the putative embryonic insult remains somewhat speculative but probably occurs earlier than previously suggested, before or during the phase of vasculogenesis. The insult must take place before the migration of the neural crest and mesodermal cells occurs, to account for the widespread distribution of lesions, similar to CAMS, CVMS, or SAMS. The target is represented by the arterial forerunners (structural defects) or cascades (functional or signaling defects) involved in their modeling. Neural crest involvement has been proposed, but cannot be defended if one postulates a single target to be responsible for all manifestations. The neural crest and neural plate share a common lineage; indeed cells of the lateral border of the developing neural plate (i.e., the neural folds) under inductive influence of the adjacent epithelium, and possibly mesoderm, develop into crest cells, hence their common metameric origin with the cells of the hindbrain (Baker 1997). Moreover, it appears that all neural plate cells can become crest cells given the appropriate signals, and vice versa, and even epithelial cells can, in vitro, contribute to the neural crest lineage. They also share a metameric relationship with the adjacent cephalic mesoderm. It is well recognized from chimera experiments that the neural crest gives rise to a wide range of cell types, including skin, connective tissue, and skeleton of the craniofacial region, forebrain meninges, and the tunica media of the blood vessels of the face and forebrain (the endothelial cells here and elsewhere are derived from mesoderm). Le Douarin et al. (1999) have shown in avian embryos that crest cells forming the walls of the internal and external carotid arteries and their branches arise from the same metameric levels as the developing cerebellum. The supply to the posterior fossa in most birds originates from the caudal division of the ICA and the hypoglossal or proatlantal remnants. A lesion of the neural crest (or even the crest and adjacent neural plate for cerebellar involvement) alone is not sufficient to explain the complete spectrum of abnormalities seen in the PHACES syndrome. The nature and trigger of this early insult remains unclear, but neither in our series, nor in previous reports is there any evidence of a familial tendency, making a germ-line mutation unlikely.

PHACES, a Congenital Malformation and a Proliferative Disease

631

12.3 PHACES, a Congenital Malformation and a Proliferative Disease The hemangiomatous proliferations seen in infants seldom start in utero (Fig. 11.6) and usually regress spontaneously without inflammatory manifestations. Such unsuppressed proliferation and delayed apoptosis suggest improper signaling from vascular cells that should not have persisted and became proliferative for a while. It should be recalled that the posterior fossa lesions, the arterial anomalies, and the hemangiomas when lateralized are on the same side, even in the diffuse type of nonPHACES hemangiomas (Rossi et al. 2001; Metry et al. 2001; Waner et al. 2003). Stenotic lesions of cervical arteries and distal MCA or ACA branches are in favor of a very potent type of effect, which is not very selective and geotropically undetermined even if the targets are. The pseudo-rete (Mahadevan 2004) at the skull base in one of our cases, the arterial stenoses in infancy, and the progression over time all demonstrate that the vessel wall disease is triggered at an embryonic phase (embryonic persistence), a fetal phase (agenesis, and early regression with pseudo-rete or dolicho vessels), during the perinatal phase (hemangiomas), and in infancy and early childhood (occlusive manifestations). It also points to the impossibility or deficiency of the remodeling function. Associated occlusive arterial disease is most likely caused by abnormal mural angiogenesis (non-sprouting); it normally leads to an increase in lumen caliber, when the correct remodeling signals induce the apoptosis of the unnecessary vessel wall components. Lack of remodeling produces centripetal and longitudinal proliferation, hence lumen reduction, or sometimes ectasias, elongated arteries and aneurysms, as seen on some persisting embryonic arteries. These observations point to the role played by the apoptotic mechanisms and the correct development of the vasculature and cerebral structures, in particular in the early embryonic stages and later during the perinatal phase (Oppenheim 1991; Martinou 1995). It is impossible at this stage to focus on a single target responsible for the complete phenotypic expression of PHACES syndrome. Yet an event impairing the cascades involved in cell death management can be grossly dated to the 5th– 10th weeks. Multiple subsequent targets will be impaired by such functional damage.We are then describing a malformation type of disease, yet it is intracellular. Intriguingly, this hypothesis links the true nonproliferative malformations (e.g., coarctation, Dandy-Walker) to true proliferative manifestations (e.g., hemangiomas with new vascular lumen, aneurysms with axial centrifugal vessel wall proliferation, occlusive disease with axial centripetal vessel wall proliferation, and dolicho arteries with longitudinal vessel wall proliferation Figs. 12.6, 12.9) within the same causative disorder.

13 Cervicofacial Vascular Malformations

13.1

Introduction 634

13.2

Postulated Embryogenesis 638

13.3

Diagnostic and Pretherapeutic Evaluation 640

13.4

Clinical Diagnosis of a Vascular Malformation 640

13.5 13.5.1 13.5.1.1 13.5.1.2 13.5.2 13.5.2.1 13.5.2.2 13.5.3

Arteriovenous Shunts 641 Soft Tissue AVMs 643 Intramuscular AVMs 643 Cutaneous AVMs 644 Intra-osseous AVMs 646 Mandibular and Maxillary AVMs 646 Signs and Symptoms 651 Metameric Cerebrofacial AVMs 657

13.6

Intra-osseous Slow-Flow Malformations 659

13.7

Arteriolar-Capillary Malformations 659

13.8

Capillary Venous Malformations 659

13.9

Venous Vascular Malformations 660

13.10

Complex Cerebrofacial Venous Syndromes (CVMS or Sturge-Weber Syndrome) 670

13.11

Lymphatic Malformations 670

13.12

Mixed Vascular Malformations 681

13.13

Multifocal AVMs 681

13.14 13.14.1 13.14.2

False Maxillofacial Vascular Malformations 681 Idiopathic Facial Vascular (Venous) Dilatations 681 Facial Venous Dilatation Associated with Intracranial Vascular Lesions 685

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13 Cervicofacial Vascular Malformations

13.1 Introduction Vascular malformations are errors of vascular morphogenesis (Fishman and Mulliken 1993; Mulliken and Young 1988; Wisnicki 1984). Although generally considered to be present at birth, they are usually not apparent and become evident or symptomatic only later in life. They grow in proportion to the growth of the affected child (Fig. 13.1) but may increase in size secondary to specific triggering factors, including hemodynamic or rheological changes such as increased blood flow, resulting in vessel elongation and dilatation, obstruction, or thrombosis. The development of individual lesions, especially high-flow lesions, may be stimulated by various factors, including endocrine factors (puberty, pregnancy), trauma, and iatrogenic insults such as incomplete surgery, proximal embolization, and infection (Fig. 13.2). It is likely that the principles related to cerebral arteriovenous malformations (CAVMs) also apply to those in the maxillofacial region. Since most vascular malformations are not visible at birth and some become apparent, on occasion in a spectacular fashion over time (Fig. 13.3), most prevailing in AVMs involving the soft tissues, a quiescent preexisting defect must be postulated as well as the influence of revealing triggers. The specific growth of the maxillofacial region is probably active enough to trigger the appearance of a lesion among the rest of the adjacent structures. What is referred to as vascular malformations may correspond to a defective remodeling process where remodeling makes up the final stages of vessel formation and where the vasculature becomes a stable, mature vessel bed (Folkman and D’Amore 1996), rather than to an embryonically malformed vascular architecture. Although no hereditary maxillofacial vascular malformations exist, the defect might be genetically based and expressed secondarily (or perhaps under-expressed) in the first few years of life (see “Hereditary Hemorrhagic Telangiectasia” in Chap. 3, this volume). In addition to cell regulation and morphogenesis, there may be other physiologic events such as the presence of high flow that can further impact the outcome. Although a curative management would be ideal, the price to achieve this may not warrant the risk, and therefore a less ideal and less aggressive intervention (closing a high-flow AVF, reducing the venous hypertension, etc.) may palliate the symptoms or slow the progression of the disease. In children under 10 years of age with a symptomatic vascular lesion of the maxillofacial region, additional problems that do not occur in adults are encountered, such as the natural growth and maturation of the maxillomandibular skeleton, the potential for growth of the lesion with stimulation and induction of angiogenesis, interfering with bone growth, teeth eruption, and malocclusion of the mouth, modeling defects due to external pressure of the forming bones or sinuses (Scheme 13.1) (Lasjaunias et al. 1985), where early intervention can arrest and even reverse such changes (Figs. 13.26, 13.30, 13.33). Endovascular therapists have long promoted their techniques in the management of various vascular lesions of the maxillofacial region. Over the last 10 years, advances in surgical techniques added by pre-, intra-, or postoperative embolizations have created the opportunity for new treatment strategies by specialists

Introduction

635

Fig. 13.1A–D. Capillary vascular malformation. A Girl, 7 weeks of age, with a lesion that was present since birth. B At 15 months of age, the lesion has the same geographical distribution, but has developed high-flow shunting (arrow), manifested by the development of a thrill and a bruit. C Lateral angiogram of the posterior auricular mid-arterial phase shows a capillary malformation, with an area of AV shunting. D At age 3 years, after laser photocoagulation, there is still additional treatment to be performed on the remaining areas

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13 Cervicofacial Vascular Malformations

Fig. 13.2. A A 15-year-old girl with a high-flow AVM that expanded at the onset of menses (arrow). B, C Lateral digital subtraction angiography (DSA) of the left ECA (LTECA) demonstrates a high-flow AVM, with a very prominent draining vein (arrow). Note the multiple AV shunting. D One week after acrylic embolization of the AVM, note regression of the prominent vein

combining competence in endovascular, plastic, and reconstructive head and neck surgery in children (Berenstein et al. 1986; Persky and Berenstein 1987; Persky et al. 2003; Riles et al. 1993; Rodesch et al. 1998; Waner and Suen 1999a, b; Seccia 1999; Hubbell and Ihm 2000; Lee and Ter Brugge 2003). It is imperative to understand that vascular malformations are not tumors, and the prime goal of treatment is to restore and preserve function, stop and control bleeding, and improve cosmesis, which are all quality-of-life improvement goals.

Introduction

637

Fig. 13.3. A Soft-tissue AVM at 3 years of age; only targeted embolization was done. B Twenty-three years later, the lesion shows proliferative activity with ulceration and bleeding

Scheme 13.1. Oral sensorimotor pathways and their contribution to the corporeal scheme

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13 Cervicofacial Vascular Malformations

13.2 Postulated Embryogenesis Vascular malformations are traditionally classified according to the channel abnormalities present and their flow characteristics (Table 13.1) (Lasjaunias and Doyon 1980; Mulliken and Glowacki 1982; Burrows et al. 1983; Jackson et al. 1993). The mechanism of formation of maxillofacial vascular lesions has been deduced from the work of Woolard (1922) on the maturation process in the capillary network of the limb bud of the pig. However, the analogy between the development of the limb and that of the head and neck must be questioned, as several important differences in the embryogenesis of these two regions exist. The progressive centrifugal development of the limb around a fixed arterial source requires a constantly growing vascular bed, similar to a growing tree. The various forms of vascular lesions have been considered to be caused by arrests occurring at different stages of vascular development. For example, Kaplan, who based his conclusions on the vascular development of the extremities, related the capillary lesions to an early stage-1 abnormality (undifferentiated capillary network); later in the same stage, the lesion would be of the cavernous type. An arrest in the second stage (retiform stage) would produce an arteriovenous shunt (AVS) (single-hole or true AVM with a nidus). Finally, at stage 3 (maturation stage), arrests would lead to venous or lymphatic malformations. The rarity of fetal diagnosis of most vascular malformations (with the exception of the lymphatic malformations) suggests an embryonic or fetal cellular defect rather than an already abnormal architecturally demonstrable abnormality. The development of the head and neck area involves different and more complex changes (rotations, invaginations, migrations) of the tissues, which locally crumple or blossom during the first weeks in uterus. We know from Paget’s work (1948) that during normal development of the head and neck the vasculature undergoes a series of changes in its branching patterns. Regressions and annexations of some arterial sources or territories account for the unique bi-directional flow in every branch of the head and neck area and for the variability in the territories supplied by a given artery. Due to the Table 13.1. Clinical manifestations in maxillofacial vascular malformations Clinical findings

Capillary

Arteriovenous

Capillary venous

Venous

Venolymphatic

Pulsatility, thrill Bone Enlargement Vascular space Phleboliths Compressible Progression Progressive Acute crisis, regressive Valsalva swelling

±

+ (Can be absent)

–

–

–

– – – –

– + – –

± – ± –

– – + +

+ – ±

+ – –

± – –

± ± ±

– – +

± + –

+, Frequent; ±, possible; –, not seen.

Postulated Embryogenesis

639

nature of the specific modeling of the maxillofacial buds, it may be predicted that the vascular system of adjacent buds will overlap and eventually compete, leading to the annexations and regressions mentioned above. It then becomes almost impossible to find what might correspond to the initial central or peripheral portion of the maxillofacial buds and therefore to elaborate further on a strictly morphological basis. Delay in bud fusion produces specific arterial anatomic variation, because the usual bridging tissue has been omitted (or destroyed). If the maturation of the capillary network is simultaneously delayed, vascular lesions may be seen in association with the arterial variations without clefts. Facial clefts and their various locations can be related to specific arteries (Tessier 1976; Lasjaunias and Berenstein 1987). Study of the arterial vasculature of the palatine clefts (Fredericks 1973) shows that the clefts behave like anatomic barriers to vascular development and that their margins are highly vascularized (Ricbourg 1981). If this embryonic abnormality (the cleft) is associated with persistence of the embryonic state of the capillary network, vascular malformations should be found on the margin of the clefts or on Tessier’s corresponding upper and lower meridian (Tessier 1976). In the conclusion of her analysis of the palate cleft arterial supply, Fredericks rejected an ischemic phenomenon due to lack of vessels as a cause of the morphological gap. Even if the malformation is present during the traditional development stages, we know that they will remain as a quiescent defect that will be triggered to produce an irreversible fetal, neonatal, child, or adult vascular malformation. HHT, which produces de novo vascular anomalies over time, often referred to as malformations, corresponds to a genetic transforming growth factor (TGF) deficiency involving endoglin (McAllister et al. 1994). The role of growth factors, involved in vascular remodeling, is probably not restricted to their primary effect, but rather they serve as multipurpose agents with, for example, a qualitative and quantitative impact on the endothelium (e.g., promoters, inhibitors, angiogenic factors, matrix regulators). The same agent may have simultaneously or consecutively different effects on the vessel wall. In vascular malformation, the local revealing trigger has produced the dysfunction, which in turns creates -malformation-induced shear stresses that then shift the remodeling process of adjacent unaffected vessels to an abnormal state (highflow angiopathy; see Chap. 2, this volume). This emphasizes the role of the revealing trigger as compared to the original defect. Couly et al. (1995), using quail to chick embryo isotopic isochronic chimeras, demonstrated that endothelial cells of the cephalic region have a regionalized origin. In general, the neural crest and mesodermal cells originating from a given transverse level occupy the same facial territories and the two cell types co-operate in both myogenesis and vasculogenesis. Thus muscles are formed by myocytes of mesodermal origin and connective cells of neural crest origin. Similarly, the endothelium and the media of blood vessels are derived from mesoderm and neural crest, respectively (with the exception of in the mesencephalic region and the

640

13 Cervicofacial Vascular Malformations

spinal levels, where they both originate from the mesoderm). Some particularities are encountered in this context: 1. The pre-chordal mesoderm supplies few endothelial cells. 2. The rostral mesoderm supplies the prosencephalon and the nasofrontal and maxillary areas. 3. The middle mesoderm supplies part of the diencephalon and the first branchial arch derivatives (from the lateral portion of the middle mesoderm, giving rise specifically to the supply to the arch; there is no contribution to the brain). 4. The caudal mesoderm supplies endothelial cells and media to the mesencephalon and metencephalon bilaterally and the most lateral part of the ipsilateral second branchial arch derivatives caudally; the par-axial mesoderm, the mesodermal structures and their vascularization have the same segmental origin. Based on this contribution, we can recognize some of the clinical syndromes described in the literature and can postulate a link between apparently unrelated territories. Regions that are spared in Sturge-Weber and Wyburn-Mason syndromes are as characteristic of the syndrome as those involved by the pathological process (see Chaps. 6, 8, and 12, this volume). Finally, the migration process of the endothelial cells creates phenotypical characteristics along its path that make an endothelial cell of the maxillary artery (or vein) different from an endothelial cell of the middle cerebral artery (or vein), despite their originating from the same mesoderm region. In addition, the abluminal environment further influences the response of endothelial cells to the same triggers (Scheme 2.17).

13.3 Diagnostic and Pretherapeutic Evaluation The questions faced when dealing with vascular malformations in children have remained the same: What is the nature of the malformation? What type and extent of damage already exists? What is the potential for further development? To what extent can the process be stopped and repaired, further damage prevented, or simply can time be gained as our understanding of their progression and newer therapeutic strategies evolve?

13.4 Clinical Diagnosis of a Vascular Malformation The diagnosis of a vascular malformation is usually made clinically, from the history and physical examination and from cross-section noninvasive imaging, which should be done judicially and is helpful to determine the extent of the lesion and to demonstrate associated lesions or multifocal involvement. Rarely is there a need for any invasive procedures to establish the diagnosis and the type of malformation involved.A thorough history and careful attention given to the child’s complaints are often sufficient to establish the diagnosis. If the cosmetic aspect is dominant, then direct communication should always be established with the child in order to temper the demands of the parents. Certain symptoms are so

Arteriovenous Shunts

641

typical of a specific type of lesion that their absence suggests that such a lesion is not present. Magnetic resonance imaging (MRI) is the most useful single imaging modality in the investigation of vascular malformations (Siegel et al. 1989; Yuh et al. 1991). The combination of multiplanar spin echo imaging and flow-sensitive sequences permits characterization of the nature and extent of most lesions. Computed tomography (CT) is less helpful in defining flow characteristics and the extent of vascular malformations, but has a role in demonstrating the nature and extent of bony involvement and the presence of phleboliths, which are pathognomonic of venous malformations. Ultrasound, including Doppler techniques, is a modality for determining tissue and flow characteristics in superficial lesions, but is suboptimal in demonstrating the extent of lesions. Angiography is reserved for patients in whom a decision has been made to intervene and is generally performed at the same time as embolization. Exceptionally, angiography may be necessary to confirm the diagnosis and to demonstrate the extent of the soft tissue capillary or arteriovenous malformations or fistulas. In addition, past and present photographs of the patient must be obtained.

13.5 Arteriovenous Shunts An AVM consists of a nidus or network of abnormal vascular channels that are interposed between feeding arteries and draining veins (Fig. 13.4). Except for the extremely rare high-flow AVFs, seen with parachordal lesions (see Chap. 14, this volume), most soft tissue AVMs are usually asymptomatic during the first or second decade of life. They often manifest as a cutaneous blush with or without underlying soft tissue hypertrophy. Clinical findings include local hyperthermia, pulsations, thrill, and bruit. The clinical progression of these lesions often seems to be precipitated by hormonal factors (puberty, pregnancy, hormone therapy), trauma, infection, or iatrogenic causes (surgery, embolization) (Figs. 13.2, 13.3). Close follow-up is essential, as AVM may extend, especially after incomplete surgical intervention or proximal embolization,into tissues or territories that initially did not appear to be involved. Venous hypertension may result in tissue ischemia, ultimately leading to pain and skin ulceration, often associated with severe bleeding (Figs. 13.3, 13.5). As an overall strategy, if complete eradication cannot be obtained with combined approaches and when a clinical manifestation requires stabilization, we recommend partial, targeted endovascular control of the lesion with liquid embolic agents. In general, we are opposed to partial surgical treatment,which in our experience often further triggers the arteriovenous lesions. Such surgery may be warranted where severe functional or life-threatening bleeding needs to be controlled, although most of the time this can also be achieved by transarterial or direct percutaneous embolization. In many cases, the subsequent increase of the abnormal network is rendered difficult to treat, as it involves normal, reactive vascularization. Any attempt at this stage to correct the appearance leads to ischemic manifestations, including true angiogenesis.We also try to delay major facial surgical reconstructions involving the skeleton until after the completion of maxillofacial growth.

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13 Cervicofacial Vascular Malformations

Fig. 13.4A–D. An 8-year-old boy presented with a port-wine stain in the territory of the left V3 nerve. A–D When he was admitted, he had several gingival hemorrhages associated with a gum, lower cheek, and mandible arteriovenous lesion of the capillary type with rapid venous shunting. He had several loose baby teeth, which were removed. Embolization was performed transarterially and by direct puncture into the mandible, which resulted in obliteration of the intraosseous vascular lake with glue

Intramuscular AVMs

643

Fig. 13.5A, B. A 6-year-old girl presented with a portwine stain from the pinna. A, B Ischemic ulcer and a varix indicate an underlying arteriovenous shunt. This particular child was not treated until a few months later in an emergency procedure after a traumatic insult to her external ear resulted in severe hemorrhage

The main indications for early active management of vascular malformations are:







Dental arcade stabilization Osseous remodeling Recurrent hemorrhagic complications Mass effect (swallowing, growth) Episodic swelling and airway compromise Neurological impairment

Finally, we monitor the maxillo-mandibular growth conditions and try to anticipate any induced dystrophic change before it requires specific surgical management by a combination of embolization and orthodontic treatment.

13.5.1 Soft Tissue AVMs 13.5.1.1 Intramuscular AVMs

Intramuscular AVMs may be associated with pain (e.g., trismus). These arteriovenous lesions are rarely strictly limited to a single muscle and, when they are, they usually involve a masticator muscle. Some of these lesions are small (micro-AVMs) and are clinically difficult to detect. These appear as recurrent hematomas, particularly in the masseteric muscle where the lysed hematoma may be diagnosed as a cystic lesion that secondarily bled. Surgical exploration of these lesions demonstrates small malformations on the wall of the cavity. Most of the other vascular lesions involving the masticatory muscles are of the venous type.

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13 Cervicofacial Vascular Malformations

13.5.1.2 Cutaneous AVMs

Cutaneous AVMs initially demonstrate a superficial blush and warmth (Figs. 13.1–13.6).As they develop, the color intensifies and tortuous, tense veins may appear (Figs. 13.1, 13.2, 13.7). Dystrophic changes, ulceration, bleeding, and persistent pain may follow (Fig. 13.5). MRI confirms the diagnosis of an AVM and will demonstrate its extent, although it is often difficult to distinguish between the actual nidus and the feeding and draining vessels. Trauma is a frequent source of lesional growth with hemorrhagic complications, particularly in children and with external ear AVMs. On clinical examination, midline-located arteriovenous fistulas (AVFs) of the forehead can (and should) be differentiated from sinus pericranii. Focal arteriovenous sites in the facial cutaneous area are not associated with intracranial sites unless seated on the midline (see Chap. 6, this volume). Treatment must be planned carefully to avoid stimulating progression and interfering with future management. In particular, proximal ligation or embolization or coiling of feeding vessels must be avoided (Lasjaunias 1987; Riles 1993). Selective targeted arterial embolization is indicated to decrease symptoms such as pain, bleeding, and ischemic ulceration (Burrows et al. 1987; Forbes et al. 1986; Lasjaunias and Doyon 1980; Jackson et al. 1993; Komiyama et al. 1992; Riles et al. 1993; Terada et al. 1991). Where possible, it should be performed with permanent agents, such as tissue adhesive. High-flow cervicofacial AVMs are difficult to obliterate by arterial embolization alone. They are best managed by combined approaches. Lesions that are amenable to complete excision are probably best treated with presurgical embolization and excision (Figs. 13.7, 13.8) (Berenstein et al. 1986; Lasjaunias and

Fig. 13.6A, B. Cutaneous AVM in a 2-year-old child. A There is skin discoloration, the lesion is warm, with pulsations, but no thrill. B After direct ethanol embolization

Cutaneous AVMs

645

Fig. 13.7. A Cutaneous capillary malformation that has evolved from a flat discoloration to tortuous venous channels. The lesion was embolized with polyvinyl alcohol foam (PVA) particles mixed in 30% ethanol, with preservation of the main facial trunk. B Two years after a split skin graft, with no clinical recurrence 23 years later

Fig. 13.8. Scalp high-flow AVM with a mature tissue expander in the normal territory

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Doyon 1981; Mulliken and Young 1988; Goldberg et al. 1993; Persky et al. 1986, 2003). Large lesions involving the skin surface may do well with extensive excision and microvascular soft-tissue grafting or preparation with tissue expanders (Fig. 13.8) (Marotta et al. 1994). Conservative treatment should not be considered as a failed treatment decision, but sometimes is the least mutilating option, particularly in certain ear AVMs. Lesions in periorbital sites may require transophthalmic catheterization and embolization (Alvarez et al. 1990; Matsumaru et al. 1997). A direct percutaneous approach is an adjunct to arterial embolization and may be effective in obliterating the nidus (Jackson et al. 1993; Yakes 1992) if the nidus cannot be reached during transarterial embolization.

13.15.2 Intra-osseous AVMs

Intra-osseous AVMs are rare and have been overdiagnosed in most instances. The misdiagnosis results from an erroneous interpretation of associated features caused by a superficial soft-tissue AVM. The associated bone hypertrophy results from the indirect consequences of venous and lymphatic interference by the adjacent subcutaneous or muscular lesion; and must be distinguished from truly intraosseous AVMs.

13.15.2.1 Mandibular and Maxillary AVMs

Dental AVMs (e.g., those involving the maxilla or mandible) are particularly dangerous, as patients may present with life-threatening hemorrhage related to tooth eruption, dental infection, spontaneous loosening of the teeth, and dental extraction. Such hemorrhage can be managed by arterial embolization followed by extraction of any loose or involved teeth (Persky et al. 1986, 2003; Burrow et al. 1988; Lasjaunias et al. 1982, 1985; Rodesch et al. 1998). Bone erosion surrounding teeth may be best shown with CT or Panorex radiography (Fig. 13.4). In our experience, selective arterial embolization, often followed by direct injection of the intramandibular nidus and draining vein with tissue adhesive, has resulted in stable obliteration or even complete exclusion of the nidus with reossification of the affected mandible (Figs. 13.9–13.11). This approach is preferred to mandibulectomy, especially in the immature facial skeleton (Chiras et al. 1990; Flandroy and Pruvo 1994; Resnick et al. 1992; Shultz et al. 1988; Van Den Acker et al. 1987, Persky et al. 2003). Over the years, many authors have advocated various treatment strategies for intraosseous vascular malformations of the head and neck, including embolization, surgical resection, and combined treatments. Immediate results usually have been successful regardless of the methods employed; however, long-term outcomes are disappointing, with recurrence of these malformations and occasionally progression of disease. From past experience, three definite conclusions can be made on the treatment methods of these malformations:

Mandibular and Maxillary AVMs

Fig. 13.9A–E. Right mandibular AVM presenting with severe dental bleeding, a loose molar, and a painful mass. A Note the facial asymmetry. B CT scan shows the bony erosion and expansion. C Lateral DSA of the right common carotid artery (RTCCA) shows a high-flow AVM. D Superselective submental catheterization under flow arrest permitted reaching the vein with good acrylic penetration. E CT 1 year later demonstrates reossification of the mandible

647

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1. External carotid artery ligation inevitably leads to recruitment of collateral circulation from the internal carotid, vertebral, and the contralateral external carotid circulations, making subsequent treatments more difficult, and must be avoided at all cost. 2. Proximal vessel ligations, or embolization do little to decrease blood flow since recruitment of new feeding vessels quickly re-establishes blood supply to the lesion, and the reactive nonsprouting angiogenesis may become indistinguishable from the nidus and should be avoided at all costs. 3. Only complete removal, either by surgical resection or embolic devascularization of the vascular malformation, results in a cure. The principle of targeted embolization may apply to those where cure is not feasible. Cure is defined as the complete eradication of disease resulting in permanent resolution of symptoms. In 2003, we analyzed our long-term experience in 31 patients with vascular malformations involving the maxilla and mandible, treated primarily with endovascular therapy from 1979 to 2001 (Persky et al. 2003). All patients underwent embolization either as definitive treatment, palliative therapy, or preoperatively in preparation for a planned surgical resection. The malformations were categorized into maxillary, mandibular, and combined maxillary/mandibular vascular lesions to help characterize and predict the treatment outcome of these patients. Outcome results were measured as “cured,” “improved” (improvement of facial deformity and associated clinical symptoms), “stable” (control of bleeding symptoms), or “progressive” (active and persistent symptomatic vascular malformations causing bleeding, pain, swelling, or ulcerations). In our series, 31 (16%) of 190 head and neck disease patients with vascular anomalies had vascular malformations involving the mandible and/or maxilla (Table 13.2). The treatment group consisted of 13 males and 18 females (1:1.5) with a mean age of 16 years at initial presentation (range, 1–55 years), 20 patients were under 16 years of age. The average duration of follow-up was 6.7 years (range, 1–22 years). Seventeen patients had the right side involved and in 14 patients, the left side was affected. There were 13 cases of mandibular involvement, 13 patients with maxillary malformations (Fig. 13.11), and five with combined maxilla and mandible malformations. Twenty-six (84%) of the vascular malformations were arterial and five (16%) malformations were venous or capillary (one patient). Adjacent soft-tissue involvement with vascular malformation was most extensive with patients who had both maxillary and mandibular disease, which usually included the entire hemi-face, neck, and orbit. Moderate soft tissue involvement occurred with maxillary malformations such as the face, orbit, or cheek in various combinations. There was one maxillary vascular malformation with no soft-tissue involvement. Mandibular malformations often involved adjacent soft tissues but to a limited extent.

Mandibular and Maxillary AVMs

649

Fig. 13.10A–D. An 11-year-old girl presenting with hemorrhages from the gum. A Panoramic radiogram performed at the time of hemorrhagic complication related to molar eruption (arrow). Note the density of the lower portion of the adjacent maxillary sinus (arrowheads). B Selective injection of the internal maxillary artery before embolization. C Direct injection into the maxillary extension of the lesion of isobutyl cyanoacrylate deposition. D Panoramic radiogram 1 year later. Note the satisfactory eruption of the teeth, disappearance of the maxillary sinus extension, and the radiopaque iso butyl cyanoacrylate (IBCA) (open arrow). Ten years later, there had been no recurrence, and the patient was able to work as a fashion model

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Fig. 13.11. A A 14-year-old girl with a maxillary arteriovenous malformation (AVM), presenting with progressive soft-tissue overgrowth and oral bleeding after placement of braces. B One week after NBCA embolization, she underwent surgical intervention and removal of the soft tissue lesion with no recurrence 12 years later

Table 13.2. Intraosseous vascular malformations (mandible-maxilla) (modified from Persky et al. 2003) Case

Sex

Age

Follow-up (years)

Site

Adjacent soft tissue

Type

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31

F F F F F F F F F F M M M F F F F F M M M M M M M M F F M M F

6 8 11 35 5 10 11 12 27 40 11 17 38 18 5 8 10 10 11 11 27 4 10 23 55 1 12 18 15 31 6

1 1 2 2 10 1 11 1 6 1 8 12 1 17 5 22 5 12 1 7 8 10 4 3 3 10 11 10 2 5 14

MN MN MN MN MN MN MN MN MN MN MN MN MN MX MX MX MX MX MX MX MX MX MX MX MX MX MX/MN MX/MN MX/MN MX/MN MX/MN

None None FOM Lower lip, FOM Cheek, neck, soft palate None Cheek Preauricular, ear Masseter muscle None Lower lip Masticator space, FOM, neck Masticator space Cheek Masticator space Face, orbit Cheek Face, orbit None Masticator space, sphenoid Face, upper lid Cheek, orbit Lower lid Cheek, neck, orbit, postauricular Face, orbit Nose, forehead Face, neck, ear, orbit Masseter, FOM, brain Face, orbit Face, neck, ear Face, ear

Art Art Art Ven Art Art Art Art Art Cap Art Art Art Art Art Art Ven Art Art Art Art Ven Art Ven Art Art Art Art Art Art Art

MN, mandible; MX, maxilla; Art, arterial vascular malformation; Ven, venous vascular malformation; Cap, capillary vascular malformation; FOM, floor of mouth.

Signs and Symptoms

651

13.15.2.2 Signs and Symptoms

Table 13.3 reviews the signs and symptoms of the patient cohort. Twentyeight patients (90%) had bleeding and all patients with mandibular and combined maxillary/mandibular vascular malformations presented with this symptom. Most bleeding originated from the gingival or alveolar ridge and was spontaneous following dental eruption or loosening of the teeth. The second most common cause of bleeding was iatrogenic from attempted biopsies, mass excisions, or dental extractions. Epistaxis was a common presenting symptom with maxillary vascular malformations. Facial asymmetry and swelling occurred in 61%, followed by pain in 35% of cases. Bruits, thrills, and/or pulsations were hallmark signs of all arterial vascular malformations. As expected, these signs were absent in venous or capillary malformations. Six females (33%) experienced exacerbation of their symptoms with hormonal changes during their menstrual cycle or pregnancy. One patient had no evidence of her vascular malformation until pregnancy initiated the presenting symptoms of swelling and subsequent oral bleeding. Two patients with arterial vascular malformations of the maxilla/ mandible and extensive soft tissue involvement experienced high output cardiac failure. In our experience, embolization proved to be the treatment of choice, and was the only treatment in 81% of cases (Persky et al. 2003). In 19% of patients, embolization was followed by surgery. Bleeding symptoms were controlled in all patients, and no patients had progression of disease.

Table 13.3. Signs and symptoms

Bleeding Spontaneous Iatrogenica Epistaxis Minor traumab Facial asymmetry Swelling Pain

Mandible 13 patients

Maxilla 13 patients

MN/MX 5 patients

Total 31 patients

13 (100%)

10 (77%) 6 5 0 2 9 (69%) 10 (77%) 4 (31%)

5 (100%) 5 1 5 0 5 (100%) 2 (40%) 2 (40%)

28 (90%) 4 0 1 1 19 (61%) 19 (61%) 11 (35%)

5 (38%) 7 (52%) 5 (38%)

MN/MX, mandible/maxilla. a Brushing teeth or eating. b Dental extractions, biopsies.

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13 Cervicofacial Vascular Malformations

Among patients with mandibular lesions, regardless of the type of malformation, nine patients (70%) were cured, two patients (15%) improved, and two patients (15%) were stable (Table 13.4). All patients with malformations isolated to the mandible without soft tissue involvement were cured. A lower cure rate of 46% (six patients) was obtained for patients who had maxillary vascular malformations, and none of the patients with combined mandibular/maxillary malformations were cured of their disease, although four of these patients (80%) had stabilization of their lesions. Overall, 15 patients (48%) were cured, five patients (16%) had improved, and 11 patients (35%) had stable lesions. The average number of years since the last intervention was 2.2 years (range, 1–11 years).

Six patients undergoing surgical resection with preoperative embolization had arterial vascular malformations of the maxilla (four patients) or maxillary/mandibular lesions (two patients) with extensive soft-tissue involvement. Two patients in this group had subtotal resections of their maxillary arteriovenous malformations requiring maxillectomy and rehabilitation with prosthetic obturators and were cured of their disease 4 and 6 years after surgery. Four patients had partial resections of their lesions following preoperative embolization. Two of these patients had resection of only the overlying skin.An additional patient underwent extensive soft-tissue excision for impending life-threatening hemorrhage and another patient required a maxillectomy for radiation osteomyelitis with resection of the facial skin. These four patients have had no progression of their residual vascular malformations for 1–6 years following their surgery. Maxillary/mandibular and maxillary malformations tended to be more extensive and required more treatments and various combined interventions to obtain acceptable therapeutic results. In the continuing care of these patients, 11 had dental extractions under general anesthesia after angiography and embolization. This provided the necessary controlled conditions for potentially severe hemor-

Table 13.4. Therapeutic agents Approach

Architectural target

Direct puncture (glue, alcohol)

Mass (capillary type) Vascular space (venous lymphatic cyst) Bone (AVM, AVF)

Arterial embolization Particles (PVA) Particles + alcohol NBCA

Capillary lesions Arteriovenous shunts (soft tissue or bone)

AVM, arteriovenous malformation; AVF, arteriovenous fistulas; PVA, polyvinyl alcohol; NBCA, N-butyl cyanoacrylate.

Signs and Symptoms

653

Fig. 13.12. Foreign body reaction to acrylic embolization of an intramandibular AVM. After debridement, there is healing by granulation

rhage. Twelve (39%) patients in the study required blood transfusions at some time during the course of their treatment. One drawback of acrylic embolization in these areas is the development of delayed local foreign body reaction to the embolization material; it requires several series of surgical debridement to remove sequestered pieces or infection from retained foreign body embolic material (Fig. 13.12). No hemorrhage has been noted in this occurrence. Laser treatments for cutaneous manifestations of vascular malformations in three patients resulted in improved cosmesis. Thirteen patients had treatment complications, none of which were permanent: ischemic ulceration and necrosis in seven patients, osteomyelitis and infection in seven patients, and temporary visual disturbance in three patients. One patient developed significant orbital edema and increased intraocular pressure after direct puncture of a venous vascular malformation, requiring a lateral canthotomy. His visual acuity was not impaired and the orbital edema completely resolved. Temporary numbness along the inferior alveolar nerve distribution, transient facial nerve paralysis, pulmonary embolism from dislodgement of embolic material, and development of cataract from radiation were additional complications, all successfully treated without further consequences. Facial AVMs can be embolized even after proximal ligation of the external carotid artery by direct puncture of the feeding arteries or nidus (Figs. 13.7, 13.13), or by an arterial cutdown or surgical arterial reconstruction (Fig. 13.14) (Riles et al. 1993) (Table 13.2). Arterial reconstruction may, however, lead to massive facial and airway edema; this complication emphasizes further the role of embolization as the primary form of treatment in most facial AVMs (Riles et al. 1993). The advent of 3D rotational angiography is expanding our ability to study the angioarchitecture of these intraosseous AVMs in greater detail, as well as the risks and strategy involved in the venous approach in order to avoid upstream congestion and teeth hemorrhage (Fig. 13.15).

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13 Cervicofacial Vascular Malformations

Fig. 13.13A–C. Direct puncture of the mandible with a sternal needle (A). A conn ecting tube and a Y-connector allow a microcatheter to be introduced inside the mandible vascular spaces without manipulating in the vicinity of the needle and X-ray beam (B, C)

Fig. 13.14A,B. Legend see p. 655

▲

Signs and Symptoms

655

Fig. 13.14A–E. A 23-year-old woman who underwent ECA ligation at the age of 7 years (A, B), with progressive enlargement of the lesion and airway compromise requiring a tracheostomy (C) and reanastomosis of the ECA allowing multistage transarterial embolization with IBCA (D) acrylic cast. E After embolization there was significant reduction of the mass effect.

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Fig. 13.15A–D. A 3D reconstructed rotational angiography of bilateral mandibular AVMs. A View from posterior. B, C Right maxillary artery showing the venous congestion outlining the teeth’s roots. D The external carotid artery had been previously ligated. All the drainage of this bilateral mandibular AVM occurs on the left side. E–G see p. 657

Metameric Cerebrofacial AVMs

657

Fig. 13.15E–G. (continued) The mandible is punctured from the right side where glue is deposited as high as possible; then the left portion of the mandible is embolized from the right side with hydrocoils and glue. CT shows the communication between both sides from inside the mandible (E, F) and the embolic agents deposited (G). This 14-year-old girl is no longer presenting pain or bleeding. She is still being treated

13.15.3 Metameric Cerebrofacial AVMs

Complex orbitofacial arteriovenous malformations can be seen as part of the cerebrofacial metameric syndromes (CAMSs) (see Chap. 6, this volume). They involve both the soft tissues and the bones. Actually in two patients we have found the posterior fossa-associated lesion incidentally during screening for a symptomatic mandibular AVM.

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Fig. 13.16A–D. Intraosseous slow-flow malformation. A 7-year-old boy with a nonpainful right mandibular mass, underwent attempted needle biopsy with red blood return. A, B A 3D reconstruction demonstrates an expansive bony destruction. C, D Lateral DSA of the distal mid-arterial RTECA and late-phase study demonstrates slight pooling of contrast. E Oblique DSA of the direct puncture of the lesion. F,G see p. 659

Capillary Venous Malformations

659

Fig. 13.16. (continued) F Axial preoperative CT demonstrates the bony abnormality. G Axial postoperative CT, with reossification and normal appearance, after direct ethanol sclerotherapy

13.6 Intra-osseous Slow-Flow Malformations Intraosseous slow-flow malformations constitute a rare group of intraosseous vascular malformations that present with expansion of the bony cortex, present as a nonpainful mass, with bony changes of expansion suggestive of an aggressive behavior (Fig. 13.16). We have seen three such cases. An attempted biopsy resulted in bleeding. We have done angiography, which fails to show vascularity in the arterial or capillary phase, but may show some pulling of contrast material in the late phase of the angiogram. All have responded to direct alcohol sclerotherapy, with reossification.

13.7 Arteriolar-Capillary Malformations Formerly believed to be arteriolar-capillary malformations, these lesions constitute a rare subgroup of vascular lesions that at present are recognized as noninvoluting capillary hemangiomas (NICH) (Enjolras et al. 2001) (see Chap. 11, this volume).

13.8 Capillary Venous Malformations Capillary venous malformations include port-wine stain and telangiectasias (Enjolras and Mulliken 1993; Mulliken and Young 1988; Wisnicki 1984) and usually involve the skin surface.

660

13 Cervicofacial Vascular Malformations

Port-wine stains are often associated with progressive thickening of the skin and subcutaneous layers as well as overgrowth of the underlying facial skeleton, often resulting in facial asymmetry and dental malocclusion. These port-wine stains are early alterations of cell characteristics, as they are almost always present in infancy. The color may vary from one patient to the next and change over time.While most port-wine stains are isolated vascular anomalies, they may be associated with an underlying vascular malformation (lymphatic or capillary) (see Chap. 8, this volume) (Luo et al. 2003). Examples include port-wine stain over the spine, which may be associated with underlying spinal dysraphism or myelomeric AVMs (SAMS, see Vol. 2, Chap. 11 and Chap. 15, this volume).

13.9 Venous Vascular Malformations Venous vascular malformations (VVMs) are the most frequent vascular malformation of the head and neck area; they have a variable clinical presentation, depending on their depth and extent (Enjolras and Mulliken 1993; Mulliken and Young 1988). When superficial or when they involve mucosal surfaces, they are characterized by a bluish discoloration of the skin and/or mucosa (Fig. 13.17), they are soft, compressible, and refill over several seconds; the skin temperature over the lesion is normal. They can be discreet (Fig. 13.17) or can become disfiguring and may on occasion compromise the airway or swallowing pathways (Fig. 13.18). When they are located in deeper planes, there may be no skin involvement or discoloration, and they can present as fluctuating masses, which change in size with Valsalva maneuvers (Fig. 13.19), with changes in head position, or mastication when they involve the muscles of mastication (Fig. 13.20). Most of these lesions consist of spongy masses of sinusoidal spaces and have variable communications with adjacent veins. Alternatively, some venous malformations involve varicosities or dysplasias of small and large venous channels (Burrows and Fellows 1995; Dubois et al. 1991). The lesions are typically nonpulsatile, soft, and compressible, distend with Valsalva maneuvers and are easily emptied by manual compression, and are frequently multifocal and bilateral. They typically contain phleboliths, which when present are pathognomonic of these lesions (Berenstein 1990) (Figs. 13.19, 13.20). Characteristic MRI findings include focal or diffuse areas of high T2 signal, often containing identifiable spaces of variable size separated by septations (Meyer et al. 1991; Jackson et al. 1993) (Fig. 13.20). Small fluid levels may be visible. Phleboliths may be evident as areas of signal void, which are most prominent on gradient echo images. Flow-sensitive images demonstrate no high-flow vessels within or around the lesions, but may show evidence of old thrombus. Contrast administration results in variable enhancement, ranging from dense enhancement similar to that in adjacent veins to non-homogeneous or delayed enhancement. CT imaging likewise shows variable contrast enhancement with or without rounded lamellate calcifications (Fig. 13.19). Angiography is not necessary to make the diagnosis, but typically shows either no filling of the malformation or delayed opacification or sinusoidal spaces with a grape-like appearance when using a long con-

Venous Vascular Malformations

661

Fig. 13.17. A Venous vascular malformation in a 4-year-old girl that was barely present at birth, with slow progressive enlargement. B Six months after surgical excision. C At age 12, there was a significant recurrence. D One year later, two alcohol sclerotherapy treatments were given. Five years later, the treated area remains stable, and there has been some discoloration in untreated areas

trast injection with or without dysplastic draining veins (Fig. 13.21) (Burrows et al. 1983). Direct percutaneous catheterization of the malformation with contrast injection shows the interconnecting sinusoidal spaces (Figs. 13.19–13.22). Communications with adjacent veins may be small or large, and adjacent venous channels may be normal or dysplastic and varicose. Careful attention should be paid to the communication between the drainage and transcranial, orbital, or vertebral venous channels (See Vol. 2, Chap. 14 and Chap. 8, this volume) (Lasjaunias and Berenstein 1987). Direct injection of a sclerosing agent (98% ethanol, sodium tetradecal, or sodium ducal) results in thrombosis and gradual shrinkage of the malformation and is the preferred treatment (Berenstein and Hieshima 1987;

662

13 Cervicofacial Vascular Malformations

Fig. 13.18. Venous vascular malformation with significant disfiguration and compromise of the airway and alimentary tract

Anavi et al. 1988; Burrows and Fellows 1995; de Lorimier 1995; Goebel and Lucartorto 1976; Govrin-Yehudain et al. 1987; Lasjaunias and Berenstein 1987; Yakes et al. 1989, 1992). Several other agents have been used, including Ethibloc or Aetoxysclerol (Gelbert et al. 2000), but we have had no experience with either agent. Ethibloc, another sclerosing agent composed of amino acids, 40% ethanol and contrast medium, has been used in Europe and Canada as a sclerosing agent for venous malformations, usually prior to surgical excision (Dubois 1991). This material is usually diluted with additional ethanol or oily contrast medium prior to injection. It is more viscous than the other sclerosing agents. It can be injected without general anesthesia and is reported to result in chronic, progressive fibrosis. The technique of sclerotherapy involves the percutaneous catheterization of the malformation using a needle or Teflon-sheathed needle cannula (see Vol 2, Chap. 14, Fig. 14.3) (Fig. 13.22). After confirming free blood return, contrast is injected, recorded with serial angiographic imaging or road-mapping to document the cannula position within the malformation and the presence or absence of venous outflow (Fig. 13.22). In the presence of significant venous outflow, local compression is applied and contrast injections repeated until the venous outflow no longer fills (Fig. 13.23).

Venous Vascular Malformations

663

Fig. 13.19A–D. Intramasseteric venous malformation in a 15-year-old girl with facial swelling and discomfort. A, B Coronal CT images demonstrating contrast-enhanced soft-tissue mass containing phleboliths (arrows). C Coronal T2-weighted MRI demonstrating the high-signal septated mass containing a phlebolith (arrow). D Radiograph obtained after intralesional contrast injection demonstrating contrast stasis within the sinusoidal spaces and outlining a phlebolith (arrow). E,F see p. 664

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13 Cervicofacial Vascular Malformations

Fig. 13.19. (continued) E Clinical photograph obtained 24 h after intralesional ethanol injection, demonstrating marked swelling and skin discoloration. F Clinical photograph obtained 6 months after a single intralesional ethanol injection showing resolution of the mass

An estimation of the volume of the cannulated compartment within the malformation is calculated from the contrast material injection, as the venous drainage is seen, and the walls of the compartment are convex outward. Contrast medium is then aspirated or pressed out of the compartment and a similar quantity (usually one-third less of the calculated volume) of sclerosing agents is injected; 98% ethanol is usually opacified by mixing it in a 1-to-3 Ethiodol or Pantopaque-toethanol ratio. Ethanol denatures the blood cells within the malformation and dehydrates and scleroses the vessel wall if sufficient contact between the sclerosing agent and the endothelium is attained. The injected part of the malformation becomes firm and noncompressible because of thrombus formation within approximately 10 min. If the lesion does not become firm, and if there is persistent blood return from the cannula, additional ethanol may be injected, as swelling correlates with outcome (Donnelly et al. 2000). The total volume of injected ethanol should not exceed 0.3 ml/kg in children below the age of 2, and 0.5 ml/kg in older children.

Venous Vascular Malformations

665

Fig. 13.20A–D. A 6-year-old child presenting with venous malformation of the right masseteric region. A, B Presence of phleboliths confirmed the diagnosis of venous malformation. C Typical MRI appearance. D In view of rapid, permanent swelling, the child was treated at the age of 11 years by selective injection of alcohol into the large pouch. Postinjection swelling indicated that good sclerosis was achieved. Two-year follow-up showed a stable result, and no more swelling was noted

Mason (2000) reported the serum ethanol level in children, and that patients fulfilled the criteria for legal intoxication with a mean amount of ethanol administered to these patients of 0.87 ml/kg bw ± 0.18 (SD) (range, 0.55–0.99 ml/kg). Such numbers, however, do not apply to situations where a bolus of pure alcohol would be circulating suddenly. One must be careful to prevent alcohol from escaping into the systemic circulation, as it may produce cardiopulmonary arrest, which in peripheral VVMs has been reported to be fatal (Yakes and Baker 1993; Chapo 2003).

666

13 Cervicofacial Vascular Malformations

Fig. 13.21A, B. Recurrent venous malformation of the upper lip in a 10-year-old girl after partial surgical resection. A Right facial arteriogram, early and B late phases, demonstrating no arteriovenous shunting and only minimal opacification of abnormal venous channels around the margin of the malformation, in a grape-like pattern

If at time of alcohol injection, or shortly thereafter, there is a change in PO2, the treatment of choice is the immediate administration of epinephrine. Of extreme importance is to be even more careful in peripheral lesions, in particular if they drain in to the Azygos system (Fig. 13.22). Alcohol injection is extremely painful, and should be done under general anesthesia; the subsequent swelling is pain-free if the agent has been injected within the malformation itself. In the treatment of these benign conditions, it is our preference to stage the sclerotherapy to diminish the risk of complication. Treatment of large malformations is therefore invariably staged. Recanalization of previously treated lesions depends on the single vs multicompartmental nature of the lesion.A single cavity is likely to be excluded in one treatment, in contrast to a multicompartmental lesion or previously operated malformations, which require several punctures and will give incomplete results (Fig. 13.22). The commonest complications of ethanol sclerotherapy are skin or mucous necrosis (Vol. 2, Chap. 14) and neuropathy. Skin blistering or full-thickness necrosis are most likely to occur if the malformation involves the skin or mucosal covers. Other complications are related to over-injections of alcohol or controversial management of the overall malformation: cardiovascular complications, including bradycardia, arrhythmias, and cardiac arrest (Yakes and Baker 1993). Histological examination of animals injected with this drug re-

Venous Vascular Malformations

Fig. 13.22A–E. Multifocal venous vascular malformations. A 2-year-old girl with a large submandibular VVM and a lateral chest wall lesion. A Note the large soft tissue mass in the neck. B Opacification of the lesion after direct percutaneous cannulation of the lesion; note the connecting sinusoidal spaces with poor drainage. C DSA of the progressive injection of 98% ethanol (two-thirds) and one-third Ethiodol for radiopacity. Note the droplet appearance of the oily mixture. Plain film after injection. D During surgical excision 36 h after sclerotherapy, note the thrombosed channels within the lesion permitting easy removal, as the swelling permits the development of a clear surgical plane. E Thrombosed surgical specimen

667

668

13 Cervicofacial Vascular Malformations

Fig. 13.23A–D. Venous vascular malformation of the upper lip. A Note the extension toward the nasolabial fold; there is some bluish discoloration of the skin. B Twentyfour hours after the sclerotherapy, the lesion was thrombosed. C Surgical dissection was facilitated by the thrombosis, and the edema provides clear surgical plane demarcation. D Six weeks after surgery, there was small residual swelling

vealed marked inflammatory reaction with fibrosis (Govrin-Yehudain et al. 1987; De Lorimier 1995). One of us (AB) has been using facial monitoring to avoid facial nerve damage (see Vol. 2, Chap. 14). In general, the more localized deep venous malformations respond well to direct injection of a sclerosing agent (Fig. 13.24). Likewise, small cutaneous lesions, such as those in patients with multiple venous malformations, often respond very favorably (Fig. 13.17). In venous malformation involving the gingival mucosa, the treatment can be very effective, but one should be cautious not to use large amounts of sclerosing agent in order to avoid mucosal necrosis (Fig. 13.25). Diffuse lesions are much more resis-

Venous Vascular Malformations

669

Fig. 13.24A–C. Monocompartmental VVM. A A 4-year-old girl with significant facial asymmetry. B Progressive contrast injection demonstrates a monocompartmental lesion with very poor outflow, a very favorable lesion for sclerotherapy as the sole treatment. C Three months after treatment

tant to treatment by sclerotherapy. Venous malformations of the tongue and airway can often be successfully treated with sclerotherapy following tracheostomy, although more recently the use of laser photocoagulation has also proven to be very effective (Waner and Suen 1999c). In spite of the tendency for some lesions to recur, staged sclerotherapy can have a dramatic effect in reducing extensive cervicofacial venous malformations over time (Vol. 2, Chap. 14, Fig. 14.11). In very young children,VVMs may create remodeling of the maxillofacial bones and early intervention can reverse this (Fig. 13.26). More recently we have performed surgical excision of VVMs 24–36 h after sclerotherapy in certain well-defined lesions, taking advantage of the thrombosis within the malformation and the surrounding edema, which facilitates the development of a surgical plane of demarcation between the malformation and normal tissue (Figs. 13.22–13.23).

670

13 Cervicofacial Vascular Malformations

Fig. 13.25A, B. VVM involving the gingival mucosa. A Prior to sclerotherapy. B After two stages of sclerotherapy

Fig. 13.26A, B. VVM in a 14-month-old girl with bony deformity. A CT demonstrates the VVM, forward deformity of the zygoma, and nondevelopment of the maxillary sinus. B Follow-up CT 1 year after sclerotherapy. Note the remodeling of the bone, and full development of the maxillary sinuses

13.10 Complex Cerebrofacial Venous Syndromes (CVMS or Sturge-Weber Syndrome) Complex venous anomalies and orbitofacial complex venous malformations will be seen with the cerebrofacial venous metameric syndromes (Chap. 8, this volume)

13.11 Lymphatic Malformations Lymphatic malformations may be classified as macrocystic (Figs. 13.27– 13.29) or microcystic (Fig. 13.30). Those in the head and neck result from maldevelopment of the cervicofacial lymphatic system, which normally begins as paired jugular lymph sacs sprouting from the primitive jugular venous plexus in the 6-week-old embryo (Van de Putte 1975). The jugular

Lymphatic Malformations

671

Fig. 13.27A–E. Macrocystic lymphatic malformation in a 10-month-old infant with a progressively enlarging supraclavicular mass. A Clinical photograph at 10 months of age showing the localized supraclavicular mass with normal overlying skin. B Axial contrast-enhanced CT image through the mass demonstrated a predominantly intramuscular, low-density mass with no enhancement of the contents. C Axial T2-weighted MRI demonstrating the fluid level, with high signal in the supernatant. D Coronal T2weighted MRI through the anterior portion of the mass demonstrated the typically high signal intensity and showed the lesion to be bordered by the adjacent neurovascular structures inferiorly. E Clinical photograph obtained 2 months after aspiration of the cysts and injection of Ethibloc. During 3 years of follow-up, the lesion did not recur

672

13 Cervicofacial Vascular Malformations

Fig. 13.28A–C. Macrocystic lymphatic malformation in a 14-year-old boy. A, B Lateral view after contrast material injection, note the large, macrocystic compartment. C One year after ethanol sclerotherapy

Lymphatic Malformations

673

Fig. 13.29A–D. Cystic hygroma present since birth in one of two monozygotic twins (A, B) at 4 months of age and at 3 years, the lesion has grown commensurate to the child’s growth (C, D)

674

13 Cervicofacial Vascular Malformations

Fig. 13.30A–F. Legend see p. 675

▲

Lymphatic Malformations

675

Fig. 13.30. A, B Microcystic lymphatic malformation involving the maxillofacial area, interfering with the airway, requiring a tracheostomy, tongue involvement (lymphovenous malformation). C, D Note the characteristic lymphatic vesicles and the severe malocclusion. E Noncontrast and F contrast MRIs demonstrate a diffuse multifocal lesion with heterogeneous areas of enhancement and severe encroachment into the airway

sacs and channels normally spread to connect with the subclavian (axillary) lymph sacs, which then extend caudally, anastomosing with the internal thoracic, paratracheal, and thoracic ducts. Extensions of the jugular sac channels ultimately communicate with lymphatic channels of the head, neck, and upper limb that have sprouted from peripheral veins (Mulliken and Young 1988). The macrocystic types of lymphatic malformations (cystic hygromas) are thought to result from maldevelopment of the primitive jugular subclavian and axillary sacs, possibly by failure to re-establish venous connections. Interruption or obstruction of the peripheral lymphatic channels presumably results in diffuse or microcystic lymphatic malformations (i.e., lymphangiomas). Lymphatic malformations are usually, but not always, evident at birth. Some are diagnosed in utero. Macrocystic lesions most commonly are located in the neck (Fig. 13.29), axilla, and chest wall, may be massive, and can interfere with the birth process. Microcystic lesions usually present as diffuse soft-tissue thickening, often associated with an overlying capillary malformation of the skin or mucosal vesicles (Fig. 13.30). The lesions typically grow proportionally with the child, but undergo episodic swelling, often associated with signs of inflammation, either spontaneously or in association with regional infections. Acute enlargement may be related to lymphatic obstruction or hemorrhage. Communications between the macrocystic lymphatic malformations and adjacent veins are frequently present (Fig. 13.31). On physical examination, lymphatic malformations have a rubbery or cystic consistency. Typically, they cannot be manually compressed like venous malformations. The overlying skin may manifest capillary malformation, vesicles, or both. MRI findings in macrocystic lymphatic malformations include cystic fluid collections, often with fluid-fluid levels associated with rim or septal contrast enhancement (Meyer et al. 1991; Siegel et al. 1989; Figs. 13.27, 13.32). Evidence of hemorrhage or thrombosis may be present. Enlargement of adjacent veins, including the jugular, paravertebral, and superior vena cava, have been described in cervicofacial lymphatic malformations (Gorenstein et al. 1992; Joseph et al. 1989). Microcystic lymphatic malformations typically appear as diffuse sheets of bright signal on T2-weighted spin echo MRI, usually with various contrast enhancement patterns (Fig. 13.30). The adjacent subcutaneous fat often shows evidence of lymphoedema. CT best demonstrates the bone distortion and shows the soft tissue component of the malformation to be of lower density than surrounding muscle. Treatment of macrocystic lymphatic malformations generally consists in staged early surgical excision (Mulliken and Young 1988; Ravitch and Bush 1986); in selected cases of extensive lesions, the use of sclerotherapy may be successful (Figs. 13.28, 13.32). Residual or recurrent cysts may also be treated by injection of sclerosing agents.

676

13 Cervicofacial Vascular Malformations

Fig. 13.31A–C. Venolymphatic malformation of the tongue in a 3-year-old girl with a known lingual lymphatic malformation and a 3-week history of acute swelling and bleeding, with extension to the floor of the mouth. The tongue could not be replaced fully in the mouth after the onset of swelling. A Clinical photograph obtained prior to embolization showing the diffusely enlarged, dark reddish tongue. Note the hemorrhagic vesicles on the tongue surface, which are indicative of an underlying lymphatic (venolymphatic) malformation. B Lingual arteriogram demonstrating increased vascularity within the tongue with early opacification of a dilated lingual vein. C Clinical photograph obtained 1 week after embolization showing that the tongue has returned to normal size, permitting closure of the mouth

A wide range of sclerosing drugs have been used in the past with variable results. The most recent sclerosing agent reported to be effective in some lymphatic malformations is deoxycylcline, OK 432 (Picibanil), a derivative of the streptococcal bacterium, which has been used, predominantly in Japan, to induce inflammation and subsequent fibrosis (Ogita et al. 1991; Giguere et al. 2002; Rautio et al. 2003). In 1977, Yura reported the use of bleomycin in cystic hygroma with encouraging results, and sporadic reports exist, with the experience on bleomycin use reported by Muir in 2004 on 95 patients with heman-

Lymphatic Malformations

Fig. 13.32A–H. Multifocal lymphatic malformation, presenting with repeated episodes of swelling and bleeding (A, B). C–E MRI demonstrates the multifocality of the lesions. Note the macrocystic nonenhancing cyst, the subtemporal (double arrow), and medial orbital involvement. F Direct puncture demonstrates the macrocystic compartment and the retained ethanol-Ethiodol sclerosing material. G, H One month later, note the regression of the malar cyst component. F–H see p. 678

677

678

13 Cervicofacial Vascular Malformations

Fig. 13.32F–H. Legend see p. 677

giomas, cystic hygromas, and venous malformations. Complete resolution was noted in 49% of hemangiomas, 32% of VVMs, and 80% of cystic hygromas. Significant improvement was seen in an additional 38% of hemangiomas, 52% of VVMs, 13% of cystic hygromas, and 50% of lymphatic malformations. Bleomycin is a cytotoxic anti-tumor antibiotic. It has a dual effect in human tissue: it can induce DNA degradation and has a specific sclerosing effect in human endothelium (Yura 1977). We have had good long-lasting results with ethanol sclerotherapy in macrocystic cases (Figs. 13.28, 13.32). In multifocal lesions, or those that have repeated bleedings and involving the orbit and conjunctiva, a combination of sclerotherapy can be very effective (Fig. 13.32). More recently, the addition of laser photocoagulation can further enhance the treatment of conjunctival involvement.

Lymphatic Malformations

679

Fig. 13.33A–E. Venolymphatic malformation of the tongue in a 3-year-old girl. A–C One year after embolization of both lingual arteries with polyvinyl alcohol (PVA), the patient could close her mouth but still had open-bite syndrome. D This was corrected by a course of orthodontic therapy. Using this combined approach, the tongue and dental functions were preserved and mutilating surgery was avoided. E Follow-up 5 years after the initial embolization. F, G see p. 680

680

13 Cervicofacial Vascular Malformations

Fig. 13.33. (continued) F, G At 27 years of age, the result in this patient was excellent, although she had occasional episodes of moderate swelling

In lymphatic malformations that involve the forehead and eyelid, surgical intervention to open the eye is the treatment of choice, to prevent blindness or amblyopia. Sclerotherapy or intralesional injections are performed in a similar fashion to the treatment of venous malformations. The cystic spaces in lymphatic malformations often do not interconnect, making treatment by injection less effective. In larger compartments, a yellowish, or serosanguinolent fluid is encountered, and a similar volume of ethanol is injected. Microcystic lymphatic malformations are difficult to treat by any means, because of their diffuse nature and infiltration of the tissue layers. The role of sclerotherapy is limited for symptomatic areas of repeated swelling and bleeding (Fig. 13.32). A very important part in the overall management of these children is the need for long-term prophylactic antibiotic therapy that will prevent or ameliorate the repeated infectious episodes. Venolymphatic malformation (hemolymphangiomas) are often located in the tongue, where they provoke macroglossia. The lymphatic character is established from the acute swelling with benign nasosinusal infections, their usual regression, and the residual mucous vesicles. The venous character is expressed by the dark, often black color of the tongue during the crisis and the slightly hemorrhagic aspect of the dry tongue permanently protracted during the swelling episodes (Figs. 13.31, 13.33). To avoid teeth problems, a residual open bite syndrome, and mandible growth difficulties, early embolization is recommended. In our experience, the response of such tongue lesions (and probably only the tongue because of its particular anatomic situation) to transarterial embolization with particles has usually been excellent, with a decrease in the frequency and intensity of swelling or even disappearance. Orthodontic

Idiopathic Facial Vascular (Venous) Dilatations

681

treatment can correct most open bite syndromes resulting from the permanent macroglossia (Fig. 13.33). In some instances, cuneiform glossectomy has been performed following additional embolization to allow the tongue to remain behind the teeth.

13.12 Mixed Vascular Malformations Mixed vascular malformations are quite common. In particular, capillary malformations of the skin are often present in association with deep AVMs or deep lymphatic or venous malformations. Another common combination is that of combined lymphatic and venous malformations. The lymphatic and venous systems develop very closely in time, and it is not unexpected that malformations of both systems co-exist. A diffuse lymphatic malformation is often associated with varicosities of adjacent draining veins. In particular, lymphatic malformations of the head and neck are frequently associated with markedly dilated brachiocephalic veins, and sometimes the superior vena cava. In addition, dysplastic venous channels may co-exist with lymphatic malformations, and hemorrhage into lymphatic cysts, which is relatively frequent and assumed to be caused by communications between the lymphatics and veins.

13.13 Multifocal AVMs There are infrequent cases of locally aggressive, recurrent vascular malformations, associated with de novo appearance of other cutaneous vascular lesions that do not correspond to a specific metameric distribution or genetic disorder. They can be very challenging in their management (Fig. 13.34) and must correspond to an unknown systemic disorder.

13.14 False Maxillofacial Vascular Malformations Vascular malformations should be differentiated from vascular abnormalities and from facial venous dilatations resulting from intracranial vascular lesions or transorbital collateral circulation. This latter concept is sometimes called false craniofacial vascular lesions (Rodesch et al. 1994).

13.14.1 Idiopathic Facial Vascular (Venous) Dilatations

Parents and pediatricians are sometimes concerned about prominent facial veins in infants and young children. Auscultation of the head increases this anxiety if it reveals a cranial pulsatile bruit. In our experience, and according to the literature, such a pulsatile bruit, regardless of whether or not it is associated with facial veins (mainly in the naso-orbital region), is benign and regresses spontaneously; while its frequency is increased up to the age of 3 years and then diminishes (Pruvost et al.

682

13 Cervicofacial Vascular Malformations

Fig. 13.34A–F. Legend see pp. 684

Idiopathic Facial Vascular (Venous) Dilatations

Fig. 13.34G–L. Legend see p. 684

683

684

13 Cervicofacial Vascular Malformations

Fig. 13.34A–N. Complex multifocal aggressive AVM. A A 2-year-old boy, born with a reddish discoloration of the nose, forehead, and left upper lip; at 2 years old the lesion had grown. B, C Frontal and lateral DSA of the distal facial demonstrate a capillary network. D Five days after embolization (PVA and ethanol), there are two small ulcerations. E–G One year later, de novo development of multiple small capillary malformations in the shoulder, axillary region, abdominal area, forearm, and lateral chest skin, not present before, which have remained static, whereas the nose lesion continues to evolve. H Lateral angiogram shows increased flow, with an increase in size from the facial artery, and larger venous lakes. I, J Acrylic cast. K One year later, he developed severe epistaxis, and a large pulsatile varicosity in the nose. Direct puncture before alcohol embolization was chosen. L Two weeks later, he developed necrosis where the varix was. M One month later spontaneous healing. N Final result after surgical removal of the nose and reconstruction

1989). These bruits are rare in neonates. They are likely to be due to blood turbulence in the veins of the maturing skull base. The growing skull base and sinus remodeling can more or less rapidly adapt to the hemodynamic venous conditions of the walking child. These dilated facial veins indicate the early opening of the brain venous outlets into the cavernous sinus (see Chaps. 2, 3, and 10, this volume). When confronted with dilated frontal facial veins associated with an intracranial bruit and without any other clinical manifestation (e.g., macrocrania), we still need to exclude the possibility of an early manifestation of an intracranial AVS.An MRI of the brain in this situation is usually enough to eliminate an AVS or a unilateral dural sinus occlusion (see Chaps. 4, 7, and 10, this volume), and diagnostic angiography is not needed. We have not encountered any AVMs revealed only by an intracranial bruit in the pediatric population in the presence of a normal MRI. Clinical follow-up is mandatory in order to confirm the spontaneous disappearance of the veins and the bruit before the age of 7 years. If the MRI is abnormal, diagnostic angiography should be performed to accurately outline the abnormality.

Facial Venous Dilatation Associated with Intracranial Vascular Lesions

685

13.14.2 Facial Venous Dilatation Associated with Intracranial Vascular Lesions

Under these circumstances, the facial veins provide evidence of important hemodynamic intracranial disorders where the venous blood is rerouted toward the cavernous plexus. During infancy, this becomes a possible outlet for cerebral venous drainage, and the orbit is then an alternative communication passage between the endocranium and the facial veins via the superior ophthalmic vein. Two different situations are associated with transorbital drainage: (1) the brain drains through the orbit, while the intracranial AVS drains separately into the posterior sinuses or (2) the jugular foramen is occluded and both the lesion and the brain compete to drain through the orbit, but often also transcranially across the vault (see Chaps. 2 and 3, this volume). In the former situation, neurocognitive prognosis is excellent, as the brain does not suffer the consequences of the shunt; conversely, in the latter situation, the neurological prognosis is poor and early management is required to avoid seizures, deficits, or hemorrhagic episodes. Regression of these facial veins (false vascular malformations) can only be obtained once the treatment is completed. In some instances, regression is not complete, particularly if the posterior outlets are no longer patent and if the communications across the skull base are insufficient. In certain cases, non-vascular lesions of the craniofacial region can mimic vascular malformations, for example teratoma, cysts, and ectopic choroid plexus.

14 Parachordal Arteriovenous Fistulas (Extracranial and Extraspinal Arteriovenous Fistulas)

14.1

Introduction 687

14.2

Specific Clinical Features 689

14.3

Topographic Approach 696

14.4 Branchial Arteriovenous Shunts 696 14.4.1 Maxillary Artery/Vein Arteriovenous Fistulas 697 14.4.2 Ascending Pharyngeal-Internal Jugular Arteriovenous Fistulas 699 14.5

Vertebro-vertebral Arteriovenous Fistulas 700

14.6

Paraspinal Arteriovenous Fistulas 714

14.7

Technical Management of High-Flow Fistulas 719

14.1 Introduction If we consider the entities extracranial (branchial) arteriovenous fistulas (AVFs) and paraspinal AVFs, at first glance any relation or similarities between them do not easily come to mind, and yet they do exist. There are two possible ways to analyze this issue: we can either consider the differences between both regions and identify what they have in common or look for the similarities. Fortunately, both methods define the same area of pathology. The latter method is more traditional and helps to explain our otherwise unusual grouping of these entities in a single chapter (Table 14.1). The embryonic center of these malformations is the notochord. It ends at the basisphenoid level, where it marks the junction between the somitic part of the branchial region and the prebranchial somitic part. In vascular terms, the rostral limit of the notochord is the cavernous venous plexus with the arterial supply to the region from the maxillary artery branches; it probably also includes the extradural internal carotid artery (ICA). The orbital and transorbital fissure arteries belong to the prebranchial somites. More caudally along the notochord, the segmental arteries and the vertebral venous plexus are more readily recognizable as the vascular component of the spinal notochord. Extracranial branchial and paraspinal AVFs are thus similar in nature, although they are located in different places. Because of the role of the neural crest and mesoderm in the development of the segmental vascularization, the fistulas fed by arteries supplying the craniocervical junction (both the pharyngeal and occipital and the thyro- and costocervical arteries can be included in the maxillary artery group of lesions). The vertebral arteries are intersegmental channels that bridge and link three to eight cervical

688

14 Parachordal Arteriovenous Fistulas (Extracranial and Extraspinal Arteriovenous Fistulas)

Table 14.1. Arteriovenous lesions in children Site

Cephalic

Pial (subpial)

Superficial Deep neural

BAVF BAVS Wyburn-Mason

Choroidal (leptomeningeal

Malformative Mature

Sinusal (dural)

Malformative Dystrophic Angiogenic Osteodural

VGAM Choroidal AV shunt DSM DSAVF DSAVS Cavernous sinus DAVS ECAAVF

Epidural and paraspinal

?

Subdural

–

Peripheral

Bones or superficial covers

Anterior cranial fossa DAVS Maxillofacial

Somitic

SCAVS SCAVS Multimyelomeric SCAVS No equivalent structure No equivalent structure Vertebral AV shunt Vertebrovertebral AVF Paraspinal AVF Spinal DAVS Metameric

Possible age at diagnosis Fetus

Neonate

Infant

Child

– – –

± + –

+ ++ –

++ ++ –

++

++

+

+

– ++ – – –

– +++ + – ±

– ++ ++ – ±

± + ++ + +

– – –

± – –

± + –

++ + –

±

±

+

++

+++, Very frequent; ++, frequent; +, possible; ±, rare; –, not seen; BAVF, brain arteriovenous fistula; BAVS, brain arteriovenous shunt; SCAVF, spinal cord arteriovenous fistula; SCAVS, spinal cord arteriovenous shunt; VGAM, vein of Galen aneurysmal malformation; AVF, arteriovenous fistula; DSM, dural sinus malformation; DSAVF, dural sinus arteriovenous fistula; DAVS, dural arteriovenous shunt; ECA, external carotid artery.

segmental arteries; they are a longitudinal and paraxial structure rather than an axial (metameric) one. With this in mind, the arteriovenous shunts (AVSs) supplied by the vertebral arteries can also be considered as segmental structures. We have therefore included vertebro-vertebral AVFs (VVAVFs) and the occipitovertebral fistulas (OVAVFs) in the group of extracranial and extraspinal AVFs. The most appropriate name for this group is parachordal AVF (Table 14.2). It is of interest to note that there are no other nontraumatic AVFs in the cranial region other than those fed by the metameric arteries (maxillary, ascending pharyngeal, occipital, and vertebral). At the thoracic and lumbar or sacral levels, the paraspinal AVFs are supplied by their respective segmental arteries and located according to the exact site of the shunt, either on the main trunk or on its branches. Intersegmental paraspinal anastomoses will reproduce there what is seen at the cervical level with the vertebral artery. Analysis of the similarities and differences in the venous drainage anatomy is equally enlightening, the key factor in understanding and predicting the clinical manifestations of parachordal AVF (Table 14.3).

Specific Clinical Features

689

Table 14.2. Parachordal arteriovenous fistulas Region Cephalic

Somitic

Maxillary, EJV Ascending pharyngeal, IJV Occipital, C1 vertebral or PJV Occipital, C2 vertebral or PJV Thyrocervical-vertebral or PJV Costocervical-vertebral or PJV Vertebro-vertebral vein Segmental (intercostal, lumbar, sacral), azygos vein

EJV, external jugular vein; IJV, internal jugular vein; PJV, posterior jugular vein.

Table 14.3. Modalities of venous drainage in parachordal arteriovenous fistulas Type of drainage

Veins involved

Centrifugal drainage

Jugular vein (external, posterior, internal) Vertebral vein Azygos vein Cranial sinuses Venous plexuses Cerebropial drainage Radicular vein

Epidural drainage Centripetal drainage

14.2 Specific Clinical Features The role played by the internal jugular vein and the azygos veins as lowresistance outlets may facilitate cardiac overload in some rare cases (Fig. 14.1). Conversely, the high resistance of the posterior external jugular veins, the vertebral veins, and the epidural venous plexuses explains the absence of cardiac symptoms as the clinical presentation of AVFs draining primarily into these systems (Table 14.4). If we consider only the AVFs that are located ventral to the notochord (extracranial and paraspinal), drainage of the AVFs in most cases is centrifugal and seldom epidural.At the spinal level, the AVSs located in the vertebral (nerve) foramen often opacify the epidural channels. Only rarely do branchial AVFs in the vicinity of a skull base foramen reflux toward the intracranial venous channels. From a purely academic point of view, epidural AVSs of the spine and the cavernous plexus (the adult type of dural AVSs; see Vol. 2, Chaps. 8 and 12) could be linked together, both being osteoepidural in location. When looking at the differences in the venous structures of the spine and cranial region, the absence of a dural venous sinus in the former is immediately apparent. Venous sinuses are vascular pathways within the dural sheet and can therefore hardly be considered to be the same entity as venous channels located within the epidural space. The ongoing discussion regarding the cavernous plexus vs the cavernous sinus status must also take into consideration the fact that there are no

690

14 Parachordal Arteriovenous Fistulas (Extracranial and Extraspinal Arteriovenous Fistulas)

Fig. 14.1A–F. Legend see p. 691

▲

Specific Clinical Features

691

Fig. 14.1A–H. A baby boy was found in early infancy to have a supraventricular tachycardia (200/min) and a prominent thoracic bruit. There was no neurological deficit. A–D He was medically treated and underwent cardiac catheterization. No cardiac or aortic abnormality was found, but a thoracic arteriovenous malformation (AVF) was revealed. A definitive spinal and intercostal angiogram was carried out when the patient was 9 months old, showing the fistula just lateral to the left T6–T7 intervertebral foramen with drainage into the ipsilateral intercostal veins (arrow), epidural plexus, and then cranially in the left hemiazygos vein toward the superior vena cava E, F The anterior spinal artery did not participate in vascularization of the lesion. G, H Embolization was performed in the same session and led to complete occlusion of the fistula. The child is normal after 5 years of follow-up

venous dural sinuses at the spinal level and that spinal epidural venous plexuses have the same appearance all along the notochord from the sacrum to the basisphenoid (cavernous venous plexus). These plexuses mainly drain the osseous structures rather than the central nervous system, although radicular veins drain lateral to them at certain levels. The epidural venous channels have mainly axial and longitudinal anastomoses, their venous hemodynamics are without restrictions, which means that they rarely interfere with the pial venous drainage and never with water homeostasis. This indicates that there will be no central nervous system consequences from these fistulas unless there is radicular venous and subsequent spinal cord pial veins reflux. Special locations or anatomic dispositions of the cerebral venous outlets or radicular veins at the level of the shunt may account for the pial venous opacification that is occasionally seen (Fig. 14.2). The usual venous impairment of the brain or cord seen

692

14 Parachordal Arteriovenous Fistulas (Extracranial and Extraspinal Arteriovenous Fistulas)

Table 14.4. Clinical manifestations in parachordal arteriovenous fistulas Manifestation

Mechanisms involved

Congestive cardiac failure

Internal jugular vein drainage Azygos vein drainage Pial venous congestion by epidural hyperpressure Pial venous congestion by pial reflux Compression from epidural venous ectasia Associated myelomeric arteriovenous shunt (Cobb syndrome) Pial reflux Venous infarction Neurofibromatosis type 1 Collagen diseases Rendu-Osler-Weber disease, etc.

Neurological deficits

Hemorrhage Symptoms related to associated tumors or vascular sites in specific etiologies

with intradural or dural AVSs is rarely encountered in parachordal AVFs. Most of these lesions in the pediatric age group are incidentally discovered, while others are lethal and not recognized. The chronic effect of the AVF is mainly expressed on the venous side of the lesion. There is no high-flow arterial angiopathy in the branches supplying the shunt, as the hemodynamic conditions of these segmental arteries are different from those of the central nervous system (cerebral or cervical cord) and the time elapsed is also insufficient. Flow-related aneurysms or arterial stenosis is not seen; on the other hand, venous narrowing, venous pouches, and thrombosis can be demonstrated. The effect of epidural venous congestion on the intradural structures can be seen in rare cases to be caused by direct compression of the enlarged epidural venous channels or by compression of an associated epidural hematomas (Fig. 14.3). If the AVF is part of an underlying vascular dysplasia, then the shunt may not become apparent until adulthood, when arterial changes are one of the characteristics of the disease. Collagen disorders and hereditary hemorrhagic telangiectasia (HHT) (Fig. 14.4), also known as Rendu-Osler-Weber (ROW) disease, may produce parachordal AVFs, and the flow in the former can be high, in particular at the vertebral artery level. However, it should be noted that these two diseases are different, as in collagen disorders there is rupture of a diseased arterial wall into a normal venous plexus, whereas HHT is a malformative disease of the postcapillary venule.

Specific Clinical Features

693

Fig. 14.2A–F. A 10-year-old girl was referred to our institution for investigation of progressive tetraparesis. All that was known of her history was that she had undergone two operations at the age of 5 years for craniosynostosis. When she was 7 years old, she sustained a cranial trauma,which was followed by paraparesis,the latter apparently improving after an operation, but the details of surgery were not known. On examination, she was found to be below the third percentile. Both legs were spastic and bilateral ankle conus was found.Atrophy of the right hand muscle with weakness of extension was noted, as well as a right Horner syndrome. A MRI showed a posteriorly located, right cervical paraspinal arteriovenous malformation (AVM) with B–D abnormal vessels (arrows) extending from the craniocervical junction to the T3 vertebral body (arrow, vertebral body; arrowheads, arterial feeder; open arrow, epidural vein). E Embolization with glue (double arrow) and coils (arrows) excluded the shunt entirely. E, F Follow-up angiography and MRI 1 year later confirmed the quality of the result. The child improved slightly

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Fig. 14.3A–D. Acute onset of neck pain without neurological deficit in a child. MRI (A, B) after surgical biopsy demonstrates intraspinal canal vascular lesion. C, D Angiogram demonstrates epidural fistulous communication

Specific Clinical Features

Fig. 14.4A–C. A 6-month-old girl presented with a sudden onset of intracranial SAH and ventricular hemorrhage (A). Clinical examination found spinal manifestations leading to MRI/MRA diagnosis of SCAVF (B, C). D–F see p. 696

695

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Fig. 14.4D–F. (continued) Angiography demonstrates a large fistula that could not be fully located either epidural or intradural (D–F). The ventral axis was not contributory (D); the oblique views were chosen for embolization projection; the anterior spinal is displaced but not contributing to the lesion. Complete exclusion was obtained. The child remained asymptomatic. Follow-up angiogram confirmed the exclusion of the lesion (not shown)

14.3 Topographic Approach Following the general remarks made above, it is possible to analyze each site as an individual entity, realizing at the same time that they all belong to a single group of AVSs.

14.4 Branchial Arteriovenous Shunts Branchial AVS is the name given to those parachordal AVFs that are fed by branchial arteries. These vessels constitute the arterial supply to the cranial nerves and the brain in some instances; the hazards of embolization of these vessels are thus inherently related to this anatomic coincidence. Two AVFs can be encountered, maxillary and pharyngeal AVFs (often called external carotid-jugular vein fistulas).

Maxillary Artery/Vein Arteriovenous Fistulas

697

14.4.1 Maxillary Artery/Vein Arteriovenous Fistulas

Maxillary artery/vein AVFs (Figs. 14.5) are often discovered by the mother of a child when she hears a noise while kissing or hugging the child. We have not observed a symptomatic bruit in a child, which suggests the early development of the shunt and its integration into the overall acoustic environment of the child. In other cases, the interference of the bruit with hearing and subsequent difficulties at school leads to clinical examination and diagnosis. No cardiac overload has been noted in this group, nor have any children presented with epistaxis or cranial nerve involvement, although this would be conceivable in this topography. No pain is experienced, and the only specific sign related to this location is the slowly expanding pulsatile mass in the parotid region, corresponding to the bulging maxillary veins. The clinical diagnosis and management strategy are simple at this stage. Following discussion with the child and the parents, selective transarterial angiography is performed with endovascular treatment during the same sitting. In most instances, the fistula is located at the origin of the middle meningeal or accessory meningeal artery and rarely on the distal maxillary artery (Kim et al. 2003). This region corresponds to the annexation zone of the stapedial artery by the ventral pharyngeal system (see Vol. 1, Chap. 5). The flow is usually high, and the exact location of the fistulous point is often better assessed by selective injection of the adjacent arteries in the region. Most descriptions in the literature limit the analysis of the feeder to the maxillary trunk and refer to them as external carotid AVFs, ignoring the branchial nature of the shunt. Careful assessment of the branch involved is important, and the patency of the trunk should be preserved if possible. Occlusion of the maxillary and proximal middle meningeal artery may have no immediate clinical consequences, but patency of the cranial segmental arteries should be maintained whenever possible, as these arteries provide the primary source for collateral circulation to the brain in ICA occlusive disease. These AVFs drain into the maxillary vein (rather than the pterygoid venous plexus) and secondarily into the external jugular vein. Kinking at the various maxillofacial space boundaries may produce rerouting of drainage (Fig. 14.6). The large communications of the maxillary vein and the pterygoid venous plexus can cause interference with intracranial venous drainage. However, retrograde opacification of the cavernous venous plexus with drainage toward the ophthalmic vein or superior petrosal sinus is rarely seen, but might result in regional venous congestion. Early recruitment of such a venous pathway and its persistence over time may interfere with the remodeling of the cerebral veins. Since the skull base growth is not compromised by the AVF, cavernous capture of cerebral veins can occur. If, on the other hand, venous congestion is present before this capture takes place, a pial venous collateral appearance on the cortex will be seen. In our experience, such changes are not immediately symptomatic, but such subacute or chronic venous ischemia may in time lead to mental retardation or seizures if alternative pathways for cerebral drainage are insufficient. If congestion occurs after the cavernous capture of the cerebral veins, pial reflux from the drainage of the extracranial shunt can be seen. This arrangement is more likely to be encountered in adult extracranial AVFs (Sedat et al. 1999). Risk of intracranial hemorrhage and neurological deficit should then be anticipated.

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Fig. 14.5A–D. A 3-year-old baby girl with no particular clinical history presented with a continuous bruit and thrill in the left maxillary and parotid region. The child thrived normally. The chest X-ray showed a moderate cardiomegaly. No cardiac failure was found. A, B Angiography was performed and revealed a high-flow arteriovenous fistula (AVF), the transverse facial artery draining into the external jugular system and the endocranium through the veins of the foramen ovale, the posterior fossa, the tentorial sinus, and the lateral sinus homolaterally. C Embolization was performed with glue. D A cerebral venous congestion was then found, giving rise to the pseudophlebitic appearance of the frontal veins

Ascending Pharyngeal-Internal Jugular Arteriovenous Fistulas

699

Fig. 14.6A–D. A 9-year-old boy presented with a right-sided retromandibular pulsatile mass in relation to a direct maxillary-jugular vein fistula (A). Embolization was performed in the same session with detachable balloon (B)

14.4.2 Ascending Pharyngeal-Internal Jugular Arteriovenous Fistulas

We have not encountered an ascending pharyngeal-internal jugular AVF in the pediatric age group, but we have seen one in a young adult (Fig. 14.7); however, there is no reason why such an AVF should not be found in a younger age group. Symptoms include a bruit, and this complaint in the pediatric population depends on its change over time and the onset of the lesion before or after the establishment of the child’s acoustic environment. Cranial nerve (IX, X, XI, XII) impairment can theoretically be encountered. In adults, the mechanism of the impairment is unclear, but must be related to arterial or venous ischemia rather than mechanical compression. The shunts we have seen in children opened immediately into the jugular vein at the jugular foramen without reflux in the intracranial sinuses. The absence of secondary effect on the cerebral veins suggests the moderate impact of the shunt on the drainage of the brain or its late occurrence with regard to skull base growth, reducing the chance of retrograde congestion affecting the pial venous remodeling process. Similar to what we have seen in neonatal patients with paraspinal AVF, a high-flow lesion in this topography should produce systemic manifestations, as it opens into a low-resistance system (internal jugular vein). Its predictable natural history might be that of a high-flow dural sinus AVS (infantile type; see Chap. 4, this volume).

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Fig. 14.7. A Spontaneous pharyngojugular arteriovenous fistula (AVF). B Embolization with glue

In the head and neck region, the clinical symptoms will exclusively depend not on the site of the arteriovenous communication, but rather on the venous drainage of the AVF. Specific symptoms such as cardiac overload in the pediatric population (Tekkok et al. 1992) or epistaxis (Reinhoff 1924) have been described, but they are rare. Spontaneous AVFs of the extracranial carotid system are infrequent in general and even more so in children (Sedat et al. 1999).

14.5 Vertebro-vertebral Arteriovenous Fistulas Vertebro-vertebral alteriovenous fisula (VVAVF) is a generic name covering various types of diseases that involve the vertebral arteries and veins.A clear distinction should be made between the AVFs that we describe and traumatic AV communications, the majority of cases reported in the literature. A separate group is made up of dysplastic vessels, which rupture spontaneously or following minimal injury.Although they are not described in the pediatric population, they have been encountered in young adults with collagen type III diseases (Elhers-Danlos IV) and neurofibromatosis type 1. This type of situation requires careful management of these patients because any vessel manipulation in arterial vessel wall disease may lead to further vascular damage. Simple ligation or proximal embolization of the feeding vessel carries the risk of recurrence due to the vast collateral network in the head and neck. Endovascular treatment of these AVFs has been accepted now as the treatment of choice for these lesions. It offers a very high rate of cure with low morbidity. The goal of treatment is to occlude specifically the fistulous communication with preservation, if possible, of the parent artery.

Vertebro-vertebral Arteriovenous Fistulas

701

Fig. 14.8A–F. A 10-year-old boy presented with a cervical bruit and thrill discovered incidentally. Neurological examination was considered normal with no focal deficits. Chest X-ray revealed an enlargement of the cardiac silhouette. Angiography confirmed a right vertebro-vertebral fistula. A Ipsilateral vertebral atrophy. B, C Contralateral supply. D–F Complete occlusion was obtained with balloons and glue. E,F see p. 702

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14 Parachordal Arteriovenous Fistulas (Extracranial and Extraspinal Arteriovenous Fistulas)

Fig. 14.8E,F. Legend see p. 701

An upper and a lower cervical group can be distinguished within the VVAVF group. In an unpublished series from Lariboisière Hospital (Vinchon 1992) from 1951 to 1991, six pediatric cases were seen; all were spontaneous, three at C1–C2 and three at C6. All but one was embolized. Upper VVAVFs (Fig. 14.8) are shunts developing at the C1–C2 level. The specific segmental nature of the vertebral artery at C1 explains its role at that level. The role of the occipital artery in the supply to the AVF depends on the anatomic balance between the occipital and vertebral sources (Moret et al. 1979). Pure VVAVFs or pure occipitovertebral vein AVFs can be seen, in addition to all the intermediate stages, and if the shunt is located at C2 the same rules apply (Goyal et al. 1999b). Venous drainage of the AVF uses the suboccipital and vertebral network. Congestion of the posterior jugular vein as well as a bruit and a soft posterior pulsatile mass are the usual symptoms of such fistulas. Although there is often a retrograde flow down the basilar artery and into the ipsilateral distal vertebral artery segment (Fig. 14.8), we have not observed symptoms that would correspond to a posterior fossa steal type of syndrome. On the other hand, inadvertent occlusion of the ipsilateral vertebral artery proximal to the shunt would immediately produce major neurological symptoms. Ling (2005) reported the case of a 2-week-old boy who presented with congestive heart failure. Neck bruit and thrill suggested the presence of high-flow AV shunt in the right side of the neck. CT and MR imaging disclosed enlarged bilateral vertebral arteries and a large paravertebral venous pouch, suggesting a single right-sided VVF. Enlarged epidural venous plexuses and potential reflux into the perimedullary

Vertebro-vertebral Arteriovenous Fistulas

703

veins were looked for. Because the symptoms of heart failure were mild, endovascular treatment could be delayed until the patient was several weeks older. Genetic examinations showed no definite abnormality, and no angiogram was done at that time. At 12 weeks of age, endovascular embolization of the right VVF was performed. Bilateral vertebral angiograms showed a single fistula located at the C1 level with very poor filling of the basilar artery. Retrograde catheterization of the distal right vertebral artery was performed using a 1.8F microcatheter through the guiding catheter placed in the left vertebral artery. The distal right vertebral artery entrance into the fistula was embolized with NBCA and tantalum diluted with lipiodol (mixture, 90% glue). Then the proximal portion of the fistula was also embolized in the same manner via a microcatheter introduced antegradely in the right vertebral artery. Postembolization vertebral angiograms showed successful occlusion of the fistula with antegrade filling of the basilar artery (Fig. 14.9). The postoperative course demonstrated immediate improvement of congestive heart failure with stable clinical result at 2 months follow-up. We have only once seen pial venous reflux in this location (high VVAVF), yet the drainage extended caudally all the way to C6 before refluxing into a radicular vein, and an intradural hemorrhagic complication could therefore be expected to occur (Kominami et al. 1996) (Fig. 14.10). This should be kept in mind when considering the various treatment options. Although a perfusion pressure breakthrough phenomenon in this type of lesion was once suspected and is frequently referred to, we have never encountered such a phenomenon in more than 20 years of experience with abrupt obliteration of AVFs in children (and adults). Theoretically, spinal cord symptoms might occur if the lateral spinal artery or a duplicated vertebral channel at C2 was present, but in our experience neurological manifestations are rare; they occur in unusual anatomic circumstances or as a consequence of venous drainage specificities. Understanding the clinical correlations depends on the anatomic knowledge of the operator, as does the capacity to predict the natural history. The exact location of the AVF on the segmental part of the artery (Fig. 14.8) or its intersegmental course may have an impact on the potential to preserve (or not) the patency of the vertebral artery. Intersegmental VVAVF constitutes a rupture of the vertebral continuity, and the vertebral axis may not be preserved unless the hole is small and the embolic agent can be deposited completely in the venous chamber only (Fig. 14.11). In contrast, a segmental VVAVF is a rupture of continuity in a vertebral artery branch, and in this situation the vertebral artery can more easily be preserved, even with large venous pouches (Fig. 14.8). A particular type of fistula is VVAVF at C1, distal to the occipital artery anastomosis, where the vertebral artery is no longer an intersegmental channel. In this location, the VVAVF is necessarily segmental and it is thus almost impossible to preserve the vertebral artery. The ipsilateral vertebral flow sometimes uses an intradural duplication at C2 that by-

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14 Parachordal Arteriovenous Fistulas (Extracranial and Extraspinal Arteriovenous Fistulas)

Fig. 14.9A–F. Legend see p. 705

▲

Vertebro-vertebral Arteriovenous Fistulas

705

Fig. 14.9A–H. Neonate developed mild to moderate CHF during the 1st week of life managed with medication. Initially diagnosed as possible epidural AVF not draining via radicular vein to perimedullary venous plexus reflux and therefore at no demonstrated risk for immediate intradural complications. Enhanced CT and MRI were performed during the 1st week of life (A–C). Angiography and embolization performed at 12 weeks of age (D, E). Right VVF was demonstrated and treated at 12 weeks with glue via contralateral and ipsilateral vertebral arterial systems (F–H), with good results for a lasting correction of the CCF

passes the damaged segment, but most frequently the prominent flow to the fistula crosses the midline and retrogradely fills the distal vertebral segment without constraint from the ectatic veins within its bony canal. Conversely, the ipsilateral vertebral artery is often compressed into the canal to the extent that, following occlusion of the AVF, it appears to be hypotrophic. A sump effect on all the segmental arteries in the vicinity of the AVF will eventually opacify the shunt without constituting its direct supply. The ascending pharyngeal and costocervical arteries are most frequently involved in this process. They also represent alternative pathways to the VVAVF or occipitovertebral AVF if the shunt is improperly treated. These alternative contributions should not be considered and treated as direct feeders, but as secondarily opened channels that will spontaneously regress after closure of the shunt itself. In some rare instances, an occipitovenous AVF opens into an emissary vein or into the suboccipital venous plexus (Gupta 1993). These occipitovertebral vein or suboccipital vein AVFs should not be confused with the DSMs in young children that involve the mastoid branch from a nonmetameric portion of the occipital artery opening into a distally occluded sigmoid sinus (see Chap. 7, this volume).

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Fig. 14.10A–F. An 11-year-old boy presented sudden onset of headaches and torticollis in relation to SAH. CT confirms the SAH (A) and MRI suggests spinal cord lesion (B). Angiography demonstrates a VVF draining caudally into the vertebral vein and refluxing in the spinal cord venous system at C5 (C, D). Immediate balloon treatment is carried out with successful exclusion of the VVF (E, F)

Vertebro-vertebral Arteriovenous Fistulas

Fig. 14.11A–E. A 6-year-old boy who had had an enlargement of the cardiac silhouette since the age of 4 years that was not treated by any medical therapy. A loud cervical bruit could be heard. A Typical C1–C2 vertebro-vertebral fistula (arrow; double arrow, venous drainage). B This was treated with a detachable balloon (asterisk) with vertebral preservation C–E Patient with a similar case history with ipsilateral vertebral hypogenesis and balloon (no. 16 gold valve) embolization via the opposite vertebral artery, across the midline; the ipsilateral vertebral artery, although small, was no longer patent. E see p. 708

707

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14 Parachordal Arteriovenous Fistulas (Extracranial and Extraspinal Arteriovenous Fistulas)

Fig. 14.11E. Legend see p. 707

Lower cervical VVAVFs are different from upper VVAVFs. They involve the cervical arteries, are less frequent and are usually of the slow-flow type. The enlarged dural lakes may create spinal cord symptoms, as seen in the adult population (Willinski et al. 1990c; Goyal et al. 1999a, b). Arterial steal to the cord is improbable when considering the amount of segmental supply to the cervical spinal cord at that level; however, this mechanism has been proposed to explain central nervous system manifestations in VVAVFs. Mechanical compressions in the intervertebral foramen can be seen with radiculopathies. These fistulas are most often located at the vertebral canal level and, in contrast to their upper cervical counterparts, they drain into the epidural space, where they can produce large epidural lakes bulging into the spinal canal and can compress the cord (Figs. 14.12, 14.13). Response to transarterial embolization can be spectacular, but if the shunt is not completely obliterated clinical improvement may be temporary. Under these circumstances, a transvenous approach has been proposed (Willinsky et al. 1990a). Local opening of a radicular vein may produce medullary venous reflux and the possibility of neurological manifestations, hemorrhage, ischemia, or atrophic changes (Berenstein 1992; Glasser 1993). The anatomy and pathophysiology of symptoms in this location are the same as those in paraspinal AVFs (Table 14.4; Figs. 14.12, 14.13). Low cervical epidural AVMs or AVFs are infrequent in children and in adults. Their angioarchitecture is difficult to analyze, as the flow is centrifugal and therefore high. Reflux into the radicular veins and secondar-

Vertebro-vertebral Arteriovenous Fistulas

709

Fig. 14.12A–E. A young female patient presenting with acute neck pain and stiffness and meningeal signs due to subarachnoid hemorrhage. No focal neurological signs were found. A, B MRI and C, D angiography demonstrated a low vertebro-vertebral fistula with epidural drainage and intradural venous ectasia. E Complete and stable occlusion was achieved at 1 year

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14 Parachordal Arteriovenous Fistulas (Extracranial and Extraspinal Arteriovenous Fistulas)

Fig. 14.13A–D. Legend see p. 711

▲

Vertebro-vertebral Arteriovenous Fistulas

711

Fig. 14.13A–L. At 3 months of age, difficulties in moving the distal right upper limb were noted. No abnormal movement. Brachial plexus paralysis after delivery was diagnosed. MR shows a vascular lesion at the spinal cord level with intramedullary edema. A, B Angiography diagnosed an intramedullary arteriovenous malformation with the nidus at C6–C7. The clinical situation was stable, the angiography was done at 11 months and shows paraspinal lesion draining into the intradural veins and supply via the epidural artery from both sides (C, D). Distal catheterization of the right and left feeders makes it possible to embolize the entire epidural lesion (E, F).An associated lesion involving the C5 root and adjacent muscle (G–I) is embolized secondarily. The previously displaced ASA (J) is now straight (K) and the venous drainage (L) uses the ventral vein. M,N see p. 712

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14 Parachordal Arteriovenous Fistulas (Extracranial and Extraspinal Arteriovenous Fistulas)

Fig. 14.13M,N. (continued) The child is neurologically normal and the MRI is normalized (M, N)

ily into the pial spinal cord venous plexus will lead to neurological manifestations or hemorrhagic episodes (Fig. 14.13). These lesions do not resemble the dural shunts in adults and are often mistaken for a SCAVM on MRI or even angiography if improperly analyzed. Their treatment is often straightforward, as the involved epidural contributors and their fistulous nature are favorable for glue or distal coil deposition. The clinical results in the few cases managed were excellent. Epidural and paraspinal capillary proliferation has been seen once in an infant with an excellent clinical result after microparticle embolization, suggesting the diagnosis of a benign capillary hemangiomatous lesion (Fig. 14.14).

Vertebro-vertebral Arteriovenous Fistulas

Fig. 14.14A–D. A 7-month-old girl who had had difficulty in swallowing ever since birth. At presentation, she was found to have an hemangioma on the right side of her neck. She was otherwise well. No neurological deficit was found, but there was sphincter laxity and cardiovascular abnormality. A, B MRI showed a large mass in the larynx and pharynx (arrows) that extended posteriorly into the epidural space (arrowheads). C, D These findings were confirmed by angiography; dark arrows, anterior spinal artery; open arrows, venous drainage. E see p. 714

713

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14 Parachordal Arteriovenous Fistulas (Extracranial and Extraspinal Arteriovenous Fistulas)

Fig. 14.14E. (continued) E One year after complete embolization, most of the mass had shrunk. There was no residual vascularization to the lesion

14.6 Paraspinal Arteriovenous Fistulas When looking at the anatomy of the spinal cord arteries and their spinal sources of supply, all the possible segmental paraspinal AVF locations can be anticipated. Paraxial longitudinal spinal arterial anastomoses may also be the site of the fistula; the amount of apparent supply to the shunt depends upon the type of artery involved and the individual anatomy. In general, indirect opacification of the AVF is noted following injection of the adjacent segmental arteries. The options for drainage follow the same general rules as in the other site. However, epidural reflux and some pial involvement appear to be more frequent. The direct opening of the ventrally located fistulas into the azygos vein or affluent may cause cardiac overload (Fig. 14.1). In our experience, this has never led to multiorgan failure, nor has it required emergency management. The supply to the cord prior to occlusion of the fistula must be carefully established. The prominent flow into the shunt may preclude the opacification of a radiculomedullary artery originating at the same level, and blind embolization in this case would carry the risk of major spinal cord arterial complication. With the same condition in an adult, we have seen another contributor to the ventral arterial axis of the cord opacify the AVF, a few metameres above the paraspinal lesion, via the cord, suggesting a possible arterial steal. The clinical significance of such a finding is difficult to establish, as epidural lakes were also present and might explain the cord symptoms (Goyal et al. 1999a). These thoracolumbar paraspinal AVFs are even rarer than the more rostral branchial locations both in adults and in the pediatric population. Symptoms are minimal, and the clinical symptoms appear to occur later than the probable onset of the disease itself. Progressive medullary symptoms are usually noted. Several vascular features may result in symptoms in the thora-

Paraspinal Arteriovenous Fistulas

715

Fig. 14.15A–D. SAMS 17–18. An 11-year-old girl with a previous medical history who had undergone surgery at the age of 11 months. Slight asymmetrical paraparesis (left greater than right). Progressive worsening for 3 years with low thoracic level. Note the large paraspinal and peripheral arteriovenous (AV) shunt on angiography (A, B) and MRI (C, D). E, F see p. 716

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Fig. 14.15. (continued) E, F In addition, a spinal cord AV malformation was seen at the corresponding myelomeric level. Large epidural lakes were also found

Fig. 14.16A, B. Paravertebral AVF (A) draining toward an obstructed epidural vein led to a large epidural intraspinal venous mass (B)

Paraspinal Arteriovenous Fistulas

717

Fig. 14.17A–C. Acute neurological deficit in a child caused by epidural hematoma seen on MRI (A). Cervical angiography shows the area of shunting and epidural venous filling (B, C)

columbar AVF (Table 14.4). All these different mechanisms justify a thorough analysis of all the adjacent arteries in order to choose the best possible route to reach the fistulous point. Demonstration of the supply and drainage of the cord outlines the possible interference of the lesion with the central nervous vascularization (Figs. 14.1, 14.13). In all cases of paraspinal AVF, an associated spinal cord AVS or SAMS (spinal arteriovenous metameric syndrome) should be suspected (Fig. 14.15) (see Chap. 15, this volume); this type of association is more frequent in the pediatric population than was previously thought. The poor reputation of spinal cord angiography and its perceived difficulty in children in the past perhaps account for some of this lack of knowledge and understanding of these associations. Epidural AVMs or AVFs can also be seen at the thoracolumbar level. The latter are associated with large venous pouches and suggest HHT lesions in the youngest children (Figs. 14.4, 14.16). They manifest with transdural compression of the cord and nerve roots, or retrograde spinal cord vein congestion. As seen at the low cervical spine level, the diagnosis is often that of SCAVM after MRI and MRA. Epidural AV lesions have

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14 Parachordal Arteriovenous Fistulas (Extracranial and Extraspinal Arteriovenous Fistulas)

Fig. 14.18A–C. Retrograde venous reflux toward flank hemangioma (A) from paraspinal AVF with epidural venous drainage (B, C)

Technical Management of High-Flow Fistulas

719

also been responsible for compressive hematomas. These lesions are rare and the angiographic studies for spontaneous epidural hematomas in adults and children are most often negative. Yet, from this experience, we would be more inclined to explore by angiography an epidural hematoma in a child than in an adult (Figs. 14.16, 14.17). In one case, a cutaneous hemangioma of the lower part of the abdomen was associated with an epidural fistula with a large venous lake thought to be epidural. No obvious relation between the two lesions was found (Fig. 14.18). In some metameric lesions, the paraspinal or the epidural component of the lesion is clinically dominant. A careful search for a spinal cord-associated lesion in the corresponding myelomere should be made every time associated paraspinal and epidural lesions are demonstrated or if MRI screening is suspicious. It should be remembered that small ventral SCAVMs will be MRI-occult.

14.7 Technical Management of High-Flow Fistulas The objective of treatment of parachordal AVFs is the occlusion of the AVS, with preservation of the parent artery and contributors to the supply of neural structures. In our experience, this can be achieved with glue, balloons and, in some cases, in combination with coils. The two former agents are always considered first because of the quality and stability of the result that can be achieved and the significantly lower costs; it does of course require special expertise to use these materials safely. The femoral route is always used with a 4F sheath in babies and a 5F or 6F sheath in older children. In very young children, the 4F approach offers the possibility of using glue, a latex balloon (gold valve no. 16,) with the preloaded technique or any other catheter with a 4F thin-wall system. Flow-guided catheters with over-the-wire capacities can be used through a 4F sheath without a guiding catheter, to deliver glue in high-flow lesions or coils at the fistulous sites. The same tools are used even more easily through a larger femoral port of entry, and so far we have never had to perform a cut-down or a venous approach to achieve occlusion of these fistulas. We perform spinal angiography under general anesthesia and place great emphasis on careful analysis of the angioanatomy and lesion architecture.At the spinal level, embolization may not be done in the same session as the diagnostic angiographic study, since the number of vessels catheterized tends to be high. The embolization plan is therefore established after the diagnostic procedure, and the intervention subsequently performed under general anesthesia without functional testing. Decreased arterial blood pressure during the procedure can be helpful in some rare instances before using pure N-butyl cyanoacrylate (NBCA). Coils can be used in some cases, as an adjunct to NBCA or detachable balloon occlusion or as the sole agent in AVFs. Particle embolization has no place in the treatment of parachordal AVFs. Steroids and analgesic medication are only given when a radicular branch supplying the muscle territory has been embolized together with the AVS. A cervical collar is applied for 2–3 days after balloon detachment at the upper cervical spine level to prevent mobilization of the balloon during cervical rotations.

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14 Parachordal Arteriovenous Fistulas (Extracranial and Extraspinal Arteriovenous Fistulas)

Pain symptoms, when present, are always associated with embolization of normal arterial branches and their territories. Radicular pain, muscular pain, and trismus are possible side effects that can occur if not only the AVF is occluded, but instead embolization also includes supply toward healthy adjacent territories. Pain symptoms should not occur if the occlusion is strictly limited to the venous side of the fistula. We have not observed postembolization swelling of the fistula, but extensive thrombosis of the previously draining pouches could theoretically give rise to the phlebitic type of symptoms. Immediate shrinkage of the epidural pouches is usually observed, with relief of the pressure on the cord and rapid improvement in the clinical symptoms; however, the longstanding effect of the disease may result in incomplete clinical improvement. Low-dose heparin is recommended if restriction of the venous outlets of the cord is noted and pial drainage of the fistula is suddenly interrupted following complete or almost complete occlusion of the AVF. Although morbidity can theoretically exist, we have had no neurological complications in our personal experience in the treatment of parachordal AVF. A temporary pain syndrome and trismus were noted in a child with a maxillary AVF previously treated incompletely with coils (and subsequently occluded with glue). No mortality has occurred in our experience. Direct puncture (Gobin et al. 1993) of the venous drainage of these fistulas has been proposed as an alternative approach. Such extremely hazardous techniques cannot be done without arterial control, and we do not recommend it in general, and particularly not in children. Proper management via the arterial route as a primary approach should obviate the need for this approach. In those cases in which a modified supply has occurred following failed transarterial embolization, the transvenous approach may become the most favorable one. In some instances, we have been involved in tertiary management of failed arterial and venous approaches following ineffective complex and hazardous procedures, but we have not encountered a situation in which direct surgical or radiation therapy could offer an alternative as a treatment of this condition.

15 Spinal Cord Arteriovenous Malformations

15.1

Introduction 721

15.2

Classification 722

15.3

Natural History and Clinical Aspects 737

15.4

Neonatal and Infants 737

15.5

Children Over 2 Years of Age 743

15.6

Diagnosis 750

15.7

Angioarchitecture 750

15.8

Treatment 758

15.8.1 Therapeutic Abstention 758 15.8.2 Embolization 759 15.8.3 Results 761

15.1 Introduction In line with our previous review of spinal arteriovenous shunts (Berenstein and Lasjaunias 1992b; Rodesch et al. 2002, 2003, 2004), we define them according to the anatomic space in which they are found (subpial, dural, extradural; see Vol. 2). This distinction, based on the anatomic space involved, correlates with the various pathological entities encountered: subpial and spinal cord arteriovenous malformations (SCAVMs), dural and dural arteriovenous shunts (DAVSs) embedded in the dural sheet and draining into spinal cord veins (Kendall 1977; Merland 1980), and extradural and paraspinal arteriovenous shunts (PSAVSs) (Hui et al. 1994; Goyal et al. 1999a, b). They all can lead to neurological symptoms through various physiopathological mechanisms such as venous congestion, venous compression, arterial steal, and in exceptional cases SAH (Hui et al. 1994; Ling et al. 2005; see Chap. 14, this volume). SCAVMs are rare lesions accounting for only one-tenth of central nervous system AVMs in all age groups in the Caucasian population (Cogen and Stein 1983). This number varies significantly in the literature, as failure to distinguish dural from cord AVSs has persisted long enough to bias most historical reviews on the subject. In our series in children, SCAVMs accounted for 5% of the overall group of central nervous system AVSs; however, if one considers the subpial group alone (excluding vein of Galen aneurysmal malformations,VGAMs), the number has risen to above 10% since 1982.

722

15 Spinal Cord Arteriovenous Malformations

Most SCAVMs become symptomatic during the second or third decade of life (Berenstein and Lasjaunias 1992b). They are seldom diagnosed in the pediatric population (Yasargil et al. 1984; Rodesch et al. 1995, 2002, 2004; Cullen et al. 2005; Ling et al. 2005). According to Djindjian (1978), the symptoms start at the pediatric age in 57% of cervical and in 50% of thoracolumbar lesions seen in adults, and in 6% in our current series during the first 2 years of life (Cullen et al. 2005). The pediatric series of SCAVMs reported are in fact most often regroupings of patients whose signs began during childhood, but whose lesions were not recognized until adulthood (Riché et al. 1982). The results presented may confuse what is postulated to be the earliest expression of a undiagnosed SCAVMs, with a clinical episode that could trigger secondary development of an arteriovenous lesion (see Chap. 11, this volume).

15.2 Classification We have classified (see Vol. 2, Chap. 11) spinal cord arteriovenous shunts in children into two distinct groups: 1. Niduses (Fig. 15.1), where an abnormal network is interposed between arteries and veins (SCAVMs) 2. Fistulas (Fig. 15.2), where a direct communication is seen between an artery and a vein (SCAVFs) Although both types of lesions are found in the subpial space (Nicholas and Weller 1988; Hassler et al. 1989; Maillot 1996), niduses may be buried partially or totally in the spinal cord itself. Conversely, large arteriovenous fistulas (AVFs) always remain superficial to the cord (Berenstein and Lasjaunias 1992b; Lasjaunias et al. 2000; Rodesch et al. 2002), as in the rest of the central nervous system, and can probably even be located in the subarachnoid space. The ventrally located fistulas, however, are deeper in the ventral sulcus, within the subpial space, mimicking intramedullary fistulas. The venous drainage is likely to interfere with the intrinsic venous network in both nidus and ventral AVFs; however, dorsal AVFs rapidly create congestion of the entire subarachnoid venous system and eventually produce similar effects, although often remote from the AVF site. Classification of SCAVMs according to their supply (anterior or posterior spinal, and mixed) is like classifying brain AVSs into their various vascularization types (anterior, middle, posterior cerebral, and mixed) or maxillofacial (e.g., internal maxillary, facial) AVSs. Complex classifications with various subtypes have not been used in adults or children, as they shed no light on disease management and postulate that all abnormal vessels demonstrated have the same malformative significance. In our experience, type III malformations (Di Chiro 1971, 1973; Aminoff et al. 1988; Anson and Spetzler 1992) are less typical of the pediatric or young adult population than type IV SCAVMs (Heros 1986; Barrow 1994).

Classification

723

Fig. 15.1A–C. A 12-year-old girl presented with acute posthemorrhagic tetraplegia (A). Satisfactory spontaneous recovery occurred. In order to prevent further acute episodes, in 1982 it was decided to reduce the lesion with particle embolization (B). Although some recanalization was noted 2 years later (C), no symptoms appeared. She lives a normal professional and personal life with 20 years follow-up

These detailed classifications established in adults mix inborn and acquired features: the suspected original defect and the secondary angiopathic changes induced by the hemodynamic condition, the various ischemic or hemorrhagic episodes.

724

15 Spinal Cord Arteriovenous Malformations

Fig. 15.2A–E. Legend see p. 725

▲

Classification

Fig. 15.3A–C. SAMS 10. A 9-year-old boy with progressive paraparetic symptoms associated with hematomyelia. A–C Typical aspect of SAMS 10 with Th2 vertebral and soft-tissue involvement and corresponding myelomeric location

725

Fig. 15.2A–E. A 4-year-old boy presented with permanent and severe paraparesis noted since the neonatal period. Sphincter problems were also found on neurological examination. Mild cardiac failure was found, which was medically treated. A A singlehole fistula developed from the anterior spinal artery at the conus level. B–E Most radiculopial afferents to the basket filled the fistula. The rotation and mass effect exerted on the cord made anatomic identification of the various feeders difficult

726

15 Spinal Cord Arteriovenous Malformations

Halbach et al. (1993) reported ten cases of intradural perimedullary giant SCAVFs, five of which were in children younger than 13 years, and the same observation was made in the Rodesch series where he distinguished micro- from macro-AVFs (Rodesch et al. 2004). They can secondarily be listed according to their cord level, their revealing symptoms, their angioarchitecture, and the treatment chosen. Yet we would recommend the use of a myelomeric type of segmental location of the lesion for better understanding of the symptoms and various associations (Matsumaru et al. 1999). Most spinal cord AVSs in all age groups are single; however, 28% (Berenstein 1992) can be associated with some type of dysplasia: cutaneous vascular malformation, vertebral body vascular lesion, Cobb syndrome (skin, vertebrae, cord involvement at the same segment; see Figs. 15.3, 15.4) described today as SAMSs (see Vol. 2, Chap. 11). In 9% of cases, hereditary hemorrhagic telangiectasia (HHT) (Rendu-Osler-Weber) disease and a high-flow type (Fig. 15.5) were noted, and in 5% Klippel-Trenaunay syndrome (part of the SAMS group) (Fig. 15.6). No clear reference was made concerning the age of onset, diagnosis, or treatment; nevertheless, Berenstein pointed out the very high number of associated vascular anomalies in spinal cord AVMs. In Van Halbach’s series, twofifths had HHT and one-fifth SAMS (Halbach et al. 1993). Such numbers must be taken as an approximation, since current imaging advances allow a more complete diagnosis with noninvasive techniques. This stresses the need to explore all SCAVMs as a potential metameric or systemic alteration. Reciprocally, it certainly warrants the use of MRI as a screening modality when a peripheral vascular anomaly is found. Associated SCAVMs and cavernomas have not been reported. Multifocal SCAVMs are rare. Meisel et al. (1995) (Fig. 15.7) reported single cases of multifocal spinal cord lesions (bifocal SCAVM and bifocal SAMS) in young adults. The association of a SCAVM and a cerebral AVM is exceptional (Fig. 15.8) and does not justify the systematic search for this association when either diagnosis is made (Mazighi et al. 2000). Yet both of these cases in our series were symptomatic before 2 years of age, suggesting the value of screening at that age. None of the multifocal cord lesions was associated with HHT; local mutifocality is often seen in ruptured SCAVMs (Fig. 15.7). Radicular AVSs are exceptional in this population group. The angioarchitectural appearance suggests a malformative AV sleeve around a nerve root (Fig. 15.9), which may correspond to congested radicular venules accompanying the spinal nerve. In case of associated nerve root lesion, the SCAVM has to be considered as a SAMS (Fig. 15.9). It should be pointed out that the subarachnoid location is also typical of the SAMS and CAMS 3 (Wong et al. 2003). As described in Chap. 2 of this volume for other AVMs, the spinal cord site is not an exception in the discussion of the congenital nature and postnatal development of SCAVM. However, as seen for other AVSs, careful analysis of the angioarchitecture points to the responses of the host in terms of individual biological susceptibility, age group vulnerability, and duration of stress triggers. The predominance of fistulas in children and in infants is similar to what has been described in Chap. 3 with pial CAVF.

Classification

Fig. 15.4A–C. A 3-year-old boy presenting with caudal cord AVM with a foot AVM: SAMS 26. (Courtesy of R. Piske)

727

728

15 Spinal Cord Arteriovenous Malformations

Fig. 15.5A–D. Legend see p. 729

▲

Classification

729

Fig. 15.5A–H. A 14-year-old boy presenting with acute abdominal and dorsal pain associated with neck stiffness. A lumbar puncture was performed and showed hemorrhagic cerebrospinal fluid (CSF). Neurological examination was normal, except for spasticity of both lower limbs of long duration. A MRI of the thoracolumbar junction was suggestive of large vascular channels (short arrows). B Selective injection into the right T9 intercostal artery showed the anterior spinal axis. Its descending branch (large arrow) reached the basket (curved white arrow) and opacified a radiculopial artery (small arrows), which terminated in a large venous ectasia (asterisk) through a fistulous point (long arrow). From this pouch, ascending and descending venous drainage could be assessed. C Selective injection into the right Th10 intercostal artery opacified a large radiculopial artery opening into the venous ectasia previously described through the same fistulous point. D, E Endovascular treatment of the AVF was performed with N-butyl cyanoacrylate at the site of the fistula (arrow). F Final follow-up angiogram. Injection into the right T9 intercostal artery. The AVF was totally cured. Radiculopial arteries were still patent, but did not fill any AV shunt. Neurological status remained normal, except for the previously noted limb spasticity. G The glue is shown on the CT examination (asterisk). Complete remodeling took place in 1 year’s time (H)

730

15 Spinal Cord Arteriovenous Malformations

Fig. 15.6A–E. Legend see p. 731

Classification

731

▲

Fig. 15.7A, B. A 14-year-old boy had sudden neck pain while playing, was nauseous, and vomited. However, subarachnoid hemorrhage could not be established with certainty. One month later, he was admitted due to sudden right lower-limb deficit, from which he rapidly recovered. MRI showed the lesion but no evidence of recent hematomyelia. Angiography demonstrated bifocal SCAVM with normal tissue identified between both niduses and separate slow-flow draining veins

Fig. 15.6A–E. A 12-year-old boy with Klippel-Trenaunay syndrome of the left lower limb presented with acute dorsal pain, paraparesis, and sphincter problems. A, B MRI in T1 and T2 in coronal and sagittal views revealed abnormal spinal vascular structures corresponding to a spinal cord arteriovenous malformation (SCAVM). An isosignal structure was identified, which corresponded to a hematoma (arrowhead). A substantial hypersignal was detected in the spine itself and corresponded to the congestion within the cord. C–E Selective angiography in the left T9 intercostal artery and in the left L4 lumbar artery confirmed spinal cord arteriovenous malformation (SCAVM) fed by a radiculomedullary artery giving off some indirect feeders to the lesion (double arrows). The main feeder to the SCAVM was a radiculopial artery originating from L4 and joining an intranidal arteriovenous fistula (AVF). At this level, a false venous aneurysm was detected (arrowhead). A mainly descending venous drainage was found

732

15 Spinal Cord Arteriovenous Malformations

Fig. 15.8A–D. Legend see p. 733

▲

Classification

733

Fig. 15.8A–I. A 1-year-old, 6-kg baby boy, with familial history of ROW disease, was admitted with disturbances of consciousness and intraventricular hemorrhage on CT (A). Angiography revealed three AVMs, two in the right cerebellar lobe and one SCAVM at C2 and C3. The main cerebellar arteriovenous shunt (AVS), supplied by the right AICA, appeared with an ectatic venous drainage of the posterior fossa and venous pseudo-aneurysms (B). Given the prospected risk of rebleeding related to angioarchitectural features and the location of hemorrhage, this lesion was considered to have bled and was embolized with bucrylate. At the time of discharge, the baby had clinically recovered. One month later, the child presented an acute tetraplegia. T1- and T2-weighted MRI image (C) revealed hematomyelia and swelling of the cervical spinal cord. On the angiograms, the C2–C3 nidus-type AVS was supplied by a ventral coronal branch of anterior spinal artery (D). The upper approach through the VA origin of the ASA was deemed too difficult. The coronal branch of the anterior spinal artery was catheterized rapidly through the ascending cervical contribution (E) and embolized with bucrylate. During the same session, the second cerebellar AVS was embolized. The lesion was completely excluded. Embolization with subsequent administration of steroids (1 mg/kg for 4 days) improved paresis within 1 month, with almost normal strength on upper limbs despite persistent sphincter dysfunction and lower-limb paresis Long-term follow-up shows the normalization of the spinal cord supply (F), the remaining shunt in the posterior fossa (G), and the regression of the hematoma (H). The 3-year follow-up showed significant clinical changes with improvement of the neurological deficits (I). G–I see p. 734

734

15 Spinal Cord Arteriovenous Malformations

Fig. 15.8G–I. Legend see p. 733

Classification

735

Fig. 15.9A–D. A young female patient, 13 years of age, presented with left-sided radicular pain. MRI and angiography (A, B) show transmedullary supply to dorsally located SCAVM. Presence of a network of draining veins emerging around the lower cervical nerves on the left (C). Ventral and contralateral dorsal pial arteries contributions to the dorsal SCAVM (D). E–H see p. 736

736

15 Spinal Cord Arteriovenous Malformations

Fig. 15.9E–H. (continued) Progressive devascularization of the cord lesion was obtained in five glue depositions (E, F). Following four sessions of embolization, there remain minute shunts on the sleeves of C6 (G) and C7 (H)

Neonatal and Infants

737

15.3 Natural History and Clinical Aspects SCAVM in the pediatric population is a therapeutic challenge, as the effects of the disease may produce serious functional disorders and residual handicap. The natural history of SCAVM is usually poor, with progressive worsening of the neurological symptoms and an increase in the mortality rate after a second hemorrhage (Aminoff and Logue 1974; Djindjian 1976; Houdart et al. 1978; Scarff and Riegel 1979; Berenstein and Lasjaunias 1992b). Rodesch reviewed spinal AVSs and found 64% SCAVMs, 30% dural AVSs, 4% PSAVSs, and 2% radicular AVMs. PSAVSs were mostly found in patients under 15 years of age (see Chap. 14, this volume). No dural shunts were encountered in the pediatric population, with only one exception in a HHT child operated on for a perimedullary SCAVF who subsequently developed a dural AVF in a different area (Ling et al. 2005). The majority of lesions affected the male population (male:female ratio, 2:1) in Rodesch’s series, whereas no sex dominance was seen in most other series in patients over 16 years of age (Djindjian 1976; Scarff and Riegel 1979). Etiological diagnosis is made in only 15%–20% of children under the age of 16 (Djindjian 1978; Yasargil et al. 1984; Berenstein 1990). In the 105 SCAVMs described by Rodesch (Rodesch et al. 1995b), 27% of patients were symptomatic during childhood and only 59% of them were diagnosed at that age. In 75% of patients, the diagnosis was made after the first decade of life; only 25% of pediatric SCAVMs are diagnosed before the age of 10.

15.4 Neonatal and Infants Neonatal SCAVMs are particularly rare (Fig. 15.2). The narrowed transdural venous segment makes the possibility of congestive cardiac failure from a thoracic or lumbar SCAVM exceptional. If we consider this diagnosis among the possible AVS causes of cardiac failure in neonates, then SCAVMs account for 1%–2% of them in our experience, and they correspond to the large epidural AVFs (see Chap. 14, this volume). Cullen et al. (2005) reviewed a series of 13 patients who were symptomatic during the first 2 years of life. This group illustrates the specificities of that age group; these can also be seen in babies with VGAM, DSM, pial AVFs, or even hemangiomas and PHACE syndrome. A total of 13 patients (nine male, four female) were identified within a series of 207 spinal AVM cases; the mean age at presentation was 7 months.
Nine presented with weakness or paraplegia, the other four were discovered fortuitously.
One child was born with Hirschsprung’s anomaly and rectal prolapse. There was a large cutaneous vascular lesion on the child’s lower back. Diagnostic imaging prior to surgery for the colonic abnormality identified a spinal vascular malformation that was part of a SAMS. Of note, this patient later developed neurologic symptoms that were attributed to the spinal lesion consisting of a sensory deficit primarily involving the plantar surfaces of both feet.

738

15 Spinal Cord Arteriovenous Malformations


Another patient had an audible bruit that was identified during a bout of bronchiolitis. Investigation with MRI disclosed the spinal vascular abnormality.
Three patients presented with hemorrhage: one had multiple lesions including a brain arteriovenous malformation that had produced intraparenchymal and intraventricular hemorrhage (Fig. 15.8) (Mazighi et al. 2000). He bled from that SCAVM 1 month after diagnosis. Two additional patients presented a hemorrhagic episode: hematomyelia in one patient and subarachnoid hemorrhage in another. Fifty percent of the patients had hereditary hemorrhagic telangiectasia (HHT). Two patients had a SAMS. The majority of lesions were high-flow fistulas (nine patients) (Figs. 15.10–15.12). Three patients had nidaltype arteriovenous malformations. Three patients had multiple lesions. Two patients had paraspinal fistulas, one had an epidural fistula. Two patients had associated brain and SCAVM; in both the cord lesion was symptomatic before 2 years of age, one before and one after the CAVM (Fig. 15.8). Nine patients underwent endovascular treatment by our group.All patients were treated with NBCA liquid adhesive. Of those patients who underwent treatment, in seven the lesion was completely obliterated, and in the remaining two, a 90% reduction was achieved. There was one non-neurological treatment-related complication: a patient developed persistent fever and was felt to have developed an infection, possibly related to the embolization, and responded to antibiotic therapy. There was no permanent procedure-related morbidity or mortality. Five patients were lost to follow-up, either after therapy (two patients) or after initial consultation (three patients). Of the eight patients with follow-up (mean follow-up 26.1 ± 18.6 months), all were either stable or improved. No patients with follow-up showed worsening symptoms following treatment. A number of case reports have been published that document spinal arteriovenous shunts in neonates and infants (Hoffman et al. 1976; Binder et al. 1982; Park et al. 1986; Morgan et al. 1986; Berenstein and Lasjaunias 1992b; Ikezaki et al. 2000; Bjork et al. 1994; Esparza et al. 1987; Tada et al. 1985). To our knowledge, there are no large case series addressing this disease in this population. Hoffman et al. (1976) reported one infant with progressive spastic paraparesis at age 12 months and Binder et al. (1982) reported on a 9-month-old baby with acute onset of paraplegia with a lesion producing cord dysfunction without subarachnoid hemorrhage. Park et al. (1986) reported on a 2-day-old 2.5-kg neonate with profound leg weakness and sensory deficit below Th10. CT failed to demonstrate obvious hemorrhage. No bleeding was found at surgery, but a highflow AVM with a least six prominent supplying pedicles was identified. This neonate appears to be the only patient with documented cardiac dysfunction resulting from a high-flow lesion in the spinal cord.

Neonatal and Infants

Fig. 15.10A–F. Legend see p. 740

739

740

15 Spinal Cord Arteriovenous Malformations

Fig. 15.10A–G. A 4-year-old boy presented with acute onset of paraparesis with significant sensory disturbances. MRI (A, B) shows hematomyelia in the dorsal half of the cord. C, D Angiography shows a ventral SCAVF with a false sac sitting on the midline. No familial history of HHT. E Selective catheterization and embolization were performed and (F, G) 1-year follow-up shows complete exclusion and remodeling

We have seen two more patients with very high-flow metameric AVMs and cardiomegaly but no cardiac failure. In addition, high-flow fistulas at the intervertebral foramen level caused neonatal congestive heart failure (CHF) in one patient and cardiomegaly in two others. All symptoms and signs resolved after treatment by embolization at 6 months in the former and at 2 years in the latter two. Morgan et al. (1986) reported a patient with an AVM who presented at birth with paraplegia and intraspinal hemorrhage, whose angiogram at 16 days showed a high-flow arteriovenous fistula with large venous ectasia and/or flow restriction. The association of HHT with SCAVF in children is well documented (Garcia-Monaco et al. 1995; Mont’Alverne et al. 2003; Mandzia et al. 1999). There is little in the literature, however, addressing the presentation of this disease in neonates and infants. The AVF type of SCAVM is highly suggestive of HHT as seen in CAVFs, where it has been suggested that it become one of the criteria to make the HHT diagnosis in children (Krings et al. 2005c; Mahadevan et al. 2004b; Yoshida et al. 2004; Weon 2005; Halbach et al. 1993) (see Chap. 4, this volume). The diagnosis does not require multifocality or cutaneomucous telangiectasias, which are rare at that age. The neonatal and infant age groups are a still more specific cohort within the pediatric population. For example, in contrast to an earlier report (Rodesch et al. 2004) that found that 70% of pediatric patients with spinal arteriovenous shunts of all age groups presented with hemorrhage (vs 45% of adults), in Cullen’s series (2005) of children under 2 years of

Neonatal and Infants

741

Fig. 15.11A, B. A 3.5-year-old boy presented with recurrent bouts of fever, meningeal irritation signs, and severe abdominal pain. A spinal cord MR showed some perimedullary dilated veins and a huge ectatic vein located posteriorly at the Th9 level (A). A selective spinal angiography at this level showed a direct pial bilateral high-flow arteriovenous fistula (AVF) that was nearly completely occluded by transarterial embolization. During the follow-up, the child had further meningeal signs and fever, the AVF completely thrombosed (B). The last follow-up MR image showed occlusion and reduction in size of the vascular malformation, arachnoiditis particularly from T9 to the conus with cord tethered posteriorly, formation of two spinal cystic compartments, CSF trapping, concave morphology, and atrophy of the thoracic spinal cord

age, hemorrhagic presentation was not the dominant revealing symptom (23%). In addition, while in the total pediatric population the nidal-type AVMs predominate (67%), in the series of children under 2 years of age, 77% patients had fistulas. Perhaps the most striking finding in this cohort was the association with a genetic abnormality (57%), whether hereditary such as in HHT or a nonhereditary somatic mutation as in SAMSs.

742

15 Spinal Cord Arteriovenous Malformations

▲

Fig. 15.12A–K. A 2-year-old child with a medical history beginning at 1 month of age with sudden paraparesis and hypotonia with rectal prolapsus. MRI (A) detected lesion at the level of the conus initially considered a teratoma. The patient was operated on and posterior laminectomy decompression was performed; biopsy showed nervous tissue and vascular anomaly. The child recovered totally. An angiogram shows macrofistula suggestive of (HHT1) Rendu-Osler-Weber disease (B–D). The mother presented telangiectasias and suffered from epistaxis, as does her father. The child was found to have a pulmonary arteriovenous fistula (E). The patient was referred for embolization of the macrofistula of the spinal cord, which was cured with glue (F, G). Follow-up at 6 months shows remodeling with normal venous return of the cord (H–K), H–K see p. 743

Children Over 2 Years of Age

743

Fig. 15.12H–K. Legend see p. 742

15.5 Children Over 2 Years of Age The diagnosis of SCAVM is now made more rapidly at all ages, in contrast to the previous series in the literature (4.9 years after the first symptom for Scarff and Riegel 1979): with the advances in diagnostic imaging possibilities for this disease in this particular age group, the time elapsing between the initial symptom and the diagnosis is now only a few days or weeks. Some patients may have a longer time delay before their lesion is recognized. The initial symptoms rapidly subside and the possibility of a SCAVM is not entertained until a second event occurs later. Sometimes a moderate deficit is noted early, but the child is not brought for consultation and diagnosis until a few years later. In all series, about one-third of the SCAVMs are located at the cervical level and the remaining at the thoracolumbar level. However, the mean age of onset varies according to the location (11.2 years at the cervical cord, 7.9 years at the thoracolumbar level). Most of the symptoms in the pediatric population have a sudden onset (Djindjian 1976; Scarff and Reigel 1979; Berenstein and Lasjaunias 1992b; Merland et al. 1992; Rodesch et al. 2002, 2004). This is understandable with hemorrhage, but one would expect neurological symptoms to develop more slowly when the venous drainage of the lesion creates a progressive congestion of the perimedullary pial network or because of the compression from venous ectasias. Such progressive onset of symptoms occurred in 9% of children (Djindjian 1976).

744

15 Spinal Cord Arteriovenous Malformations

In the Rodesch series (Rodesch et al. 2004), 30 patients (20 AVMs, ten AVFs) were seen before 15 years of age; most had their first symptoms at that age. No filum terminale lesion was detected in children. In this group, 70% of lesions revealed with hemorrhage. Spontaneous total or subtotal recovery of neurological comorbidity occurred in 72% of cases that had bled. Rehemorrhage occurred in 9% of the cases, prior to time of referral. The incidence of hemorrhagic onset varied according to the location of the SCAVSs: 82% of the cervical SCAVSs presented with bleeding, as did 69% of the thoracic and one-third of the lumbosacral SCAVSs. Within the group that bled, hematomyelia occurred in 52%, as proven by CT or MR. It was responsible for severe acute neurological central deficits, associating motor, sensory, and sphincter disorders in two-thirds of the cases. Forty-eight percent of children presented with subarachnoid hemorrhage (SAH) as well as with sudden onset of acute neurological symptoms. They were less severe than those who had hematomyelia. Four patients complained of SAH without neurological deficits. The diagnosis in all the SAH cases was made because of clinical signs– bloody CSF at lumbar puncture– and negative MRI that failed to show any clot in the cord. No patient died because of hemorrhage. Recovery from symptoms depended on the intensity of the bleed, leaving the patients with permanent sequelae or minimal complaints at follow-up. From the 21 patients who presented with hemorrhage, after a few weeks or months 72% had a Karnovsky score equal to or above 80. Within the Rodesch group of 30 lesions, ten out of 30 could be divided into four micro-AVFs (40%) and six macro-AVFs (60%). Five out of six of these macro-AVFs (83%) were associated with HHT and no child with a micro-AVF was suspected of having HHT. In the group of micro-AVFs, all manifested with acute posthemorrhagic neurological symptoms, hematomyelia (three out of four), and subarachnoid hemorrhage (one out of four). All macro-AVFs were located in the thoracic or lumbar region. Four out of six (67%) macro-AVFs revealed by hemorrhage (three of four SAH and one of four HM). By comparison with the group of lesions diagnosed before 2 years of age, the risk of hemorrhage is even higher in children. Hemorrhage is the most frequent symptom at presentation (Figs. 15.1, 15.6, 15.13). These figures were lower in most previous series (36%–54%) analyzed by Berenstein and Lasjaunias (1992b). This difference may be due to the capacity of MRI to reveal hematomyelia with more accuracy than CT did in the past. In some instances, however, it is difficult to dis-

▲

Fig. 15.13A–D. SCAVM in a 6-year-old boy with acute onset of paraparesis. Angiograms (A, B) show a large retromedullary aneurysm; 3D angiogram further pinpoints the situation of the nidus, superficial to the pouch, thus likely exclusively venous. Ventral SCAVM is seen as well as the remaining nidus following exclusion of the aneurysm (D)

Children Over 2 Years of Age

Fig. 15.13A–D. Legend see p. 744

745

746

15 Spinal Cord Arteriovenous Malformations

tinguish between an acute thrombosis of a ventrally located subpial vein ectasia and hematomyelia. It should be noted that contrary to what is observed intracranially, even in children there are no reports of hemorrhagic venous infarction at the spinal cord despite the role played by venous congestion in the production of ischemic neurological symptoms. Neurological deficits associated with hematomyelia vary according to the site of the clot. In general, hematomyelia gives rise to more severe neurological symptoms and longer and less complete recovery than SAH alone. Neurological deficits (without hemorrhage) revealed the SCAVM in 31%–37% (Berenstein and Lasjaunias 1992b). Rodesch et al. (2004) reported no evidence of hemorrhage in 30% of children (22% of cases presented with acute neurological symptoms while 67% had progressive deficits). With such acute presentation, the neurological symptoms are often immediately severe, suggesting hematomyelia, but the MRI fails to show evidence of a hematoma. In the other patients, the overall progression between the onset of symptoms and the first consultation extended from 2 weeks to 4 years (mean 18 months) and patients demonstrated motor deficits that completed progressively with sensory and sphincter troubles. Neurological deficits that arise suddenly are likely due to local hemodynamic disturbances following venous outlet thromboses rather than arterial steal (see Fig. 15.14) (Djindjian 1977; Heroset al. 1986; Park et al. 1986; Casascoet al. 1992; Rodesch et al. 2004). The positive impact of the use of anticoagulation in these situations, and the angiographically demonstrated venous occlusions in some rare cases (Meisel 1995), tend to support this pathophysiological mechanism. Finally, patients with single-hole arteriovenous fistulas (AVFs), which should induce steal manifestations, usually present with hemorrhage (after 2 years) and not with acute nonhemorrhagic onset. In rare situations, acute or post-traumatic low back pain without hemorrhage may lead to the discovery of an SCAVM. In other situations, pain that is localized or radiating along a nerve root may be associated with the other deficits without being the revealing symptom (Fig. 15.15). Isolated radicular symptoms are rare. The lesion can be an incidental finding discovered during screening of a cutaneothoracic vascular dysplasia in 6% of neurologically asymptomatic children. MRI may rarely fail to demonstrate any abnormal intraspinal lesion, while the SCAVM is discovered at angiography leading to the diagnosis of SAMS. In rare historical cases, the investigation of scoliosis or kyphoscoliosis led to the discovery of a SCAVM.

Children Over 2 Years of Age

747

Fig. 15.14A–F. A 15-year-old boy presented with acute paraplegia associated with radicular paroxystic pain. There was no evidence of hemorrhage at that time. The patient was referred to us 2 years later. Although his deficit had largely resolved, on neurological examination bilateral spasticity was found, as were deep and superficial sensory disorders with moderate sphincter dysfunction. A, B Selective analysis of the lesion showed a mixture of nidus type of architecture with C–E direct arteriovenous fistulas. Congestion of the thoracolumbar enlargement accounts for the ischemic onset of symptoms. F The selectivity achieved permitted the radiculopial artery to be partially embolized

748

15 Spinal Cord Arteriovenous Malformations

Fig. 15.15A–E. Legend see p. 749

▲

Children Over 2 Years of Age

749

Fig. 15.15A–G. An 11-year-old boy presenting with acute post-traumatic dorsal pain developing into severe rachialgia with muscular contraction and bilateral Lasègue sign positive at 20°. Neurological examination was normal except for the absence of cutaneoabdominal reflexes bilaterally. A MRI showed a SCAVM at Th12. B, C Angiography confirmed the lesion, which was vascularized by a radiculopial artery arising from the left Th9 and by a radiculomedullary artery arising from the right L2, both reaching a fistulous point producing local (double arrow), D ascending (small arrow), and mainly descending (arrowheads) venous congestion. E Embolization with Histoacryl was performed in a sulcocommissural branch of the radiculomedullary artery. F, G Note the decrease in size of the previously large feeders corresponding to the vascular hemodynamic remodeling after embolization. Left L2 opacified the arterial basket satisfactorily (G). The child remained neurologically normal after the procedures

750

15 Spinal Cord Arteriovenous Malformations

15.6 Diagnosis Diagnosis of SCAVM is now rapidly established with the use of MRI, the diagnostic modality of choice to be used if a spinal cord dysfunction is suspected. In fact, nearly all SCAVMs are seen on MRI with the exception of some ventrally located micro-AVFs being MR-occult (Lasjaunias et al. 2000; see Vol. 2, Chap. 11). The various provisional diagnoses made between the onset of symptoms and the recognition of the lesion described in most series can certainly be explained by the fact that MRI was not available or was not performed. SCAVMs are detected as typical serpiginous signal-void images on T1- and T2-weighted images. The bony changes usually show enlargement of the spinal canal and vertebral or soft tissue-associated involvement (SAMS). Scalloping of the posterior wall and erosion of the bony pedicles are no longer clues for diagnosis, although they are often present in SCAVM with large venous pouches (Fig. 15.16). The diagnosis is confirmed by spinal cord angiography, which remains the gold standard for precise analysis of the vascular anatomy. The information provided by magnetic resonance angiography (MRA) does not contribute to an accurate analysis of SCAVM. Global aortography has been suggested in SCAVM (Riché et al. 1982; Casasco et al. 1992; Merland et al. 1992), yet this screening method can no longer be proposed, even in atheromatous adult patients and even when looking for a dural AVS (Farb et al. 2002); such screening has no place in SCAVM and particularly not in the pediatric population. For post-MRI diagnostic and pretherapeutic evaluation, we rely on selective angiographic assessment at all ages. The procedures are performed under general anesthesia with a 4F or 5F sheath, depending on the child’s weight. Intradural spinal cord arteries in the pediatric population, and particularly in infants, have a more tortuous appearance than in adults; this aspect should not be mistaken for a pathological one. The criteria for a good-quality normal spinal angiogram in children must include the demonstration of the venous drainage of the spinal cord (Lasjaunias 1992). Only selective injections accurately demonstrate the feeding arteries, the draining veins, the angioarchitecture of the lesion, and the vascularization of the surrounding spinal cord.

15.7 Angioarchitecture Arterial stenosis and arterial aneurysms are seldom demonstrated in pediatric SCAVMs. Case reports of spinal cord artery aneurysms are rare and, if diagnosed during hematomyelia (Figs. 15.13, 15.17), may correspond to a thrombosed AVF regardless of age; those seen in the pediatric population are unruptured and always associated with thoracic SCAVMs (three out of 45 cases reviewed by Rengachary 1993). Djindjian (1978) pointed out the extreme rarity of pure aneurysms: one example in 3,000 cases of spinal

Angioarchitecture

751

Fig. 15.16A–I. A 6-year-old boy presented acute low back pain followed by paraplegia and sphincter problems with dramatic improvement after embolization. MRI shows intravenous thrombosis (A); the venous correlations are particularly accurate (B, C). (Courtesy of G. Jiraporn). MRI (D) and angiographic demonstration of the catheterization around the basket (E, F). MRA/MRI (G–I) follow-up after embolization show the spectacular changes. The child nearly completely recovered

752

15 Spinal Cord Arteriovenous Malformations

Fig. 15.16E–I. Legend see p. 751

Angioarchitecture

753

Fig. 15.17A–E. An 8-year-old boy presented with repeated SAH. MRI (A) and angiography show upper thoracic SCAVM with angiectasia and a ventral radiculopial artery supply to an organized false AA (B). Partial targeted embolization was performed; 3week follow-up showed the rearrangement of the flow in the nidus, the ASA, as well as the complete exclusion of the sac (C–E)

754

15 Spinal Cord Arteriovenous Malformations

cord angiography (on a radiculopial artery in the subarachnoid space). He quoted a 20% pseudo-arterial ectatic appearance in his review of 150 SCAVMs (all ages); no special mention was made of the frequency per decade. These figures correspond to what we have seen in our overall AVM population in the central nervous system; however, the presence of aneurysms, either flow- or dysplastic-related, is rare in children unless associated with larger syndromes (SAMS or Klippel-Trenaunay) (Figs. 15.3, 15.4, 15.6). The normal hemodynamic conditions in the cord are different enough from those of the cranial cavity to provoke different responses of the endothelial cells to AVM-induced shear stresses. Aneurysms developed on the radicular portion of the spinal cord arteries are seen in the recurrent type of SAH. Distal ones, most likely intranidal, can be seen in lesions with hematomyelia (Fig. 15.13). Pouches developed on the cord itself should be read differently: one should remember that the anterior spinal artery aneurysms are in the subpial space (Fig. 15.10). False aneurysms are thus present when hemorrhagic manifestations have occurred and they indicate the site of the rupture of the SCAVM (on the arterial or the venous side) (Figs. 15.6, 15.7). They are the weakest and the most dangerous part of the SCAVM (Hurth et al. 1978; Garcia-Monaco et al. 1993). They often result from an upstream rupture due to a downstream thrombosis. Their persistence is an indication forf targeted embolization if a complete exclusion cannot be offered. We have found that arterial rupture is more frequent in SCAVMs than in intracranial AVMs, where the hemorrhage is more likely to be of venous origin. The most remarkable architectural features, also noted in SCAVMs, still remain on the venous side of the lesions, indicating the key role played by the veins in the clinical eloquence of SCAVM. Venous ectasias and venous stenoses are frequently seen (Figs. 15.2, 15.12, 15.16). These pouches can be very large, give rise to few symptoms, and yet may enlarge the spinal canal and erode the bony margins. The pouches and ectasias are associated with the highest-flow lesions. Pial perimedullary venous reflux and congestion (absence of immediate drainage into a radicular vein and into extradural lakes; Figs. 15.10, 15.12) are almost constant. Some rare congestion of the radicular veins, particularly at the thoracocervical junction, mimic an associated AVM, covering like a sleeve the emergence of the nerve up to the epidural space where it drains (Fig. 15.9). The aspect of the nidus is sometimes misleading, with either venular congestion from a micro-AVF that can be cured with a simple embolization to a congested intrinsic network with capillary ectasia and limited venous drainage without evidence of outlet restrictions. It is rare that proliferative diseases (hemangioblastomas, metastases of paragangliomas, etc.) simulate a vascular malformation or an additional nidus at the spinal cord. In our experience, malignant angiogenic disease involving the spine at multiple levels has led only momentarily to the discussion of possible malformative lesions and the rapidly unfavorable outcome has never led to the diagnosis of a biologically or angiogenically explosive situation involving the spine.

Angioarchitecture

Fig. 15.18. A Typical anatomic appearance of a neonatal cervical and lumbar injected specimen (lateral view after sagittal section). B, C Note the regrouping of some sulcal perforators as seen on the angiography performed in a rapidly paraparetic infant. Late phases of the series outline the pial network and the dorsal limit of the cord. The rarity of the venous drainage suggested venous ischemic disease that could not be confirmed (see Chap. 18, this volume)

755

756

15 Spinal Cord Arteriovenous Malformations

Fig. 15.19A, B. Hyperemia of the cord in a 2-year-old child with an undiagnosed myelopathy. The perforators are unusually visible and produce this peculiar intrinsic network congestion with minimal venous opacification (curved arrow), in comparison to the blush demonstrated

Additional features have been encountered in children with progressive deficits starting as early as infancy. These manifestations are associated with significant angiectasia both on the pial and intrinsic network. The venous channels do not seem enlarged, yet the manifestations are suggestive of ischemia similar to what is seen in proliferative angiopathy at the brain level (see Chap. 18, this volume) (Figs. 15.18, 15.19). A case with major capillarectasia of radicular arteries at the cauda equina has been seen without formal diagnosis (Fig. 15.20).

Angioarchitecture

Fig. 15.20A–E. A 5-year-old boy presented with a progressive paraplegia and sphincter difficulties; low back cutaneous discoloration. Nephrectomy at 9 months for angioma. MRI (A–C) and angiography (D, E) were performed in an attempt to come to a diagnosis. Note the peculiar aspect of all arteries to the cauda equina and the abnormal signal throughout the cord

757

758

15 Spinal Cord Arteriovenous Malformations

15.8 Treatment Therapeutic management is proposed after analysis of the lesional and regional angioarchitecture is completed in an attempt to understand the past history of the lesion and its clinical expression and to anticipate its natural history. Our therapeutic goal is primarily to completely exclude the AVS in order to protect the child from future rebleeding or deficit. Total exclusion is rarely obtained in SCAVMs, whatever treatment is applied (Berenstein and Lasjaunias 1992b; Mourier et al. 1993), yet it is nearly always obtained in SCAVFs. Our therapeutic objectives depend upon the predictable embolization risks. If they are deemed too high for the clinical status of the child, partial occlusion constitutes an acceptable therapeutic choice if embolization is targeted at the weak points of the architecture and performed with a permanent agent. In general, the challenges involved in the management of SCAVM are different in niduses and fistulas.

15.8.1 Therapeutic Abstention

The decision not to treat results from the restriction mentioned above; this decision is made in less than one-third of the patients. In this group, follow-up is undertaken with reconsideration of the decision depending on the clinical progression. Yearly MRIs and angiography every 3 years help anticipate dangerous changes. Any new clinical event will prompt a repeat of the studies and reopens the therapeutic discussion. Many of the patients managed conservatively in the past have subsequently benefited from tool improvement facilitating embolization of ventral perforators (with proper knowledge of anatomy and high-quality equipment), with a high rate of success and low morbidity. The decision not to treat is still sometimes made because of the technical impossibility (predicted or encountered) of reaching a safe position, but these decisions are not final and can be specific to the moment and the individual. Medical aggressiveness, interpretation of the available data, personal experience, individual beliefs, and anatomic knowledge can therefore lead to very different strategies. Clinical goals and results are more important than the pictures of technical exploits. Technical failure may occur if the normal transdural narrowing of the radicular arteries (which should not be mistaken for a stenosis from high-flow angiopathy) is followed by a kink of the radicular artery in the subarachnoid space. This type of enlarged radicular artery can be gently straightened in the subarachnoid portion of the vessel, as is done with the vertebral or the carotid arteries in the cervical region, but this maneuver requires experience and particular care for a safe procedure.

Embolization

759

15.8.2 Embolization

In our experience, embolization is always chosen as the first treatment modality. Embolization of SCAVMs usually entails distal injection of a permanent embolic agent into the AVM itself and not a proximal occlusion. We have never used autologous clot, fat tissue, balloons, silk, Ethibloc, collagen, or a venous approach. In the first child treated in 1982 (spinal cord–medullary junction in an almost asymptomatic child after posthemorrhagic tetraparesis), we used polyvinyl alcohol (PVA) particles (Fig. 15.1). For the 20 years since, endovascular occlusion has been done with N-butyl cyanoacrylate (Histoacryl) (Figs. 15.10, 15.12, 15.21). The use of coils is limited to some SCAVFs. In the ruptured SCAVM group, with hematomyelia and deficit, clinical recovery and/or resorption of the hematoma is expected. Surgery for the purpose of decompression may have deleterious effects (Fig. 15.22). The first therapeutic procedure usually takes place 6–8 weeks after the initial accident. Early rebleeding is not known to occur in this disease, yet differences may exist in babies. Only once was embolization performed in an emergency (Fig. 15.8). The superselective approach of the nidus is accomplished with microcatheters of various types via the radiculopial (posterior spinal) or the radiculomedullary (anterior spinal) arteries (Magic 1.5 in MAVFs, or Magic 1.2FM, Balt Extrusion, Montmorency, France; Figs. 15.8, 11.2). Evoked potentials are used by one of us in some instances (Berenstein and Lasjaunias 1992b). The use of these tests, particularly under general anesthesia, has never proven to be useful in improving the clinical outcome of embolized SCAVMs or preventing complications with glue embolization. In our series, no special monitoring or provocative tests is employed during the intervention; intraoperative decisions are based on careful preoperative analysis of the anatomy and intraoperative distal delivery of the bucrylate with catheters of variable stiffness. The mean number of diagnostic and therapeutic sessions in our series is 3.1 per patient, and the mean number of therapeutic sessions is 1.7 per patient. In children, no mortality or permanent neurological morbidity has occurred after endovascular therapy, even when performed in the anterior spinal axis. We have not observed vasospasm during withdrawal of the microcatheter, nor has the catheter become stuck following glue injection. One should always be aware of the risk of vessel rupture with microguidewires and immediate occlusion of the artery proximal to the leakage should be carried out with coils or glue and not by injection of Gelfoam strips, which may worsen the rupture because of the amount of liquid needed to push the strips. Halbach et al. (1993) described a venous rupture associated with a balloon migration in an AVF and rapid control of the lesion was accomplished by embolization without clinical sequelae. We do not recommend the use of balloons in such lesions or in other AVFs of the central nervous system.

760

15 Spinal Cord Arteriovenous Malformations

Fig. 15.21A–F. Legend see p. 761

▲

Results

761

Fig. 15.21A–G. A 9-year-old boy presented with repeated hemorrhagic episodes with mild hemiparetic deficit. Angiography shows a small SCAVM fed by a radiculopial branch and located dorsally and lateral to the midthoracic cord (A, B). The ASA is displaced but not contributing (C). Selective embolization (D, E) allowed complete glue embolization (F, G)

15.8.3 Results

Following embolization, total occlusion is obtained in less than 20% of patients (Figs. 15.8, 15.17, 15.21). This rate is higher in both microand macro-AVFs and in babies. Half of the cases have 75% of their SCAVM excluded (Figs. 15.10, 15.12). No lesion has been embolized with less than 50% obliteration. All the patients improved after embolization, and two-thirds of them are currently neurologically normal on follow-up. Follow-up in this group ranges from 1.5 to 13 years. All children have one follow-up angiogram 1 or 2 years following the last endovascular procedure. One partial recanalization has been noted in an otherwise clinically stable child embolized in 1982 with particles. The other results obtained are stable. No rebleeding has been noted, even in partially treated lesions that had previously bled (Fig. 15.23). Although this disease is rare, particularly in this population, and despite the eloquence of the surrounding tissues, which requires specific anatomic and technical expertise, SCAVM management in the pediatric population is not a significantly different challenge from that in other AVSs of the central nervous system in this age group. The role of surgery in spinal cord vascular diseases in children is limited, provided that endovascular alternatives can lead to significant, safe, and stable results. However, in some cases when embolization was performed with nonpermanent agents, surgery has been proposed as a therapeutic adjunct (Halbach et al. 1993). In one

762

15 Spinal Cord Arteriovenous Malformations

Fig. 15.22A–F. A 7-year-old girl presented with acute paraplegia from hematomyelia. MRI shows large conus SCAVF lesion with large partially thrombosed pouch (A–C). Following decompressive surgery, symptoms worsened (D), with severe permanent sensorimotor deficit with sphincter dysfunction. Angiography shows a pial SCAVM fed by L1 (E), Th12 injection shows the radiculomedullary supply from Th11 Embolization of the fistula (F) is achieved; control in Th12 and Th10 failed to demonstrate any residual lesion

Results

Fig. 15.23A–D. An 11-year-old boy presented an acute onset of rapidly regressive paraparesis associated with hematomyelia. VA contributions (A) and the cervical contributors (B) show several areas of AV shunts located on the left half of the lower cervical cord. Following two sessions of embolization and five glue depositions, the reduction was significant (C, D). Brief walking difficulties appeared 24 h after the first embolization and subsided in few hours. Note the ASA axis and reflux in the cervical radiculomedullary artery

763

764

15 Spinal Cord Arteriovenous Malformations

Fig. 15.24A–D. Legend see p. 765

▲

Results

765

Fig. 15.24A–J. A 14-year-old girl presented sudden headaches and vomiting. Rightsided regressive deficit. CT shows the SAH (A). MRI (B) shows a SCAVM located dorsally on the surface of the midcervical spinal cord. C–D Angiography confirms the diagnosis and clarifies the fistulous character of the lesion; 3D angiography further demonstrates the anatomy (E). Microcatheterization failed twice to reach a safe position. The child was therefore operated on (E–G). The lesion was completely resected and the child asymptomatic (H–J), I,J see p. 766

766

15 Spinal Cord Arteriovenous Malformations

Fig. 15.24I,J Legend see p. 765

case, a failed attempt to embolize a dorsally located cervical lesion led to successful surgical removal with normal postoperative clinical examination (Fig. 15.24). Embolization is a generic name that encompasses many techniques and approaches. In each individual case, the results depend on the possibility of reaching the lesion via the safest route and the ability to deliver the most efficient agent (in our experience NBCA). Longer follow-up is needed to more precisely appreciate the encouraging course of these embolized SCAVMs in children. The risk of severe handicap after aggressive treatment should be balanced against the apparently favorable course of partially embolized SCAVM. At present, conventional radiotherapy, gamma knife radiosurgery, or stereotactic radiosurgery are not used in the management of pediatric SCAVMs. Children do not have dural lesions of the adult male type; however, one of us reported a very unusual familial HHT context in which one of the cousins developed a dural AVS of the adult type (Fig. 15.25).

16 Vascular Trauma and Epistaxis

16.1

Introduction 767

16.2

Traumatic Carotid-Cavernous Fistula 768

16.3

Post-traumatic Sinus Thrombosis 776

16.4

Traumatic Dissection 777

16.5

Intracranial Arterial Aneurysms 779

16.6

Iatrogenic Injury 780

16.7

Traumatic Insult of Vascular Malformation 783

16.8

Epistaxis 785

16.9

Technical Remarks 787

16.1 Introduction Vascular trauma in children is relatively rare in Western countries. Few reports have appeared in the literature, and these have dealt mainly with aneurysm, dissection, or caroticocavernous fistula of traumatic origin. Probably in relation to the increased elasticity of the vascular structures of the head and neck in children, trauma associated with vascular injury is usually severe and associated with multiple injuries. Several types of vascular damage can be encountered, and many of them require emergency management as they may compromise the medical management of the situation or the recovering capacity of the child. The following physiopathological mechanisms for clinical expression can be seen:
Arterial ischemia by sudden large-vessel occlusion, steal, or emboli (Fig. 16.8)
Hemorrhage from direct mural injury, secondary aneurysm rupture, collateral tear (Fig. 16.11)
Mass effect from hematoma (in the neck) (Fig. 16.6)
Venous ischemia from congestion related to outlet occlusion or venous reflux (Fig. 16.6)

768

16 Vascular Trauma and Epistaxis

The following types of clinical onset are seen:
Acute with clinically obvious vascular damage
Early vascular damage found incidentally because systematically suspected
Delayed clinical onset due to secondary vascular failure to remodel or secondary complication of a silent injury
Late vascular complication (dural shunt, intrasphenoidal aneurysm)

16.2 Traumatic Carotid-Cavernous Fistula Traumatic carotid-cavernous fistulas (CCFs) are infrequent and can be high-flow lesions due to a closed or penetrating injury (e.g., across the orbit; Fig. 16.1). The complications are often very different. Two major risks of associated lesions in this type of traumatic CCF have already been mentioned: 1. Subarachnoid hemorrhage from transdural extension with focal subarachnoid hematoma 2. Potential communication of the cavernous venous plexus with the sphenoid sinus and possible massive epistaxis Sometimes both are present (Fig. 16.2). In such cases, sacrifice of the internal carotid is mandatory. No attempt should be made to preserve the vessel in such a life-threatening situation. We have been confronted with these situations in children. A provisional diagnosis of internal carotid rupture was made on the telephone, and the child was then admitted to hospital, at which time profuse epistaxis with subarachnoid hemorrhage was already noted with a skull base fracture. The situation stabilized after a few hours and the child was referred to a pediatric center. Regardless of the time of admission, the interventional neuroradiology team should be activated and the child brought to the angiography room immediately to be managed as an absolute emergency. It is rare for traumatic CCFs to be revealed in the same way as a conventional one in adults, with an interval of a few weeks between trauma and the typical orbital signs (Fig. 16.3). Ophthalmic signs usually occur in minor forms of CCF. Attention should be paid to the presence of cortical venous drainage (Fig. 16.1). If treatment is staged, then the transcranial drainage should not be diminished and persistence of cortical vein congestion should not be tolerated, as it always carries a high risk of secondary hemorrhage or epilepsy. In traumatic lesions, in contrast to spontaneous ones, in which the reflux is progressive, the retrograde flow into cerebral veins is by definition sudden.Venous remodeling has no time to thicken the vessel wall. Therefore, if following the development of a traumatic arteriovenous fistula (AVF), the veins resist an initial increase in flow, but they may not absorb an additional increase after incorrect (treatment-induced) rerouting of the AVF drainage (Fig. 16.4). Thus venous approaches are contraindicated in fresh traumatic AVFs. The retrograde sinus approach should be used with extreme caution if chosen.

Traumatic Carotid-Cavernous Fistula

769

Fig. 16.1. A A 12-year-old boy presented at the age of 22 months with severe head trauma that rapidly led to symptoms suggestive of caroticocavernous fistula (CCF). As the child had recovered from the trauma, the parents refused permission for angiographic study until the child was 5 years old. Against our advice, they refused permission for endovascular treatment until he was 9 years old. B Occlusion of the fistula was then achieved with a no. 16 gold valve balloon. Four years of follow-up after occlusion of the fistula confirmed the complete disappearance of the symptoms, despite their having persisted for 7 years

In CCFs that do not involve the subarachnoid or sphenoid sinus spaces, reconstruction of the internal carotid can usually be achieved with a detachable balloon similarly to what is done in adults. If the internal carotid artery has to be occluded and if the child is old enough, testing under sedation can be carried out. If the child is young, an experienced team can certainly rely on the analysis of the child’s specific vascular anatomy. Tolerance is excellent in most cases, as the anastomotic channels are usually widely open at that age. It is sometimes difficult in complex trauma to identify the exact location of the fistula, i.e., immediately at the skull base, before the entrance of the internal carotid, or immediately after the cavernous sinus at the

770

16 Vascular Trauma and Epistaxis

Fig. 16.2. A, B Major head trauma in an 11-year-old boy presenting with subarachnoid hemorrhage, pneumoencephaly, right otorrhagia, and massive epistaxis requiring a large blood transfusion. Angiography demonstrated a carotidocavernous fistula with extracavernous opacification corresponding to the blood collection seen on computed tomography (CT). C, D Although not visible, severe epistaxis also suggested a rupture of the internal carotid artery into the sphenoid sinus. Subarachnoid rupture was confirmed by angiography demonstrating the blood collection in the upper cerebellopontine angle and the subarachnoid air in the perichiasmatic cistern. E–G see p.771

Traumatic Carotid-Cavernous Fistula

771

Fig. 16.2. (continued) E–G An emergency endovascular procedure was performed with the aim of closing the siphon in front of the leaks without attempting to preserve the artery by entering the various ruptured points. Tolerance was expected to be good. The balloon procedure was uneventful. Secondary progression was satisfactory despite associated brain contusions

level of the ophthalmic artery (Fig. 16.5). In the latter situation, there is usually a large arterial pouch protruding into the chiasmatic cistern. In our experience, such a pouch is not intracavernous and surprisingly not associated with subarachnoid bleeding. When this pouch has stabilized in a patient referred long after trauma, it remains possible to reconstruct the internal carotid siphon and electively occlude the vascular lake. It is during such complex situations that multifocal AVFs can be found. If the artery cannot be reconstructed, then the most distal fistula, the one closest to the circle of Willis, should be treated first to avoid the risk of cerebral steal after parent vessel occlusion proximal to the most proximal AVF.

772

16 Vascular Trauma and Epistaxis

Fig. 16.3A–E. A 7-year-old girl presented with minor head trauma and rapidly conjunctival hyperemia and right-sided proptosis. A, B Angiography showed a middle cranial fossa arteriovenous fistula (AVF) draining into the cavernous plexus. C–E During the same session, a microcatheter was advanced into the middle meningeal artery and pure glue delivered in situ. Rapid and complete resolution of symptoms followed embolization

Traumatic Carotid-Cavernous Fistula

773

Fig. 16.4A–D. A young boy presenting at the age of 10 years with severe orbitocranial trauma. A Two months later, he had a right-sided third nerve palsy with proptosis and hyperemic conjunctiva. B, C Angiography showed a small arteriovenous communication in the cavernous sinus between the siphon and the venous plexus. Significant pial reflux was found. After failure to penetrate the venous sector via an arterial approach, coils were delivered in the cavernous sinus via a venous approach. D After incomplete occlusion, the coil method was discontinued because of an intense spastic reaction of the vein. After pulling the catheter into the jugular bulb, it was impossible to go back into the cavernous sinus. Following lengthy discussions and as the child could not be treated earlier, he was scheduled to come back 2 months later. One month after the first session, he had a severe posterior fossa hemorrhagic complication and died

774

16 Vascular Trauma and Epistaxis

Fig. 16.5. A–F Legend see p. 775

▲

Traumatic Carotid-Cavernous Fistula

775

Fig. 16.5A–J. A–C A 15-year-old boy presented after being in a severe car accident; he remained in a coma for a long time. When he awoke, he had unilateral blindness and hemianopia. In addition, he rapidly developed symptoms connected with a high-flow caroticocavernous fistula (CCF). D, E Angiography demonstrated the high-flow lesion with posterior fossa drainage, and giant venous pouches. In view of the drainage, the arteriovenous (AV) communication was thought to be into the cavernous sinus. After detachment of several gold valve balloons, it appeared that an additional AV communication was located in the supracavernous portion. The vertebral and posterior communicating artery (PCom) route was then used to deliver coils in the distal internal carotid artery. F–H Complete occlusion of the shunt was obtained; a coil bulging into the PCom led us to prescribe aspirin for 4 months (until the next angiographic followup). I, J The child recovered from the hemianopia, and the fistula was completely occluded, despite deflation of the balloons. The PCom was still patent and the coil was likely to be extravascular by that time. Aspirin was discontinued

776

16 Vascular Trauma and Epistaxis

Associated venous lesions are often noted, particularly if the trauma involved the posterior fossa skull base. Dural venous thrombosis should also be recognized during the screening angiography. It may be responsible for changes in consciousness and should be recognized before discussing arterial mechanisms, particularly if endovascular treatment has already been carried out. Such dural vein injuries may secondarily give rise to dural arteriovenous shunt, as previously described in adults. In the few cases we have seen, it seems that secondary dural arteriovenous shunt follows a more active angiogenic phase over a longer period of time.

16.3 Post-traumatic Sinus Thrombosis Post-traumatic sinus thrombosis is a rare situation that we have never encountered in isolation (Taha et al. 1993). The clinical manifestations usually depend on the age of the child and associated manifestations caused by intracranial pressure that is too high. Injury is usually less severe than in CCF. The thrombosis can produce pial venous congestion with the theoretical risk of secondary weakness and seizures. Sigmoid sinus thrombosis following head injury should always be suspected if the recovery of cranial trauma seems to be much longer than expected. More frequently, jugular vein injury is associated with penetrating trauma of the neck (Fig. 16.6). Thrombosis or stenosis of the jugular vein corresponds at this stage to a direct traumatic venous dissection alone or in association with an arterial venous dissection.

Fig. 16.6A, B. A 15-year-old presented severe craniofacial trauma and multiple limb fractures, severe hemorrhagic shock, and emergent external carotid ligation with persisting facial bleeding. The child was transferred and embolization of the facial arteries and contralateral maxillary provided the expected hemostasis. Note at the ligature level (A) the involvement of the jugular vein, which forces the drainage toward the cervical epidural system (B)

Traumatic Dissection

777

16.4 Traumatic Dissection Traumatic dissection without penetrating injury usually involves the internal carotid artery (Fig. 16.7) at the neck, close to the temporal entrance. Manifestations are distal embolic phenomena and, in some very rare cases, compressive manifestations related to an associated large dissecting aneurysm. There is almost no distal hemodynamic failure, as the anastomotic channels are largely patent in this age group. Occasionally, dissecting injury involves the vertebral artery (Fig. 16.8); if this is the case, distal emboli occur in the basilar system. Prognosis is highly dependent on the possibility of starting medical treatment and intensive care management in the situation in which a posterior fossa syndrome is noted. Spontaneous recovery has been observed even after severe strokes. The use of fibrinolysis is extremely dangerous, since multifocal silent vascular damage may become apparent during or following such management. Aspirin is often prescribed in arterial dissections at the acute stage and later if there is a residual arterial pouch in incompletely healed mural lesions (see Chap. 18, this volume). Attention should be paid to the patency of adjacent veins if the arterial sector is responsible for the dominant symptoms.

Fig. 16.7A, B. A 2-year-old child fell out of the crib without immediate consequences. Ten days later, there was right-sided hemiplegia and mutism. On CT, the head of the caudate lacuna and no ICA flux can be observed on MRI. Angiography demonstrates the cervical (A) and intradural (B) dissection of the ICA. Spontaneous yet incomplete recovery was noted; there was no underlying arterial wall disease

778

16 Vascular Trauma and Epistaxis

Fig. 16.8A–D. A A 9-year-old boy presented with nausea and vertigo 6 days after cranial trauma. On admission, neurological examination showed an asymmetrical locked-in syndrome with bilateral pyramidal signs predominantly on the right side. B–D Angiography demonstrated a vertebral artery dissection with intracranial occlusion of the basilar artery and cerebellar branches. No fibrinolysis was performed. E see p. 779

Intracranial Arterial Aneurysms

779

Fig. 16.8. (continued) E Four months later, the child had almost completely recovered, with satisfactory reopening of the posterior fossa arteries and contribution from the circle of Willis to the supply of the mesencephalic territories

16.5 Intracranial Arterial Aneurysms Intradural arterial aneurysms are often encountered following trauma. Ventureyra (1994) and Yazbak et al. (1995) reviewed traumatic intracranial aneurysms noted in adolescence and childhood (see Chap. 17, this volume and Vol. 2, Chap. 11). They both indicated the special characteristics of these lesions. The topography of such traumatic lesions is often close to the tentorial edge or the falx cerebri. There is no evidence of bony fracture in most situations. In rare cases, the aneurysm is located in the epidural space (middle meningeal artery) or at the skull base (internal carotid artery). The aneurysms that are demonstrated are in fact usually false aneurysms corresponding to a pouch communicating with the intravascular space. A hematoma in the area (usually small) indicates extravascular leakage (Fig. 16.9). A spasm proximal to the arterial rupture indirectly points to the leakage site; superselective injection should be avoided and proximal exclusion of the stump immediately achieved. The vessel cannot usually be reconstructed and therefore filling of such pouches is not recommended. Sacrifice of the parent artery by balloon, coil, or glue is often discussed in this situation. It is not rare, however, for aneurysms in children to be diagnosed following minor trauma (Lapresle 1978). The situation is then different, and careful analysis of the pouch should aim to promote reconstructive treatment rather than sacrifice of the parent vessel.

780

16 Vascular Trauma and Epistaxis

Fig. 16.9. A A 13-year-old child presented with severe frontal trauma and large hematoma extending to the face. Persistent bleeding led to endovascular control. The global injection failed to show the point of bleeding; however, the spastic aspect of the transverse facial points to its involvement (arrow). Selective catheterization and immediate embolization was achieved and successfully obtained the hemostasis. B A 14year-old girl with similar manifestation. Angiogram points to the false aneurysm responsible for the hemorrhage; the vessel was sacrificed at the level of the aneurysm

Traumatic rupture of a skull base aneurysm or traumatic aneurysm of the internal carotid artery at the skull base can be associated with several immediate unfavorable local or regional insults: 1. Communication with the sphenoid sinus, with the risk of secondary rupture and lethal epistaxis 2. Transdural leakage, with the risk of massive subarachnoid hemorrhage 3. Damage to other vessels, particularly venous, with unexplained intracranial hypertension 4. Immediate or delayed caroticocavernous fistula (Hahn et al. 1990) worsening the cerebral venous equilibrium

16.6 Iatrogenic Injury Iatrogenic injury can sometimes be seen after maxillofacial or spinal surgery and even tonsillectomy or difficult placement of the central line in the jugular vein (Figs. 16.10, 16.11). We have seen several patients with vertebro-vertebral fistula associated with difficult venous punctures and catheter placement in children. Symptoms develop secondarily and patients arrive for consultation years after the trauma (Fig. 16.10).

Iatrogenic Injury

Fig. 16.10A–D. An 8-year-old girl presented with mental retardation. She was treated in infancy for a urinary tract infection by antibiotics through a cervical venous line on the right side. Recently a thrill was noted in the right supraclavicular area. Mild cardiac failure with tachypnea and sweating were noted. Cardiac catheterization revealed an increased cardiac output and a low cervical arteriovenous fistula (AVF). Initial surgery by the referring team was performed, but failed to occlude the pathological shunt. A, B Secondarily, more selective angiography was performed and revealed a right vertebrovertebral fistula. The child was referred to our group for endovascular treatment. C, D Occlusion of the fistula by the arterial route with a detachable no. 16 gold valve balloon was easily accomplished

781

782

16 Vascular Trauma and Epistaxis

Fig. 16.11A–D. An 8-year-old boy who underwent biopsy and partial debulking of an astrocytoma. At the time of surgery, bleeding occurred from a small branch of the right A1 vessel. A Follow-up MRI examinations were done. B Two years later, these appeared to show evidence of an aneurysm, which was then confirmed at angiography. The child was then examined again, but surgical clipping proved not to be possible because the fundus of the aneurysm was buried in the tumor. C, D He was then referred for GDC (Guglielmi detachable coils) coiling. He underwent follow-up angiography, which showed slight compaction of the coils, and he is being considered for additional coiling in the future

Traumatic Insult of Vascular Malformation

783

16.7 Traumatic Insult of Vascular Malformation Trauma of the maxillofacial and cutaneous covers of the head is common in children. Direct trauma while playing in the playground is usually benign unless an underlying lesion exists. The injury creates some hemorrhagic episodes in arteriovenous or even venolymphatic lesions, most frequently hematoma rather than external bleeding. Ear (Fig. 16.12) or tongue vascular malformation can sometimes be the source of severe hemorrhagic episodes after injury. Management of such complications should take into consideration the overall treatment of the malformation. Easy control of the complication with coils, for example, should be avoided if it compromises the future approach to the vascular malformation. In the long term, it seems that almost all superficial malformations are triggered by trauma; however, we are unable to clearly evaluate the role played by timing in the triggering effect of trauma on remodeling failure (Figs. 16.13, 16.14). We still accept that traumatic changes in maxillofacial malformations are key factors for most of their nonreversible development.

Fig. 16.12. A young female patient who has had, since childhood, a dilated pulsatile varix on the left external ear, corresponding to direct trauma and secondary development of an arteriovenous fistula under a local reddish discoloration of the skin

784

16 Vascular Trauma and Epistaxis

Fig. 16.13A–C. A 7-year-old boy who suffered from moderate cervical trauma 6 months before clinical examination. At admission, a cervical bruit and thrill were diagnosed. No previous medical history was noted, except for diagnosis of pulmonary arterial enlargement during chest X-ray performed at 2 years of age. A Magnetic resonance angiography (MRA) and B conventional angiography showed a high-flow arteriovenous fistula (AVF) considered to be post-traumatic in the absence of other common diseases in the family. Note the epidural venous drainage and the identified source of supply to the cord at that level. C Occlusion was rapidly achieved with a detachable gold valve balloon using the preloaded technique through a 4F sheath

Epistaxis

785

Fig. 16.14A–D. A 7-year-old boy who suffered a direct lumbar trauma 2 years before presentation, causing swelling of the traumatized region. Spontaneous involution occurred. Two years later, the child had a painful swelling of the previously traumatized area with right limb palsy. No anomaly was found on examination of the skin. Swelling of the paraspinal region was found, but was not provoked by any Valsalva maneuver. The most probable diagnosis was a venolymphatic paraspinal malformation. A, B Plain CT. C MRI. D CT after direct puncture

16.8 Epistaxis In our experience, trauma is the most frequent cause of epistaxis in children (30%; Table 16.1). Some cases are actually related to major lesions involving the skull base and the internal carotid artery. Hypervascular tumors (juvenile angiofibromas, etc.) are the second most common cause of epistaxis in children, either spontaneously or following biopsy (Figs. 16.11, 16.15). The other etiologies include various vascular diseases such as nasal capillary hemangiomas and other vascular proliferations, as well as some intracranial high-flow vascular lesions draining across the orbit and causing congestion of the nasal mucosa. In hereditary hemorrhagic telangiectasia (HHT) in children, epistaxis is extremely rare. It

786

16 Vascular Trauma and Epistaxis

Fig. 16.15A, B. A 15-year-old patient referred for poorly controlled epistaxis following tumor biopsy. Note the false aneurysm at the site of puncture (A). B 3D angiography medial view

Table 16.1. Etiology of epistaxis in 24 children referred for embolization Etiology

Patients (n)

Trauma Tumor (juvenile angiofibroma) Rendu-Osler-Weber disease Capillary hemangioma Idiopathic (normal coagulation) Coagulation disorders Wyburn-Mason disease (CAMS) Vein of Galen aneurysmal malformation Proliferative angiopathy

7a 6 3 2a 2 1 1 1a 1

a

One patient referred as an infant; no neonates.

seldom requires embolization, and in the few cases in which an endovascular approach was needed it was used in adolescents. Nose bleeds were moderate in most children seen in families of symptomatic HHT adult patients with severe epistaxis or in children with cerebral AVFs. Careful clinical history of epistaxis leads to the correct etiological diagnosis and appropriate management of the various diseases involved. Direct repeated self-induced nasal trauma (with the finger most frequently) should be considered if no other cause is found. As seen in vascular malformations, treatment of the bleeding episode should not compromise management of the underlying disease.

Technical Remarks

787

16.9 Technical Remarks Considering that associated lesions and management of a possible underlying lesion are the primary concern in traumatic lesions in children, there are no difficulties in technical management. Clinical tolerance is usually better in children than in adults if one considers the severity of the vascular damage sometimes observed; the capacity of recovery is also usually better than in adults. It is in pediatric trauma patients that most of the coma and evaluation scales were used to develop our evaluation scores (see Chap. 2, this volume). Clinical evaluation and proper CT and MRI are of paramount importance when rapid, efficient treatment is required (Fig. 16.16). Following the identification of a morphological goal to be reached, the technical challenges to be faced should be anticipated before the femoral puncture is carried out. It is important to predict the volumes needed for treatment in young children. Bladder filling should be verified during the procedure, as catheterization is not always done in young children, particularly boys. Choosing the most polyvalent size of the arterial access sheath is a crucial decision, and the biggest possible one for the size of the child is a poor choice if the procedure can be carried out successfully with a smaller one. One should take into consideration the difficulty of a femoral approach to deliver large devices, particularly a detachable balloon. The preloaded detachable balloon technique (Table 16.2), which we developed in 1984, is currently still the safest way to occlude high-flow fistulas with a 4F sheath in young patients. We do not use a bifemoral approach in children weighing less than 10 kg. As mentioned above, the usual tolerance to large-vessel occlusion is good, provided that all the anastomoses across the midline or with the posterior circulation have remained open. Attention should then be paid to rare, unfavorable anatomic situations. Clinical functional testing in children is always difficult, and sacrifice of large damaged arteries is not rare in emergency procedures. Interventional approaches must be mastered in order to offer the best-quality treatment in children. Anticoagulation treatment is not frequently used and should be discussed on an individual basis if thrombosis is noted. In contrast, aspirin is employed when dissection or giant aneurysm is noted. Embolization of external carotid lesions follow the same principles as those demonstrated in adults (Lasjaunias and Berenstein 1987b); in particular, embolization for epistaxis in HHT disease, coagulation disorders, or maxillofacial tumors is performed with particles (polyvinyl alcohol, PVA). High-flow fistulas draining across the orbit or large lesions of the cavernous sinus require specific management and tools. One should not aim or expect to demonstrate the point of bleeding during angiographic study. Bilateral embolization is carried out regardless of the appearance of the nasal fossa. Pre-embolization series are performed exclusively to demonstrate the skull base anatomy. Cavernous sinus and transorbital anastomoses are usually wide open at this age. If an anastomosis is demonstrated, then superselective catheterization is performed. If a false aneurysm is seen in the maxillofacial region, special precautions should be taken. When the source of bleeding is not seen as an extravasation of contrast or false aneurysm, attention should be paid to focal arterial spasm that may have provided a transient hemostasis. One should not usually enter a false

788

16 Vascular Trauma and Epistaxis

Fig. 16.16A, B. MRI appearance on T1 in a case of caroticocavernous fistula (CCF). The location of the arteriovenous (AV) communication was acceptable for a therapeutic approach; however, the presence of pial reflux cannot be assessed with enough certainty. Asterisks, venous side of the fistula Table 16.2. Preloaded system for detachable balloons Sheath 4F admits no. 16 gold valve balloona 5F admits nos. 16 and 9 gold valve balloon Balloon carrier Mini-torquer with nosea Pass valve Microguidewire, 0.014 in and below Thin-walled 4F pre shaped catheter preloaded with the balloon carrier and the balloon

aneurysm cavity; sacrifice of the parent vessel is thus recommended at the acute stage. In the external carotid system, the parent branch must be sacrificed.Wedged injection should not be performed, as the risk of rupture is extremely high. Emboli should be injected with the smallest volume of contrast or liquid; particles should therefore be avoided. Glue is certainly an excellent agent in this situation. When the cavity is seen a few months later, exclusion of the extravascular space can be carefully attempted. Late postembolization changes in traumatic patients do not require any specific management; in particular, symptomatic pouches after balloon deflation were not encountered in our experience. Glue is well tolerated and does not require additional medical treatment after delivery. No late anomalies have been noted on follow-up. In our experience in children who have undergone embolization for epistaxis or vascular trauma repair or control, there have been no direct neurological or non-neurological complications. Strict observance of pretherapeutic evaluation and decision trees combined with anatomic and technical mastery of the techniques used is vital in order to achieve the expected results in a pediatric environment.

17 Intracranial Aneurysms in Children

17.1

Introduction 789

17.2

Incidence 793

17.3

Presentation 795

17.4

Etiology 797

17.5

Traumatic Aneurysms 798

17.6

Infectious Aneurysms 803

17.7

Saccular Aneurysms 813

17.8

Dissecting Aneurysms 823

17.9

Location 835

17.10

Therapeutic Strategies 836

17.1 Introduction Participation in the management of children with intracranial arterial aneurysms (AAs) requires the diagnostic and interventional neuroradiologist to be familiar with the very unique characteristics of this disease in children. In particular, during the neonate and infant period the differences from adult aneurysms are striking (Lasjaunias et al. 2005), while during adolescence the adult aneurysm characteristics become progressively more apparent. Although rare, intracranial aneurysms in children have been discussed thoroughly in the literature (Kanaan et al. 1995; Herman et al. 1991; Proust et al. 2001; Meyer et al. 1989; Patel and Gupta 1971; Amacher and Drake 1975; Gerosa et al. 1980; Allison et al. 1998; Pasqualin et al. 1986; Storrs et al. 1982; Almeida et al. 1977; Ostergaard 1983). A limited number of case reports have described the role of endovascular treatment for childhood intracranial aneurysms (Cohen et al. 2003; Al-Qahtani et al. 2003; Massimi et al. 2003; Grosso et al. 2002; Dorfler et al. 2000), which include a few larger series by Agid et al. (2005) revisiting the Toronto series (Laughlin et al. 1997) and Lasjaunias et al. (2005) updating the Bicêtre series (Lasjaunias et al. 1997). Aneurysms are not congenital, as far as being already present at birth. Yet they reflect various types of structural or functional weaknesses already present in utero and expressed at a later age (see Vol. 2, Chap. 7). Stehbens (1972) and Ostergaard (1989, 1991) have pointed out that a combination of factors are responsible for the development of the saccu-

790

17 Intracranial Aneurysms in Children

Scheme 17.1. Model of the vasa vasorum and the 5-lipoxygenase pathway participation in leukocyte recruitment, arterial remodeling, and intracerebral arterial giant aneurysm formation, modified from Zhao et al 2004

lar type of aneurysm. These factors can be intraluminal, mural, or extravascular (Krings et al. 2005c) (Scheme 17.1). However, the associated conditions such as hypertension, cigarette smoking, and oral contraceptive use, although linked to the development of the adult type of aneurysms, can hardly be applied to the pediatric age group. Similarly, long-standing hemodynamic factors, such as shear stress representing intraluminal stimuli for aneurysmal development, frequently implicated in adults, likely play much less of a role in children. The average time of 15 years that it takes for a new aneurysm to develop in an adult patient with multiple aneurysms further testifies to the different factors influencing aneurysm development in adults vs children (Rinne and Hernesniemi 1993). On the other hand, there appears to be a clear association between various disease processes that are known to weaken the matrix of the blood vessel wall and the presence of aneurysms in the pediatric age group. In addition, these intramural factors probably play a very important role in the etiology of aneurysms in children (Pope et al. 1991; Taira

Introduction

791

et al. 1991; Brill et al. 1985; Waga and Tochio 1985; Schievink and Piepgras 1991). The concept of segmental identity and vulnerability is particularly well illustrated in the aneurysmal vasculopathies in children (Lasjaunias et al. 2000). Aneurysm is therefore a generic name encompassing various disorders involving the vessel wall. Aneurysm formation is likely to require both a local target (vessel wall structure or function) and systemic triggers that are more or less specific for that arterial segment. The increased incidence of aneurysms of infectious and traumatic origin in children indicates that the arterial vascular tree is more susceptible to an extrinsic cause (Figs. 17.3, 17.4) in the development of aneurysms than in adults. It also seems that the arterial vessel wall in children is more capable of a healing response to the aneurysmal acute events than it is in adults, as shown by the multiple reports of spontaneous thrombosis of aneurysms in children (Andrews et al. 1984; Choudhury et al. 1991; Tanaby et al. 1991) (Figs. 17.28, 17.31). Certain factors have been identified in animal experiments that enhance the healing process of the aneurysm wall (Kang 1990). This observation may actually illustrate the higher proportion of dissecting processes in the aneurysmal vasculopathies in the pediatric population as compared to those in adults. Aneurysmal vasculopathies in the pediatric age group are significantly different from those in adults (Kanaan et al. 1995):
There is a male dominance of 2–3:1.
There is a higher incidence of unusual sites (posterior circulation in more than 30% of cases in the Agid et al. (2005) and Lasjaunias et al. (2005) series and peripheral).
There is a predilection for the carotid bifurcation location (31%–54%).
There is a greater number of large and giant aneurysms (20%).
There is a lower incidence of multiple aneurysms (<10%).
The morbidity rate is lower.
There is a higher incidence of traumatic, dissecting, and infectious etiologies.
There is a higher incidence of spontaneous thrombosis.
Aneurysms are 1.6 times more frequently responsible for intracranial hemorrhage (ICH) than CAVMs in Caucasian groups.
Aneurysms are four times less frequently responsible for ICH than CAVMs in some Asian populations. These differences are more pronounced in early childhood and become less the case toward adolescence. In our opinion, the term “congenital aneurysm” to describe aneurysms in children should be abandoned, and the identification of an aneurysm in a child should rather raise the suspicion of an underlying disease affecting the blood vessel wall (Table 17.1). Pretherapeutic evaluation and treatment strategies should be carried out with this in mind.

792

17 Intracranial Aneurysms in Children

Table 17.1. Aneurysms and associated diseases (Weir 1987) Disease

Features

Aortic coarctation

Male:female ratio, 3:1 12% mortality rate from intracranial AA rupture Association at autopsy, 3% 21% of AAs in children are associated with AC 7% of PKD patients have associated AAss (clinical series) 16% of PKD patients have associated AAss (autopsy series) 15% mortality rate from intracranial AA rupture 5% of autopsied AA patients have polycystic changes (Walton 1956) 3%–4% of AA patients have PKD; not all are hypertensive Incidence of cervicocephalic FDM, 0.7% (Manelfe 1974) 20% of cervicocranial locations show AA, one-third multiple 50% cervical and ICA predominance 7% of renal FDM patients have AA; few hypertensive patients 16% mortality rate from AA rupture Associated TIA and infarctions String-of-beads sign on the cervical ICA Mainly extradural dissecting ICA AAs Proline metabolism dysfunction Urinary hydroxyproline Dominant Mitral valve leaflet prolapse AAs associated with renal tumor Cervical and intracranial AAs on ICA Multiple, fusiform, dysplastic, ICA, or VAAA Recurrent post-traumatic (minimal ruptures) (CCF) Type III collagen defect/fibroblast culture Usually dominant Chromosome 9q3; TGF disorder Associated visceral sites (AAs); 3% intracranial AAs (?) Associated multiple CAVF Skin manifestations rare in children Epistaxis, pulmonary fistulas, cerebral arterial strokes, brain abscesses, mycotic

Polycystic kidney disease

Fibromuscular dysplasia

Marfan’s syndrome

Tuberous sclerosis Ehlers-Danlos syndrome

Hereditary hemorrhagic telangiectasia

AA? Collagen deficiency state

Moyamoya disease

NF1 von Recklinghausen

Pseudoxanthoma elasticum

Collagen type III deficiency Female dominance Mitral valve prolapse association 5.6% associated AAs on noninvolved vessels Female dominance in children, 4:1 Half BA bifurcation (flow-related?) Disappearance reported after revascularization surgery 10% mortality rate from AA rupture Peripheral AAs (41%), basal ganglia are pseudo-AA Intracranial hemorrhages: ICH, 58%; IVH, 35%; SAH, 2% In children, AA rupture, 5%; in adults, 65% Incidence, 1 in 2,000–3,000 12% of cerebrovascular manifestations Chromosome 17 Cutis laxa; retinal angioid streaks AA wall calcifications Elastic tissue metabolism defect Systemic hypertension, aortic dilatation Lacunar infarcts Dominant or recessive

Incidence

793

Table 17.1. (continued) Disease

Features

Familial AAs in Finland

10% of patients with ruptured AAs have a family history of SAH from AAs No sex dominance MCA in 47% In incidentally diagnosed AAs, 12% of relatives carry AA

AA, arterial aneurysm; TIA, transient ischemic attack; CCF, congestive cardiac failure; CAVF, cerebral arteriovenous fistula; ICH, intracerebral hemorrhage; IVH, intraventircular hemorrhage; SAH, subarachnoid hemorrhage; MCA, middle cerebral artery; ICA, internal carotid artery; VA, vertebral artery; TGF, transforming growth factor; BA, basilar artery; AC, aortic coarctation; PKD, polycystic kidney disease; FMD, fibromuscular dysplasia.

17.2 Incidence The incidence of intracranial aneurysms in the general population varies between different countries and continents and ranges from 4.9% in North America, Europe, and Japan to 0.2% in some Middle Eastern countries (Locksley 1966; Bhagwati and Deshpande 1993). Intracranial aneurysms in the pediatric age group accounts for less than 5% (0.6%– 4.6%) of the total number of intracranial aneurysms in the general population (Locksley 1966; Nishioka 1966; Patel and Richardson 1971; Table 17.2). There have been no reports of incidental discovery of aneurysms during routine autopsy studies in children (Housepian and Pool 1958; Stehbens 1972). The higher incidence of intracranial aneurysms in women among the adult population is reversed in the pediatric population, in which the male:female ratio varies from 2:1 in infants up to 8 years of age to a nearly equal ratio of 1.2:1 in the 10- to 20-year age group (George et al. 1987; Heiskanen 1989; Meyer et al. 1989; Herman 1992; Hourihan et al. 1984; Choux et al. 1992). The change in sex ratio occurs at the fifth decade (male:female, 0.9:1) and reaches 0:3 (M:F) in the seventh decade. Yet in most recent series (Agid et al. 2005; Lasjaunias et al. 2005), the ratio was 3:2 (M:F) and even reversed to 1:4 (M:F) for aneurysms occurring during the first 2 years of life (Table 17.3). Analysis of the incidence of AA reported in clinical series, in particular those associated with hemorrhagic presentations, demonstrates that ethnic differences are significant (Table 17.4). The importance of AA vs arteriovenous malformations (AVMs) in the etiology of intracranial hemorrhage varies from one population to the next (see Chap. 4, this volume). In Asian populations, there are four times more hemorrhages from CAVMs than from AAs (Tamaki et al. 1992; Spillane 1972). However, these numbers should be re-evaluated with the advent of improved access to noninvasive neuroradiological techniques in these countries. In many instances, it was easier in the past to miss an aneurysm than an AVM. The results of autopsy series appear to support this observation.

794

17 Intracranial Aneurysms in Children

Table 17.2. Age at presentation (92 children under 18 years of age)

Table 17.3. Gender in pediatric aneurysms per age group in %

Table 17.4. Incidence of ruptured aneurysms per 100,000 inhabitants per year (Weir 1987)a Country

Incidence

Hong Kong (Chinese) Japan Denmark (Caucasians) Zimbabwe (Africans) Sweden (south) Zimbabwe (Caucasians) Faroe Island United Kingdom Greenland (Eskimos) New Zealand United States Finland

0.5 1.6 3.1 3.5 5.0 6.1 7.4 6.0–10.3 9.3 10.0 10.3 10.0–15.7

In Malaysia and Singapore, cerebral arteriovenous malformations (CAVM) outnumber arterial aneurysms 4:1 (Spillane 1972). a Most of the papers reviewed were published before the development of modern diagnostic neuroradiology.

Presentation

795

17.3 Presentation When assessing the entire pediatric age group, patients with intracranial aneurysms present with subarachnoid hemorrhage about 70% of the time (Batnitzky 1978; Roche 1988; Humphreys 1989b). The incidence of hemorrhage, however, is reported to be as high as 82% if only infants and children under 5 years of age are considered (Ferrante 1988; Choux et al. 1992). The incidence appears to progressively decrease and to be as low as 45% if only children over 5 years of age are considered (Schauseil et al. 1983; Herman 1992; Gerosa et al. 1980). Hladky (1992) reported that, among 419 patients younger than 20 years of age presenting with subarachnoid hemorrhage, 41% of cases proved to be caused by an AA and 28% by an AVM (see Chaps. 4 and 5, this volume). However, these figures were 10% for AA and 32.2% for AVM in an Asian population of 224 children under 15 years. About 35% of pediatric patients with giant-size aneurysms present with subarachnoid hemorrhage (Peerless et al. 1989). There are only five case reports in the literature describing a neonate presenting with subarachnoid hemorrhage (Schimauchi 1989; Newcomb 1949; Kuchelmeister et al. 1993; Choux et al. 1992; Lipper et al. 1978). Symptoms related to mass effect occur in about 20% of all children as the initial presenting symptom of an intracranial aneurysm (Herman 1992; Choux et al. 1992; Humphreys 1989b). Again, this appears to vary among the different age groups and is reported to be as high as 45% in the 5- to 18-year age group (Schauseil-Zipf et al. 1983; Gerosa et al. 1980). Other clinical presentations such as seizures and stroke (see Figs. 5.4, 5.6) are uncommon and occur in less than 10% of cases (Herman 1992; Batnitzky 1978; Choux 1992). When reviewing our own experience, it was noted that we had a relatively low percentage of patients presenting with SAH as compared to previously reported series (Herman et al. 1991; Proust et al. 2000; Allison et al. 1998). Many of the children in our studies (Agid et al. 2005; Lasjaunias et al. 2005) presented with a neurological deficit or headaches (Table 17.5). The type of presentation with subarachnoid hemorrhage (SAH) or intracerebral hematoma varied depending on the age of the child and was increased before 2 years of age and between 6 and 15 years of age, which coincided with the peak incidences of dissections and saccular aneurysms) (Table 17.6).

796

17 Intracranial Aneurysms in Children

Table 17.5. Clinical symptoms at presentation in relation to age in 92 cases under 18 years of age (Agid et al. 2005; Lasjaunias et al. 2005)

Table 17.6. Clinical symptoms at presentation in relation to etiology of aneurysm in % 96 children under 18 years (Agid et al. 2005; Lasjaunias et al. 2005)

Etiology

797

17.4 Etiology Large autopsy series in children have not detected incidental aneurysms (Housepian 1958). In addition, review of published histopathology reports of intracranial aneurysms led to the conclusion that a combination of intraluminal, mural, and extravascular factors are likely responsible for the development of saccular aneurysms rather than congenital mechanisms (Stehbens 1958, 1975). In our patient groups, clearly known causes were found in less than 50% of the aneurysms. Various subgroups of aneurysms can, however, be identified: traumatic (5%–10%), infectious (15%), saccular (30%), and dissections (about 50%). These numbers must be adjusted to the age at the time of referral, as dissection will be dominant during the first 5 years of life and saccular aneurysms occur between the ages of 6 and 15 (Tables 17.7, 17.8).

Table 17.7. Etiology (92 patients under 18 years of age)

Table 17.8. Age at presentation in relation to etiology in 96 patients under 18 years of age (Agid et al. 2005; Lasjaunias et al. 2005)

798

17 Intracranial Aneurysms in Children

17.5 Traumatic Aneurysms Traumatic aneurysms account for roughly 5%–15% of pediatric aneurysms (Herman 1992; Roche et al. 1988; Choux et al. 1992; Humphreys 1989b). Of these, approximately 40% involve the distal anterior cerebral artery complex (adjacent to the falx) (Fig. 17.1), 35% involve the major vessels along the skull base (Fig. 5.2), and 25% are cortical in location (Yazbak et al. 1995; Nakstad et al. 1986;Hahn et al. 1990; Ventureya and Higgens 1994; Fox 1983). The majority of these children present with a hemorrhagic episode about 3–4 weeks after the original injury. Seventytwo percent have sustained a closed head injury and 16% a penetrating injury, while the remainder had a history of various types of injuries, in-

Fig. 17.1. A A 5-year-old child presented with severe head trauma with a depression fracture in the frontal region. There is evidence of interhemispheric hematoma (arrowhead). B, C Angiography demonstrated a typical post-traumatic false aneurysm. (Courtesy of P. Nakstad)

Traumatic Aneurysms

799

Fig. 17.2A–D. A 16-year-old male with a grade 1 subarachnoid hemorrhage following mild head injury (A). Appearance of distal left internal artery was thought to be suggestive of dissection (arrow) but remained unchanged on 1-week and 6-week followup angiography (B). C, D Routine follow-up MRI/MRA and angiography showed a significantly enlarged lesion 6 years later

cluding surgery (Fox 1983; Ventureya and Higgens 1994; Sutton 1994). A giant-size aneurysm of the pericallosal artery in a 3-month-old infant was probably related to birth trauma (De Marinis 1991). Other vascular damage should be looked for in this type of situation (Taha et al. 1993). Ventureyra and Higgens (1994) noted 436 patients with traumatic aneurysms in the literature, of which 130 patients were less than 20 years of age. Tsubokawa et al. (1975) reported a total of 35 traumatic

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17 Intracranial Aneurysms in Children

Fig. 17.3A, B. A 9-year-old boy with Downs syndrome prior to spinal instrumentation. A Increased neck swelling (arrow) 1 week after surgical posterior fusion procedure. B Note the large vertebral false sac at the level of the material implanted

aneurysms, of which five (20%) healed spontaneously. Nakstad et al. (1986) reported three cases of post-traumatic aneurysms in children; all of these patients were operated on. Most of the aneurysms had increased in size at angiographic follow-up prior to further treatment (Fig. 17.2). In our series, there were few post-traumatic lesions in children; some of them were iatrogenic(Figs. 17.3, 17.4). Each case raises its own challenges depending on the associated lesions, the location of the vessel damaged, as well as the presence of an active bleed with a false aneurysm intracranial or across the skull base (see Chap. 16, this volume). A mortality rate of 31% has been reported in children with traumatic intracranial aneurysms that were not operated on. In this group of post-traumatic AAs, a false or pseudo-aneurysm from a ruptured vessel can occur, which corresponds to an extravascular space, usually within a hematoma. The progression of such lesions can sometimes be favorable with spontaneous healing of the leakage point. Rerupture has mainly been seen in false aneurysms associated with previously ruptured cerebral AVMs (Fig. 17.5). A false sac can also be seen in ruptured nontraumatic AAs at the time of the hemorrhagic episode; it is usually associated with a local blood collection or an intracerebral hematoma. Occluded AV fistulas may have an aneurysmal appearance that corresponds to its spontaneous thrombosis, possibly in association with a hematoma. Without a hematoma, the aneu-

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Fig. 17.4A–C. Patient was referred 2 years after hemorrhagic complication during third ventriculostomy (A). A post-traumatic dissecting aneurysm was demonstrated (B) and embolized with coils (even though healed dissecting arterial aneurysms usually do not rupture at long-term follow-up). Follow-up angiogram 1 year after uneventful endovascular treatment shows stable exclusion of the arterial aneurysms (AAs) (C)

rysm is in fact the venous stump of the previous drainage; with a hematoma, the aneurysm is likely to correspond to a false aneurysm cavity (Berenstein and Lasjaunias 1992a). This situation is typically encountered at the spinal cord level, but it can also be seen intracranially. Spinal cord aneurysms are extremely rare, and Djindjian (1978) only once identified such a spinal cord AA in 3,000 spinal cord angiograms performed in all age groups. It should be recalled that healed false aneurysms reaching the chronic phase do not rupture; but despite this well-known rule, persistence of a post-traumatic intradural arterial pouch will inevitably lead to the discussion regarding the importance of curative management (Fig. 17.4).

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17 Intracranial Aneurysms in Children

Fig. 17.5A–F. A 7-month-old infant presented with sudden loss of consciousness 2 weeks after moderate head injury (A). Endovascular treatment with coiling of post-traumatic aneurysm (B, C) included sacrifice of involved segment and excellent clinical outcome. D–F Six months after coiling of post-traumatic anterior cerebral artery, aneurysm shows the stability of the result and good collateral circulation via the leptomeningeal anastomoses. Arrow, retrograde opacification of the distal anterior cerebral artery

Infectious Aneurysms

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17.6 Infectious Aneurysms The term “mycotic arterial aneurysm” was proposed by Osler in 1901 to describe AAs seen during bacterial endocarditis. The designation has been kept to identify those AAs associated with an infectious state (Hurst et al. 1992). Today the term “infectious arterial aneurysm” (IAA) seems more appropriate (Micheli et al. 1989). While they can be caused by fungal infections, they are most often of bacterial origin (Barrow and Prats 1990; Bohmfalk et al. 1978; Horten et al. 1976). They account for 1.5%–9% of all intracranial aneurysms (pediatric and adult) (Clare and Barrow 1992) but account for less than 1%–2% of our interventional practice. The incidence of such IAAs will likely depend on certain specific local circumstances: for example, the presence of a cardiothoracic department for children. IAAs account for about 5%–15% of pediatric aneurysms (Herman 1992; Pasqualin et al. 1986; Choux et al. 1992; Humphreys 1989b; Whithfield and Bullock 1991; Kanaan et al. 1995; Fig. 17.6). The most common organism has been Staphylococcus, followed by Streptococcus and other Gram-negative organisms (Choux et al. 1992) (Fig. 17.7). They often complicate bacterial endocarditis in infants with congenital or rheumatic heart disease. Twenty percent of children with aneurysms of infectious origin die despite antibiotic treatment (Choux et al. 1992) (Fig. 17.8). IAAs may involve the intracavernous ICA by contiguity following severe sphenoid sinus infections with osteomyelitis and cavernous sinus thrombophlebitis (Suwanwela et al. 1972; Marsot-Dupuch et al. 2000). Cavernous IAAs are often bilateral (19%) and caused by staphylococcus infection (50%) (Fig. 17.9). They occur more frequently in children (56%). In half of the cases, their size increases on follow-up angiography, but they will disappear in 25% of cases with antibiotic treatment, with occlusion of the ICA in one-quarter of them. Another extravascular cause is meningitis. The time interval between the infectious emboli and IAA development, including rupture, can be as short as 24–48 h. The direct involvement of the arterial wall is the mechanism most often advocated. It involves an infectious process progressing from the lumen to the extravascular space (Clare and Barrow 1992). Infection extending from the outside toward the lumen involves infectious emboli originating from the vasa vasorum (Patra et al. 1986; Rice et al. 1997) (Fig 17.1). In 15% of cases, new IAAs will appear (Weber et al. 1982), and treatment should therefore be discussed carefully in every case following an appropriate course of medical treatment. Early endovascular management is sometimes mandatory for ruptured IAAs responding poorly or not at all to treatment. This may require sacrifice of the involved arterial segment. The relevance to treat several locations or unruptured IAAs will need to be discussed case by case, taking into consideration the apparent efficacy of the antibiotics on the infectious disease, the morphological changes under appropriate treatment, and the postulated risk carried by certain locations in case of hemorrhage (sphenoid sinus). The need for anticoagulation in some specific cardiac situations may also prompt in-

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17 Intracranial Aneurysms in Children

Fig. 17.6A–D. A 10-year-old boy presented with acute subarachnoid hemorrhage (SAH) and a small intracerebral hemorrhage (ICH) in the right sylvian fissure (A). This bleed was due to the rupture of a bi-lobed fusiform arterial ectasia located on the parietal branch of the middle cerebral artery (B, C). A mycotic aneurysm was suspected despite lack of evidence of an infectious focus. Conservative treatment with antibiotic therapy was chosen because of the eloquence of the territory fed by this vessel and the appearance of the AA. Thrombosis of the lesion was noted on the 6-month follow-up angiogram (D)

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Fig. 17.7A, B. Grade III SAH in 15-year-old girl with bacterial endocarditis (A). Note the basilar tip aneurysm (arrow, B)

tervention. Surgery has little to add in this pathology unless a decompressive operation for ICH needs to be performed. Several reports of aneurysms associated with the human immunodeficiency virus (HIV) can be found in the literature (Husson et al. 1992; Kure et al. 1989; Philippet et al. 1994; Fig. 17.10). These AAs are mostly fusiform. Many of them are seen in the course of an opportunistic infection. The vasculopathy is concomitant with a severe immunodeficiency; however, although an infectious cause is suspected, the agent is seldom detected. AAs develop over a short period of time, and symptoms often include ischemic strokes with arteritis and, in rare cases, hemorrhage (Philippet et al. 1994). Few cases have been described in babies, despite the frequency of septicemia in neonates (Whithfield and Bullock 1991). In our experience, these patients make up a particular group, with most lesions located in the anterior circulation (14/15 in Lasjaunias et al. 2004), which can be seen at any age. Yet the concept of infection is too narrow to account for the complexity of the disorders encountered under this heading. In fact, the term “infectious and immune” indicates the agent and the host, describing the two components of the same disorder. In addition, the mechanism of generation of these aneurysms is most likely the same: dissecting.Yet they are included in a special subgroup, as the infectious or immune environment is dominant compared to other diseases, leading to spontaneous dissections similar to Elhers-Danlos or other arterial vessel wall diseases. In children, neurovascular manifestations of AIDS differ markedly from those in adults. Whereas vascular complications in adults usually consist of vascular occlusions associated with distal emboli and compli-

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17 Intracranial Aneurysms in Children

Fig. 17.8A–E. A 1-year-old girl’s CT scan 3 h after presentation with loss of consciousness (A, B). Angiogram at 6 h after presentation demonstrated irregular-shaped middle cerebral artery (MCA) aneurysm (C). MRI at 9 h after presentation demonstrates evidence of infarction. MRA at 9 h after presentation showed apparent occlusion of several left MCA branches. Autopsy demonstrated infectious aneurysm with extensive thrombosis (D, E)

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807

Fig. 17.9A, B. A 5-year-old female presented with persistent recent headaches and acute bilateral IIIrd nerve palsy. Clinical examination found severe infectious syndrome. Angiography found bilateral cavernous internal carotid artery (ICA) infectious aneurysms (A, B) Medical treatment was provided with excellent results and remodeling occurred on the left carotid, whereas the right carotid occluded without symptoms

cations of thrombocytopenia, in children, cerebrovascular lesions are mostly due to arteritis composed of arterial sclerosis, vascular occlusions, and formation of intracranial aneurysms (Dubrovsky et al. 1998; Philippet et al. 1994; Shah et al. 1996). Although these lesions were initially considered as relatively specific (Park et al. 1990), we observed similar features in chronic mucocutaneous candidiasis (CMCC). CMCC is a rare and familial disorder of unknown etiology, characterized by recurrent infections of the mucous membranes, nails, and skin with Candida albicans (Leroy et al. 1989; Groubi et al. 1998; Sedat et al. 1999) (Fig. 17.11). CMCC is a familial disease with a primary immunodeficiency disorder that should be distinguished from the opportunistic candidosis seen in globally immunocompromised patients (steroid therapies, chemotherapies). The association of CMCC with cerebral vasculitis or aneurysm is very rare, and only three cases have been described to date: none of these patients presented bacterial, fungal, or viral infections at the time of the diagnosis, nor any coagulopathy, metabolic abnormalities, or CNS infection.

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17 Intracranial Aneurysms in Children

Fig. 17.10A–D. A 14-year-old boy suffering from acquired immunodeficiency syndrome (AIDS) with severe immunosuppression. He presented with a sudden right hemiplegia, from which he spontaneously recovered without evidence of hemorrhage

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The case reported by Sedat (Sedat et al. 1999) is typical of the type of diseases encountered in immune-deficient patients. A 7 year-old boy was admitted to emergency care for moderate headaches and vomiting of acute onset without fever. He had a long history of recurrent buccal candidosis, with episodes of onyxis lesions caused by Candida albicans. CMCC had been diagnosed at the age of 5 years. Biological and immunological investigations were unremarkable except for a slight deficit in the Ig G2 subclass. His mother and one of his brothers presented the same mucocutaneous symptomatology. Angiography of the left internal carotid artery showed a fusiform arterial dilatation of the supraclinoid internal carotid artery and a large fusiform aneurysm of the basilar artery involving the proximal part of the left posterior cerebral artery; another identical aneurysm of the distal part of the left vertebral artery at the vertebrobasilar junction was demonstrated. A follow-up angiography performed 6 months later showed an aneurysm on the left posterior cerebral artery that had appeared despite proper medical treatment. None of these aneurysms was deemed treatable. One year later, the boy presented a new subarachnoid hemorrhage. MRI and angiography showed worsening of the previously described lesions. The child died a few weeks later from massive intracerebral hemorrhage. At pathology, rupture of an aneurysm of the left ICA was suspected. Few cases of HIV-infected children with multiple and fusiform intracranial aneurysms have been described in the literature. The lesions observed were almost all of the same type: they consisted of multifocal fusiform arterial dilatations involving the major vessels of the circle of Willis, with a noted predominance for the ICA and its supraclinoid portion as well as the basilar artery. These lesions did not affect the distal parts of cerebral arteries (i.e., A3, M2–3, and P2–3 segments), with these distal arterial segments showing mostly typical appearance of arteritis including stenosis and thrombosis. In Sedat’s series (Sedat et al. 1999), the HIV cases are very illustrative of the clinical context faced in children. A 4-year-old African boy was HIV-infected by blood transfusions because of malaria. The infection was diagnosed after several bacterial pulmonary infections at that time. When he was 14, he suddenly developed right faciobrachial hemiparesis. CT and MRI revealed a recent infarct in the left internal capsule and basal ganglia; older stroke stigmata were found in the left occipital and temporal lobes. Diffuse dilatations of the left internal carotid artery (ICA) and of the left middle cerebral artery (MCA) were also demonstrated. Cerebral angiography diagnosed fusiform aneurysms of the left supracavernous ICA, extending toward the proximal part of both the MCA and anterior cerebral artery (ACA) as the same lesions on both posterior cerebral arteries (PCAs). Thrombosis in the left distal MCA territory was also confirmed. Analysis of the CSF, blood, and urine failed to reveal any bacterial, mycobacterial, viral, or fungal infection.

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17 Intracranial Aneurysms in Children

▲

Fig. 17.11A–E. Multiple fusiform AA in a 7-year-old child with familial candidosis. A, B Three-dimensional angiography shows a fusiform AA of the right ICA. C–E Three-dimensional angiography of the left vertebral artery shows a large fusiform basilar artery (BA), AA, and another fusiform AA of the distal part of the left vertebral artery at the vertebrobasilar junction. (From Sedat et al. 1999, with permission). E see p. 811

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811

Fig. 17.11E. Legend see p. 810

This 8 year-old boy was infected prenatally with HIV. He presented a severe immunologic deficit with a decreased level of T4 lymphocytes and was treated for 2 years with AZT. He had never presented any infectious problem. Neurological evaluations were normal until the patient suffered three generalized tonic-clonic seizures with no postictal deficit, but followed 2 days later by an acute stroke with right hemiparesis. CT revealed several diffuse and dilatation of the right supracavernous ICA. Cerebral angiography confirmed fusiform dilatations of the right distal ICA extending to the posterior communicating artery, and to the MCA. Identical features were observed on the left A1 segment. Occlusion of an insular branch of the left MCA was also demonstrated.

A 9-year-old girl, prenatally infected with HIV, had a long history of multiple lung infections and viral meningitis. During one of her hospitalizations for meningoencephalitis, she presented a left hemiparesis of acute onset. CT revealed focal infarction in the right internal capsule and suspected abnormal intracranial vascular dilatations. Cerebral angiography demonstrated fusiform aneurysms involving the main cerebral arteries and showed that these were associated with irregular stenotic aspects of distal cortical branches of both MCAs. No vascular thrombosis was observed. Chemical and bacteriological analysis of CSF failed to reveal any infection. The level of T4 lymphocytes was 280. None of the patients had evidence of coagulopathy, collagen vascular disease, or familial hereditary diseases, but most of them suffered from severe immunosuppressive disorders or syndromes with a long history of multiple opportunistic infections preceding the diagnosis of cerebral arteriopathy.

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17 Intracranial Aneurysms in Children

The pathogenesis of fusiform aneurysms in HIV-infected children has been discussed by several authors (Dubrovsky et al. 1998; Park et al. 1990; Philippet et al. 1994), and remains controversial. Some have proposed the vasculopathy to be secondary to an infectious cause (Dubrovsky et al. 1998; Park et al. 1990). In a review of the literature, Dubrovsky et al. (1998) found two patients with Mycobacterium avium intracellular infection, one with cytomegalovirus (CMV) infection, four patients with herpes zoster virus (HZV) infection, and two others with elevated spot-checked HZV antibody titers. On the other hand, Kure et al. (1989) and Park et al. (1990) found one incidence of a major HIV transmembrane glycoprotein (gp41) in the walls of aneurysmal arteries, suggesting a direct cause of the HIV in the formation of the arterial dilatations. Lang et al. (1992) did immunohistochemical studies but failed to detect glycoprotein gp41 in the wall of such lesions. A mycotic origin (primary infection of the arterial wall by an infectious agent) of these aneurysms is unlikely: histological and bacteriological analyses of these lesions have rarely been performed, but, when available, they have failed to detect the presence of any infectious agent. Furthermore, none of these patients had a laboratory-confirmed CNS infection at the time of the diagnosis, and no time relationship was noted between the moment of the diagnosis of the aneurysmal lesions and an infectious episode. No patient improved despite proper medical treatment. Shah et al. (1996) suggested that the aneurysmal dilatations, as the arterial thromboses and stenoses seen in this population with severe immune deficiencies, were in fact caused by lesions of panarteritis resulting in the destruction of the lamina elastica with subintimal fibrosis. This author postulated that these lesions resulted from ischemia of the arterial wall because of an inflammatory reaction involving adventitia and vasa vasorum. Krings et al. (2005c) and Zhao et al. (2004) pointed to this adventitial inflammatory cascade involving vasa vasorum and leading to arterial wall damage and dissection (Scheme 17.1). The restricted presence of vasa vasorum intracranially suggests the location of these aneurysms despite their relationship to an infectious state. The similarities between cerebral aneurysms in CMCC and in AIDS (multifocality and multiplicity, location, fusiform aspect, association with lesions of vasculitis, and absence of proven infectious cause) are remarkable. These fusiform aneurysms present the same topographic distribution and a similar vascular expression with involvement of the vessels of the base. The sparing of the distal territories and other vascular systems is also noteworthy. Such observations support the concept of segmental susceptibility of the cerebral arterial system. In Sedat’s cases (Sedat et al. 1999), the midline ventral vessels were primarily involved. Thus, it can be postulated that intracranial aneurysms in CMCC and AIDS in children reveal areas of the cerebral vasculature that apparently share the same identity or vulnerability (Campos et al. 1998; see Chap. 2, this volume). The immune disease exposes these areas to either specific or nonspecific triggers depending on the

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pre-existence of a segmental structural weakness. These vascular markings correspond to topographic anatomic phenotypes. The fact that aneurysms are not present on the distal cerebral vasculature or small vessels may reflect the interaction between the vessel wall and the perivascular space (subarachnoid for the large arteries of the circle of Willis and aneurysms vs subpial for smaller arteries and thrombosis/stenosis). Apart from their topography, the vulnerability of these arterial segments appears time-related: their expression evolves from fusiform ectasia (in the pediatric population) to occlusive arteritis (in adult patients). All these observations suggest that, more so than any direct effect on the vessel, the vascular biology is a major key to the formation of these particular diseases (Leroy et al. 1989). The fact that the lesions do not repair despite medical therapy (as is often the case with mycotic aneurysms) may indicate that these fusiform dilatations are not directly related to a pathogenic agent, but result from biological damage caused by an agent of a different nature than the classically proposed infectious or hemodynamic one.

17.7 Saccular Aneurysms The saccular type of aneurysms (mistakenly called congenital aneurysms; Fig. 17.12) remain as controversial in the pediatric age group as they are in adults. Between 50% and 70% of aneurysms in the pediatric population are believed to be of this type (Herman 1992; Choux et al. 1992). Despite their location at the bifurcation of various vessels, intrinsic hemodynamic factors almost certainly play less of a role than in adults. Mural or systemic factors are considered to be more important. A variety of case reports have described the association of AAs in the pediatric population with systemic disorders such as collagen vascular diseases (Table 17.1). Ehlers-Danlos syndrome, Klippel-Trenaunay syndrome, hereditary hemorrhagic telangiectasia (HHT), tuberous sclerosis, moyamoya syndrome, coarctation of the aorta, and fibromuscular hyperplasia have all been documented to occur in association with aneurysms in children (Pope et al. 1991; Taira et al. 1991; Roy et al. 1990; Brill et al. 1985; Waga and Tochio 1986; Takeshita et al. 1986; Vles et al. 1990) (Figs. 17.13–17.16). Evans (1983) reported a case of a 9-year-old Indian boy with an aneurysm of the left internal carotid artery. The vessel was heavily atherosclerosed and dilated. Serum lipid estimations showed the presence of type IIB hyperlipoproteinemia, with evidence of the disease in the patient’s identical twin sibling and 37-year-old father. There was also a marginal increase in serum triglycerides in a younger (4-year-old) brother. The patient’s 29-year-old mother was not affected. The patient had suffered hemolytic disease as a newborn, which resulted in subsequent mental retardation. This incident is considered to have been the result of a proven glucose-6-phosphate dehydrogenase deficiency. The aneurysm was resected and arterial continuity was ensured by using an end-to-end anastomosis.

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17 Intracranial Aneurysms in Children

Fig. 17.12A, B. Incidental discovery of a carotico-ophthalmic aneurysm in an adolescent male during exploration of an unrelated cerebral arteriovenous malformation (AVM) revealed by a seizure crisis (A). Three years after complete exclusion of the AVM, the unchanged aneurysm was successfully coiled (B)

Familial occurrence has been reported in children (Kuchelmeister et al. 1993; TerBerg 1987; Weil et al. 1988; Lozano and Leblanc 1987; Ronkainen 1993), but appears to be less frequent than in adults. Again, this observation shows that either the restricted application of neuroimaging in the pediatric population or the role played by unknown triggers over time, either as qualitative or quantitative factors, will be needed to morphologically reveal an AA. The association of autosomal dominant polycystic kidney disease (PKD) and intracranial aneurysms (IAs) is a well known occurrence in the adult age group but is rare in children. The association between the recessive form and AA is exceptional. The recessive form (infantile form) involves chromosome 4 (De Blasi et al. 1997). Most of the comments below on PKD are related to the autosomal dominant form on chromosome 16. PDK1 and PDK2 are the two recognized genes of PKD (Fig. 17.13). They are located on chromosome 16 (translocation that represents 85% of PKD, in the vicinity of Bourneville disease), and on chromosome 4, respectively. PDK is genetically heterogeneous, with two chromosomal loci accounting for the disease. When the mutation is located on chromosome 16p13.3, the so-called PKD1 gene, extrarenal manifestations such as the rupture of ICA are well known. In case of localization on chromosome 4, the PKD2 gene, the phenotype is mild and only three case reports have associated PKD2 with AA (van Dijk et al. 1995; De Blasi et al. 1997).

Saccular Aneurysms

Fig. 17.13. A A 13-year-old boy with a recessive (chromosome 4) form of polycystic kidney disease (PKD) with liver fibrosis, diagnosed when he was 4 years old, presented with SAH. Angiography showed three intracranial aneurysms: one basilar tip AA (responsible for the bleed) and a bilateral mirror-type aneurysm of MCA bifurcation. B Genetic disorders of PKD are carried by chromosome 16 or chromosome 4

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17 Intracranial Aneurysms in Children

Fig. 17.14A, B. A 5-year-old girl with neurofibromatosis NF1. Note the bilateral cavernous sinus lesions (arrows, A) and the dysplastic appearance of the ICA with fusiform ectasias (arrows, B)

Fig. 17.15. A Frontal and B lateral vertebral angiogram. Nonhemorrhagic acute medullary syndrome. Angiography demonstrates a dissecting AA involving a suspected distal vertebral artery dysplasia. Note the arterial narrowing proximal and distal to the neck of the dissecting AA

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817

Fig. 17.16A–C. A 10-year-old female patient with family history of Ehlers-Danlos IV. Sudden onset of headache without neurological deficit. Repeated headache over a 3-month period. A On MR examination, presence of thrombosed arterial pouch with surrounding edematous reaction. B, C At angiography, presence of fusiform aneurysms. The presence of a second ectasia argues for multifocal (or systemic) dysplastic disease with acute repeated dissections. (Courtesy of G. Rodesch)

The case reported by De Blasi was of particular interest:
The patient was a boy, as many children with intracranial aneurysm (IA), but different from children with IA in PKD where a female dominance is noted.
The age of bleeding was low (actually the second youngest case reported), with a good Hunt and Hess grade.
The location of the IA, usually on the anterior circulation, was on the basilar artery (laterobasilar); the IA was multifocal.
The renal function and blood pressure were normal.
The endovascular GDC approach achieved a good result and an excellent long-term clinical outcome.

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17 Intracranial Aneurysms in Children

The occurrence of bleeding at that age raises the issue of screening to ensure earlier diagnosis using noninvasive techniques such as CTA, MRA, or MRI with enhancement. The risk for future SAH from an unruptured IA discovered at screening is currently unknown. It seems that bleeding during follow-up in PKD patients mostly occurs from IAs that have not been previously demonstrated (Chauveau et al. 1994). For the associated MCA aneurysm in De Blasi’s case, there was a contraindication for endovascular treatment: a very large neck. The small size of the IA (<4 mm) and the fact that it had never bled before led to conservative management and angiographic follow-up at 5 years, confirming its stability and the long-term embolization result. No data exist regarding the outcome of unoperated children presenting with saccular AAs. Most of the familial diseases associated with AA do not express themselves during childhood, as if additional triggers with subsequent alteration of the disease or loss of compensation (second hit) is needed for the AA to develop. Heiskanen (1981) reported a mortality rate of 30% for untreated aneurysms in patients presenting with subarachnoid hemorrhage; Choux et al. (1992) reported a mortality rate of 80% in Hunt and Hess grades 4 and 5 subarachnoid children caused by AA. Nonsymptomatic vasospasm associated with ruptured intracranial aneurysms has been demonstrated in 50% of children during the first 3 days after ictus (Ostergaard and Boldby 1983), while symptomatic vasospasm occurred in 6% of patients with subarachnoid hemorrhage according to Peerless et al. (1989). In the series of Lasjaunias et al. (2004), there were a total of 24 saccular aneurysms in 16 patients. The mean age of presentation was 9 years. Out of 24 aneurysms, 21 were located on the anterior circulation. The remaining three were at the basilar tip. The most common presentation was hemorrhage in 13 out of 16 cases. Three of the patients had multiple aneurysms and among eight of the lesions diagnosed, seven aneurysms were asymptomatic. These were provisionally managed conservatively: 12 of 13 patients (92.3%) were treated (13 aneurysms in all), one of 13 were managed conservatively (branches incorporated in the aneurysm), three of 16 patients did not come for treatment, 83.3% of the lesions were completely excluded on shortterm follow-up, and in three of four of them long-term angiographic follow-up could not be obtained. One child had incomplete stable treatment. One patient died from liver fibrosis. There were several children with familial diseases associated with aneurysms: cystic fibrosis associated with multiple berry aneurysms, PKD, tuberous sclerosis (with dissecting aneurysms), and sickle cell anemia with single saccular aneurysm. Multiple saccular aneurysms in the same patient, frequently seen in adults, are rare in children (Kanaan et al. 1995) (Figs. 17.17, 17.18). Only 2% of children with saccular aneurysms in a review by Choux et al. (1992) showed multiple aneurysms. The incidence of multiplicity is higher in children with aneurysms of infectious origin (15%; Choux et al. 1992). In fact, the multiplicity is low in the saccular aneurysms in comparison to

Saccular Aneurysms

Fig. 17.17A–E. Twin aneurysms: ICA anterior division bifurcation. Young female presented with grade 1 SAH. Angiography at day 1 failed to show any aneurysms (A, B). At day 30, repeated examination shows ICA bifurcation aneurysm (C). On the right side, a similar lesion, although smaller, was seen at 1 year (D) and 2 years (E)

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17 Intracranial Aneurysms in Children

Fig. 17.18A–D. Grade 2 SAH in a 12-year-old child (A, B). Note the unusual twin aneurysms at the ICA bifurcations (C, D). Both were coiled in several sessions

adult groups but is high if one considers the dissection etiology group and even more so among the infectious and immune-compromised children. Flow-related aneurysms associated with CAVMs are not seen in the pediatric population. Although the highest flowing shunts are encountered in this age group, no report exists of flow-related AAs; most cases are in fact false AAs in ruptured AVMs. The microlesion may not be seen at the acute stage, and the false sac becomes the actual therapeutic target (Fig. 17.19) (see Chap. 5, this volume). Obviously, the remodeling capabil-

Saccular Aneurysms

Fig. 17.19A–C. A 4-year-old boy presented with a deep-seated hematoma with angiographic evidence of a false aneurysm (A). The lesion was immediately embolized with glue (B, C)

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17 Intracranial Aneurysms in Children

Fig. 17.20. Juvenile dural AVS. Note the aneurysms on the middle meningeal artery

Fig. 17.21A, B. Two cases of PHACE syndrome with intratympanic aneurysms developed from a segmental ICA agenesis (A) and from a tympanomeningeal variant (B)

ity, the impact of shear stress, and time elapsed constitute some of the variables involved in the differences from the adult population that can be observed. The only lesions that are associated with aneurysmal formation in relation to secondary shear stress changes are observed in the juvenile type of dural AVS and actually involve the external carotid dural branches and occur at their bifurcations (Fig. 17.20) (see Chap. 7, this volume).

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823

Fig. 17.22A, B. External carotid aneurysm on the maxillary (A) and facial (B) arteries in a patient with CAMS 2

Additional aneurysms seen in children and likely to correspond to an underlying specific dysplastic disease are the ones associated with the PHACE (Chap. 12, this volume) (Fig. 17.21) and CAMS (Chap. 6, this volume) (Fig. 17.22) syndromes. These two syndromes illustrate the angiogenic nature of some aneurysmal vasculopathies.

17.8 Dissecting Aneurysms The incidence of dissecting AA is probably underestimated, since a narrow segment of the parent vessel proximal or distal to the AA is often present but ignored in this population. Such a feature is relatively frequent in supraclinoid or ICA termination AAs (see Fig. 17.23). In Agid’s study (Agid et al. 2005), the diagnosis of dissection was made by the angiographic appearance (preaneurysmal narrowing and fusiform shape) or the presence of overt dissection involving the other vertebral artery. Most of the dissecting aneurysms in her series were found to involve the posterior circulation, which was also the case in more than 50% of Lasjaunias’s (2005) cases. Both recent series contained a large number of nontraumatic dissecting aneurysms as compared to the numbers reported in the literature (Massimi et al. 2003; Ohkuma et al. 2002, 2003). This is probably still an underestimation of nontraumatic dissection as a cause of aneurysmal dilatation in children. In most institutions, this is mainly because some of the dissections were probably diagnosed as transient angiopathy of childhood and thus not recorded in the aneurysm groups (Agid et al. 2005).

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17 Intracranial Aneurysms in Children

Fig. 17.23A–F. Legend see p. 825

▲

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825

Fig. 17.23A–F. A 4-year-old boy presented after gastroenteritis syndrome with significant headaches and vomiting. No deficit was found on neurological examination. A, B Computed tomography (CT) revealed a bilobed, rounded structure in the sellar and left cavernous sinus region. Angiography showed C the internal carotid artery (ICA) aneurysms and D spontaneous supply from the opposite side. E The ICA was sacrificed. F Follow-up tests at 1.5 years confirmed the stability of the result. Note the preservation of the supply to the orbit and the visibility of the choroid crescent

Fig. 17.24. A Early and B late phase of a common carotid angiogram. Fusiform dysplastic segmental AA of the ICA in a child. The first cervical ICA segment is involved and the glomus as usual is preserved. (Courtesy of S. Pongpech)

The dissecting aneurysm group is related to a specific type of mural damage, which may actually ignore the fact that spontaneous dissections in babies may result from an unrecognized immune type of segmental aggression or segmental vascular failure (Figs. 17.24, 17.25). The frequency of dissecting aneurysms in the pediatric age group is four times that of adults. The mean age of the child with dissecting aneurysm was 6 years. Dissecting aneurysms are difficult to manage, as they may form on a dysplastic artery.

826

17 Intracranial Aneurysms in Children

Fig. 17.25. A 12-year-old boy who presented with segmental fusiform dysplastic AA

In Lasjaunias’s series (2005), out of 34 dissecting aneurysms in 33 patients:
Eight patients (24%) did not come for treatment.
Of the 25 remaining, – Three of 25 patients (12%) were treated conservatively, as they were at high risk for neurological deficit from treatment. – Seven of 25 (28%) underwent spontaneous thrombosis: five of seven underwent complete thrombosis, and two of seven had a small residual, which was treated. – Seventeen of 25 (68%) underwent treatment including the two mentioned above. – Eleven of 17 (64.7%) underwent primary parent artery sacrifice. – Two of 17 (11.8%) had proximal arterial occlusion with reversal of flow. – One of 17 (5.9%) underwent coiling selectively to occlude the aneurysm. – Three of 17 (17.6%) underwent surgery. In one case, a dissecting intradural VA aneurysm was successfully treated by proximal parent artery occlusion in a 2-month-old infant. The aneurysm was controlled and remained excluded. Two years later, she had a fatal hemorrhage in the same region of the previously existing aneurysm. In our experience, this is unlikely to have been a failed treatment but rather a new expression of an uncontrolled disease, as observed with the de novo aneurysms seen in the adult group (Vol. 2, Chap. 7). Focal arterial stenotic segments are often observed proximal or distal to the dissecting aneurysm, suggesting mural damage. Impaired vessel wall with stenosis can induce spontaneous thrombosis. Isolated cases of spontaneous thrombosis of aneurysms in the pediatric age group have

Dissecting Aneurysms

827

Fig. 17.26A–C. A 20-month-old girl presented with sudden right-sided deficit. Occlusion of the left MCA with a roundish lesion and possible mural hematoma, suggesting dissection (A, B). At angiography, the lesion is fully thrombosed (C)

been reported (Waga and Tochio 1985; Andrews et al. 1984; Choudhury et al. 1991; Tanabe et al. 1991; Figs. 17.26–17.28). In our series, spontaneous thrombosis of a large part of the dissecting aneurysm could occur in 3 weeks to 7 months. Some of the dissecting aneurysms heal spontaneously, leading to associated occlusion of the parent artery. This is often well tolerated in the child due to good collateral circulation via the circle of Willis or pial collateral anastomoses. Often the dissecting aneurysm requires endovascular parent artery occlusion as treatment. Dissecting aneurysms of the MCA (M1), or ACA (A1) are the most difficult cases to manage because of the absence of a neck and the involvement of perforating arteries arising from the dissected aneurysmal wall. These tend to be unstable and rebleed rapidly (Figs. 17.29, 17.30).

828

17 Intracranial Aneurysms in Children

Fig. 17.27A–D. A 7-year-old boy with unremarkable personal and family history presented with headaches and vomiting following minor head injury. Persistence of the symptoms led to CT (A), MRI (B) and MRA, which showed a partially thrombosed giant MCA AA without SAH. The lesion is deemed to be unrelated to the trauma. Neurological examination is normal. Four days later, angiography (C, D) showed complete thrombosis of the AA. There is evidence of MCA temporal branch occlusion with focal narrowing, as shown from the frontal ICA projection and the collateral circulation around the temporal lobe on the vertebral injection, suggesting a spontaneously repaired MCA branch dissection

▲

Fig. 17.28A–F. A 2-year-old boy in good health until 12 days prior to admission, when he experienced a sudden onset of right-sided hemiplegia and aphasia and left-sided third nerve palsy. A The patient was admitted to a local hospital, where he was investigated by CT, which showed a suprasellar lesion of blood density, extending to the left cerebral peduncle with surrounding edema. A, B MRI confirmed this finding. The child gradually recovered from this deficit with persisting right-sided hemiparesis. C, D Cerebral angiography was performed and confirmed a basilar tip aneurysm that was partially thrombosed. The child was treated with aspirin and 1 year later complete remodeling was noted on MRI (E, F) associated with normal neurological examination

Dissecting Aneurysms

Fig. 17.28A–F. Legend see p. 828

829

830

17 Intracranial Aneurysms in Children

▲

Fig. 17.29A–G. A 16-year-old female patient presented with progressive right-sided deficit without headaches. A MRI shows a deep-seated stroke in relation to a fusiform AA, as seen on MRA (B) and angiography (C). Occlusion of cortical arteries and the aspect on 3D (D) and endoscopic (E) views argue for the diagnosis of embolic events from a partially thrombosed AA. Dissection is suspected. During the subsequent 3 weeks, she recovered from her stroke while on antiplatelet therapy. She was scheduled 2 weeks later for M1 occlusion with superficial termporal artery-middle cerebral artery anastomosis, but 1 week before her admission for such treatment, she presented with SAH (F, G) and a GCS of 3. The AA likely was an unruptured fusiform AA that continued to dissect, initially involving M1 perforators and subsequently extending into the subarachnoid space. E–G see p. 831

Dissecting Aneurysms

Fig. 17.29E–G. Legend see p. 830

831

832

17 Intracranial Aneurysms in Children

Fig. 17.30A–C. A 13-month-old boy presented recurrent SAH and ICH 2 weeks apart. Angiography in conventional (A), 3D (B), and endoscopic view (C) shows acute dissecting aneurysm of the MCA

They often require the sacrifice of the parent artery, frequently not done early enough in view of its eloquence and the feared risk of associated neurological deficit. In these instances, surgery faces the same challenge with a paper-thin arterial wall. Dissecting aneurysms presenting with deep-seated ischemic infarcts should therefore be analyzed with great care. Schematically two types of dissections can be encountered (Agid et al. 2005; Lasjaunias et al. 2005): 1. Extensive vessel wall damage (fusiform or wide-neck saccular aneurysms) without evidence of mural hematoma; patients may present with a deep-seated stroke or a SAH. Early recurrence of rupture often occurs during the first few days. Aggressive treatment is recommended Fig. 17.29).

Dissecting Aneurysms

833

Fig. 17.31A–D. A 16-year-old male patient presented with right-sided weakness and left ophthalmoplegia. A, B Midbrain infarct (arrow). Evidence of a dissecting P1 PCA AA (small arrow), well demonstrated on vertebral angiogram (C). Anticoagulation treatment for 6 months resulted in complete clinical recovery with aneurysm healing and arterial remodeling (arrow) (D)

2. Focal lesions that can be of large size (giant or large saccular aneurysms) with evidence of recent mural hematoma on CT or MRI. Presentation is often ischemic and spontaneous healing with completion of the lumen thrombosis is frequently observed; medical treatment with aspirin or even anticoagulation is recommended; anti-inflammatory treatment may have to be discussed (Krings et al. 2005c) (Figs. 17.28, 17.31). Repeated small hematomas that are intramural in location may lead to formation of the onionskin pattern of thrombotic layers on CT and MRI. The clots associated with the giant aneurysms are not intraluminal in location but are intramural.

834

17 Intracranial Aneurysms in Children

Fig. 17.32A–F. A 2-year-old boy presented with increasing headaches and vomiting. MRI (A, B) shows a giant partially thrombosed ICA AA mistaken for pituitary tumor. C, D Complex shape with multiple communicating chambers from a large partially thrombosed saccular lesion of the intradural ICA. The ICA was sacrificed with excellent clinical tolerance. Two years later, shrinkage of the mass is completed (E, F)

Location

835

Giant aneurysms, as seen in adults (see Vol. 2, Chap. 7), should not only be distinguished because of their size, but also as a group within the dissection category. They seem to constitute a specific type of mural failure (perhaps disease). The natural history of these unruptured AAs differs depending on their size (International Study of Unruptured Intracranial Aneurysms Investigators 2003), but the presence of mural clot distinguishes them from the fully patent lumen of the saccular aneurysms. Their frequency is higher in children. Giant-size aneurysms are roughly four times more common in children than in adults. A 20% incidence of giant-sized aneurysms has been reported in children under 20 years of age (Herman 1992; Choux et al. 1992), although an even higher incidence rate has been reported in certain centers (Humphreys 1989b, 29%; Peerless et al. 1989, 48%; Meyer et al. 1989, 54%) (Figs. 17.28, 17.32).

17.9 Location Almost three times as many aneurysms involve the posterior circulation in the pediatric age group as in adults (15% vs 5%; Choux et al. 1992). This incidence has been reported to be even higher in certain referral centers (Myer et al. 1989, 42%; Amacher et al. 1979, 59%). A fivefold increased incidence of internal carotid artery termination aneurysm has been noted in comparison to adults. Various authors have reported an incidence of 24%–54% for this location (Mazza et al. 1986; Heiskanen 1981; Pasqualin et al. 1986; Hourihan et al. 1984; Almeida et al. 1977; Gerosa et al. 1980; Sedzimir et al. 1973; Storrs et al. 1982; Patel and Richardson 1971; Ostergaard and Boldby 1983, 1989) compared to an incidence of less than 5% in adults (Locksley 1966). The anterior communicating artery location is rare in infants and young children but becomes the most common site (35%) in children over 15 years of age (Pasqualin et al. 1986). Recent reviews (Agid et al. 2005; Lasjaunias et al. 2005) demonstrate that depending on the type of referral the most frequent location will in fact vary (Table 17.9). This observation accounts for the wide range of numbers quoted in the literature that did not discriminate among the various etiologies. In particular, among infectious, immune, and saccular aneurysms, there is a clear preference for involvement of the anterior circulation, whereas the posterior circulation predominantly involves dis-

Table 17.9. Location of 112 aneurysms (from Agid et al. 2005; Lasjaunias et al. 2005)

836

17 Intracranial Aneurysms in Children

Table 17.10. Location of 112 arterial aneurysms in 96 children under 18 years of age in relation to etiology (Agid et al. 2005; Lasjaunias et al. 2005)

sections. The age profile of the referred children will also impact the type of etiology faced and consequently the location of the aneurysms (Table 17.10). The likelihood of multiplicity of the lesions in a given child will also depend on the etiology of the aneurysm (Sedat et al. 1999; Agid et al. 2005; Lasjaunias et al. 2005)

17.10 Therapeutic Strategies The treatment of children presenting with saccular aneurysms has so far largely consisted of surgery, with a good outcome in 60%–80% of children operated on (Pasqualin et al. 1986; Mazza et al. 1986; Myers et al. 1989; Kanaan et al. 1995). Surgical mortality rates reflect both the natural history of the disease and the degree of surgical difficulty, and are reported to be in the 20% range (4%–40%; Myers et al. 1989; Humphreys 1989b; Choux et al. 1992). In a cooperative study, Roche et al. (1988) reported that, taking all grades of lesions together, 63.4% of the children were cured without any sequelae, 19.5% were 1 year behind at school but were able to lead a normal life, and 4.8% remained severely handicapped; the overall postoperative mortality rate was 12.3%. Cerebral plasticity and tolerance of spasm in children are fundamental features of this aneurysmal pathology, which partially explains the favorable result obtained by surgery. Giant aneurysms have been surgically treated, although mostly by means of trapping, proximal occlusion (Little et al. 1986) and various bypass procedures, and in less than 30% by surgical clipping of the

Therapeutic Strategies

837

Fig. 17.33. Saccular type of aneurysm illustrating the relevant parameters involved in the pretherapeutic evaluation of the endovascular treatment. A Largest aneurysm diameter; O, largest orifice diameter; PA, parent artery diameter. The A/O ratio indicates the stability of the coils, whereas PA/O predicts the preservation of the parent artery

aneurysm. In the series of Proust et al. (2001), a microsurgical procedure was performed in 17 out of 22 children (77.3%), an endovascular approach used in four (18.2%), and a combined approach in one (4.5%). The overall outcome was favorable in 63.6%, with a mortality rate of 22.7%. Traumatic aneurysms can be surgically treated, although the outcome is directly related to the severity of the underlying head injury. The difference between false and dissecting aneurysms is crucial. No endovascular filling of a ruptured pouch should be performed or, if it was, then only under very restrictive conditions. Infectious aneurysms are primarily treated with antibiotics, but in some instances early clipping or coiling has been performed, often associated with no reconstruction of the parent artery. Balloon occlusion of large aneurysms, with sacrifice of the parent vessel, was first reported in a child by Lapresle et al. (1979) and subsequently by Higashida et al. (1991) and Banna et al. (1991) with a good outcome, while Numaguchi et al. (1992) described a case of intra-aneurysmal deposition of platinum coils in a child with a good outcome. Endovascular treatment of aneurysms in children (Figs. 17.33–17.35) follows the path already established for endovascular treatment of vascular malformations in childhood and aneurysms in adults (Berenstein and Lasjaunias 1992a; Casasco et al. 1993; Fox et al. 1987; Guglielmi et al. 1992; Halbach et al. 1994; Higashida et al. 1991). Most of the literature regarding the results of endovascular treatment for pediatric aneurysms are case reports (Cohen et al. 2003; Al-Qahtani et al. 2003; Massimi et al. 2003; Grosso 2002; Dorfler 2000), and only a few publications report management strategies and outcome of larger series (Agid et al. 2005; Lasjaunias et al. 2005) (Tables 17.11–17.13). In our combined experience of nearly 100 cases, the overall management was the following: 20% of the aneurysms were treated surgically (clip, ligation, completion with coils), 50% by endovascular means (coils; Figs. 17.34, 17.35), reversal of flow changes induced by remote vessel occlusion (Fig. 17.36), parent artery occlusion with balloons (Fig. 17.23), coils (Figs. 17.37, 17.38), or glue (Figs. 17.39, 17.40), and 30% were managed conservatively either because of

838

17 Intracranial Aneurysms in Children

Fig. 17.34A–D. Carotid termination aneurysm presenting with grade IV subarachnoid hemorrhage (A); the aneurysm (arrow) (B) was coiled in emergency (arrow; C). Despite neck remnant, 1-year follow-up shows completion of the exclusion (arrow; D)

Therapeutic Strategies

839

Fig. 17.35A, B. Typical aspect of 3D angiogram in a ruptured aneurysm of the anterior communicating artery in a child (A, B)

Table 17.11. Aneurysm treatment strategies per age group

spontaneous occlusion or because an acceptable approach could not be proposed. Global results in aneurysm management in children are meaningless and the results per type report small numbers. Yet the indications for treatment are endovascular for saccular lesions and conservative and medical management for infectious and dissecting lesions, in particular when multifocal. Surgery has few indications and stenting, although of theoretical interest, still has no established place in the armamentarium of tools to be used in children. Revascularization and active sacrifice associated with large-vessel wall tears, on the other hand, must be rapidly carried out to counterbalance the very poor natural history of this specific type of dissection in children (Figs. 17.41, 17.42). Overall, our capacity

840

17 Intracranial Aneurysms in Children

Table 17.12. Aneurysm results in 92 patients under 18 years of age

Table 17.13. Embolization results in 53 aneurysms treated with more than 5 years of follow-up

Therapeutic Strategies

841

Fig. 17.36. A–C A young boy treated after SAH when he was 7 years old by occlusion of both vertebral arteries. Progression of good collaterals to posterior inferior cerebellar artery (PICA) but still open to the same aneurysm. Second SAH 3 years after occluded VA (D, E). Retrograde catheterization via the posterior communicating artery was achieved and the residual aneurysm coiled (F, G). Then we were able to occlude the aneurysm (and mid-basilar flow) with no complications. Excellent recovery, but the patient needed a shunt. (Courtesy of J. Bakke). E–G see p. 842

842

17 Intracranial Aneurysms in Children

Fig. 17.36. E–G Legend see p. 841

▲

Fig. 17.38A, B. A 13-year-old girl presented with migraines associated with trigeminal type of neuralgias. Note the pons artery aneurysm (A). One year after coil embolization, the results are satisfactory and the patient is asymptomatic (B)

Therapeutic Strategies

Fig. 17.37A–C. A 12-year-old girl presented with recurrent episodes of seizures or transient ischemic attacks (TIAs). PCA dissecting aneurysm (A) was treated with endovascular coiling (arrow) and sacrifice of ectatic vessel segment (B). Asymptomatic following intra-aneurysmal vessel sacrifice with excellent collateral flow (arrows) to the distal territory (C)

Fig. 17.38A, B. Legend see p. 842

843

844

17 Intracranial Aneurysms in Children

Fig. 17.39A–E. An 8-year-old boy presented with intraventricular hemorrhage (A) and focal hematoma in the temporal lobe (B) 2 weeks after minor trauma. A PCA aneurysm was demonstrated on the angiogram (C) and immediately successfully embolized with glue (D, E)

Therapeutic Strategies

Fig. 17.40A–F. Legend see p. 846

845

846

17 Intracranial Aneurysms in Children

Fig. 17.40A–I. An 8-year-old girl. Acute cerebellar syndrome without hemorrhage MRI shows a roundish aneurysm with stagnant flow, suggesting dissection (A). Angiography (B, C) and embolization with glue (D) were immediately performed. Since the parent artery was preserved (E), an early follow-up was scheduled to verify the stability of the dissecting process. Three weeks later, the angiogram showed an increase in the aneurysm size and opacification of the lumen (F); the child has almost completely recovered. The parent artery was then sacrificed with glue. Six-month follow-up showed complete exclusion (G). The child worsened with the residual cerebellar syndrome following this session (H, I) and is currently recovering

Therapeutic Strategies

Fig. 17.41A–D. Legend see p. 848

847

848

17 Intracranial Aneurysms in Children

Fig. 17.41A–G. A young boy presenting with grade 1 SAH had this dissecting aneurysm of the intradural internal carotid (A–C). He was operated on and during the operation dissection was confirmed. Only partial clipping was done. The follow-up angiogram 10 days after the initial one (D, E). Two weeks later, he came to the consultation with a CT performed the day before (F). There is evidence of a temporal tip hematoma. An angiogram was immediately done and leakage from the aneurysm was noted during the examination. Despite sacrifice of the ICA, he died a few days later from this second hemorrhage and ischemic complications (G)

to recognize the disease process involved will result in a management strategy that ranges from conservative management to the most aggressive interventions. In our experience, rebleed after endovascular or surgical treatment is extremely rare and has occurred only once in a dissecting aneurysm that was clipped (Fig. 17.41). It certainly warrants early angiographic followup with immediate embolization if needed when the primary result is not fully satisfactory (Figs. 17.40, 17.42). Antiplatelet medication such as aspirin is used to prevent distal stroke of thrombotic origin from a large partially thrombosed AA or following the sacrifice of the parent vessel in a giant AA. We tend to make frequent use of this preventive measure.

Therapeutic Strategies

Fig. 17.42A–F. Legend see p. 850

849

850

17 Intracranial Aneurysms in Children

Fig. 17.42A–G. A 15-month-old boy presented with SAH (A). Angiography and embolization were done in emergency circumstances (B, C). Three weeks later, recurrent SAH; angiogram showed enlargement of the previous pouch (D). The parent artery was occluded with coils (E–G). No further recurrence. (Courtesy of P. Courteoux)

18 Arterial Ischemic Stroke

18.1

Introduction 851

18.2

Epidemiology 852

18.3

Pathophysiology 852

18.4

Clinical Presentation 853

18.5

Imaging of Arterial Stroke in Children 856

18.6

Outcome and Prognosis 860

18.7

Etiology 866

18.8

Cardiac Disorders 867

18.9

Acute Regressive Cerebral Arteriopathy 870

18.10

Dissections 878

18.11

Moyamoya Disease 885

18.12

Hematological Disorders and Coagulopathies 892

18.13

Metabolic Disorders 893

18.14

Proliferative angiopathy 893

18.15

PHACE 899

18.16

Hereditary Hemorrhagic Telangiectasia, or Rendu-Osler-Weber Disease 899

18.17

Spinal Cord Strokes 899

18.18

Treatment and Management 905

18.1 Introduction Although isolated cases of stroke in the pediatric population were documented in the eighteenth and nineteenth centuries, no significant epidemiological data became available until the late 1970 s. Most case reports and review articles in the past focused on the various causes of underlying pathologies that can occur in children presenting with stroke. Few reports have dealt with the outcome of stroke in the various age groups, why such differences might occur, and how treatment might affect them. In fact, the treatment of stroke in children has been mainly geared toward the management of the underlying causes, and few reports concern the active treatment of the stroke itself, such as blood-vessel reperfusion techniques and brain protection methods. Today both approaches need to be dealt

852

18 Arterial Ischemic Stroke

with simultaneously, as they deal with two different challenges, immediate and late: understanding the etiologies open to future more elective care and preventive measures. Confusion has resulted from gross epidemiological figures that confused significantly different diseases and outcomes. A vast amount of data has recently become available through basic research and neuroimaging techniques, shedding new light on the chain of events that occur in ischemic stroke in animal models and in the adult population. Whether this new information can also be applied to the pediatric population remains to be seen, but it is likely that the active management of children with acute ischemic stroke in the near future will include blood-vessel reperfusion methods and brain protection treatments.

18.2 Epidemiology Vascular occlusive disease in children is rare and probably varies in children with different ethnic backgrounds. Two population-based studies in the United States have indicated the incidence rate of ischemic and hemorrhage stroke to be 2.52 cases per 100,000 per year (Schoenberg et al. 1978) and the rate of ischemic stroke to be 1.2 cases per 100,000 per year (Broderick 1993). Prospectively collected data from 1985 to 1993 in France found the incidence to be 8 per 100,000 (Giroud et al. 1995). These data were for children less than 15 years of age and did not include stroke caused by germinal matrix hemorrhage. Unpublished data from the Canadian Pediatric Ischemic Stroke Registry (DeVeber et al. 2000; DeVeber 1995, personal communication) suggest the combined incidence rate of ischemic stroke and sinovenous thrombosis in Canadian children to be 1.2 per 100,000 per year. Arterial ischemic stroke occurred three times more frequently than sinovenous thrombosis in this population. The age distribution of stroke reveals a fairly equal incidence from age 2 onward and a significantly increased incidence during the neonatal and infancy periods. Seasonal peaks have also been noted (Riikonen and Santavuori 1994; Sébire 1995)

18.3

Pathophysiology

Interruption of blood flow to part of the brain has a destructive effect related to the high cerebral metabolic rate and the paucity of energy stores in the brain (Trescher 1992). The cerebral metabolic rate for oxygen is 3.5 ml/100 mg brain per minute with virtually no oxygen reserves available, creating rapid loss of consciousness if the oxygen supply is interrupted. Brain glucose storage is slightly larger, allowing for survival of brain tissue for up to 90 min if adequate oxygen is supplied. Neonates can use lactate as a substrate for the production of energy, but this capability is quickly lost (Hernandez et al. 1980). Neuronal activity determines the cerebral metabolic rate; seizures increase such activity, while coma reduces it. Metabolic activity is maintained by adequate cerebral blood flow (CBF). In adults, CBF is 50 ml/100 mg brain tissue per minute. In children under 3 years of age, CBF is approximately

Clinical Presentation

853

30–50 ml/100 mg brain tissue per minute, while in children aged 3–10 years these levels significantly increase to about 100 ml/100 mg brain tissue per minute and diminish again to the adult level during the late teens.Other factors influencing CBF are perfusion pressure, intracranial pressure, and vascular resistance (Volpe et al. 1982). Increased concentration of oxygen causes vasoconstriction, while increased concentration of carbon dioxide causes vasodilatation of the intracranial vasculature. Autoregulation has not been very well studied in the pediatric population, and its role is in particular not well understood in neonates and preterm infants (Golden et al. 1989). Focal interruption of blood flow produces regional hypoxia, depletion of high-energy compounds such as adenosine triphosphate (ATP), and decreased carbohydrate stores.With the depletion of ATP, critical energy-dependent enzymes become inactive. Some of these control the important ion pumps that maintain the gradients of Ca2+, Na+, K+, and Cl– (Trescher 1992). A major factor in the pathophysiology of neuronal injury is the overactivation of excitatory amino acid (EAA) receptors. This leads to increased entry of Ca2+ into the neuron through specific receptor-mediated channels. Ca2+ is toxic to the neuron through a variety of mechanisms, including activation of degrading enzymes, impairment of mitochondrial function, and altered gene expression (McDonald et al. 1990). Regional hypoxia, which develops during ischemia, produces a shift from oxidative metabolism to glycolysis. Under such conditions in adults, glucose is metabolized to lactate, which accumulates and produces acidosis, which in turn exacerbates hypoxic injury.In the neonatal brain, perhaps because of differences in glucose and lactate metabolism, this effect does not appear to occur (Vannucci et al. 1990). Another important process contributing to neuronal injury is the formation of free radicals. Free radicals are atoms or molecules with an uneven number of electrons in the outermost orbit. Under hypoxic-ischemic conditions, the normal mechanisms for metabolizing free radicals are impaired. The free radicals contribute to tissue injury by damaging the fatty acid components of cell membranes (Trescher 1992). Damage to neurons and glia and destruction of the blood–brain barrier produce localized cerebral edema, which in turn compresses capillaries and causes further damage (Golden 1989). The localized region of metabolic acidosis produces dilatation of surrounding blood vessels; this increased vascularity is called luxury perfusion. Occlusion of venous structures initiates a similar chain of events, and because of the increased venous pressure there is a tendency for blood vessels to rupture and produce bleeding and for increases in intracranial pressure to occur.

18.4 Clinical Presentation The in utero occurrence of stroke has been reported (Ong et al. 1983; Clark et al. 1954), although the clinical expression was often not apparent until days or weeks after birth, depending on the extent of the infarction. Autopsy findings in babies who died shortly after birth have demonstrated infarcts to have occurred in utero (Barmada et al. 1979).

854

18 Arterial Ischemic Stroke

Fig. 18.1A–E. Legend see p. 855

Clinical Presentation

855

Fig. 18.1A–G. Presentation of three members of a family with HHT (Rendu-Osler-Weber) disease. A, B A 7-month-old boy presenting with a neonatal left-sided hemiparesis with right third nerve paralysis. MRI performed prior to consultation resulted in pictures compatible with the diagnosis of vascular malformation. Eight months later, there was already some atrophy and retraction without evidence of recovery. In the family history, there had been two additional cases of stroke in childhood. C, D A 24-year-old man presenting at birth with a right-sided hemiparesis. The deficit was not explored; he went to school and at the age of 8 he had repeated convulsive episodes several times a week. He has a major deficit with severe hemiatrophy of the right upper limb. E, F A 26year-old man presenting with a left-sided hemiparesis at the age of 12 years. He has a mild faciobrachial deficit and no sensory deficit or telangiectasia; chest X-ray demonstrated typical pulmonary fistula (G). The rest of the family has epistaxis or tongue malformation (see genealogical tree, Scheme 2.16). The diagnosis of hereditary hemorrhagic telangiectasia (HHT) (Rendu-Osler-Weber) disease was easily made. Careful search for pulmonary fistula has already proved fruitful in one of them

Neonates with strokes tend to present with convulsions and rarely, if ever, with an appreciable focal neurological deficit in the acute phase. The neurological deficit slowly becomes apparent over the next few months to year (Bouza et al. 1994). Delayed presentation of neurological deficit such as decreased hand use (Fig. 18.1) occurred in 18 of 22 patients with presumed prenatal or perinatal arterial ischemic stroke and 12 of 22 developed permanent signs of speech, cognitive, or behavioral deficits on longterm follow-up (Golomb et al. 2001).

856

18 Arterial Ischemic Stroke

Table 18.1. Clinical manifestations of ischemic stroke in children (review of 34 patients; Sébire 1996) Manifestation

Patients (%)

Hemiplegia Disturbed consciousness Aphasia Convulsion Lateral hemianopia Locked-in syndrome Biopercular syndrome Ataxia Diplopia

76 35 18 17 6 6 3 3 3

Infants tend to present with pathologically early hand preference as a sign of previous stroke. The actual time of onset of the stroke often cannot be determined (Lanska et al. 1991). In fact, progression is often similar to that in patients whose strokes were (incidentally) identified during the perinatal period. The clinical presentation not infrequently consists of fever, convulsion, and coma.In children, presentation of stroke in later childhood is typically an acute neurological deficit, usually hemiparesis with or without seizures and with improvement of the deficit over time (Fig. 18.7). Seizures, fever, headaches, and altered levels of consciousness may occur, but these are much less frequently associated with stroke in older children (Trescher 1992; Niagara et al. 1994; Sébire 1995; Table 18.1).

18.5 Imaging of Arterial Stroke in Children Imaging studies are helpful in distinguishing ischemic and hemorrhagic infarction from cerebral hemorrhage as a cause of sudden neurological symptoms. CT is still considered to be the modality of choice to detect the presence of hemorrhage acutely after the onset of symptoms, but is often normal within the first 12 h after ischemic stroke (Ball 1998). MRI is able to demonstrate evidence of early infarction even in the first few hours after the onset of symptoms (Fig. 18.2), but is probably less accurate than CT in detecting hemorrhage at that stage. Cerebral angiography is still considered to be the best method to visualize the extra- and intracranial vasculature, but continued improvements and refinements in time-of-flight MR angiography (MRA) or MRI with contrast enhancement have made this modality a realistic noninvasive alternative, particularly in the pediatric population (Fig. 18.2) (Wiznitzer and Masaryk 1991; Vogl et al. 1992; Zimmerman et al. 1992; Allison et al. 1994; Maas et al. 1994; Husson et al. 2002). While MRA and DSA were equally sensitive in diagnosing large-vessel involvement, MRI tended to overestimate vessel stenosis and lead to misinterpretation of slow-flow conditions and not recognize small-vessel luminal abnormalities (Husson et al. 2002). Nevertheless, MRA is now felt to be sensitive enough to provide an adequate initial evaluation of arterial brain disease in childhood.

Imaging of Arterial Stroke in Children

857

Fig. 18.2. A, B A 3-year-old boy with cerebrovascular accident (CVA). MRI on day 1 after onset of neurological deficit (C, D). A 7-year-old girl who had had chicken pox 3 months earlier. MR and MRA aspect 4 days after the ictus aspect 1 year later (E, F)

858

18 Arterial Ischemic Stroke

Fig. 18.3A–D. A 22-month-old girl, treated for rhinopharyngitis for 8 days 2 weeks before, presented with recurrent transitory right-sided hemiparesis. The neurological examination and blood test were normal at admission; angiographic evidence of focal MCA narrowing (A). 3D angiogram (B, C), and endoscopic views (D)

Similarly, the imaging modalities of choice in the investigation of children with possible intracranial venous occlusive disease are now MRI and MRA. Three-dimensional angiography today offers a variety of possibilities to visualize narrowed segments and analyze the overall vascularization in order to plan the appropriate therapeutic approach, whether medical, endovascular, or surgical (Figs. 18.3, 18.4).Detailed analysis of the angiographic findings in pediatric moyamoya disease has revealed the incidence of aneurysm and intracranial hemorrhage to be extremely

Imaging of Arterial Stroke in Children

859

Fig. 18.4A–D. A 3.5-year-old boy presented trisomy 21 with left-sided regressive deficit with recurrences over 3 weeks; angiographic evidence of focal middle cerebral artery (MCA) narrowing (A) associated with contralateral narrowing (not shown). Various manipulations to analyze the stenosis (B–D)

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18 Arterial Ischemic Stroke

low (1.5%) compared to that of adult moyamoya disease (Satoh et al. 1988; Shirane and Yoshimoto 1992). It is anticipated that angiography in the future will become an integral part of the treatment management strategy as the role of endovascular thrombolytic therapy becomes more established and better defined in combination with brain-protective agents.

18.6 Outcome and Prognosis Prognosis for children after stroke has generally been thought to be better than for adults, although few reports in the literature present sufficient data regarding long-term follow-up to substantiate this observation. In addition, because pediatric arterial stroke is multifactorial (as opposed to that in adults), it is very important to realize that outcome data published in the literature often ignore the various etiologies responsible for pediatric ischemia and combine the data by age groups rather then by etiology. In doing so, it is often difficult to comprehend subtle but definite differences in outcome based on stroke etiology in children. Long-term follow-up of children after neonatal ischemic stroke revealed mental and motor developmental delay in nearly all patients (Koelfen et al. 1993). On the other hand, among a prospectively collected series of 123 Canadian children (33 neonates, 90 infants and children) presenting with arterial stroke, it was demonstrated that the neonates with arterial ischemia had fewer poor outcomes than the older infants and children (deVeber et al. 2001). In the same cohort, it was shown that while 31% of neonates had a poor outcome this was increased to 46% in infants and children presenting with arterial stroke. Approximately 85% of children survived 5 years after their onset of stroke in one population study (Schoenberg et al. 1978). However, depending on the underlying condition, residual deficit has been reported in 75%–100% of patients (Schoenberg et al. 1978; Eeg-Olofson and Ringheim 1983; Satoh et al. 1991; Higgins et al. 1991; Koelfen et al. 1995). In addition to physical disabilities, functional outcome analysis of children with sickle cell disease affected by stroke revealed that most of the children had intellectual deficits ranging from borderline to moderate mental retardation (Hariman et al. 1991). This information is in contrast with other data in the literature, which appear to indicate a more favorable outcome in children (Powell et al. 1994) or infants (Trauner et al. 1993) affected by stroke, underscoring the need for thorough outcome analysis studies in the pediatric stroke population with extension of follow-up well into adulthood. One feature of childhood stroke rarely seen in adults is seizures at the onset of stroke (Fig. 18.4) (Lanska et al. 1991). This may in fact have prognostic implications, as 60% of children below the age of 3 years who presented with a seizure or convulsion at the onset of stroke will have severe developmental delay on long-term follow-up, and 75% continue to have persistent seizures (Aicardi et al. 1969). On the other hand, among those who did not have seizures at onset, only 20% were noted to be severely impaired and less than 10% continued to have seizures. Since seizures are more common in children under 3–4 years of age, younger children

Outcome and Prognosis

Fig. 18.5A–C. A 12-year-old girl presented with a sudden onset of loss of consciousness with right hemiplegia. She had had a similar episode at the age of 15 months that was not explored at the time. A Distal internal carotid narrowing involving the adjacent portion of the M1 and A1 segments can be seen. B, C Follow-up angiography initially demonstrated a worsening of the occlusive process with no clinical manifestations and then a progressive reopening

861

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18 Arterial Ischemic Stroke

Fig. 18.6A, B. Angiogram 5 days after CVA. Note stranding (double arrow, A). The angiogram 5 months after CVA shows a worsening of the aspect (B)

appear to have a worse prognosis for long-term development (Trescher 1992). Perhaps an under-recognized phenomenon is also the occurrence of movement disorders as a long-term sequelae following childhood basal ganglia infarction (Pettigrew and Jankovic 1985). The risk of recurrent stroke in children is reported to be low, although the duration of follow-up in most reports is less than 5 years. Recurrence has been estimated to be as high as 20% in one long-term series (Isler et al. 1984), and the long-term recurrence may thus be underestimated in the literature. Certain disorders such as sickle cell disease are known to be associated with a high rate of recurrence, which can be counteracted by various treatment strategies (Miller et al. 1992; Pegelow et al. 1995). At this point, the repair capacity of the vascular system should be mentioned, as it clarifies a variety of clinical progression and tempers aggressive therapeutic attempts. There is often worsening of the angiographic aspects without necessary aggravation of symptoms (Figs. 18.5–18.7). Some of these repair phenomena can actually mimic aneurysmal progression, in particular in dissections (Fig. 18.8). Complete resolution and vessel reopening can be noted following anticoagulation without manipulation of devices within the lumen (Fig. 18.9). Intermittent deficits are often noted during the treatment, in particular in the vertebrobasilar system, which correspond to collateral claudication and not to recurrent embolic phenomena (Figs. 18.8, 18.9).

Outcome and Prognosis

Fig. 18.7A–C. A 15-year-old boy presented hemiparesis while playing basketball. Cardiac and biologic examinations normal. The boy was treated with aspirin. Complete clinical recovery. Severe MCA stenoses (A), which subsided in 2 years (B, 6-month follow-up; C 2-year follow-up)

863

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18 Arterial Ischemic Stroke ▲

Fig. 18.8A–E. A 5-year-old boy presented with paraparesis. NF1 disease in the mother, associated factor XII deficit. Angiography shows subendothelial (A–C) dissection and distal emboli from intradural vertebral duplication. Spontaneous progression with medical treatment 6 months later shows “aneurysmal” healing (D, E). E see p. 865

Outcome and Prognosis

865

Fig. 18.8E. Legend see p. 864

Fig. 18.9A–B. A 7-year-old boy presented with repeated episodes of headaches and nystagmus, but no history of trauma. A, B Intraluminal clot proximal to the transdural portion of the VA. C,D see p. 866

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18 Arterial Ischemic Stroke

Fig. 18.9C–D. (continued) One year later, after anticoagulation treatment for 6 months, note C the partially recanalized distal basilar artery, the reopened VA, and D the residual fusiform ectasia corresponding to a possibly healed dissection or focal dysplasia

18.7 Etiology The etiologies of arterial ischemic stroke in childhood are often multifactorial and different from adults in whom arteriosclerotic disease is the single most common etiology (Table 18.2). Therefore, extensive investigations will need to be conducted to facilitate the understanding of its pathogenesis in children. Often infections, vaccinations, and minor trauma are found a few weeks before the onset of symptoms, thus suggesting various etiologies. Complete blood count; serum electrolytes; C-reactive protein or erythrocyte sedimentation rate; coagulation times and fibrinogen titer; transparietal echocardiogram; standard electroencephalogram (ECG); prolonged (24-h) ECG recording; blood samples to measure triglycerides and cholesterol, amino acid chromatography, lactates, protein C, protein S, and antithrombin III antiphospholipid antibodies; urine samples for amino acid chromatography and organic acid chromatography; cerebrospinal fluid examination for cell count and protein titration; viral antibody titers (varicella zoster, cytomegalovirus, herpes type 1, measles) in serum and cerebrospinal fluid (CSF) by enzyme-linked immunosorbent assay (ELISA) or complement fixing and polymerase chain reaction (PCR) for varicella zoster virus DNA in CSF constitute some of the examinations done to determine the cause used in the etiological diagnosis of stroke in children. The causes of ischemic stroke in children are varied and differ significantly from the underlying causes in adults; in the majority of children (80%), a specific etiologic cause for the stroke can be found.

Cardiac Disorders

867

Table 18.2. Etiologies (Western) Main causes Emboli of cardiac origin 15% Intracranial acute arteriopathy (infections) 30% Dissection of cervical arteries 15% Moyamoya disease 15% Total 75% Other causes and unknown 25% Hemopathies (sickle cell disease), meningitis, HIV, NF1, FMD, neonatal stroke, C-, S-protein deficit or anti-III, resistance to activated C-protein-like or Leiden factor mutation or antiphospholipid instead give venous infarcts, migraines (?)

We have excluded from this overview the strokes associated with revealing a giant aneurysm (see Chap. 17, this volume) or arteriovenous shunts (see Chap. 5, this volume), in which ischemic manifestations are more likely to be venous than arterial. We have included ischemia related to proliferative angiopathy. Few etiologies are encountered in 75% of children in Western populations in Europe (Sébire et al. 1996; Chabrier et al. 1998). Different causes can be found according to geography, including sickle cell anemia in North America or infectious causes in India or subSaharan countries. The remaining 25% of etiologies gather many different diseases: sickle cell anemia, metabolic disorders, PHACE, and proliferative angiopathy. It should be remembered that etiologies are sometimes closely interlinked and their mechanisms combined. All children have some sort of infection every 6 months and are exposed daily to more or less benign trauma while playing. Postinfectious, post-traumatic etiologies are often discussed, dissection, concentric proliferation, and emboli are the mechanisms envisaged, and proximal hemodynamic or distally occlusive mechanisms are the final cause of ischemia. Any combination of these can be seen in stroke in children.

18.8 Cardiac Disorders The most common identifiable cause of childhood stroke is congenital heart disease (CHD). Emboli from the heart or from the periphery through a right-to-left shunt are the usual causes of ischemic stroke (Figs. 18.1, 18.10). The most common underlying cardiac conditions are Fallot’s tetralogy and the transposition of the great vessels. Thrombi can also form on prosthetic cardiac valves and be another important cause of cerebral emboli. Mitral valve prolapse is not considered to be an increased risk factor for stroke in infants (Nishimura et al. 1985b). Children older than 2 years with CHD tend to present with brain abscess rather than ischemic stroke (Dusser et al. 1986). Hereditary hemorrhagic telangiectasia (HHT) disorder or Rendu-Osler-Weber (ROW) disease, in children can be associated with early stroke (neonatal or infant) in relation to a pulmonary arteriovenous fistula (AVF; Fig. 18.11). Brain abscesses are a classic complication of pulmonary AVF in HHT patients regardless of their age. Discovery of this condition requires specific treatment to pre-

868

18 Arterial Ischemic Stroke

Fig. 18.10A–D. A 14-year-old girl presented with a sudden onset of right-sided hemiplegia with aphasia. Following a short worsening of symptoms, regression of symptoms was noted in 12 h. A, B CT showed probable thrombosis of the M1 left middle cerebral artery (MCA). Angiographic follow-up C at diagnosis and D 3 months later confirmed the cruoric nature of the embolic phenomenon and the restitution ad integrum of the occluded segment. The etiology could not be determined

Cardiac Disorders

Fig. 18.11A–E. An 11-year-old boy presented with an acute left-sided hemiplegia (A, B). Emboli from cardiac origin was diagnosed in view of an intermittent cardiac arrhythmia (C–E, arrow)

869

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18 Arterial Ischemic Stroke

vent cerebral complications. The search for pulmonary AVF is actually the only systematic possibility in patients presenting with the disease and diagnosed for another location (see Chaps. 4 and 5, this volume). The causes include cyanogenic cardiopathies (known in only half of cases), arrhythmia, hemodynamic or embolic strokes, PAVF, and HHT1.

18.9 Acute Regressive Cerebral Arteriopathy Fever or evidence of infection is common in children presenting with cerebral infarction. Bacterial or viral meningitis can be responsible for an infectious type of arteritis resulting in stroke in children (Powell et al. 1994; Chiu et al. 1995; Silverstein and Brunberg 1995). Chicken pox had occurred in the 12 months prior to the onset of symptoms in 31% of children presenting with arterial ischemic stroke (Askalan et al. 2001). Stroke has been described as a rare complication in children infected with the human immunodeficiency virus (HIV), occurring in about 1% of affected children, although autopsy evidence of infection has been documented in 10%–30% (Moriarty et al. 1994; Philippet et al. 1994; Fig. 18.12). Acute regressive cerebral arteriopathy is characterized by a transient attack of cerebral arterial wall and accounts for 26% of childhood strokes in Sébire’s series (1996) (Table 18.3). This arteriopathy is likely to be due to acute angiitis, triggered by infectious agents such as varicella zoster virus (Figs. 18.2, 18.3, 18.13) (Chabrier et al. 1998; Sébire et al. 1999; Askalan et al. 2001). Nine out of 34 children were selected from the entire series of ischemic stroke patients observed at Bicêtre Hospital, Paris, between 1984 and 1995. All the children were previously in good health. Chickenpox rash occurred before the initial stroke in five patients. Mean age at first stroke was 6 years and 2 months (range, 2 years and 9 months to 13 years and 4 months). All the children presented with acute hemiplegia. Stroke recurred in three patients at the latest 3 months after the initial infarct. In all patients, cerebral imaging showed small subcortical infarcts located in the basal ganglia and internal capsule. Arteriography revealed multifocal lesions of arterial wall (focal stenosis or segmental narrowing), all located in the carotid area. Longitudinal arteriographic follow-up prolonged for up to 6 months after the initial stroke showed initial worsening of arterial lesions (n=5) for a maximum duration of 7 months, followed by complete regression (n=2), improvement (n=5), or stabilization of the lesions (n=2). Two patients had residual disabilities. One of the most striking features of this arteriopathy was the transient action of the pathological process. This was demonstrated both angiographically, by repeated examinations showing– often after initial worsening– regression or stabilization of arterial lesions (Fig. 18.5) and clinically by long-term follow-up showing a lack of late recurrence. Such acute regressive arteriopathy might be an important part of ischemic strokes in childhood. Previous studies highlighted the frequency of subcortical in-

Acute Regressive Cerebral Arteriopathy

Fig. 18.12A–C. A 6-year-old girl who had three convulsive episodes on the right side starting with a right-sided clonic phenomenon and followed by loss of consciousness for 40 min. Clinical examination showed mild residual hemiparesis. The child had human immunodeficiency virus (HIV) disease transmitted during pregnancy with a severe immunologic deficit. B, C Angiography demonstrated a middle cerebral artery bifurcation stenotic segment

Table 18.3. Intracranial acute arteriopathy Mean age 6 years (1–12 years) Healthy child A few weeks after infection (varicella-zoster: chicken pox 70%) Sudden hemiplegia Basal arteries, MCA territory Recurrence 25% (1–3 months following initial event) Good outcome in 75%

871

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18 Arterial Ischemic Stroke

Fig. 18.13A, B. A 3-year-old girl presented with a sudden onset of hemiplegia with mutism that spontaneously subsided in 48 h. B Angiography shows M1 stenosis. B Spontaneous regression was confirmed at 6-month follow-up

Fig. 18.14A, B. An 11-year-old boy presented with partial cheiro-oral seizure; angiography shows complete occlusion of the right internal carotid artery (ICA). Note the stenosis involving the anterior cerebral artery (ACA)

Acute Regressive Cerebral Arteriopathy

873

Fig. 18.15A–C. A 19-month-old boy presented right-sided hemiplegia after varicella. Angiography shows complete occlusion of one middle cerebral artery (MCA) trunk (A–C)

farcts in childhood found in 18%–65% of pediatric stroke patients (Dusser et al. 1986; Powell et al. 1994). The angiographic appearance, characterized by focal or segmental stenosis and tail-like occlusions, does not suggest either an embolic or a thrombotic process, but is consistent with abnormalities of the arterial wall (Figs. 18.14–18.20). The pathophysiology of such arterial lesions cannot be established on an angiographic basis. The acute and regressive course is consistent with an acute process such as arteritis, dissection, or vasospasm. Lack of anamnestic events (e.g., drug absorption, trauma, or meningeal hemorrhage) and persistence of arterial lesions makes unlikely the hypothesis of a vasospasm or dissection.

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18 Arterial Ischemic Stroke

Fig. 18.16A–C. A 12-year-old girl felt dizziness and abdominal ache after a shower, then presented upper limb and facial paralysis on the right side. The neurological examination was otherwise normal. Note the tight narrowing on the MCA division (A–C)

In a prospectively collected series of 70 consecutive Canadian children with arterial ischemic stroke, 22 (31%) patients were noted to have had a varicella infection in the preceding year (Askalan et al. 2001). Children in the varicella cohort were more likely to have hemiparesis, basal ganglia infarcts, large-vessel stenosis, recurrent transient ischemic attacks, and recurrent strokes and were less likely to present with seizures as compared to the nonvaricella cohort. Thus an inflammatory process affecting the arterial wall, possibly triggered by infection, is the most likely pathophysiological hypothesis. A temporal relationship between ischemic strokes in young patients and

Acute Regressive Cerebral Arteriopathy

875

Fig. 18.17A, B. A 9-year-old girl suffered from sudden headache and fell down. She remained conscious, but then presented aphasia, hemiparesis on the right side, and central facial paralysis on the same side. When she was admitted 24 h later, aphasia subsided. She nearly totally recovered from hemiparesis, except subtle weakness of the upper limber 48 h later. Note the focal ICA stenosis (A, B, arrow)

Fig. 18.18A, B. A 4-year-old girl presented several episodes of lost strength on the left side without convulsions or loss of consciousness. Normal neurological examination and CT. Varicella 2 months before. Seven days later while in the hospital, sudden nonregressive hemiplegia. MR shows a deep-seated ischemia on the right side. Angiography shows focal narrowing involving a perforator (A, B). Following aspirin and physiotherapy, recovery was almost complete at 1 year

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Fig. 18.19A, B. A 5-year-old boy presented with sudden hemiplegia following herpes zoster. Note the narrowing of the ICA termination (A, B)

infectious diseases (i.e., tonsillitis, cervical lymphadenopathy, varicella zoster virus infection, or general inflammatory processes have been indicated) was mentioned in several earlier studies (Riikonen and Santavuori 1994; Harwood-Nash et al. 1971; Raybaud et al. 1981; Syrjanen 1993). Pathological confirmation of an inflammatory process is available in a few reports; presence of varicella zoster virus (VZV) antigens could even be demonstrated on the segment of the middle cerebral artery involved in a lethal stroke in a 4-year-old child with a previous history of varicella (Berger et al. 2000). Banker (1961) reported an occlusion of the internal carotid artery in a 9-year-old boy corresponding to acute arteritis. Media and adventitia were infiltrated with polynuclear leukocytes, lymphocytes, and macrophages. In a 1-year-old boy presenting with acute hemiplegia, Shillito (1964) found histological changes consistent with vasculitis in the middle cerebral arterial wall. Among the infectious agents that might be involved, one of the more easily recognized is the varicella zoster virus (Bodensteine et al. 1992; Eda et al. 1983; Frank et al. 1989; Ichiyama et al. 1990; Inagaki et al. 1992). In Sébire’s series (Sébir et al. 1995), five children had clinically diagnosed varicella prior to stroke (confirmed by antibody titration in three children).

Acute Regressive Cerebral Arteriopathy

877

Fig. 18.20A–C. A 2-year-old girl with an ischemic hemorrhagic stroke and right hemiplegia. NF1 was diagnosed during hospitalization. Angiography shows an occlusion of the M1 segment of the left MCA (A, B). Extracerebral network opacifies the MCA branches downstream from the occlusion (C)

Occlusion of cortical veins or dural sinuses may also occur with purulent meningitis or with infections of the paranasal sinuses and gives rise to convulsions, neck stiffness, altered levels of consciousness associated with venous occlusive disease of infectious origin. In Asian and African countries, stroke associated with meningitis is not rare and involves most often the basal arteries (tuberculosis). Noninfectious vasculitis such as periarteritis nodosa and systemic lupus erythematosus, which are known to be associated with cerebral infarction in adults, rarely cause stroke in children. Isolated angiitis of the central nervous system in children is even rarer: only ten cases have been reported to date (Lanthier et al. 2001). The process tends to affect small vessels but can also be demonstrated to involve medium-sized and large vessels, and consequently neuroimaging may show evidence of multiple areas of infarction in the former and reveal areas of arterial stenosis in the latter. Subarachnoid hemorrhage may

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18 Arterial Ischemic Stroke

occur and should raise suspicion of vasculitis in children. CNS biopsy is indicated to establish the diagnosis of primary CNS vasculitis in order to institute treatment (prednisone and cyclophosphamide) to decrease early morbidity (Lanthier et al. 2001).

18.10 Dissections In the Great Ormond Street series (1993–1999, Ganesan et al. 2003), 115 strokes were studied at the acute stage: 10% were related to dissection. Similar numbers were reported by Schievink et al. (1994), Chabrier et al. (2001), and Chabrier and Buchmuller (2003). Slightly more were reported in the ICA territory and the vertebral artery (Khurana et al. 1996; Figs. 18.21, 18.22). A traumatic event is often found, but this link is seldom proven. Emboli are frequent (posterior circulation and neck ICA) in comparison to hemodynamic strokes (intracranial ICA). In the literature, truly spontaneous strokes are often mixed with clearly traumatic strokes on the basis of stroke symptoms. The repair capacities and recurrence of stroke is, however, unlikely to be the same. Clinical findings in dissections were characterized by a higher mean age (<10 years, with a slight male dominance), previous head or neck traumatism (1–7 days before), strokes preceded by headache in all cases, occurrence of seizures, and a very poor prognosis (mortality 33% in the anterior circulation, 2% in the posterior circulation), recurrence of stroke or transient arterial attacks (TIAs) in 10% of anterior circulation strokes vs 16% for posterior circulation strokes, and overall 63% residual deficits (meta-analysis through Medline; Fullerton et al. 2001). Numbers reported belong to published series. Morbid mortality is likely to be lower because diagnosis is now made more often (Chabrier et al. 2001) in more benign unreported cases. Dissection affects the ICA intracranially just after the cavernous sinus and often bilaterally nonsymmetrically and more rarely at the cervical level. Conversely, the VA is often involved at the level of C1 or C2 spaces, where it presents as a focal narrowing with intraluminal clotting and distal emboli (Chabrier and Buchmuller 2003). The lesions are subependymal with typical lumen narrowing. Partial or complete repair is seen with sometimes pseudo-aneurysmatic scarring (Fig. 18.8). Underlying familial or nonfamilial arterial wall dysplasias are seldom found (Fig. 18.23). Treatment in neck dissections with emboli includes neck immobilization with sand bags or collar or anticoagulants (low-molecular weight heparin at the acute stage 1 mg/kg, then warfarin or LMWH for 3–6 months). Pseudo-embolic recurrence can be noted in particular in the posterior fossa in relation to transient hemodynamic failure of the collateral circulation without recurrence of the causative phenomenon (Figs. 18.24, 18.25). Careful analysis of the dissection segment and collateral circulation should differentiate between the two phenomena, in particular if they occur while treated. It should be recalled that dissections in children often involve both subintimal and ischemic strokes (from involved perforators or emboli) and subadventitial extensions with subarachnoid hemorrhage and fusiform aneurysms (Fig. 17.29).

Dissections

879

Fig. 18.21A–C. A 6-year-old presented transient left-sided ischemic stroke. Angiography shows bilateral probable spontaneous dissection with complete occlusion of the supracavernous ICA on the left and retrograde narrowing of the cervical portion (A, B). The opposite ICA is also narrowed at the supracavernous level (C)

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Fig. 18.22A–D. A 19-month-old presented with a deep-seated stroke (A, B). The angiogram suggests a thrombosed dissected segment with an aneurysmal portion (B, C). An accessory MCA provides collateral circulation to the left hemisphere (D)

Intraoral trauma or injuries to the neck may cause ischemic stroke in children. The injury may cause dissection of the carotid or vertebral arteries with subsequent thrombus and embolus formation. The onset of neurological symptoms may be delayed by hours or days after the injury and may have a sudden onset or a stepwise progression; a history of trauma may be trivial or absent (Graham et al. 1991; Garg et al. 1993; Randall et al. 1994; Chabrier and Buchmuller 2003). Horner’s syndrome

Dissections

881

Fig. 18.23A–D. A 6-year-old boy presented with regressive headaches and vertigo. Recurrence 1 month later with repeated episodes of vertigo. He also showed a dysmorphic syndrome of chromosome 2. MRI shows posterior circulation ischemia (A, B).Angiography demonstrates typical C2 vertebral dissected segment (arrow, C, D)

raises the possibility of ipsilateral adventitial carotid artery involvement. Postirradiation-induced arterial occlusive disease is a rare cause of stroke in children and may occur 6 months to several years after treatment with irradiation for intracranial brain tumors (Mitchell et al. 1991; Nishizawa et al. 1991). From a total of 213 Canadian children with acute ischemic stroke, 16 (7.5%), eight boys and eight girls, with a median age of 9.4 years, were identified with the clinical and radiological diagnosis of arterial dissection (Rafay et al. 2005). Among these, 37.5% of patients had warning symptoms. Head and/or neck trauma was presumed to be related to dissection in 50%. Clinical features included headache (44%), other signs of raised

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18 Arterial Ischemic Stroke

Fig. 18.24A–C. A 14-year-old boy fell while roller skating. A few days later, he presented several episodes of vertigo, hemiparesis, and diplopia. Normal cardiac ultrasound, normal biology. Distal emboli were shown on the angiogram (A) as well as the dissected segment of the C2 vertebral artery (arrow, B, C)

intracranial pressure (63%), motor deficits (93%), cranial nerve abnormalities (37.5%), speech deficits (50%), visual defects (25%), and seizures (19%). Initial diagnosis of arterial ischemic stroke was established on CT scan in 13 (81.25%) and on MRI in three (18.75%). MRA was performed in 11 and conventional angiography was performed in all. Of the dissections explored, 25% were intracranial and 75% extracranial. The anterior circulation was involved in 53% and the posterior circulation in 47%. Antithrombotic treatment consisted of heparin in 14 (87.5%) followed by coumadin in six (37.5%) and subsequently aspirin in all. Follow-up was available in 14 (87.5%) and showed that complete recovery occurred in 43%, mild to moderate deficits were documented in 44%, and severe deficits were present in 13%. Recurrence of ischemic symptoms was noted in two (12.5%) in this cohort of pediatric patients (Rafay et al. 2005).

Dissections

883

Fig. 18.25A–D. An 11-year-old girl presented with a rapidly progressive hemiparesis with extraocular motor nerve dysfunction (A). MRI shows a brain stem stroke involving a paramedial arterial territory. Angiogram shows an adherent clot inside the lumen of the basilar artery at the level of the stroke (arrow, B–D)

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Fig. 18.26A–E. Legend see p. 885

Moyamoya Disease

885

18.11 Moyamoya Disease Moyamoya disease (Fig. 18.26) is a primary vascular disease characterized by progressive stenosis and eventual occlusion of the supraclinoid portion of the internal carotid artery and the adjacent segments of the middle and anterior cerebral arteries (Table 18.4, Scheme 18.1). In response, an abnormal vascular network of small collateral vessels develops to bypass the area of occlusion (Scheme 18.1). This disease may affect children as well as adults, who in turn tend to present with hemorrhage. The most frequent symptoms in childhood are multiple transient ischemic attacks, with permanent residual deficit following some episodes

Table 18.4. Moyamoya disease 10%–15% of stroke children Stenosis or occlusion of ICA, M1, A1, rarely P2 and P1 Transhemispheric angiogenic network Basal transdural angiogenic network Symmetrical impairment Simultaneous impairment and responses Little or no leptomeningeal recruitment

▲

Scheme 18.1. Moyamoya itself is more a peculiar type of response than a disease

Fig. 18.26A–E. A 2-year-old boy presented with a left hemiplegia occurring 48 h after pyrexia. The lumbar tap was normal and an initial diagnosis of herpetic encephalitis was made. A, B Angiography revealed total occlusion of the right supraclinoid internal artery. In the left internal carotid artery, there was slight stenosis at the same level; segmental narrowing was also noted on both anterior cerebral arteries and on the right posterior cerebral artery. These aspects were considered compatible with a diagnosis of moyamoya disease. Two years later, the neurological situation of the child improved with partial regression of the hemiparesis. C Slight microcrania was noted with a significant right-sided postischemic brain atrophy. Angiography revealed the typical appearance of moyamoya disease, albeit asymmetrical. Occlusion of the left M1 segment was complete (D, E)

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Fig. 18.27A–D. A baby boy presented at 5 months of age with generalized seizures. At 3 years of age, the parents noted a right facial palsy with aphasia and gait troubles. A diagnosis of meningoencephalitis was made after cerebrospinal fluid (CSF) analysis, electroencephalogram (EEG), and CT. The child was treated with acyclovir and antibiotics. Twenty-four hours later, headaches and vomiting occurred associated with disturbed consciousness and right hemiparesis. A CT was performed again and revealed diffuse cortico-subcortical hypodensities. B–D Cerebral angiography showed a typical moyamoya disease appearance with occlusion of the right internal carotid artery, with transdural revascularization. The posterior fossa was normal. The clinical situation of the child worsened, and he died 8 weeks later. From an etiological point of view, a biological confirmation of necrosing encephalitis was never obtained

Moyamoya Disease

887

Fig. 18.28A–D. A boy aged 3 years and 5 months with a first episode of weakness of the right upper limb at 8 months. He presented seizure at 18 months leading to the diagnosis of stroke responsible for right hemiparesis and mental development delay. He had hepatic occlusive disease associated with severe portal hypertension, delay in acquisitions; he presented acute ataxia and myoclonias. Angiography shows typical aspect of bilateral and symmetrical moyamoya (A–D). Burr holes were drilled bilaterally with dramatic clinical results

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Fig. 18.29A, B. A 6-year-old boy (twin birth) suffering from right renal hypoplasia associated with a slight arterial hypertension that was not treated. At the age of 3 years, the child suddenly had monoplegia of the right upper limb that spontaneously regressed in 5 min. A, B Angiography showed a severe stenosis of both intradural internal carotid arteries with leptomeningeal collateral circulation arising from the vertebrobasilar system and transdural supply from the external carotid artery. The posterior fossa was normal, as were the lenticulostriate arteries. The appearance is compatible with a diagnosis of moyamoya disease. Neurological development remained normal, with total disappearance of the hemiparesis. The child was treated with aspirin and has grown normally since then

Moyamoya Disease

889

Fig. 18.30A, B. A 14-year-old boy with trisomy 21 presented severe right hemiplegia (A). Angiography shows the complete occlusion of the MCA segment (B)

(Satoh et al. 1991). The disease expresses both angiectatic and neoangiogenic responses from the pial and dural vasculature (Yoshimoto et al. 1996). Less often, patients present with sudden hemiparesis or with transient ischemic attacks without the development of a fixed neurological deficit. Seizures occur in 33% of children under the age of 6 years. The disorder may remain stable, but more often follows a relentlessly progressive course (Figs. 18.27, 18.28) with severe motor impairment and intellectual deterioration (Maki et al. 1976; Suzuki and Kodama 1983; Golden 1989; Yoshida et al. 1993, Fukui et al. 1997). Primary and secondary moyamoya account for 10%–20% of strokes in children. Many pseudo-moyamoya patterns can be seen, with slowly progressive large-vessel vasculopathy with collateralization in childhood; however, the symmetry, parallel progression on both sides, the transdural angiogenesis, the absence of leptomeningeal collateral circulation with large transdural contribution, the normal appearance of posterior fossa vascularization, and the role of lenticulostriate vessels (Fig. 18.29) suggest true moyamoya disease. It can be considered that moyamoya syndrome or moyamoya phenomena are responses to different triggers on different weaknesses, rather than true diseases (Figs. 18.30, 18.31). Specific vulnerability includes a familial occurrence noted in 10% of cases with linkage to chromosomes 17q25 (Yamauchi 2000) and 3p24.2–26 (Ikeda and Yamor 1999).

890

18 Arterial Ischemic Stroke

Fig. 18.31A–D. Legend see p. 891

▲

Moyamoya Disease

Fig. 18.31A–I. A 4-year-old girl. Angiography shows diffuse narrowing of cerebral arteries with bilateral occlusion of the cervical ICA (A, D). On the left side, vasa vasorum at the neck transdural collateral and rete along the optic tract contribute to the collateralization (B, C). On the right, the same resources are recruited (D–F). Extremely unusual involvement of the posterior fossa is present (G–I)

891

892

18 Arterial Ischemic Stroke

18.12 Hematological Disorders and Coagulopathies Sickle cell anemia (SCA) is the most common hemoglobinopathy associated with cerebrovascular disease and is the cause of 6% of hemiplegia in North American children. Roughly 25% of patients with SCA develop cerebrovascular complications (one of three are clinically apparent), and 80% of these are under 15 years of age (Wood 1978). Stroke occurs as part of the thrombotic crisis. The annual risk of stroke is 0.7% per year. Occlusion of small and larger blood vessels by sickled erythrocytes leads to local anoxia, and further sickling causes progression to occlusion. Focal or generalized seizures precede the onset of motor deficit in 70% of children. The risk associated with angiography is decreased with good hydration and transfusion therapy. After the first stroke, the second occurs in 50%–75% in untreated children; 80% of them within the next 36 months. The preventive role of long-term transfusion therapy in order to reduce the levels of hemoglobin S to below 30% has been documented, although certain side-effects may occur (Miller et al. 1992; Pegelow et al. 1995). Transcranial Doppler studies are a noninvasive means of following the progressive large-vessel vasculopathy and determining stroke risk in these patients. Certain inherited abnormalities of the clotting system may predispose patients to thrombosis and stroke (Figs. 18.4, 18.8), which can be arterial or venous. Protein C, protein S, antithrombin III, and dysfibrinogenemia should all be considered in cases of unexplained stroke in the pediatric population (Hart and Kanter 1990; see Chap. 7, this volume). The presence of certain antiphospholipid antibodies, including the lupus anticoagulant, may result in abnormal coagulation and cerebral infarcts in children. These antiphospholipid antibodies are autoantibodies directed against phospholipids in cell membranes and are present in systemic lupus erythematosus as well as other autoimmune disorders and in otherwise apparently healthy individuals (Roddy and Giang 1991; Schoning et al. 1994). A drop in the titer of these proteins is observed during the acute phase and the following months of a stroke, regardless of its cause. Some authors have suggested there is a causative effect between low C or S protein levels and stroke. Most reports are missing late dosages or genetic studies. Antiphospholipid antibodies have been noted in various inflammatory (lupus) infections or neoplastic situations and stroke. Their pathogenetic role is still unclear. The antiphospholipid syndrome should be clinically suspected with cutaneous and hematologic manifestations associated with the high titer of antibodies (Lockshin 1995).

Proliferative angiopathy

893

18.13 Metabolic Disorders Homocystinuria due to cystathionine b-synthase deficiency is one of the metabolic disorders known to predispose patients to arterial and venous thrombosis with cerebral infarcts. Infarcts may occur before the other features of the diseases, such as dislocation of the lens, developmental delay, and a marfanoid habitus, become evident (Mudd et al. 1985). Fabry’s disease caused by b-galactosidase deficiency predisposes patients to cerebral infarction, but the infarcts (usually the lacunar type) tend to occur in early adulthood. MELAS syndrome (mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episodes) has been described in children presenting with episodes of nausea, vomiting, headaches, seizures, hemiparesis, and cortical blindness. CT and MRI show areas of infarction typically, but not necessarily, in the occipital areas (Pawlakis et al. 1984; Riikonen and Santavuori 1994). Takayasu’s disease represents arteritis mainly involving the aorta and its branches and is characterized by hypertension, absent pulses, and vascular bruits. Stroke occurs in 5%–10% of patients. The disease most commonly affects females between 15 and 20 years of age, but has also been reported in infants (Kohrman et al. 1986). Migrainous strokes meet the criteria determined by the International Headache Society, i.e., history of migrainous neurological aura, migrainous crisis identical to the previous one with an incompletely regressive deficit in 7 days and/or imaging evidence of an infarct of the topography of the symptom presented by the child.

18.14 Proliferative angiopathy Moyamoya disease, moyamoya-like syndromes, and proliferative angiopathy in children are the most typical disorders in this group (Figs. 18.32, 18.33). They combine neoangiogenesis (production of lumen) and angiectasia (production of vessel wall), which may be difficult to differentiate. However, in such instances there is a discrepancy between the apparent size of the nidus-like network of vessels and the draining veins that are often normal or slightly enlarged. In angiectasia, the architecture of the nidus is homogeneous and appears normal, while it is unpredictable in angiogenesis. The rapid venous filling is usually due to a faster capillary transit time and seldom caused by true AV shunts in capillary ectasia (in some DVAs, for example). The progression of these proliferative diseases is unpredictable but tends toward proximal arterial occlusion evolving in the most extreme forms to moyamoya aspects (see Vol. 2, Chap. 1). In proliferative angiopathy, while seizures are the most common clinical symptom at presentation, headaches and progressive deficits are also possible, whereas hemorrhage is exceptional. In our experience, since the risk of hemorrhage is low at presentation, the risk of recurrence once a hemorrhagic episode has occurred is significantly higher than in CAVM. Transdural supply in remote locations (supra- and infratentorial, bilateral) confirms the diffuse character of the angiogenic activity of the disease, suggesting an unrepressed response to cerebral subischemic manifestations (Ducreux et al. 2004b). Proliferative angiopathy is still often confused with CAVMs and

894

18 Arterial Ischemic Stroke

Fig. 18.32A–E. A 15-year-old female patient presenting with generalized seizures and referred to us with the diagnosis of large arteriovenous malformation. This aspect corresponds to what we describe as proliferative angiopathy. Note on the MRI section (A) the amount of dilated vessel running at the surface of the cortex. Angiographically speaking, there are several cortical artery interruptions with local explosive angiectasia (B, C). Dural involvement at the base and the convexity testify for the active angiogenic activity of this lesion. Despite medical treatment, the patient died 4 years after the diagnosis from major ischemic stroke (D). Pathologie specimen shows “normal” arterioles within brain parenchyma

Proliferative angiopathy

895

Fig. 18.33A–C. A 15-year-old male patient with tonicoclonic seizures on the right side. Typical aspect of proliferative angiopathy on MRI (A–C)

thought to represent a diffuse nidus. Proper recognition and classification is important, as it identifies the presence of normal brain tissue intermingled with the vascular spaces (Fig. 18.33). Treatment should therefore not be embolization (nor surgery or radiation therapy) unless areas of the angioarchitecture suggest zones of weakness or demonstrate obvious constraints to the eloquent brain. Headaches are often dramatically alleviated by a partial and limited arterial embolization in noneloquent areas, without treatment of the dural component. Localized forms of proliferative angiopathy can be seen in children, probably developing at an older age, since they are not associated with mental retardation or local cerebral atrophy. Today the perfusion MR (Ducreux et al. 2004b) has reinforced the suspicion of chronic ischemic disease with angiogenic activity, as in moyamoya (Fig. 18.34), and similar treatment with burr holes has already been given in a handful of cases with immediate good clinical results on both the headaches and the seizure response to medical treatment (Fig. 18.35).

896

18 Arterial Ischemic Stroke

Fig. 18.34A–F. Legend see p. 897

▲

Proliferative angiopathy

897

Fig. 18.34A–F. A 10-year-old boy with congenital sinus pericranii since the age of 5.5 years. Over a 1-year period, he had several transitory left hemiplegias that regressed spontaneously, resulting in nonregressive deficit with partial seizures. Surgical revascularization at 11 years of age. This 11-year-old boy showed (A, B) draining of an active proliferative angiopathy; typical aspect on MRI (C, D). Perfusion MRI shows significant hypovascularization of the right hemisphere (E, F)

Fig. 18.35A–D. Paresthesic crisis every 2–3 days responding to medical treatment. One year later, permanent right-sided deficit and headaches. Typical angiographic appearance of proliferative angiopathy with holo hemispheric nidus of cortical arteries narrowed M1 MCA and at that time poor transdural supply (A–D). E–J see p. 898

898

18 Arterial Ischemic Stroke

Fig. 18.35E–J. (continued) Four years later, burr holes on the left have triggered the transdural supply and stabilized the narrowing process (E–J). Clinical improvement of the deficit, headaches subsided

Spinal Cord Strokes

899

18.15 PHACE The description by Burrows et al. (1998) of progressive arterial occlusive disease together with the four cases in Bhattacharya’s series (Bhattacharya et al. 2004) illustrate the susceptibility of the large- and medium-caliber arteries in children with PHACE syndrome very well (Fig. 18.36). In Burrows’s series, the onset of occlusive disease was between birth and 18 months age. This correlates with the timing of the proliferative phase of the associated hemangiomas. However, in Bhattacharya’s patients presentation was much later: from 4 to 14 years of age, by which time involution of the hemangiomas is long past. The stenotic lesions are mostly located at the anterior division of the ICA or the M1 segment, as they do in children with other vascular diseases. Intradural extracerebral pial collateral circulation is predominantly recruited; we have not observed true moyamoya phenomena or significant transdural supply. The lesions are usually unilateral and can involve P1. Cortical arteries on the supratentorial vascular bed can be involved. The unsuppressed vessel wall proliferation (angiogenesis) leads rapidly to centripetal narrowing of the lumen and to collateral angiectasia and some neovascularization. The occlusive phenomena may not stabilize at the same time as the hemangiomas involute, and this can in turn lead to neurological manifestations. Treatment will include antiplatelet therapy and surgical cortical stimulation of angiogenesis (Fig. 12.8).

18.16 Hereditary Hemorrhagic Telangiectasia, or Rendu-Osler-Weber Disease HHT disease can cause arterial strokes in children. Most of them are embolic in nature and they may be septic or aseptic. They are usually due to a pulmonary AVF. Three of our patients presented at neonatal and childhood age with postembolic hemiplegias, showing a familial type of cerebral stroke disease. In this particular family, the diagnosis of HHT was established on clinical presentation of the rest of the family (see Chaps. 2, 4 and 5, this volume; Fig. 18.1).

18.17 Spinal Cord Strokes Strokes at the spinal cord level are exceptional in children. In most instances, acute onset of spinal cord manifestations is likely due to a vascular malformation rather than to occlusive diseases (Fig. 18.37). One child with primary vasculitis of the spinal cord has been reported (Giovanni et al. 2004). Some aspects are peculiar and similar to what we described with proliferative angiopathy (Fig. 18.38–18.40, 15.19). The diagnosis is unclear and the neurological prognosis poor despite anticoagulation.

900

18 Arterial Ischemic Stroke

Fig. 18.36A–C. PHACE in a 6-month-old girl who presented with right-sided frontoorbital hemangioma and progressive neurological deficit, chorea, and headaches. Imaging findings were 50% stenosis of the left supraclinoid ICA, occlusion of the left anterior cerebral artery (ACA) A1 segment (A), occlusion of the right ICA bifurcation (A, B), and occlusion of the distal basilar artery. An extensive network of collateral vessels was noted. Several arterial anomalies were identified. There was a segmental agenesis of the right ICA, and a right persisting trigeminal artery (C). The external carotid system via the skull base contributed to the supply of the ACA territories bilaterally (see also Fig. 12.7)

Spinal Cord Strokes

901

Fig. 18.37A–C. A 10-year-old boy presented with a sudden onset of right lower-limb pain during the night. The morning after, he was paraplegic; he recovered progressively, but a right lower limb sensory motor deficit persisted. A, B Angiography failed to demonstrate any arteriovenous malformation, but revealed a small area of parenchymography compatible with the diagnosis of ischemic sequela of the spinal cord. C The entire anterior spinal axis can be seen

902

18 Arterial Ischemic Stroke

Fig. 18.38A–C. A 15-month-old boy, presenting with short and fluctuating instabilities since 8 months of age, weakness involving both upper and lower limbs. MRI (A–C) shows extensive hypersignal to the cord extending to the medulla cranially. Evidence of vascular structures around the cord itself. D–F see p. 903

Spinal Cord Strokes

903

Fig. 18.38D–F. (continued) Angiography shows hyperemia of the entire cord with minimal venous opacification despite capillary blush (D–F)

904

18 Arterial Ischemic Stroke

Fig. 18.39A, B. A 16-month-old girl with torticollis; difficulties walking at 20 months with variable deficits. Angiography shows hyperemia of the entire cord with minimal venous opacification despite capillary blush (A, B)

Fig. 18.40A–C. Legend see p. 905

Treatment and Management

905

18.18 Treatment and Management

▲

Treatment after acute cerebral infarction should follow guidelines for standard medical care of the ill child. Since autoregulation of the cerebral vasculature is impaired, care should be taken to avoid both hypo- and hypertension; careful blood pressure and fluid management is therefore mandatory (Trescher 1992). Serum glucose should also be carefully monitored, as hyperglycemia is known to exacerbate the size of the infarct, while hypoglycemia also worsens the effects of stroke (Vanucci 1990; Pulsinelli et al. 1991). Body temperature control is important, as hyperthermia may exacerbate ischemic brain damage, while hypothermia is known to protect against brain damage. The role of specific therapy for acute stroke in children has not been established. Anticoagulation has been accepted as the treatment of choice in the management of children with cardiogenic emboli and prethrombotic disorders, but its role is unclear in acute stroke of undetermined etiology. Calcium channel antagonists, EAA receptor antagonists, free radical scavengers, and antioxidant drugs will most likely play a role in the future treatment of cerebral infarcts in children for the purpose of brain protection. The role of systemic or intra-arterial thrombolytic therapy currently actively pursued in adults has so far been rarely explored in children with acute onset of arterial ischemic stroke. Surgical management of proliferative diseases with stroke (PHACE, moyamoya disease and phenomena, and proliferative angiopathy) that have not stimulated cortical transdural supply should be discussed: rather than STA-MCA anastomosis, burr holes in these instances will improve headaches and seizures (Figs. 18.35, 12.8). In some instances, the moyamoya network and even the proximal narrowing seemed improved following surgery (Figs. 18.41, 18.42). These cases remain rare and careful assessment of failures and successes is needed. The concept of having a proliferative disease producing occlusive manifestations by concentric enlargement of the vessel wall suggests medical management rather than mechanical management.

Fig. 18.40A–C. Evidence of vascular structures around the cord itself. Angiography shows hyperemia of the entire cord extending to the medulla cranially, with minimal venous opacification despite capillary blush. (Similar case as Figs. 18.37–18.39). (Courtesy of P. Burrows)

906

18 Arterial Ischemic Stroke

Fig. 18.41A–D. A 4-year-old boy with progressive headaches and acquisition regression. Familial moyamoya. Severe moyamoya lesions in both impaired brothers (A). Bilateral burr holes were drilled (B). Two years later, the supply was taken over by the ECA (C), as shown on the late phase (D). Parallel clinical improvement was noted

Treatment and Management

Fig. 18.42A–F. Legend see p. 908

907

908

18 Arterial Ischemic Stroke

Fig. 18.42A–G. A 3-year-old Korean boy with psychomotor delay and cleft palate presented a sudden left hemiplegia and epilepsy (A). There was no history of inflammation, trauma, or infection. Angiography showed bilateral ICA narrowing without transdural supply and poor leptomeningeal collateral (B, C). Following burr hole surgery, there was a slight improvement in the ICA contribution to the supply of the brain (D, E and F, G), with a decrease in the moyamoya-like network

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Yoshii N, Seiki S, Samejima H, Shibata K, Awazu S (1978) Occlusion of the deep cerebral veins. Neuroradiology 16:287–288 Yoshimoto T, Houkin K, Takahashi A, Abe H (1996) Angiogenetic factors in moyamoya disease. Stroke 27:2160–2165 Young W, Berenstein A (1984) Somatosensory evoked potential monitoring of intraoperative radiology. Symposium on Neuroimaging. Neurol Clin 2:873–902 Young WL, Pile-Spellman J (1994) Anesthetic considerations for interventional neuroradiology. Anesthesiology 80:427–456 Yu YL, Chiu EKW, Woo E, Chan FL, Lam WK, Huang CY, Lee PWH (1987) Dystrophic intracranial calcification: CT evidence of “cerebral steal” from arteriovenous malformation. Neuroradiology 29:519–522 Yuh WTC, Buehner L, Kao SCS, Robinson RA, Dolan KD, Phillips JJ (1991) Magnetic resonance imaging of pediatric head and neck cystic hygromas. Ann Otol Rhinol Laryngol 100:737–742 Yura J (1977) Bleomycin treatment of cystic hygroma in children. Arch Jap Chir 46:607–614 Yuval Y, Lerner A, Lipitz S et al (1997) Prenatal diagnosis of vein of Galen aneurysmal malformation: report of two cases with proposal for prognostic indices. Prenat Diagn 17:972–977 Zadok D, Levy Y, Nemet P (1996) Regression of remote capillary haemangioma after local intralesional injection of corticosteroid. Eye 10:759 Zagzag D, Goldenberg M, Brem S (1989) Angiogenesis and blood-brain barrier breakdown modulate CT contrast enhancement: an experimental study in a rabbit braintumor model. AJNR 10:529–534 Zampella EJ, Aronin PA, Odrezin GT, Duvall ER (1988) Conservative management of thrombosed vein of Galen malformations. Pediatr Neurosci 14:264–271 Zarem HA, Edgerton MT (1967) Induced resolution of cavernous hemangiomas following prednisone therapy. Plast Reconstr Surg 39:76–83 Zellem RT, Buchheit WA (1985) Multiple intracranial arteriovenous malformations: case report. Neurosurgery 17:88–93 Zerah M, Garcia-Monaco R, Rodesch G, ter Brugge K, Tardieu M, de Victor D, Lasjaunias P (1992) Hydrodynamics in vein of Galen malformation in 43 cases. Childs Nerv Syst 8:111–117 Zervas NT, Liszczak TM, Mayberg MR, Black P (1982) Cerebrospinal fluid may nourish cerebral vessels through pathways in the adventitia that may be analogous to systemic vasa vasorum. J Neurosurg 56:475–478 Zhang ET, Inman CBE, Weller RO (1990) Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J Anat 170:123 Zhao L, Moos MP, Grabner R et al (2004) The 5-lipoxygenase pathway promotes pathogenesis of hyperlipidemia-dependent aortic aneurysms. Nat Med 10:966–973 Zimmerman RA, Bogdan A, Gusnard DA (1992) Pediatric magnetic resonance angiography: assessment of stroke. Cardiovasc Interv Radiol 15:60–64 Zingessar LH, Schechter M, Kier EL, O’Brien M (1969) Vascular malformations of the posterior fossa including the tentorial hiatus. AJR 105:341–347

Subject Index for Volume 3

A abnormality – acquired 34 – cerebellar 611 – sporadic 34 – vascular 34 accessory MCA 880 acquired immunodeficiency syndrome (AIDS) 805, 808 acrylic 605 acute arteritis 876 acute heart failure 266 Adult Glasgow Coma Scale 78 Adult Glasgow Outcome Score 78 adventitia 812 aetoxysclerol 662 agenesis – of major arteries 622 – of the falx 518 AIDS, see acquired immunodeficiency syndrome alcohol sclerotherapy 661 alobar holoprosencephaly 517, 521 amblyopia 565 amrinone 199 anaplastic astrocytoma 24 anencephaly 517 aneurysm 229, 327, 380, 610, 782 – associated diseases 792 – dissecting 823, 826 – distal flow-related 327 – flow-related 234, 324, 820 – formation 791 – in the facial artery 369 – intranidal 328, 337 – intratympanic 822 – maxillary artery 369 – of the AICA 43 – on the middle meningeal artery 822 – proximal flow-related 327 – treatment strategies 839 angiectasia 283, 289, 293, 295 angiogenesis 33, 292, 324–326, 378, 449, 491, 562, 578, 627, 899 angiogenic activity 32, 895

angiopathy 96 – arterial 324 – hemorrhagic 37, 51, 307 – proliferative 51, 56, 297, 306, 310, 756 – venous 311 anterior cerebral artery (ACA) stenosis 872 anterior choroidal artery 251 anticardian antibodies 539 antiphospholipid antibodies 866, 892 antithrombin III 892 anuria 195 aorta – coarctation 624, 792 – diastolic steal 218 – right-sided 617, 627 aortotomy 210 Apert syndrome 556 apoptosis 95, 564, 623 arachnoid cyst 246, 247, 610 arachnoiditis 741 arrhythmia 666 arterial – anastomosis between both middle cerebral arteries 525 – aneurysm, familial 793 – angiopathy 324 – – high-flow 325 – – transdural supply 324 – diastolic flow 309 – dilatation 293 – enlargement 326 – ischemia 767 – ischemic stroke 851 – – anticoagulation treatment 866 – – antiphospholipid antibodies 866, 892 – – autoimmune disorders 892 – – autoregulation 853 – – bilateral spontaneous dissection 879 – – cerebral blood flow 852 – – childhood stroke 860 – – clinical manifestations 856 – – CT 856

– – – – – – – – – – – – – – – – – – – – – – – –

– – – – – – – – – – – – – – – – – – – – – – – –

deep-seated 880 etiology 867 healed dissection 866 hypothermia 905 in utero 853 incidence 852 infants 856, 860 inflammatory process 874 luxury perfusion 853 MRA 856 MRI 856, 857 neonates 852, 860 recovery 882 recurrence 882 recurrent stroke 862 residual fusiform ectasia 866 seasonal peaks 852 STA-MCA anastomosis 905 thrombolytic therapy 860, 905 transcranial Doppler 892 transfusion therapy 892 traumatic event 878 vessel reopening 862 worsening of occlusive process 861 – – worsening of the aspect 862 – pulmonary hypertension 194 – steal phenomenon 65, 73, 714 arterio-veno-lymphatic tree 30, 465 arteriovenous communication – basal pial 48 – remote cortical 48 arteriovenous fistula (AVF) 229, 252 – at the interventricular foramen 120, 122 – balloon 719 – basilar tip 247 – bilateral occipital lobe 243 – cerebellum 255 – cerebral 37 – cervical collar 719 – cingular gyrus 265 – coils 719 – direct puncture 720 – dural 303 – focal 459 – from the right PICA 262, 269

968

Subject Index for Volume 3

– from the right superior cerebellar artery 278 – frontal 254 – – interhemispheric 250 – genotypes 90 – glue 719 – in the posterior fossa 287 – infratentorial – – age at diagnosis 249 – – age at presentation 249 – – clinical features at presentation 257 – – prenatal diagnosis 250 – large venous pouch 258 – macro-AVF 744 – micro-AVF 744 – multifocality 90 – multiplicity 285 – neonates 275 – parasagittal – – fed by the anterior cerebral system 284 – parietal 285 – petromastoid-sigmoid sinus high-flow 396 – pial 247 – posterior inferior cerebellar artery 264 – preloaded technique 719 – premature baby 252 – prenatal diagnosis 267 – progressive thrombosis 271 – pulmonary 347 – radicular pain 720 – staged embolization 259 – steroids 719 – subpial meningeal space 227 – supratentorial – – age at diagnosis 249 – – age at first treatment 249 – – referral 249 – surgical resection 266 – sylvian 266 – temporal occipital lobe 231 – thrombosed 750 – trismus 720 – venous approach 720 arteriovenous lesion in children 688 arteriovenous malformation (AVM) 88 – alar 364 – association of DVA 475 – bilateral mandibular 656 – cerebral 37 – – development 99 – – enlargement 377 – chiasmatic 376 – chorodial type 106, 113 – cingulate gyrus 114

– – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – –

clinical presentation – in children 342 – in infants 341 – in neonates 341 coiling 644 dental 646 expander 645 external ear 644 facial 382, 653 false pial 306 fistulous type 35 high-flow 636 – maxillofacial 360 holocallosal 377 hypothalamic nerve 371 intracerebral floor of the IVth ventricle 246 intradural 234 isolated brain 35 large posterior fossa – neonates 313 macro-AVM 35 mandibular 367, 382 maxillary 382, 650 – braces 650 – oral bleeding 650 medium-sized 36 mesencephalic 309, 334 micro-AVM 35, 43, 242, 331, 643 – cortical 245 – mesenphalic 245 multifocal 299 – aggressive 684 – in the brain stem 338 multiple 342 multiple CNS 240 myelomeric 480 nasal 382 nidus type 35, 242 of the brain 49 – multifocality 49 of the caudate nucleus 340 of the soft tissue – proliferative activity 637 olfactory 378 optic nerve 371, 373 pial – age at first diagnosis 301 – radiotherapy 355 – surgical treatment 349 posterior fossa 303 primary trigger 97 proximal ligation 644 qiescent 97 radiation therapy 352 radiosurgery 350 recurrent vascular malformations 681 – retinal 372, 374 – revealing trigger 97

– right mandibular 647 – – reossification of the mandible 647 – scalp high flow 645 – scarring reactions 449 – screening 382 – spaces 35 – spinal cord 242, 716 – spontaneous thrombosis 330 – stereotactic radiosurgery 354 – surgical removal 350 – targeted embolization 353 – thalamic 114 arteriovenous shunt (AVS) – angiogenesis 641 – dural 477 – induced micro-AVS 437 – intradural 234 – – recurrence 449 – low pressure 437 – mural 396 – partial targeted endovascular control 641 – pial 437 – radicular 726 – secondary transdural supply 449 – slow-flow multiple 400 – surgery 641 artery to the skull base 391 aspirin 579, 775, 777, 828, 863, 888 astigmatism 590 astrocyte process 18 astrocytoma 782 atherosclerotic lesion 96 atrophy – cerebellar 73 – focal 315 – hemispheric 265, 266 – of the spinal cord 741 – subependymal 67 AVF, see arteriovenous fistula AVM, see arteriovenous malformation AVS, see arteriovenous shunt B bacterial – endocarditis 805 – infection 23 – meningitis 870 ballooning of the transverse sinus 398 balloon thrombectomy 544 basic fibroblast growth factor (bGFG) 561 basilar tip aneurysm 828 Bean syndrome 465 Bicetre Admission and Outcome Score 81

Subject Index for Volume 3 Bicetre Neonatal Evaluation Score 81, 150 bilateral – carotid agenesis 614 – chronic papilledema 549 – sigmoid sinus occlusion 136,172, 180 birthmark 479 bleomycin 678 blindness after radiosurgery 358 blood–brain barrier 23 blue rubber bleb nevus (BRBN) 44, 465, 503 – cerebral venous malformations 507 – HHT1 507 – intracranial manifestations 506 – with DVA 504 bone – defect 464 – hemangioma 597 – hypertrophy 178, 383, 483 – – frontal 490 – – sphenoid 490 – morphological protein 515 Bonnet-Dechaume-Blanc syndrome 39, 359 Bourneville disease 86, 814 bradycardia 666 brain – calcification 396 – damage 147, 274, 401, 408 – – CT 147 – – ultrasound 147 brainstem 258 – stroke 883 – symptom 189 Brunet-Leisine test 161 buphthalmus 478 burr hole 887, 898, 905 – surgery 626, 908 C CADASIL 87 calcification – in the putamina-caudate nuclei 163 – in the subcortical region 164 calcium deposit 112 calvarial hemangioma 404 – underlying DSM 404 CAMS, see cerebrofacial arteriovenous metameric syndrome Canadian Pediatric Ischemic Stroke Registry 852 Canadian stroke register 537 capillary – diffuse bilateral hemangioma – – spontaneous regression 568

– hemangioma 64, 415 – – of the cheek 594 – vascular malformation 635 – venous proliferation 481 carbon dioxide laser 580 carcinoma of the subarachnoid space 25 cardiac – failure 147, 272, 282 – insufficiency 249 – manifestation 192 – – in large hemangiomas 143 – – in VGAM 143 – output 192 – ultrasound evaluation 193 cardiogenic shock 192 cardiomegaly 64 cardiovascular malformation 608 carotico-ophthalmic aneurysm 814 carotid-cavernous fistula (CCF) 768 – balloon 769, 771 – direct traumatic venous dissection 776 – glue 771 – proptosis 771 – retrograde flow into cerebral veins 768 – transcranial drainage 768 – unilateral blindness 775 cataract 481 catecholamine release 194 catheter glue 210, 217 cavernoma 726 – deep-seated 475 cavernous – capture 405, 414, 425 – hemangioma 563 – malformation 459 – plexus fistula 444 – sinus – – matures 128 – – thrombophlebitis 803 – – capture 62, 154 CCF, see congestive cardiac failure, carotid-cavernous fistula cephalic – ectomesoderm 361 – mesoderm 485, 608 cerebellar – arteriovenous shunt 733 – atrophy 73 – cortical dysgenesis 610 – hemorrhage 319 – hypoplasia 610 – hypoplastic hemisphere 612 – pial congestion 180 cerebral arteriovenous fistula (CAVF) 37, 227 – asymptomatic – – management 280

969

– endovascular management 281 – – complications 281 – incidence 234 – infratentorial – – angioarchitectural features 235 – male:female ratio 249 – multiple 231 – natural history 265 – radiosurgery 280 – single 228 – supratentorial 280 – – angioarchitectural features 235 – – prenatal diagnosis 257 – – revealing symptoms 257 – – topography 235 – surgery 280 – targeted embolization 280 cerebral arteriovenous malformation (CAVM) 292, 814 – angioarchitecture 298 – associated conditions 302 – complete exclusion 330 – draining into a DVA 302 – epilepsy after surgery 345 – familial occurrence 302 – hemorrhagic episodes 344 – hemorrhagic event 292 – HHT-related – – angioarchitecture 241 – infants 340 – mimicking conditions 306 – neonates 340 – partial treatment 336 – partial, targeted treatment 98 – pial cerebral – – dural supply 447 – presenting symptom 240 – surgery 345 – targeted embolization 336 – technical management 345 – tectal 113 – treatment 330 cerebral emboli 867 cerebral melting process 59 cerebral vascular malformation (CVM) 504 – familial 504 – metameric 504 – nonfamilial 504 cerebral venous thrombosis (CVT) – annual incidence 537 – cerebral calcification 540 – cerebral parenchymal infarcts 545 – chronic systemic disease 539 – cortical vein occlusion 546 – CT 545 – enlarged facial veins 547 – fibrinolytic therapy 557 – focal neurological deficits 547

970

Subject Index for Volume 3

– hemorrhagic complications 556 – infections 539 – low-molecular-weight heparin 556 – malignant tumor 539 – MRI 545 – neonates 539 – prothrombotic state 539 – seizures 547 – systemic anticoagulation 556 – thrombotic therapy 557 – water-related manifestations 537 cerebro-dural facial venous disease 503 cerebrofacial arteriovenous metameric syndrome (CAMS) 39, 40, 50, 359, 362, 364, 365, 372, 487, 823 – angiogenic activity 380, 384 – bilateral thalamic location 370 – bone hypertrophy 383 – CAMS-1-like syndrome 388 – de novo location in the brain 384 – metameric lesion 376 – olfactory region 376 – progressive visual loss 376 – proliferative 384 – pseudogrowth 384 – schematic representation 363 – skull base bones 490 – topographic distribution of vascular lesion 363 – transdural arterial supply 377 – visual acuity 376 – visual field defects 376 – visual tract involvement 375 cerebrofacial vascular metameric syndrome (CVMS) 39, 47, 385, 486, 487, 554, 555 – bony changes 490 – involvement of forehead and nose 486 – mandible involvement 490 – maxilla 486 – maxillary involvement 490 cerebro-meningeal haemorrhage 169 cerebrospinal fluid (CSF) 65, 66 – nonchoroidal formation 65 cervical – artery dissection 867 – spine vein 400 cervicofacial vascular malformation 633, 669 – direct puncture 652 – direct puncture of the mandible 654 – ECA ligation 655 – embolization 652 – foreign body reaction 653 – healing 653

– 3D rotational angiography 653 – signs and symptoms 652 – surgical resection 652 – treatment complications 653 CHD, see congenital heart disease chicken pox 857 chimera 639 choroid – fissure 7, 110 – plexus hypertrophy 481, 491 choroidal artery – spontaneous regression 207 chronic mucocutaneous candidiasis 807 circle of Willis – stenotic phenomena 295 cleft 128 – palate 141, 388, 399 – schizencephalic 474 clinical evaluation score 77 coagulation disorder 400, 411 coarctation 128 – of the aorta 608 Cobb syndrome 48, 726 coil 247, 251, 269, 279, 288, 424 – after transarterial catheterization 289 – arterial 451 collagen 95 – deficiency 792 – disorder 692 – fiber 22 – type III disease 700 collateral circulation 438 coloboma 481, 627 color flow Doppler examination 269 complex – orbitofacial arteriovenous malformation 657 – venous lesion 469 compressive hematoma 719 congenital – aneurysm 791 – heart disease (CHD) 867 congestive cardiac failure (CCF) 63, 142, 143, 151, 270, 396, 574, 757 – medical treatment 149 – MR 146 – MRA with 3D 146 – spontaneous evolution 144 congestive heart failure, see congestive cardiac failure conjoined – sinus 520, 526 – – superior sagittal 520 – twins 511 consumption coagulopathy 579, 581 cord – compression 717 – hypersignal 902

coronary perfusion 193 corporal scheme 637 – oral references 637 corpus callosum 15, 164, 376 cortex dysplasia 246 cortical – cerebellar vein 494 – cerebral vein, pseudo-phlebitic 201 – migration anomaly 468 – ribbon 8 – vein – – anomaly 471 – – occlusion 484 – – phlebitic aspect 173 – – pseudo-phlebitic appearance 162 – – reflux 181 – – thrombosis 481 cranial – bone enlargement 67 – nerve impairment 699 – vault 152 – – bone thickening 72 craniopagus 507 – angiography 510 – balloon redistribution 527 – CT scans 531 – epidural lakes 527, 529 – functional testing 531 – MRA 531 – MRI 531 – MRV 531 – postoperative imaging studies 531 – surgery 510 – tentorium 510 – three-dimensional CT reconstruction 534 – twins 524, 533 – – presurgical 3D models 524 – – shared common sagittal sinus 533 – – surgical management 534 – – surgical separation 533 craniopharyngioma 23 cryptophthalmos 627 CSF, see cerebrospinal fluid cutaneous – capillary malformation 645 – – polyvinyl alcohol 645 – vascular malformation 726 CVM, see cerebral vascular malformation CVMS, see cerebrofacial vascular metameric syndrome CVT, see cerebral venous thrombosis cyanogenic cardiopathy 870 cyanosis 148 Cyrano’s hemanioma 574

Subject Index for Volume 3 cystic – hygroma 672 – lesion 643 D Dandy-Walker syndrome 608, 610 de novo cavernoma 102, 399 deep venous drainage, see venous drainage delayed hemorrhage 344 Denver test 161 deoxycycline 676 detachable balloon 787, 788 – preloaded system 788 developmental venous anomaly (DVA) 305 – bilateral thalamic 502 – deep-seated development 456 – giant cerebellar 505 – right occipital 502 – tumors 459 diaphragm-like obstacle 434 digoxin 198 discoloration 479 disease development – structural weakness 30 dissecting aneurysm – anticoagulation 833 – antiplatelet medication 848 – infants 832 – infarct 833 – ischemic complication 848 – partial clipping 848 – remodeling 833 disseminated intravascular coagulation 602 distal – basilar artery – – occlusion 620 – emboli 777, 864, 878, 882 – sigmoid venous occlusion 70 diuretics 198 dobutamine 199 dolichocervical ICA 617 dolicho-P1 segment 628 dopamine 199 Doppler ultrasound 196, 204 Down’s syndrome 800 drug absorption 873 DSM, see dural sinus malformation ductus arteriosus 96, 148, 608 – reopening 199 dural arteriovenous shunt (DAVS) 41, 180, 447, 776 – adult type 395 – – in children 444 – age groups 392 – cavernous sinus 446 – classification 390

– – – – – – – –

disease groups 392 embolization 444 incomplete surgery 444 infants 299, 436 juvenile type 48, 311, 394, 441, 822 natural history 396, 436 partial embolization 441 partially thrombosed vein of Galen 451 – prenatal diagnosis 393 – remote ligation 444 – sigmoid sinus 445 – spontaneous thrombosis 445 – superior sagittal sinus 442 – therapeutic window 453 – treatment 451 – vein of Galen 447 – – aneurysmal dilatation (VGAD) 116 dural sinus – high flow 312, 313 – malformation (DSM) 393, 393, 465, 500 – – enlargement 46 – – in utero MR diagnosis 41 – – large middle cranial fossa 406 – – location 418 – – partially thrombosed 398 – – psychiatric manifestations 445 – – thrombosis 418 – – with giant pouch 398 – occlusion – – dysmaturation of the jugular bulbs 167 – proliferation 399 – shunt – – sigmoid sinus 178 – – torcular sinus 178 – sump 437 – thrombosis 180 DVA, developmental venous anomaly dysmaturation 62 dysmorphic syndrome of chromosome 2 881 dysplastic venous channel 681 E echocardiography 196 ectasia 321 – of the venous collector 459 ectatic vein 741 ectopic choroid plexus 573 edema 669 Ehlers-Danlos syndrome 302, 700, 792, 813, 817 elastin 95 emboli – cruoric nature 868 – from cardiac origin 869

971

– of cardial origin 867 embolization 420, 424, 426, 459, 492 – transarterial 451 – with glue 429, 434 embryogenesis 638 embryonic tentorial sinus 406, 429 encephalocraniocutaneous lipomatosis 246, 248 encephalomalacia 58, 61, 142 – periventricular 148 encephalotrigeminal angiomatosis 479 endoglin 238 – deficiency 90 endothelial cell – mediator 95 – receptor 95 enophthalmos 496 epidermal – fistulous communication 694 – hemangioma – – cavernous type 597 – – vascular space 530 – hematoma 398, 692, 717 – intraspinal venous mass 716 – plexus 511 – sinus 513 – space 513 – venous drainage 784 – venous plexus 513 epidermoid cyst 23 epilepsy 142, 162, 249, 485 epinephrine 666 epistaxis 169, 238, 374, 378, 651, 767, 768, 770, 785, 855 – etiology 786 – false aneurysm 786 – tumor biopsy 786 erratic venous embolic material 219 E-selectin 561 ethanol 581, 605 – sclerotherapy 659, 672 Ethibloc 662, 671 exophthalmos 71, 376 external carotid aneurysm 823 external carotid artery ligation 648 extracranial arteriovenous fistula 687 extraspinal arteriovenous fistula 687 eyelid hemangioma 591 – blindness 590 – intralesional steroid injection 591 F Fabry’s disease 893 facial – asymmetry 651 – capillary-venous malformation 480

972

Subject Index for Volume 3

– circulation 170 – cleft 639 – collateral circulation 71, 172 – dysmorphia 608 – hemangioma 500, 518 – – distribution 386 – vein 138, 169, 438 – – collateral circulation 142, 169 – – dilatation 681 – – dilated 684 failure to thrive 163 false aneurysm 316, 327, 329, 353, 780, 800, 821 falx 521 – cerebri 520, 779 familial – candidosis 810 – disease 85 – hemiplegic migraine 85 – multiple cavernoma 503 – paraganglioma 87 Fc gamma receptor II (FcγRII) 561 fibrinolysis 778 fibromuscular dysplasia 792 fistula in the prefrontal branch 70 flank hemangioma 718 focal – atrophy 315 – cerebral atrophy 314 foramen ovale 148 frontal – bone hypertrophy 490 – varix 467 fronto-orbital – lymphatic malformation 497 – venous malformation 498 fusiform – aneurysm 624 – arterial ectasia 804 – intrapetrous aneurysm 615 G β-galactosidase deficiency 893 galenic vascular lesion 39 Gelfoam – powder 581 – strips 759 genealogical tree 86 genetical disease 30 genital bleeding 238 germinal matrix 5, 468 giant – aneurysm 836, 867 – – formation 790 – distal arterial aneurysm 322 – dural sinus lake 501 – lymphatic malformation of the face 495

– MCA – – partially thrombosed 828 – pouch 396 – – mass-related symptoms 231 gingival hemorrhage 642 glaucoma 480, 626 glia limitans 18, 22 glioblastoma multiforme 24 glue 248, 277, 424, 426, 642, 657, 719, 771, 846 – drop 218 – fragmented 218 GLUT 1 561 granulation 59 growth differentiation factor 515 guidewire 420 guiding catheter 204 H head circumference 150 headache 895 heart failure, see cardiac failure hemangioendothelioma 584 – infiltrative 606 hemangiogenesis 564 hemangioma 141, 143, 399, 559, 560, 713 – airway obstruction 577 – alcohol 583 – angiography 571 – bilateral facial 571 – bleeding 574 – blindness 575 – calvarial 404 – capillary blush 572 – central nervous system involvement 564 – CO2 laser 588 – congestive heart failure 574 – cosmetic suffering 598 – Cyrano’s hemangioma 574 – destruction of facial features 574 – direct intralesional angiogram 583 – direct percutaneous puncture embolization 582 – direct puncture 585 – disseminated form 564 – distribution 386 – ectopic choroid plexus 573 – embolization 575, 576, 581, 587, 588 – facio-orbital 565 – fatty fibrous tissue 569 – female:male ratio 560 – fibrofatty residual 565 – geographic distribution 566 – healed ulceration 569 – highly proliferative 600, 601

– – – – – – – – –

histochemical analysis 560 hormone receptor 578 indications 577 intracranial 613 intralesional embolization 583 involution 566 laser treatment 583 local steroid treatment 578 malformation of capillary type 585 – mandibular growth alteration 575 – monozygotic twin 569 – MRI 571 – multifocal 564 – multiple session 582 – of the bone 597 – of the eyelid 591, 598 – of the mandible 593 – of the tongue 596 – oral 592 – orbital 572 – pain 577 – pattern of tumor growth 566 – perichondral involvement 577 – radiation therapy 579 – side effects 579 – skin scar 574 – somatic mutation 563 – spontaneous involuting phase 566 – subglottic 589 – surgical excision 581 – tumor specimen 581 – ulceration 566, 574 – ultrasound Doppler imaging 571 hemangio-pericytoma 595 hematoma 316 – compressive 719 – epidural 398 – intracerebral 335, 396, 460 – intraparenchymatous 459 – mural 827 – subcortical parietorolandic 345 – subdural 421 hematomyelia 725, 731, 740, 763 hemiatrophy 855 hemiplegia, right-sided 177 hemispheric atrophy 265, 266 hemodynamic obstacle 320 hemolymphangioma 680 – tongue lesions 680 hemolytic anemia 602 hemoptysis 238 hemorrhage 220, 249, 797 – angiopathy 37, 51, 307, 356 – capillary 415 – cerebellar 319 – delayed 285, 344 – gingival 642 – infarction 261, 457 – intracerebral 317, 328, 329, 538

Subject Index for Volume 3 – intracranial 317, 374, 393 – intraventricular 44 – subarachnoid 24, 44, 357 – venous infarction 315 heparin 204, 405, 579, 882 – low-molecular 421 hereditary hemorrhagic teleangiectasia (HHT) 37, 43, 86, 236, 239, 303, 347, 639, 692, 738, 785, 792, 855 – criteria 238 – genotype 236 – hormonal events 237 – neonates 273 – patients 867 – phenotype by age 241 – progression 237 – screening of the CNS 244 – seizure 284 herpes zoster 876 Heubner artery 124, 340 HHT, see hereditary hemorrhagic teleangiectasia high-flow angiopathy 98, 99 high-flow fistula in the prefrontal branch 70 Hirschsprung’s anomaly 737 holo hemispheric nidus 897 holoprosencephaly 513 homocystinuria 893 human immunodeficiency virus (HIV) 805, 811, 870, 871 hydrocephalus 152, 155, 255, 400 hydrocoil 657 hydrodynamic disorder 64, 152, 341 – interstitial water 66 – lymphatic system 66 hydromyelia 142, 189 hydrovenous – disorder 618 – dysfunction 62 – manifestation 77 – maturation process 67 – – suture fusion 67 hyperemia – conjunctiva 773 – of the cord 756, 903, 904 hypoglossal artery 617 hypothermia 905 hypoxia – injury 853 – regional 853 I iatrogenic – injury 780 – – cardiac failure 781 – – coiling 782 – occlusion 218 immunodeficiency 807

infarction 610 – bacterial 23 – multifocal 315 infectious arterial aneurysm (IAA) 803 – antibiotic treatment 803 – cavernous internal carotid artery 807 – cavernous sinus thrombophlebitis 803 – infarction 806 – infectious emboli 803 – osteomyelitis 803 – sphenoid sinus infection 803 – thrombosis 806 inferior – petrosal sinus 170 – striate vein 138, 468 inflammation 23 infratentorial pial reflux 180 inotropic agent 199 interferon 591 internal capsule 10 internal carotid artery (ICA) 825 – dissection 777 – focal stenosis 875 – rupture into the sphenoid sinus 770 – traumatic aneurysm 780 internal iliac artery occlusion 210 interparietal suture 517 interperiosto-leptomeningeal space 513 interventricular – foramen 124 – – arteriovenous fistula 120, 122 – – arteriovenous shunt 124 – septum pattern 194 intracerebral – hematoma 335, 396, 460 – hemorrhage 317, 328, 329, 538 intracranial – acute arteriography 867, 871 – arterial aneurysm 779 – – tentorial edge 779 – arteriovenous shunt – – age groups 56 – – cerebral manifestations 76 – – frequency of various types 57 – – hydrodynamic manifestations 64 – – in utero manifestations 63 – – neurological symptoms 76 – – symptom groups 63 – – systemic manifestations 64 – bruit 684 – hemangioma 613 – hemorrhage 300, 317, 374, 393, 697

973

– hypertension – – ventricular shunting 160 – pulsatile bruit 548 – subarachnoid location 621 – vascular malformation – – clinical presentation 58 intracranial aneurysm – fusiform 809 – in children 789 – – age at presentation 794 – – 3D angiogram 839 – – antiplatelet therapy 830 – – associated conditions 790 – – autopsy series 797 – – clinical symptoms at presentation 796 – – embolic event 830 – – etiology 796, 797 – – gender 794 – – location 835, 836 – – occlusion of both vertebral arteries 841 – – retrograde catetherization 841 – – seizure 795 – – spontaneous occlusion 839 – – stroke 795, 830 – incidence 793 – multiple 809 – neonates 795 intradural venous ectasia 709 intramasseteric venous malformation 663 intramedullary – arteriovenous malformation 711 – edema 711 intranidal aneurysm 328, 337 intraosseous slow-flow malformation 658 – ethanol sclerotherapy 659 – reossification 659 intraosseous vascular malformation 650 intraparenchymatous hematoma 459 intratympanic aneurysm 822 intraventricular hemorrhage 44 ischemia in the lower limb 218 ischemic – deep-seated infarct 832 – hemorrhagic stroke 877 – sequela of the spinal cord 901 – stroke 347 – ulcer 643 Ischemic Stroke Registry 852 J jugular – bulb 396 – – bilateral stenosis 75

974

Subject Index for Volume 3

– – bilateral occlusion 177 – – DSM 434 – – dysmaturation 136, 158, 167, 414, 423, 431 – – occlusion 168 – – progressive occlusion 181 – – stenosis 169 – dysmaturation 43 – foramen – – closure 62 – stenosis 183 K kaposiform hemangioendothelioma 581, 603, 604 Karnovsky Scale 78 Kasabach-Merritt syndrome (KMS) 580, 584 Klippel-Trenaunay syndrome 491, 726, 731 kyphoscoliosis 746 L laryngotracheoplasty 588 laser photocoagulation 635, 678 late neurological disorder 162 lateral – atrial vein 495 – mesencephalic vein 135 leptomeningeal collateral circulation 888 leptomeninges – metastases 25 – nerve supply 22 – pia mater 21 – transforming growth factor 21 leukemia 539 Lewis Y (LeY) antigen 561 limbic – arch 129 – – persistent 126 – circle – – anterior choroidal 126 – system 128 – – midline fusion 130 Lineac 358 lingual lymphatic malformation 676 lip hemangioma – prenatal diagnosis 567 – spontaneous involution 567 lipoma 246 locked-in syndrome 778 longitudinal vessel wall proliferation 631 lupus anticoagulant 540 lymphatic malformation of the cranial cervical region 411 lymphoma 24

lymphovenous maxillofacial abnormality 399 M macrocrania 61, 152–154, 185, 201, 249, 254, 547 – hydrocephalus 142 – normal curves 83 macrocystic lymphatic malformation 670 – CT imaging 671 – ethanol sclerotherapy 672 – hemorrhage 675 – in utero 675 – jugular lymph sacs 670 – MRI 670 macrofistula 742 malignant – melanoma 25 – vascular tumor 595 mandibulectomy 646 mandibular malformation 648 Marfan’s syndrome 792 masseteric muscle 643 maxillary – artery/vein fistula – – cranial segmental arteries 697 – – high-flow 698 – – neurological deficits 697 – – venous congestion 697 – hypertrophy – – bony involvement 482 – vascular malformation 648 maxillary-jugular vein fistula 699 – systemic manifestations 699 maxillofacial vascular malformation – arteriovenous 638 – capillary 638 – capillary venous 638 – clinical manifestation 638 – venolymphatic 638 – venous 638 MCA, see middle cerebral artery medial occipital sinus 516, 528 medullary vein 152, 164, 456 – reflux 708 melena 238 melting-brain syndrome 62, 73, 75, 296, 396, 413, 465, 501, 541, 618 – CT 147 – severe supratentorial 184 meningoencephalitis 886 mental retardation 438 mersin 561 mesencephalic – aqueduct 152 – AVM 334 mesoderm 640

microcystic lymphatic malformation 675 microgyria 465 microphthalmos 627 middle cerebral artery (MCA) 251 – trunk – – embolic material 273 – aneurysm 91 middle cerebral steal 195 migraine 293, 300 – stroke 893 migrant cell 8 mirror aneurysm 491 monogenetic disorder 34 movement disorder 165 moyamoya – disease 51, 53, 144, 324, 325, 608, 627, 792, 867, 885, 888, 892 – – bilateral 887 – – neonatal 131 – – symmetrical 887 – – familial 906 – network 120 moyamoya-like – network 908 – syndrome 893 multifocal – familial cerebral cavernomatous malformation 476 – lesion 234 – lymphatic malformation 677 – – orbital involvement 677 multiorgan failure 142, 146 multiple – arteriovenous fistula 233 – berry aneurysm 818 – cavernoma – – familial case 45 – – hemorrhagic changes 46 – cutaneous and mucosal venous malformation (MCMVM) 87, 465, 503 – hemangioma 385 mural – angiogenesis 631 – hematoma 827 – impairment 327 mutation – germinal 34 – postnatal 34 – somatic 34 mycotic arterial aneurysm 803, 804 myelination 11 – gliosis 13 myocardial – perfusion 193 – reserve 194

Subject Index for Volume 3 N N-butyl cyanoacrylate (NBCA) 584 necrosing encephalitis 886 necrosis 591 neonatal – dural covering – – falx 2 – – lateral sinus 3 – – superior sagittal sinus 2 – – torcular region 2 – score 150 Neonatal Coma Scale 80 nerve palsy 278 neural crest 485, 608 – derivative 609 – disorder 478 – mesoderm contribution 491 – migration 91 neuroblastoma 539 neurocognitive – delay 161 – evaluation 82 neurocutaneous syndrome 360, 609 neurofibromatosis 302, 304 – type 1 692, 700, 792, 816, 864 neurological deficit 142, 162, 169, 218, 249 newborn – capillary network 4 – tentorium 4 nidus – multifocal 298 – single 298 NO 198 non-Hodgkin lymphoma 539 noninvoluting capillary hemangioma (NICH) 567, 583, 587, 659 notochord 514 O occipital – artery anastomosis 703 – horn 167 occipito-vertebral arteriovenous fistula 705 occlusive – extracranial artery 610 – intracranial artery 610 OK 432 676 oliguria 195 open bite syndrome 681 ophthalmic – artery 614 – vein 172, 269 – – manual compression 395 optic – nerve 376 – – hypoplasia 627

– radiation 14 oral hemangioma – surgical treatment 592 – teeth eruption 591 orbital – hemangioma 572 – phlebolith 464 osteomyelitis 803 osteopetrosis 550 otorrhagia 770 P pachygyria 465, 471, 472, 483 papilledema 174 parachordal arteriovenous fistula 687 – associated tumors 692 – cephalic 689 – clinical manifestations 692 – collagen diseases 692 – congestive cardiac failure 692 – embolization 696 – epidural AVS of the spine 689 – hemorrhage 692 – neurological deficits 692 – somitic 689 – venous drainage 689 paraganglioma, familial 87 paraparesis 725, 744 paraplegia 747 paraspinal arteriovenous – fistula 693 – – SAMS 17-18 715 – malformation 693 parent vessel occlusion 771 Parinaud syndrome 333 partial targeted – embolization 336, 337 – session 205 partial thrombosis 242 – of the pouch 321 pathology specimen 109 PCA aneurysm – glue 844 PDGF, see platelet-derived growth factor Pediatric Glasgow Coma Scale 79 perforating artery 827 perfusion break-through phenomenon 220 periarteritis nodosa 877 perimedullary – pial network congestion 743 – vein 703 perimesencephalic – vein 168 – network 212 perinidal angiogenesis 306 peripontine vein 168

975

persistent – ductus arteriosus 196 – embryonic artery 622 – limbic arch 126 pervascular space 22 – of arteries 24 petrous vein 135 PHACE syndrome 385, 487, 491, 518, 562, 610, 822, 867 – antiplatelet therapy 630 – associated hemangioma 899 – clinical imaging features 611 – female predominance 612 – proliferative disease 612 – pseudo-rete 631 – spectrum of lesions 610 – transdural supply 627 phakomatosis 360, 478 pharyngojugular arteriovenous fistula 700 phenotypic expression 33 phlebolith 498, 663 pia mater 21 pial – arteriovenous communication 311 – arteriovenous shunt 35 – – secondary to sinus high-flow lesions 309 – nidus 477 – reflux 414, 422, 424, 436, 444, 697, 773 – – in the temporal vein 177 Picibanil 676 pinna 643 placenta-associated antigen 561 platelet-derived growth factor (PDGF) 94 pneumoencephaly 770 polycystic kidney disease (PDK) 792, 814 – recessive form 815 polymicrogyria 473 port-wine stain 478–480, 642, 659 posterior – communicating artery route 775 – embryotoxon 627 – fossa 891 – – arteriovenous shunt 269 – – DVA 431 – – hematoma 473 – – hemorrhagic complication 773 – – malformation 297, 611, 615 – – sinus 516 – – venous congestion 417 postischemic luxury perfusion 306 post-traumatic – dissecting aneurysm 801 – – coiling 802 – – collateral circulation 802

976

Subject Index for Volume 3

– – infants 802 – false aneurysm 798 – – age at presentation 797 – sinus thrombosis 776 precocious puberty 163 prednisone 578 premature baby 144 pro-atlantal artery 610 – type-1 624 procollagen type III 87 progressive – motor deficit 258, 338 – neurological deterioration 378 – thrombosis 300 proliferating – cell nuclear antigen (PCNA) 561 – angiopathic disease 448 – – dural contribution 448 – angiopathy 51, 56, 297, 306, 310, 893, 895 proptosis 771 prosencephalon – median vein 109, 110 prostaglandin E1 199 protein – C 539, 892 – S 539, 892 pseudo-aneurysm 733 – scarring 878 pseudo-moyamoya pattern 889 pseudo-phlebitic – cortical cerebral vein 201 – venous cortical network – – three-dimensional view 173 pseudo-tumor cerebri syndrome 547 pseudoxanthoma elasticum 792 pulmonary – arterial hypertension 192 – arteriovenous fistula 742, 867 – edema 195 – fistula 855 – vascular resistance 148 pulse dye photocoagulation 580 putamina-caudate nuclei 163 – calcifications 163 R rapidly involuting capillary hemangioma (RICH) 567 rebleeding 344 reflux, dysmaturation of the jugular bulbs 167 regionalized mesoderm 361 rehemorrhage 744 remote pial shunt 439 Rendu-Osler-Weber disease 236, 692, 855

retinal vascular malformation 365, 480 revealing trigger 103 rhinopharyngitis 858 ROW disease 88, 733 rt-PA 557 ruptured aneurysm, incidence 794 S saccular aneurysm 813, 836 – balloon occlusion 837 – clip 837 – coil 837 – glua 837 – ligation 837 – parent artery occlusion 837 – pretherapeutic evaluation 837 SAH recurrence 850 SAMS 39, 387, 487 SCAVM, see spinal cord arteriovenous malformation schizencephaly 465 sclerotherapy 662 segmental agenesis 610 seizure 219 – classification 343 – various types 343 semioval center 14 severe cardiac failure 271 – clinical characteristics 197 shear stress 94, 96, 98 sickle cell disease 862, 867, 892 sigmoid sinus – AVF 434 – bilateral occlusion 172, 190 – bilateral thrombosis 178, 413 – glue 209 – occlusion 549 – reopening 183 – thrombosis 548, 776 signaling in the human embryo 515 sinus – pericranii 128, 139, 399, 405, 464, 467, 468, 556, 897 – – surgical revascularization 897 – reflux 137 slit ventricle syndrome 68 sodium – ducal 661 – tetradecal 661 sonic hedgehog 515 SPECT 482 sphenoid – bone hypertrophy 490 – sinus – – communication 780 – – infection 803 spinal artery aneurysm 754

spinal cord – aneurysm 800 – arteriovenous malformation (SCAVM) 88, 721 – – 3D angiography 765 – – aneurysm 744 – – basket 751 – – bifocal 731 – – bruit 738 – – cardiac failure 725, 737 – – coils 759 – – cutaneous discoloration 757 – – dorsal pain 729 – – embolization 733 – – evoked potentials 759 – – false AA 753 – – false sac 740 – – fistula 722 – – gamma knife radiosurgery 766 – – Gelfoam strips 759 – – glue 736, 759 – – incidental finding 746 – – infants 740, 755 – – intraventricular hemorrhage 738 – – ischemic neurological symptoms 746 – – large venous ectasia 729 – – long-term follow-up 733 – – male:female ratio 737 – – MRA 750 – – MRI 750, 751 – – multiple lesions 738 – – myelomeric location 725 – – neonates 737, 738 – – neurological deficits 746 – – nidus 722 – – paraparesis 744 – – partially thrombosed pouch 762 – – particle embolization 723 – – polyvinyl alcohol (PVA) particles 759 – – procedure-related morbidity and mortality 738 – – proliferative disease 754 – – radiotherapy 766 – – recovery from symptoms 744 – – repeated hemorrhagic episodes 761 – – scalloping 750 – – stereotactic radiosurgery 766 – – surgery 761, 765 – – therapeutic sessions 759 – – transdural narrowing of the radicular arteries 758 – – transmedullary supply 735 – cavitation 72 – vein congestion 717 spinal dysraphism 480

Subject Index for Volume 3 spontaneous thrombosis 128, 184, 231, 500 sporadic abnormality 34 staging 205 stapedial artery persistence 615 stenotic – distal internal carotid artery 628 – kinking 321 stenting 424, 452 sternal – clefting 610 – defect 518 strabismus 610 straight sinus 124, 422 streptokinase 579 striate vein congestion 164 Sturge-Weber syndrome 47, 478, 479, 493 subarachnoid hemorrhage 24, 44, 262, 356, 357, 709, 744, 768 subcallosal anastomosis 130 subcortical – cavernoma 474 – leukoencephalomalacia 267 – parietorolandic hematoma 346 subcutaneous midline varix of the forehead 466 subdural – hematoma 421 – sequelae 157 subependymal – anastomosis 136, 138 – arterial supply 211 – artery – – spontaneous regression 207 – atrophy 67, 156, 163 – – prenatal 144 – cavernoma 167 – reflux 215 – vein – – hemorrhage 172 – – reflux 137 subependymal-striate anastomosis 124 subgaleal mass 409 subglottic hemangioma – embolization 589 – symptoms 589 subpial – damage 59 – hemorrhage 24 – space (sps) 17, 22 – – inflammation 19, 20 – – spinal 19 – – tumors 20 – venous congestion 298 sulcal perforator 755 sulcocommissural branch 749 superior sagittal sinus 512

suprasystemic pulmonary hypertension 198 supratentorial pial congestion – dysmaturation of the jugular bulbs 167 sylvian arteriovenous fistula 266 syringomyelia 142, 189 systemic – disorder 448 – lupus erythematosus 877 T Takayasu’s disease 893 targeted embolization 353 teleangiectasia 43, 44, 90, 506, 566, 580, 585, 659, 742 – deep-seated 505 temporal – hemangioma – – prenatal diagnosis 570 – vein – – pial reflux 177 tetraplegia 723 thoracic arteriovenous malformation, embolization 691 thrombocytopenia 602, 807 – transfusion 605 thrombolysis 544 thrombosed – distal sigmoid sinus 400 – lesion 49 – venous pouch – – angiogenic colonization 215 thrombosis 128, 229, 315 – dural sinus malformation 418 – of the deep venous system 538 – of the straight sinus 544 tongue hemangioma 595 tonsillar prolapse 43, 62, 68–71, 142, 180, 189, 412, 415, 417, 440 tooth extraction 382 torcular 528 transcerebral – collateral circulation 179 – venous collateral circulation 164 – venous system 455 transcortical bilateral collateral circulation 553 transdural revascularization 886 transependymal resorption 61 transforming growth factor b1 (TGF-b1) 94, 238 transient – hemiparesis 283 – ischemic attack (TIA) – seizures 843 transophthalmic catheterization 646 transtorcular approach 172

transverse sinus 544 trauma 444 traumatic – aneurysm 798 – – dissection 799 – dissection 777 – insult of vascular malformation 783 – stroke 878 trigeminal – artery 610, 620 – nerve territory 486 triggering event 33 trisomy 21 889 – regressive deficit 859 tuberous sclerosis 792 tumor suppressor gene 504 twin – aneurysm 819, 820 – pregnancy 144 – sibling 813 type IV collagenase 561 U umbilical artery 204 unilateral – dural sinus thrombosis – – clinical manifestation 540 – sinus occlusion 549 urokinase 557, 561 V Valsalva maneuver 65, 469 varicella 873, 857 – zoster virus (VZV) 876 varix of the left external ear 783 vasa vasorum 449, 790, 812 vascular – abnormality 34 – anomaly 34 – disease 30 – – classification 31 – – genetics 32 – – classification 31 – – genetics 32 – endothelial growth factor 481, 561, 622 – lesion – – age 33 – – causative trigger 562 – – children 62 – – in utero 58 – – infants 62 – – neonates 59 – – revealing trigger 562 – – subtypes 35 – malformation 560 – – CT 641

977

978 – – – – – – –

Subject Index for Volume 3

– Doppler technique 641 – MRI 641 – target 102 – timing 102 – trigger 102 – ultrasound 641 mapping of the cephalic region 609 – morphogenesis 633 – remodeling 256 – – modulators 95 – systemic resistance 192 – trauma 767 – – anticoagulation 787 – – arterial spasm 787 – – CT 787 – – detachable balloon 787 – – false aneurysm 787 – – mass effect 767 – – MRI 787, 788 – vulnerability – – phenotypic expression 92 vasculature vulnerability 103 vasculogenesis 33, 504 vasodilatator 198 VEGF, see vascular endothelial growth factor vein of Galen – aneurysmal dilatation (VGAD) 112, 115, 116 – – dural arteriovenous shunts 117 – aneurysmal malformation (VGAM) 38, 105, 117, 118, 447 – – age at diagnosis 207 – – age at first consultation 207 – – age groups 108 – – arterial supply 109, 118 – – brain damage 60 – – cardiac parameters 196 – – cerebellar arteries 118 – – choraoidal type, neonatal specimen 112 – – clinical evaluation 192 – – color Doppler ultrasound 146 – – complications 219 – – compressed feeder 120 – – consumption of coagulation factors 220 – – dural contribution 120 – – embryology 110 – – endovascular treatment 203 – – epsilon shape 124 – – evaluation of renal and liver function 192 – – femoral puncture 203 – – fluid level 187 – – follow-up 205 – – in neonates 60, 61 – – limbic arterial arch 118 – – mental retardation 162

– – – – – –

– – – – – –

morbidity 210 morphological results 208 natural history 141, 142 neonates 191 neurocognitive delay 142 neurological outcome by age group 221 – – neurosurgical management 223 – – nidus 122 – – optimal therapeutic window 142, 199 – – overall mortality 220 – – pretherapeutic evaluation 149 – – proposed treatment 207 – – radiotherapy 189, 224 – – regrowth 191 – – rupture 205 – – seizures 162 – – shrinkage of the mass 187 – – spontaneous disappearance 38 – – spontaneous occlusion 190 – – staging 205 – – stereotactic radiosurgery 165, 224 – – subenpendymal contribution 125 – – subependymal arteries 118 – – sudden death 220 – – surgery 221 – – technical management 203 – – therapeutic abstention 208 – – therapeutic decision 207 – – therapeutic results 208, 221 – – total exclusion 205 – – transhemispheric network 121 – – transvenous treatment 223 – – treatment measures 191 – – whirling phenomena inside the pouch 187 – – with patent sinuses 162 – prenatal diagnosis 57 – varix 117 venolymphatic – malformation 679 – – orthodontic therapy 679 – – polyvinyl alcohol 679 – paraspinal malformation 785 venous – angioarchitecture 298 – angioma 455 – angiopathy 311 – brain damage 541 – cerebral infarction 451 – congestion 255, 440 – disconnection 444 – disposition – – anatomical analysis 522 – dissection 776 – drainage

– – alternative embryonic routes 109 – – epsilon shape 134 – – infant 70 – – neonatal cerebral 70 – – types 132 – ectasia 229, 754 – enlargement 321 – hemorrhage 316 – high-flow angiopathy 312 – hypertension 641 – infarction 219, 292, 396, 410 – – bilateral 411 – ischemia 315, 457, 539, 755, 767 – lake 403 – malformation of the orbit 496 – pouch 229, 321, 322 – pseudoaneurysm 318, 320 – reflux 69 – remodeling 426, 432, 433 – return – – epsilon shape 135 – steal 437 – stenosis 754 – stroke 411 – stump 800 – system – – epsilon shape 133 – thrombosis 62, 316 – vascular malformation 665, 668 – – airway 660 – – alcohol sclerotherapy 661 – – cardiac arrest 666 – – CT imaging 660 – – estimation of the volume 664 – – facial asymmetry 669 – – MRI 660, 665 – – mucosal necrosis 666, 668 – – of the upper lip 666 – – recanalization 666 – – recurrence 661 – – remodeling of the bone 670 – – resolution of the mass 664 – – sclerotherapy 669 – – serum ethanol level 665 – – skin necrosis 666 – – surgical specimen 667 – – swallowing pathway 660 – – Valsalva maneuver 660 – – volume of injected ethanol 664 ventricular – afterload 194 – hemorrhage 215 – preload 193 – shunting 68, 154, 158, 200 – – intracranial hypertension 160 ventriculocortical gradient 67 ventriculostomy 157 venular occlusion 457

Subject Index for Volume 3 vertebro-vertebral arteriovenous fistula – congestive heart failure 702 – balloon 706 – C1-C2 707 – embolization via opposite vertebral artery 707 – epidural drainage 709 – hemorrhagic complication 703 – lower cervical 708

– neonates 705 – SAH 706 VGAD, see vein of Galen aneurysmal dilatation VGAM, see vein of Galen aneurysmal malformation villi 65 vincristine 604 viral – infection 807 – meningitis 23, 811, 870

979

Virchow Robin space 23, 59 VVAF, see vertebro-vertebral arteriovenous fistula W white matter calcification 165 Wyburn-Mason syndrome 39, 359