Microneurosurgery: volume 3A

Microneurosurgery In 4 Volumes M. G. Ya§argil Collaborators: P. J. Teddy and A. Valavanis Contributors: bL M. Duverno...

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Microneurosurgery In 4 Volumes

M. G. Ya§argil Collaborators: P. J. Teddy and A. Valavanis

Contributors: bL M. Duvernoy, H. M. Keller, St. Kubik, M. Marin-Padilla Illustrated by R Roth

III

A AVM of the Brain, History, Embryology, X J L Pathological Considerations, Hemodynamics, Diagnostic Studies, Microsurgical Anatomy

Geotg Thieme Verlag ТЫете Medical Publishers, Inc, Stuttgart • New York New York

PIONEERS OF MEDICINE

Harvey 1578-1657

Marcello Malpighi 1628-1694: "Omne vivum ex ovo"

Thomas Willis 1622-1675

Rudolf Virchow 1821-1902: "Omnis cellula e cellula"

Microneurosurgery in 4 Volumes

M.G.Ya§argil I Microsurgical Anatomy of the Basal Cisterns and Vessels of the Brain, Diagnostic Studies, General Operative Techniques and Pathological Considerations of the Intracranial Aneurysms II Clinical Considerations, Surgery of the Intracranial Aneurysms and Results

III A AVM of the Brain, History, Embryology, Pathological Considerations, Hemodynamics, Diagnostic Studies, Microsurgical Anatomy

III В AVM of the Brain, Clinical Considerations, General and Special Operative Techniques, Surgical Results, Nonoperated Cases, Cavernous and Venous Angiomas, Neuroanesthesia

IV Clinical Considerations and Microsurgery of the Tumors

Georg Thieme Verlag Thieme Medical Publishers, Inc. Stuttgart • New York New York

I

ТУТ Д

AVM of the Brain, History, Embryology, Pathological Considerations, Hemodynamics, Diagnostic Studies, Microsurgical Anatomy M. G. Ya§argil Collaborators: P.J.Teddy, A.Valavanis Contributors: H. M. Duvernoy, H. M. Keller, St.Kubik, M. Marin-Padilla Illustrated by P. Roth 242 partly colored Figures in 808 Illustrations, 34 Tables

1987 Georg Thieme Verlag Stuttgart • New York

Thieme Medical Publishers, Inc. New York

IV Addresses Yajargil, M. G., M.D., Professor and Chairman Neurosurgical Department University Hospital, Zurich

Teddy, P.J., DPhil, FRCS, Consultant Neurosurgeon The Department of Neurological Surgery Oxfordshire Health Authority The Radcliffe Infirmary, Oxford

Duvernoy, H.M., M.D., Professor Laboratoire d'Anatomie Universite de Besangon, Faculte de Medecine Besancon

Valavanis, A., M. D., Professor Department of Neuroradiology University Hospital, Zurich

Keller, H.M., M.D., Ph.D., Professor of Neurology Zurich

Roth, P., Scientific artist Neurosurgical Department University Hospital, Zurich

Kubik, St., M.D., Professor Institute of Anatomy University of Zurich Marin-Padilla, M., M.D., Professor Department of Pathology Dartmouth College Hanover, New Hampshire

Important Note: Medicine is an ever-changing science. Research and clinical experience are continually broadening our knowledge, in particular our knowledge of proper treatment and drug therapy.insofar as this book mentions any dosage or application, readers may rest assured that the authors, editors and publishers have made every effort to ensure that such references are strictly in accordance with the state of knowledge at the time of production of the book. Nevertheless, every user is requested to carefully examine the manufacturer's leaflets accompanying each drug to check on his own responsibility whether the dosage schedules recommended therein or the contraindications stated by the manufacturers differ from the statements made in the present book. Such examination is particularly important with drugs that are either rarely used or have been newly released on the market.

Some of the product names, patents and registered designs referred to in this book are in fact registered trademarks or proprietary names even though specific reference to this fact is not always made in the text. Therefore, the appearance of a name without designation as proprietary is not to be construed as a representation by the publisher that it is in the public domain. This book, including all parts thereof, is legally protected by copyright. Any use, exploitation or commercialization outside the narrow limits set by copyright legislation, without the publisher's consent, is illegal and liable to prosecution. This applies in particular to photostat reproduction, copying, mimeographing or duplication of any kind, translating, preparation of microfilms, and electronic data processing and storage.

© 1987 Georg Thieme Verlag, RudigerstraBe 14, D-7000 Stuttgart 30, Germany Thieme Medical Publishers, Inc., 381 Park Avenue South, New York, N.Y. 10016 Printed in Germany. Typesetting: R. Hurler, D-7311 Notzingen, typeset on Linotron 202; Printed by K. Grammlich, D-7401 Pliezhausen ISBN 3-13-645001-9 (Georg Thieme Verlag, Stuttgart) ISBN 0-86577-258-4 (Thieme Medical Publishers, Inc., New York) 1 2 3 4 5 6

I _____

V

I Acknowledgement

A number of colleagues assisted me in the preparation of this manuscript. To all of them I owe my most sincere thanks. The original groundwork on the section of central AVMs was prepared some time ago by Dr. St. C. Boone. The early work on cerebellar AVMs was done by Dr. R. M. Crowell. Dr. M. D. Lusk composed much of the work on hemodynamics of AVMs. Dr. R.D. Smith, New Orleans, reviewed and compiled the clinical material. Professor P. Kleihues reviewed the section on pathogenesis. Professor R. Meyermann contributed the section on histology and electron microscopic findings. Dr. H. G. Imhof reviewed the statistics regarding hemodynamics. Virtually the entire work was then reorganized and expanded. Many new ideas and concepts were introduced and older ones reevaluated in the light of more recent literature. The manuscripts were then redrafted. In doing this I was helped by my colleagues Professor A. Valavanis and Dr. P.J. Teddy, to whom I owe speciaHhanks. Dr. K. R. Smith, St. Louis, reviewed the manuscript during his visit to Zurich in summer 1986. Final careful review of the entire manuscript with

corrections and proofreading of the galley proofs were then done by Dr. G.F. Cravens, Dr. M.V. Reichman and Dr. M. V. Yancey. The anatomical pictures, figures, and the text were contributed by Professor St. Kubik. Mr. O. Reinhard and his co-workers (Department of Surgical Photography), produced the excellent photographic reproductions for the text. One of the most outstanding contributions to the whole series of these books has been that of Mr. P. Roth. He has done all of the drawings and diagrams and helped me meticulously in preparing the lay-out and the corrections. A very special thanks goes to both Mrs. M. Traber and Mrs. M. Jent who worked wonders with typing of the manuscript, verification of statistics and literature references, and deciphering illegible handwriting. Finally I would like to cordially thank Dr. h.c. G. Hauff, owner of Georg Thieme Verlag, and his staff, especially Mr. R. Zeller, for their help, cooperation and patience in the preparation of these volumes. M.G. Ya$argil

VI

Preface The operative treatment of vascular malformations using microsurgical techniques began in Zurich in January 1967. During the next 20 years, 414 patients with AVM of the brain and 71 with spinal AVM have been treated surgically. In the same time period 86 patients with cerebral AVM were discharged from our department without operation: In 40 cases the AVMs were operable but the patients refused surgery; in 24 cases the risk of neurological deficits delayed the decision for operative intervention until a later time; in 22 cases (22/500 = 4.4%) the lesion was deemed inoperable. The present volumes III A-III В are intended to relate and analyze our experience gained in the evaluation of 414 operated and 86 nonoperated patients with intracranial AVMs, to review what has been accomplished before and since the advent of microsurgical techniques and to identify the problems remaining in the treatment of these often difficult lesions. Other operated intracranial vascular lesions such as cavernomas (22 cases) and venous angiomas (5 cases) of the brain are also covered briefly. Interventional neuroradiological and surgical procedures for the treatment of cranial dural, spinal dural and medullary AVMs, and

of carotid-cavernous fistulae are not included and will form separate subsequent monographs. The third volume, part A, contains: History, embryology, pathological considerations, hemodynamics, Doppler-techniques, neuroradiology, neurosurgical anatomy, microcirculation, anatomy of the calcarine sulcus. The third volume, part B, contains: General operative techniques, the specific treatment and results of surgery for AVMs of specific locations like convexial (frontal, temporal, insular, parietal, occipital and cerebellar) and deep central (limbic system, corpus callosum, striocapsulothalamic, mesodiencephalic, vein of Galen, splenial, plexal, pontine), special and general statistics regarding morbidity and mortality, complications, the follow-up of nonoperated cases, and a chapter concerning the cavernous and venous angiomas and finally a chapter on neuroanesthesia technique, as utilized in Zurich. M. G. Ya$argil

Introduction This volume attempts to provide the basis for an informed approach toward operating upon AVMs and for learning the actual operative techniques favoured by the authors. It is not meant to be a comprehensive review of all that has been written in the past upon the subject. While much of the material is based upon the findings and theories of others, some is also new. Historically, the development of new surgical disciplines has usually created a need for ever more detailed study of the embryology, anatomy, physiology and anesthesia relevant to that field. The particular needs of the surgeon have often stimulated new methods of carrying out these studies. Neurosurgery has been no exception. Initially, there was the need for a general understanding of the gross anatomy and the relationships and physiology of fiber tracts, cranial nerves and cortical structures, which would allow the surgeon to operate with relative safety within the limits imposed by the instrumentation, anesthesia, and illumination available at that particular time. Cerebral angiography has been a real "breakthrough", not only for diagnostic purposes but also for a better understanding of the hemodynamic and therefore the functional anatomy of the central nervous system. Neuroradiological anatomy, with entirely new perspectives was born and stimulated the neurosurgeon to expand his surgical activities. Refined angiography has permitted accurate study of vessels within the living brain, complementing the work of the pure anatomist. Selective and superselective angiographic techniques have been created as well as interventional neuroradiology. Endovascular neurosur-gery was nothing more than the logical consequence of this accelerated development that has occurred within the last 20 years. Again the perspective concerning the anatomy of the central nervous system has been broadened. The introduction of stereotactic techniques has led to the development of precise atlases of deep areas within the brain (Szikla et al. 1977) and now to computerized three dimensional maps of some

of these structures (Salamon and Huang 1980, Unsold et al. 1982)._________________ I At the same time, microtechniques were introduced into neurosurgery. The ability to reach areas, previously deemed inaccessible, with comparative safety, has dictated the need for a new perspective of the microanatomical and topographical relationship of almost every part of the cranial contents. The work of Basset (1952), Huang (1946-1985), Stephens and Stilwell (1969), Duvernoy (1969-1983), Waddington (1974), Newton and Potts (1974), Williams and Warwick (1975), Lang (1981), Seeger (1978,1980, 1984), has given us, in large part, the necessary topographical details. The elegant series of studies by Rhoton and his associates (1976-1985) describe precise microsurgical details of various brain areas, with their corresponding vasculature, from the point of view of the neurosurgeon. These neuroanatomical publications offer, besides profound and scientifically proven knowledge, very detailed geometrical, trigonometrical-arithmetical data concerning lengths and diameters of various bony, nervous and vascular structures, as well as distances between them. These painstaking precise elaborations are essential background information, indispensable for every neurosurgical procedure. These major works, dealing with the brain stem vasculature comprise a precise review of the neurosurgical anatomy of the base of the brain, brain stem and circle of Willis. Our own account of the basal cisterns and circle of Willis has been described in Volume I. ___ __ Unlike the great majority of aneurysms, arteriovenous malformations and cerebral tumors are not confined to the basal regions of the brain. A new perspective must therefore be adopted, namely the awareness that even the deepest structures may often be reached by working carefully within the sulci and fissures of the brain. The basic patterns of these important anatomical structures should now be studied. Detailed accounts of sulcal and fissural anatomy are rare and generally incomplete but neurosurgery would certainly, benefit from more precise studies in the future.

Introduction Introduction

For this reason it seemed necessary to study, analyze and present the brain anatomy in a new concept, from the view point of the sulcal and fissural systems as well as their relation to the vessels. Originally we planned to study the detailed anatomy of these systems in collaboration with Professor Kubik of Zurich, and to include these results in the present publication. This undertaking, however, turned out to be much more time-consuming than originally estimated. The sulcal system showed an amazing degree of variation giving the impression of being a highly irregular system. As this study proceeded, however, it was realized that this irregularity of the sulcal system conforms to certain general principles. Despite the fascinating preliminary observations, we finally decided not to further delay the publication of this volume and to include here only the detailed anatomy of the calcarine sulcus and its variations and to present some representative displays of general sulcal anatomy. From this contribution by Professor Kubik, the reader will certainly become aware of the fascinating world of j sulci. This interesting work will be continued and ' published later. ' Although knowledge of sulcal and fissural anatomy is extremely important for angioma and tumor surgery, an equally detailed knowledge of microvascular anatomy is essential in order to perfect microsurgical techniques. Only with this knowledge can the neurosurgeon fulfil his goal, which is to preserve and protect the brain parenchyma adjacent to the lesion. Since the pioneering work of Heubner (1872) and Duret (1873) on cerebral microvascularization and microcirculation, subsequent generations of anatomists further refined and extended their original concepts. Stimulated by the recent, excellent work of Duvernoy et al. of Besancon, France, we invited Professor Duvernoy to provide a concise chapter on cerebral microvascularization in order to stimulate younger colleagues to pursue the endeavours of modern anatomists. We have been fortunate to have Professor Marin-Padilla of Hanover/New Hampshire, USA, who has contributed a concise chapter on the embryology of brain vessels, also summarizing the history in this field and adding his new ideas regarding the possible formation of cerebral vascular malformations. The development and maldevelopment of the cerebral venous system was intentionally not included in this volume, since this has been comprehensively described by Huang et al. as recently as 1984. As we already noted in the first volume on aneurysms, the detailed anatomy of an AVM can

References p. 369

only be completely and definitely evaluated at microsurgical exploration and not by any imaging technique. Although superselective angiography provides essential information regarding the composition of an AVM, we would like to have even more sophisticated angiographic techniques for even more precise study of the vascular composition and the hemodynamics of the AVM nidus and its compartments; this is already practiced daily by interventional neuroradiologists for vascular lesions of the skull base as well as head and neck. Professor Valavanis of Zurich, who performed all pre- and postoperative neuroradiological procedures since 1978, has been invited to provide the chapter on the neuroradiological evaluation of cerebral vascular malformations, also summarizing the relative role of CT, MRI and angiography. We refused to perform invasive studies to assess the hemodynamics of AVMs in our patients. However, we routinely applied non-invasive Doppler-ultrasound pre- and postoperatively. Professor Keller of Zurich, has contributed a separate chapter on his Doppler-ultrasound technique, summarizing the principles and the results of this method. Modern neurosurgery is inherently dependant on the advances in neuroanesthetic techniques. During the last 20 years, five groups of anesthesiologists were involved in our daily work. The results achieved in the surgical management of intracranial AVMs were also possible thanks to the great effort of our neuroanesthesiologists, especially Drs. M. Curcic and Dr. M. Kis, who have been responsible for neuroanesthesia during the last 10 years. In Volume III В of this series, the surgical techniques and results as well as the neuroanesthetic technique will be presented in detail.

VII

Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgement

1 History. . . . . . . . . . . . . . . . . . . . . . . . . . . . A Short History of the Diagnosis and Treatment of Cerebral AVMs . . . . . . . . 3 Pre-17th Century . . . . . . . . . . . . . . . . . . . . 3 17th-19th Century . . . . . . . . . . . . . . . . . . . 3 Treatment of Extracranial AVM in Earlier and Present Time. . . . . . . . . . . . . . . . . . . . 5 Intracranial Angiomas . . . . . . . . . . . . . . . . 5 The Contributions of Virchow and his Contemporaries . . . . . . . . . . . . . 5 Early Clinical Observations on Intracranial AVMs . . . . . . . . . . . . . . . 6 Surgical Treatment of Cerebral AVMs (18891930) . . . . . . . . . . . . . . . . . . . . . 7

Neurosurgical Approaches Prior to the Introduction of Angiography (1928) . . . . . 9 Neurosurgical Treatment of Intracranial AVM Following the Introduction of Angiography (1930) . . . . . . . . . . . . . . 10 The Limitations of Surgery . . . . . . . . . . . 12 Conservative versus Surgical Treatment . . 14 luminary and Outlook . . . . . . . . . . . . . . . . diagnosis . . . . . . . . . . . . . . . . . . . . . . . . . iurgery . . . . . . . . . . . . . . . . . . . . . . . . . .

20 20 20

2 Embryology. . . . . . . . . . . . . . . . . . . . . . Miguel Marin-Padilla A. Embryogenesis of the Early Vascularization of the Central Nervous System . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction . . . . . . . . . . . . . . . . . . . . . . . Perineural Vascular Territory of the CNS Vasculature . . . . . . . . . . . . . . . Interneural Vascular Territory of the CNS Vasculature . . . . . . . . . . . . . . . Composition and Organization of the Pial Vascular Plexus . . . . . . . . . . . . . . . . Vascular Perforation of the CNS Surface by Pial Vessels . . . . . . . . . . . . . . . . . . . . Vascular Approach and Contact with the CNS Surface. . . . . . . . . . . . . . . . . . . Endothelial Filopodia Perforation of CNS Surface . . . . . . . . . . . . . . . . . . .

23 23

24 31

In Situ Formation of New Intraneural Vessels . . . . . . . . . . . . . . . . . . . . . . . . . 37 Establishment of the VRC and Interneural Vascular Territory . . . . . . . . . . . . . . . . . 37 Intraneural Vascular Territory of the CNS Vasculature . . . . . . . . . . . . . . . 39 Conclusions . . . . . . . . . . . . . . . . . . . . . . . 44

31

В Vascular Malformation of the Central Nervous System. Embryological Considerations

32

Capillary Telangiectasias and Cavernous Angiomas Venous and Arteriovenous Malformations . . 46 Sturge-Weber-Dimitri's Disease . . . . . . . . . 47

32 32

VIII

Contents

3 Pathological Considerations. . . . . . .

49 Enlargement, Growth, and Regrowth of AVMs. . . . . . . . . . . . . . . . . . . . . . . . . .

Pathogenesis . . . . . . . . . . . . . . . . . . . . . . . Classification of Vascular Malformation

Nomenclature . . . . . . . . . . . . . . . . . . . . . . Classification . . . . . . . . . . . . . . . . . . . . . . The Author's Classification . . . . . . . . . . .

58 61

Location of AVMs . . . . . . . . . . . . . . . . . . . 63 Localization . . . . . . . . . . . . . . . . . . . . . . . 63 Localization of the AVM Within the Brain . . 63 I. Surface Lesions (visible on exploration on the surface of the brain) . . . . . . . . 64 II. Deep Lesions (invisible at exploration on the surface) . . . . . . . . . . . . . . . . . 64

Compact and Diffuse Lesions . . . . . . . . . . .

Enlargement . . . . . . . . . . . . . . . . . . . . . . . 140 Growth . . . . . . . . . . . . . . . . . . . . . . . . . . 146 Pseudo-Growth . . . . . . . . . . . . . . . . . . . 146 True Growth of the AVM . . . . . . . . . . . . 155 Spontaneous Thrombosis and Regression of AVMs.. . . . . . . . . . . . . . . . . . . . . . . . .

161

Multiple AVMs . . . . . . . . . . . . . . . . . . . . . 165 Multiple Cerebral AVMs . . . . . . . . . . . . . . 165 Intracranial and Intraspinal AVMs. . . . . . . . 182 Association of Persistent Trigeminal Artery and AVM . . . . . . . . . . . . . . . . . . . . . . . . .

The Nidus. . . . . . . . . . . . . . . . . . . . . . . . . The Concept of Compartments . . . . . . . . . .

138

74 76

Association of Persistent Trigeminal Artery and AVM . . . . . .

182

Sizes, Shapes, and Elements of AVMs . . . . . 85 Sizes of AVM. . . . . . . . . . . . . . . . . . . . . . 85 Shape. . . . . . . . . . . . . . . . . . . . . . . . . . . . 92 Pure Fistulous AVM . . . . . . . . . . . . . . . . 100 Elements of an AVM . . . . . . . . . . . . . . . . . Ill Arterial Feeders. . . . . . . . . . . . . . . . . . . Ill Venous Drainage . . . . . . . . . . . . . . . . . . 118 Sinuses . . . . . . . . . . . . . . . . . . . . . . . . . 138

Intracranial AVM with Stenosis and Occlusion of Major Vessels . . . . . . . . . . 190 Arterial . . . . . . . . . . . . . . . . . . . . . . . . . . 190 Moya-Moya Disease . . . . . . . . . . . . . . . . . 192 Venous . . . . . . . . . . . . . . . . . . . . . . . AVM Associated with Other Pathological Entities Tumors . . . . . . . . . . . . . . . . . . . . . . . . . . 211

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

213

Autoregulation . . . . . . . . . . . . . . . . . . . . . 220

4 Hemodynamics. . . . . . . . . . . . . . . . . . . . 214

Normal Perfusion Pressure Breakthrough . . 221

The Physics of Fluids and Blood Flow . . . . . Pressure, Flow, and Resistance . . . . . . . . . . The Nature of Blood . . . . . . . . . . . . . . . . . Laminar versus Turbulent Flow . . . . . . . . . . Tortuosity of Vessels . . . . . . . . . . . . . . . . . Vascular Distensibility . . . . . . . . . . . . . . . .

214 214 215 215 216 216

Comments on the Normal Perfusion Pressure Breakthrough Theory . . . . . . . . . . . . . . . . 222 Effects of AVMs upon Cerebral Function . . . 227

Cerebral Circulation: Functional Anatomy of the Cerebral Circulation . . . . . . . . . . . . . . . . . . . . . . . .

217

Systemic Effects. . . . . . . . . . . . . . . . . . . . 235

Neuronal Innervation. . . . . . . . . . . . . . . . . Microcirculation . . . . . . . . . . . . . . . . . . . .

217 218

Operative Considerations with Regard to Hemodynamics . . . . . . . . . . . . . . . . . . . 237

AVM Structure. . . . . . . . . . . . . . . . . . . . .

218

Enlargement of AVMs . . . . . . . . . . . . . . . .

218

Preoperative Evaluation. . . . . . . . . . . . . . . 237 Operative Techniques . . . . . . . . . . . . . . . . 237 Postoperative Care . . . . . . . . . . . . . . . . . . 239

Local Mass Effect . . . . . . . . . . . . . . . . . . . 227 Obstruction . . . . . . . . . . . . . . . . . . . . . . . 227 Hemorrhage . . . . . . . . . . . . . . . . . . . . . . . 227 Vascular Steal . . . . . . . . . . . . . . . . . . . . . . 228

Contents

IX

5 Diagnosis and Follow-up of Patients with Cerebral AVM using Doppler Ultrasound

I

Herbert M. Keller

6 Neuroradiological Evaluation A. Valavanis Computed Tomography . . . . . . . . . . . . . . .

250

Magnetic Resonance Imaging (MRI) . . . . . .

259

Cerebral Angiography . . . . . . . . . . . . . . . .

260

Technique . . . . . . . . . . . . . . . . . . . . . . . . Erroneous Findings . . . . . . . . . . . . . . . . . . Angiographic Classification . . . . . . . . . . . . Angiographic Investigation. . . . . . . . . . . . .

260 260 267 269

Limitations of Conventional Selective Angiography . . . . . . . . . . . . . . . . . . . . . . . 276 Venous Phase . . . . . . . . . . . . . . . . . . . . . . 280 Associated Aneurysms . . . . . . . . . . . . . . . . 280 Spasm . . . . . . . . . . . . . . . . . . . . . . . . . . . 280 Summary . . . . . . . . . . . . . . . . . . . . . . . . . 283

284 The Collateral Circulation. . . . . . . . . . . . . 333

7Microsurgical Anatomy of the Brain Supratentorial Sulci and Fissures Fissures . . . . . . . . . . . . . . . . . . . . . . . . . . 296

Interhemispheric (Longitudinal) Fissure . . . . Sylvian Fissure . . . . . . . . . . . . . . . . . . . . . Transverse Fissure . . . . . . . . . . . . . . . . . . .

296 298 301

Vascular Patterns Relating to Supratentorial Sulci

Infratentorial Sulci and Fissures . . . . . . . . . 312 Organization of the Cerebral Microcirculation The Venous System of the Brain . . . . . . . . . 327

I Extracranial Arterial Circle . . . . . . . . . . . II Dural Arterial Circle . . . . . . . . . . . . . . . III Basal Cerebral Arterial Circle of Willis .. IV Cortical Interhemispherical and Intrahemispherical Arterial Circle . . . . . V Cerebellar Arterial Circle . . . . . . . . . . . . VI Transcranial Arterial Circle . . . . . . . . . . VII Spinal Arterial Circle . . . . . . . . . . . . . . VIII Vertebrocervical Arterial Circle . . . . . . IX Primitive Arterial Circle . . . . . . . . . . . .

334 334 334 334 334 334 336 336 336

Pathology of Collateral System . . . . . . . . . . 337

The Veins of Posterior Fossa. . . . . . . . . . . . 332

8 Cortical Blood Vessels of the Human Brain H. M. Duvernoy Blood Vessels of the Cerebral Cortex. . . . . . I Pial Vessels . . . . . . . . . . . . . . . . . . . . . . The Pial Arterial Network . . . . . . . . . . . . The Pial Venous Network . . . . . . . . . . . . Pial Vessels: Discussion . . . . . . . . . . . . . .

338 338 338 339 340

Intracortical Vessels. . . . . . . . . . . . . . Blood Vessels of the Cerebellar Cortex . . . . 345

I Pial Vessels . . . . . . . . . . . . . . . . . . . . . . . . II Intracortical Vessels . . . . . . . . . . . . . . . .

345 347

Contents

9 Anatomy of the Calcarine Sulcus 5. Kubik and B. Szarvas Development . . . . . . . . . . . . . . . . . . . . . . 351 Nomenclature of the Various Parts of the Calcarine Sulcus . . . . . . . . . . . . . . . . 351 The Location of the Meeting Point . . . . . . . 352 Anatomical Variations of the Pars Posterior . 352

Pars Anterior of the Calcarine Sulcus. . . . . . Variations in Course . . . . . . . . . . . . . . . . . Connections and Side-Branches . . . . . . . . .

356 357 357

Inner Structure of the Sulcus Calcarinus . . . 357

Measurements. . . . . . . . . . . . . . . . . . . . . . 366 The Relationship Between the Sulcus Calcarinus

Variations in the Terminal Part of the Pars Posterior and the Calcar Avis, Posterior Horn and Optic . . . . . . . . . . . . . . . . . . . . . . . . . 352 Radiation . . . . . . . . . . . . . 366 Side-Branches and Connections . . . . . . . . . 355 References

.......................

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1

History

A Short History of the Diagnosis and Treatment of Cerebral AVMs As attested by F. Henschen (1955) angiomatous malformations and tumors have been, since Virchow's time, a "problem child" of pathologists. Hamby (1958) defined the main problems posed in understanding the pathology of these lesions and his statements are valid even today: "The origin and anatomy of the cerebral angiomas has frustrated pathologists over the years as much as their treatment has baffled surgeons. An extensive literature has developed, replete wjthj3ictur-esque nomenclature based upon attempts to describe the appearance of lesions seen at the operative table or at necropsy. The surgical descriptions are not entirely basic nor accurate because the bulk of the lesion is largely submerged under the cortex and hence invisible to the examiner. The pathologic descriptions have been faulty because of deflation of the lesion at the time of examination by lack of the expansile blood stream that characterizes them in life. Also confusing the picture of the dead lesion are the alterations produced in the component vessels by blood under arterial pressure, which dilates veins and "arterializes" them to withstand the added stress. Vascular resistance being lowered by the shunt, arteries dilate to carry more blood under less than usual pressure, and lose some of their usual characteristics." However, the introduction of cerebral angiography (Moniz 1927) together with the continuing improvements in the quality of angiograms and the remarkable developments in vascular catheterization techniques (Seldinger 1953, Djindjian 1962) has opened up new dimensions in the study of the morphological and hemodynamic aspects of AVMs. This short historical review may help to understand how we have arrived at the present day

interpretations of AVM pathology and development and how modes of treatment have evolved.

Pre-17th Century Descriptions of vascular malformations of the skin and other visible organs such as eye, lips and ear with occasional comments about their often ugly appearance and the difficulty or impossibility of treatment may be seen in some of the earliest recorded historical manuscripts. The Papyrus Ebers (ca. 1500 ВС) contained descriptions of hemorrhoids, skin tumors, hydro-celes, varicose veins and aneurysms. Kharadly (1956) showed that hernias and aneurysms were operated upon even in those times but not AVMs. The warning, "You must keep your hands off — Noli me tangere" is stated in the relevant chapter Г" Virchow cited prominent physicians like Hippokrates, Galen, Celsus, Aetius, Avicenna, and Vidus Vidius, who were dealing with the diagnosis and treatment of different types of external vascular malformations. Von Bramann (1886) showed that Galen and Delia Groce knew of varicose pulsating swellings and took them to be simple arterial aneurysms. Osier (1915) noted that references to vascular malformations are to be found in the works of Antyllus (2nd Century) and Abulcasis (10th Century).

17th-19th Century The great breakthroughs in the understanding of the systemic circulation and of the cerebral circulation were made by Harvey (1628) and Willis (1664) respectively.

4

References p. 369

1. History

William Hunter ( 17 1 8 - 1 7 8 3) (By kind permission of the President and Council of the Royal College of Surgeons of England)

John Hunter (1728-1793)

The work of Harvey and Willis was subsequently complemented by the discovery of the capillary system by Malpighi (1661) and this paved the way for modern theories regarding the evolution and pathology of AVMs. In the following century (1757) William Hunter was able to identify the clinical characteristics and some hemodynamic aspects of extracranial AVMs. In "Observations on arteriovenous malformation, London Medical Observations and Enquiries, 1762" he wrote: "Vascular malformations of the extremities are caused by an abnormal communication between arteries and veins." Enthusiastic phlebotomists of that period prepared two perfect examples of arteriovenous aneurysm for W. Hunter, which he was quick to recognize (cit. Dandy 1928); at the point of communication between the artery and the vein, he recognized a loud hissing bruit and a strong tremulous thrill: large~tortuous sacs were seen to pulsate; the brachial artery was greatly enlarged and serpentine cephalad to the arteriovenous fistula, but distal to it, the artery became smaller than on the other side. He was able to reduce the size of the vein, stop their pulsation and eliminate both the bruit and the thrill by pressing on a localized spot, which he recognized to be the opening between the artery and vein. It was William Hunter who first suggested the term "anastomosis" to denote the union of the two vessels, whereas the term "collateral" was introduced by his

younger brother John Hunter who also ligated the femoral artery in a case with popliteal aneurysm and proved the efficiency of the collateral arterial system. The broad scientific approach concerning the nature of these impressive aberrations began with pathologists and surgeons 200 years ago who described them as '^erectile tumors" and swellings of the skin and organs. The advent of medical journals enabled the scientists to publish their observations. After 1850 the number of publications concerning these erectile tumors increased rapidly. Between the time of William Hunter (1762) and Sonntag (1919), 65 such publications are to be found: Plenck (1776), Bell (1796), Cruveilhier (1816), Meckel (1818), Dupuytren (1834), Vidal (1846), Rokitansky (1846), Virchow (1851), Gerdy (1852), Schuh (1853, 1866), Busch (1854), Luschka (1854), Esmarch (1854), Lebert (1857), Bennet (1854), and Alibert (1871). More detailed information regarding these papers may be found in the works of Heine (1869), Weber (1869), Korte (1880) and Heineke (1882). Pathological classification based upon varied anatomical descriptions was already becoming clumsy and confusing. By 1894 Wagner had collected from the current literature 24 different nomenclatures. In parallel with changing pathological concepts, the surgery of extracranial AVMs was undergoing a gradual evolution.

References p. 369

Treatment of Extracranial AVM in Earlier and Present Time The endeavours of general surgeons in dealing with the dangerous and disfiguring extracranial vascular malformations (scalp, external ear, eyelids, orbits, cheeks, lips, tongue, palate and neck) are most informative for the interested neurosurgeon (Beck, Berger, Billroth, Brodie, von Bruns, Bryant, Busch, Caradec, Clairmont, Dalrvmple, Dupuytren, Emanuel, Enderlen, German. Goldmann, Heineke, Krause, Lefort, Lieb-kin. Nelaton, Pilz, Roth, Russell, Schwalbe, Schwartz). Their methods of treatment have, in the past, included: 1) Injection of the lesion with: ferrous chloride, glycerin, tannin, chlorzin, carbonic acid, alcohol, I Electrocauterization, 5' Ligation, 4) Extirpation. The variety of modern therapy of external vascular malformations (Williams 1983) shows that therapeutic difficulties still remain in the treatment of these easily approachable lesions: 1) Corticotherapy (new born children), 2) Radiotherapy, 3) Electrocoagulation, -i) Cryotherapy, 5) Surgery, h i Use of laser beam, ~i Embolization. As in neurosurgery, the advice of most plastic surgeons is that simple ligation of feeding vessels is inadequate and inadvisable.

Intracranial Angiomas The Contributions of Virchow and his Contemporaries After exhaustive research work on cavernomas of the liver, Rokitansky (1842-46) came to the conclusion that these were eitherjDenign or malignant tumors independent of the surrounding vascular system. Volume 6 of Virchow's Archive (1854) contains 3 remarkable papers: Esmarch (pp. 34-57): "Uber cavernose Blutgeschwulste", Luschka (pp. 458-470): "Cavernose Blutgeschwulste des Gehirns" and Virchow (pp. 526-554): Uber cavernose (erectile) Geschwulste und Teleangiektasien." Esmarch und Luschka fully supported the neoplasia hypothesis of Rpki-I tansky.

Intracranial Angiomas

Luschka provided one of the earliest descriptions of an intracranial arteriovenous anomaly in a patient with a frontal cavernoma. Luschka recognized two types of "Blut-Geschwulste": 1) Telangiectases (non neoplastic) arising due to a metamorphosis of capillary systems. 2) Cavernous tumors (neoplastic) containing large blood-filled compartments. The young Virchow, who was involved with research into infection of blood vessels, also published (1851) a remarkable paper concerning "the dilatation of small vessels". In this paper he described and discussed thoroughly his own observations and thoughts and clearly refuted the hypothesis of Rokitansky. In 1863 Virchow published a comprehensive study which may be called the first real milestone in the history of the AVM. In the 3rd volume of his monograph, 200 pages (pp. 306-496) are devoted to the phenomenon of the physiological and pathological changes of blood vessels in all organs. His descriptions profoundly contradicted contemporary opinion. He described telangiectases, venous, arterial, arteriovenous and cystic angiomas (nowadays angioblas-tomas), and their transitional types, and discussed in detail the pathogenesis of these malformations. He reflected on the atlas of Cruveilhier and the pioneering work of John Bell (The Principle of Surgery, London 1826, Volume 3, pp. 326-383, First Edition, London 1796). Bell described cavernoma, AVM and angioblastoma but gave all of them the nomenclature of "Aneurysm per Anastomosis". Virchow said: "This description is still perfectly valid, (p. 328): Aneurysm per anastomosis is an entire change of structure; it is a dilatation of veins, in which they are forced and enlarged by the diseased action of their corresponding arteries. Those happen in consequence of original malformation, a violent action of arteries, and a mutual enlargement of arteries and veins, while the intermediate substance of the part is slowly distended into large intermediate cells, which are dilated to formidable reservoirs of blood. — The blood is poured into the cells of such a tumor by innumerable arteries: from these the blood is continually following into veins, which receive it with such patent orifices etc. The veins form a conspicious part of such a tumor, but the intermediate cells are an appreciable part of the structure. . . (p. 397). All this proves that it is a tissue of small arteries and veins; it fills not like a varix slowly; its filling is by distinct thrombs; it is filled by its small and numerous arteries, and its swelling is (like the erection of the penis) produced by the pulsation of

1. History

the arteries, stroke after stroke, pouring out their blood into cells." "The tumor is ajxmgeries of active vessels and the cellular substance through which these vessels are expanded, resembles the cellular parts of the penis, the_gills of a turkey cock or the substance of the placenta, spleen worms." It is interesting to speculate as to whether Bell was describing a cavernoma or an AVM. It certainly jspunds like the modern description of an AVM and its nidus. Virchow (1854), cited Gerdy (1852), who differentiated eight types of "erectile tumors" and noted the great number of publications concerning the "erectile tumors" and the difficulties with their classification. He preferred the term of "angioma" which was introduced by J. Hughes Bennet (1854) instead of the term of "angionoma" which was advocated by Follin (1861). He credited to Plenck (1776) the term "cavernoma", a nomenclature well recognized in the German literature (Meckel 1818). Gushing and Bailey (1928) concluded, quite wrongly, that Virchow believed in the neoplastic nature of vascular malformations as proposed by Rokitansky. This error was most likely due to difficulties with translation of'the original papers. Virchow (1863) divided angiomas into cavernous, simple telangiectatic, racemose, and lymphatic types. Racemose angiomas were divided further into arterial and venous types. Page 474 of Virchow's 3rd Volume (1863) relates to a case of a large extracranial parietooccipital AVM in a man from Florence and described by Vidus Vidius in 1665. Virchow commented that this type of malformation originates through accommodation between artery and vein with consequent dilatation of them (arteriectasie and phleb-ectasie, p. 471). They are of congenital origin (p. 475). They may grow or spontaneously regress (p. 482). The following nomenclature has been used: aneurysma per anastomosis (Bell) or aneurysma anastomoseon (v. Walther), aneurysma per transfusionem (Dupuytren 1834) and other authors used the term of aneurysma arteriovenosum, or aneurysma varicosum. Virchow argued (p. 472) that aneurysms would not arise as a result of arteriovenous communication in traumatic cases, therefore the best term would be aneurysma spurium arterio-venosum. Virchow's main concern was not so much nomenclature as the pathophysiology of the lesions. The founder of cellular pathology had a profound interest in pathophysiology. He performed injection studies on the pregnant uterus and placenta and was fascinated by the temporary but enor-

References p. 369

mous increase in capacity of vessels during _gestation. In 1851 he spoke of "The physiologic paradigm in the corpora cavernosa of sex organs and the paradigm of pathology in cavernoma and telangiectasis", and further questioned as to whether one type of angioma can transform into another by changes in flow and pressure or by cellular proliferation.

Early Clinical Observations on Intracranial AVMs Pfannenstiel (1887) and Kaufmann (1897) observed young (22 and 23 years) primipara patients, who died with acute cerebral symptoms. Autopsy study showed a ruptured varicose anomaly of left thalamus opticus and the vena Galeni in one case, and a ruptured varicose anterior callosal anomaly in another. D'Arcy Power (1888) found, a large AVM in the left sylvian fissure at autopsy on a 20-year-old man who had suffered a hemiplegic stroke and died. Steinheil (1894) described the history and pathologicoanatomical findings in a patient (59 years) with a large right frontal AVM which drained partially to the vein of Galen. He may thus be credited as being among the earliest to describe the symptomatology of the disease. Rizzoli 1873 observed a right occipital pulsating swelling in a 9year-old girl. The pulsation disappeared on compression of the left occipital artery. The girl died from an apparent meningitis (perhaps, in fact, from an intracranial hemorrhage). At autopsy she was found to have an AVM of the occipital region (-duralpial) with drainage to the transverse sinus. There was a defect in the occipital region of the skull so that the pulsation in the AVM could be felt externally. The first clinical diagnosis of a cerebral AVM was made by Hoffmann (1898). Isenschmid followed the history of this patient, who was presented to medical colleagues in Heidelberg, and discussed the differential diagnoses (1912). He pointed out that the clinical diagnosis of cerebral angiomas had never before been made. With the onset of operations for brain tumors around 1890, the number of cases of AVM observed clinically, pathologically and surgically began to rise sharply. At that time, contralateral parietal craniotomy for cases of Jacksonian epilepsy occasionally produced an unexpected AVM. Between 1890 and 1936 there were more than 90 reports of around 120 cases of cerebral AVMs. In the cases of Rizzoli (1873), Hoffmann (1898), Isenschmid (1912), Haenel (1926), Eimer and Mehlhose (1927) and in some of the cases of

References p. 369

Dandy (1928) and Cushing and Bailey (1928) the diagnosis was made clinically. The list of authors who published cases of AVM prior to the angiographic era includes: Morris (1871), Rizzoli2 (1873), von Braman (1886), Pfannenstiel (1887), D'Arcy Power (1888), Giordano1 (1890), Guldenarm and Winkler1 (1891), Pean1 (1891), Starr and McCosh1 (1894), Steinheil (1895), LucasChampionniere1 11896), Kaufmann (1897), Emanuel (1898), Hoff-mann2 (1898), Ribbert (1898), Beadles (1899), Shoyer (1900), Struppler (1900), von Bergmann1 (1901), Chipault1 (1902), Deetz (1902), Rotgans and Winkler1 (1902), Kreutz (1903), Bail (1904), Drysdale (1904), Heitmuller (1904), Simmonds (1905), Strominger (1905), Sternberg (1905, 1907), Falk (1906), Lavillette1 (1906), Diirck (1907), Enders (1908), Krause1 1908), Stertzing (1908), Leischner1 (1909), Ranzel (1909), Tuffier1 (1909), Blank (1910), Therman (1910-13), Znojemsky1 (1910), Abrikosoff (1911), Astwazaturoff (1911), Cassirer and Miihsam1 (1911), Isenschmid2 (1912), Schmolck (1912), Wichern (1912), von Eiselsberg and Ranzi1 (1913), Kaiserling (1913), Wischnewski (1913), Castex and Bolo (1914), Leunenschloss (1914), Maklakow1 (1914), Orbison1 (1915), Verse (1918), Bort (1920), Castex and Romano (1920), Schmidt (1920), Bannister (1921), Hammes (1921), Magnus1 (1921), Nonne1 (1921), Campbell and Ballance1 (1922), Deist (1922), Worster-Drought and Ballance (1922), Miiller (1923), Wohak (1923), Elkin (1924), von Lehoczky (1924), Miihsam1 (1924), Rienhoff (1924), Esser (1925), Federoff and Bogorad (1925), Klimesch (1925), Laves1 (1925), Marx (1925), Reid (1925), Dowling (1926), Glo-bus and Strauss (1926), Haenel2 (1926), Klimesch (1926), Leeser (1926), Bregman (1927), Eimer and Melhose (1927), Herzog (1927), Olivecrona and Lysholm1 (1927), Perthes1 (1927), Worster-Drought and Dickson (1927), Buckley (1928), Cushing and Bailey1'2 (1928), Dandy1 (1928), Ruehl (1929), Yates Paine Brockman1-2 (1930), Brock and Dyke (1932), Krug and Samuels (1932), Dimitri and Balado (1933), Levine (1933), Love (1933), Schaltenbrand (1938), Sattler (1939).

1

Diagnosis made at exploration Diagnosis made clinically rest: Diagnosis made at autopsy 2

Intracranial Angiomas

Surgical Treatment of Cerebral AVMs (1889-1930) Most of these early procedures were carried out by general surgeons (Table 1.1). Giordano is credited to have operated upon the first cerebral AVM in 1889. Regarding his original paper, however, it is clear that he simply ligated a pathological vessel on the left parietal surface and did not expose the remainder of the AVM located in the deep subcortical tissue.

Jules Emile Pean (1830-1898) (By kind permission of Prof. H. M. Koelbing, Director of the Institute of Medical History, University of Zurich)

The first complete excision of a cerebral AVM was made 98 years ago by the famous French surgeon Pean. He treated a 15-year-old boy who had suffered a left sided Jacksonian fit, and made a diagnosis of a right sided central tumor. The operation took place in May 1889 and was described thus by Pean: "Au cours de Г operation, nous nous trouvames en presence d'un angiome des meninges en communication avec les sinus longitudinal superieurs. Malgre sa richesse vasculaire, malgre son etendue, la tumeur put etre enlevee en totalite, sans perte de sang, grace au pincement temporaire et defini-tif des vaisseaux variqueux, dilates, erectiles, dont elle etait composee. A ce propos, nous avons recherche, dans la science les faits de ce genre, qui avaient ete publics et nous n'en avons trouve

8

References p. 369

1. History

aucun qui fut exactement semblable, aucun surtout qui cut ete opere." Pean's conclusion is optimistic: "— De meme qu'il existe des angiomes extracraniens communiquants a travers la voute du crane avec le sinus longitudinal superieur, il existe une variete d'angiomes intracraniens communicants egalement avec les sinus longitudinal

Table 1 . 1

superieurs, mais developpes dans 1'epaisseur des meninges et situes entierement a 1'interieure du crane. Les tumeurs sont justiciaries de la trepanation, 1'hemorrhagie et notamment celle due a la communication avec les sinus, et facilement arretee par le pincement temporaire et definitif."

General surgical operations for cerebral AVM

Pean Giordano 1889

Localization

Operation

Follow-up

R central L parietal

Extirpation Ligature of

good good

1889

vein

Guldenarm

1890

R parietal

Partial extirpation

no follow-up

Guldenarm

1891

R parietal dura-varix

Ligature Extirpation

good

Starr and McCosh

1894

L parietal small angioma

Extirpation

good

Lucas-Championniere

1896

R parietal

Extirpation

good

Rotgans et al.

1897

R parietal

Partial extirpation

good

Rotgans et al.

1898

L parietal

Ligature

good

Chipault

1897-1898

L parietal

3 operations, partial

no follow-up

Von Bergmann

1901

L frontoparietal

Ligature

death, hemorrhage

Lavillette

1906

R parietal

Ligature

no follow-up

Krause

1907

L parietal

Ligature

good

Von Eiselsberg and Ranzi

1907-1908

R parietal (2 cases)

Ligature

good

Leischner

1907

L central

Ligature

good

Tuffier

1909

L central

Ligature

good

Znojemsky

1910

Cerebellum

Exploration

death, hemorrhage

Cassirer and Muhsam

1910

R frontoparietal

Extirpation

good

Von Eiselsberg and Ranzi

1913

R paracentral

Ligature of vein

unchanged

Wischnewski

1913

R parietal

Ligature

good

Magnus

1914

L central

Exploration

x-ray, good

Maklakow and Minz

1914

Cerebellum

Exploration

death

Orbison et al.

1915

-

-

-

Nonne

1921

L parietal

Partial extirpation

good

Campbell and Ballance

1922

R parietal

Ligature 2 operations

hemiplegia

Laves

1922

L sylvian fissure

Ligature

death, hemorrhage

Perthes

1923

R parietal

Ligature

good

Yates and Paine

1930

V. Galeni

Exploration

death

Brock and Dyke

1932

R frontoparietal

Exploration

x-ray, good

The original descriptions of these impressive and dramatic attempts to remove cerebral AVMs make fascinating reading.

References p. 369

Neurosurgical Approaches Prior to the Introduction of Angiography (1928) Gushing (1909-1928) and Dandy (1921-1926) each described their operative experiences in 14 and 15 cases respectively, of venous and arteriovenous malformation and added cases from the literature. Both of their series were published in the same year (1928) and reading the original descriptions it seems likely that all their cases were true arteriovenous malformations. Dandy felt that the only way to cure an arteriovenous aneurysm was to ligate the entering arteries or to excise the whole vascular tumor. Earlier, he had lost one patient from hemorrhage during the operation and a second case from intracerebral hemorrhage following total extirpation and he wrote: "But the radical attempt at cure is attended by such supreme difficulties and is so exceedingly dangerous as to be contraindicated except in certain selected cases... As in most cerebral lesions, however, each case should be considered a law unto itself. There are large aneurysms and small ones; those which are mostly arterial, others mainly venous; some are superficial, others deep, some are in highly important areas of the brain, others in portions largely silent. All of these factors, and finally the patient's wishes in the matter, must be weighed. An aneurysm in the left cerebral hemisphere in a right handed person is surely noli me tangere under all conditions. Any attempted cure, even if successful, would almost surely result in disturbances of speech or motor power, or of both... there is more reason to attempt to cure a patient who has an arteriovenous aneurysm in the right hemisphere." Cushing's experience with operations for cerebral angiomas dated back to 1909. Some brief extracts from his excellent operative accounts follow: Case 1: A 39-year-old patient presented with raised intracranial pressure thought to be due to a cerebral neoplasm and was operated upon on 3.2.1909: "Left subtemporal decompression was made... The dura was not particularly tense. When opened a large thin-walled venous lake was disclosed, from which branches spread in various directions... It seemed unwise to attempt it." Case 2: A 4-year-old child with right sided congenital exophthalmos and bulging in the right temporal area; September 4, 1920: "When the dura was reflected there came into view a mass of hugely dilated vessels, evidently veins, which covered the entire temporal lobe. Two of the main vessels were ligated but extirpation was obviously impossible."

Intracranial Angiomas

Case 3: 30-year-old male, operated on March 18, 1921: "A left osteoplastic exploration was made. When the dura was opened an enormous tangle of dilated veins was disclosed spreading upward from about the region of the arm-center. The larger vessels were fully as big as the little finger. The chief emerging vein was ligated but all attempts to get beneath or between the larger vessels were accompanied by so much bleeding that their ligation or extirpation was deemed impossible." Case 4: "April 25, 1921: . . . On reflecting the dura an exceedingly wet brain was disclosed with two huge veins on the surface, one running largely in the sylvian fissure. The other, more vertical, lay in the precentral fissure... Since the operator felt some regrets at not having been more radical in his attacks upon the lesion in the preceding case, a ligature was first thrown around the large descending vein at the point. . . A second ligature was then put on, which must have started trouble from stasis in the main varix which became hardened and swollen... Finally bleeding began to occur from around the sides of the varix and a rupture seemed imminent. There was evidently only one thing to do - to catch the base of the protruding lesion with a large curved clip and to throw a ligature around the whole mass. This desperate step was taken and the cavity, which continued to bleed after the ligature was placed, was finally filled with a slab of muscle taken from the patient's leg, before the excessive venous hemorrhage could be controlled. There had been a sharp fall in blood pressure from which she finally recovered without transfusion. . . As was to be expected, the patient showed a postoperative right hemiplegia and aphasia... Nearly seven years since her operation, regards herself, aside from some remaining weakness of her right arm, as in normal health." Depressed following such an experience Gushing wrote: "One could hardly have chosen a worse place than over the lower motor area of the leading hemisphere in which to attempt the surgical removal of a racemose varix." The untoward results of the procedure in this case resulted in a more cautious attitude when a similar lesion was disclosed in the next patient (left postcentral region): "December 28, 1922: No attempt was made to treat the lesion by ligature or otherwise." Gushing reviewed the poor results of other workers and warned: "The surgical history of most of the reported cases shows not only the futility of an operative attack upon one of these angiomas, but the extreme risk of serious cortical damage which

10

1. History

is entailed... How many less successful attempts, made by surgeons less familiar with intracranial procedures, have gone unrecorded may be left to the imagination." "The lesions, in short, when accidentally exposed by the surgeon, had better be left alone, and how muchj^adiation may accomplish for them is undetermined though there are favourable experiences on record. So long ago as 1914 Wilhelm Magnus of Oslo unexpectedly exposed at operation a venous angioma of the left rolandic region, a decompression was made with the intention of treating the lesion with radium therapy which at that time was known favourably to influence cutaneous angiomas. After treatment, the decompression, which was bulging, receded, and the epileptiform attacks, from which the patient was suffering, became infrequent and finally disappeared ..." The publication of Reichert (1946) is unique, as he reported 15 cases of premotor vascular anomalies causing Jacksonian epilepsy, which were treated successfully by coagulation of the dural and pial vessels of the lesion (1935 to 1941).

References p. 369

Neurosurgical Treatment of Intracranial AVM Following the Introduction of Angiography (1930) As we have seen, surgical excision of AVMs was carried out between 1889 and 1930, both by general surgeons and neurosurgeons. Some of these cases met with success, others ended disastrously. After one or two bad results most surgeons did not risk further attempts at excision. With the advent of cerebral angiography the position began to change, for it became possible not only to diagnose the AVM but also to obtain some idea as to its location, its size and construction and the number of feeding and draining vessels. Angiography, however, was still somewhat primitive and the contrast material imperfect. Only a few angiographic demonstrations of cerebral AVMs were published before 1936 (Dott 1929, Lohr and Jacobi 1933, Moniz 1934 and 1951, Olivecrona and Tennis 1936). Dott provided the first demonstration of the angiographic aspects of cerebral AVMs at the Neurosurgical Conference in Stockholm in 1935. However, the full benefits of cerebral angiography came only with improved techniques which were not widely available until the 1950s. Olivecrona had a disappointing experience in 1923 when exploring for an infratentorial tumor (case 65). He was confronted with a highly vascular AVM and the patient died. In another case (66), Left carotid angiogram showing a frontoparietal AVM. In the monograph of Egas Moniz, "L'Angiographie Cerebrale", Masson, Paris 1934.

Intracranial Angiomas

with right parietal AVM, two surgical attempts remained unsuccessful. In future years Olivecrona (1927) urged caution in attempting surgery for an AVM found unexpectedly at operation. In this respect, his attitude was similar to that of Gushing and Dandy. On May 5, 1932 Olivecrona carried out his first successful radical removal of a left cerebellar AVM on a 37-year-old male. The preoperative diagnosis was tumor or tuberculoma. The stormy operation was performed under local anesthesia, took 8 hours and the patient needed a transfusion of 2000 ml. The postoperative course was uneventful and the patient left the hospital 3 months later. In the next case (a 52-year-old female with right temporal AVM) diagnosis had been made preoperatively and verified on angiography. Olivecrona's 16 cases together with 6 cases operated upon by Tennis and 4 venous angiomas were presented in their classical monograph in 1936 (Bergstrand et al. 1936). Out of 26 cases only 2 dural and 3 parenchyma! AVMs could be extirpated. They were cautions in advising operation saying that "Some polar AVMs and those in silent areas of the right hemisphere have been declared to be extirpable and curable, but in most cases the situation seemed to be unfavourable. A successful removal can be accomplished if all the feeders are eliminated, but this is only possible in a few cases." The authors did not recom-

Diagram of a temporooccipital AVM. Published in "An Introduction to Clinical Anatomy", 1932, London, by Traquair. The angiography was performed by Norman Dott in 1929 with sodium iodide. Also published in the monograph of Egas Moniz, "L'Angiographie Cerebrale", Masson, Paris 1934.

11

mend techniques of cerebral decompression or ligature of the internal carotid artery. Twelve years later Olivecrona published his extensive experience in 64 cases and mentioned also the surgical results of Penfield and Erickson (1941) and Pilcher (1946 a, b) together with the 7 successfully extirpated cases described by Dott in a personal communication Olivecrona and Riives (1948). By 1954 Olivecrona had removed 81 cerebral AVMs with quite exceptional results (Table 1.2). Table 1.2 Olivecrona and Ladenheim (1957)

The overall mortality for the series was 9% (7 cases), but most of these were early cases. In between 1951 and 1956 there was only a single operative death. The opinion that small to moderate sized AVMs in silent areas of the brain should be operated upon while, others in nonsilent areas were better left untouched, found general acceptance among neurosurgeons. Within 25 years (1932-1957) approximately 500 patients with cerebral AVMs had undergone surgery; Olivecrona and Lysholm

12

1. History

1927. Dott 1929, Tonnis 1934, Puusepp 1935, Bergstrand, Olivecrona and Tonnis 1936, Rottgen 1937, Moniz 1938, Seeger 1938, Sorgo 1938, Singleton 1939, Northfield 1940/1941, Krayenbuhl 1941, Penfield and Erickson 1941, Asenjo and Uiberall 1945, Jaeger and Forbes 1946, 1950, Pilcher 1946, Dott 1948, Olivecrona and Riives 1948, Pluvinage 1948, Trupp and Sachs 1948, Norlen 1949, Olivecrona 1949, 1950, Sorgo 1949, McKissock 1950, Pilcher et al. 1950, Sunder-Plass-mann 1950, Basset 1951, Gros and Martin 1951, Kraus 1951, Petit-Dutaillis and Guiot 1951, 1953, Thiebaut et al. 1951, Wechsler et al. 1951, Whitney 1951, Amyot 1953, Arne et al. 1953, Druckemiller and Carpenter 1953, Ebin 1953, Gil-lingham 1953, Krayenbuhl and Ya§argil 1953, Laine and Delandsheer 1953, 1956, Lazorthes and Geraud 1953, McKenzie 1953, Montrieul et al. 1953, Pompeu and Niemeyer 1953, Selverstone and White 1953, Tonnis and Lange-Cosack 1953, Falconer 1954, Logue and Monckton 1954, Martin and Brihaye 1954, Milletti 1954, Pimenta and da Silva 1954, Pluvinage 1954, Scott et al. 1954, Carton and Hickey 1955, Gould et al. 1955, Olsen and Wood 1955, Potter 1955, Hayne et al. 1956, Leppo et al. 1956, Lundberg et al. 1956, Paillas et al. 1956, Paterson and McKissock 1956, Philip-pides et al. 1956, Asenjo et al. 1957, Baker 1957, Hamby 1957, Krayenbuhl and Ya§argil 1957,1958 (90 cases, 26 radical removal), Ley 1957 (23 cases, 9 extirpations), McKissock and Hankinson 1957 (100 cases, 68 operated), Milletti 1957, Niemeyer 1957, Norlen 1957, Olivecrona and Ladenheim 1957 (100 cases, 81 operated), Paterson 1957, Tolosa 1957, Tonnis 1957, Af Bjorkesten 1959, Paillas et al. 1959, Tonnis et al. 1958. The results achieved were remarkable. The mortality for small AVMs was between 0 to 5%, and for moderate sized AVMs was generally between 6 and 10%, although some authors found mortality rates of over 20%. Over 60% of patients returned to a full working capacity after operation and serious morbidity was around 10%. Norlen (1949) was particularly successful in that he was able to remove AVMs totally in 10 patients with no mortality and only a small and temporary morbidity. Norlen's other principal contribution was his statement that "The malformation may cause cerebral circulatory failure. Notice that the arteries of the hemisphere surrounding the AVM, which are hardly seen in the preoperative angio-gram, filled normally with contrast once the AVM has been removed. In most cases the postoperative angiograms show that the enlarged and tortuous proximal feeding vessels returned to a normal diameter usually within 2 or 3 weeks." Follow-

References p. 369

ing on from this concept, Murphy (1954) first described the concept of "^cerebral steal syndrome". The First European Congress of Neurological Surgeons (Brussels 1957) included discussion on experience gained in operating on cerebral AVMs. It was generally accepted that palliative procedures such as decompression, ligation of the carotid artery or partial coagulation and partial removal of the lesion were ineffective and that complete removal should be the aim in all possible cases. There remained uncertainty regarding the operability of small or moderate sized lesions in eloquent areas of the brain and in cases of large AVMs. Nevertheless, the first approaches in this direction were already being made by Laine et al. (1956) and Houdart and Le Besnerais who published their results in 1963.

The Limitations of Surgery Eloquent Areas of the Hemispheres Pluvinage (1954) predicted a tendency towards more radical removal of all AVMs with the size, shape and location of the lesion becoming a secondary problem. Tonnis (Tonnis and Schiefer 1959, Tonnis 1961) carried out careful studies of general and localized blood flow and presented 215 patients with cerebral AVMs in which he had achieved complete removal in 118 cases, with 54 AVMs being in eloquent areas. He felt that total removal of an AVM was certainly possible and was the best form of treatment. Preoperative deficits frequently declined after operation and newly acquired deficits were mostly of a temporary nature. He concluded that 1) The location of an AVM is not a primary reason for inoperability, 2) The preoperative neurological deficits may be reduced after surgery, 3) The mortality in selected cases was 9.5%, 4) Major contraindications to surgery were large voluminous AVMs and elderly patients. Kunicki and Zoltan described their experience at the 1967 Madrid Meeting of the Congress of European Neurological Surgeons: Kunicki had successfully removed 2 AVMs from the motorsensory area and Zoltan described 38 cases of removal of AVMs lying predominantly in the motor cortex or speech areas, in the region of the middle cerebral artery. Of these patients, 4 died postoperatively, and just 2 had mild postoperative neurological disorders. Of 5 patients who had suffered severe hemiplegias following pre-

References p. 369

vious hemorrhage 3 were improved after surgery. These authors felt that the main reasons for their success were that the vessels comprising the anomaly did not contribute in any way to the cerebral circulation and that the parenchyma included within and immediately adjacent to the angioma was functionallyliselessrZoltan (1968) reemphasized this latter point. Further successes in operating upon AVMs in delicate areas of the brain were presented by Petit-Dutaillis et al. (1953), Laine et al. (1956, 1957), Achslogh et al. (1957), Houdart and Le Besnerais (1963), Pertuiset et al. 1963 and Christensen (1967). Deep Seated AVMs Deep seated AVMs lying within the striate, thalamic, parathalamic, limbic, intra- and paraventricular and callosal areas together with most infratentorial AVMs and those within the brain stem had always been generally declared inoperable. However, several surgeons did approach these lesions before microsurgical techniques became available. Olivecrona (1923), David et al. (1934), Alpers and Forster (1945), Boldrey and Miller (1949), Guillaume et al. (1950), Hamby (1952), French and Peyton (1954), Logue and Monckton (1954), McGuire et al. (1954), Carton and Hickey (1955), Strully (1955), Laine et al. (1956, 1957), Leppo et al. (1956), Poppen (1958), Caram et al. (1960), Dereux et al. (1959), Bonnal et al. (1960), Litvak et al. (1960), Pampus et al. (1960), Poppen and Avman (1960), Ralston and Papatheodorou (1960), Odom et al. (1961), Ver-biest (1961), Ciminello and Sachs (1962), Levine et al. (1962), Houdart and le Besnerais (1963), Pertuiset et al. (1963), Castellano et al. (1964), Kunc (1965), Mount (1965), Pool and Potts (1965), Laine and Galibert (1966), Walter and Bischof (1966), Lapras et al. (1968), Milhorat (1970), Montant et al. (1971), Fenyes et al. (1973), Ribaric (1974)________________ t Kunc (1967) declared that: "For arteriovenous' malformations in the basal ganglia and thalamus, ligation of feeding arteries may be the procedure • of choice. This, however, carries the danger of ' producing unintentional infarction owing to the great anatomical variability of the blood vessels at the basal structures of the brain. The same oper-ation can be very successful in one case and produce serious consequences in another. Very good results were achieved with this simple procedure in 2 cases of arteriovenous malformation on the anterior inferior cerebellar artery. To limit the operation to the ligature of supplying arteries is inadequate when the lesion is widespread for the

Intracranial Angiomas

13

arteriovenous shunt will increasingly attract blood from its small tributaries, which very soon become enormously dilated. Radical removal is the only effective method of treatment, if it is feasible." Morello (1967), at the congress in Madrid was of the opinion that "The outlook for patients with angiomas of the basal ganglia is very poor. There are a few accounts of fortunate cases in which the malformation, being small and emerging in the lateral ventricle, could be attacked directly with success, but unfortunately they are often large and cannot be removed." Nevertheless, Schurmann and Brock (1967) stated that "The reservations concerning the surgery of AVMs located in vital brain stem centers remain justified. The operability of such lesions seemed to depend upon site, size and clearcut delineation of the angioma, the number, caliber and source of the afferent vessels also whether their origin be uni- or bilateral, and the age of the patient together with the clinical course and picture of the illness." In 1967 microtechniques (including the operating microscope, bipolar coagulation, microinstruments and suture material) were introduced and the initial experience in 14 cases (including 4 deep seated AVMs) was published in the monograph of Ya§argil (1969). _Splenial and large cerebellar AVMs could be completely removed with good results as presented to the 4th European Congress in Prague 1971. The Symposium in Giessen (1974) was devoted to the problem of cerebral AVMs and the contributions were published by Pia in 1975. The papers showed a tendency toward more active surgery (Lapras 1975), with the introduction of new techniques such as microtechniques (Pia 1975, Bushe et al. 1975), electrothrombosis (Handa et al. 1975), cryosurgery (Walder 1975) and stereotaxy (Riechert 1975). The Sixth International Congress of Neurological Surgery in Sao Paulo (1977) dealt once more with deep seated AVMs of the brain. Kunc gave an excellent survey of the achievement and limitations: "It must be recognized that deep seated AVMs are the cause of greater disability and mortality than those at other sites. Hemorrhages threaten function and vitally important structures." The large series from the Burdenko Institute was presented by Filatov et al. (1978). In 160 cases the AVM was totally removed, in 60 patients endovascular occlusion of the feeding arteries was performed and 56 other patients underwent various palliative procedures. Of 60 deep seated AVMs, 37 were totally removed and in 16 cases balloon

14

1. History

occlusion was performed. There was only one death. Steiner's presentation at this meeting, showing results in 35 patients treated with stereotactically directed gamma rays, was a further milestone in the treatment of AVMs. Lesions up to 3 cm in diameter showed startling resolution after such treatment. Another promising radiation technique, especially for large lesions was presented by Kjellberg et al. (1977) in 33 patients.

Conservative versus Surgical Treatment Cerebral AVMs may now be treated by conventional or loupe surgery, microsurgery, embolization and radiation techniques, either alone, or in combination. With each advance and refinement of these methods, especially together with the improvement of neuroanesthetic techniques, and the increase of our knowledge concerning cerebral hemodynamics, there has followed a greater tendency throughout the world towards intervention in cases of AVM, as soon as the diagnosis has been made. This has lead to a good deal • of uncertainty regarding the natural history of untreated lesions and to a continuation of the uneasy feeling expressed by many authors that in a great many instances the outcome might be more favourable if the patient is left untreated. Until very recently (Crawford et al. 1986) the outcome in untreated cases had usually been described in only a very small number of patients in any given series. Comparison of treated and untreated groups is also made difficult by virtue of possibly selecting out of favourable cases for surgery i.e. patients who might anyway have had a favourable outcome had they been left untreated. Olivecrona and Riives (1948) stated that in the end, probably most, if not all unoperated patients die of hemorrhage or are completely incapacitated. Olivecrona (1957) found that 25% of his untreated patients were to die of further bleeding, one third were to suffer serious morbidity, but that 25% were to remain healthy and almost asymptomatic many years after diagnosis. He stressed that the two groups of operated and non-operated patients could not be compared as they were no doubt selected according to differing points of view. Botterell (1966) pointed out that progressive neurological deterioration may occur even though follow-up arteriography showed no change in the size of an AVM and he contributed this to progressive gliosis of surrounding cerebral tissue.

References p. 369

Paterson and McKissock (1956) stressed that the follow-up of untreated cases in their series did not contribute substantially to the knowledge of what might be termed the natural history of intracranial angiomas, largely because insufficient time had elapsed since their patients had been diagnosed. Yet it was worthy of note that few of them were severely incapacitated even after many years. Although angiomas may, through hemorrhage, lead to death or permanent incapacity, they felt they were much less likely to rupture than intracranial aneurysms/ They felt that Potter (1955) had published figures which lent support to their view; 27% of his patients survived for more than 20 years after the onset of symptoms and more than half of them had only slight disability or none at all. The increasingly aggressive attitude toward the surgical treatment of AVMs raised two controversial and interrelated issues: 1. Many retrospective series, although based on relatively small numbers of patients, seemed to prove that unoperated patients had a better prognosis. 2. The mortality and morbidity rates of operated cases in some series were not low (up to 18%). Svien and McRae (1965) from the Mayo Clinic considered that 85% of patients with angiomas were best treated conservatively. Perret and Nishioka (1966) analyzed 545 cases of AVM in a Cooperative Study and stated that the operative mortality should be less than 10% and the postoperative morbidity should be better than, or comparable to patients treated conservatively, for surgery to be justifiable. They found that the mortality in unoperated cases was 5% and in operated cases was 12%. These authors included palliative surgical treatments such as carotid ligation or partial resection in their surgically treated group. Therefore it is clear that a true comparison between operated and unoperated groups is impossible._____________________._ Г Pool and Potts (1965) collected523_cases from the available literature. They found that the mortality and morbidity of the conservatively treated group was 56%, while that for 187 patients treated by radical excision was only 26%. They suggested that "on the basis of these data, excision of a symptomatic AVM seems advisable whenever surgery can be done with reasonable safety since it offers the best chance of saving a patient from progressive neurological and mental deterioration, epileptic seizures, or death from hemor-rhage. This is because excision improves the circulation to those areas deprived of normal blood

References p. 369

- -Pply by the arteriovenous malformation of nor~dl blood supply and removes the threat of a ser.ous hemorrhage. On the other hand, excision is obviously contraindicated if the patient may become worse after surgery due to his age, condition, or the location and extent of the lesions. Excision of lesions in the occipital lobe or the posterior part of the temporal lobe may, for example, ^ead to permanent homonymous hemianopsia, but :his seems a small price to pay for relief from the threat of progressive brain damage or a fatal •emorrhage./ Under favourable conditions, moreover, an arteriovenous malformation can usually be excised without sacrificing significant amounts of intact tissue, even if this does lie adja;ent to the sensory or motor cortex or involves the dominant temporal lobe." "As a rule children tolerate excision particularly well. Good results can also be expected from excision if the arteriovenous malformation is small and the patient is under 50 years of age and in a good preoperative condition. In patients over 50 years of age the need for excision is less urgent than in younger ones, since progressive enlargement of the arteriovenous malformation is less Likely." They concluded: "In our experience, approximately 75% of patients recover well following excision while some reports indicate even better results." French et al. (1964) considered that "AVMs are not in any sense to be considered new growths, but they may enlarge with time by expansion of jhe vessels and dilatation of aneurysmal sacs". This seemed an important factor to be included in the evaluation of the necessity of surgical excision. On this basis the practice of surgical intervention seemed unquestionably superior to nonsurgical management. However, in 1970, Troupp reported on 137 patients seen between 1942 and 1969 with angiographically verified AVMs. These were not operated upon, except for exploratory craniotomy in 2 cases (Troupp et al. 1969, 1970). At that time, he felt their follow-up figures indicated a more cheerful outcome than that postulated by others, notably Olivecrona and Riives (1948), Pampus et al. (1960) andNorlen (1966). After 7 years Troupp reviewed the same 137 cases and changed his mind somewhat, for only 27 cases were well. Fourteen were described as fair but 28 were disabled and 9 more had died from hemorrhage (total 23). The only factor of interest he could relate concerning the prognosis was the location of the AVM. Of those situated in the frontal, temporal and occipital regions, only 2 patients died from bleeding while 21 of those situated in

Intracranial Angiomas

15

the parietal, central and infratentorial regions ruptured fatally. Drake's observations (1979) concurred with the view that while the initial course of an AVM is reasonably benign, the long-term outcome is less favourable. Waltimo (1973) discussed the increasing size of an AVM in terms of prognosis: In a study of 21 patients with AVM subjected to serial angiograms (with a median time between examinations of 44 months), it was noted that 12 of the lesions increased in size, 8 remained unchanged, and one became smaller. He also found that smaller AVMs were the most likely to increase in size and the largest were the most likely to reduce in size. Hook and Johanson (1958) found that in 12 cases: 8 increased in size, 4 remained unchanged and 1 disappeared and Stein (1984) found in his series that one third increased, one third remained unchanged and one third became smaller. Kelly etal. (1969) followed 33 patients for an average of 15.5 years after their initial hemorrhage from an AVM. There was a mortality rate of 28% and half of the patients had little, if any disability. Fults and Kelly (1984) found that the prognosis for patients presenting with seizures was more favourable than for patients presenting with hemorrhage, and that the mortality associated with recurrent hemorrhage did not increase significantly with successive bleeds. Patients with posterior fossa AVMs fared considerably worse than patients with an AVM located elsewhere in the brain. Pellettieri (1979), however, found that the risk of death in an unoperated group of patients followed over a period at 18 years, to be 2.5 times greater than in an operated group. The prognosis for children with intracranial AVM was not different to that for adults. The size of the AVM did not dictate either the clinical outcome for the patient or the risk of hemorrhage. There seemed to be no correlation between pregnancy (or delivery) and hemorrhage from a cerebral AVM in a female patient. The publication of Pellettieri etal. (1979) was a milestone in the literature on the natural history of the AVM as the authors applied a differential analysis to their cases. By relating the results to 6 or 7 variables (age, sex, AVM-size, AVM-location, symptoms at onset and neurological findings at admission) it was possible to grade each variable with respect to prognostic importance. The most favourable risk factors were age below 40 years, absence of a neurological deficit, a superficial and small AVM in a silent area, female

16

1. History

sex. and SAH at onset. These variables were assigned numerical values, and grouped on a scale ranging from +16 to -16. The AVMs with values of -10 or below were found to have a poor prognosis whether the condition was treated surgically or conservatively. In those ranked -8 or above, surgical treatment was considered to give consistently better results and in the AVMs with risk values between -2 and +2, a significantly better outcome could be expected with surgical or conservative management. Their conclusions probably reflect the opinion of most neurosurgeons: "A favourable combination of variables gives relatively good results with both modes of therapy. Results deteriorate proportionally with falling values on the risk scale in both groups. Although surgery tends to give better results, the difference is only significant within a limited range on the risk scale. This probably explains the controversy between those who advocate surgery and those who prefer conservative treatment." Calica et al. (1984), recently took the idea of risk prediction a step further, using a complicated regression formula involving 14 variables to assess outcome (6). When they applied this formula to their 78 patients with intracerebral AVMs, it divided 85% of them into low (3% became impaired), medium (42% became impaired), and high (94% became impaired) risk groups. Citing the paper of Calica et al., Wilkins (1985) has predicted that it may become possible with additional experience to use computerized paradigms to predict with greater accuracy the outcome of an intracranial AVM without surgery or with any of several possible treatment protocols so that the best approach can be planned. Until then, we must still rely on fragmentary published information about the "natural history" of such lesions and on a realistic assessment of our ever-changing abilities to deal with them surgically. Wilkins felt it had been difficult to assess the natural history of intracranial vascular malformations because they are varied in nature, they are frequently silent clinically, they are often treated when they are discovered and untreated lesions are not often followed in an organized way. We would add to this argument the fact that many published data relate to unsufficiently analyzed cases. We agree also with the remarks of Mohr (1984), "The enormously accumulated studies concerning the natural history of the AVM is retrospective and the rarity of these lesions precludes any definitive prospective study of the natural history. Furthermore, the clinical picture of many of these lesions spans years if not

References p. 369

decades. The remarkable variation of clinical material from center to center has become apparent and with it a hesitancy to offer such experience for publication." Most recently (1986) Crawford et al. reported upon 217 out of a total of 343 patients with cere bral AVMs, who were managed without surgery. He followed them for a mean of 10.4 years and, using life survival analyses, found that there was a 42% risk of hemorrhage, 29% risk of death, 18% risk of epilepsy and 27% risk of neurological defi cit over a 20-year period. This represents the larg est series of untreated cases studied over a long time span. He found, interestingly, that although small AVMs, as described by many authors, are more likely to present with hemorrhage in the first instance (82%) they did not subsequently carry a higher risk of recurrent hemorrhage. The opera tive rate in this series was only 34% with the ten-, dency to leave untreated those AVMs which were large and deep, more posteriorly situated, in the left hemisphere or crossing the midline. However, the authors felt that the size, depth, and possibly the site of the arteriovenous malformations did not significantly affect outcome. The main influencing factors in their opinion were recurrent hemorrhage and increased age at diagnosis. Although the overall mortality at 20 years was 29%, only 65% of the deaths could be attributed directly to the AVM and then most commonly from hemorrhage. The risk of epilepsy is increased with temporal lobejesions. I There are reasons other than those put forward by Mohr which make comparisons between operative and conservative management difficult: a) The inclusion of ligation of extra- or intracra nial vessels, coagulation and partial removal of the lesion and complete removal of the AVM under the term: "operated cases" is incorrect (Paterson and McKissock 1956, Pool and Potts 1965) (Tables 1.3 and 1.4). The retrospective study of the 186 AVM cases of Krayenbuhl (1936-1966) required separa tion of the patients into 3 groups: I Untreated, II Palliative treatment and III Complete remo val of the AVM (Table 1.5). A second analysis 15 years later (1984) clearly proved that the patients with complete removal of the cerebral AVM presented much better late results than the patients in group I-II (Table 1.5).

p. 369

References p. 369

Intracranial Angiomas

17

18

1. History

Twenty-one patients (20%) out of groups I—II had recurrent hemorrhages, whereas group III no case of recurrent hemorrhage occurred. Long-term clinical examinations have shown that only 15% of non-operated cases with large and moderate sized AVMs remain in a good clinical condition. The remainder of the cases develop within the following 10 to 15 years after diagnosis a progressive clinical deterioration characterized either by repeated hemorrhages or a progressive mental and neurological symptomatology ultimately leading to irreversible invalidism or even death. A precise analysis of these cases will be provided in Vol. IIIB. b) Differences in retrospective studies are mainly caused by analyzing collected cases using different criteria applied to unoperated and operated cases. The statistics may give satisfactory information concerning age, sex, symptoms of the patient and size and site of the lesion, but they cannot necessarily provide a guide to treatment, as an "inoperable" lesion for some neurosurgeons, is deemed operable by others. It is remarkable that in some series 30-50% of AVMs are still deemed inoperable. c) Authors with conservative attitudes may argue that the operated cases are "easy" lesions whereas the unoperated patient would be regarded as having more high risk characters (size, site etc.). This argument is only partially correct. Many operated cases are not elective "easy" lesions, but occur as emergency cases because of hemorrhage or progressive neurological and mental deficits. Some patients with "easy" operable lesions refuse surgery as they will not accept any operative risk. Some informed patients prefer to gamble on an early favourable clinical course in order to await further technological advances (Drake 1979). d) Some patients accept surgical risk only after deterioration of their symptoms. Such cases which have been conservatively treated are, however, most often not included in the statistics of unoperated cases, but rather in those of operated cases. Without this recourse to surgery the statistical outlook of unoperated cases might be less favourable. Intracerebral hemorrhage is the most serious complication. Its frequency varies from about 40% to 68% in most series (Pia 1975) with those cases presenting initially with hemorrhage being at greater risk (Crawford et al. 1986). e) As a result of discussion between neurologists, neuropathologists and particularly neurosurgeons, technical developments within the last

References p. 3691

30 years (microsurgery, modern neuroanesthe-l sia, high energy radiation, selective emboli-j zation) have offered new approaches in treat-1 ment. In many publications with large series of operated cases there is no clear separation o f[ statistical data, as to which cases have been operated using conventional surgical technique, pure microsurgical techniques or using combined techniques such as embolization and microsurgery or surgery and radiation. These data are more clearly given in publications of smaller series, especially those concerning the surgery of "deep seated AVMs". f) Other variables have rarely been considered. It is necessary to indicate not just the size of an AVM, in cm2 or cm3, but also its precise construction (single or multiple niduses and compartments, single or multiple AVMs, plexiform, fistulous or diffuse) and its relation to the venous system (Dobbelaere et al. 1979, Vinuela et al. 1985). The precise location should be given not just as frontal, parietal, temporal etc., but as a location within a lobe (polar, dorsal, ventral, lateral, medial, superficial or sulcal etc.). g) Statistics concerning the surgical mortality and morbidity are rarely discussed in detail. Generally, the operative mortality in the collected literature is 11.0% (among this number are large - giant AVMs, deep seated AVMs, patients in condition IV-V, some with large hematomas). The statement that the mortality is 5—6% in good risk cases and 20-30% in poor risk cases is helpful but not sufficient to obtain a proper indication as to individual operability. Useful information has been provided in the series of 81 patients of Haerer (1982) (Tables 1.6 and 1.7).

Table 1.6 Outcome related to treatment: 7-year follow-up of 81 patients (from Haerer, A. F.: in Smith, R.R., A. F. Haerer: Vascular Malformations and Fistulae of the Brain. Raven, New York 1982)

References p. 369 Table 1.7 Outcome related to size of lesion during 7-year follow-up of 81 patients (from Haerer, A. F.: in Smith, R. R., A.F. Haerer: Vascular Malformations and Fistulae of the Brain. Raven, New York 1982)

h) The simultaneous development of three new techniques, microsurgery, embolization and radiation, over the past 20 years has provided, to some extent, healthy competition, yet it has also been exasperating. The success of stereotactic gamma-radiation in the treatment of small to moderate sized AVMs (up to 3 cm in diameter) was and is a factor which reduces just that number of surgically suitable cases for the teaching of young neurosurgeons. In cases of large to giant AVMs, selective embolization and proton beam application are attempts at treatment in otherwise hopeless situations. The results have not as yet been convincing. The information gained from CT, MRI and selec tive angiography concerning size, site, shape, pre cise construction and composition of an AVM, and the studies with Doppler sonography, PET etc. (see Chapter 4: Hemodynamics) still does not allow us to make any prognostic conclusion about the behavior of the AVM with regard to hemor rhage, ischemia, and growth. Statistical studies showing that AVMs are more benign lesions than aneurysms (Crawford et al. 1986) are unsatisfac tory. For a given single patient, nobody can readily predict what is going to happen. The exact risk that these lesions present is far from clear (Symon 1976). It remains a 'perplexing disease' (Fults and Kelly 1984). Over the past 30 years the number of publications on cerebral AVM and the number of operated cases have increased enormously: Anderson and Korbin 1958, Hook and Johanson 1958, Tonnis et al. 1958 (134 cases), Guillaume et al. 1959, Paillas et al. 1959 (70 cases), (80 cases), Poppen 1960, Krenchel 1961 (98 cases), Margolis et al. 1961, Dott and MacCabe 1963, Frugoni and Ruberti 1963 (54 cases), Houdart and Le Besnerais 1963 (44 cases, 3), Sano 1964, Kunc 1965, 1974, 1975, 1977, Pool and Potts 1965 (523 col lected cases), Sharkey 1965, Svien and McRae 1965 (95 cases), Perret and Nishioka 1966 (545 collected cases), Pool 1965, 1968, Schatz and Botterell 1966, Walter and Bischof 1966 (72 cases),

Intracranial Angiomas

19

Henderson and Gomez 1967, Houdart 1967, Carrea and Girado 1968, Castaigne et al. 1968 (53 cases), Kempe 1968, Kunicki 1968, Pertuiset 1968, Verbiest 1968, Weir et al. 1968, French and Chou 1969, Salibi 1969, Vianello 1969, Bartal and Yahel 1970 (43 cases, 37 operated), Maspes and Marini 1970, Milhorat 1970, Muller et al. 1970 (99 cases), Troupp et al. 1970, 1977 (137 cases), Montaut et al. 1971, Perria et al. 1971, Raskind 1971, Amacher et al. 1972 (55 cases), Bushe et al. 1972 (42 cases, 10 operated), Forster et al. 1972 (150 cases between 1930-1960), Green and Vaughan 1972, Krayenbuhl and Ya§argil 1972 (523 cases, 303 operated; 187 extirpated), Pia 1972, Amacher and Shillito 1973, French and Seljeskog 1973, Morello and Borghi 1973 (154 cases, 102 operated), Peserino and Frugoni 1973 (91 cases), Waltimo 1973 (43 cases), Boldrey and Pevehouse 1975, Bushe et al. 1975 (56 cases, 46 operated), Chou et al. 1975, Pia 1975 (124 cases), Sano et al. 1975 (205 cases, 165 operated), Pertuiset et al. 1976, Towfighi et al. 1976, Ya§argil et al. 1976, French 1977, Luessenhop and Gennarelli 1977 (300 cases, 49 operated), Filatov et al. 1978 (588 diagnosed, 276 operated, 160 radical removal, 60 endovascular occlusion, 56 palliative procedures), Juhasz 1978, Kosary et al. 1978 (12 cases), Mingrino 1978 (196 cases, 98 operated), Patterson and Voorhies 1978 (50 cases), So 1978, Vigouroux et al. 1978, Andreussi et al. 1979, Dobbelaere et al. (Laine) 1979 (370 cases), Drake 1979 (166 cases, 140 radically operated), Pellettieri et al. (Norlen) 1979 (166 cases, 119 operated), Pertuiset et al. 1979 (162 cases), Sundt 1979 (38 cerebral cases, It), Wilson et al. 1979 (183 cases, 65 radically operated), Da Pian et al. 1980, Guidetti and Delitala 1980 (145 cases, 95 operated, 92 radically, 50 conservatively), Laine et al. 1980, 1981 (500 cases), Parkinson and Bachers 1980 (100 cases, 90 operated, lOt), Viale et al. 1980, Gerosa et al. 1981. Pertuiset et al. 1981, Aimard 1982 (100 cases), Albert 1982 (178 cases, 140 operated), Debrun et al. 1982 (46 cases, acrylate), Heros 1982. Malis 1982, Martin and Wilson 1982 (116 cases, 16 occl. operated), Patterson 1982, Smith et al. 1982, Suzuki 1982, Graf et al. 1983 (191 cases between 1976-80), Hassler et al. 1983 (35 cases), Ojemann and Crowell 1983, Yonekawa et al. 1983. Black and Farhat 1984, Fujita and Matsumoto 1984, Fults and Kelly 1984 (131 cases, 48 operated between 1979-82), Grisoli et al. 1984, Martin et al. 1984, Rutka and Tucker 1984, Wilson and Stein 1984 (180 cases, 175 radically, 5 subtotally operated, 2t), Adelt et al. 1985 (43 cases), Aoki and Mizutani 1985, Bonnal 1985, Davis and Symon 1985 (129 cases, 69 operated

20

1. History

between 1948-1980, It), Jomin et al. 1985 (128 cases), Salcman et al. 1985, Samson and Batjer 1985. 1985, Waga et al. 1985, Crawford et al. 1986. Drake 1986.

Monographs Comprehensive monographs including history, embryology, anatomy, pathological and clinical considerations, analyses of results in operated and nonoperated patients with intracranial AVMs have been published since 1928 by: Gushing and Bailey 1928, Dandy 1928,

References p. 369

Bergstrand, Olivecrona and Tonnis 1936 (in German), Asenjo and Uiberall 1945 (in Spanish), Olivecrona and Ladenheim 1957 (in English), Ley 1957 (in Spanish), Pool and Potts 1965, Lange-Cosack two separate chapters in Olivecrona and Tonnis: Handbook of Neurosurgery, Vol. IV, 1966, Norlen in Olivecrona and Tonnis: Handbook of Neurosurgery, Vol. IV, 1966, Smith, Haerer and Russel 1982, Ojemann and Crowell 1983, Wilson and Stein 1984, Fein and Flamm 1985.

Summary and Outlook Five aspects of vascular malformations have always been, and still remain, controversial: 1) Pathogenesis, 2) Nomenclature, 3) Classification, 4) Diagnosis, 5) Treatment. The first 3 aspects are discussed on pages 49-61.

Diagnosis A vast increase in the number of angiographic studies performed from 1928 onwards, has given rise to the impression that AVMsbf all types have become more frequent in their presentation to the clinician. Once any of these lesions have become symptomatic it is generally felt that it has become a more dangerous lesion to that patient. Whether this is true for all types of vascular malformation is uncertain. There is even an argument as to the frequency of occurrence of the various types of anomaly. Earlier, it was generally considered that venous and cavernous malformations were rare, but McCormick (1985) in his large pathological series found that the opposite was true and that venous malformations were 10 times more common than the arterial or arteriovenous forms. The next most frequent form of malformation was the cavernoma. Improved angiographic techniques (Constans et al. 1968, Wendling et al. 1976, Preissig et al. 1976) and the routine use of CT scanning and radionucleide scanning (Partain et al. 1979, Fierstien et al. 1979) demonstrated the increasingly frequent occurrence of venous malformations. The incidence of cavernous malformations

has also apparently increased enormously since the intruduction of the MRI scan. Huang et al. (1984) have further revived the 200 year old dispute regarding nomenclature.

Surgery In terms of surgical treatment: a) Decompression (Ray 1941 and others), and extra- or intracranial ligature of carotid arteries are now techniques of the past. Potter's criticism is valid: "The ligature invited arterial blood from somewhere on the 'easy term' of low resistance at the expense of normal brain." b) Radical excision is the surgical goal whenever possible, but must minimize damage to the normal parenchyma and function of the brain. Hypotension, temporary occlusion of involved vessels (Gillingham 1953), identification of afferent and efferent vessels with fluorescein angiography (Feindel et al. 1965), intracranial, intraoperative flow measurement (Nornes and Grip 1980), multiple stage operations (Pertui-set and Sichez 1978) and interdisciplinary attack (embolization by neuroradiologist and removal by neurosurgeon, Stein and Wolpert 1980) are recently available useful technical adjuncts. Stereotactic approaches (Guiot et al. 1960, Riechert and Mundinger 1964, Wijnalda and Bosch 1975, Kandel and Peresedov 1977), electrothrombosis (Handa et al. 1977), and cryosurgery (Walder et al. 1970) have not found widespread acceptance. Techniques of hypothermia, circulatory arrest and circulatory bypass and the use of steroids (Edgerton 1983, Nagamine et al. 1983) have all been employed

references p. 369

with some success. Yet other techniques such as gamma radiation (Steiner et al. 1972), proton beam therapy (Kjellberg 1978) and selective embolization (Brooks 1930, Luessen-hop and Spence 1960, Sano et al. 1965, Djind-jian 1970, Doppman et al. 1971, Serbinenko 1974. Hilal et al. 1974, Wolpert and Stein 1975, Debrun et al. 1975, Russell and Berenstein 1981. Merland et al. 1983, and others) have great potential.

Surgery

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2

Embryology Miguel Marin-Padilla

A. Embryogenesis of the Early Vascularization of the Central Nervous System Introduction Тhе Vascularization of the central nervous system (CNS) is a complex process, best described as an integrative vascular metamorphosis continuously adapting to its developmental modifications, Embryonic development of the CNS itself is also complex. It consists of the progressive transformation of a tubular structure (neural tube) into several regions, each with a different and specific structural organization. The Vascularization of each of these regions is an integrated process which adapts to its particular growing structural and functional needs. While these regional vascular differences are clinically and surgically relevant. there are common features in the early vascularization of the CNS shared by all its regions. In the present chapter, common developmental features that characterize the general vascularization of the CNS, rather than regional differences, will be emphasized. The available information concerning anatomic, histologic, pathologic, radiographic, clinical and surgical aspects of the formed CNS vasculature is enormous and can be readily obtained from a variety of books, monographs and review articles Kaplan and Ford 1966, Taveras and Wood 1964, Van den Bergh 1967, Van den Bergh and Vander Eecken 1968, Stephens and Stilwell 1969, Kety 1972, Newton and Potts 1974, Peters et al. 1976, Kautzky et al. 1982, Dudley 1982, McCormick 1983, Ya§argil 1984). Although, information is also available concerning the embryonic development of the CNS vasculature (Mall 1904, Streeter 1918, Padget 1948, 1957, Moffat 1962, Klosovskii 1963, Pessacq and Reissenweber 1972, Hamilton et al. 1972, Bar and Wolff 1972, Gamble 1975, Hauw et al. 1975, Wolff et al. 1975, Pape and Wig-

glesworth 1979) some early aspects of it remain poorly understood. The actual perforation of the CNS surface by embryonic vessels as well as the sequential establishment of its vascular territories needs further investigation. Information is also needed concerning the interrelationships between the development of the CNS vascular territories and that of the meningeal, the Virchow-Robin and the intra-neural glial tissue compartments. Early in embryonic development the neural tube, as a specialized epithelial (neuroectoderm) tissue, lacks an inherent vasculature (Sabin 1917, Streeter 1918, Strong 1961, Hamilton et al. 1972, Marin-Padilla 1985b). Therefore, it should be possible to study the early embryonic Vascularization of any of its regions. The Vascularization of the neural tube follows a caudal-cephalad gradient which is synchronous with that of its ascending differentiation and maturation. In any given region of the developing CNS, embryonic vessels must first surround and organize around (outside of) it; secondly, they must perforate the CNS external basal lamina and marginal glia, which constitute an anatomic barrier; and, thirdly, they must grow within the developing neural tissue while adapting to its growing structural and functional needs. Thus, three different vascular territories must progressively emerge in the early Vascularization of every region of the developing CNS. They are the perineural, the interneural and the intramural vascular territories, respectively. The term "neural" used to describe these three vascular territories encompasses "nervous (neural) tissue". In other words, vascular territories which embryologically evolve outside (peri), in between (inter) and inside (intra) nervous tissue, respectively.

24

2. Embryology

Each vascular territory, though interrelated, evolves sequentially, independently, and within a different and specific tissue compartment. Each territory gives rise to different types of vessels. The main arterial and venous systems of the CNS, which are components of the perineural vascular territory, evolve embedded within the meningeal compartments. Most of the perforating arterioles and venules of the CNS vasculature, which are components of the interneural vascular territory, evolve within the Virchow-Robin compartment (VRC) and hence are outside, "in between" the nervous tissue proper. Thus, the term interneural is introduced to characterize this territory of the CNS vasculature. Finally, the capillaries, apparently the only vessels that penetrate the nervous tissue proper, constitute the intraneural territory of the CNS vasculature. Intraneural capillaries also evolve embedded within a specialized compartment represented by the perivascular glia. The early embryonic development and sequential establishment of each of these three vascular territories will be analyzed in association with the development of the meningeal, the VirchowRobin, and the intraneural perivascular glia compartments, respectively. Since a study of the early vasculogenesis of every region of the CNS would be too complex and beyond the scope of this text, only that of the embryonic cerebral cortex will be considered in detail (see also: Marin-Padilla 1970, 1971, 1978, 1982, 1983). Nevertheless, it should be emphasized that the observations presented and discussed should be fundamentally applicable to the early vascularization of all regions of the CNS.

Perineural Vascular Territory of the CNS Vasculature Vasculogenesis starts in situ from consolidated angioblastic cell islands found throughout the mesoderm, the yolk sac and the body stalk of the young embryo. The cellular elements of these islands seem to undergo progressive cytoplasmic liquefaction (Sabin 1917, 1920) which results in their eventual canalization. However, the process of canalization of these islands as well as that of growing capillaries remains poorly understood and controversial (Manasek 1971). Progressive canalization of the angioblastic islands results in the formation of a precirculatory plexus of primordial vessels which are large, irregular and composed of several endothelial cells joined by tight junctions. They are surrounded by a thin and

References p. 379

often incomplete basal lamina, and grow actively by sprouting. Zones of vascular growth are deprived of basal lamina and their leading endothelial cell or cells produce numerous long filopodia able to advance into the surrounding tissue (see Figs 2.11, 2.12). Blood cells are also believed to evolve from the original angioblasts (Streeter 1918, Sabin 1920) and they are identified very early in the lumen of embryonic vessels. The precirculatory vascular plexuses eventually establish communication through the arterial and venous systems with the heart and blood starts to circulate throughout the embryo. Among the earliest and most prominent vascular plexuses recognized in the developing embryo is the head plexus. It is formed around the cephalic region of the CNS. By the 4th week of human embryonic development the head plexus is already a prominent vascular organization (Streeter 1918, Padget 1948, 1957, Hamilton et al. 1972). By the 6th week of age, some of the main arteries, veins and venous sinuses, which characterize the adult brain, are already recognizable (Fig 2.1). The vascularization of the developing CNS begins at the myelencephalon and ascends progressively through the metencephalon, mesencephalon, diencephalon, striatum and telencephalon (cerebral cortex) which is the last region to be vascula-rized (Streeter 1918, Bar and Wolff 1972, Marin-Padilla 1985b). Therefore, it follows an ascending sequential gradient which keep pace with the CNS ascending differentiation and maturation. By the 7th gestational week of human development early vascularization of the medulla (Fig 2.2A), the pons (Fig 2.2B), the diencephalon, and the striatum (Fig 2.2C) is already underway. However, the cerebral cortex (Fig 2.2D) still lacks its intrinsic vasculature. The human cerebral cortex does not start to vascularize until around the 8th week of embryonic age. Its vascularization follows a ventro-lateral-medial sequential gradient which is synchronous with its advancing differentiation and maturation. The cephalic region of the developing CNS is surrounded by the embryonic meninges. They constitute a prominent and quite large tissue compartment (Fig 2.2). The embryonic meninges are well vascularized before the vascularization of the CNS begins (Figs 2.2, 2.3). Three distinct primordial lamellae: the dura, the arachnoid and the pia mater are recognizable (Fig 2.3). However, there are no distinct separations or tissue spaces between them. The blood vessels of the embryonic meninges can also be separated into three distinct strata (Figs 2.2, 2.3). The outer stratum (Fig 2.3) carries the dural vessels from which the ve-

г^егепсез р. 379

Perineural Vascular Territory

25

sagiftaiis

j 2.1 Reconstruction of the cephalic vascular plexus of a 21 mm human embryo of about 50 days illustrating the organization and distribution of its embryonic vessels. Many of the main arteries, veins and venous sinuses which char-acterize the adult brain can already be recognized. All vessels illustrated are components of the perineural vascular terri-tory of the CNS vasculature. However, the pial vascular plexus is not illustrated. A portion of the cerebral cortex has been removed to demonstrate the vascularization of its choroid plexus, the anterior cerebral artery and the sinus rectus. The thin embryonic cerebral cortex still has no intrinsic vasculature at this age. (From Streeter, G. L: Contr. Embryol. Car-neg Instn8:5, 1918.)

nous sinuses of the CNS evolve. The intermediate | stratum, which is the largest, carries the arachnoi-dal vessels from which the main arterial and venous systems of the CNS evolve. The inner stratum carries the pial vessels from which the pial vascular plexus evolves. The embryonic pial plexus covers the entire surface of the developing CNS, and adapts intimately to its variable external morphology (Figs 2.2, 2.3). Its formation always precedes the intrinsic vascularization of any of the CNS regions (Fig 2.2). All perforating vessels which enter into the various regions of the developing CNS originate from their overlying pial vascular plexus. All meningeal vessels, including the dural, the arachnoidal and the pial vessels, constitute together the perineural vascular territory of the CNS vasculature.

The subsequent development of the head vascular plexus (Fig 2.1) is complex because it actually comprises the concomitant formation of three different but interrelated vascular systems, dural, arachnoidal and pial — strata. The sequential embryonic development of the main arteries, veins and venous sinuses of the perineural vascular territory of the brain has been studied in great detail by several investigators (Streeter 1918, Padget 1948, 1957, Bar and Wolff 1972, Wolff et al. 1975). These studies represent the most complete account of the vasculogenesis of any region of the developing CNS. Figs 2.4 and 2.5 are reproduced from the original works of Padget (1948, 1957). In these diagrams the complete prenatal development of each of the main vessels of the brain can be analyzed and fol-

26

2. Embryology

References p. 379

Fig 2.2 Composite figure illustrating a parasagittal section ( 1 ) of the head of a 50 day human embryo, and a coronal section (2) of the anlage of the cortical choroid plexuses from a younger, 43 day old, human embryo. The parasagittal section illustrates the major regions of the developing brain, the abundant and well vascularized arachnoidal tissue (a), and the pial vascular plexus (p). The lateral (LV), third (III), and fourth (IV) ventricles; and, aqueduct of Sylvius (S) identify the embryonic cerebral cortex, the diencephalon, the cerebellar primordium and the mesencephalon, respectively. The intrinsic vascularization of the medulla (A), the pons (B) and the striatum (C) is already underway while that of the cerebral cortex (D) has not yet started. The abundant arachnoidal tissue (a) and the pial vascular plexus (p) are also illustrated in these four CNS regions. The coronal section illustrates the dural (d), the arachnoidal (a) and the pial (p) vessels around the still unvascularized embryonic cerebral cortex (cc). The cortical pial vascular plexus (p) extends into the anlage of the choroid plexuses (cp) establishing its tela choroidea from which its vascularization will evolve. (From Hamby, W. В.: J. Neurosurg. 1 5 : 65-75, 1958.) H&E preparations, parasagittal section, x20.

r References p. 379

Perineural Vascular Territory

27

Fig 2.3 Camera lucida drawings of the embryonic meninges covering the cerebral cortex of a 50 day human embryo, illustrating its composition and structural organization. Three primordial lamellae are recognized in it. The outer or dural lamella (D) is composed of closely arranged elongated cells which congregate below the developing membranous neurocranium. The intermediate or arachnoidal lamella (A) is composed of loosely arranged stellate cells with long fine cytoplasmic processes with apparently empty spaces between them. The inner or pial lamella (P) has fewer cells and more vessels than the other two and is in contact with the surface of the cerebral cortex. The surface of the cerebral cortex is composed of the closely apposed endfeet (G) of the marginal glia covered by the CMS external basal lamina. Some meningeal vessels have attachments of non-endothelial cells (arrows), which might represent precursors of pericytes and smooth muscle cells, and have circulating blood cells in their lumina. The thickness of the cortical meninges illustrated is approximately 100 micrometers. (Compare with Fig 2.13.)

lowed in detail. It should be emphasized that the illustrations (Figs 2.4,2.5) only represent the prenatal development of the main arterial and venous systems of the brain. They do not supply information regarding the development of the arachnoidal connecting vessels nor of the pial vascular plexus, which are also important components of the perineural vascular territory of the CNS vasculature. The perineural vasculature undergoes an integra-tive development continuously adapting to the changing external morphology of the growing brain. The extraordinary development of the human cerebral cortex represents perhaps the most significant single factor underlying the

remarkable developmental metamorphosis of the intracranial vasculature (Figs 2.4, 2.5). The cerebral cortex evolves from a small vesicle at the anterior end of the brain (Fig 2.2) to a large structure which comes to occupy practically the entire cranial cavity (Figs 2.4, 2.5). The adaptative metamorphosis of arteries and veins to the expanding cerebral cortex are clearly demonstrated in the accompanying illustrations (Figs 2.4, 2.5). It is quite obvious from these illustrations that in the course of embryonic development the location and distribution of the different blood vessels change continuously. This adaptative vascular metamorphosis is the result of continuous and

28

2. Embryology

References p. 379

Fig 2.4 Series of diagrams illustrating the prenatal developmental metamorphosis of the major arterial systems of the human brain. The illustrations are self explanatory. (From Padget, D. H.: Contr. Embryol. Carneg. Instn 32: 207, 1948.) Fig 2.5 Series of diagrams illustrating the prenatal developmental metamorphosis of the major venous systems and sinuses of the human brain. The illustrations are self explanatory. (From Padget, D. H.: Contr. Embryol. Carneg. Instn 34: 79, 1957.)

References p. 379

Perineural Vascular Territory

29

30

2. Embryology

concomitant capillary angiogenesis and capillary reabsorption. The original anastomotic plexus formed by the perineural vessels undergoes continuous remodelling by the addition of new links (angiogenesis) around growing or expanding regions and by the elimination of others (reabsorption) when no longer needed. Undoubtedly, the loose structural organization of the embryonic arachnoidal mesh and its abundance (Figs 2.2, 2.3) provide an ideal tissue substratum for these vascular adaptations. In spite of their obvious significance, the dual embryonic processes of capillary angiogenesis and reabsorption have been little studied and remain poorly understood. However, these processes have been studied in more detail in neovascularization using a variety of experimental models including tumor angiogenesis (Folkman 1976, 1982, Cotran 1982, Hunter and Gabbiani 1982, Glaser and Patz 1983, Sholley et al. 1984). In the course of embryonic development, the arachnoidal mesh is traversed by numerous vessels of various calibers linking the main arteries and veins with the pial vascular plexus (Figs 2.2, 2.3). The size, number, location and distribution of the connecting arachnoidal vessels also undergo continuous developmental modifications and rearrangements by both capillary angiogenesis and reabsorption. Early in development, these vessels are large, irregular, thin walled, and composed of several endothelial cells joined by tight junctions (Fig 2.3). There are no recognizable arteries or veins and all of them appear to be growing actively by sprouting. Later in development, the arachnoidal arteries and veins become surrounded by arachnoidal cells which isolate them from the Table 2.1

Composition and development of the meninges

References p. 379

cerebrospinal fluid (CSF) compartment. The adult arachnoidal vessels thus become enclosed within distinct perivascular tissue spaces which seem to be analogous and continuous with those of other vessels of the body (see Fig 2.13). Furthermore, according to recent observations (Casley-Smith et al. 1976, Krisch and Buchheim 1984, Pile-Spellman et al. 1984) the perivascular spaces of the adult arachnoidal vessels seem to drain independently through the lymphatic system. The simple structural organization of the embryonic meninges is also progressively transformed to accommodate the vascular modifications (Table 2.1, see Fig 2.13). The three original lamellae of the embryonic meninges become eventually duplicated and distinct tissue spaces are formed between them (Table 2.1). The progressive establishment of different meningeal tissue spaces and their association to its vessels are indicative of the acquisition of important functional roles, some of which are not yet clearly understood. The possible functional roles of these meningeal spaces, their relationships to the perivascular spaces, to the cerebrospinal fluid (CSF) compartments, and to the CSF circulation have recently received the attention of several investigators (Andres 1967a,b, Morse and Low 1972, Nabeshina et al. 1975, Oda and Nakanishi 1984, Krisch et al. 1983, 1984). However, the embryonic timing for the establishment of the various meningeal compartments and their association to the development of the perivascular tissue spaces need to be more accurately determined. Although, the pial vascular plexus is a component of the perineural vascular territory of the CNS vasculature, its embryonic development, composi-

p. 379

-tructural organization, and functional role "e best appreciated in conjunction with the .. . .opment of the interneural vascular territory.

Interneural Vascular Territory of the CMS Vasculature

Interneural Vascular Territory

to the changing external morphology of the CNS surface by capillary angiogenesis and reabsorption. The pial vessels are separated from each other by the cytoplasmic processes of pial cells, by fine collagen fibers, and by tissue spaces (Figs 2.6, 2.7, 2.9). The primitive pial cells are elongated elements lacking distinctive features. They are frequently associated with fine collagen fibers and some contain vacuoles in their cytoplasm (Figs 2.6, 2.7). Embryonic pial cells are specific meningeal elements (Andres 1967a.b. Krisch et al. 1983, 1984). They share features of fibroblasts (collagen formation), of mesodermal cells (phagocytosis), and of epithelial cells (formation of epithelial-like lamellae). Pial vessels have a distinct but thin basal lamina which is lacking in zones of active angiogenesis. The leading endothelial cells of its growing vessels have characteristic features. They show considerable membrane activity with the formation of pseudopodia and fine filopodia which project both inside and outside of their lumina (Figs 2.6, 2.7, 2.9). They are also characterized by a prominent and abundant granular endoplasmic reticulum filled with dense and fine granular material (Figs 2.6, 2.7, 2.9). The accumulation of this dense material often causes dilation of the endoplasmic reticulum. Although, the nature of this dense material remains unknown, its association with the advancing endothelial cells of growing capillaries suggests two possibilities. First, it could represent proteinaceous secretion for the formation of the basal lamina of the newly formed vessel, second, this material could be used in the formation of the first lumina (canalization) between the advancing endothelial cells of a growing vessel (Manasek 1971). Further investigation will be necessary to elucidate the nature of this proteinaceous material and its possible role in embryonic angiogenesis. The surface of the embryonic cerebral cortex is composed of the closely apposed glial endfeet of the marginal glia covered by CNS external basal lamina (Figs 2.6, 2.9). The CNS external basal lamina, together with the marginal glia constitute a distinct anatomical barrier which must be perforated by the pial vessels in order to penetrate the nervous tissue.

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2. Embryology

Vascular Perforation of the CNS Surface by Rial Vessels Recent electron microscopic studies (Marin-Padilla 1985a,b) of the early vascularization of the embryonic cerebral cortex have demonstrated the sequential nature of the vascular perforation of the CNS surface by pial vessels. Three fundamental stages have been demonstrated in this type of vascular perforation. First, the pial vessel approaches and establishes direct contact with the surface of the developing CNS. Then endothelial filopodia from these glia-touching vessels perforate through the vascular and the CNS basal laminae and penetrate into the nervous tissue. The original opening enlarges gradually, thus allowing an entire endothelial cell or cells to penetrate into the nervous tissue. Finally, the proliferation of penetrating endothelial cells results in the formation in situ of new intraneural vessels.

Vascular Approach and Contact with the CNS Surface Embryonic pial vessels are separated from the CNS surface by pial cells, tissue space, collagen fibers and by their corresponding basal laminae (Figs 2.6, 2.7, 2.9). Occasionally, some pial vessels approach and establish direct contact with the surface of the CNS (Figs 2.6, 2.7, 2.9). The endothelium of these glia-touching vessels becomes parallel to the surface of the CNS and their corresponding basal laminae establish direct contacts at some points (Fig 2.6, insert). The only appreciable separation between these vessels and the surface of the CNS is that of their corresponding basal laminae (Fig 2.6, insert). The leading endothelial cells of these glia-touching vessels produce numerous filopodia, which project both inside and outside of vessel lumina (Figs 2.6, 2.7, 2.9). Some of the outside projecting filopodia perforate through the vascular basal lamina and establish direct contact with that of the surface of the CNS (Fig 2.6, insert). This type of vascular contact with the surface of the CNS is considered to be a prerequisite for its subsequent perforation.

Endothelial Filopodia Perforation of CNS Surface The actual perforation of the CNS surface is carried out by the endothelial filopodia of glia-touching pial vessels (Figs 2.7, 2.9). This type of filopodial perforation occurs through areas in which the vascular and the CNS basal laminae are in contact (Fig 2.7). The perforating endothelial filopodia seem to be able to disintegrate (digest) both

References p. 380

basal laminae and to pass through them into the nervous tissue (Fig 2.7). The filopodia enter the CNS tissue usually between adjacent glial endfeet (Figs 2.7, 2.9). The penetrating filopodia advance freely into the nervous substance and are deprived of recognizable basal lamina. This type of perforation can be carried out by several filopodia arriving from the leading endothelial cell or cells of the glia-touching capillary. The glial endfeet between the perforating filopodia often undergo swelling, vacuolization and their membrane disintegrate with the formation of myelin figures (Marin-Padilla 1985b). The endothelial filopodia of growing embryonic capillaries are able to perforate through anatomical barrier and to cause focal disintegration of the membrane of the glial endfeet of the CNS surface. Although the nature of this active process remains unknown, proteolytic enzymes, possibly produced by the endothelial filopodia, could participate in it (Ausprunk 1979). Although filopodia have been described in the leading endothelium of growing capillaries in the CNS (Klosovskii 1963, Bar and Wolff 1972, Wolff et al. 1975, Press 1977) and in a variety of experimental situations (Schoefl 1963, Ausprunk and Folkman 1977, Ausprunk 1979, Madri et al. 1983, Sholley et al. 1984) their possible significance and functional role in angiogenesis have been inadequately investigated. At the site of the perforation the vascular and the CNS basal laminae fuse together around the perforating filopodia (Figs 2.7, 2.9). Their fusion creates a central opening through which the leading filopodia and subsequently the entire endothelial cell or cells are able to penetrate into the nervous tissue. The fusion of both basal laminae thus establishes anatomical continuity between the vessel wall and the surface of the CNS. The fusion of both basal laminae also establishes a shallow "pial-funnel" around the perforating vessels (Figs 2.7-2.9). This embryonic pial-funnel will play a significant role in the establishment of the VRC (Figs 2.8, 2.9).

Fig 2.6 Ultrastructural composition and organization of the pial vascular plexus and upper region of the cerebral cortex of a 12 day old hamster embryo. The pial vessels (*) are of differing calibers and are composed of several endothelial cells joined by tight junctions (arrows). The pial vessels are separated from each other and from the cortical surface by pial cells (F), intercellular spaces and fine collagen fibers. The marginal glia (G) covered by the CMS external basal lamina represents an anatomical barrier which must be perforated by the pial vessels. The pial vessel illustrated near the center of the figure approaches the cortical surface and its leading endothelial cells (1 and 2) have filopodia which project inside and outside its lumen. Some of these filopodia

have established contact with the cortical surface. The endothelium of these glial-touching pial vessels becomes parallel to the cortical surface (insert) and the vascular and CMS basal laminae establish contacts at some points. Some filopodia from this gliatouching pial vessel (insert arrows) have perforated through the vascular basal lamina and have established direct contact with that of the cortical surface. This type of contact between the vascular and the CMS external basal laminae is considered to be a prerequisite for the subsequent perforation of its surface by the pial vessels. Few primitive neurons (N) are recognized in layer I. (From Marin-Padilla, M.: J. сотр. Neu-rol. 241: 237-249, 1985), x5500.

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2. Embryology

References p. 380

Fig 2.7 Detail of the perforation of the cortical surface by the leading filopodium (arrow head) of a glia-touching pial vessel (*). The filopodium has perforated the cortical surface between two adjacent glia endfeet (G). The vascular and the CMS external basal laminae fuse around the perforating filopodium creating an opening through which whole endothe-lial cells eventually penetrate into the nervous tissue. The endothelial cell (E) of the upper pial vessel shows the prominent granular endoplasmic reticulum filled with dense material which characterize those of growing capillaries. Also illustrated are the processes of pial cells (F) and the tight junctions (arrows) of the pial vessels. (From Marin-Padilla, M.: J. сотр. Neural. 241: 237-249, 1985), x7000.

Interneural Vascular Territory Fig. 2.8 Detail of the ultrastructure of the newly formed intracortical capillary depicted in the left lower corner insert. Proliferation of penetrating endothelial cells (insert) results in the in situ formation of new intracortical vessels. At the entrance of the vessel a shallow pial-funnel (arrows) is formed between the fused vascular and CNS external basal laminae. This pial-funnel will elongate accompanying the newly formed intracortical capillary into the nervous tissue. It represents an embryonic Virchow-Robin compartment (VRC) and contains cytoplas-mic processes of pial cells, fine collagen fibers and intercellular tissue spaces around the perforating vessel. The embryonic VRC and its vessels become separated from the nervous tissue by new glial processes (G) which become continuous with those of the marginal glia of the cortical surface. This newly formed glial wall is covered by new basal lamina material which becomes continuous with that of the CNS surface. (From Marin-Padilla, M.: J. сотр. Neurol. 241: 237-249, 1985), хЮООО.

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2. Embryology

References p. 380

Fig 2.9 Schematic drawings illustrating the three fundamental stages of the vascular perforation of the surface of the embryonic cerebral cortex (G) by pial vessels (P). The following stages (from left to right) are illustrated: a) the early endothelial filopodia perforations; b) the endothelial cell perforation and proliferation with the in situ formation of a new intracortical vessel; and c) the establishment of the Virchow-Robin compartment (VRC). The fusion of the vascular and CMS external basal laminae around the perforating vessel and its participation in the formation of both the pial-funnel and the embryonic Virchow-Robin are also illustrated. The composition and organization of the embryonic VRC viewed in longitudinal and transverse (thick arrow) perspectives are also illustrated. The embryonic VRC represents a perivas-cular tissue space (ICS) formed between the vascular and the CNS basal laminae (BL). It contains the perforating vessel (E) with paravascular cells (P) enclosed within its basal lamina (curved arrows), the cytoplasmic processes of pial cells, and fine collagen fibers. The vessels within the VRCs constitute the interneural vascular territory of the CNS vasculature. At various depths into the nervous tissue the VRC closes off with the fusion of the vascular and the CNS basal laminae into a single layer which surrounds and accompanies the penetrating vessels into the CNS substance. Only capillaries arriving from the vessels of the VRC actually penetrate into the nervous tissue proper. They grow actively establishing short-link anastomotic plexuses throughout the nervous tissue. They constitute the intraneural vascular territory of the CNS vasculature. The three insert drawings (А, В, С) illustrate the type of progressive vascularization observed in the developing cerebral cortex. New pial vessels perforate the cortex between previous perforation sites, thus progressively vascularizing the expanding cerebral cortex. The ependymal cell layer (E) with its multiple mitoses is also illustrated. The composition and structural organization of both the embryonic and the adult VRC (compare with Fig 2.10) are essentially indentical.

References p. 380_______________

in Situ Formation of New Intraneural Vessels

outside of and "in between" the nervous tissue proper, and hence, within the embryonic VRC. However, the leading endothelial cells of perforating vessels continue to advance freely, without recognizable basal lamina, into the developing nervous tissue (Fig 2.9). Different stages of vascular perforations are recognized during early development in all regions of the CNS. In the cerebral cortex, new vascular perforations occur during its entire prenatal development. As the cortex expands, new perforations occur between previous ones, following a sequence which is schematically illustrated in Fig 2.9 (A,B,C, inserts). The formation of the embryonic pial-funnel and its role in the establishment of the embryonic VRC are also illustrated (Fig 2.9). Finally, it is important to emphasize that pial vessels always perforate the external basal lamina and marginal glia of the CNS surface to enter the nervous tissue, but do not perforate them to exit. Therefore, it would seem that in the course of embryonic development the direction of the blood flow eventually determines which vessels will be transformed into entering arterioles, and which into existing venules.

Interneural Vascular Territory

37

Establishment of the VRC and Interneural Vascular Territory The early pial-funnel established around the entrance of the perforating vessel, by the fusion of both basal laminae, undergoes significant modifications in the course of embryonic development (Figs 2.8, 2.9). Between the two fused basal laminae a shallow space is formed which communicates with the tissue spaces of the pia mater. This space elongates downward and accompanies the perforating vessel, for a short distance, into the nervous tissue. It is subsequently invaded by pial cellular elements, fine collagen fibers, and nonendothelial paravascular cellular elements (Figs 2.8, 2.9, arrows). Thus, the original pial-funnel is progressively transformed into a distinct perivascular compartment known as the VRC (Figs 2.8, 2.9). The embryonic VRC becomes progressively walled by new glial processes which are arranged in a manner structurally similar to that of the marginal glia of the CNS surface. Therefore, its vessels remain outside of "in between" the nervous tissue proper (Fig 2.9). The embryonic composition and structural organization of the VRC does not significantly change in the course of embryonic development (Fig 2.10). Both, the embryonic and the adult VRC (Jones 1970) have similar composition and overall organization (compare Figs 2.8 and 2.10). However, the early communication of the embryonic VCR with the pial space is eventually obliterated, as recently pointed out by some investigators (Krisch et al. 1983). As the VRC becomes disconnected from the pial space it is transformed into a specific perivascular compartment entirely outside of the nervous tissue proper. The VRC (Figs 2.9, 2.10) is established between the vessel wall and the glial wall of the nervous tissue. Its embryonic vessels are transformed into arterioles and venules which can reach to considerable depths within the nervous tissue, without penetrating the neural parenchyma (Duvernoy et al. 1981). Although the VRC of the cerebral cortex could reach down as far as the white matter, its vessels remain outside and walled between the nervous tissue (Jones 1970). Therefore, the VRC vessels constitute an important and specific vascular territory of the CNS vasculature. This interneural vascular territory must be distinguished from the perineural and the intraneural territories. The perivascular spaces around the VRC vessels are anatomically independent from the meningeal compartments and from the perivascular glia compartment of the perineural and intraneural vascular territories, respectively. The

38

2. Embryology

References p. 3801 Fig 2.10 Ultrastructural composition and organization of a fully developed Virchow-Robin compartment from the cerebral cortex of an adult cat. Its perivascular tissue space (PS) is clearly visible between the vascular and the CNS basal laminae (BM). This space contains the cytoplasmic processes of leptomeningeal (pial) cells (arrows), collagen fibers and the perforating vessels with perivascular pericytes and/or smooth muscle cells (S) enclosed within their basal laminae. Therefore, the basic composition and structural organization of the Virchow-Robin compartment remain practically unchanged in the course of embryonic development (compare with Fig 2.9). (From Jones, E. G.: J. Anat. [Lond.] 106: 507, 1970), X17000: insert) x2500.

drainage of the VRC is also independent from the meningeal compartments. It seems to be connected with the perivascular tissue spaces of the arachnoidal vasculature, and hence with the lymphatic system (Krisch and Buchheim 1984, PileSpellman et al. 1984). The early development of these anatomical differences undoubtedly results in the acquisition of different and specific functional roles for each of three vascular territories which characterizes the CNS vasculature. The establishment (embryonic timing) and the nature of these different functional roles have not been adequately studied. In the course of embryonic development, as the original pial perforating vessels enlarge they become more directly connected with the arachnoidal vasculature. Some adult perforating vessels lose their original relationship with the pial vascular plexus, thus crossing directly from arachnoid

into the CNS (Fig 2.13). Small perforating arteries and veins as well as arterioles and venules are primarily subjected to these developmental modifications (Figs 2.13, 2.14). As the cerebral cortex increases in thickness, the VRC and its vessels elongate vertically, thus maintaining a perpendicular orientation to its surface (Figs 2.9, 2.13, 2.14). The universal perpendicular orientation of the VRC and its vessels to the surface of the cerebral cortex, as well as their considerable depth, can be best appreciated by vascular injections studies (Fig 2.14) such as those described by Pape and Wigglesworth (1979).

p. 380

Intraneural Vascular Territory

39

This classic method deposits fine silver chromate granules within the membranes of various neural elements, including capillaries, rendering them visible against a transparent background (Figs 2.11, 2.12). Intraneural capillary angiogenesis is extraordinary during the early stages of development of the CNS. Growing endothelial cells produce many long and fine filopodia which advance freely without basal lamina among the neural elements (Fig 2.11). These fine filopodia emanate radially from the original endothelial cell and grow for a considerable distance. Their length ranges between 20 to 40 um and their diameter between 0.3 to 0.6 ^m (Figs 2.11, 2.12). Their vessel at the CNS surface (Fig 2.9). The newly size, length, multidirectional growth, and structural penetrating vessels grow actively establishing short- variability can be clearly appreciated in Golgi link anastomotic plexuses throughout the stained preparations (Figs 2.11, 2.12). The fine substance of the developing CNS (Figs 2.11, 2.12, filopodia of growing capillaries seem to search for 2.14). They give rise to the extensive intraneural developmental clues (angiogenetic factors) which capillary bed which characterizes the nervous tissue will determine the directional growth of the parent (Figs 2.12, 2.14). Together they constitute the vessel (Marin-Padilla 1985b). They are also caintraneural vascular territory of the CNS vascula- pable of perforating through anatomical barriers (CNS surface), and of establishing contacts among ture. Although the newly formed intraneural capillaries them during the formation of anastomotic plexgrow freely at first among the nervous elements, uses (Figs 2.11, 2.12, 2.14). Intraneural capillaries they too eventually become surrounded by peri- form short-link anastomotic plexuses throughout vascular glial processes. Intraneural capillaries are the developing CNS (Fig 2.12). It should be surrounded by a single basal lamina (formed by emphasized, that although intraneural capillary the re-fused vascular and the CNS basal laminae) angiogenesis seems to be a random phenomenon, and by a ring of perivascular glia, separating them the formation and location of their anastomotic from other neural elements. The intraneural peri- plexuses is specific, and always associated with vascular glia constitutes also a specific tissue com- actively growing regions of the CNS (Streeter partment which is anatomically independent from 1918, Bar and Wolff 1972, Marin-Padilla 1985b). that of the VRC. Therefore, the circulating blood In the cerebral cortex, the first recognizable through the intraneural capillaries remains sep- anastomotic plexus is the one formed throughout arated from the neuronal elements by a vascular- the paraventricular matrix zone, the first region of the developing CNS to begin differentiation. glial (blood-brain) barrier. As the VRC gradually elongates vertically, its ves- Anastomotic plexuses are subsequently formed in sels continues to give-off new capillaries which Layers I and VII following the formation of the penetrate the CNS substance at different levels cortical plate (Marin-Padilla 1971, 1978). These (Fig 2.14). The number of penetrating capillaries early anastomotic plexuses undergo continuous arriving from the VRC increases in the course of modification and remodelling by both capillary cortical development. These penetrating capillaries angiogenesis and reabsorption. The progressive establish short-link anastomotic plexuses between remodelling of the intraneural plexuses again contiguous VRCs (Fig 2.14). These anastomotic represents an integrative vascular process plexuses also undergo continuous developmental continuously adapting to the growing structural remodelling by capillary angiogenesis and and functional needs of each particular region of reabsorption. The penetrating capillaries and their the developing CNS (Marin-Padilla 1985b). The anastomotic plexuses constitute the intraneural intraneural anastomotic plexuses evolve by the vascular territory of the CNS vasculature and the addition of new links (capillary angiogenesis) only elements to participate in the so-called throughout growing and differentiating zones and by the removal of other links (capillary blood-brain barrier. Intraneural capillary angiogenesis can best be reabsorption) throughout zones in which they are studied with the rapid Golgi method or with similar no longer needed. procedures (Klosovskii 1963, Chilingarian and Paravian 1971, Press 1977, Marin-Padilla 1985b).

Intraneural Vascular Territory of the CNS Vasculature

40

2. Embryology

Capillary reabsorption is observed throughout the developing CNS. In Golgi preparations, it is characterized by the progressive reduction in the size and caliber of the regressing capillary and the

References p. 380 eventual disappearance of anastomotic links (Fig 2.12). The nature of embryonic capillary regression and reabsorption remains poorly understood and also needs further investigation.

Fig 2.11 Examples of intracortical capillary angiogenesis from rapid Golgi preparations of the cerebral cortex of 13 day hamster embryos. Each illustration represents the tip of a growing intracortical capillary. The leading endothelium of growing capillaries produces numerous radiating filopodia which advance freely, without a recognizable basal lamina, among the neural elements. Their number, size, length, structural variability and multidirectional growth can be readily appreciated in these illustrations. x800.

References p. 380

Intraneural Vascular Territory

41

42

2. Embryology

References p. 380

Fig 2.13 Schematic drawings demonstrating the mature lamellar composition and structural organization of themenin-geal, the Virchow-Robin and the perivascular glial compartments of the cerebral cortex. Also illustrated are their corresponding vascular territories, namely: the perineural, the interneural, and the intraneural, respectively. The blood vessels of the perineural (meningeal) and interneural (Virchow-Robin) territories are enclosed within specific perivascular tissue compartments, while those of the intraneural vascular territory are enclosed by perivascular glia. The Virchow-Robin space closes off with the fusion of the vascular and the CNS basal laminae into a single lamina which accompanies the penetrating capillary into the neural tissue proper. The obliteration of the pial (P) space at the entrance of the Virchow-Robin compartment is also illustrated. D = dura mater, NT = neurothelium, EA = external arachnoid lamella, IA = inner arachnoid, lamella, EP = external pia lamella, IP = inner pia lamella, GL = marginal glia, P = pial space, ICR = intercellular compartments. The insert shows the vascular basal lamina and its relationship to the meningeal, Virchow-Robin and perivascular glial compartments, respectively, as well as the location of the various intercellular tissue compartments. (From Krisch, В., Н. Leonhardt, A. Oksche: Cell. Tiss. Res. 238: 459, 1984.)

jferences p. 380

Intraneural Vascular Territory

43

44

2. Embryology

Conclusions The embryonic vascularization of the CNS is characterized by the sequential development of three independent, though interrelated, vascular territories. In order of appearance and development they are: the perineural, the interneural and the intraneural vascular territories (Table 2.2). Embryologically, each vascular territory evolves and remains within a distinct and specific tissue compartment, namely: the meningeal, the Virchow-Robin and the perivascular glial tissue compartment, respectively. In the course of embryonic development, the vasculature of each of these territories undergoes an integrated metamorphosis, continuously adapting to the growing structural and functional needs of each particular region of the developing CNS. This progressive vascular metamorphosis is the result of continuous remodelling of the original anastomotic plexuses in

References p. 380

which both capillary angiogenesis and capillary reabsorption are active processes. The three vascular territories and the different and specific types of vessels that characterize each one can be easily recognized at any time in the course of embryonic development (Fig 2.14). The separation of the CNS vasculature into three different and specific vascular territories and associated tissue compartments implies significant structural as well as functional differences among them. Undoubtedly, a clear understanding of these structural and functional differences is important and relevant both to the clinician and the neurosurgeon. In this context, it is interesting that only the intraneural capillaries and associated perivascular glia (intraneural vascular territory) are actually involved in the so-called blood-brain barrier, since the meningeal and the VirchowRobin vasculatures actually evolve and remain outside of the CNS substance.

Vascular Malformation of the Central Nervous System

45

Refences p. 380

В Vascular Malformation of the Central Nervous System. Embryological Considerations should be of great significance in the study of these malformations to be able to distinguish and to separate their primary or original features from the secondary or acquired ones. Any pathologic alteration (rupture, hemorrhage or thrombosis) of a vascular malformation will not only transform the affected vessels but the sur rounding tissue as well. A reparative inflamma tory process will take place around the affected vessels resulting in fibrosis and or gliosis and more importantly in the obliteration of the perivascular tissue compartment which originally surrounded the vascular malformation. The secondary obliter ation of the perivascular tissue compartment could lead to confusion about the original location of the malformation and the CNS vascular territory ori ginally involved. Furthermore, the inflammatory process around injured vessels of the original mal formation will result in the formation of many new or secondary vessels. The presence of postinflammatory vessels should be recognized because they could also obscure the original architecture of the vascular anomaly. ___________ The recognition of these facts is important because in the interpretation any type of vascular malformation of the CNS the following aspects must be clearly established: a) type of vessels originally affected; b) vascular territory and perivascular tissue compartment originally involved; and, c) original location of the anomaly. The establishment of these facts is sine qua поп for the understanding of the nature of these vascular malformations as well as for the selection of the most ad-equate During the early vascularization of the CNS three distinct vascular territories evolve sequentially. These have been named: perineural, interneural, and intramural vascular territories respectively, because of their specific relationship to the nervous tissue (see Chapter: Embryogenesis of the Early Vascularization of the Central Nervous System). Each of these three vascular territories is characterized by distinct types of vessels and most importantly by a specific perivascular tissue compartment. These compartments are: the meningeal, the Virchow-Robin, and the perivascular glia, respectively. The three basic types of vascular malformations of the CNS will be analyzed separately and correlated embryologically with the vessels of its different vascular territories and tissue compartments. method for their neurosurgical removal.

46

2. Embryology

Capillary Telangiectasias and Cavernous Angiomas Capillary telangiectasias are small vascular malformations composed solely of abnormally dilated capillaries. They vary greatly in caliber and saccular or fusiform dilatations are common. They lack an anomalous arterial supply and their venous drainage may be dilated but not abnormally so. The actual number of capillaries may not be increased in these malformations. The overlying pia mater and arachnoid are normal. The intervening tissue between the dilated capillaries is normal and both glial and neuronal elements are recognized in it. These vascular anomalies are frequently found in the pons, the cerebral cortex, the cortical white mater and rarely in the spinal cord. Capillary telangiectasias rarely show pathologic alterations such as hemorrhages, thromboses or ruptures. Therefore, they are usually clinically silent and most are found by chance at autopsies. Embryologically, these are vascular malformations which involve only the capillaries of the intraneural vascular territory of the CNS and should be enclosed within the perivascular glial tissue compartment. Cavernous angiomas are large vascular malformations composed of cystic vascular spaces lined by a single layer of endothelial cells. These vascular spaces vary greatly in size and are often very irregular suggesting secondary changes. The vascular spaces of these malformations probably represent abnormal capillaries since no recognizable arteries or veins are found in them. These vascular spaces are structurally similar to those found in capillary telangiectasias. These vascular malformations may be circumscribed but not encapsulated and could be lobulated. Like telangiectasias, they lack either abnormal arterial supply or abnormal venous drainage. They are found in the cerebral cortex, the pons and rarely in the spinal cord. Cavernous angiomas invariably show areas of thromboses with subsequent organization, recent and old hemorrhages with hemosiderin laden macrophages, fibrosis and or gliosis, focal calcification and even areas with bone formation. The overlying pia mater and arachnoids are stained, thickened and fibrosed. All of these changes are obviously the result of pathological (secondary) alterations. There is no normal nervous tissue between the abnormal vessels in these malformations, probably because it has been progressively destroyed. Eliminating the prominent acquired pathologic changes, cavernous angiomas could

References p. 380

represent large telangiectasias, an idea which has been often expressed previously (Russell 1931. Russell and Rubinstein 1977). Embryologically, cavernous angiomas can only be large vascular malformations involving the capillaries of the intraneural vascular territory of the CNS since no distinct arteries or veins have been recognized in them. They could represent large capillary telangiectasias with a greater £r_ojpensity_ to undergo pathologic alterations. These alterations will result in the complete obliteration of the perivascular glial compartment and in the progressive reactive fibrosis and gliosis of the intervening nervous tissue causing its complete destruction. The neurosurgical treatment of cavernous angiomas will necessarily involve the removal of some of the normal nervous tissue around the malformation.

Venous and Arteriovenous Malformations Venous malformations are vascular anomalies composed solely of abnormally dilated and tortuous veins. They may be composed of a single greatly dilated and tortuous vein or of small number of them. They involve primarily the pia-arachnoidal veins and few of its intramedullary tributaries. They can be located in the spinal cord, and occasionally in the drainage territories of the vein of Galen and of the cerebellum. Secondary pathologic alterations including muscular hypertrophy and or hyalinization (fibrosis) of the vessel wall, and thromboses with subsequent organization are frequent findings in these malformations. However, more important alterations are those caused by the compression of the spinal cord by the anomalous veins, and the compression of the nervous tissue by the dilated intramedullary tributary veins. Cord atrophy and ischemic changes are often sequelae in long standing cases. Embryologically, venous malformations are developmental anomalies which involve primarily the veins of the perineural vascular territory of the meningeal (pia-arachnoid) tissue compartment, and also some tributary veins of the interneural vascular territory of the Virchow-Robin tissue compartment. Therefore, uncomplicated venous malformations should be entirely outside the nervous tissue proper and hence liable to their complete microneurosurgical removal. On the other hand, secondary pathological alterations affecting these venous malformation will result in the obliteration of their perivascular tissue compartments

References p. 380

making their neurosurgical treatment more difficult requiring the removal of some of the surrounding unaffected nervous tissue. Arteriovenous malformations are large and complex vascular anomalies composed of abnormally developed arteries and veins. They involve primarily the vessels of the leptomeninges with extension into the fissures and sulci. They could also involve deeper vascular territories of the cortex, midbrain, cerebellum and choroid plexuses. These vascular malformations are also character-ized d by the participation of regional perforating vessels which could also be abnormally developed, tortuous and dilated. The presence and location of the abnormal perforating vessels should always be explored because they could be the cause of serious damage to the nervous parenchyma and must be treated adequately during the micro-neurosurgica[ removal of the malformation. The main arteries and veins leading to and from the malformation are usually dilated and a secondary collateral circulation could be prominent in some of them_______________________ Arteriovenous malformations are subject to pathologic alterations including: ruptures, hemorrhages, trombosis, atrophy, and progressive reparative fibrosis and or gliosis. The arach noid around the malformation as well as the underlying or adjacent nervous tissue show rusty pigmentation and fibrosis or gliosis. Microscopic examination of both the arteries and the veins of these malformation show abnormalities involving their elastic and muscular elements. Some vessels also show atheromas, organized thrombus, focal calcifications and postinflammatory fibrosis or gliosis.

Sturge-Weber-Dimitri's Disease This congenital vascular malformation is characterized by an increase in the number of capillaries and of few small veins throughout the affected pia mater and underlying surface of the cerebral cortex ._ This extensive capillary-venous cerebral malformation is associated with a homolateral cutaneous angioma over the trigeminal nerve distribu-tion. This vascular malformation is also characterized by significant pathologic alterations, severe damage to the nervous parenchyma, and abua-dant mineral granular deposition of calcium and iron. While a pial capillary plexus is a prominent feature during the embryonic vascularization of the CNS, the adult cortical pia mater either lacks or has very few capillaries (Duvernoy et al. 1981). Embryologically, the persistence of the embryonic pial vascular plexus with its numerous connections to the superficial cortical vasculature could explain this type of vascular malformation. There is no adequate neurosurgical treatment for this fortunately rare condition.

Исправленная стр 47

Embryologically, these malformations involve: a) vessels (arteries and veins) from the perineural vascular territory of the CNS within the meningeal tissue compartment; and b) some perforating or emerging vessels (arterioles or venules) from the interneural vascular territory within the VirchowRobin tissue compartment. Therefore, unaffected arteriovenous malformations should lie outside of the nervous tissue proper and should be liable to complete removal by microneurosurgery. On the other hand, in arteriovenous malformations which have undergone pathologic alterations, the meningeal and Virchow-Robin perivascular compartments might be obliterated making their microneurosurgical treatment more difficult since it must involve the removal of the surrounding nervous tissue.

49

3

Pathological Considerations

Pathogenesis The pathogenesis of angioma is generally attributed to maldevelopment of the cerebral vascular system occurring during the second to fifth stage of Streeter's craniocerebral vascularization. However, the underlying anomaly ultimately responsible for the vascular malformation still remains a matter of controversy. Old hypotheses assumed that embryologic fore-runners_of arteries and veins were separate. Based on meticulous injection techniques Evans (1911) was the first to show that a primary vascular plexus existed as a capillary network, preceding the more definable vascular system. In a prgcess called metamorphosis, fusion of some of the channels of this primordial vascular plexus and dissolution of others takes place and ultimately leads to the differentiation of arteries and veins (Dandy 1928). This process of angiogenesis is controlled by hemodynamic and genetic factors. There is a steady development, not only of the arteries and veins, but also of the capillaries during successive embryological development phases. All investigators concerned with the problem of pathogenesis of cerebral vascular malformations uniformly accept that an error of development occurs during this very early metamorphotic phase. Dandy (1928) postulated a retentiqn,of primordial vascular connections between arteries and veins. Olivecrona and Ladenheim (1957) assumed an embryonic agenesis of the capillary system, ultimately resulting in discharge of arterial blood directly into the venous system through a tangle of abnormal vessels of varying caliber. A concept basically similar to that of Dandy was introduced by Kaplan and Meier (1958). Based on observations made in specimens obtained at autopsy, they concluded that arteriovenous malformations within the cerebral hemisphere represent a perpetuation of a primitive arteriovenous

communication, which otherwise would be replaced by an intervening capillary network during the normal embryological development of the cerebral vascular system. Hamby (1958) approached the problem from a hemodynamic jtandpoint, concluding that the basic characteristic of arteriovenous malformations is a lack of vascular resistance in the area involved by the lesion. Since the normal cerebral vasculature resistance is provided by the capillary bed, Hamby's concept is similar to that of Olivecrona and Ladenheim and based on the agenesis of capillaries.________________ ______ Gold et al. (1964) and Lagos (1977) recognized two types of vascular malformation: 1) a direct end-to-end anastomosis between the arteries and veins of normal structure, representing arteriovenous fistulae and 2) a network of poorly differentiated and immature vessels interposed between the arterial and venous system, representing typical arteriovenous malformations,________ Stein and Wolpert (1980) and Warkany et al. (1984) assumed an arrest of normal development of primitive arteries, capillaries and veins, resulted in the formation of direct arteriovenous communications through immature, poorly differentiated vessels, without an intervening capillary bed. Parkinson and Bachers (1980) maintained that the essential feature of arteriovenous malformations is a shunt responsible for the short-circuiting of the arteriocapillary bed and proposed the descriptive definition of a "congenital arteriovenous fis-tulous malformation" occurring as a consequence of a local angioblastic error. Based on Sabin's (1917) original concept of the development of the primitive vascular plexus, Garretson (1985) recently proposed that AVMs arise from persistent direct connections between the future arterial and venous sides of the primi-

50

3. Pathological Considerations

tive vascular plexus, with failure to develop an interposed network. In summary, most of the theories developed to explain the origin of cerebral vascular malformations have in common the hypothetical concept of total agenesis, or poor development of the capillary network. It is known, however, that normal angiogenesis takes place in a capillarofugal direction and that the predisposing factor for the formation of arteries and veins lies within this primordial capillary network. If there is a primary agenesis of the capillary network and therefore of the driving force for the development of arteries and veins, then this territory must be ultimately avascular. If, however, the theory of primary capillary agenesis is not correct, one must assume a secondary destruction or disappearance of capillaries, in order to explain the absence of a capillary network as the pathogenetic mechanism for vascular malformations. Such a secondary destruction would have to occur through the action of a factor having the capacity to destroy capillary vessels after arteries and veins have been formed from them. In such a situation the arteries and veins would then form

direct communications. Fig 3.1A-G Artist's drawing of the different types of cerebral vascular malformations. A Arterial malformation.

В Arteriovenous fistulous malformation.

С Arteriovenous plexiform malformation. D Arteriovenous plexiform micro-malformation. E Cavernous malformation. F Capillary malformation (telangiectasia).

G Venous malformation.

References p. 381

A capillary destroying factor has not yet been found. Also, if this theory of secondary destruction of capillaries is correct, one would expect to see only cases with direct arteriovenous fistulae. rather than all the commonly known varieties of AVMs in which coiling convoluted vessels are interposed between arteries and veins. For this reason it seems appropriate to discuss another hypothesis: There is neither a primary agenesis nor a secondary destruction of capillaries, but a local or regional disease of capillaries. In a given primitive vascular territory, the normal development of capillaries is disturbed, however, these capillaries do not disappear entirely, but proliferate and thereby develop metamorphotic. dysplastic vessels (Luschka 1854. Dandy 1928). This disease may be defined as a 'proliferalive capillaropathy' of unknown origin (Fig 3.1). It isi characterized by maldevelopment of an area of the primordial capillary plexus into metamorpho-tic vessels. These vessels do not fulfil thejiistolog-ic criteria of arteries, jveins or capillaries. It is, in fact, well known, that it is difficult if not impossible to typify histologically the vessels comprising the core of a vascular malformation. These vessels

Terences p. 381

have been called "unidentifiable type of vessels" by Hamby (1958) (Fig 3.2) and "structural hybrids" by Burger and Vogel (1976). In a histologic study of three cases of arteriovenous malformations, Sorgo (1938) classified the vessels constituting the malformation into three main types, according to the composition of their wall. He also found similarities between the wall [of vessels composing arteriovenous malformations and the wall of normal embryonic vessels. Based on bis observations he postulated that at least one of the described types of vessels may well arise from capillaries. The results of recent electron microscopic studies are in accordance with our proposed concept. Meyermann and Yas,argil (1981) found that the ultrastructural composition of small vessels of 41 surgically obtained arteriovenous malformations could be divided into two distinct types; vessels with a closed and vessels with a fenestrated endothelial cell layer. This second type of vessel, char-

Pathogenesis

51

acterized by a fenestrated endothclial coat is clearly abnormal, since fenestrations of endothelial cells do not occur in the normal brain vasculature with exception of the area postrcma, choroid plexus, pineal and pituitary glands, intercolumnar tubercle, and certain nuclei within the hypothalamus (Lee 1971). Another observation of this study was the sprouting of new capillaries in the fibrotic arachnoid surrounding superficial pathological vessels. This finding supports the concept of a proliferative capillaropathy (Figs 3.3, 3.4). Depending on the extension and distribution of the capillary disease involving the primitive vascular plexus, vascular malformations may therefore be defined as localized, multiple or diffuse collections of metamorphotic vessels, abnormal in number, in structure and in function. ______ The result of this primary disease of capillaries is a mal-production and therefore a mal-formation of both arteries (or arterioles) and veins (or venules), i.e. a metamorphotic angiodysplasia or capillaropathy.

52

3. Pathological Considerations

References p. 381 Fig3.3A-B A Sinusoid-type vessels of AVMs are coated by fenestrated endothelial cells. The fenestrae are indicated by arrows. In the normal cerebral vas-culature this type of endothelial coat is only present in certain distinct areas of the CNS. The cytoplasm of the endothelial cells is filled with cross-sectioned filaments and some vacuoles. The arrowhead indicates a so called Weibel-Palade body. This organelle can only be found in endothelia, and is a rare feature in a normal cerebral vessel wall. Bar = 1 цт В Although some gaps in the endothelial cell layer of AVM are demonstrated as in A, some cell contacts of adjacent endothelia are tight as seen in normal cerebral vessels. Bar = 1 |im. By courtesy of Dr. R. Meyer-mann. Fig 3.4 Arteriovenous malformation surgically resected from the left occipital lobe of a 24 year old female patient (see Fig 3.78). Note the considerable variation of vessel size with dilated, partially arteria-lized veins (V) and occasional small arteries (arrow). In the lower half malformed compact vessels with little or no intervening parenchyma prevail, thus resembling a cavernous angioma (Elastica van Gieson, x10). By courtesy of Prof. P. Kleihues, Zurich.

p. 381

Terences p. 381

chyma between the vascular spaces of the malformation, and 3. the state (normal or gliotic) of the intervening neural tissue. Based on these morphological parameters vascular malformations are divided into four main types: 1. arteriovenous malformations 2. venous malformations 3. cavernous malformations and 4. capillary malformations (or telangiectasias) (McCormick 1966).______ Despite this attempt to separate various different forms, certain observations support the hypothesis of a single underlying primary lesion. Transitional forms exhibiting the histologic char-acteristics of more than one of the above men-tioned types are sometimes encountered within the same malformation. It is, in fact, difficult to distinguish histologically between telangiectasia and venous angioma. Also telangiectasias have been reported to be a component of venous angio-mas (McCormick 1966, Manuelidis 1950). Combinations of cavernous and telangiectasias (Roberson et al. 1974), as well as venous angio-mas and arteriovenous malformations (Huang et al. 1984), have been reported to occur within the same malformation. Also multiple lesions of different histologic types can occur in the same individual (McCormick 1966). Although absence of capillaries has usually been described as the hallmark of arteriovenous malfor-

Pathogenesis

53

mations, abnormal proliferation of capillaries may be observed within the malformation or even in adjacent tissue. Hamby (1958) in a unique histologic study of a specimen of an arteriovenous malformation of the brain, demonstrated not an agenesis or absence of capillaries, but a multitude of different types of capillary-like vessels, clearly distinguishable from the entering arteries and the draining thin-walled tortuous veins. These capillary-type vessels found in the central core of the malformation form a complex of coiling and intercommunicating vessels (see Fig 3.2). Dilated capillaries or capillary-like spaces are found in telangiectasias, which are therefore also called capillary malformations, as well as in cav-ernomas (Huang et al. 1984). By the same reasoning certain vascular malformations of the subcutaneous tissue are also called capillarovenous malformations (Merland et al. 1983). In histologic studies of Cabanes et al. (1979) cases of venous angioma with a clear participation of capillaries are demonstrated.

54 исправленная Considerations

3. Pathological

We should also, perhaps, remember Virchow's statement of 1851 - that "one type of angioma can transform into another by changes in flow and pressure or by cellular proliferation". Histologically, the presence or absence of inter vening neural parenchyma, as well as its state (normal or gliotic) are used as parameters for clas sifying vascular malformations. Usually, arteriovenous malformations surround gliotic tissue, ve nous malformations and telangiectasias have nor mal intervening tissue, and cavernous malforma tions contain no intervening parenchyma. Both histologic studies and intraoperative observations show, however, that an intervening neural paren chyma and even gliosis within it may occur with all types of cerebral vascular malformations. Cavernous malformations are classically described as being compact, with the vascular spaces being contiguous with one another and lacking interven ing tissue. During operation on such lesions, however, one may observe through the operating microscope, small cavernous spaces located at the periphery of the mass and being clearly separated from it by brain parenchyma. ви; In a histologic study, Manuelidis (1950) clearly demonstrated neural tissue between the vascular spaces of an otherwise typical case of cavernous angioma. A finding common to all types of cerebral vascular malformation is spontaneous thrombosis, occurring most frequently in the venous space of the lesion. Although such spontaneous thromboses have been most often reported in cases of true AVM, they clearly also occur with the other types, especially venous and cavernous malformations. The histological character of the resected lesions and the relative frequency are given in Table 3.3. Table 3.3

Histological findings in 398 AVMs

Mixed type

374 cases

(94.0%)

More arterial

12 cases

( 3.0%)

More venous

1 2 cases

( 3.0%)

398 cases Not investigated 16 galenic and 2 fistulous lesions.

Hemorrhage, which most frequently occurs in arteriovenous malformations, may also be observed with other types of vascular anomalies. Microscopic hemorrhages with foci of hemosiderin laden macrophages are frequently found in arteriovenous malformations, but may also be seen in venous, cavernous and even capillary-type malformations.

From these pathologic-anatomic observations it becomes evident that cerebral vascular malformations have characteristics in common with respect to their histologic nature, their vascular composition, and regressive changes, irrespective of their type. Using cerebral angiography, the different morphologic types of vascular malformation described above can usually be distinguished (Tables 3.2, 3.4). Arteriovenous malformations typically appear during the arterial phase of the angiogram and are characterized by large feeding arteries, a more or less compact conglomeration of coiled vessels and prominent draining veins. Venous angiomas most frequently appear during the venous phase and are characterized by numerous dilated, linearly arranged medullary veins, producing an umbrella-shaped configuration and converging towards a markedly dilated central paren-chymal vein. Cavernous angiomas may cause an avascular mass effect, but remain invisible with usual angiographic techniques, owing to their slow circulation and the lack of prominent feeding arteries. A blush, representing pooling of contrast material within the vascular spaces of the lesion, may however appear, if either prolonged injection angiography (Numaguchi and Nishikawa 1979) or a repeated injection series (Huang et al. 1984) is performed. In telangiectasias, angiography is usually negative, owing to their small size and their slow circulation time. Occasionally, however, telangiectases may show a small stain or blush during the venous phase of the angiogram (Huang et al. 1984). Although the different morphologic types of cerebral vascular malformation are distinguishable on angiography, certain observations support the concept of a single underlying cause, common to all types of vascular malformation. One may occasionally demonstrate both transitional forms as well as the coexistence of two or more different types of lesion within the same vascular malformation. A pure venous type of malformation was demonstrated angiographically in 1958 by Krayenbuhl and Ya§argil. The histological examination showed no arterial component in the lesion (Fig 3.5). According to Huang et al. (1984) 14% of cases of venous angioma contain fine arteries which form a reticular blush in the arterial phase of the angiogram. This indicates the presence of an arterial or low-flow arteriovenous component in certain venous angiomas. It clearly contradicts the classical definition, according to which venous angiomas lack arteriovenous shunts or an arterial component and become visible only in the late venous phase of the angiogram. Similar observa-

Pathogenesis

References p. 381

55

Fig 3.5 A-C This may be the first angiography demonstration of a venous angioma. (54 year old male presenting with subachnoid hemorrhage. From Krayenbuhl, H., M. G. Ya§argil: Series Chirurgia Geigy 4: 76 1958.) A normal arterial phase of carotid angiography. В Venous phase of carotid angiogram after a SAH shows the lesion in the right temporal lobe. It drains into the dilated basal vein of Rosenthal. In 1958 this malformation was called "Arteriovenous malformation visible only in the venous c Histological examination shows venous malformation with arterial components. mal veins adjacent to the angioma are hypoplastic or even absent and that the adjacent superficial or cortical veins may be poorly developed. Also hypoplasia of the internal cerebral veins, poor development or even absence of certain major subependymal veins and a paucity of superficial cortical veins have occasionally been observed" (Huang et al. 1984). Veins pursuing an unusual course, most probably representing persistent fetal or intrauterine venous structures, are frequently observed angiographically in such cases (Huang et al. 1984). Similar anomalies of the venous system may also be observed in cases of arteriovenous malformation. Unfortunately, angiographic study of the venous drainage patterns of cerebral vascular malformations has been generally neglected (see below). Review of our own angiographic material disclosed an unsuspected 30% incidence of associated anomalies in the venous drainage system of AVMs similar to those reported to occur with venous angiomas (see Vol. Ill B, Table 9.2). Our own operative findings have also demon-

56

3. Pathological Considerations

strated clear overlaps of histological types of malformation within single lesions. There have been AVMs with a predominance of arterial or venous components, cavernous malformations with definite feeders bearing aneurysms, capillary caverno-mas with no visible arterial or venous connections and virtually isolated from surrounding tissue by firm encapsulation, and venous malformations with arterial components found at operation and confirmed histologically but which could not be demonstrated angiographically. Upon comparing the clinical features of the different types of cerebral vascular malformation, it becomes evident, that with the exception of a bruit and some symptoms associated with steal phenomena, which exclusively occur with certain high-flow arteriovenous malformations, all other symptoms such as epileptic seizures, hemorrhage, progressive neurological deficit, and headache, may occur with any type of vascular malformation albeit with some variations in incidence (Table 3.5). There is therefore pathological, anatomical, angiographic, surgical and clinical evidence for a common underlying pathogenesis of all forms of

References p. 381

cerebral vascular malformation, based upon a disease of capillaries. The seemingly distinct forms of cerebral vascular malformation described by pathologists, diagnosed angiographically by neu-roradiologists and operated upon by neurosur-geons represent nothing more than different manifestations of the same disease. This concept supports the theory of van Bogaert (1935), who doubted that the different types of cerebral vascular malformations represent different disease entities,and expressed the opinion that there is only one Angioma-Disease (maladie angiomateuse) with a variety of subgroups. He was able to explain the pathogenesis of this disease by assuming a disturbance in the development of small vessels as the underlying mechanism.

Nomenclature

57

Case 3.5 Clinical features of the different types of cerebral vascular malformations AVM

Venous malformation

Cavernous malformation

Telangiectasis

Patology

Usually gliotic brain parenchyma, but not in compact AVM-cases

Usually normal brain parenchyma

No intervening brain parenchyma

Usually normal brain parenchyma

Patogenesis

Cong. agenesis of capillaries?

Agenesis of connecting Sinusoid change of Dilatation of capillaries venous segment! capillary-venous system

Localiization

Every layer, every site

Cerebral, cerebellar

Everywhere, extrinsic, intrinsic

Rons >

Heredity

Seldom (7 cases in literature)

?

Seldom

?, Rendu-Osler

Unknown

Unknown

?

?

?

7

Associated Seldom Malformatio ns Sex Male > female 1.4 = 1 Age

20-40 years, children seldom

Middle age, children rarely

Middle age

Middle or old age

Multiple

Seldom

Solitary

Solitary > multiple

?

Aneurysm

10%

7

?

1 case (own)

Size

Occult — > giant

Small - large strip

Ovoid 2-5 cm

Very tiny

piape

Spider-, wedge-shaped

Umbrella-, medusaHoneycombed, shaped, mushroom-like mulberry-, raspberrylike

Petechial

binic

Silent = stormy

Silent = acute

Silent = acute

Silent = acute

Skull x-ray Calcification (rare) Calcification (except.) Calcification frequent CT Small > Small > Micro > Small > Small > Small > + + + rarely "blush" MRI Angiography

Occult Occult Occult Occult

Atemodynami Volume increased > c Speed increased >

Normal Normal

Normal Normal

Classification of Vascular Malformation "The classification of the vascular malformations of the brain has been the subject of considerable discussion and the extensive literature on this topic reflects a varying and, at times, confusing nomenclature." (Bebin and Smith 1982, p. 13). The confusion continues and applies not only to vascular malformations of the brain but also to those of all other organs. We agree with Mulliken 11983) "the words to describe the common vascular birthmarks reflect our ignorance of their pathogenesis". There are majors problems with both nomenclature and classification.

Normal Normal

Nomenclature A. Both Greek and Latin roots are used: Vascular malformation (Latin roots), Angiodysplasia (Greek roots). B. The suffix oma (= neoplasm) is commonly used not only for true vascular tumors such as hemangioblastoma, but also for vascular malformations. The use of the suffix osis (e. g. "angiomatosis") has sometimes been inappropriate. The term should be reserved for diffuse or multiple lesions only.

58

3. Pathological Considerations

At the present time the English version of "malformation" has found general acceptance and there is little point in entering further into sophisticated linguistic struggles. Classification As ever more sophisticated means of studying vascular malformations have developed, systems of classification have diversified from the early descriptive terms based purely on gross morphological observation. In some instances, old terminology has been retained, in others changed and in yet further (often simultaneous) publications regrouped under different headings. Noran presented and discussed all the proposed classifications in the literature up to 1945 and concluded: "a comprehensive evaluation of the literature is warranted in order that one may arrive at some correlation between these various nomenclature and classification." Within the last 40 years further new concepts have been proposed. Table 3.6a contains some of the more notable historic and modern classifications, and shows the development of thinking regarding the malformations. Virchow (1863) conducted his own thorough studies and described 4 main types of malformation and stated, as early as 1851: "one type of angioma can transform into another by changes in flow and pressure or by cellular proliferation." The venous anomalies, and plexiform angioma of Dandy's classification (1928) would nowadays be called AVM, and the cyst with angioma in the wall a hemangioblastoma. We assume that he did not describe any "venous angiomas" as now recognized by Huang et al. (1984) and McCormick (1985).

References p. 3821 Table 3.6a Virchow (1863) 1. Angioma simplex Telangiectasia (can change to cavernoma) 2. Cavernous angioma 3. Racemous angioma a. Arterial (aneurysma anastomoseon) b. Venous angioma c. Arteriovenous aneurysm 4. Lymphangioma Dandy (1928) 1. Angioma a. Cyst with angioma in the wall (actually angioblastoma) b. Cavernous angioma c. Plexiform angioma (nowadays a form of AVM) 2. Arteriovenous aneurysm (nowadays a form of AVM) 3. Venous abnormalities (nowadays also AVM) Gushing - Bailey (1928) 1. Hemangioblastoma (true neoplasm) a. Cystic b. Solid a capillary (3 cellular у cavernous (nowadays = cavernous angioma) 2. Angiomatous malformation a. Telangiectasias b. Venous angiomas c. Arterial or arteriovenous angiomas (AVM) Bergstrand - Olivecrona - Tonnis (1936) 1. Angioma cavernosum 2. Angioma racemosum a. Telangiectasias b. Angioma capillare et venosum calcificans (Sturge-Weber disease) c. Angioma racemosum arteriale d. Angioma racemosum venosum e. Aneurysma arteriovenosum 3. Angioblastoma, angioreticuloma or Lindau tumors 4. Angioglioma (!) Turner - Kernohan (1941) (spinal cord) 1. Vascular malformations a. Telangiectasia b. Angioma or hamartoma a angioma venosum P angioma arteriovenosum or Y angioma arteriale 2. Vascular neoplasms a. Capillary a capillary hemangioma |3 hemangioendothelioma Y capillary hemangioblastoma b. Cavernous a cavernous hemangioma p cavernous hemangioblastoma c. Hemangiosarcoma

p. 382

Classification

59

Table 3.6a Continuation

Wyburn-Mason - Holmes (1943) (spinal) 1. True tumors a. Hemangioblastoma a angioreticuloma P extradural hemangioblastoma 2. Malformations a. Telangiectasia b. Venous malformation a secondary venous anomalies (3 venous angioma c. Arteriovenous angioma d. Arterial anomalies Menuelidis (1950) 1. Telangiectasia a. Primary b. Secondary 2. Cavernous hemangioma 3. Venous hemangioma 4. Arteriovenous hemangioma Zuich ( 1 9 5 1 ) 1. Angioreticuloma 2. Malformation a. Cavernous angioma b. Racemous capillary angioma (telangiectasia) c. Capiliar et venous angioma (Sturge-Weber) d. Venous angioma e. Arteriovenous aneurysmatic angioma Asenjo (1953) I. Congenital lesions A. Expansive malformation a. Arteriovenous aneurysm b. Arterial racemous aneurysm c. Venous racemous aneurysm B. Angiosis d. Congenital arterial aneurysm e. Meningeal varix f. Sinus pericranii II. Acquired lesions A. Aneurysms a. Arteriosclerotic b. Mycotic c. Syphilitic B. Carotid-cavernous fistula C. Traumatic aneurysms II. Tumors A. Hemangioblastoma a. Benign b. Malignant B. von Hippel-Lindau disease C. Angiomatous meningioma

Pluvinage (1954) I. Angioreticuloma II. Angioma 1. a. Cavernous angioma b. Telangiectasia 2. Sturge-Weber 3. Venous angioma a. Cerebral varix b. Racemous venous angioma c. Peleton de veines (!) 4. Arterial angioma a. Racemous arterial angioma b. Arteriovenous aneurysm Olivecrona - Ladenheim (1957) Etiology 1. Acquired 2. Congenital a. Anomalous arteriovenous b. Angiomatous arteriovenous Pathology 1. Cavernous 2. Racemous a. Telangiectasia b. Sturge-Weber c. Venous racemous d. Arterial racemous e. Angiomatous arteriovenous Russe/ - Rubinstein (1963) 1. Hemangioblastoma 2. Vascular malformation a. Capillary telangiectasia b. Cavernous angiomas c. Venous and arteriovenous malformation McCormick (1985) (in Fein and Flamm) I. Angioblastoma Angiomas 1. Venous angiomas 2. Capillary angiomas (telangiectasias) 1 1 2 cases 3. AVM 41 cases 4. Cavernous angiomas 5. Transitional 11 cases 5 cases Classification of Plastic Surgeons Kaplan 4 cases (1983) A. Stage 1 (undifferentiated capillary network) 1. Capillary hemangioma 2. Cavernous hemangioma B. Stage 2 (retiform plexus) 1. Diffuse microfistula 2. Localized macrofistula

60

3. Pathological Considerations

References p. 382

Table 3.6a Continuation

C. Stage 3 (mature vascular malformation) 1. Venous hemangioma 2. Venous hypoplasia (Klippel-Trenaunay syndrome) 3. Hemangiolymphangioma (vascular hamartoma) Spira (1983) A. Benign hemangiomas 1. Typical a. Capillary hemangioma b. Cavernous hemangioma c. Mixed-combined hemangioma d. Port-wine stain - nevus flammeus e. Angioma racemosum f. Angiokeratoma (Mibelli) 2. Atypical a. Sclerosing hemangioma b. Pyogenic granuloma c. Spider telangiectasia (nevus araneus) d. Glomus tumor e. Hemangiopericytoma f. Juvenile nasopharyngeal angiofibroma g. Venous lakes B. Syndromes - diseases 1. Rendu-Osler-Weber syndrome 2. Sturge-Weber-Dimitri syndrome 3. von Hippel-Lindau disease 4. Maffucci syndrome 5. Blue Rubber Bleb syndrome 6. Kasabach-Merritt syndrome 7. Klippel-Trenaunay syndrome C. Malignant hemangiomas 1. Angiosarcoma 2. Kaposi sarcoma 3. Dermatofibrosarcoma protuberans Classification of Neuroradiologists Merland et a/. (1983) 1. Pure arterial dysplasia (2 cases) 2. A-V dysplasia (macroscopic shunt) a. Simple direct A-V fistula vertebra-vertebral, vertebra-jugular carotido-cavernous, carotido-jugular b. A-V malformation (60 cases) 3. Capillary and capillary-venous malformation (26 cases) a. Pure capillary (Rendu-Osler) b. Capillary-venous malformation

4. Venous and cavernous ectasias (100 + 4 cases) 5. Additional types a. Unmature angioma of the newborn b. Portwine stain angioma c. Unusual angiomas Hemodynamic Classification 1. Active (large blood flow, direct A-V fistula) high flow 2. Inactive vascular

Huang et al. (1984) I. Those that involve feeding arteries and draining veins (easily demonstrable angiographically) 1. Superficial type (pial or superficial AVM): involving mostly the cortical gray matter (and subjacent white matter) 2. Deep or central type (deep or central AVM): involving the subcortical (or central) gray matter and the adjacent white matter 3. Medullary type (AVM with a medullary component): involving primarily the medullary arteries and veins Classical pyramid-shaped AVMs are mostly a combination of the superficial type and the medullary type II. Those that primarily involve capillaries 1. Cavernous capillary malformation 2. Rendu-Osler-Weber disease 3. Louis-Bar syndrome III. Those that primarily involve veins 1. MVM a. Without an arterial component. Sturge-Weber disease should also be included here b. With an arterial component. (This should not be confused with an AVM with medullary component) 2. Cavernous venous malformation 3. Phlebectasia or varix (most of these cases, if not all, are MVMs) IV. Any combination of the above

References p. 382

Gushing and Bailey (1928) were the first to separate two groups: I. Angioblastoma (true neoplasm), II. Angiomatous malformation. They did not consider cavernous angioma as a separate entity and listed it under angioblastoma. Their venous angiomas would be called AVMs today. Bergstrand et al. (1936) added to the neoplastic £roup the angiogtioma of Roussy and Oberling. These are to a large degree still not accepted, yet appear to have been occasionally identified (Bon-nin et al. 1983). Bergstrand doubted the existence of a true arterial aneurysm as described and illustrated by Simmonds (1905) (Figs 3.5, 3.6).

Classification

61

Huang et al. (1984) noted the wide acceptance of Russel and Rubinstein's (1963) classification. However, they pointed out the disadvantages of attempting to differentiate histologically between many cavernous venous malformations and venous angiomas and showed that some areas within venous angiomas may be similar to capillary malformations or even an AVM. The classification of Huang et al. has put forward new and important elements for consideration. We include the classification of Merland et al. (1983) as a very stimulating view of the external angiomas, seen from the perspective of the inter-ventional neuroradiologist. The classification of Kaplan (1983), Spira (1983) show up the similar problems experienced by plastic surgeons in describing cutaneous malformations.

The Author's Classification Our own classification is based on the relative preponderance and contribution of the various vascular elements, arteries, veins, capillaries» and abnormal channels (Table 3.6c). There may run a spectrum from theoretically completely arterial lesions to completely venous lesions and from large fistulae to extensive convoluted vessels. While the lesions can conveniently be grouped into four primary headings, there are at each level examples of transitional lesions, e.g. AVMs with slow flow or venous malformations with increased flow. Part of the definition of the lesion must rest with dynamic properties related to flow and shunting, which cannot be examined by the pathologist in the resected specimen or at autopsy. We propose the following classification more for practical use in ncuroradiology, neurology and neurosur-gery but hope that neuropathologists will be stimulated to undertake further investigation of these lesions.

62

3. Pathological Considerations

References p. 382

Table 3.6c Authors classification I. Vascular neoplasms 1. Hemangioblastom a a. Cystic b. Solid 2. Angioglioma (mixed and glioma)

hemangioblastoma

3. Angioblastic meningioma 4. Hemangiopericytic meningioma (hemangiopericy-toma of the meninges) 5. Angiosarcoma II. Malformations 1. Telangiectasia 2. Cavernous malformation a. Intrinsic b. Extrinsic 3. Venous malformation a. Cortical b. Subcortical (medullary) a superficial p deep 4. Arteriovenous malformation a. Plexiform (dilated, tortuous pathological vessels with thickened or thinned (or combined) walls, arteriectasia, aneurysms, phlebectasia, varices; they can be cryptic, occult, micro, moderate, large or giant in size. They may be uni- or multilocular. They may have a mono-nidus with mono- or multi-compartments) b. A-V Fistula (direct communication between arteries and venous channels (veins and sinuses) without the interposition of a convolute, a simple: - carotid = cavernous, carotid = jugular, - MCA = v. Labbe or v. Trolard or Sylvii, - АСА = inferior sagittal sinus, - pericallosal artery = v. Galen, - PCA = v. Galen, PCA - transverse or sigm. sinus, - vertebro = vertebral, vertebro = jugular, - AICA = lateral rec. vein or petrosal sinus, - SCA = transverse sinus, - basilar artery = galenic vein P complex: pericallosal + PCA + MCA = v. Galeni, - MCA + dural branches = herophilic sinus or SSS, - PCA + dural branches = herophilic sinus or transverse sinus.

c. Transitional type between a-c a more fistula > less plexiform (network) p more network > less fistula 5. Transitional malformations Combinations 1+2, 1+3, 2+3, 1+2+3, 3+4 (Huang) 1+3+4 (Huang) Vascular malformation and vascular tumor associated! with phacomatosis (Phacomatotic angiomatous diseases) Neurocutaneous syndromes 1. Angioblastoma (angioreticuloma) (von Hippel-Lir-dau) (angioblastomatosis) 2. Encephalofacial angiomatosis = neuro-oculocu-taneous (Sturge-Weber-Krabbe-Dimitri) 3. a. Hereditary hemorrhagic telangiectasia (Rendu-Osler-Weber) (cutaneous, mucosa and visceral capillary malformation) b. Ataxia telangiectasia (Louis-Bar) facial naevus, cerebellar angioma, angioma of the choroid of the eye, defective immune glo-bulin system of the IgA class 4. Encephaloretinofacial } (Wyburn-Mason) angiomatosis J (BonnetDechaume-Blanc) 5. Orbitothalamoencephalic angiomatosis (Bregeat syndrome) 6. Diffuse corticomeningeal capillovenous familial angiomatosis (non calcifying) (DivryVan Bc-| gaert) 7. Cutaneomeningospinal angiomatosis (Cobb) 8. Congenital venous dysplasia (extremities, spinaij (Klippel-Trenaunay-Weber syndrome) 9. Glomangiomatosis (glomus tumor) (Bailey) 10.Dyschondroplasic hemangioma (MaffucciKost 11. Angiokeratosis naeviformis (?) 12. Extensive cavernous hemangioma + thromboc.-| topenia and purpura (KasabachMerritt syndromet 13. Blue Rubber Bleb syndrome 14. Malignant hemangioma

Localization of AVM

p. 382

63

The gliotic area surrounding an AVM may represent the brain reaction to pulsation of the AVM, to ischemia, to microhemorrhage or to a primary developmental phenomenon (lack of an astrocytic layer around vessels, therefore diffusion of metabolites) . It is assumed that because of the dysplasia of a capillary bed, there is no functioning brain tissue within the AVM itself, at least in compact lesions. However, we do not know at what distance from the lesion normal cerebral architecture is preserved and this must vary in each case. A better understanding of the pathophysiology of the lesion thus awaits a more comprehensive embryo-logical and histological analysis. Localization Besides the 'pure' AVM occupying a single intra-cranial compartment we have seen examples of AVMs involving multiple anatomical layers including skin, muscle, bone, dura, arachnoid, brain, and ventricle. The following combinations have been described: If the vascular malformations do indeed represent the result of an early deep fistula with remote effects, it is surprising that the lesions are not multiple more often, as many areas of the vascula-ture would be at risk. Garretson (1985) has categorized cerebral AVMs I which, incidentally are seen most frequently involving branches from the MCA, less often the ACA, and least frequently the PCA) as those involving the epicerebral, transcerebral and sub-ependymal circulations (see also section on micro-circulation). He notes that AVMs involving only the transcerebral (long perforating) arteries are not visible on the surface of the hemisphere yet arterialized veins may frequently be seen owing to the anastomoses between the transcerebral and epicerebral veins. A rare group of AVMs remains confined to the pial surface of the brain stem. Neuropathological studies have shown that brain tissue around an AVM is frequently gliotic and exhibits cystic changes. Besides these subcortical changes which may extend very deep into the white matter there may occasionally be seen cases of severe encephalomalacia with atrophy of gyri or lobules in the neighbourhood of the AVM and also changes of the arachnoid-pia-layer. In some cases this change is combined with hemorrhage, but in others there is no sign of bleeding. The superficial and deep changes are not clearly related to the site or size of the AVM. Neurosur-gical Localization of the AVM WithintheBrain observations do not confirm that gliotic change around AVMs do not always involve all layers of the brain from the convolutions is, as often stated, a "pseudocapsule or surface arachnoid down to the ventricle (Figs 3.7A-B, matrix" in every case. 3.8). From the surgical perspective they may be divided into the following groups and subgroups:

64

3. Pathological Considerations

References p. 382

I. Surface Lesions (visible on exploration on the surface of the brain) 1. Dorsal surface (frontal, ternp., occip., cerebetl.) 2. Basal surface (frontal, ternp., occip., cerebell.) 3. Polar surface (frontal, ternp., occip.)

a. cortical - sub-cortical (Fig 3.9A-C) b. cortical + subcortical + subependymal (intraventricular) (Fig 3.9D)

II. Deep Lesions (invisible at exploration on the surface) 1. Sulcal (all sulci, especially precentral, postcentral, inferior parietal, parietooccipital, calcarine) 2. Fissural lateral (Sylvii) fiss. interhemispheric fiss. transverse fiss . 3. Deep white matter (semiovale center) 4. Deep gray matter (striate, thalamic etc.) 5. Subarachnoidal (cisternal)

6. Intraventricular

a. cortical -<- subcortical (Fig 3.10A-C) b. cortical + subcortical h subependymal (intraventric-ular) (Fig 3.10B-D) a. subcortical (Fig 3.8) b. subcortical + subependymal (Fig 3.8) a. paramesencephal (v. Galeni) (see Fig 3.13B) b. parapontine c. parabufbar a. trigonurn, temporal horn b. Illrd ventricle c. IVth ventricle (Fig 3.11AB).

-e'srences p. 382

Localization of AVM

65

13.7B Infratentorial AVMs with extension to the IVth ventricle, with (1) and without (2) ventricular obstruction.

66

3. Pathological Considerations

References p. 382

11-2-3 Surface Lesions Surface lesions may involve only the cortex or the white matter and the subependymal layer tc extend into the white matter or extend through reach the ventricular system (Figs 3.8, 3.9A-D).

Fig 3.8 Artistic drawing of the possible locations and extensions of hemispheric AVMs: A with connection to ventricular system В without connection to ventricular system.

'erences p. 382

Localization of AVM

67

Fig 3.9A-D Cortical-subcortical AVM (A-B) on the visible surface, with (D) and without (C) subependymal extension.

68

3. Pathological Considerations

II 1 Within the Suici An AVM may appear to be superficial on angiog-raphy but at operation only a red draining vein is present, or there may be no evidence of the AVM at all as it is deep within the suici. The lesion is still

References p. 382

a cortical + subcortical one but hidden deep within a sulcus which may be two or three centimeters or more below the actual surface of the brain. Dissection through the arachnoid of the sul-cus will expose the lesion (Fig 3.10A—D).

Fig 3.10A-D Cortical-subcortical AVM located in the depth of suici (with [D] and without [C] subependymal extension L (B) and therefore not visible on the surface (A). ~

^erences p. 382

Localization of AVM

69

j>lied primarily by perforating arteries of the АСА, MCA, PCA, PcoA, anterior and posterior ch о ro idal_arteries, AICA, PICA, SCA, vertebral and basilar arteries. II 5 Cisternal (Subarachnoidal) (see Fig 3.13B} Although angiography of an AVM of the vein of Galen shows the lesion in the very center of the brain, surgical experience has shown that they lie entirely within the cisternal system. Surgical explorations have further demonstrated that there exist pure cisternal (subaraehnoidal) AVMs which may be paramcsencephalic (ventral or dorsal), parapontine (ventral or ventrolateral within the cerebellopontine angle) and parabulbar (around the medulla oblongata). These paramcdullary superficial AVMs of the brain stem seem to be an intracranial equivalent to some paramedullary spinal AVMs. II 6 Intraventricular (see Fig 3.11) A few totally intraventricular AVMs of the cho-roid plexus within the trigonum are known. These lesions may be approached through jhe corpus eallosum. We have seen 2 cases with an AVM of the tela chorioidea of IITrd ventricle, three cases of lateral ventricle, and two cases of an AVM of the plexus chorioideus of the IVth ventricle.

F i g 3 . 1 1 A - C Surgically observed loca- lization para- and intraventricular AVMs with ostruction of ventricular system. A Anterior catlosal and septal (1}, Fig3.11B, С

70

3. Pathological Considerations

продолжение

Fig3.11B, С

В Paraventricular. С Varix, intraventricular.

As can be proven angiographically, AVMs in groups I la, 2a, За and II la, 2a, За (see page 64) are supplied by cortical arteries rather than perforators whereas in groupsi Ib, 2b, II Ib, 2b, 3, 4, 5, 6 the reverse is true. Cisternal AVMs. particularly vein of Galen malformations, appear to be supplied about equal])' by cortical and perforating vessels (Figs 3.12-13). {Fig 3.12A-D The cerebral and cerebellar AVMs are similarly composed. Angiographically the flow to the AVM can be visualized .from mainly 1 (A), 2 (B) or 3 (C) sources {АСА, MCA, PCA or PICA, AICA, SCA) or only from perforators (D). a = anterior cerebral artery, m = middle cerebral artery,_p__= posterior cerebral artery, d = deep perforators.

References p. 382

Localization of AVM

71

Fig3.13A-d

A Cerebral convexial AVM supplied mainly by cortical branches of АСА, MCA, PCA. Possible participation of dural branches. The perforating feeders very often participate in the supply of the AVM even though they may be invisible angiographically.

B AVM of vein of Galen is usually supplied by both cortical and perforating branches

Fig3.13C, D

72

3. Pathological Considerations

References p. 382

Fig 3.13C Deep, e.g. thalamic, parathalamic AVMs, are mainly supplied by perforating arteries.

Fig 3.13D Infratentorial convexial AVMs are composed similarly to cerebral convexial AVMs. These are mainly suppliec by cortical (SCA, PICA, AICA) and perforating feeding arteries, from basilar artery and its branches.

-eferences p. 382

The Nidus

73

Histologically, the nidus is composed of vein-like structures whose walls are often thickened and hyalinized. These have been termed arterialized veins in that the intima and muscularis are thickened but there is no elastic tissue characteristic of arteries. Saccular (varicose) enlargements may occur in these veins. The walls may also contain calcium or amyloid deposits. Deshpande and Vidyasager (1980) suggest that these structures represent persistent embryonic veins histologically comparable to venous structures found in the 20—80 mm embryo. Brain tissue within the nidus is usually gliotic and may show deposits of hemosiderin from previous microscopic hemorrhages. AVMs can broadly be divided into two main types: those with a single nidus (with all the vascular channels somehow interrelated) and those with more than one nidus in which there are adjacent but individually separated components of the malformation (Table 3.8) (Figs 3.14-3.18).

Table 3.8 Nidus (Epicenter) /.

Single, compact a. Without fistula b. With A-V fistulae of every size (associated with varix) c. Only A-V fistula visible (convoluting invisible)

//. Multifocal (multicentric - polycentric) compact (subdivided into a-b-c as in I) 1. 2. 3. 4. 5. 6.

Unilateral Bilateral Supra-, infratentorial Orbital and cerebral Cutaneous, dural and cerebral (4 and 5 combined)

///. Diffuse (no visible nidus) (non-nidus) (Scattered pathological arteries and pathological veins without recognizable connections (angiogra-phically or at operation) a. b. c. d. e.

Small areas Large areas Entire hemisphere Both hemispheres Supra- and infratentorial

74

3, Pathological Considerations

References p. 382,

The Concept of Compartments In AVMs with a single nidus, a wide spectrum of structural variation is possible, depending on the complexity of arterial supply and venous drainage. Just as one or more arterial branches may feed the lesion, one or more veins may drain it. Arteries may be branches of a single arterial system, may involve two or more cortical arteries such as anterior and middle cerebral arteries, or may be composed of combinations of cortical and perforating arteries (see Fig 3.12A—D). In the case of multiple niduses these may be confluent or separated by brain parenchyma. The blood supply may be provided by one or by different cortical or perforating arterial systems whether or not the niduses are separated by brain tissue. The individual draining veins may converge into one large collecting vein or the venous drainage may be accomplished by separate venous systems. (It seems by definition that there should be one vein for each nidus if it is really to be considered a separate entity). A single compact nidus may be very simply constructed having only one feeder and one or more draining veins (monocompartmental). The elimination of the single feeder leads to collapse of the entire malformation. A single nidus, however, may have considerable complexity with variations depending on the number and type of feeding arteries and draining veins. Either one or more arterial branches may feed the lesion and one or more veins may drain it. Arteries may be branches of a single system of arteries, may involve two or more cortical arteries, or a combination of cortical and perforating arteries.

Fig3.15A-E Single nidus - single compartment. A-B With 1 or 2 cortical feeders with 1 or 2 or more draining veins. C-D With 1 or more cortical feeders and perforating fee ers. E With multiple perforating feeders only.

Fig 3.14A-C Composition of AVM nidus. A Single monocompartmental nidus. В Single multicompartmental nidus. С Multiple niduses.

References p. 382

The Concept of Compartments

75

Fig 3.17A-C Relation of the feeding arteries and draining veins to different compartments of an AVM. A Supplied from same artery with single or 2 compartments, single or multiple veins. В Supplied from 2 arteries, single or multiple compartments and single or multiple draining veins. С Supplied from 3 arteries, single or multiple compartments and single or multiple draining veins. Fig 16A-C Multiple niduses. A Supplied from same artery (e.g. АСА, РСА, MCA). B Supplied from different arteries. C Vith nidus of perforators and subependymal drainage.

Fig 3 18A-E Variations in venous drainage of different compartments. A single cortical feeder and corresponding cortical drainvein. B single cortical feeder and combined cortical and subependymal drainage. C Single cortical feeder, absence of cortical draining vein, drainаgе only towards subependymal system. D Cortical and perforating feeders with expected cortical and subpendymal draining veins. E Possibility of reversed draining system (hitherto unobserved)

76

3. Pathological Considerations

The nidus may be composed of a single or of multiple compartments. These compartments are, however, not anatomical entities. They represent hemodynamic units and this may best be exemplified _as follows: j If angiography by contrast injection into the feed-' ing branches arising from АСА, MCA and PCA shows equal filling of the entire AVM there is no dominance of any system. Each vessel must have equal flow pressure. This is a monocompartmental nidus. At operation, the clipping of one or two feeders does not change the volume or the color of the AVM (see Fig 3.12A-D). However, if in an AVM consisting of three systems of arterial supply А, В and C, and one system is dominant, for example A, then the clipping of the A-system is followed by partial or total collapse and color change (to blue) of the AVM, only for it to refill_and to turn red once more. This happens because the В and С systems are no longer dominanted by the A system pressure. For the operation to be successful both the В and С systems must also be eliminated (see Fig 6.17, Chapter 6). If, after clipping of the A-system a part of the AVM is collapsed and remains collapsed and blue, whereas other smaller or larger parts of the AVM remain red and turgid, this signifies the presence of multiple compartments or even multiple niduses. These may be confluent or may be separated by small nonfunctional or even functional brain parenchyma. Every neurosurgeon will recall that after most operations for AVM it is possible to describe the real construction of the lesion while in a few cases the picture remains confusing. The complexity of composition of AVMs can be enormous. Only superselective angiography with temporary balloon occlusion of individual feeders may provide the neurosurgeon with the necessary information concerning the actual angioarchitecture of AVMs. Interventional neuroradiologists are already using this technique in AVM patients who are candidates for embolization. It should as readily be used for the patients who cannot be embolized, but require operation. Although far more detailed knowledge is yet required it is helpful for the surgeon to know that the following constructions of AVMs are possible: 1. Single compact nidus a. monocompartmental, b. multicompartmental. 2. Multiple compact niduses Each of the niduses may be: a. monocompartmental, b. multicompartmental.

References p. 382

Also, the multiple compact niduses may be located very close together (this is more frequent or they may be located at a large distance from each other (even within another hemisphere, or combined supra- and infratentorial) see Fig 3.193.23. We hope that MRI might yet provide us with more information, especially in those cases belonging to the group of multiple compact niduses, as to whether there is functional brain parenchyma between the niduses. In one of our patients (see Fig 3.21A-H), a large left parietooccipital AVM received feeders from anterior, middle and posterior cerebral arteries as well as through dural-pia^ collateral arteries. MRI in this case showed a large compact AVM without intervening brain tissue The right handed patient had full neurologica function with regard to speech, reading etc. Am attempt at operation would cause her neurological deficit.

Compact and Diffuse Lesions The generally accepted view is that AVMs are usually quite compact with no (or a minimum of normal brain tissue between the pathologic^ loops of the malformation. There would be nc normal brain architecture or capillary bed within the lesion. Residual brain tissue is scarred by gliosis and ma;. contain hemosiderin deposits and calcification Adjacent to the lesion the brain tissue is sometimes also changed, and a separation between normal tissue and AVM may be created by hematoma, cyst or gliosis. The adjacent cortex may b; atrophic and is sometimes functional and sometimes not. This describes a compact AVM havin; single or multiple compartments. However, surgical experience shows that AVMs may differ considerably from this typical description. — There are (even large) AVMs without any atrophy of the adjacent cortex and having nc changes of arachnoidal, cortical, or subcortict layers. — There are AVMs without gliotic changes, without gliotic cleavage around the lesion, withou: pseudocapsule or matrix, but just normal surrounding brain tissue. — There are angiographically well-documente; cases with "non-compact" (or more proper!) diffuse AVMs which are scattered throughou: lobes, one or both hemisphere or even bilaterally in the deep gray matter. In two of our owr cases there were no connections visible between pathological arteries and pathologica veins (see Fig 3.24).

References p. 382

Compact and Diffuse Lesions

77

Fig3.19A-l This 16 year old female patient suffered a stroke and CT showed a large right frontal hematoma which was removed in another hospital An AVM was seen and left in place. A-B Preoperative CT showed cortical-subcortical AVM in the right frontal opercular area extending to the frontal horn.

C-D Right frontal carotid angiogram showed the size and extent of the AVM. The feeding arteries arose from M2 and A2 and supplied the cortical portion of the nidus. A1 branches supplied the subcortical portion of the nidus. i E Lateral view of arterial phase. F Unusually large single vein draining the cortical nidus towards the vein of Labbe. The subcortical nidus drained to the internal cerebral vein via subependymal veins (D). The AVM was completely removed. Fig 3.19 G—I ^

78

3. Pathological Considerations

References p. 382

Fig 3.19G-I Postoperative angiography showed norma' sized middle cerebral artery and anterior cerebral artery as I well as M1 and A1 perforators (G-H). The displacement o' the anterior cerebral artery to the right was due to right frontal atrophy as seen on CT (I). The postoperative course | was uneventful.

References p. 382

Compact and Diffuse Lesions

79

Fig3.20A-D

A--B A 7 year old boy presented with subarachnoid hemorrhage. Vertebral angiography showed an AVM composed of 2 niduses located in the left mediobasal occipital Iobe. Each nidus drained into a different venous system.

Fig 3.20C-D Postoperative angiography and CT after complete removal of the lesion. Preoperative quadrantanopia remained unchanged.

80

3. Pathological Considerations

Fig3.21A-H This 29 year old fema patient presented with chronic headache, cardiac murmur and epileptic seizure. CT (A) and MR (B) showed a giant m formation involving not only the left parietal lobe but also adjacent structures and the corpus callosum. С Left carotid angiogram showed multiple niduses supplied by M1 , M2 M3 branches. The A1 is poorly seen

Compact and Diffuse Lesions

81

82

3. Pathological Considerations

References p. 382j Fig 3.22A-E A A compact AVM at the end ofj the left insula is seen on carotid angiography in a 32 year old patient. В Diffuse type AVM scattered within the left occipital lobe is seen on vertebral angiography The insular AVM is also demcr-strated to be filled through collaterals. Inoperable case! C-Е CT fails to disclose whether there was a single largei nidus or multiple niduses.

Compact and Diffuse Lesions

83

F i g 3.23A-E Large right parietooccipital dorsolateral (A-C) and mediobasal (B-D) AVM with multiple niduses (arrow). The malformation had a dural component supplied by occipital and middle meningeal branches (E). Note absence of saraight sinus. This 55 year old female with mitral stenosis died of a heart infarct following completion of surgery (see cnapter Complications, Vol. Ill B).

84

3. Pathological Considerations

References p. 36:

Fig 3.24A-C

A-B Left carotid angiogram showed a diffuse AVM т frontoparietal paramedian area in a 25 year old male. С Vertebral angiogram showed a further nidus located posterior to the first. Note absence of straight sinus Inoperable case.

Sizes of AVM

References p. 382

85

Sizes, Shapes, and Elements of AVMs Sizes of AVM AVMs may vary enormously in size and the following types may be described: 1. Occult Not seen on angiography, not found at surgery and not demon strated pathologically but assumed present in cases of otherwise unexplained cerebral hemorrhage particularly in young, normotensive patients. 2. Cryptic Invisible on angiography, invisible at surgery. They may be recognized by histological examination if the hematoma is carefully removed and not sucked away. 5. Micro Just visible on angiography, 0.5-1 cm sometimes only as an abnormal

arteriole without draining veins. Sometimes only an abnormal draining vein is seen and the feeding vessels remain undetectable. At other times tiny lesions with classical appearance = pathological arterioles and pathological draining veins. Often invisible to the surgeon. 1-2 cm. 4. Small 5. Moderate 2-4 cm. 46 cm. > 6 6. Large cm. 7. Giant In the latter four groups the arterial component may be more dilated elongated, and tortuous, and therefore more impressive. Alternatively, the venous component may predominate or both may be similar in size and form (8 cases) (Figs 3.25-3.32).

86

3. Pathological Considerations

References p. 382

D Fig 3.26A-D A Left carotid angiography of an 18 year old female shows small AVM supplied by M1 and M2 feeding arteries. Location] is lateral to the caudate nucleus (arrow). В In the later phase, the deep drainage towards the internal cerebral vein is seen (arrow). The AVM could be completely! removed. C-D Preoperative (C) and postoperative (D) CT. The postoperative course was uneventful.

Sizes of AVM

88

3. Pathological Considerations

References p. 38Г

Fig 3.28A-C This 25 year old male patient presenting with subarachnoid and intraventricular hemorrhages. A-B Right carotid angiography demonstrated a small AVM associated with an aneurysm. The AVM is located within • right trigone (arrow). Drainage of the AVM occurs through subependymal veins into the galenic vein. The AVM, wh was compressed by hematoma, was removed through an interhemispheric transcallosal approach. The postopera: course was uneventful. Visual field was preserved. С СТ 7 years after removal of the AVM.

References p. 382

Sizes of AVM

89

Fig 3.29A-C An 8 year old boy presented with subarachnoid hemorrhage. A "Coronal CT showed a small enhancing lesion on the superolateral corner of the left trigone (arrow). В The postoperative coronal CT showed the interhemispheric approach through cingular gyrus to the trigone (arrow). The malformation was completely removed. This approach was chosen in order to avoid any parenchymal damage to the dorsolateral left parietal cortex. С The small AVM was only visible in the arterial phase of left carotid angiogram (arrow). The venous drainage was invis-ible. The postoperative course was uneventful. The visual field was preserved.

Fig 3.30A-B This 23 year old female patient presented with a right parietal hematoma. Carotid angiogram showed a bar ely visible (arrow) AVM. Draining veins were not visible. The AVM and the hematoma were removed by a lateral approach through the deep end of the right lateral Sylvian fissure. Preoperative left hemiplegia improved remarkably, whereas homonymous hemianopia remained unchanged. В Postoperative angiography.

90

3. Pathological Considerations

References p. 382

Fig3.31A-D A A 60 year old male patient presented with subarachnoid hemorrhage and Parinaud syndrome had a small enhancir: nodule located over the left superior colliculus shown on CT (white arrow). В Postoperative CT 2 months after removal of the lesion. C-D Frontal and lateral vertebral angiography showed a barely visible nidus (black and white arrow) with draining veir On lateral vertebral angiography only early filling of the v. Galen and the straight sinus was seen. The 5 x 5 mm AVM was explored and removed through a supracerebellar approach. No additional neurological deficit after operation. Total disappearance of Parinaud syndrome within 6 months.

References p. 382

Sizes of AVM

91

' Fig 3.32A-D This 14 year old boy had subarachnoid hemorrhage. A Carotid and lateral vertebral angiography were normal. AP vertebral angiography showes a small nidus with an early draining vein located over the left dorsal mesencephalon (arrow). Surgery confirmed a small AVM located over the left | superior colliculus. The AVM was radically removed. В Postoperative vertebral angiography. С Preoperative CT showed a small enhancing lesion in the area of the left superior colliculus (arrow). D The postoperative (CT) showed no parenchymal defect in the mesencephalon. The postoperative course was uneventful. No Parinaud syndrome.

92

3. Pathological Considerations

References p. 3

Shape The classically described AVM as a pyramidal, conical or wedge shaped lesion occurs in only about 40% of cases. Their appearance as a transcerebral dissecting structure is always very impressive and therefore frequently used for illustrations. In reality most AVMs, both giant and small have an amorphous, irregular, ameboid shape. They may be described as being more spheroid, oval, globular or striplike, sometimes likened to a bag of worms, a head of a Medusa, or spiderlike. Such literary descriptions express the fears of the neurosurgeon and do not contribute to solving the problem as to how such a lesion can be properly removed. For surgical treatment new perspectives are necessary. We have to analyze the subject in a different way, studying the feeding arteries and draining veins with more attention, comparing the compactness or diffuseness of the lesions, and trying to understand the concepts of "nidus" and "compartments" (Figs 3.33-3.43).

Fig 3.33A-C Right frontal paramedian cortical-subcortical AVM with typical pyramidal shape. Feeding vessels arosr from M3 and A3 as well as from M1 (A-B). The drainage occurred towards an ascending superficial cortical vein as we as through the dilated thalamostriate vein associated with a varix. The internal cerebral vein (C) was hugely dilatec Stenosis of straight sinus. This 35 year old female refused surgery.

References p. 382

Shape

93

Fg3.34A-B

A On frontal view of a right carotid angiogram, the typical pyramidal shape of a parietal cortical-subcortical AVM were seen. Multiple niduses were also visible. The feeding arteries arose from M1, M3 and M4. The AVM drained into both the superficial and deep venous systems. В A lateral angiogram showed a different shape from the frontal view. This was explained by the fact that the AVM was located entirely within the postcentral sulcus. Absence of the straight sinus. This 43 year old male refused surgery.

94

3. Pathological Considerations

A-B Right polar and mediobasal temporal AVM shown on carotid (A) and vertebral angiography (B) with a plexiform appearance of the nidus. The drainaging veins appeared in the late phase of angiography. С СТ showed the exact location and extension of the AVM (arrows). D Postoperative CT. The postoperative course was uneventful in a 29 year old female.

References p. 382

Shape

95

Fig 3.37A-B An unusually shaped plexiform type AVM in the right temporal polar area. A Preoperative angiography. Note pathological vessels with microaneurysms at the origin of participating branches of the transit vessels. B Postoperative angiography showed normal shaped temporal and anterior choroidal arteries. The postoperative course was uneventful in this 30 year old female.

Fig 3.38A-B A 39 year old female presented with chronic headaches and occasional Jacksonian attacks, but no neurological deficit. Left carotid angiogram (A-B) showed dilated M3 and M4 branches supplying a diffuse type AVM of the entire parietal lobe. Any attempt to remove this cortical-subcortical lesion probably would have been followed by Gerst-mann's syndrome. Radiation therapy was refused by the family of the patient. This case has been followed for 12 years as an untreated case. She continues to be plagued by headaches and seizures.

96

3. Pathological Considerations

Fig 3.39A-C This 53 year old patient presented with epi leptic seizures. Right carotid angiogram showed a diffuse AVM scattered within the entire frontal lobe. Inoperable.

Shape

Fig 3.40A-E A 53 year old male patient with right occipital hematoma. Preoperative CT (A), postoperative CT (B). Vertebral angiography (C) showed a dorsal occipital moderatesized AVM (D). Varicose veins drained to the transverse sinus (E). Remarkable in this case was the dilatation of the entire artery of the angular gyrus. The postoperative course was uneventful. The preoperative homonymous hemianopia remained unchanged.

97

98

3. Pathological Considerations

References p.

Shape

99

100

3. Pathological Considerations

References p.

Fig3.43A-B

A This 43 year old patient with cerebellar symptoms progressively disabled and finally bedridden. Vertebral angiography showed a giant AVM of the left cerebelar hemisphere. В On frontal vertebral angiography involvement of the i cerebellar hemisphere was seen as well a varicose dis tation of right cerebellar veins. The lesion could be completely removed in a one stage operation. However.the patient died due to bilateral parietal epidural hematoma which could not be recognized in time. CT-scan was not available in 1974 (see chapter Surgical results, Vol. III B

Pure Fistulous AVM More important is the recognition of the construction of the nidus, i.e. if it is plexiform, mixed plexiform and fistulous or pure fistulous. The following cases (Figs 3.44-3.53) demonstrate pure fistulous type AVMs.

Fig 3.44 Fistula between the middle cerebral artery ( 1 ) and the vein of Labbe (2) (see Fig 82a, p. 143. Yasargil. G. M.: Microsurgery Applied to Neurosurgery. Thieme, Stuttgart 1969).

References p. 378

Fig 3.45A Direct A-V fistula between A3 segment of pericallosal artery and inferior sagittal sinus with drainage to the vein of Galen. (From Smith, R. R., A. F. Haerer, W. F. Russell: Vascular Malformations and Fistulas of the Brain. Raven, New York 1982.)

Shape

101

В Cerebral angiography (lateral images) showed left parietotemporal arteriovenous malformation supplied by a dilated branch of the sylvian bifurcation and draining into the lateral sinus: possible participation of smaller arteries of the sylvian group. (From Stroobant, G., et al.: Neuro-chirurgie 32: 8 1 , 1986.)

Fig 3.46C, D Fig 3.46A-D A A-V fistula between a dilated temporal branch of the left middle cerebral artery and a markedly dilated vein of Labbe, and emptying mainly retrogradely into the rolandic vein (arrow). The connection to the transverse sinus was hypoplastic. В Postoperative angiography.

102 3. Pathological Considerations продолжение

Fig 3.46C Postoperative angiography: venous phase.

Fig3.47A-F A-C A dilated single opercular branch of the left middle cerebral artery with fistulous connection to a varicosely dilated superficial vein was seen in this 37 year old female patient.

References p. 382

Fig 3.46D Postoperative CT. Uneventful postoperative course in 60 year old male.

10

1. History

is entailed... How many less successful attempts, made by surgeons less familiar with intracranial procedures, have gone unrecorded may be left to the imagination." "The lesions, in short, when accidentally exposed by the surgeon, had better be left alone, and how muchjadiation may accomplish for them is undetermined though there are favourable experiences on record. So long ago as 1914 Wilhelm Magnus of Oslo unexpectedly exposed at operation a venous angioma of the left rolandic region, a decompression was made with the intention of treating the lesion with radium therapy which at that time was known favourably to influence cutaneous angiomas. After treatment, the decompression, which was bulging, ^^ecededj and the epileptiform attacks, from which the patient was suffering, became infrequent and finally disappeared ..." The publication of Reichert (1946) is unique, as he reported 15 cases of premotor vascular anomalies causing Jacksonian epilepsy, which were treated successfully by coagulation of the dural and pial vessels of the lesion (1935 to 1941).

References p. 369

Neurosurgical Treatment of Intracranial AVM Following the Introduction of Angiography (1930) As we have seen, surgical excision of AVMs was carried out between 1889 and 1930, both by general surgeons and neurosurgeons. Some of these cases met with success, others ended disastrously. After one or two bad results most surgeons did not risk further attempts at excision. With the advent of cerebral angiography the position began to change, for it became possible not only to diagnose the AVM but also to obtain some idea as to its location, its size and construction and the number of feeding and draining vessels. Angiography, however, was still somewhat primitive and the contrast material imperfect. Only a few angiographic demonstrations of cerebral AVMs were published before 1936 (Dott 1929. Lohr and Jacobi 1933, Moniz 1934 and 1951, Olivecrona and Tennis 1936). Dott provided the first demonstration of the angiographic aspects of cerebral AVMs at the Neurosurgical Conference in Stockholm in 1935. However, the full benefits of cerebral angiography came only with improved techniques which were not widely available until the 1950s. Olivecrona had a disappointing experience in 1923 when exploring for an infratentorial tumor (case 65). He was confronted with a highly vascular AVM and the patient died. In another case (66), Left carotid angiogram showing a frontoparietal AVM. In the monograph of Egas Moniz, "L'Angiographie Cerebrale", Masson, Paris 1934.

102

3. Pathological Considerations

Fig 3.46C

Postoperative angiography: venous phase.

Fig 3.47A-F

A-C A dilated single opercular branch of the left middle cerebral artery with fistulous connection to a varicosely dilated superficial vein was seen in this 37 year old female patient.

References p. SE2

Fig 3.46D Postoperative CT. Uneventful postoperative course in 60 year old male.

эпсез р. 382

r

ig 3.47D-F Postoperative angiography. Uneventful postoperative course.

Shape

103

104

3. Pathological Considerations

References p

Fig 3.48A-F

A-D A fistulous connection between the right anterior temporal artery and a varicosely dilated vein in the temporal pole area, emptied into the ascending frontal and parietal veins in this 35 year old man. The application of a clip on the anterior temporal branch was followed by immediate collapse of the malformation.

References p. 382

Shape

Fig 3.48E-F Postoperative angiography. The postoperative course was complicated by a local epidural hematoma. Full recovery after its removal. Fig 3.49A-H Because of one epileptic seizure and bruit, a CT (A) was performed on this 9 year old patient. It showed a large temporal malformation. В СТ after removal. С Left carotid angiogram shows mainly fistu-lous connections between three dilated branches of middle cerebral artery and a hugely dilated vein of Labbe. D Frontal view of vertebral angiogram showed dilatation of P1 and P2 segments, and the posterior cerebral artery giving off dilated terminal branches to the malformation. The smaller plexiform portion of the AVM was visible only in this view. See also Fig 5.3.

105

106

3. Pathological Considerations

References p. 382

Fig 3.49E The venous phase of vertebral angiography showed varicose dilatation of the draining vein and the unusual fenestration of the torcular Herophili and the internal occipital vein. F-H Angiography performed 6 months after operation confirms the complete removal of the lesion. Note the normal size of the previously dilated draining veins but still dilated middle cerebral artery. Postoperative course was uneventful.

References p. 382

Shape

107

A B Fig 3.50A-B A-V fistula in a 3 year old boy. Vertebral angiography showed a fistulous connection between the basilar artery and the torcular HerophiliJThe available angiograms do not allow precise analysis of the fistula. Inoperable case.

f С

Fig 3.51 A-C In this 11 year old boy who presented with cerebellar symptoms, angiography showed an A-V fistula between the hugely dilated right superior cerebellar artery and the transverse sinus. The transverse sinus seems to be occluded bilaterally. The patient's family refused surgery. The patient died 3 years later.

References p. 382

Shape

107

-ig 3.50A-B A-V fistula in a 3 year old boy. Vertebral angiography showed a fistulous connection between the basilar artery and the torcular HerophilUThe available angiograms do not allow precise analysis of the fistula. Inoperable case.

Fig 3.51 A-C In this 11 year old boy who presented with cerebellar symptoms, angiography showed an A-V fistula between the hugely dilated right superior cerebellar artery and the transverse sinus. The transverse sinus seems to be occluded bilaterally. The patient's family refused surgery. The patient died 3 years later.

108

3. Pathological Considerations

References p. 382

Fig 3.52A-H

A Because of trigeminal neuralgia CT was performed on this 34 year old nurse. It showed an AVM in the left cerebellopontine angle (arrow). В Postoperative CT.

C - Е Vertebral angiography demonstrated fistulous connections between lateral branches of the left superior cerebellar artery and a dilated AICA and the petrosal vein. The petrosal vein emptied through an unusual vein into the straight sinus. F-H Angiography performed 1 . 5 years after operation showed elimination of the fistulae. Postoperative course was uneventful. She married and had 2 children.

References p. 382 Fig 3.52

Shape

109

110

3. Pathological Considerations

References p. 382

Fig 3.53A-G An 18 year old female presented with symptoms of occlusive hydrocephalus. CT showed a dilated vein of Galen (A). В Postoperative CT showed a collapsed vein of Galen. C-Е 4-vessel angiography demonstrated a single fistula between a dilated left posterior cerebral artery and the vein of Galen.

Elements of an AVM

References p. 382

111

Fig 3.53F-G Carotid and vertebral angiography performed 6 months after operation showed elimination of the fistula and the preserved slightly dilated posterior cerebral artery. Postoperative course was uneventful. The visual field was preserved.

Elements of an AVM

Table 3.9

Frequency of involvement by given arteries Left

Arterial Feeders Feeding arteries to the malformation are derived r'rom 5 main groups^ of arteries in the supratento-rial compartment - the anterior, middle, and pos-terior cerebral arteries, the perforating branches of these respective arteries, and the choroidal arteries. Similarly, infratentorial AVMs may be fed from the superior, anterior inferior, and posterior inferior cerebellar arteries, perforating branches of these arteries, and perforating arteries of the basilar and vertebral arteries. Dural branches of the external carotid, internal carotid, and vertebral arteries also contribute feeding _arteries to AVMs.__________________ As any given AVM can derive its feeding arteries from a single artery or a number of arteries there are over 60 possible combinations of feeding vessels for that lesion (Table 3.9).

Right

Total

ACA

85

93

178

MCA

95

99

194

PCA

111

85

196

AchoA

12

10

22

SCA

28

28

56

AICA

19

15

34

PICA

30

19

49

(See Chapter 6)

Cerebral arteries may be related to a malformation in one of three ways: as a terminal feeding artery, a transit (partially participating) feeding artery, or as an artery en passage (non-participating) non-feeding artery (Figs 3.54-3.56).

112

3. Pathological Considerations

References p. 381 продолжение

Fig 3.54 Artist's drawing of the different types of vessels in the vicinity of an AVM which can be recognized only by microsurgical dissection or possibly by superselective angiographic mapping. A terminal artery ends in the nidus (a),a transit artery participating in the supply of the AVM through small terminal branches also gives branches to the normal brain (b), a transit artery following a route close around the AVM but without sending branches to the AVM (c), a single draining vein dividing into 2 branches (d).

Terminal Artery Arteries which terminate directly in the AVM may arise as far proximal as the first segments of the anterior, middle or posterior cerebral arteries, or as distal as the fourth or fifth branchings of these vessels. Marked dilatation and tortuosity of the feeding arteries may give the parent trunks a pathological appearance whereas only branches of these arteries are true terminal arteries. It has been noted on angiography that these large arteries often decrease in caliber following excision of the lesions. Transit Artery with Participation

These arteries are usually enlarged and seem to enter the malformation. In fact, they give off side branches which feed the malformation and they then continue on to supply normal brain beyond. These must be traced to the point where actual branches enter the malformation before definitive ligation is undertaken.

Transit Artery without Participation

These arteries are not enlarged but are running in the vicinity of the AVM and simply share a sulcus or gyms with the AVM and appear to be part of the lesion. They can be completely separated from the AVM. Although superselective angiography has improved preoperative recognition of the types of arteries involved, the decision must often be madeduring operation as to which artery type is present (Figs 3.56-3.58).

References p. 382

Elements of an AVM

113

Fig 3.55A-I

A A large right insular AVM with 2 niduses. Preoperatively it was difficult to understand the true construction of the AVM. B On carotid angiography the middle cerbral artery and its branches seemed to end within the convolutions of the AVM. No distal branches were visible. C Vertebral angiography showed a second nidus with significant dilatation of posterior cerebral artery branches.

Fig 3.55D-I

114

3. Pathological Considerations

References p. 3£

'References p. 382

r

ig 3.55H-I

Pre- and postoperative CT.

Elements of an AVM

115

116

3. Pathological Considerations

Fig 3.56A-C Construction of AVMs. Pure fistulous (A), mixed fistulous plexiform (B) and plexiform (C).

References p. 382

Fig 3.57A-C Further variations of AVMs. A Single large terminal feeder - multiple veins. В Multiple feeders - single vein. С Multiple feeders - multiple veins.

Elements of an AVM

117

118

3. Pathological Considerations

References p. 38*

Fig 3.58 An AVM with 2 transit branches supplying terminal branches to the AVM. A transit artery located on the surface and being therefore immediately recognizable (a), a transit artery looping deeply into a sulcus and giving termin; branches to the AVM in the depth of the sulcus and thus being unrecognized {b} without precise dissection.

Venous Drainage A single large vein often forms the main drainage of an AVM. Drainage starts in the center or toward the_apex of the lesion with the vascular channels of the AVM gradually coalescing into a large vein which finally drains into one of the venous sinuses. The large draining vein is frequently dilated as it emerges from the AVM but then ta pers distally as it courses toward the sinus. In such cases, the drainage is reminiscent of a venous malformation with several veins draining into a large dilated vein. The vein is thus comma shaped with a large origin and a gradual loss of caliber distally (Figs 3.59-3.68). Multiple draining veins may represent one of two configurations. First the large draining vein may divide as it emerges from the nidus of the lesion and the separate branches course toward one sinus or take different directions and drain into different sinuses, such as the superior sagittal and transverse sinuses. Secondly, there may be two or more distinct draining veins, perhaps draining different niduses of the lesion or related in some other way to its internal architecture. Again the course of the multiple veins may be toward one or more collecting sinuses.

Draining vessels are usually divided in to .superficial groups which drain in the sagittal, sphenopari-etal, cavernous, transverse and sigmoid sinuses and deep groups which pass to the subependymal collecting system and subsequently into the internal cerebral veins, basal vein of Rosenthal, internal occipital vein, into the vein of Galen and hence into the straight sinus and torcular or petro-sal sinuses.

Elements of an AVM

References p. 382 Fig 3.59A-B Observed variations of venous drainage. Single draining vein with varix (A) and without varix (B).

A

119

120

3. Pathological Considerations

References p. 38J

Fig 3.60 Artistic drawing of observed variations of supe" ficial and deep draining veins.

Fig 3.61A-B This 40 year old female dentist with a left frontobasal AVM presented with subaractinoid hemorrhage. A-B Note the large main draining vein dividing into a frontal ascending and Sylvian branch.

, References p. 382

Elements of an AVM

121

Fig 3.62C-G

122

3. Pathological Considerations

References p. 382 Fig 3.62C Postoperative angiography confirmed radical removal. D Preoperative MRI. E Postoperative MRI.

References p. 382

Fig3.62F-G Artist's drawing. The AVM was located in the medial surface of the superior temporal gyrus which was not precisely localized by CT or MRI.

Elements of an AVM

123

G

124

3. Pathological Considerations

References p. 382 I

Fig 3.63A-C A 16 year old female patient presented wit*subarachnoid hemorrhage. A-B Carotid angiography showed a left posterior front AVM with a single comma shaped draining vein. С Postoperative angiography. The postoperative course was uneventful.

Elements of an AVM

References p. 382

- : 3.64A-C

Left insular AVM with plexiform

I -3.

A arterial phase. B Single draining vein (of Labbe). C The malformation was completely removed. The postoperative course was uneventful in this 42 year old male.

125

126

3. Pathological Considerations

References p. 382

Fig 3.65A-D A 22 year old female patient with a right parietooccipital cortical-subcortical AVM. Carotid (A) and vertebral (B) angiography. Note the single draining ascending vein. Preoperative (C) and postoperative (D) CT. The malfo--mation was completely removed with an uneventful recovery.

References p. 382

Elements of an AVM

127

Fg 3.66A-B Small left AVM of the head of the caudate nucleus. This 62 year old female refused surgery after present-irg with subarachnoid hemorrhage. A single draining subependymal vein was seen,

:

: 3.67A-D A 36 year old female with a right frontoopercular AVM had a single subarachnoid hemorrhage. A - B Preoperative angiography showed a bizarre venous drainage. Note the single vein.

Fig 3.67C, D

128

3. Pathological Considerations

References p. 382 Fig 3.67C-D Postoperative angiography. Uneventful postoperative course.

:

eferences p. 382

Elements of an AVM

129

3.68A-B This right frontoopercular AVM with a single draining vein, was seen in a 16 year old girl who presented subarachnoid hemorrhage. Uneventful postoperative course.

Posterior fossa AVMs tend to drain toward the v. Galeni or tentorium if they lie in the upper half of the fossa. Those that lie on the ventral cerebellar surface drain toward the petrosal sinuses and those occupying the lower half of the fossa may even drain superiorly toward tentorium or anteriorly toward the petrosal sinuses or in a combined fashion (Fig 3.69). In most cases drainage seems to follow the expected cortical or subcortical vein in the area, but at times bizarre routes of drainage are noted, reflecting either preexisting embryonic channels or perhaps normal small transcerebral venous sys-

tems, which have been expanded by the presence ofjthe malformation/Thus a superficial AVM may at times drain only into the deep venous system, while a deeply placed AVM may unexpectedly drain outward to the superficial venous system and ultimately into the sagittal or transverse sinuses. A lesion virtually adjacent to the superior sagittal sinus may drain into the transverse sinus (Fig 3.74A—B), a posttemporal lesion can drain upward into the superior sagittal sinus (Fig 3.76), and a frontal lesion drain toward the occipital pole and vice versa (Figs 3.73 and 3.78).

130

3. Pathological Considerations

Fig 3.69A-D

A-B A 20 year old female patient presented with a right upper paravermian AVM located in the anterior quadrangular lobe. Note the single dilated draining superior cerebellar vein. C-D Postoperative angiography. The postoperative course was uneventful.

References p. 382

Elements of an AVM

131

Fig 3.70A-G Artistic drawing of some expected (usual) .enous drainage of AVMs in various locations: Frontal and sarietal AVMs usually drain into superior sagittal sinus (A). Cingular-callosal AVMs drain into superior and inferior sagittal sinus and via subependymal veins to internal cereига! veins (B). Callosal AVMs drain into septal and internal cerebral vein (C).

Fig3.70D-G

132

3. Pathological Considerations

Fig 3.70D-E Parietal AVMs may drain into superior sagittal sinus (D) or in transverse sinus (E). F-G Occipital AVMs may drain into transverse sinus (F) or into superior sagittal sinus (G).

References p. 382

Elements of an AVM

References p. 382

133

В

Fig 3.71A-B Artistic drawing of unexpected (unusual) venous drainage of AVMs. Occipital AVM drains anteriorly into cavernous sinus (A). Frontal AVM drains posteriorly into posterior part of superior sagittal sinus (see also Fig 3.73).

Fig 3.72 The well known drawing from the publication of Steinheil 1895 showing an unusual drainage of a frontal AVM.

\

\

134

3. Pathological Considerations

References p. Fig 3.73 Right frontobasal AVM with unusual drainage. The postoperative course was uneventful.

Fig 3.74A-B This right frontal paramedian AVM was found in a 43 year old patient presenting with epileptic seizures (A-B). Note the unusual course of draining vein towards vein of Labbe instead of towards the superior sagittal sinus. The postoperative course was complicated by a local hematoma. Full recovery after 2nd operation.

eferences p. 382

Elements of an AVM

Fig 3.75A-B This AVM of the right paracentral cingular area in a 28 year old male had unexpected drainage to the deep venous system via a thalamostriate vein. Successful removal.

Fig 3.76A-B This left posterolateral temporal AVM in a 53 year old male did not drain as expected, into the sigmoid sinus but rather showed flow reversal through the vein of Labbe to superior sagittal sinus. Successful removal.

136

3. Pathological Considerations

References p.

Fig 3.77A-B A 29 year old male had an intrinsic mesencephalic AVM on vertebral angiography with an unusual course of the draining vein. Inoperable case because of its intrinsic nature.

Fig 3.78A-G This 24 year old student had left occipital headaches and epileptic seizures and showed a left occipital AVM on left carotid angiography (A). B-C Carotid angiography showed a very unusual superficial draining vein ascending retrogradely from occipital to pre-central area.

References p. 382

Elements of an AVM Fig 3.78D-F MRI showed a left occipital lateral AVM. The operation disclosed 2 niduses. G Postoperative CT 1 week after surgery. Visual field was preserved.

137

138

3. Pathological Considerations

References p. 38?

Sinuses

Table 3.10

Just as the venous drainage of any given AVM may be quite anomalous and unexpected, so the sinuses themselves may be altered in one or more of several ways. Flow directions may be abnormal owing to increased pressure of the arterial input of the AVM being reflected in the venous drainage, or to anomalous construction of the sinuses themselves. There may be agenesis or obliteration of the sigmoid, transverse, straight and even sagittal sinuses. With sinus obliteration (in cases with vein of Galen or callosal, thalamic, parathalamic, occipital or cerebellar AVM) embryonic connections which normally involute may persist (Agee and Greer 1967, Handa et al. 1975, Dobbelaere et al. 1979, Vinuela et al. 1985, Jomin et al. 1985). There is frequently a communication between the vein of Galen and the superior sagittal sinus when the straight sinus is occluded (Table 3.10, see also Table 9.2 in Vol. Ill B). (See also Figs 3.1163.126 and Chapter 6, Figs 6.4, 6.5.) As with any high pressure intracranial fistula, flow may be reversed in the veins and reflux back through the sinuses rather than continue forward. Flow reversal has been demonstrated in the straight, transverse and sagittal sinuses (see Fig 4.5A-B and pages 54, 55, 193-211, 217, 224 and Vol. Ill B, Table 9.2).

sss

154

ISS

24

Galenic

176

Transverse

62

Sigmoid

15

Petrosal

31

Sphenoid

13

Cavernous

9

Frequency of involvement by given sinuses

Interestingly, despite the frequent involvement of the ophthalmic venous system with carotid arter\ cavernous sinus fistula, involvement of this venousystem has not been seen in a review of over 80 angiograms of AVMs seen at the University of Zurich in the last 30 years, even when the transverse and sigmoid sinuses were occluded bilaterj ally and venous drainage went through the cavernous sinus. There are only 7 cases in the literature attesting to the rare involvement of ophthalmic I veins in intracranial AVM (Cecile et al. 1971, one case, Dobbelaere et al. 1979, 4 cases, Huang et al. 1984, one case). (See pages 242, 244 and 280.)

Enlargement, Growth, and Regrowth of AVMs Progressive enlargement of AVMs has been referred to in pertinent literature (Olivecrona and Riives 1948, Shenkin et al. 1948, Norlen 1949, Sorgo 1949, Potter 1955, Tonnis and Schiefer 1955, Paterson and McKissock 1956, Padget 1956, Decker and Freislederer 1957, Anderson and Korbin 1958, Hook and Johanson 1958, Perria and Crudeli 1958, Huber 1959, Kaplan et al. 1961, McCormick 1969, 1978, 1985, Kelly et al. 1969, Porter and Bull 1969, Lakke 1970, Isfort 1972, Sundbarg et al. 1972, Waltimo 1973a,b, Spetzler and Wilson 1975, Krayenbuhl 1977, Parkinson and Bachers 1980, Stein and Wolpert 1980, Delitala et al. 1982, Huber 1982, Peeters 1982, Luessenhop 1984, Stein 1984, Wilkins 1985).

In 1948, Olivecrona and Riives reported a 31-yearold patient in whom a second angiogram performed 10 years after the first, showed that the volume of the AVM had increased. In the same year Shenkin et al. (1948) reported a case in which the documented growth interval was 16 years. Tonnis and Schiefer (1955) reported on a 25-yearold patient, who was operated on for a left frontolateral AVM in 1938; two feeding arteries were clipped and the red draining vein collapsed. Sixteen years later (1954) the angiogram showed a large AVM in the same location. Delitala et al. (1982) collected 37 cases from the literature and added one of his own, which showed in 1952 a small left temporal AVM; repeat angiography

References p. 383

Enlargement, Growth, and Regrowth of AVMs

139

Szepan (1977), rejecting the hypothesis of autonomous growth, contended that underlying the increase in size of an angioma is a vicious circle, namely, a disturbance of embryonal development with circulatory disturbance and consequent hemorrhage and thrombosis, together with degeneration of the surrounding zones with an ever-increasing growth of collateral vessels (secondary growth). The incidence of fully documented growth of AVMs in various series may represent only a small fraction of the actual prevalence of progressively enlarging lesions. Such figures as are available from studies of untreated cases are those of Luessenhop (1984) who described a series of 49 untreated patients with AVM. Of these, 51% enlarged, 6% became smaller, and 6% totally disappeared with time. Stein (1984b) mentioned that of 18 untreated patients followed up by serial angiography one third had lesions which enlarged, one third remained constant in size, and one third regressed.________________________ The two main theories put forward to explain enlargement of AVMs are those of the continuing effects of hemodynamic stress upon the thin walled, undifferentiated vessels forming the fistulous shunts (Hook and Johanson 1958, Kaplan et al. 1961, Waltimo 1973b), Huber 1976, Parkinson and Bachers 1980, see also Krayenbuhl 1977, Spetzler and Wilson 1975, Garretson 1985), and enlargement due to repeated, small, clinically silent hemorrhages (Paterson and McKissock 1956^Hamby 1958, Delitala et al. 1982). These hemorrhages would destroy surrounding supportive tissue and thereby allow further vascular dilatation and pseudoaneurysm formation in the malformation. Two other theories which have been considered are those of recruitment of vessels from previously uninvolved tissue (see McCormick 1984) and of autonomous growth of the AVM. Krayenbuhl noted that most patients had their first symptoms in early childhood and small lesions grew far more rapidly than large ones so that increased size of the AVM might be not so much a consequence of enlargement of congenitally pathological vessels but rather of actual growth. In common with Friede (1975) he subscribed to the view that either there was a congenital A-V shunt, the shunt stimulating abnormal growth of the pathological vessels, or that the abnormalities in the structure of the vessels were the cause of the growth, with the shunting merely incidental. Central to the whole concept of the growth of AVMs is the basic underlying cause of the initial development of the malformation. As noted

140

3. Pathological Considerations

above, despite some major flaws in the evidence (late onset of symptoms, absence of familial cases, rarity of associated lesions etc.), this is generally stated to be a congenital failure of development of capillaries at the 3 week embryo stage, thus allowing direct communication between arteries and veins. The poorly differentiated fistulous vessels may dilate and proliferate progressively and there is histopathological evidence to suggest that in many cases there is a lack of normal brain tissue between the folds of the malformation itself. Arteries entering the AVM are said to passively enlarge secondary to high flow volume from the low peripheral resistance of the shunt and the veins to dilate and become increasingly tortuous because of prolonged increase in venous pressure. Although we cannot offer any conclusive supportive evidence we would suggest, on the basis of our own findings, an alternative pathological mechanism to explain the etiology, character, progression and apparent regrowth of intracerebral AVMs. It is conceivable that AVMs result not from a congenital deficiency of capillaries but from an acquired disease involving pathological changes in vessels (starting with the capillaries) originally "programmed" to develop normally during early embryonic life. This process may begin in many cases during the 3rd week of embryogenesis but not become sufficiently widespread or of sufficient severity to produce effects until much later in life. The focal nature of most lesions is difficult to explain, but no more so than on a congenital basis. It would explain the rarity of all the usual associated features of congenital disease. It might also reasonably be held to explain the rarity of multiple lesions and the rarity and odd distribution of associated aneurysms in respect of traditional concepts of hemodynamics. One could suggest that the disease process remains active in some patients but relatively quiescent in others. Although hemodynamic factors and progressive gliosis of surrounding tissue should not be discounted as playing an active role in growth and regrowth and in producing clinical symptoms in cases of AVM, they may yet prove to be largely secondary phenomena in a primary disease process. The congenital aberrations which lead to the formation of telangiectatic lesions and cavernous angiomas are not difficult to appreciate, but a defect of capillary formation allowing direct and simple union of separate arterial and venous systems, even at crossing-points (Padget), is rather more difficult to comprehend. Tentative support for a theory which does not ascribe the characteristics of AVMs to a single

event early in embryogenesis may be gained by ye: more detailed angiographic study. Based on the analysis of the angiograms of the operated and non-operated patients of our serie-(500 cases), two main types and their subgroups o: AVM growth were distinguished:

Growth types of AVMs; 0 Enlargement @ Growth A. Pseudo-growth — incomplete angiographic evaluation (2 cases) — incomplete angiographic visualization (4 cases) — incomplete removal/regrowth (2 cases) B. True Growth (8 cases)

Enlargement In a group of patients with AVM not operated for I at least 5 years after the initial angiographic diag-1 nosis, or having been treated by radiation therapy. I repeat angiography disclosed enlargement of feeding arteries, draining veins or of associated aneurysms an^ varices, ranging from slight tc marked, in almost all cases. Enlargement of the AVM occurred, independent of the patients age as it was observed in both younger and older patients (Figs 3.79-3.81).

s'erences p. 383

Enlargement

141

Fig 3.79A-G CT (A) and carotid angiography (B-C) performed on a 10 year old girl with progressive left hemiparesis demonstrated a strio-capsular AVM. D-E Vertebral angiography showed the right thalamic extension of the lesion. Note the occlusion of the straight sinus С and F). Fig3.79F, G >•

142

3. Pathological Considerations

References p. 3?"

Fig 3.79F-G This inoperable AVM was irradiated in Boston. A repeat angiography performed 3 years later showec change in the size and shape the AVM.

Fig 3.80A-I A slowly growing left thalamic AVM in a 7 year old girl was found after she presented with epileptic seizures. A 1975. В 1977. С 1985. D Vertebral angiography showed the thalamic extension of the AVM.

Terences p. 383

Enlargement

143

E-F Note also the absence of the straight sinus (F) (arrow), and reversed flow through transcerebral channels.

Fig3.80G-l

144

3. Pathological Considerations

References p, :•

Fig 3.80G CT showed the location and extension of the malformation. The 18 year old patient shows progressive hemiparesis. This inoperable AVM was treated in 1977 with conventional radiation. H-l MRI performed 11 years later. Note the dilated contralateral parietal veins (I), due to the occlusion of the straight sinus seen on F.

^ferences p. 383

Enlargement

145

Fig 3.81A-F This 29 year old female patient first presented with subarachnoid hemorrhage in 1970. On right carotid angiography an AVM was found in the right striocapsular area (A). Note the varix on the basilar vein and stenosis of the galenic vein and straight sinus with collaterals to petrosal sinus (B). The patient received conventional radiation. 4 years later repeat carotid angiography (C-D) was performed because of slow but progressive mental deterioration. Angiography shows further growth of this plexiform type AVM as well as enlargement of the venous varix. E-F The growth and enlargement can also be appreciated on frontal views. 1970 (E), 1984 (F). The family refused surgery because the patient had chronic mental changes. This lesion could probably be removed with some risk of hemiparesis.

146

3. Pathological Considerations

Growth This type may be subdivided into two groups; namely "pseudo-growth", in which a variety of factors may stimulate or give on angiography the erroneous impression of growth, and "true growth".

Pseudo-Growth Incomplete Angiographic Evaluation Growth of an AVM may be simulated if the initial angiographic evaluation was incomplete and followed by incomplete removal of the AVM. This applies specifically to AVMs of the temporal, parietal and callosal or paracallosal areas which are usually located in the territories of the internal carotid and vertebro-basilar-posterior cerebral systems. In such cases the neurosurgeon may find and remove the entire AVM. However, if angiographic investigation was incomplete, there is the inherent danger that he will only remove l /i, Vz or 2 /з of the AVM. Repeat angiography performed either as a routine postoperative control or because of recurrence of symptoms will visualize the rest of the AVM, which may be of small or even larger size. Three cases of our own material belong to this group (Fig 3.82).

Fig 3.82A-C

A A 4 year old girl suffered from very severe headache, followed by an attack of unconsciousness lasting for several minutes. Lumbar puncture revealed bloody cerebro-spinal fluid. The right carotid angiogram showed barely discernible microangiomas (arrows). At exploration a huge intraventricular hematoma was evacuated (Dr. del Vivo) from the right lateral ventricle, and a small arterio-venous malformation was seen and removed from the floor of the right frontal horn (1969). Histological examination revealed an arteriovenous malformation. Postopera-tively, a left hemiparesis gradually disappeared. В 6 years later she suffered another hemorrhage, and a right brachial angiogram demonstrated multiple AVMs within the entire corpus callosum. The AVM and a large intracallosal hematoma were removed microsurgically. The postoperative course was uneventful. С Postoperative angiography 3 months later demonstrated that the malformation had been completely excised.

References p. 3fi

*cferences p. 383

Incomplete Visualization of the AVM In cases with large intracerebral hematomas which compress and displace the nidus of the AVM, complete angiographic evaluation may fail to reve al the actual size of the lesion. On surgical

Growth

147

exploration of such cases the hematoma and a portion of the AVM will be removed. However, other portions of the AVM may remain undiscovered and left in place. This was observed in 4 cases of the present series (Figs 3.83-3.85).

Fig 3.83A-D At the age of 14 years, this patient was operated abroad for a left temporal lobe hematoma which was removed. Histology showed an AVM. A-B 4 years later another subarachnoid hemorrhage occured. Angiography showed displacement of middle cerebral branches and a small plexiform tangle (arrow) of pathological arteries (A), as well as an umbrella shaped venous drainage (B). At the second operation a large hematoma was removed along with an AVM in side the superior temporal gyrus. The postoperative course was uneventful. Postoperative CT did not show any pathology. The patient was able to continue his studies. 4 years after the second operation another stroke occurred. C-D Carotid (C) and vertebral (D) angiog-raphy demonstrated a more posteriorly and medially located AVM in the paratrigonal area.

148

3. Pathological Considerations

References p. 383 • Fig3.84A-F This 26 year old enginersuffered a stroke. CT showed a right frontal hematoma (A). В СТ after removal of hematoma and or the AVM.

Fig 3.84C-D On carotid angiography the AVM exhibited unusual venous drainage. The patient fully recovered from a comatose condition but only partially, from a left sided hemiplegia. E-F 2 years later, a repeat angiogram showed tiny pathological vessels within the deep frontal white matter. We believe that this portion of the AVM was compressed by the hematoma and could not be recognized during surgery. We do not believe that this represents regrowth of the AVM. Further surgery is recommended but the patient is reluctant to accept it.

p. 383

Fig 3.85A-E A 24 year old male presented clinically with stroke. MRI showed a large right frontal hematoma (A). In a lower section, a small frontoopercular AVM was seen (B). C-D Arterial and venous phases of carotid angiography showed the compressed AVM with cortical and subependymal drainage. E The hematoma was removed and the compressed AVM located on the basal aspect of the hematoma was believed to have been eliminated. The postoperative course was uneventful. 4 weeks later angiography showed a residual AVM supplied by M1 feeders (E). His present situation is the same as the previous case.

Growth

149

150

3. Pathological Considerations

References p. 383^

Incomplete Removal or Regrowth of the AVM There are mainly two situations in which an AVM may be removed incompletely: 1) Portions of the AVM may be really hidden and thus inaccessible or 2) due to bipolar coagulation technique, the surgeon may dissect through the AVM, leaving some portions of it untouched. In a case with a right frontolateral subcortical AVM the lesion was believed completely removed. This was also confirmed by postoperative angiography, performed one week after operation. Three years later the patient presented with a new intracerebral hemorrhage, located in the area of the removed AVM. Angiography surprisingly revealed a large AVM in the identical location as the initial lesion (Fig 3.86). Two explanations may be given for this phenomenon:

Fig 3.86A-H

A-B This 17 year old female patient's right carotid angiogram revealed a wedged shaped AVM located in the fronta opercular area. It was supplied by arteries arising from M1 and M2 segments of the middle cerebral artery, as well as fror A1 and A2 segments of anterior cerebral artery. The venous drainage occured through a superficial ascending vein anc through the internal cerebral vein. The AVM was removed in 1977.

-erences p. 383

Growth

151

3.86C-D Angiography performed 10 days after operation seemed to show complete removal of the AVM.

Fig 3.86E-F 7 years later another subarachnoid hemorrhage occurred and repeat angiography showed, surprisingly, an AVM identical to that seen on the first angiogram.

Fig 3.86G, H

152

3. Pathological Considerations

References p. 383

Fig 3.86G-H Second operation was also uneventful and angiography (G) and CT (H) performed 4 months later, con firmed the radical removal. This case raises the question of whether there was a true regrowth of the rnalformatio or whether the first removal was incomplete.

References p. 383

Growth

Fig 3.87A-J A 13 year old girl presented with subarachnoid hemorrhage. CT showed an unusually located AVM on the medial surface of the right superior temporal gyrus extending towards the mediobasal temporal lobe (A). Carotid and vertebral angiography (B-D) confirmed the presence of an AVM. The AVM was removed through a sulcal approach. CT 1 week after surgery (E) was interpreted as normal. The repeat CT 6 months later however, showed a suspicious finding within the previous operative field (F).

Fig3.87G-J

153

154

3. Pathological Considerations

References p. 3el

Fig 3.87

This symptom-free patient underwent repeat angiography which showed a small AVM in the same location as before the operation with feeding arteries arising from M1, M2 and P2 segments (G-H). A second operation was performed and the AVM was removed.

Postoperative angiography (I-J) performed 9 months later showed complete disappearance of the AVM. We believe f in this case the AVM was not completely removed at the first operation, despite the fact that the first postoperative С failed to show any pathology. Remarkable in this case is the rapid growing or enlarging tendency of the AVM (at lea according to CT).

References p. 383

Growth

155

AVMs). AVM growth was proven in all cases by both CT and angiography. All cases were characterized angiographically by an increase in diameter of the vessels as well as by a numerical increase of the feeding arteries (Figs 3.88-3.90).

Fig 3.88A-F This 3 year old boy first presented with an episode of subarachnoid hemorrhage. Angiography performed in 1966 was normal (A-B).

Fig3.88C-F

156

3. Pathological Considerations

продолжение References p.

эгепсез р. 383

Growth

157

Fig 3.89A-F

A This 28 year old female patient had been admitted in 1963 at the age of 16 to the neurosurgical clinic of Bern because of a SAH. Left carotid angiography showed a small paracallosal AVM (arrows). No operation was performed. Several acute attacks of bilateral sciatica have occured. They usually cleared up quickly after bed rest but a severe attack followed 12 years later in 1975. The angiographic study by Prof. Huber of Bern, showed marked enlargement of the callosal-splenial and left parasplenial AVM (B-D).

Fig3.89C-F

158

3. Pathological Considerations

References p. 35'

References p. 383

Growth

159

Fig3.90E-l

160

3. Pathological Considerations

References p.

References p. 384

Spontaneous Thrombosis and Regression

161

Spontaneous Thrombosis and Regression of AVMs Spontaneous Thrombosis and Regression Altogether, some 50 cases of spontaneous total or partial regression of intracranial (cerebral and dural) AVMs have been reported over the past 40 years (Norlen 1949, Svien and Peserico 1960, Pecker et al. 1961, Castaigne et al. 1961, Fischer et al. 1969, Lakke 1970, Kushner and Alexander 1970, Abroms et al. 1971, Conforti 1971, Eisenmann et al. 1972, Sukoff et al. 1972, Kirn et al. 1973, Levine et al. 1973, Spetzler et al. 1974, Magidson and Weinberg 1976, Hansen and Soogard 1976, Kendall and Claveria 1976, Scott and Garrido 1977, Dyck 1977, Mabe and Furuse 1977, Bell et al. 1978, Sartor 1978, Endo et al. 1979, Leo et al. 1979, London and Enzmann 1981, Huber 1982, Omojola et al. 1982, Nehls and Pittmann 1982 (see Table I, p. 778), Wharen et al. 1982, Wakai et al. 1983 (see Table on p. 379), Mitnick et al. 1984, Stein 1984a,b, Pasqualin et al. 1985). The regression has been judged to be confirmed either by angiography or by isotope or CT scan. The exact incidence of spontaneous regression is uncertain, although Pasqualin et al. (1985) found total occlusion in 2.2% of their series of 180 intracranial AVMs. Stein (1984b) found that in his series, of the 10% of AVMs which remained unoper-ated, one third became smaller with time. Operative and autopsy findings of a totally throm-bosed AVM, which had been angiographically invisible, together with more recent CT scan evidence of thrombosed AVM (Kendall and Claveria 1976), suggest that, perhaps, spontaneous thrombosis and regression of intracranial AVMs is more common than formerly suspected. However, such findings usually relate to previously unsuspected lesions with no earlier angiographic evidence of their existence. It therefore remains uncertain as to whether these newly-found thrombosed lesions represent an endstage of some other form of regression or even a malformation which had undergone spontaneous occlusion during embryonic development. Spontaneous regressions of AVMs must be differentiated from those achieved by treatment aimed at thrombosis through the use of embolization, glue, ligation and radiotherapy. The difficulty in producing total occlusion of a large AVM by these means perhaps gives some clue as to why spontaneous total thrombosis does not occur more frequently. Pasqualin et al. (1985) concurs with the notion (Conforti 1971, Omojola et al. 1982) that spontaneous complete thrombosis is more likely to occur in small AVMs drained by a single vein. of AVMs.

Case reports are too few in number to draw any firm conclusions as to the distribution of AVMs within the brain or as to the distribution of feeding vessels to lesions undergoing spontaneous resolution. Most reported cases of spontaneous regression of AVM have occurred in adults between the ages of 30 and 60 and the time course for complete occlusion has varied from around 6 months to 21 years. In most instances the regression has been acute with no change in size of the lesion until apparently complete obliteration has occurred. Kushner and Alexander (1970) and Lakke (1970), however, have described gradual (angiographic) regression of intracranial AVMs. The exact mechanisms involved in spontaneous AVM regression are uncertain but the most common is almost certainly that of compression of the lesion (leading to acute intravascular thrombosis) from intracranial hemorrhage. Other possible mechanisms are included in Table 3.11 (see Pasqualin et al. 1985). Sukoff et al. (1972) described a case of spontaneous subtotal acute occlusion of a large AVM fed principally by the MCA. They speculated as to whether the underlying cause of the thrombosis was embolism or possibly atheroma in the MCA induced by hemodynamic changes in the vessel. There was no supportive evidence for either cause and it was felt that retrograde thrombosis from the AVM itself had possibly occluded the vessel. Table 3.11 Possible mechanisms underlying spontaneous regression of intracerebral AVMs 1. Acute thrombosis from intracranial hemorrhage. This may be due to compression from mass effect or edema, or to reduced flow secondary to vasospasm 2. Subacute thrombosis. This may be due to increased blood coaguability or turbulence or to alterations in flow - particularly in dural AVMs 3. Occlusion of feeding vessels from atheroma and embolism 4. Occlusion of draining veins and sinuses 5. Destruction of occult, cryptic and micro AVMs from hemorrhage

162

3. Pathological Considerations

A cautionary note on the interpretation of angiographic features suggesting regression of AVMs in the presence of SAH was recorded by London and Enzmann (1981). Vasospasm secondary to a bleed from one of multiple aneurysms coincidental to a large AVM led to transient changes in vessel caliber suggesting regression of the AVM. Repeat angiography after the vasospasm had resolved showed the AVM in its original form. We have seen one similar case (see Chapter 6, Fig 6.21). Although an AVM which has undergone spontaneous thrombosis/regression may be demonstrated as an incidental finding on CT, or may be clinically silent, those cases in whom thrombosis is secondary to a significant intracerebral bleed are likely to present at the time with the typical symptoms of raised intracranial pressure, focal neurological signs or epilepsy. [There is a high incidence of continuing epilepsy reported by several authors in cases of thromxbosed AVM (Wharen et al. 1982). The surgeon should not become complacent regarding the risk of continuing hemorrhage even after repeated angiography has suggested significant or total regression of an AVM. This is well shown in a case of Huber (1982) (p. 163). See case report (Fig 3.91). In our own series, frequently single thrombosed, white coloured vessels, and in 12 cases (3%), partial AVM thrombosis, have been seen at surgical exploration. There have been two cases among the unoperated group, of spontaneous total occlusion, demonstrated only angiographically. However, in one case the MR showed a persistent AVM (Fig 3.92). The management of seemingly totally thrombosed AVM seen on CT scan will depend upon the age and general condition of the patient, the site of the AVM within the brain and its surgical accessibility, the presence of intractable epilepsy and the angiographic findings. If the scan suggests total thrombosis and the AVM is invisible on angiography, then exploration and extirpation of the lesion to prevent recurrent bleeding seems unwarranted. ) Continuing epilepsy in the face of comprehensive j medical treatment may constitute grounds for excision of the lesion in appropriate cases.

References p. 3841

References p. 384

Spontaneous Thrombosis and Regression

Fig 3.91A-E This was an impressive case of total spontaneous regression of an occipital AVM as demonstrated on successive angiograms. Despite complete angio-graphic disappearance of the AVM, hemorrhage occurred. E CT scan. Massive intraventricular hemorrhage from angiographically invisible AVM containing calcifications. Progressive thrombosis involved a portion of the malformation. The non thrombosed part of lesion fed by the posterior cerebral artery was destroyed by hemorrhage (confirmed at necropsy) (case reported by Huber 1982).

163

164

3. Pathological Considerations

References p.

References p. 385

Multiple Cerebral AVMs

165

Multiple AVMs Even though AVMs are considered to be of developmental origin arising at an embryonic stage, which would make multiple lesions likely, there have been few reports of more than one intracranial AVM arising in any single patient. WyburnMason (1943) called attention to the coexistence of multiple arteriovenous lesions. Ferret and Nishioka mentioned 3 such cases in 1966 but did not elaborate further (angiomas other than true AVMs may have thus been included). Other reports were those of Voigt et al. (1973) and of Schlachter et al. (1980) who described 4 possible multifocal AVMs. In one case, however, a second cryptic lesion was assumed but not radiologically proven, and in 2 of the remaining cases there was no absolute proof that the demonstrated lesion did not represent a single large malformation. Other single case reports include those of Hook and Johanson (1958), Jellinger (1957), and Paterson and McKissock (1956). Tarnaki et al. (1971) described a single patient having AVMs of the scalp, dura, retina, cerebrum and posterior fossa treated by radiotherapy. As stressed by Schlachter et al. (1980), comprehensive neuroradiological investigation is essential to identify multiple lesions, but even then they may be missed if a lesion is partially thrombosed or compressed or is very small. Suspicion may be raised as to the presence of a second "occult" lesion by an area of enhancement or of unexplained atrophy with ventricular dilatation on the CT. Zellem and Buchheit (1985) noted a strong family history of cerebrovascular disease in their case, but were not able to show evidence of AVMs as a cause for cerebral hemorrhage in other members of the family. Multiple telangiectases are well known to occur in the autosomal dominant OslerWeber-Rendu disease but the only recorded cases of multiple anomalies of different types (e. g. combined telangiectasies, cavernoma and venous medullary malformation, medullary venous malformation with cryptic AVM within it) are those described by Huang et al. (1984) and McCormick (1984). McCormick (1985) described 6% of autopsy cases having multiple angiomas but the incidence of AVM among these is not stated.

Multiple Cerebral AVMs Hanieh et al. (1981) described a case of right frontal and left parietal AVM associated with subcutaneous vascular malformations in the hand. Berenstein (1981) reported on a case of angiographically proven bilateral thalamic AVM supplied by the lateral and medial lenticulostriate arteries. Stone et al. (1983) documented a single case of proven biparietal AVMs. Zellem and Buchheit (1985) reported a single case having 3 separate supratentorial AVMs (L frontal, L temporal, R temporal) confirmed angiographically, of which 2 were removed surgically. Multiple intracranial AVMs may be unilateral (within one hemisphere) or bilateral, or in the midline, such as in the corpus callosum. Treatment of multiple AVMs is essentially the same as for single lesions. Each must be regarded as a source of potential recurrent hemorrhage such that the aim should be complete obliteration of those lesions which are amenable to surgical excision or to transvascular occlusion. Of our own cases there were 15 patients (3.0%) of the total observed 500 cases: — Two patients with scattered diffuse AVMs in both hemispheres (Figs 3.93, 3.94), — Two patients with extensive bilateral strio-capsulo-thalamic AVMs (Figs 3.95, 3.96), — One case with left sided thalamic and orbital AVM (Fig 3.97), — One case with supra- and infratentorial parapontine and mesencephalic and orbital AVMs (only the infratentorial AVM could be operated) (Fig 3.98), — Two cases with combined supra- and infratentorial AVMs (Figs 3.99, 3.100), — One case with galenic and mesencephalic AVMs (Fig 3.101), — One patient with left parietal and right thalamic AVMs has been operated in two stages (Fig 3.102), — Two out of three patients with multiple callosal and plexal AVMs have been operated in the same approach (Figs 3.103-3.105), — One patient with left medial temporal AVM who died showed another small angiographically non-visualized AVM on the right frontal lobe at autopsy.

166

3. Pathological Considerations

References p. 385 Fig3.93A-F A 19 year old patient came in with epileptic seizures. A Right carotid angiography showed г diffuse type AVM scattered in fronto-operculo-insular area. It was supplied by middle cerebral artery branches. В Left carotid angiography demonstrated diffuse type callosal and septai AVMs.

References p. 385

Multiple Cerebral AVMs

167

Fig 3.93C-D Frontal view of right and left carotid angiogram showed the diffuse cortical and subcortical AVM being supplied by feeding arteries arising from A1 and M1 segments. E-F Vertebral angiography showed further AVMs in middle callosal and splenial area. The venous phase showed two separate venous systems draining the AVMs. With such extensive AVMs operation could not be recommended.

168

3. Pathological Considerations

References p. 36: Fig 3.94A-C This 30 year old patient with repeated attacks of subarachnoid hemorrhages had bilateral carotid angiography pe-formed in 1974 (A right side, B-C left side) which showed dif fuse type hemispheric bilateral with multiple distal aneurysms. j Inoperable case. Radiation recommended.

References p. 385

Multiple Cerebral AVMs

169

Fig 3.95A-F Four vessel angiography was performed on an

18 year old female patient after subarachnoid hemorrhage. There were multiple (3 or 4) AVMs visible in deep portions of both hemispheres strio-capsulo-thalamic. A Right carotid angiography. В Left carotid angiography. С Vertebral angiography.

Fig3.95D-F

170

3. Pathological Considerations

References p. 385

Fig3.95D-F Frontal view of right, left and vertebral angiography. Irradiation was performed in Boston in 1977. Note the aplasia of the straight sinus and the course of draining veins to ascending parietooccipital median veins. She lives to South America and no follow up is available.

References p. 385

Fig 3.96A-C In another case with bilateral AVMs in the strio-capsulothalamic region, radiation was recommended. Note the aplasia of the straight sinus (C).

Multiple Cerebral AVMs

171

172

3. Pathological Considerations

Fig 3.97A-H A-B A 7 year old boy, with subarachnoid hemorrhage had a diffuse AVM in thalamus shown on left carotid angiography in 1966. No therapy was performed. Note findings suspicious for AVM in the orbit. C-D Repeat left carotid and vertebral angiography performed in 1974 showed enormously enlargement by dilatation of the thalamic AVM. Note also the dilated ophthalmic artery supplying a second plexiform type retrobulbar AVM whiccaused exophthalmos. E-F Carotid (E) and vertebral (F) angiography shows the extension of the AVM within the thalamus. No therapy w a s performed. G CT in 1986 shows a large thalamic lesion and occlusive hydrocephalus. H The MRI in 1986 shows absence of the straight sinus. Severe mental and neurological deterioration, blindness bedridden.

References p. 385

Multiple Cerebral AVMs

173

174

3. Pathological Considerations

Fig 3.98A-D Three AVMs were found in this 16 year old girl. A-B Vertebral angiography showed a lateral prepontine AVM as well as a second AVM in the dorsal mesen-cephalon (arrows).

References p. 385

Fig 3.99A-C This 52 year old patient had two AVMs one supratentorial in the right parietal area, and a second in the territory of the right PICA. The patient refused the surgery.

Multiple Cerebral AVMs

175

176

3. Pathological Considerations

References p. 385

Fig3.100A-B A 37 year old male patient presented with a thalamic and a mesencephalic AVM. No operation was performed. Note the absence of the straight sinus.

Fig 3.101A-B Pre-(A), postoperative (B) angiograms (1976) in a 3 year old boy with AVM of vein of Galen showed afis-tulous connection of the left PCA to the vein of Galen plus a mesencephalic nidus (arrows). He will be radiated in StocK-holm (1986).

References p. 385

Multiple Cerebral AVMs

177

E-F Preoperative brachial angiography showed the right thalamic AVM, whereas the left carotid angiogram did not show the left parietal lesion. Note the stenosis of the straight sinus. Histology confirmed a typical AVM in both locations. The patient remains an invalid as he was preoperatively.

178

3. Pathological Considerations

References p. 385

A-D Carotid (A-B) and vertebral (C-D) angiograms showed a combination of multiple nidus AVMs located within the entire corpus callosum as well as in the choroid plexus of the Illrd ventricle. Each AVM had its own venous drainage.

References p. 385 Fig. 3.103E-G All AVMs were removed in one session through a paramedian frontoparietal osteoplastic craniotomy and interhemispheric approach. This was followed by impressive recovery of a preoperative paraplegic condition and mental retardation of an 8 year old girl la shunt operation was done before craniotomy).

Multiple Cerebral AVMs

179

180

3. Pathological Considerations

References p. 385

Fig3.104A-D

A A combination of multiple AVMs located within the corpus callosum, septum pellucidum and choroid plexus. В Each AVM has its own separate venous drainage towards the superior sagittal sinus, internal cerebral veins, basal veins and petrosal veins. С One part of the AVM drains into the inferior and superior sagittal sinuses, whereas another part drains into the internal cerebral and basal veins, and ultimately towards the petrosal sinus. The straight sinus is poorly visualized. D Removal of all 3 malformations was accomplished through a frontoparietal paramedian craniotomy and interhemispheric approach. Stormy postoperative course ensued with mental deterioration. Slow recovery followed shunting. 9 years after surgery the patient is able to care for himself but is not able to work as a computer engineer. The patient refused postoperative angiogra-phy. CT showed no evidence of AVM (D).

References p. 385 Fig 3.105A-C Carotid and vertebral angiography showed three AVMs: one in the genu of corpus callosum, a second in splenium and third in the choroid plexus in this patient .vho did not accept surgery. Note the stenosis of the straight sinus (arrow) and the unusual redistribution of . snous flow.

Multiple Cerebral AVMs

181

182

3. Pathological Considerations

Intracranial and Intraspinal AVMs Only 7 such cases have been recorded until recently (Wyburn-Mason 1943, Krayenbuhl et al. 1969, DiChiro and Werner 1973, Hash et al. 1975, Hoffman et al. 1976). Parkinson and West (1977) added a rare case of SAH first from intracranial

References p. 385-36f and then intraspinal AVM, each of which was sucl cessfully removed. Hoffman et al. (1976) de-scribed a case of extensive spinal cord AVM and right temporal AVM in a child. In our series there was no such combination. however, 2 patients did present with combined AVMs of medulla oblongata and cervical spinal cord.

Association of Persistent Trigeminal Artery and AVM One might also expect a frequent association of AVMs with other vascular anomalies known to be of congenital origin. With the exception of aneurysms, known to occur in 2.7-16.7% of cases with AVM, other congenital vascular anomalies, such as persistent embryonic caroticobasilar anastomoses are extremely rarely observed. The first case was reported by Krayenbuhl and Ya§argil (1957). Jayaraman et al. (1977) collected and tab-

ulated 11 cases of persistent trigeminal artery associated with an arteriovenous malformation from the literature and added one further case. Among a series of 105 cases of cerebral arterio- venous malformations, Moody and Poppen (19701 observed only one case associated with a persistent trigeminal artery. No occurrence of persistent. trigeminal artery was observed in this series of 500 AVMs.

Association of Aneurysm and AVM The first descriptions of an association between intracranial aneurysm and AVM was credited by Anderson and Blackwood (1959) to Laves in 1925 and Stewart and Ashby in 1930-31. Since then there have been many sporadic reports of these lesions occurring together and several attempts have been made to confirm the various theories which have been postulated to explain this association (Walsh and King 1942, Arieti and Gray 1944, Moniz and Guerra 1953, Christensen and Larsen 1954, Kane and Foley 1954, King et al. 1954, Murphy 1954, Paillas et al. 1956, Paterson and McKissock 1956, Descuns et al. 1956, Ley 1957, BoydWilson 1959, Anderson and Black-wood 1959, Caram 1959, Fine et al. 1960, Gibson and Rocha Melo 1960, Cronqvist and Troupp 1966, Ferret and Nishioka 1966, Locksley 1966, Nocola and Rizzoli 1966, Sakata et al. 1968, Murakami et al. 1971, Shenkin et al. 1971, Arai et al. 1972, Voigt et al. 1973, Fujino et al. 1976, Tsu-chita and Miyazaki 1976, Baba et al. 1977, Fukawa et al. 1977, Onuma et al. 1977, Yamagu-chi et al. 1977, Arabi and Chambers 1978, Higashi et al. 1979, Suzuki and Onuma 1979, Hatanaka et al. 1980, Hashimoto et al. 1980, Niino et al. 1980, Parkinson and Bachers 1980, Takara et al. 1980, Hayashi et al. 1981, Koulouris and Rizzoli 1981, Gamache et al. 1981, Kassell 1981, Malis 1982, Miyasaka et al. 1982, Gacs et al. 1983, Hudgins et

al. 1983, Gardeur et al. 1983, Kikuchi et al. 1984. Okamoto et al. 1984, Garza-Mercado et al. 1984 Waga et al. 1985, Nehls and Carter 1985, Batjer et al. 1986). This topic has already been discussed in

-Terences p. 386

Association of Aneurysm and AVM

183

common developmental vascular abnormality producing both aneurysm and AVM was first propounded by Arieti and Gray (1944). Boyd-Wilson (1959) suggested that the lesions were merely coincidental whereas Paterson and McKissock (1956), Shenkin et al. (1971), and Gacs et al. (1983) support a theory of hemodynamic factors, including the role of a hyperdynamic circulatory state. Gardeur et al. (1983) found 85 cases in the literature, added 8 cases of their own, and discussed the hemodynamic origin of the aneurysms. Okamoto et al. (1984) added 5 cases of their own to 73 cases previously reported in the literature and carried out a statistical analysis, comparing these 78 cases (associated with 119 aneurysms) with over 500 cases of isolated aneurysm from the Cooperative Study. The principal aim was to study the distribution of aneurysm by site and relate this to their occurrence on potential and real feeding vessels in the two populations. Their figures and statistical comparisons are difficult to follow, but they concluded that since the distribution of aneurysms (in the study group) on any given feeding artery to an AVM was greatly in excess of the expected distribution in the absence of an AVM, then there presumably exists an underlying cause, such as hemodynamic stress, in the development of associated aneurysms. Aneurysms occurring at sites well distant from AVMs or their major feeding vessels were felt to be purely coincidental.

Fig 3.106A-B Occurence of associated aneurysms related and unrelated to high flow, a Small aneurysms in the vicinity of AVM. b Aneurysms on a proximal related segment, с Aneurysms on unrelated arteries.

184

3. Pathological Considerations

In Ferret and Nishioka's 37 combined cases (1966) the aneurysms were located on major feeding vessels to the AVM in 37%, well proximal on the feeding vessels in 21% and unrelated to the AVM in 42%. Miyasaka et al. (1982) reviewed the angiograms of 132 consecutive patients with AVM and found 43 aneurysms in 22 of these patients (16.7%). Thirteen patients had single aneurysms. They found that aneurysms were more likely to occur in older patients and in those patients with larger AVMs. They further suggested (based on the findings of Stehbens, 1972) that since the prevalence of AVMs in a large autopsied series of patients with cerebral aneurysms was not significantly higher than in a control group without aneurysm, then the same developmental defect is unlikely to account for both lesions. Similarly, the theory of coincidental association was thought to be unlikely. The distribution of aneurysms and of infundibula on major feeding vessels to the AVMs, remote from the circle of Willis, was such that they concluded that hemodynamic changes in the arteries supplying the malformation must have some role in the etiology of concurrent aneurysm. These conclusions supported the views of Hayashi et al. (1981). Nehls and Carter (1985) described a case of multiple unusual aneurysms (left meningohypophyseal trunk, left ICA, right ICA and MCA) in association with a left occipital AVM. They concluded that the aneurysm on the meningohypophyseal feeder to the AVM may have been produced through hemodynamic changes within this vessel whereas the other nonhemodynamically related aneurysms represented a more generalized tendency toward the formation of vascular lesions in this patient. Our own observations and thoughts (Table 3.13) force us to question some of the conclusions described above. We would make the following points: 1. If increased flow alone factors plays a significant role in the etiology of concurrent aneurysms then we should see far more aneurysms than have been observed either directly related to feeding arteries or even ipsilateral to the AVM (Table 3.14). 2. Similarly, if increased flow were the primary factor, we should see more aneurysms associated with fistulous communications and with giant or large AVMs with high flow rates. Our own figures show that this is not the case (Table 3.13).

References p. 386 Table 3.13 Frequency of type of operated AVM and associated aneurysms AVM patients Number with Frequency aneurysms

Type of AVM Fistula (high flow)

10

0

0

V. of Galen AVM

16

0

0

Giant AVM

17

2

1 1 .8%

Large AVM

142

15

10.5%

Moderate AVM

174

20

1 1. 5%

Small AVM

61

8

13.1%

This present series comprises a total of 500 cases of AVM; 86 of these were not operated, of which 5 had aneurysms (5.8%). Of the 414 operated cases, 45 (10.86%) had associated aneurysms. In 3 cases (0.7%) the aneurysms were totally unrelated to the AVM (contralateral angiographically nonparticipating arteries like ICA, АСА, MCA or PCA) (see Vol. I, p. 312). The remainder were ipsilateral lesions. Some were large, readily evident lesions on angiography and at surgery, while others were smaller and seen only at surgery (presumably not filling readily on angiography owing to abnormal regional flow). These latter lesions, however, were distinguished from common small blebs which are not considered significant. The\ were related to the AVMs as shown in Table 3.14. The term distant implies an aneurysm on a major vessel of the circle of Willis (usual aneurysm site i whereas close implies an aneurysm arising in an unusual position and within 1—2 cm of the AVM. Table 3.14 Size of aneurysm

3-20 mm

Small <3 mm

Distant from AVM

24

6

18

Close to AVM

16

4

12

40

10

30

2.5% 9.7%

7.2%

sferences p. 386

Association of Aneurysm and AVM

185

giant, large, moderate, and small forms of AVM. There were no aneurysms found in direct relation to the forms of AVM known to have the very highest flow rates (see Table 3.13). Considering the obvious high flow to some of the surgically explored AVMs, it is indeed surprising that there was not a greater total incidence of aneurysm if hemodynamic factors are chiefly responsible for aneurysm production. Perhaps the aneurysms which do occur on these vessels are in some way part of the total developmental abnormality and should not be considered as saccular aneurysms in the usual sense. Clearly, further histopathological studies of these lesions are required. Thus, in this present series, no direct relationship has been found between size of AVM, the apparent degree of flow as suggested by angiography, and the presence of aneurysm (Figs 3.107-3.111). Aneurysms have been found in association with low flow AVMs and have been observed even with cavernous malformation in other patients.

Fig 3.107A-B A left cingular AVM in a 55 year old man who presented with severe neurological and mental deterioration. The AVM was associated with multiple unruptured aneurysms located on the proximal and distal portions of the feeding arteries (arrows). A lateral, В frontal carotid angiography. The AVM was removed and the aneurysms were clipped in a one stage operation. The patient's condition remained unchanged after surgery (see chapter Complications, Vol. Ill B).

186

3. Pathological Considerations

References p. 386 Fig 3.108 Association of large ruptured aneurysm (arrow) of M1 segment of the left middle cerebral artery and a small insular AVM in a comatose 44 year old male patient who died before scheduled surgical intervention.

Fig 3.109A-F A left temporal AVM associated with 2 unruptured aneurysms (arrows) of the middle cerebral artery. Preoperative frontal carotid angiogram (A), postoperative frontal carotid angiogram (B), after removal of AVM and clipping of aneurysms, pre- (C) and postoperative lateral carotid angiograms (D).

srences p. 386

Association of Aneurysm and AVM

187

Fig 3.109E-F Preoperative lateral vertebral angiogram (E), postoperative lateral vertebral angiogram (F). The postoperative course was uneventful in this 28 year old female.

188

3. Pathological Considerations продолжение

References p. 386

Fig 3 . 1 1 1 A - C An AVM of the right cerebellar hemispheric associated with unruptured multiple aneurysms of the right PICA (arrows) (A). Three other smaller aneurysms, invisible on vertebral angiography (B), were discovered on exploration and clipped. The AVM with its large hematoma was removed. The postoperative course in this 50 years old male was uneventful. C Artistic drawing of the AVM and aneurysms.

References p. 386

Association of Aneurysm and AVM

The sites of AVM and frequency of associated aneurysms are shown in Table 3.15. Table 3.15 Sites of AVM and frequency of associated aneurysms No. of patients with No. AVM Site of AVM Total aneurysms %age Frontal

48

12

25.0

Parietal

49

2

4.1

Temporal

53

6

11.3

Insular

23

5

21.7

Occipital

30

7

23.3

Cerebellar

58

6

10.3

261

38

14.6

Amygdalohippocampal 17

2

11.8

Parasplenial

40

2

5.0

Callosocingular

41

3

7.3

Hd. Caud. Nc.

11

-

0.0

Strio-cap-thal.

15

-

0.0

Galenic

16

-

0.0

Mesencephalic

6

-

0.0

Pontine

4

-

0.0

Plexal

3

-

0.0

153

4.6

Of interest here is that the convexity AVMs, especially in the frontal and occipital areas present significant incidence of aneurysms, whereas central AVMs, especially the galenic AVM and pure fis-tulous connections are surprisingly not associated with concurrent aneurysms. Of the 45 patients recorded, 34 had single and 11 had multiple aneurysms (9 patients with 2 aneurysms, and 2 patients with 3 aneurysms). Previous reports of giant aneurysms associated with AVM are sparse. Hatanaka et al. (1980) described a patient with a large AVM and 2 giant aneurysms and Suzuki et al. (1984) described a case of hemorrhage from a giant aneurysmal dilatation as part of a large frontal AVM in a 3 year old child.

189

Hemorrhage in cases (group 2) in which both AVM and aneurysms are found simultaneously may be either from the AVM or from the aneurysm. Despite both CT scan and angiographic study it may be difficult to decide which lesion has bled, although the identification of extravasated blood on CT remains the most accurate way of identifying the source of bleeding prior to surgery. We observed 4 such cases. Hemorrhages in group 1 and 3 (peripheral related and unrelated aneurysms) can be identified more easily (Fig 3.106). It is clearly preferable to manage both lesions at one operation if this is possible. Otherwise, the initial management should be aimed at the lesion which has bled. Reviewing the previous findings of Ferret and Nishioka (1966), Suzuki and Onuma (1979) and Gacs et al. (1983) and in the light of their own case, Nehls and Carter (1985) conclude that in general, when SAH occurs in patients with both AVM and aneurysm, the site of bleeding is more commonly the AVM, except in special circumstances such as cerebellar lesions where the trend may be reversed. In the case of Waga et al. (1985) the aneurysm caused recurrent subarachnoid hemorrhages. Drake and Girvin (1976) and Luessenhop et al. (1965) report isolated instances of associated aneurysms rupturing soon after treatment (surgery or embolization) of an AVM, but this appears to be a rare event. It is, perhaps, only of concern in the treatment of large aneurysms proximal to very high flow AVMs which cannot be dealt with simultaneously. After surgical or embolization treatment of an AVM there is usually a decrease in size of the feeding arteries and their principal branches. Reduced perfusion may lead to shrinkage or thrombosis of an untreated associated aneurysms, as demonstrated on repeat angiography, and may render further treatment unnecessary (Shenkin et al. 1971, Hayashi et al. 1981, Miyasaka et al. 1982). Aneurysms which do not regress may be treated as any other unruptured aneurysms after excision of the AVM.

190 3. Pathological Considerations

References p.

Intracranial AVM with Stenosis and Occlusion of Major Vessels Arterial Just two cases of associated occlusion of intracranial arteries have been reported in the literature. The first was that of Sukoff et al. (1972) which is discussed in the section on spontaneous regression of AVMs above. This was a case of subtotal acute thrombosis of an AVM associated with MCA occlusion. The other case is that of Aoki and Mizutani (1985) in which angiography revealed an occluded right MCA with an ipsilateral AVM fed by the posterior temporal artery through collaterals from PCA. Removal of the AVM resulted in immediate hemorrhage in the AVM bed and in massive brain swelling. This was ascribed to normal perfusion pressure break through. The patient recovered and repeat angiography showed that excision of the AVM was complete but there was now marked filling of the middle cerebral hemispheric branches in the region of the previously occluded MCA. In the absence of any source of

emboli and with no evidence for focal or generalized atheroma it is difficult to be sure as to the underlying cause of thrombosis in the MCA. Two further unique cases from the series of Zurich of an AVM associated with occlusion of the 1CA were reported by Schubiger (1979). In both cases unusual and extensive collateral pathways through a dural rete mirabile and capillary anastomoses between thalamic arteries were observed angiographically (Fig 3.112). Since 1979 only one patient was found to have a small left temporal AVM and a moderate stenosis at the siphon of the right 1C A. One would also expect that due to the high-flow load on the vessel wall the incidence of atherosclerotic occlusion in cases with cerebral AVM should be higher than it actually is. It is probably the significantly reduced vascular resistance in cases with AVM which may account for the rare occurrence of arterial occlusions in such cases.

Fig 3 1 1 2 A - F This 56 year old male presented with an ischemic stroke and had an unusual occlusion of the supracli-noid internal carotid artery shown on this left carotid study (A). Note the extra-intracranial collaterals. В Lateral view of left external carotid angiography showed an extensive collateral network resembling a rete mirabile arising from internal maxillary and middle meningeal arteries. There was surprising visualization of a pial parietal AVM through this dural collateral systems.

References p. 387

Arterial

191

Fig 3 . 1 1 2 C Late phase showing the nidus and a single draining vein. D Contralateral frontal carotid angiography showed a second nidus in the callosal area. Note the moyamoya like collaterals replacing the left A1 (arrow), and also supplying the left M1.

Fig 3.112E-F Lateral vertebral angiography disclosed a further nidus in the left parasplenial and thalamic areas seen also on frontal view (F).

192

3. Pathological Considerations

Moya-Moya Disease Of our own cases, none has been found to have an AVM together with evidence of Moya-Moya disease. The possibility of an occasional association between AVM, arterial stenosis and Moya-Moya is, however, interesting from several points of view. Moya-Moya has, in the past, been considered as being an arteriovenous malformation, although the developmental defect presumably occurs much later than in the case of the true AVM, perhaps even postnatally. (It may even represent a secondary rather than a primary defect.) Kodama et al. (1976) have suggested that ipsilateral periventricular hemorrhage may occur in a region supplied by a stenosed cerebral vessel

References p. 387

which may be identical to that of Moya-Moya disease. New collateral vessels which develop appear extremely friable and susceptible to hemorrhage, thereby possibly mimicking an occult or cryptic AVM (Fig 3.113)! Nagayama et al. (1985) reported a case of a 33year-old male with a typical angiogram of a Moya-Moya disease in stage III combined with a right frontal AVM fed by basal moyamoya vessels and drained to the Trolard and Sylvian veins in the right frontal lobe. In a large series of 2000 cases of Moya-Moya disease collected by Yonekawa et al. (1986) 6 cases. i.e. 0.3%, were found to be associated with an AVM whereas 2.8% of the cases had an aneurysm. Fig3.113A-E A-B This left frontobasal AVM with unusual drainage towards sigmoid sinus, associated with highgrade stenosis of the M1 segment of the left middle cerebral artery (C-D) suggested Moya-Moya disease in a 47 year old female who refused surgery.

References p. 387

Venous

193

Fig 3.113E Vertebral angiography showed dilated perforating arteries and posterior choroidal arteries (arrow).

Venous Our own findings in relation to the high incidence (see Table 9.2, Vol. Ill B) of major venous sinus agenesis and occlusion, associated with AVM, together with a brief outline of the frequently bizarre non-segmental venous drainage of the lesions have been described in the section on elements of the AVM (Figs 3.59-3.78, 3.116-3.126 and Chapter 6, Figs 6.4, 6.5), and on hemodynamics (Chapter 4, Fig 4.5A-B, p. 219). Relatively few other workers have emphasized what may be a very important aspect of AVM pathophysiology with particular reference to postoperative complications (Figs 3.114, 3.115, see also page 138).

Handa et al. (1975) described a case of a dural occipitomastoid AVM with occlusion of both sigmoid sinuses, although earlier reports of posterior fossa AVMs and sinus occlusion had been published by Robinson and Sedzimir (1970), Gottschaldt et al. (1971), De Senarclens et al. (1972) and Matsumoto et al. (1975). Handa et al. commented that the apparent "high grade disturbance of the cerebral circulation in a widespread area, and the incidence of focal neurological deficits or of increased intracranial pressure is much higher and the prognosis graver in patients with this phenomenon than those without".

194

3. Pathological Considerations

Dobbelaere et al. (1979) analyzed the venous drainage of 370 operated vascular malformations, furthering the earlier work of Agee and Greer (1967) who had described the anomalous venous drainage in aneurysm of the vein of Galen. They divided their cases into three groups: AVMs associated with an isolated absence of the "sinus droit" (straight sinus), AVMs with absence of the sinus droit and major venous anomalies, and those with major venous anomalies but a normal sinus droit. They stressed the importance of full arterial and venous phase angiography in assessing operability of and approach to a given AVM. Brainin and Samec (1983) on the basis of 3 cases, put forth the interesting proposal that the underlying cause of growth of some posterior fossa dural AVMs might be that of altered venous dynamics (a result of sinus thrombosis, obstructed CSF outflow). This could lead to the opening up of otherwise insignificant dural vascular communications. Jomin et al. (1985) emphasized Dobbelaere's comments that prognosis following surgery for AVM may depend above all upon the normality or abnormality of the mode of drainage into the venous system, and upon the effects on the remaining venous drainage when the veins draining the AVM (and possibly normal areas of brain) were occluded surgically. These views found support in the work of Vinuela et al. (1985). They found the angiographic evidence of major venous wall irregularities or stenoses of the galenic system in 14 cases and occlusion of the deep venous system in 7 cases of a total of 53 patients with AVM. Numerous venous collaterals through medullary and cortical regional veins were noted and there was a late drainage through the basal vein of Rosenthal in all cases. They suggested that the abnormal hemodynamic patterns produced by the drainage from AVMs into the vein of Galen and straight sinus might lead to a high incidence of venous stenosis and occlusion. This might, in turn, lead to a higher than expected incidence of intracranial hemorrhage for deep seated AVMs which tend to have such drainage patterns. In our experience the most frequent finding among anomalies of the sinuses is agenesis and stenosis or occlusion, particularly of the straight, transverse and sigmoid sinuses. This is mostly observed in cases of vein of Galen AVMs, large parietal, occipital and posterior fossa AVMs, as well as in AVMs with a significant fistulous component. If the normal dural sinuses are absent, the vein may course towards primitive embryonic channels or even out to the skull and scalp. Because of impaired venous outlets in such cases,

References p. 387

there may be reflux into the internal cerebral vein as well as reversal and redistribution of venous flow. See further Figs in Vol. Ill A 3.21H, 3.80E-F, 3.81B, 3.90D-F, 3.104C, 3.105C, 3.114-126, 4.5A-B, 6.4, 6.5 and in Vol. Ill В 4.29В, 4.30С, G, 4.44M, 4.48F, 4.49G, 4.54E, 4.56E, 4.57В, 4.71С, 4.72C, 4.73F-G, 4.84E-F, 4.85В, 4.101Е, 4.107В, 4.108С, 4.109C, 4.110C, 4.111A, E, 4.113C, 4.115H, 4.124F, 4.130C, 4.137G, 4.146D, 4.147F, 4.148E, 4.152D, 4.153C, 4.154C, 5.IB, 5.3В, 5.7В and Table 9.2.

Venous

References p. 387

в F i g 3 . 1 1 4 A - B Occlusion of straight sinus (red arrows). The possible routes of redistribution of venous flow are shown in artistic drawing.

Fig3.115A-B Occlusion of left transverse sinus (red arrows). The possible routes of redistribution of venous flow are shown in artistic drawing.

195

196

3. Pathological Considerations

Fig 3.116A-G This 25 year old female suffered a first hemorrhage 12 years before. Carotid (A) and vertebral (B) angiog-raphy showed an AVM of the internal capsule, unchanged in size and shape since conventional radiation therapy was performed several years before. Note the absence of the straight sinus with reversed flow in an antegrade direction (C) as well as towards the opposite side (D). E-G MRI showed the deep location of the AVM in the posterior limb of the left internal capsule. Inoperable. She has severe hemiparesis and some mental changes, unable to work but lives fairly happily with her family.

References p. 387

Venous

197

Fig 3.117A-B A diffuse type AVM with multiple niduses scattered in the temporo-occipito-parietal and thalamic areas in this 40 year old man. Note the absence of vein of Galen (?) and of the straight sinus. Antegrade reversed venous flow. Inoperable.

Fig 3.118A-E AVM in the left insulocapsular area. A-B Lateral carotid and vertebral angiograms, arterial phase.

Fig3.118C-E

198

3. Pathological Considerations

References p. 387

Fig 3.118C-D Frontal carotid and vertebral angiograms, arterial phase. E Venous phase of carotid angiography showed poor flow through the straight sinus with redistribution of venous flow anteriorly through the basal vein. Inoperable case. No follow up available.

References p. 387

Venous

1

Fig3.119A-B A callosal AVM with absence of the straight sinus causing redistribution of venous flow in an anterior direction (A-B vertebral angiog-raphy lateral view) was seen in this 37 year old male, who refused surgery. He died same year.

200

3. Pathological Considerations

References p. 387

Fig 3.120A-G A right sided, so called "parasplenial AVM" with absence of the straight sinus (?) and a very unusual pattern of venous drainage (A-B). Frontal view (C-D).

References p. 387

Venous

Fig 3.120

Postoperative angiography (E-G) showed elimination of the AVM and preservation of the posterior cerebral artery branches. Recovery without neurological deficit. The venous phase of postoperative angiography still shows absence of straight sinus but normalization of venous flow (F).

201

202

3. Pathological Considerations

Fig 3 . 1 2 1 A - F This 12 year old boy presented with a right parasplenial AVM (A) and a hypoplastic straight sinus (?); well as bizarre flow redistribution in multiple directions (B), similar to Fig 3.120B. C-D Frontal views of vertebral angiography showed that the main venous flow was towards the contralateral side.

References p. 387

Venous

203

Fig3.121E-F Postoperative angiography confirmed complete removal of the AVM. The postoperative course was uneventful. This visual field was preserved.

Fig3.122A-E An example of a large AVM located in the center of the occipital lobe and causing local hematoma in a 38 year old female (A, CT). Postoperative CT (B).

Fig3.122C-E

204

3. Pathological Considerations продолжение

References p. 387 I

Fig 3.122C-D Preoperative angiogra-phy showed a fistulous connection of right posterior cerebral artery to the occipital vein which drained partially to the poorly seen straight sinus but mainly into an ascending parietooccipi-tal vein (arrow). E Postoperative angiography performed 10 months later showed complete removal of the AVM. The preoper-ative left homonymous hemianopia remained unchanged.

References

References p. 387

Fig3.123E, F

Fig3.123A-F A-D This mainly fistulous type left paraspleni-al AVM had subependymal drainage to the galenic vein and stenotic straight sinus (?) but also had unusual drainage to the superficial veins of the temporal lobe. There is also complex flow through the vein of Labbe into the sylvian vein which empties into the superior sagittal sinus.

Venous

206

3. Pathological Considerations

References p. 387 Fig 3.123E-F Postoperative angiography after radical removal of the lesion. Uneventful postoperative course. The 10 year old boy remained mentally retarded as before surgery.

References p. 387

Venous

207

D Fig 3.124A-D Left cerebellar AVM with multiple niduses. Note the absence of the left transverse sinus (?) and the drainage occurring through the hugely dilated precentral cerebellar vein into the galenic vein and right transverse sinus. Note the transcerebellar venous channels coursing through the right cerebellar hemisphere (D). Operation was refused. Radiation therapy in Boston was ineffective (this angiographic study was performed 2 years after radiation).

208

3. Pathological Considerations

References p. 387 Fig 3.125A-G Multiple (at least 3) AVMs in a 12 year old boy with occlusion of straight sinus and bizarre multidirectional venous drainage. Right carotid angiography (A) showed a parietal AVM. Recognition of cingular AVM requires careful study of the frontal view (C). Note the perforating feeders arising from M1 segment. Note also an aneurysm. Lateral (B) and frontal (D) views of left carotid angiography show the right cingular AVM with drainage into the vein of Galen and reflux into the internal cerebral and basal veins by occlusion of straight sinus.

References p. 387

Fig3.125E-G Vertebral angiography showed the third AVM in the posterior callosal area supplied by thalamoper-forating arteries. A fourth AVM was seen within the cuneus (E). The venous phase (F-G) shows absence of the straight sinus (?) and unusual retrograde bilateral venous drainage to the vein of Rosenthal. Radiation therapy was performed in Boston.

Venous

209

210

3. Pathological Considerations

References p. 387

Fig3.126A-F

A-B This arteriovenous fistula between the right superior cerebellar artery and a superficial cerebellar vein which empties into the torcular Herophili, was found in a 31 year old patient presenting with cerebellar ataxia and gait disability but no subarachnoid hemorrhage. C-D The left transverse sinus was absent (D). The right transverse sinus was dilated. The right sigmoid sinus was occluded. There was reverse flow (C) from the transverse sinus to the vein of Labbe which drained further anteriorly to the sphenoparietal sinus. Note the unusual thickness of the calvarium.

References p. 388

Tumors

211

Fig3.126E-F The a-v fistula was explored through a right subtemporal transtentorial approach. The application of 2 clips on the dilated superior cerebellar artery was followed by immediate color change and collapse of the previously red and turgid venous system. His postoperative course was uneventful. Postoperative angiography showed elimination of the a-v fistula.

AVM Associated with Other Pathological Entities Tumors We have seen a case of a frontal AVM in which an ipsilateral metastatic carcinoma was also present but which was not diagnosed until exploration. In another case a frontal AVM was associated with an ipsilateral acoustic neurinoma. Fischer et al. (1982) described 2 cases of cerebral hemangioma in association with gliomas and dis-

cussed the possibility that cavernous malformation may have a more than coincidental association with tumors of the glioma series. McCormick (1984) has observed a possible link between cavernous malformations and both oligodendrogliomas and Schwannomas. Adequate statistical evidence for any of these associations being more than coincidental is, as yet, lacking.

4 Hemodynamics

4

213

Hemodynamics

Introduction Fascinating insights into the historical aspects of the study of the cerebral circulation, the measurement of cerebral blood flow, and arteriovenous malformations may be gained by reading the splendid papers by Sir William Osier (1915) and Bell (1984). We learn that investigation of the physiology of the cerebral circulation and of arteriovenous aneurysm began over 200 years ago and the modern age of understanding of the neurohumoral control of CBF was heralded by the prophetic remarks of Ch. Roy and Sir Charles 'Sherrmgton (1890). Following on from the pioneering work of Pick (1870) and Kety and Schmidt (1945) there has been an enormous acceleration in the development of increasingly sophisticated techniques (the most recent being PET scanning) to allow quantitative measurement of CBF in normal individuals and its changes in pathological states (Gibbs et al. 1947, Shenkin et al. 1948, Lassen and Munck 1955, 1959, 1966, 1983, Greitz 1956, Lassen and Ingvar 1961, Meyer et al. 1963, Leszcynski et al. 1963a,b, Feindel and Perot 1965, Haggendal et al. 1965, Oeconomos et al. 1969, Feindel et al. 1971, Heiss et al. 1972, Mathew et al. 1972, Obrist et al. 1975, Drayer et al. 1978, Lassen et al. 1978a, Ter-Pogossian et al. 1978, Thompson et al. 1978, Fieschi 1980, Frackowiak et al. 1980, Celsis et al. 1981, Olson et al. 1981, Sokoloff et al. 1981, Baron et al. 1982, Pertuiset et al. 1982, Phelps et al. 1982, Herscovitch et al. 1983, Deutsch 1983, Ackermann et al. 1984). The experimental and clinical studies on cerebral blood flow in normal and pathological conditions which were initiated by the pioneering work of Schneider (1950) and Hirsch et al. (1957) found continuation in the research of Brockman and Jude (1960), Gottstein et al. (1961), Plum et al. (1963), Crowell et al. (1970), Hossmann and Kleihues (1973), Branston et al. (1974), Sundt et al.

(1974), Symon et al. (1974, 1975, 1980), Michenfelder and Milde (1975), Heiss (1976, 1983), Fieschi (1980), Astrup (1980, 1981, 1982), Siesjo (1981), Jones et al. (1982), Olsen et al. (1983), Plum (1983). Despite the fact that abundant, well-known data have been elaborated on the manifold thresholds of brain energy systems such as like blood-flow-, circulation time-, temperature-, oxygen-, CO2-, glucose-, lactate-thresholds and ionic equilibrium, as well as thresholds of functional and morphological needs and that definitions have been created like "ischemic penumbra" or "luxury perfusion", little is known about the metabolic requirements and the blood supply of affected and non-affected tissue in strokes. We therefore agree with Astrup et al. (1981) that, "measures that maintain or raise the residual perfusion in the area of acute focal ischemia are probably all-important determinants of the final outcome in stroke. At present, such therapeutic intervention is "blind", since the effect on hemody-namics in the ischemic area cannot be monitored. This problem is, however, being approached by the development of instrumentation for repeat-able noninvasive three-dimensional imaging of regional cerebral blood flow and metabolism". The position is even worse in cases of AVM with apparent vascular steal phenomena. Surgeons may feel that they must attempt to return the cerebral circulation back to what will be regarded as completely normal. Nevertheless, we have yet to develop the system which would be of most benefit to everyday neuroradiological, neurosurgical and neurological practice and that would be a suitable method of measuring local changes in the precise metabolic needs of the brain under varying circumstances, an investigation we might name "parenchymography".

214

4. Hemodynamics

The descriptions and comments in the following section of normal and abnormal physiology are based largely upon the works of others. A short section on applied dynamics has been included here simply to relate basic physical prin-

References p. 388

ciples to the surgery of AVMs. It is fully appreciated that there are many inaccuracies as the vessels themselves are not passive tubes but active organs and the neural, muscular, humoral, hormonal and cellular influences involved are both complex and poorly understood.__________

Hemodynamics The Physics of Fluids and Blood Flow Though weighing less than one-thirtieth of the entire body, the brain receives 20% of the cardiac output. Lassen et al. (1977) report a mean of 52 with ranges of 36 to 82 ml/lOOgm/min in normal subjects. Values greater than 170 ml/100g/min have been found in patients with cerebral arteriovenous malformations (Deutsch 1983). The grey matter has a large capillary density and" receives three to five times as much blood as the white matter. The carotid arteries conduct nearly 2/з of the cerebral blood flow, with the remaining Уз supplied by the vertebral arteries. The construction of the arterioles, venules and capillaries within the brain and their regional structural differences have been recently described by Saunders et al. (1965), Magno'(1965), Dahl (1973), Hammersen (1977), Lang (1977), and Duvernoy (1983). (See also the Chapter on Surgical Anatomy.)

Pressure, Flow, and Resistance Regardless of the fluid flowing through it, the smaller the calibre and greater the length, the greater the resistance to flow. Flow is indirectly proportional to resistance. The power which drives the fluid is known as pressure, but it is the difference in pressure between the two ends of the vessel that determines the rate of flow and not the absolute pressure in the vessel. The flow of any fluid can be calculated as follows:

in which Q is the flow, ЛР is the difference in pressures (pl-p2), and R is the resistance. In patients with intracranial AVM the blood perfusing cerebral structure (Qc) is equal to the total

blood flow (Q) minus that which goes to the AVM (Qm). This is the basis for the theory of cerebrovascular steal, generally considered as having great clinical importance. As can be seen in Fig 4.1, vessels in parallel will have less resistance than vessels in series. An (AVM must be considered as a_combination of ! both (Fig 4.2). Vessels supplying both brain and the malformation are necessarily represented in parallel. If they were in series, the flow through one would have to equal that of the other (see Fig 4.2). Other factors affecting resistance have also been formulated and are valid for laminar blood flow, 8nl

where_n_is the viscosity (in poises) ,_1 is the length of the vessel in centimeters andjMs the radius of the vessel in centimeters. Substituting this into the original formula we get the Poiseuille-Hagen formula which may be used for the calculation of blood flow:

This formula may help explain the difficulty of coagulating punctured AVM vessels (Yamada 1982). If a venous loop of an AVM is ruptured, the distal pressure (p2) becomes zero (atmospheric pressure). In addition to increasing ЛР, the resulting increased flow increases the forces on the vessel walls. The ruptured AVM is often seen to become redder and more pulsatile with un-resisted arterial flow. If a significant rupture occurs on the arterial side of the malformation, the blood will be diverted away from the AVM. This latter effect could be of theoretical use, in terms of creating an A-V fistula as a prelude to excision of large AVMs, to divert blood from the lesion.

References p. 388 Fig4.1A-B Vascular resistance. Vessels in parallel (B) have a lower resistance than vessels in series (A).

Fig 4.2 In parallel arrangement of vessels supplying brain and feeding an AVM. Q = flow, с = cerebrum, m = malformation.

Laminar versus Turbulent Flow

The Nature of Blood The flow of blood differs from that of water because of its plasma and cellular components. The viscosity of blood is approximately 3 times that of water but is exponentially proportional to the number of red blood cells present. Because of the nonuniform nature of blood, interesting changes occur in viscosity as the diameter of a vessel is altered. As the size of vessels diminishes and the blood flow decreases, viscosity increases probably owing to rouleaux formation, with a resulting increase in friction. However, in vessels with diameter of less than 0.5 mm, but larger than the smallest capillaries, the viscosity of blood can decrease to almost half of that in vessels of slightly larger size. This Fahraeus-Lindqvist effect is secondary to the alignment of red blood cells in an orderly fashion. In the final capillaries, the red cells may become impeded for varying lengths of time, producing ^sludging. This raises the local hematocrit and thus the viscosity. During surgery, if blood replacement and crystalloid fluids are reduced to a minimum, there will be a lower vascular volume, a fall in blood pressure, a decrease in the vascular lumenal distension, and a

215

rise in the hematocrit. All these factors will increase viscosity.

Laminar versus Turbulent Flow Blood flowing through a long smooth vessel exhibits laminar, rather than turbulent flow. When laminar flow occurs the velocity of blood in the center of the vessel is greater than that closer to the intima, since the red blood cells next to the vessel wall will be slowed by friction and by plasma film between the vessel wall and corpuscular components. When fast flowing blood is not streamlined (as when passing over an atheromatous plaque, making an acute turn, or meeting a branching point), the flow will become turbulent. Turbulence causes a decrease in the velocity of blood flow. The tendency for the flow to become turbulent is expressed by the formula,

216

4. Hemodynamics

where Re is known as Reynold's number and is a reflection of the tendency for turbulence to occur. v is the velocity of flow, 2r is the diameter of the vessel, and 5 is the density of blood. (Flow is related to its velocity by the following equation: Q = vr2 п) In small vessels, Reynold's number is never high enough to cause turbulence. Blood within the first several centimeters of major draining veins of an AVM may be very turbulent. As the surgeon progressively ligates arterial feeders, the flow within the vein tends to diminish and become streamlined. Because of this streamlining, red arterial and blue venous blood do not quickly mix within the vein, an observation which may be used as an index of elimination of afferent supply.

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Fig 4.3 Schematic representation of a buckled segment of a vein. F = force, P = pressure, A = cross sectional area of the vessel, M = bending moment.

Tortuosity of Vessels Tortuosity will develop in any pliable cylindrical object if subjected to sufficient pressures by the flow of fluids within it. The pressure difference between the ends of the vessel represents the internal pressure (Fig 4.3). The force (F) applied is equal to the pressure (P) times the cross-sectional area (A):_____ The force causing a pipe to bend away from its linear form is known as the Bending moment (M). It has been shown that factors favoring vessels to become tortuous are high internal pressure, small diameter, and long lengths. In addition, because of the external force opposing the Bending moment, vessels surrounded by other structures are less likely to become tortuous than those in a less restricted environment (i.e., in the subarachnoid cisterns), as evidenced by the tortuosity commonly seen with the basilar artery. Because blood pressure (a squared factor) is the major component tending to cause buckling, and because arteries have a significantly smaller capacity to dilate (less compliance), they tend to become tortuous more readily than veins. This helps to explain why the proximal AVM is highly tortuous, while the large draining veins tend to be comparatively straight.

Vascular Distensibility Unlike rigid pipes, blood vessels are able to distend and contract. This can greatly affect the volume and rate of blood flow through them. Because vessels are not rigid, they require a certain amount of pressure within them to remain patent. In arterioles and larger vessels, the amount of pressure required for distension is also highly dependent upon muscular tone.

Because veins always contain smaller amounts of muscular and elastic tissue, they are more readily distensible but tend to collapse when intraluminal pFessures are low. On average, a vein is 6 to 10 times more distensible than an artery. The expansibility of veins allows them to hold a large capacity of blood: Vascular capacitance = Distensibility x Volume. A vein generally holds 3 times the blood volume of a comparable artery and therefore ^t|_gprn£liance or capacitance tends to be 18 to 30 times as great. In a venous circuit large volumes of blood are needed to raise the pressure by even 2 mmHg. The capacitance in the circulatory system in a 70 kg man necessary M offset each 1 mmHg rise in arterial pressure is approximately 100 ml. Alteration of cerebral blood volume will have profound effects on the quantity of blood flow. The measurement of CBF is a measure of the volume of blood passing through 100 gms of tissue per minute,

where_V_equals volume and t is the time variable. at any one point gives a The slope value for instantaneous blood flow and may be used in devising methods for decreasing blood loss during AVM resection. The phenomenon of delayed compliance describes acute pressure changes in blood vessels followed by slow adaptation towards normal (Fig 4.4). After maximum stretching of their elastic components, vessels show a gradual lengthening of their muscular and/or fibrous walls. This phenomenon

References p. 388

Neuronal Innervation

217

Fig 4.4 Diagram to illustrate delayed compliance and stress-relaxation. (Effect of injecting a small volume of blood into a venous segment with varying intravascular pressure.)

is a characteristic of smooth muscle and is known as stress-relaxation (Fig 4.4). When an increase in blood volume has subsequently been reduced, vessels which have undergone enlargement by delayed compliance are unable for some time to constrict sufficiently to raise the blood pressure back to normal. When placed under higher pressures, the ability of stressrelaxed vessels to regulate distal flow by constriction is greatly impaired. Closely related to the subject of compliance, is that of rupture. Laplace's law states that, the internal force exerted on the walls of a vessel is directly proportional to the product of the pres-sure times the diameter of the vessel. Thus, the

regions of an AVM most likely to rapture are the proximal regions of the enlarged venous channels (high pressure and large diameters). A normal vessel placed under chronic high pressure will undergo hypertrophy (Folkow 1956). The vessel wall may become sclerosed, with a concomitant diminution in its ability to dilate or contract. However, vessels in an AVM tend to continue enlarging with thinning of their walls, suggesting some important anatomical deviation from normal cerebral vasculature. The occurrence of stenosis or occlusion of some major sinuses remains unexplained. (See pages 193-209 and Vol. Ill B, Fig 9.1 and Table 9.2.)

Cerebral Circulation: Functional Anatomy of the Cerebral Circulation Neuronal Innervation In the brain, the degree of functional significance of neuronal innervation remains speculative. Purkinje in 1836 and Remak in 1841 described nerve fibers along the arteries of the circle of Willis. This was confirmed by Penfield in 1932, who showed an intricate network of nerves on both the superficial and deep cerebral arteries and veins. The complexity and degree of innervation were depicted by Peerless and Ya§argil in 1971 using fluorescent staining monoamines. These studies revealed a dense plexus of adrenergic fibers within the deeper layers of the adventitia. Nerve fibers

were not found within the muscle layers. The basilar artery appeared to have a relatively sparse adrenergic innervation. The anterior cerebral arteries and, to a lesser extent, the carotid and middle cerebral arteries were richly supplied by large nervous terminals. Nerves could be followed in diminishing numbers on all superficial arteries down to a diameter of approximately 15 microns (pre-capillary size). Of the intracerebral vessels, the choroidal arteries and arterioles of the choroid plexus showed an intense fluorescence. The remaining penetrating vessels, most of which were

218

4. Hemodynamics

References p. 388

arterioles, were sparsely innervated with the exception of those entering the anterior part of the diencephalon and the small cluster of vessels irri-

gating the medulla. The deep and superficial veins were supplied with only occasional adrenergic fibers.

Microcirculation

body, but their presence in the brain remains disputed (Hasegawa et al. 1967). These studies on normal cerebral vessels serve only to underline the lack of detailed parallel • knowledge in cases of AVM. Careful investigations in these fields may produce results of therapeutic value in the treatment of malformations (see pages 320-321).

(See also Chapter 8) A typical systemic capillary bed contains precapillary arteriovenous shunts. These shunts or thoroughfare channels (Chambers and Zweifach 1944), have been confirmed in every organ in the

AVM Structure There are five major components to any cerebral arteriovenous malformation: Feeding arteries, the nidus, the compartments of the AVM, the draining veins and the venous sinuses, and the adjacent brain, which may or may not be gliotic. A more detailed description of the anatomy of the various vessel components is given in Chapter 3, pages 111-138. Terminal arteries supply only the malformation whereas transit arteries may or may not communicate with the AVM but certainly go on to supply normal cerebral structures beyond the malformation. Clipping this latter type of artery may lead to cerebral infarction. Terminal arteries may occasionally feed directly into a vein but more often there is an intermediate shunting arteriole ranging from 50 to 200 microns in size (Yamada 1982). Such vessels often have walls which are deficient in media, may have undergone delayed compliance, and, because of their size, may allow a decrease in blood viscosity as evidenced by the Fahraeus-Lindqvist effect. They are thus extremely resistant to coagulation and have a poor contractile ability. The draining veins are a much.more complex com-

ponent of the AVM than was hitherto believed and they are discussed in detail on pages 118-138 and 193-209. Apart from the production of hydrocephalus as a secondary phenomenon resulting from altered venous drainage in the presence of an AVM, there have been few comments about this very important facet of the pathophysiology of these lesions (Fig 4.5A—B). In the present series of cases not only have bizarre patterns of venous drainage frequently been encountered but many instances of agenesis, stenosis and occlusion of majors venous sinuses have been noted. (See Chapter 3, Figs 3.21, 3.23, 3.46, 3.51, 3.59-3.80. 3.90, 3.95, 3.100, 3.102, 3.104, 3.105. 3.116-3.126 and Chapter 6, Figs 6.4, 6.5.) Reversal of flow through the sinuses has also been found (see Figs 3.114, 3.115) and when the channels have been obstructed (either primarily or secondarily) in cases of galenic AVMs, the occluded veins have been found to be almost black. The underlying cause of such findings and their influence on the well being of the patient are uncertain (see the phenomenon of backflow on pages 193-194).

Enlargement of AVMs As surgically created A-V fistulas in the extremities enlarge, unlike cerebral AVMs, the walls of their veins become morphologically similar to arteries, and this seems to be independent of an intact neural bed. Long veins characteristically undergo hypertrophy when used as arterial grafts. It has been demonstrated by angiography that major cerebral vessels proximal to an AVM will enlarge. These facts suggest that there normally exists

some mechaflisrn whereby low distal pressures result in dilatation, and high proximal pressure induces wall hypertrophy. Enlargement of cerebral AVMs without wall thickening may occur in part because the veins in the head are above the level of the heart, and therefore are generally under negative or zero pressure. As a result the AVM vessels perceive low distal pressures and subsequently follow "normal" physiologic growth patterns of dilatation without media hypertrophy.

References p. 388

Fig4.5A-B

A High flow may cause backflow and redistribution of venous outflow, as shown in a case of mesencephalic AVM.

Enlargement of AVMs

219

В High flow into the transverse sinus may cause redistribution of the normal venous flow.

220

References p. 388

4. Hemodynamics

Autoregulation

Autoregulation is an inherent property of all organs by which a constant blood flow isTsupplied to the tissue despite changes in systemic blood pressure and volume. Blood flow to the brain can be constantly maintained between the approximate systemic pressures of 60 to 180 mmHg. t Beyond these pressure limits, cerebral blood flow ' changes in direct proportion to the systemic blood ' pressure (Fig 4.6). Mechanisms controlling autoregulation are artificially classified into long and short term components. Long term controls include morphological changes such as increased vascularity, hypertrophy of vessels, and the formation of a collateral circulation. Short term autoregulation then depends upon local, myogenic, neuronal, and humoral factors overlaying these morphological adaptive changes. Dilatation of the major cerebral vessels feeding an AVM has been well documented angiographically. Whether this dilatation is secondary to increased flow to the AVM or a response to reduced flow in the tissues surrounding the AVM is uncertain. Following resection of the AVM, or in cases of spontaneous thrombosis, enlarged vessels will slowly diminish to normal size (Norlen 1949).

96(mean pressure)

Fig 4.6 Schematic drawing of pressure gradients in normal and AVM sector. (From Tonnis, W., W. Schiefer: Zirkulationsstorungen des Gehirns im Serienangiogramm. Springer, Berlin 1959.)

Chronic hypoxemia may increase capillary density by 50% (Purves 1972) yet increased vascularity, as a means of establishing long term autoregulation in association with AVMs, has not been described in the pathological literature (McCormick 1966, Meyermann and Ya§argil 1981) nor in the neurosurgical literature. Feindel discusses the subject of "hyperemia" (Feindel and Perot 1965, Feindel 1971) as does Penfield (1932) in terms of increased flow following periods of ischemia either from temporary arterial occlusion or from disrupted cerebral metabolism, such as after a seizure. Feindel et al. (1967) mention an increase in fluorescence (hyperemia) occurring in the cerebral tissues surrounding the AVM following excision of the latter, although no mention was made of increased vascularity. "Collateral" circulation has been commonly described in cases of AVM but the developing channels have been felt to feed only the malformation. Recently, however, by selective angiography Russel and Berenstein (1981) have shown collateral vessels which have also supplied surrounding cerebral tissue whose temporary occlusion was followed by temporary neurological deficits (see Chapter 6, Fig 6.13). Angiography has shown that there are some constant patterns of redirected flow through the circle of Willis such that in the presence of large left sided AVMs supplied by the MCA, the left АСА will obtain its supply from the right carotid artery through the anterior communicating artery and vice versa. There is controversy regarding the importance of sympathetic innervation to cerebral arteries in either the long or short term autoregulation of cerebral blood flow. In most organ systems vascular resistance is maintained primarily by the arterioles, while in the brain it appears that at least 40—50% of the cerebrovascular resistance is exerted by the extraparenchymal arterial system (Kanzow et al. 1970). Sympathetic innervation is normally responsible for maintaining local vascular tone in accordance with changes in blood pressures (Deshmukh et al. 1971/72), while cerebral metabolites (especially CO2) and cerebral oxygen demands are responsible for changes in local cerebral blood flow (Murphy 1954). Whether these local responses also trigger a neuronal regulatory mechanism is unclear. The contribution of sympathetic activity to possible alterations in autoregulation in cases of AVM is essentially unknown.

References p. 388

Normal Perfusion Pressure Breakthrough

Since the AVM is a chronic lesion, short term mechanisms attempting to deal with A-V shunt may play a smaller role than long term mechanisms. However, it has been shown that short term mechanisms in the "normal" cerebral tissues surrounding an AVM are responsible for more acute changes in blood flow, such as vigilance tasks (Okabe et al. 1983), and rapid crlangesln blood pressure (Pertuiset et al. 1981, 1982). This regulation is also of sufficient magnitude to significantly increase or reduce blood flow through the malformation (Deutsch 1983). The exact nature of this control (local metabolites, neural control, or

221

hormonal, and/or a combination of these) has been fully discussed by Murphy (1954). in the Congress Publication edited by Brock et al. (1969), Meyer et al. (1969), Guyton (1981). and Heistad and Kontos (1983). The mechanisms whereby AVMs disrupt normal autoregulatory processes are uncertain, but in some cases, in which the normal autoregulatory capacity is thought to have been chronically working at its full limits, additional acute hemodynamic changes may be disastrous. This embodies the theory of normal perfusion pressure breakthrough.

Normal Perfusion Pressure Breakthrough Although described clinically by Olivecrona and Riives (1948), Spetzler et al. coined the term "normal perfusion pressure breakthrough" (NPPB) in 1978, in order to describe the onset of acute or subacute brain swelling and/or hemorrhage following excision of large AVMs. Pertuiset et al. (1979) referred to this as "vasogenic turgescence of the brain", and stated that it was their most common cause of complication following AVM surgery. Rupture of vessels adjacent to the resection site are said to be characteristic features of NPPB. Vessels directly associated with the AVM are said to rupture as a result of two mechanisms. First, because of the high arterial pressure, they may exhibit delayed compliance. This will occur especially in those proximal channels having progressively more media. Such vessels would lose their immediate capacity to constrict in order to prevent high perfusion pressures; i.e., they would lose their ability to autoregulate. After removal of the AVM, high blood volumes thus overwhelm these vessels resulting in interstitial edema and hemorrhage. Secondly, even if some normal-looking vessels remain, they may still not have a completely normal morphology (lack of innervation and/or stretch receptors, or other defects in the vessel wall). Thus they cannot adjust properly to changes in blood pressure or flow and are subject to easy rupture. This bleeding is distinct from spontaneous SAH associated with AVMs which often results from rupture of ballooned venous dilatations of the AVM. One might expect that juxtaposed vessels may lose their autoregulatory capacity. However, distal cerebral lobes are sometimes found to undergo swelling and occasional hemorrhage. This is

thought to be a result of vessel enlargement, in attempt to decrease vascular resistance and increase flow. The vessels do not exhibit delayed compliance, as this occurs only in vessels under excessive pressure. What happens (Folkow and Siverstsson 1968) is that they simulate chronically hypotensive beds, i. e. the vessels exhibit a reduction of the muscular media, an increase in luminal diameter, and a decrease in their maximal contractile strength (with steepening of the resistance curve). Once the AVM has been obliterated, these vessels are still too large, and despite their contractile efforts, are incapable of preventing excessive blood flow from passing more distally with time (Norlen 1949), they slowly reduce to normal dimensions. Hence, this type of "breakthrough" bleeding is supposed to occur from excessive blood going through morphologically normal, but physiologically enlarged vessels. Nornes and Grip (1980) noted an immediate rise in "stump pressure" in arteries feeding an AVM following test occlusion. By correcting for a decrease in venous pressure following occlusion, the rise in adjacent cerebral tissue blood flow becomes even more dramatic.

222

4. Hemodynamics

References p. 388

Comments on the Normal Perfusion Pressure Breakthrough Theory The descriptions above reflect, perhaps, more "classical thinking" regarding the application of physiological principles to the removal of AVM. We would like to clarify our own views on the controversial topic of NPPB as follows. On the basis of unanticipated swelling and hemorrhage occurring postoperatively in 4 patients (of Wilson's series of 83 patients), the normal perfusion pressure breakthrough theory was proposed. This implies that following clipping of the feeding arteries in large malformations, CBF and perfusion pressure is increased to the vascular bed or the brain tissue which had previously been chronically dilated in an effort to meet tissue demand in the face of a large shunt and was now unable to handle the increased flow with resultant edema and hemorrhage. One consequence of this theory is the recommendation that the treatment of the AVM be staged into two or more procedures involving either embolization or multiple craniotomies. Mullan et al. (1979) presented a retrospective analysis of 5 patients of whom 3 developed complications attributed to postoperative hyperemia. In one case uncontrollable bleeding occurred from middle cerebral artery branches proximal to ligation of AVM feeders and in a second case brain swelling occurred when the MCA was ligated and then receded after removal of the clip. The third case had a deep hemispheric hemorrhage 26 hours after an embolization procedure which temporarily blocked the distal internal carotid and proximal middle cerebral arteries. These authors felt the complications in these 3 patients were best explained by hyperemia proximal to the AVM in normal brain tissue, which could not handle the sud-"den increased volume of blood presented to it. Day et al. (1982) presented 3 cases who underwent resection of AVMs with uncontrollable bleeding at the time of operation which was attributed to NPPB. In commenting on this paper, Peerless (1982) discussed the difficulty of coagulating tiny feeding vessels deep in the lesion which may represent vessels transitional to the AVM and which do not respond well to coagulative and hemostatic techniques. He questioned the concept of perfusion breakthrough. Solomon and Michelsen (1984) presented a case which they felt demonstrated defective autoregu-lation and perfusion breakthrough. This patient had a large left frontal AVM with occlusion of the

left ICA distal to the AchoA and with filling of the AVM by the right ICA through the AcoA and by the left ECA through an anomalous ophthalmic artery. Seven days after operation the patient was found to have a hemorrhage in the head of the right caudate nucleus which they ascribed to perfusion breakthrough. Interestingly, the hemorrhage was in the distribution of the recurrent artery of Heubner, yet the anterior cerebral arteries were seen on neither the pre- nor postoperative angiogram. A case report submitted by Aoki and Mizutani (1985) describes uncontrollable bleeding and swelling, due to NPPB, into a previously ischemic area immediately following excision of a posterior temporal AVM. Preoperative angiograms showed no filling of MCA branches although the patient had no focal neurological signs. Postoperatively, some filling of MCA branches was demonstrated. Hassler and Gilsbach (1984) reported on their angiographic and Doppler findings in 12 of 35 cases felt to be at risk for NPPB showing postoperative edema or hemorrhage. They stressed that [ the length of arterial feeders to the AVM had an • important relationship to hyperperfusion complications. In each of their cases exhibiting postoperative edema, the feeding vessels were a minimum / ,pf 8 cm measured from the circle of Willis. They v never found swelling in AVMs with short feeders and implied that longer feeders would give off more branches to cerebral tissues before termination in the malformation. These branches would. _of necessity, be maximally dilated in order to 'capture' the blood tending to pass preferentially into the lower resistance AVM. This would hold true for both the long transit arteries as well as for the long vessels terminating in the malformation. We did not observe such a postoperative course in our cases (Figs 4.7-4.9). Based on so few cases, the theory of normal perfusion pressure breakthrough must remain speculative. It remains to be demonstrated whether the brain tissue outside the AVM exhibits changes in ! vasomotor response of its vascular bed and whether increased perfusion pressure in feeding arteries is in fact transmitted to the microcirculation where edema and microhemorrhages can 1 occur. While the theory is based on solid physiological principles, it does carry the danger that untoward results will be blamed on a phenomenon which is

References p. 388

Comments on the Normal Perfusion Pressure

Fig 4.7A-C

A Scheme of a parietooccipital AVM with long segmental dilatation of feeding arteries which arose from MCA and PCA and prevented adequate visualization of the branches to normal brain areas. В Angiography after surgical removal of the lesion showed improved filling of the branches from MCA and PCA to normal brain areas but only a moderate decrease in size of feeding vessels. С 3-6 months after removal of the lesion, all hemispheric arteries had returned to their normal size.

somehow independent of technical difficulties such as leaving residual AVM or compromising nutrient arteries. This is a view to which Spetzler himself has subscribed several times. The suggestion that partial operations should be performed for fear of this complication or that postoperative hypotension is necessarily beneficial must be critically examined. In no case in the present series of 414 AVMs was surgery carried ouUn sjages to avoid NPPB. Strict attention was paid to clipping the terminal arteries close to the malformation and not to compromise transit arteries supplying normal brain tissue beyond the malformation. In 30 cases (7.5%) hematoma formed in the bed of the AVM. If reoperation was required, it could generally be seen that some venous oozing or, in some cases, a residual piece of

223

AVM was present to account for the bleeding. In no case did significant swelling seem to occur in the surrounding brain. In a further 52 patients temporary postoperative impairment of neurological deficit was observed, but no evidence ofNPPB. None of our 6 patients presenting with a pure fistulous high-flow AVM and angiographic evidence of steal syndrome developed NPPB-syndrome after one-stage removal of the fistula. On the other hand, following one-stage removal of large AVMs 12 patients developed neurological impairments which we would like to describe as "temporary blocked syndrome" (TBS). These patients awakened after surgery with either hemiplegia, aphasia or hemiplegia and aphasia, which persisted for one to three weeks. Some other patients exhibited an unusual stuporous condition which persisted for some days postoperatively and then suddenly disappeared. In these cases postoperative angiography, EEG, and CT were of no help in explaining these unusual conditions. The clinical condition of these patients resembled that of patients after status epilepticus. All of these patients recovered fully within a few days. Such rapid recoveries have not been seen during the postoperative course of patients after complicated aneurysm or tumor surgery.

224

4. Hemodynamics

References p. 388

Fig 4.8A-C Preoperative (A) and postoperative (B) angiograms of a 25 year old female with a left frontal AVM demonstrated how the vessels have returned to almost normal size after removal of an AVM: clear visualization of the branches of АСА and MCA to areas of normal brain tissue. The feeding artery (C) is still dilated (sludging effect).

Plum (1983) remarked "The challenge for the therapeutically minded investigator became the reverse of the traditional question from 'why are certain parts of mammalian brain selectively vulnerable' to 'why are certain parts of the brain selectively resistant and how can we enhance the resistance'." We have to go further and ask the question 'why is the brain of AVM patients, in contrast to patients with aneurysms, more resistant to such a longlasting circulatory strain and to insults (like a large hematoma), and also, in some cases, to difficult neuroradiological and surgical procedures?' A further thought regarding NPPB is that until now. all the features of this theoretical complication have been attributed to problems with the arterial system. Very rarely has the venous system

been considered to contribute to postoperative hemorrhage or edema. Yet in the present series we have seen at least 30% of cases with obviously abnormal patterns of venous drainage (in large or giant AVMs almost 100%). These have occurred not only in cases of vein of Galen aneurysm but also with AVMs in other areas and other forms of the lesion. They have taken the form of agenesis, stenosis, or occlusion of major venous sinuses, especially of the straight, transverse and sigmoid sinuses. Normal or very bizarre collateral systems have often formed. This blockage or partial blockage of the major venous system was described for vein of Galen aneurysms by Agee and Greer in 1967. The contribution of abnormal venous drainage from AVMs

References p. 388

Comments on the Normal Perfusion Pressure

225

Fig 4.9A-F An occipital AVM in a 40 year old male. A-C Preoperative angiography showed a right paramedian occipital AVM of moderate size with dilatation of feeding vessels arising from АСА, MCA, PCA.

Fig4.9D-F

226

4. Hemodynamics

References p. 388

Fig 4.9D-F 2 months later, postoperative angiography showed almost complete normalization of diameter of the previously dilated feeding vessels, with sludging effect (arrows). The normal vessels were more visible. The postoperative course was uneventful. The visual field was preserved.

to such complications as edema and hemorrhage has been emphasized in the papers of Brainin and Samec (1983), Dobbelaere et al. (1979), Vinuela et al. (1985) and Jomin et al. (1985). (See our cases in Chapter 3 on pages 138, 193-211 and Chapter 4 in Vol. Ill A, in Vol. Ill B, Chapter 4 and 5, Table 9.2.) In summary, one might say that NPPB may be theoretically sound but probably occurs rarely in practice. The inherent danger of the theory is that it will undoubtedly be used to explain away the

results of faulty surgical technique and surgeons should direct their attention more towards total elimination of all residual parts of the AVM, the avoidance of coagulation of transit vessels, and towards more careful study of the venous system in their surgical cases. More information regarding cerebrovascular autoregulation and NPPB in cases of AVM may be forthcoming from careful transcranial Doppler studies such as those of Hassler (Acta neurochir. Suppl. Vol. 39, Springer 1986).

References p. 388

Hemorrhage

227

Effects of AVMs upon Cerebral Function ~~A~rteriovenous malformations often exhibit predictable pathological effects within "The~central nervous system. These include local mass effect, obstruction, possible impaired venous drainage from normal areas, hemorrhage and cerebrovascular steal.

Local Mass Effect Supratentorial un-ruptured AVMs rarely have a significant mass effect (Wortzmann 1983). On CT scan, there is seldom displacement of the ventricular structures and the adjacent gyral and sulcal patterns are generally unchanged. Craniotomy for an AVM generally reveals the dura to be slack, and the brain pulsates normally. However, closer examination of the CT scan often reveals an area of low density around the AVM (Drake 1979, Norman 1984). This may be shown to represent gliosis rather than cerebral edema (McCormick 1966, Wortzman 1983). The gliotic "pseudocapsule" is irregular and penetrated by numerous vessels of the AVM. Whether it results from local mass effect from the bounding pulsations of the AVM vessels, a reaction of the brain to hemorrhage, or is simply cerebral tissue which has undergone necrosis through anoxia is speculative. Other factors contributing to gliotic reaction around an AVM might be reduced circulation of CSF, impaired venous drainage and metabolites released from the vessels of the AVM to the tissue.

Obstruction Obstruction to CSF outflow, may occur in several ways: Direct obstruction causing hydrocephalus, indirect obstruction at the pacchionian granulations and increased venous pressure leading to communicating hydrocephalus. Blood or increased protein within the CSF or increased pressure in the venous system causes stagnation of CSF circulation and poor resorption. Compression of the Sylvian aqueduct by arteriovenous malformations of the vein of Galen and posterior fossa frequently leads to obstructive hydrocephalus (Rosenheck 1937, Graf 1946, French and Peyton 1954, Logue and Monckton 1954, Litvak et al. 1960, Poppen and Avmann 1960, McCormick et al. 1968, Zingesser et al. 1969, Amacher and Shillito 1973, Defeo et al. 1976, Ya§argil 1976, Esparza et al. 1980). Russell

and Nevin documented obstructive hydrocephalus due to an aneurysm of the great vein of Galen in 1940. Infratentorial AVMs, including dural arterial venous fistulas, lead to obstructive symptoms more frequently than supratentorial malformations (Brainin and Samec 1983, Defeo et al. 1976, McCormick et al. 1968). As with infratentorial tumors, this is felt to be secondary to compartmental^estraints and an inability to accommodate space occupying lesions. Dandy and Blackfan (1914) suggested that CSF absorption would be hindered by increasing the venous backflow pressure in the dural venous sinuses. In 1948, Krayenbuhl and Luthy stated that hydrocephalus occurred from increased venous pressure with some vein of Galen aneurysms. Blockage of venous outflow may also account for the appearance and growth of arterial meningeal fistulas (Brainin and Samec 1983). Many clinical studies have shown that increases in superior sagittal sinus pressure leads to pseudotumor cerebri (Gardner 1939) and/or communicating hydrocephalus (Esparza et al. 1980, Sainte-Rose et al. 1984). It has been shown that ventricular and subarachnoid enlargement can occur in cases where the patient is young and still has a distensible skull (Haar and Miller 1975, Lamas et al. 1977, Rosman and Shands 1978, Sainte-Rose et al. 1984). Cronqvist et al. (1972) and Lamas et al. (1977) made similar findings in patients with arteriovenous malformations. Hydrocephalus commonly occurs with vein of Galen aneurysms (Ya§argil 1976). In all patients with vein of Galen aneurysms over the age of 2 years, the hydrocephalus was obstructive. McCormick et al. (1968) found that out of 157 patients with posterior fossa AVMs, 10 cases of hydrocephalus were identified. Of those, 7 were shown to be obstructing the aqueduct, while 3 had signs of ventricular dilatation without mechanical obstruction. McCormick noted that 2 of the 3 had experienced a SAH. He could not find a cause in the third case.

Hemorrhage Repeated hemorrhage may occur from feeding vessels close to the AVM, within the malformation, or from draining veins of the lesion. It may also occur from aneurysms found on the feeding vessels either close to or distant from the malformation.

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4. Hemodynamics

Hemorrhage takes two basic forms. The first results in a intracerebral hematoma, with or without intraventricular extension and destruction of cerebral tissue. The pathophysiology of such bleeds is dependent upon their size and location. As noted earlier (Laplace's law), hematomas associated with AVMs are usually secondary to venous rupture (Nornes and Grip 1980), or at least on the venous side of the malformation (Pellettieri 1979), and therefore are rarely as devastating as most arterial hemorrhages. Nornes and Grip (1980) studied the pressure in draining veins in cases of AVM finding the average pressure to be 17 mmHg in those patients with a history of hemorrhage, and 14 mmHg in those without. These values were Obtained during open craniotomy. Interestingly the AVM patients who suffered from large, even extensive hematomas due to a rupture, have a remarkable tendency to recover even without surgical removal of the hematomas, whereas the patients with hematomas due to the rupture of aneurysms are usually more seriously troubled (Fig 4.10). The second type of hemorrhage is the classical subarachnoid hemorrhage. AVMs have a lower incidence of presentation with subarachnoid hemorrhage, of recurrent hemorrhage, and of mortality from hemorrhage when compared to cerebral aneurysms. A subarachnoid hemorrhage is usually not associated with vasospasm even though the hemorrhage may be similar in magnitude and site to an aneurysm. The reasons for the lack of even local arterial spasm remain unclear. We saw spasm in only 1 of 500 AVM cases (Fig 6.21D). Deep seated AVMs present earlier (Nystrom 1978) and more often with symptoms related to hemorrhage than superficial malformations. | Superficial AVMs are considerably more epileptogenic, which accounts for their second most common clinical presentation. Pellettieri (1979) confirmed that, with exception of vein of Galen mal-) formations, the deep central AVMs have a greater . propensity to bleed than superficial ones. He proposed that this was because the deeper lesions have a greater number of fragile arterial feeders and poorer venous drainage. Interestingly, hemorrhage is also more common in smaller arteriovenous malformations (Paterson and McKissock 1956, Hook and Johanson 1958, Kaplan et al. 1961). Pellettieri first reported the phenomenon of backflow in 1979. Blood in a large draining vein of a convexial AVM flowed in a retrograde fashion into veins draining normal cerebral areas. Pellettieri's results indicated that AVMs with backflow

References p. 388

into diversionary veins were less likely to bleed than AVMs lacking such backflow. In addition, this retrograde flow appears to be more common with high shunt flow AVMs. Pellettieri proposed that the "reduced bleeding tendency in AVMs with backflow might be due to a circulatory adaptation of the vascular bed, with a larger volume on the venous side, which in turn should mean a lower intravascular pressure". This explanation is in accordance with the observation that large convexial AVMs also have a smaller tendency to rupture. See Vol. Ill B, Chapter 9, Final comments concerning venous system. Repeated subarachnoid hemorrhages take a progressive toll on the brain. The pathological changes may include communicating hydrocepha-lus, direct mechanical and chemical destruction of neighboring neurons, and progressive cicatrix formation with vascular or glial-neuronal cytoplasmic impediment. Steiner et al. in 1975 analyzed the effects of repeated subarachnoid hemorrhages in dogs. They confirmed the findings of Burch et al. (1954), Eichbaum and Bisetti (1965), and Cruickshank et al. (1974) and demonstrated that high I intracranial pressures can cause varying degrees of myocardial damage.

Vascular Steal Murphy described this concept in 1954 as "a steal from the brain," with descriptive adjectives such as "a parasite on the circulation" being used by Pool and Potts (1965). The idea of cerebral steal arises from the logical observation that if blood normally destined for neural structures is siphoned off by an arteriovenous shunt, then those same neural structures would be deprived of vital blood flow. Despite the logic of this theory, it remains a highly controversial topic. J. F. Fulton (1928) noted an increased 'intensity' of a bruit in a patient with an occipital AVM during visual stimulation. This phenomenon of increased blood flow to areas of cerebral activity is well known, but its occurrence in association with an

Fig4.10A-G This 22 year old male fell down some stairs and remained unconscious for a few minutes. Afterwards he complained of right sided hypesthesia. On admission lumbar puncture showed bloody CSF. Further examination revealed a left capsular AVM with a single huge draining vein. The patient, who had no neurological deficit, refused surgery. The next attack occured 1'/2 years later accompanied by intraventricular hematoma. Two months later the patient regained consciousness and showed remarkable improvement of hemiplegia and aphasia. Radiotherapy in Stockholm was refused. The decision regarding surgery is still open.

References p. 388 A-B CT scan.

C-D Carotid and vertebral angiograms, arterial phase, lateral view. E-F Carotid and vertebral angiograms in frontal view: The plexi-form part of the AVM is located within the internal capsule, whereas the varix is in the cella media (body of the lateral ventricle). G Venous phase (carotid) shows unusual fusiform dilatation of the thalamic, internal cerebral and galenic veins. Note backflow towards the basal vein and the delayed appearance of straight sinus.

Vascular Steal

229

230

4. Hemodynamics

AVM has important implications with respect to the viability of cerebral autoregulation in adjacent tissues. McRae and Valentine in 1958 found that generalized or local atrophy was the most common pneumoencephalographic finding in patients with AVMs. It was not stated whether this occurred in all patients, or just in older patients, and whether or not the atrophy was more common in patients with larger AVMs, prior history of subarachnoid hemorrhage, etc. Atrophy is certainly found in children with AVMs of the vein of Galen and in

References p. 388

large AVMs in young and elder patients (Fig 4.11). In 1938 Elvidge angiographically demonstrated that in the presence of angiomas, there existed a rapid circulation time with early filling of draining veins and a comparatively poor filling of the normal arterial branches. Norlen (1949) found that dilatation of the arterial feeders regressed to normal after removal of the A-V shunt and that vessels in the brain around the AVM, which did not fill well before excision, filled in a normal angio-graphic pattern 2 to 3 weeks postoperatively.

Fig4.11A-l A A 27 year old female presented with a large right parieto-occipito-temporal AVM containing multiple fistulas. A right carotid angiogram showed dilatation of the right carotid artery and temporooccipital branches of MCA and poor visualization of the other branches of MCA. Note the associated aneurysm of the ICA. В Vertebral angiography, lateral view, showed dilatation and elongation of the basilar artery and the posterior cerebral artery. The parietooccipital and calcarine arteries are not visualized. С Left carotid angiography, frontal view, showed an enlarged left A1 segment and filling of both A2 segments. D After elimination of pial (M3 branches) and dural feeders at the first operation left carotid angiography clearly showed increased participation of the right A2 in the supply of the AVM.

References p. 388 Fig4.11E-F MRI showed the location and extent of the AVM. It was remarkable that this patient did not have any visual field defect preoperatively. G-H Coronal CT showed left frontal and less pronounced parietal atrophy (arrow). Preoperatively she suffered from mental deterioration because of a steal syndrome. Postoperatively gradual improvement was observed. I Postoperative CT scan after complete removal of the AVM. The visual field could not be preserved.

Vascular Steal

231

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4. Hemodynamics

Bessman et al. reported similar arterial regression following surgery in 1952 (Fig 4.12). In 1959, Tonnis published an important analysis of AVM physiology based on angiographic studies. Serial angiography revealed that the increase in cerebral blood flow was to the AVM and not to , the remainder of the brain. Both the volume and I the rate of blood flow were found to be substan-ч tially higher in the AVM (1.8-3.0 seconds difference). Lesczynski et al. (1963) found similar differences in circulation times, and also demonstrated that feeding vessels filled 0.1-0.2 seconds earlier than those supplying the surrounding brain. However, angiography revealed that this difference was substantially smaller for larger AVMs. Tonnis suggested that this significant reduction in the rate of blood flow through the AVM was secondary to increased turbulence. As the vessels of large AVMs tend to be massively dilated, Reynold's number (turbulence) becomes significant. Schurr and Wickbom (1952) published an angiographic picture demonstrating this slowing. However, evidence is lacking that AVMs with

References p. 388

greatly enlarged vessels may have less steal effect than similar sized AVMs with smaller vessel diameters. Fluorescein angiography (Feindel et al. 1967, 1971) has led to important observations with respect to cerebral steal. Rapid circulation times with early filling of veins and relatively poor filling of normal arteries in adjacent brain with conversion of shunt flow to perfusion flow have been seen following extirpation of AVMs. By using Doppler probes Nornes et al. (1979) were able to analyze the cerebral hemodynamics of arteriovenous malformations intra-operatively. Doppler analysis determines blood velocities (cm/ sec) and only indirectly measures flow, the latter being expressed conventionally as cc/100 gms of brain/min. For physiologic discussions, Nornes was able to identify areas of turbulence and laminar flow (whose parabolic front obtained speeds of twice mean velocity), and, importantly, to identify AVM arterial feeders by the nature of their increased velocities. Fig4.12A-H A left parietal (postcentral sulcus) AVM in a 33 year old male. A-B Preoperative CT showed the extent of the AVM. The malformation was removed in one session. The postoperative course was initially uneventful. Subacute deterioration occured two days later. С CT shows hematoma in the operative field which was immediately removed. D CT performed 7 months later. He had remarkable improvement of his hemiparesis and full return of his speech.

References p. 388

Vascular Steal

233

Fig 4.12E-H Pre- and postoperative carotid angiography showed normalization of the diameter of the previously dilated АСА and MCA branches after surgery. Full recovery.

Hassler and Gilsbach (1984) investigated 35 patients undergoing AVM resection with intraoperative Doppler flow velocities and immediate postoperative angiography. Following excision of the AVM Doppler studies showed reduction in diastolic flow velocity, slow flow in the large arteries, and a steep pulse curve indicating increased resistance and higher pressure in the arteries. Angiographic studies showed improved demon-

stration of the circulation in 27/35 patients, reduction in diameter of the ipsilateral extradural ICA, and the presence of "stagnating arteries" with slow flow. Twelve of 35 patients had complications of edema or hemorrhage. The authors related these to AVMs with high flow preexcision and slow flow and high resistance postexcision, to the presence of long feeding arteries, and to enlarged pial arteries around the site of excision.

234

4. Hemodynamics

They felt these patients were at risk for perfusion pressure breakthrough. Currently the most common method for analyzing cerebral blood flow employs radioisotope quantitative detection based on the Pick principle (1870). Shenkin et al. (1948), were the first authors to study patients with arteriovenous malformations using N2O. They demonstrated an increase in cerebral blood flow of 3-4 fold despite normal levels of oxygen consumption, concluding that the increased blood was shunted past cerebral structures. Lassen and Munck in 1954 reported the first use of radioactive krypton to evaluate cerebral blood flow in man. This method measured total but not regional blood flow. Xenon has replaced krypton, and, because of sophisticated instrumentation and the advent of the computer, moderately good analysis of regional cerebral blood flow can now be obtained noninvasively. Yet the Pick principle has significant flaws when applied to lesions of high flow. Gas analysis of cerebral blood flow classically reveals "high shunt peaks". These peaks reflect the high volume and fast rate of radioisotope flow through an AVM compared to the lower and longer curves obtained over regions of normal brain (Heiss et al. 1970). By selectively analyzing the two curves, a quantitative measure of blood flow through the AVM can be obtained. Closure of the main arterial feeder, and/or excision of the AVM is followed by a reduction in amplitude and prolongation of the isotope flow curve. Following operative excision of an AVM, Feindel found an increase in perfusion flow in the surrounding normal brain, thus confirming the angiographic findings of Norlen and others. Confirmation of Fulton's observation (1928) of alteration of blood flow through an occipital AVM by visual stimulation was achieved by Deutsch in 1983 using xenon 133 inhalation analysis. Visual stimulation in normal subjects produces increase in CBF to the occipital lobes (Lassen et al. 1977). In Deutsch's case of an occipital arteriovenous malformation, concentrated visual activity also produced a higher flow to the occipital lobe containing the AVM. Most interestingly, however, with non-visual stimulation the AVM "stood out as a region of high blood flow during a relaxed state, while it approached normal flow levels when there was attentional demand". That is, certain nonvisualization mental activity "normalized" the blood flow through the AVM. Thus a degree of autoregulation existed for regions of the brain distant to the AVM of sufficient strength to 'steal' blood away from the AVM! Autoregulation can

References p. 388

also be assumed to be present in the effected occipital lobe. If the AVM was stealing blood from the adjacent occipital cerebrum, then during non-visualization tasks, when the frontal lobes appropriated more blood, the patient might experience visual symptoms reflecting borderline hypoxia. Though reports of acute symptoms of this nature are lacking, chronic effects on cerebral tissues are clearly documented. Clever use of the CT scan was introduced to evaluate specific patterns of regional cerebral blood flow (Meyer et al. 1980, Lassen et al. 1981). Stable xenon gas, like iodine, has a high atomic number and thus absorbs x-rays, but unlike iodine it is a freely diffusible contrast agent. Okabe et al. in 1983, studied regional blood flow before and after excision, comparing the classical method of scintillation detection of radioactive xenon and non-radioactive xenon analysis with CT. They also analyzed regional CBF (rCBF) values for patients with AVMs and compared their results to normal age-matched healthy volunteers. Mean rCBF values in AVM patients were significantly reduced in regions adjacent to the AVM in both grey and white matter. Contralateral hemispheric flows were significantly reduced compared to normal controls for grey matter but not for white matter. The difference between the two inter-hemispheric grey matter flows were also significantly different in patients with AVMs (but, of course, equal for normal patients). After successful surgical removal of the AVM, mean regional cerebral blood flows for grey matter returned to normal in both the hemisphere containing the AVM and the contralateral hemisphere. The white matter flow in the AVM-containing-hemisphere improved significantly, but flow improvement in the contralateral hemisphere was not statistically significant. This overall increased blood flow was mirrored by clinical improvement in Okabe's series of patients. However, in those patients in whom surgery was not performed, CT-CBF analysis showed either no improvement or, in most cases, a progressive decline in rCBF, concomitant with clinical deterioration of the patient. Okabe's finding that the grey matter was subject to the greatest degree of vascular steal is important and might be expected, in that grey matter normally receives proportionally more blood than does the white matter. A similar pattern was described by Meyer et al. (1982) while studying the effects of by-pass procedures in patients with hemispheric ischemia.

References p. 388

Single Photon Emission Computerized Tomography (SPECT), introduced by Kuhl in 1963, has recently gained significant clinical importance (Las-sen 1983, Lassen et al. 1978) and may prove useful in a more refined study of AVMs. Pertuiset et al. (1981) analyzed the effects of hypotension on cerebral blood flow and auto-regulation using technetium 99 labeled red blood cells. Nearly 90% of 27 patients with AVMs studied showed evidence of autoregulation. During periods of hypotension the CBF in the adjacent brain would increase, while that in the AVM would "passively" decline in proportion to the pressure drop. Conversely, when normal pressures were reinstituted the CBF would appropriately decline in the surrounding tissues, while again passively rising within the malformation. Thus the pathologic vessels were passive while the adjacent tissues showed evidence of autoregulation during changes in blood pressure. However, when the curves for CBF were compared to similar studies in patients with associated saccular aneurysms, for example, the AVM peaks were distinctly less clearly defined. Pertuiset also demonstrated that arteries not seen during normal angiography, filled under hypoten-sive conditions. During hypotensive angiography, the capillary phase on the contralateral hemisphere also became more prominent. These later observations added angiographic support to Deutsch's findings that adjacent cerebral tissues may or may not have exhausted their autoregula-tory drives; and when not yet at their maximal

Systemic Effects

limits for autoregulatory dilatation (even in the presence of steal) the vessels in surrounding brain were capable of adequately providing the tissues they supplied. The controversy regarding cerebrovascular steal has not been so much a question as to whether in occurs, which it must by all the laws of hemodynamics, but whether it is of clinical significance. That is, in the presence of viable autoregulation are the cerebral tissues still capable of acquiring enough perfusion to meet their needs? Many patients presenting in middle age or later in life with hemorrhage or epilepsy from an AVM have previously been physically extremely active people and have included sportsmen (world master and Olympic gold medal winners in athletics), pilots, and women who have had multiple pregnancies, a hypermetabolic state. In such cases there has been little to suggest the presence of significant cerebrovascular steal. Nevertheless, the natural history of AVMs may be one of progressive mental decline even in the absence of hemorrhage or other pathological mechanisms. Cerebrovascular steal must be considered a malignant cause of morbidity although, as pointed out by Drake (1979) and Yamada (1982), bleeds may often go unrecognized by the physician or by the patient and symptoms of progressive neurological decline may be more a result of minor bleeds or even perhaps be due to as yet undiscovered metabolic influences of the AVM itself.

Systemic Effects The effects of most cerebral arteriovenous malformations on the remainder of the cardiovascular system, with the exception of vein of Galen aneurysms occurring in infants (Glatt and Rowe 1960, Levine et al. 1961), are generally of little concern to the neurosurgeon. Even in the absence of cardiac failure, however, systemic pathophysiological mechanisms have been well documented in adults (Schlesinger and Hazen 1954, Leslie et al. 1960, Wallace et al. 1965) (Fig 4.13). Wallace et al. (1965) deduced that fistula flow and cardiac effects when standing would be less than expected when recumbent. They found that an injection of isoproterenol caused not only an increase in systemic flow secondary to the drop in systemic resistance, but also a decrease in the amount of blood flowing to the AVM. This supports the theory that the vessels supplying the AVM, and the AVM itself, are maximally dilated

and therefore cannot decrease their resistance in order to maintain their perfusion. Exercising muscle will normally increase its blood flow in order to meet its metabolic requirements. Binak et al. (1960) showed that when muscles supplied by arteries feeding an adjacent A-V fistula were exercised, the fistula would not only acutely enlarge, but also increase its rate of growth. Based on blood flow studies Fulton 1928, Lassen et al. 1977, Sokoloff 1981, Deutsch 1983, and others hypothesized that growth of cerebral AVMs might similarly be affected, not because the malformation becomes "stronger", but because of the increased flow to its vicinity. Bauer et al. (1975) reviewed the literature and presented his own findings on the effects of cerebral AVMs on the cardiovascular system. He concluded that:

236

4. Hemodynamics

References p. 388 Fig 4.13A-E 31A> year old boy with a vein of Galen AVM with fistulous and plexiform components. A Carotid angiogram showed a fistulous connection between АСА, РСА and the vein of Galen and a second plexiform thalamic nidus draining into the internal cerebral vein (visualization in arterial phase of angiogram). В Vertebral angiography showed dilatation of both PCAs and their perforating branches and drainage into internal cerebral veins and galenic vein. Plexiform thalamic AVM. С This frontal view of the vertebral angiogram. D CT scan. E Chest radiograph showed significant cardiomegaly.

References p. 388 продолжение

1. The larger the AVM, the faster the circulation time and volume. This included the systemic as well as the cerebral circuits. High O2-saturation values in the inferior and superior v. cava indicated a hyperkinetic circulation even in adults. 2. Despite the hyperkinetic state, there was no

Operative Technique

237

increase in the right ventricular or pulmonary artery systolic or end diastolic pressures (i.e., no cardiac failure). 3. No cardiomegaly was seen. 4. Only in children, where the size of the AVM presents as a greater proportion of the circulation, will signs of heart failure become paramount.

Operative Considerations with Regard to Hemodynamics Preoperative Evaluation There is growing evidence that those patients with a high surgical risk can be identified preoperatively. In his outstanding monograph discussing surgical versus conservative treatment of intracranial arteriovenous malformations, Pellettieri (1979) was able to identify several prognostic variables and risk factors to predict long term results and, although operative cases did better overall, these factors had the same predictive quality for patients who did not undergo surgery. This work has recently been largely substantiated for conservatively treated patients by Crawford et al. (1986). Patients with the poorest outcomes were those who 1) had preoperative neurologic deficit, 2) were over 40 years of age, 3) had deep seated AVMs in 4) "non-silent" regions of the brain, and 5) were males with 6) large AVMs showing evidence of 7) prior subarachnoid hemorrhage. These variables are not necessarily concomitant. For example, smaller AVMs have the highest risk of presenting with a bleed (Graf et al. 1983), but not of recurrent hemorrhage (Crawford et al. 1986), but present less often with signs of progressive cerebral steal (Pellettieri 1979). On the other hand, larger AVMs generally occur in older patients, but the poorer the neurological status, the less risk of recurrent hemorrhage (Graf et al. 1983). Pellettieri's two most significant predictors fbr Jong-term results were age and neurological status on admission. If one considers NPPB to be an important factor in AVM surgery then one must define those patients at greatest theoretical risk for NPPB as having AVMs causing the greatest amount of steal. This would result in the largest number of vessels in the tissues surrounding the AVM being dilated and incapable of autoregulation. Wilson et al. (1979) suggested that this can be anticipated when, 1) the AVM is large, 2) there is evidence of

rapid fistula flow preventing visualization of normal circulation by angiography, and 3) when the patient is experiencing progressive neurologic deficit (in the absence of hemorrhage and mass effect) suggesting hemispheric ischemia. These factors may be assessed using Luessenhop's grading system (Luessenhop and Gennarelly 1977) whereby the number of major feeding vessels (1 to 4) are correlated with the degree of surgical difficulty. High flow shunts could be expected to have acquired a greater number, if not just an increased size, of feeding arteries (Pellettieri 1979).

Operative Technique The physiological principles and theories outlined above may specifically be adapted towards techniques aimed at improving the ease with which an AVM can be removed and towards altering the "normal" physiology of the malformation. Physiologic alterations which will prevent the rupture of an AVM, and once ruptured, will decrease the amount of blood loss from the AVM, are those which reduce blood flow through the malformation. This may be accomplished by: 1) Pre- or peroperative embolization. 2) Staging of surgical resection. 3) Intra- and postoperative hypotension. 4) Temporary bypass between the common carotid artery and the jugular vein by side-to-side _anastomosis (Bleasel 1985).___________ 5) Reduction of carotid artery blood flow by use of a Selverstone clamp (Bonnal et al. 1985). 6) Diversion of the arterial flow through the AVM by a surgically placed temporary fistula from a major arterial feeder to a draining vein. 7) Improvement of venous drainage in case of agenesis or obstruction of a main venous sinus with the help of an intra-extracranial venovenous bypass procedure. 8) Pre- and postoperative dehydration.

238

4. Hemodynamics

(1) Preoperative embolization as a method of decreasing flow to an AVM has been advocated by numerous authors (Luessenhop et al. 1965, Luessenhop and Rosa 1984, Hilal 1985, Hilal et al. 1973, Wolpert and Stein 1975, Stein and Wolpert 1985, and Bercnstein and Epstein 1982) and preoperative cannulation_of arterial feeders has been used by Drake (1979). The major disadvantages to such techniques are three: 1) The risk of embolizing arterial feeders which still contribute to vital cerebral tissue distal to the AVM. 2) The irreversibility of such embolization, should it be followed by neurological deterioration (Kvam et al. 1980, Jones et al. 1982a), and 3) as pointed out by its advocators (Luessenhop and Rosa 1984); they were "not convinced this led to easier or safer surgery; in fact, the reverse may be true because blocking the major feeding arteries leads to greater participation of the deeper, surgically less accessible arteries" (Drake 1979). This problem has been partially avoided by using balloons which can be deflated should signs of clinical deterioration arise prior to permanent release of the balloon (Serbinenko 1977, Luessenhop and Rosa 1984). (2) Staging of the surgical procedure has many advocates (Spetzler et al. 1978, Drake 1979, Wilson and York 1980, Day et al. 1982, Yamada 1982, Pertuiset et al. 1985, U 1985). The theoretical advantages are similar to those offered by embolization and were summarized by Yamada (1982) as follows: 1. Thrombosis propagates from the coagulated arterioles and venules into the AVM core, allowing the surgeon to continue to an advanced stage of the procedure. Therefore, the active part of the AVM with which the surgeon would have to cope at the first operation is bloodless at the second operation. 2. Postoperative angiograms demonstrate feeding arteries and draining veins more discerningly, since some part of the AVM has already been blocked with thrombi during and after operation. Thus, it is safe to handle the deep-seated portion of the AVM. 3) The less the cerebral traction, tissue manipujlation, and electrical coagulation, the less the 'cerebral edema. Cerebral function quickly recovers from the operative insult after each operation. 4. The cerebral tissue surrounding the AVM can adjust to a new circulatory environment after the interruptioh of communicating arterioles and venules. In addition, should delayed breakthrough occur, it is likely to be less severe than if all the arterial feeders to the AVM had been clipped at once.

References p. 388

Experience in Zurich has not shown the need for staged operation for fear of NPPB, even in cases of giant AVM. Indeed, it is strongly recommended that the practice of staged operation not be carried out routinely for large AVMs as it is felt that there is a greater risk of bleeding after such staged procedures from parts of the AVM left behind. Subjecting the patient to repeated operations also increases the potential risk from general complications such as jmesthetic misadventure, chest infection, and pulmonary embolism. (3) Along with the advent of the microsurgical approach to arteriovenous malformations, we are also seeing ^resurgence of the use of intraopera-tive hypotension. A thorough review of hypoten-sive surgery, and especially the pathophysiological effects of hypotension upon the cerebral autoregu-! latory mechanisms can be obtained in Pertuiset's I monograph (Pertuiset et al. 1981). Hypotensive ' surgery during intracranial vascular procedures has been reported by a number of authors (Pool and Potts 1965, Drake 1966, Patterson 1968, and Hamby 1969). Pertuiset found that he could maintain patients in a state of "profound hypotension" with mean arterial pressures of 30-40 mmHg for periods of 30 minutes without risking cerebral damage. Needless to say, these pressures are considerably below the minimum autoregulatory limits. Profound hypotension, though very useful in many patients, could be disastrous for those patients in whom autoregulatory mechanisms had already forced vessels supplying normal tissue into a state of maximum dilatation. Thus as hypotensive values were approached, no compensation could be made by the taxed cerebral vessels, and blood flow in them would follow a "passive" decline, in conjunction with that observed in the malformation. If the tissues were already experiencing the deleterious effects of chronic vascular steal, it is probable that infarction would ensue. Nornes et al. (1979) note this possibility in their article, stating that they have abandoned the use of any hypotension during AVM surgery. Reflecting upon the Poiseuille-Hagen formula for blood flow, and the observations of Yamada (1982), Nornes coined the term "surgical steal". If blood flow to an AVM increases when one of its draining veins is accidently ruptured during resection, this increased flow will deprive the adjacent tissues of further blood. This surgical steal is as deleterious to the brain as temporary occlusion of a cerebral artery (Nornes). When considering cerebrovascular and surgical steal phenomena it is interesting to note that for some time, our neuroradiological colleagues have

References p. 388

angiographically demonstrated, after simple occlusion of the main feeding vessels to an AVM, vessels which were previously invisible on the radiographs. They have coined the term "neuroradiological steal". We recommend the use of hypotension in moderation. Thus during the coagulation of feeders from deep, friable perforating vessels, we use mild hypotension down to a mean of 70 to 80 mmHg, which is safely above the lower limits of autoregulation. We modify this upwards for older or hypertensive patients. If bleeding becomes difficult during resection of the remaining deep apex of the malformation, we use profound hypotension as necessary. (4) As many surgeons have attested, we find that it is the remaining deep small fragments of the AVM which produce the greatest difficulty. If an artificial shunt were created to divert blood from these fragile regions, could their extirpation be facilitated? Before starting to remove the AVM one could take an artery, which by angiography and inspection is terminating in the malformation. The artery may be carefully dissected free, a proximal temporary clip placed on the vessel, and the artery sewn end-to-side into a convenient vein draining the malformation. In one such case, when the clip was removed the malformation mass could be seen to shrink, and have diminished pulsations. Though promising, this technique has yet to be properly developed, like the other proposed techniques (5,6,7). (5) Dehydration: One source of postoperative edema, that of fluid overload, is frequently overlooked. A common cause of this is the over anticipation of surgical blood loss resulting in the administration of excessive amounts of saline or plasma-expanding substances to the patient. We are very careful not to over-hydrate the patient preoperatively (especially during induction of anesthesia), or during surgery. If hypotension ensues, replacement is made by whole blood in small quantities as necessary. This serves not only to maintain a low volume and pressure, but also to increase viscosity as well.

Postoperative Care In cases in which it is felt there is a high risk of postoperative hemorrhage (for example where there has been great difficulty in coagulating deep feeding vessels) Pertuiset's technique of maintaining hypotension while keeping the patient on the operating room table for a full 2 hours after skin closure could be of great benefit. This helps to

Postoperative Care

239

prevent poorly coagulated vessels from rupturing (i.e. more time for solid clot formation, avoids patient developing raised intracranial pressure from coughing). Pertuiset advocates maintaining the patient in a hypotensive state for up to a week or so following excision in cases of particularly large, high-flow and .malicious malformations. While this has not been found necessary in Zurich we whole-heartedly agree with gentle transfer of the patient to his bed, with the use of "deep" extubation, and with careful control of blood pressure. We have not resorted to the use ofhyperventilation or barbiturate therapy (Day et al. 1982) in the postoperative phase, feeling these are of dubious value.

240

5

Diagnosis and Follow-up of Patients with Cerebral AVM using Doppler Ultrasound Herbert M. Keller

Arteriovenous malformations account for approximately 1% of strokes of all types, i.e. the annual incidence rate is in the magnitude of 1 to 3 per 100 000 persons (Mohr et al. 1978, Mohr 1984). The point prevalence rate of AVMs is approximately 0.1-0.5%, i.e. one seventh as prevalent as cerebral aneurysms (McCormick 1984, Michel-sen 1979, Ferret and Nishioka 1966). AVMs are located supratentorially in about 90% of patients and infratentorially in the other 10% of patients (Drake 1979). An AVM is detected in rare instances in its asymptomatic state, but in most patients when symptoms occur. These can be disastrous if major intracranial bleeding occurs. In some patients, however, minor symptomatic bleeding may occur, sometimes jnyriicking_ focal neurologic symptoms as observed in transient ischemic attacks (TIA), reversible ischemic neurologic deficit (RIND), or ischemic stroke with only minor residual disability. Furthermore, focal or generalized seizure, intracerebral steal with isch_gmic symptoms, headache (sometimes of the migraneous-type), pulsesynchronous tinnitus, and, if a major AVM is already present at birth, enlargement of the heart and/or head in infancy can be the symptoms leading to the presentation of a patient with an AVM (Krayenbuhl and Ya§ar-gil 1972, Luessenhop 1984, McCormick 1984, Mohr 1984). Patients with "major" or "minor" symptoms of an AVM may be referred to clinics which have available different diagnostic facilities, e.g. computertomographic (CT) scanning, intravenous or intraarterial digital subtraction or conventional angiography, and various ultrasonic devices. We have used an extracranial cerebrovascular Doppler examination (based on continuouswave equipment) as a routine noninvasive cerebrovascular procedure in patients with angio-

graphically proven AVM and with major arteriovenous blood flow through the malformation (Btidingen et al. 1982, Keller et al. 1978, Keller 1982). Additional quantitative blood flow measurements in the common carotid arteries with a pulsed 14channel Doppler instrument, as well as transcranial blood flow velocity measurements in the territory of the middle cerebral arteries with a pulsed 2-Megahertz Doppler device have also been made in some of these patients (Aaslid et al. 1982, Keller et al. 1976). We have sought to evaluate the usefulness and cost-effective of these non invasive examinations in indicating further diagnostic work-up, such as CT scanning and angiography, and particularly in the follow-up of AVM patients without or with specific treatment for their lesion. Between 1976 and 1984, 44 patients with AVM were evaluated. Of these, 18 patients were males and 26 patients females, 33 patients were adults 17 to 66 years of age (mean 36 years) and 11 patients were children 2 months to 16 years of age (mean 11.4 years). After an initial clinical examination, all patients had a full 4-vessel intraarterial angiographic study before or after the specific neurovascular examinations with Doppler ultrasound. The specific neurovascular examinations with Doppler instruments included our routine extracranial cerebrovascular Doppler examination in all patients, and additional quantitative blood flow measurements in both common carotid arteries in 19 patients, and transcranial registrations of blood flow velocity signals from the major intracranial cerebral arteries in another 5 patients (Fig 5.1). In the extracranial cerebrovascular Doppler examination, based on continuous-wave equipment, blood flow signals proportional to the mean instantaneous blood velocity are recorded with

References p. 394

Doppler Ultrasound

241

Fig 5.1 A schematic representation of major extra- and intracranial cerebral arteries, measurement locations (dotted circles), and arteries to be compressed digitally (arrows) for the extracranial cerebrovascular Doppler examination with continuous-wave Doppler instruments (emission frequency between 5 to 10 MHz). The area of the dynamic blood flow balance between branches of the external and internal carotid arteries in the region of the orbit, as well as the intracranial portions of the arteries, are marked (---). The blood flow signals of the vertebral artery are picked up near the branching of the subclavian artery, (through the mouth) from the cervical portion, and in the region of the mastoid process from the atlas loop portion. The probe is pressed with very little force against the skin when blood flow signals of the veins in the region of the orbit or blood flow of the jugular vein in the region of the neck are registered. The measurement locations are identical with those for arterial blood flow registration in these regions. For intracranial arteries the Doppler probe is held over the temporal bone and the focused 2 MHz pulsed ultrasound beam is directed towards the middle, the anterior and the posterior cerebral arteries. A. = arteria, com. = communis, int. = interna, ext. = externa, dex. = dexter, sin. = sinister.

_zero-crossing techniques and signal characteristics interpreted with the human ear as the "natural" frequency analyser (Keller et al. 1978, Keller 1982). A bidirectional Doppler device with loudspeakers/earphones and a two-channel recorder is used. To evaluate the patency of the carotid arteries and identify a possible feeding artery from the carotid artery to an AVM, "indirect" and "direct" criteria are used. For "indirect" criteria, recordings are performed from the terminal branches of the ophthalmic artery, i.e. the supratrochlear and supraorbital arteries without and with digital compression of branches of the external carotid arteries and the common carotid arteries over a period of 2 to 4 cardiac cycles. If an AVM "steals" blood from the ophthalmic artery, decreased blood flow signals compared to contralateral recordings, or inverted blood flow direction in the ophthalmic artery, i.e. from extra- to intracranial can be expected. In the latter situation, blood flow sig-

nals will decrease, if its feeding artery, e.g. the superficial temporal or facial artery is compressed digitally. For "direct" criteria, recordings from the common, internal and external carotid arteries are performed with the Doppler probe held in a dorsal-caudal direction for the proximal portion of the common carotid artery, and in a dorsal-cranial direction for the middle and distal portion of the common carotid artery, the carotid bifurcation, and the extracranial portion of the internal carotid artery, as well as .the external carotid artery and its branches. Oscillation maneuvers are used to identify the external carotid artery and its different branches, e.g. by digitally tapping the superficial temporal artery in the region of the zygomatic bone. If a carotid artery or one of its larger branches is the major feeder for an AVM, increased blood flow signals can be expected with or without turbulence/blood flow inhomogeneity at the site of the carotid bifurcation indicating

242

5. Diagnosis and Follow-up with Ultrasound

"relative stenosis", i.e. blood flow volume is higher than that for which the vessel is "constructed". To evaluate the patency of the vertebral arteries and a possible feeder artery of these arteries to an AVM, "direct" recordings are performed from the subclavian arteries with the Doppler probe held in a dorsal-caudal direction in the supraclavicular region. Furthermore, blood flow signals from a vertebral artery are picked up from its proximal portion with the supraclavicular approach, and from its distal portion with the mastoidal approach (Keller et al. 1978, Keller 1982). By compressing the common carotid arteries and by digitally tapping the atlas loop of the vertebral arteries, the proximal portion of the latter can be identified and differentiated from other arteries in the supraclavicular region and in the oropharynx. Increased blood flow signals can be expected in one or both vertebral arteries if these vessels are major feeders to an infratentorial AVM, or if both vertebral and carotid arteries supply blood to a major supratentorial AVM. Recordings from the periorbital veins are obtained with the Doppler probe pressed with very little force against the skin over the target vessel, i.e. the supratrochlear, supraorbital, angular and facial veins (Keller 1982, Keller et al. 1982). Normally, periorbital veins drain blood into the cavernous sinus, i.e. venous blood flow is directed from extra- to intracranial and Doppler velocity signals are hardly recordable. In the presence of a major supratentorial AVM, increased venous blood flow in a reversed direction in one or several of these periorbital veins can be expected. Venous blood flow signals will decrease if major draining veins, e.g. the facial vein, or the venous plexus of the dorsum of the nose are compressed digitally. Increased venous blood flow signals in the jugular vein can be expected and recorded with Doppler from its neck portion near the carotid bifurcation if this vessel is a major draining vein for an AVM. For quantitative blood flow recordings from the common carotid arteries, a pulsed 14-channel Doppler device described elsewhere has been used (Keller et al. 1976). The normal range of blood flow values is between 300 and 450 millimeters per minute. If a carotid artery is a major feeder to an AVM, increased values can be expected. Intracranial Doppler measurements have been measured using a pulsed 2-Megahertz transcranial Doppler device, recently developed by Aaslid, in the last 6 patients of our series, since this device has only been at our disposal since the beginning of 1984 (Aaslid et al. 1982). Blood velocity recordings with Fast Fourier spectral

References p. 394

analysis are performed from the siphon portion of the internal carotid arteries by the transorbital approach and from the anterior, middle and posterior cerebral arteries, usually at a depth of 5 to 6.5 cm by the transtemporal approach (Fig 5.1). Using the transforaminal approach blood velocity signals from the distal portion of the vertebral arteries before its union to the basilar artery can be recorded as well as from the basilar artery itself. To identify the intracranial branches of the carotid arteries, carotid artery compression maneuvers over 2 to 4 cardiac cycles are performed. If branches of a carotid, vertebral or basilar arteries are major feeders to an AVM. increased blood flow velocity signals in these arteries can be expected. Clinical manifestations of angiographically proven intracranial AVM in the 44 patients ranged from major intracranial bleeding with loss of consciousness and serious neurologic deficit to minor symptoms such as unspecific headache or intermittent pulse-synchronous tinnitus (Table 5.1). An asymptomatic AVM was found incidentally in one patient. Seven patients had a hemiparesis. Of these, 3 patients had transient symptoms of the "little-stroke type", i.e. 4 patients were free of symptoms after 24 hours, and 3 patients had a minor neurologic deficit. CT scans demonstrated a major supratentorial AVM in all 7 patients, as well as ischemic infarction in 4 of these patients and minor bleeding in the other 3 patients. Angiographically, the AVM was located supratentorially in 38 patients and infratentorially in the other 6 patients. In 19 patients, angiography was performed after the initial clinical and noninvasive neurovascular examination with Doppler instruments and confirmed the findings of a major supratentorial intracerebral or dural (3 patients only) AVM. In all 6 patients with an infratentorial AVM, angiography was performed before the noninvasive neurovascular examinations. The results of the extracranial cerebrovascular Doppler examination based on continuous-wave equipment are demonstrated in Tables 5.2a-d. Increased blood flow in one or several extracranial feeding arteries to the AVM was found in 37 patients. Two additional patients with a supratentorial AVM had normal blood flow signals in all extracranial cerebral arteries but steal from the ophthalmic artery to the AVM, indicated by decreased or reversed blood flow in the periorbital branches of the ophthalmic artery. Thus, 39 of 44 AVM had pathological findings in the extracranial cerebrovascular Doppler examination, indicating an overall sensitivity of 89%. For supratentorial AVM, sensitivity was 92%, and for infratentorial

References p. 394 Table 5.1

Doppler Ultrasound

243

Symptoms in the 44 patients with an AVM leading to their clinical attention One or seve in a give [-]

ral symptoms зп patient [%]

Major sympt in a give [-]

om complaint эп patient [%]

Major intracranial bleeding

16

36.4

16

36.4

(Recurrent) seizure

13

29.5

10

22.7

Hemiparesis (minor bleeding/ischemic)

7

15.9

7

15.9

Headache

9

20.5

4

9.1

Pulse-synchronous tinnitus

8

18.2

3

6.8

Enlargement of heart/head

3

6.8

3

6.8

Accidental finding

1

2.3

1

2.3

Table 5.2 Results of the extracranial cerebrovascular Doppler examination in the 44 patients with a major AVM angiographically a 37 patients had increased blood flow signals in one or several extracranial cerebral arteries No. of patients

Location

of AVM

supratentorial

infratentorial

One carotid artery only

13

13

One or both carotid arteries

4

4

One carotid artery and one or both vertebral arteries

7

7

Both carotid arteries and one or both vertebral arteries

9

9

One or both vertebral arteries only

4

Normal all

7

4 5

2

b 16 patients had steal from one or both ophthalmic arteries to the (supratentorial) AVM One side only

9

Both sides

5

One side without increased blood flow in 2 the carotid artery

с 5 patients (with supratentorial AVM) had pathological periorbital venous blood flow

d 16 patients (with supratentorial AVM) had increased jugular venous blood flow signals

One side only

3

One side only

13

Both sides

2

Both sides

3

244

5. Diagnosis and Follow-up with Ultrasound

AVM 67%. Decreased or reversed blood flow in the ophthalmic artery was found in 16 patients, all of whom had a supratentorial AVM. Of these all but 2 patients had increased blood flow in one or several extracranial cerebral arteries. Intra- to extracranial venous blood flow in perior-bital veins was present in 5 patients, i.-e. in these, increased venous flow through the AVM changed venous blood flow direction from extra-intracra-nial to intra-extracranial. In these patients, venous blood flow pressure in the cavernous sinus was increased and periorbital veins could no longer drain their blood towards the intracranial sinus. Increased venous blood flow in the jugular vein was found in these 5 patients and in a further 11 patients, all of whom had a supratentorial AVM. Quantitative blood flow measurement in the common carotid arteries in 20 patients with a supratentorial AVM and with pathological findings in the extracranial Doppler examination demonstrated increased blood flow in 19 patients, usually on the side of the AVM. In 2 of these patients increased blood flow was recorded in both common carotid arteries. Maximum values were in the range of 1700 ml per minute, i. e. a 4-fold increase of common carotid artery blood flow (Table 5.3). Transcranial Doppler examination of the middle cerebral artery in 5 patients with supratentorial AVM demonstrated a major increase in flow velocity with values between 130 and 150 cm per second as compared to the contralateral normal values in the range of 40 to 100 cm per second (Table 5.4). Twenty patients were reexamined following a specific treatment measure for their AVM, 2 patients had catheter embolization with silastic material and one patient had irradiation. Before treatment, 19 of these patients had pathological findings on Doppler examinations. After treatment, normal findings were present in all 20 patients, indicating that a major part of the AVM was removed or major feeding arteries were obliterated. Typical findings of the extracranial cerebrovascular Doppler examination are demonstrated in Figs 5.2 to 5.4. In one of the 3 patients, the results of the additional transcranial Doppler examination also are demonstrated. Fig 5.2 shows the findings in a 26-year-old patient who presented with one generalized epileptic seizure. Otherwise the patient felt well. Normal per-fusion in the periorbital arteries was found, but the common and internal carotid artery on the right side showed increased diastolic blood flow signals. Transcranial Doppler examination demonstrated a major increase of blood flow velocity in the right middle cerebral artery with

References p. 394

Table 5.3 Results of the additionally performed quantitative blood flow measurements in the common carotid arteries in 19 patients with a supratentorial AVM. The range of the asymmetry index, i.e. the ratio of blood flow values in the common carotid artery on the side of the AVM vs the values on the contralateral side was 1.0-3.1 (mean 1.6) No. of patients Normal range (300-450 ml per minute)

5

Increased values (>450-1700 ml per minute)

14

Table 5.4 Results of the additionally performed transcranial Doppler measurements of blood flow velocity in the middle cerebral artery on the side of the supratentorial AVM in 5 patients (increased values were between 130-150 cm per second) No. of patients Normal range (40-100 cm per second)

-

Increased values (> 100-150 cm per second)

5

mean values of 150 cm per second as compared to the normal values on the left side (60 cm per second). A major supratentorial AVM in the territory of the right middle cerebral artery was demonstrated angiographically. The AVM was removed surgically. Fig 5.3 demonstrates pre- and postoperative findings of extracranial Doppler examination in a 10year-old boy with bruits over the base of the heart, the neck, and over temporal bones since the age of 3 years. The head was disproportionally big and dilated vessels were present on both sides of the neck. Blood flow signals from the periorbital arteries indicated alternating blood flow, i.e. intra- to extracranial blood flow direction during systole and extra- to intracranial blood flow direction during diastole. Increased blood flow signals also were present in both common carotid arteries and a loud bruit could be heard at the side of both carotid bifurcations. Angiography demonstrated a huge supratentorial AVM with major feeding from the left carotid and vertebral artery and to a lesser extent from the right internal carotid artery. The AVM was removed neurosurgically and postoperative measurements demonstrated normal "indirect" and "direct" findings in the region of both carotid bifurcations with recordable blood flow signals from the external and internal carotid arteries.

References p. 394

Doppler Ultrasound

245

Fig 5.2 Findings of the extracranial and transcranial Doppler examination in a 26 year old patient who suffered one generalized epileptic seizure. No bruit was heard in the clinical examination, neither in the region of the neck nor over the skull. The extracranial Doppler examination demonstrated normal perfusion in the periorbital arteries, i.d. the supratrochlear and supraorbital arteries (first 3 registrations from top). The internal carotid artery on the right side showed increased diastolic blood flow signals as compared to the left side (4th registration from top on the left side of the figure), and similarly, the diastolic blood flow signals in the right common carotid artery were also increased (5th registration from top in the middle portion of the figure). Blood flow signals from the subclavian and vertebral arteries were normal. The transcranial Doppler examination showed symmetrical blood flow velocity values in the posterior cerebral arteries and increased values in the right middle cerebral artery (mean value 150 cm/sec.), as compared to the normal values in the left middle cerebral artery (60 cm/sec.). These findings indicate major arteriovenous shunt blood flow volume in the territory of the right middle cerebral artery. A major arteriovenous malformation in the territory of the right middle cerebral artery with major blood supply from the right internal carotid artery was demonstrated by subsequently angiography. AST = a.supratrochlearis, ASO = a.supraorbitalis, С = compression phase, V = velocity (flow) signals, t = time, I = calibrateable frequency (velocity) unit, 1 - 6 = localization of compression points (see Fig 5.1, even numbers = right side, odd numbers = left side).

246

5. Diagnosis and Follow-up with Ultrasound______________References p. 394

Fig 5.3 Pre- and postoperative findings of the extracranial cerebrovascular Doppler examination in a 10 year old boy with bruits over the base of the heart, the neck and over both temporal bones, found at the age of 3 years. The boy's head was enlarged and dilated vessels were present on both sides of the neck. Preoperative findings (upper part of the figure): Blood flow in the supratrochlear arteries (AST, top registrations in the figure) was alternating in direction, i.e. was intra-extracranially in systole and reverse in diastole. No alterations of blood flow signals occurred when the homolateral superficial temporal, facial, or contralateral common carotid arteries were compressed (2, 4, 5, and 1, 3, 6 respectively). A cessation of blood flow in the supratrochlear artery occured when the common carotid artery was compressed digitally at the measurement sites (6 and 5 respectively, 2nd registrations from top of the figure). The averages of blood flow signals of the supratrochlear arteries over 20 cardiac cycles are depicted in the middle top portion of the figure. Blood flow in the supraorbital arteries (ASO, 3rd registrations from top of the figure) also was alternating, and forward flow increased, when the homolateral superficial temporal artery was compressed digitally (2 and 1 respectively). A loud flow inhomogeneity was heard at the level ot the carotid bifurcation, thus individual registrations of blood flow signals from the external and internal carotid arteries were not possible with zero-crossing techniques. The common carotid arteries

showed increased diastolic blood flow on both sides, and quantitative blood flow measurement with a pulsed Doppler ultrasound system demonstrated blood flow values of 500 ml per minute in the right common carotid artery and 900 ml per minute in the ieft common carotid artery (normal values between 300 to 500 ml per minute). Cerebral angiography demonstrated an arteriovenous malformation on the left temporal surface of the brain with major blood supply from the left internal carotid and left vertebral arteries (angiograms on the right top side of the figure). Operation was performed and the arteriovenous malformation was be extirpated in toto. Postoperative findings (lower part of the figure) were normal in supratrochlear, supraorbital, external, internal and common carotid arteries. Quantitative measurements of blood flow showed 300 ml per minute in the right common carotid artery and 420 ml per minute in the left carotid artery (range of normal values and normal left/right difference). (For abbreviations see legends of Figs 5.1 and 5.2.)

Fig 5.4 Findings in a 41 year old female with migraine type headache attacks since the age of 10 years, mostly on the left side. One attack was accompanied by transient paraesthesia and paresis of the right hand lasting 30 minutes. A 2/6 cardiac murmur was present over Erb's point and the aorta and radiated into both carotid arteries. Furthermore, a 2-3/6 systolic-diastolic bruit was auscultated over the left temporal bone. The extracranial Doppler findings demonstrated reverse blood flow in the left supratrochlear artery (AST sin., top registration

in the middle portion of the figure) with a decrease of blood flow signals when the superficial temporal, facial or common carotid artery on the left side were compressed digitally (marked with 1, 3, 5). Increased venous blood flow could be registrated in the middle angle of the orbits on both sides (VST dext. and sin., 3rd registrations from the left top portion of the figure). Venous blood flow decreased on both sides when facial veins were compressed digitally which indicates intra- to extracranial venous blood flow (normally, periorbital veins drain into the cavernous sinus). The left common carotid artery also showed increased diastolic blood fl ow as compared to the right side (4th registration from top in the middle portion of the figure) and major turbulence was heard at the side of the left carotid bifurcation and in the left internal carotid artery (not depicted in the figure). Furthermore, increased blood flow signals could also be registrated from the left vertebral artery (bottom registrations). Quantitative blood flow values in the left common carotid artery were increased twofold (960 ml per minute) as compared to the right side. Angiography demonstrated filling of a huge arteriovenous malformation on the left side of the cortex with major filling from the left internal carotid artery and, to a lesser extent, from the right internal carotid artery, the left external carotid artery and the left vertebral artery. VST = vena supratrochlearis (for other abbreviations see Fig 5.1 and 5.2).

248

5. Diagnosis and Follow-up with Ultrasound

Fig 5.4 demonstrates the findings in a 41-year-old female patient with migranous headaches from the age of ten. The patient presented when one headache was accompanied by transient paresthesia and paresis of the right hand lasting 30 minutes. Reversed blood flow signals in the left supratrochlear artery were found, as well as increased diastolic blood flow in the left common and internal carotid artery. Increased blood flow in the left vertebral artery was recorded, as well as pathologically increased venous blood flow in the periorbital veins on both sides, directed intra- to extracranially. Angiographically a huge supratentorial arteriovenous malformation was demonstrated on the left side with major filling from the left internal carotid artery, and to a lesser extent from the right internal carotid, left external carotid, and left vertebral arteries. The diagnosis of an AVM is usually made by angiography and CT-scanning (Newton et al. 1984, Norman 1984). In the management of a patient with an AVM, angiography is mandatory since all arteries that contribute to the malformation, as well as the draining veins must be delineated in detail. With digital substraction angiography, following intravenous bolus injection of contrast material, an intracranial AVM can be demonstrated, but the resolution of the images is not always sufficient to delineate all important feeding arteries and major draining veins (Newton et al. 1984). CT-scanning can clearly demonstrate an AVM and its associated lesions (focal atrophy, ischemic infarction, bleeding, calcification). Further refinement of diagnosis can be obtained with scans taken after intravenous bolus administration of contrast material. By this means, large vessels running towards, within, and from an AVM, as well as enhancement of the vascular compartments of the AVM and contrast leaks, can be visualized, although not with enough accuracy to dictate appropriate treatment (Norman 1984). Mi-croangiomas or (spontaneously) regressed AVM may only be seen on CT scans. Thus, both angiography and CT-scanning are necessary in the diagnostic work-up of a given patient with a suspected AVM since the two methods are complementary. Results of noninvasive methods, such as Doppler examination, sonic detection, or Xenon inhalation techniques have been described in small groups of patients or in individual case reports of patients with an angiographically proven AVM (Budingen et al. 1982, Diener et al. 1981, Keller 1982, Kosugi et al. 1983, Menon and Weir 1979). Intraoperative Doppler measurements have been performed to quantify altered hemodynamics in vivo within and around an AVM (Nornes et al. 1979, Nornes

References p. 394

1984). In our 44 patients the ratio between supratentorial and infratentorial AVM was in the order of 10:1, as similarly described in large series (Drake 1979). The results of our extracranial cerebrovascular Doppler examination based on continuous-wave equipment confirm those results in the report dealing with noninvasive Doppler diagnosis of AVMs. Our findings yielded a positive diagnostic sensitivity of 92% for supratentorial AVM in the 38 patients with such a lesion. For Doppler diagnosis of a supratentorial AVM, increased blood flow signals obtained from one or several extracranial cerebral arteries (33 of 38 patients), steal from the ophthalmic artery towards the AVM with or without major increases of blood flow in one or both carotid arteries (14 of 38 patients, and 2 of 38 patients respectively), increased blood flow signals in the jugular vein on the side of the AVM (11 patients), and pathological blood flow in the periorbital veins directed from intra- to extracranial (5 of 38 patients) were reliable parameters. The sensitivity of the routine Doppler examination for infratentorial AVMs is lower than for supratentorial AVMs: Only 4 of 6 patients with such a lesion had increased blood flow signals by Doppler in one or both vertebral arteries. All patients with increased blood flow signals in the routine extracranial cerebrovascular Doppler examination in one or both carotid arteries feeding a major supratentorial AVM also had increased quantitative blood flow values obtained with the 14-channel pulsed Doppler device. In those patients in whom surgery or other form of treatment for their supratentorial AVM was performed, normal "direct" and "indirect" blood flow signals were obtained in the post-treatment routine Doppler examination. These results were confirmed by quantitative measurements with the 14-channel pulsed Doppler method. Thus, measurements of quantitative blood flow values in the common carotid arteries are of interest to estimate blood volume shunted through a supratentorial AVM, but are neither necessary for the diagnosis of the presence of an AVM, nor to document the effect of specific treatment on common carotid artery blood flow. Transcranial Doppler examination, as performed in the last 5 patients of our series, was helpful to estimate blood flow velocity in the middle cerebral artery or other larger intracranial feeding arteries to a supratentorial AVM. Increased velocity values could be found in all 5 patients on the side of the AVM. This measurement was not essential to the diagnosis of the malformation and merely represents an additional

References p. 394

interesting feature of blood flow in the vicinity and within a supratentorial AVM. Further experience in patients with an infratentorial AVM in whom measurements of blood flow velocity in the vertebral arteries before its union to the basilar artery, the basilar artery itself, and the posterior cerebral arteries may, however, improve the sensitivity and accuracy of noninvasive diagnosis of these malformations. Noninvasive diagnostic tools based on Doppler ultrasound do not replace CT-scanning or angiography which are still necessary to see parenchymateous changes in detail. Noninvasive examinations, however, are not superfluous, as demonstrated in those 19 patients of our series in whom a supratentorial AVM was correctly diagnosed by these means. The patients presented with "minor" symptoms of the TIA-, RIND-, and little stroke type, or with seizure, headache, or tinnitus synchronous with the pulse. Thus, the noninvasive methods are useful with respect to diagnosis and differential diagnosis in patients with suspected cerebrovascular disease, and as indicators for further diagnostic work-up. The techniques are at present, perhaps, more useful in the follow-up of patients with a known AVM, in whom specific neurosurgical or other treatment is performed, and in those in whom treatment is judged impossible because of the localization or the size of the lesion. In 19 of the 20 patients of our series with a supratentorial AVM who presented initially with pathological Doppler findings, normal Doppler results could be found after treatment (Table 5.5). Thus, immediate postoperative angiography may not be necessary to document the success of treatment (Hassler et al. 1983). Recurrence of a supratentorial AVM was documented by noninvasive means in one patient of our series, in whom the malformation was extirpated 16 years before the second admission and who complained of a tinnitus synchronous with the pulse not present until 6 months before the examination. The diagnosis of a recurrent AVM was subsequently confirmed by CT scans and angiography. Spontaneous regression of an AVM has not been documented in any patient of our series, although, this is known to occur in rare instances (Endo et al. 1979, Hansen and S0gaard 1976, Omojoly et al. 1982, Wakai et al. 1983). Patients presenting with evidence of some form of neurovascular dysfunction will ultimately be seen in either a neurological/surgical or a vascular clinic in which CT scan and/or angiographic facilities are available. It would be useful to effectively screen such patients (for AVM) using a quick, cheap and

Doppler Ultrasound

249

Table 5.5 Results of Doppler examination in 20 patients who underwent specific treatment for their AVM and in whom post-interventional measurements were performed. 17 patients had neurosurgical extirpation of the AVM. 2 patients had embolization, and one patient had x-ray treatment No. of patients with normal findings

pathological findings

Before intervention

1

19

After intervention

20

-

noninvasive investigation such as Doppler ultrasound. However, the diagnostic accuracy, although high in our series of (large) supratentorial AVMs, is not absolute, therefore if there is clinical uncertainty, the CT scan and angiography are still necessary. The initial cost of the ultrasound equipment and the skills necessary for its application and interpretation probably preclude its use in smaller hospitals without full neuroradiological facilities. Nevertheless, the method provides useful (noninvasive) information on the hemodynamics of cerebral AVMs, certainly provides useful follow-up information on treated and untreated patients, and may yet be further refined to provide an accurate screening method to exclude AVM in patients with suspected cerebrovascular disease.

250

6

Neuroradiological Evaluation A. Valavanis

Computed Tomography Computed tomography has become the neuroradiological procedure of choice for the initial evaluation of patients suspected clinically of harbouring a cerebral vascular malformation. Generally, there are three clinical situations in which vascular malformations may be detected by computed tomography. 1. In patients presenting with signs of acute intracranial hemorrhage. In these cases computed tomography is usually performed as an emergency procedure in order to delineate and localize a hematoma, to assess its size and the associated mass effect and to detect an underlying ruptured AVM. 2. In patients presenting with a history of headaches, epileptic seizures, progressive neurologic deficit, stroke or other less common neurological symptoms. 3. Occasionally, a cerebral vascular malformation is detected incidentally on computed tomography in asymptomatic patients, or in patients being examined for other reasons. As a general rule, the definite diagnosis of an AVM by computed tomography depends on the administration of intravenous iodinated contrast material. Therefore, an AVM can only be regarded as excluded if a complete series of a contrastenhanced CT scan is normal. Besides detecting an AVM, CT is also helpful in localizing the lesion topographically and in detecting associated brain parenchyma! changes. For topographic localization reliance upon the usual axial CTsections has proved unsatisfactory. Additional direct coronal scans and sagittal reformations are essential for localization of cortical and subcortical AVMs of the central area, as well as of deeply located AVMs of the basal ganglia, thala-mus and corpus callosum. Furthermore, coronal and sagittal images have the advantage of direct

comparaison with frontal and lateral angiograms. adding precision to the preoperative localization of the lesion (Figs 6.1-6.3). Because of its ability to detect parenchyma! changes, computed tomography is also useful in assessing the state of the brain tissue within and adjacent to the AVM. Changes which may be observed in conjunction

Fig 6.1 A-F These axial (A) and coronal (B) CTs precisely showed the location of an AVM in the right basal medial frontal lobe in a 20 year old female. Note the bifrontal intraventricular hematoma. Postoperative CT (C-D).

References p. 394________________________Computed Tomography

251

fig 6.1 Pre (E) and postoperative (F) right carotid angiograms (frontal views). The postoperative course was uneventful.

Fig 6.2A-D This 20 year old female presented with subarachnoid hemorrhage. A Frontal view of vertebral angiography showed a midline AVM (arrow). B On the lateral view of vertebral angiography the AVM was barely recognized and appeared right paraventricular in

location (.arrow). No draining veins were seen.

252

6. Neuroradiological Evaluation

References p. 394 Fig 6.2C CT with sagittal reformation allowed precise localization of the AVM in the choroid plexus of the IVth ventricle. Succesful removal. The postoperative CT (D) indicated complete removal of the lesion. The patient refused postoperative angiography.

Fig 6.3A-E A 10 year old patient presented with subarachnoid hemorrhage. A On lateral view of vertebral angiography the AVM is seen to be located in the inferior vermis. It is supplied by dilated vermian branches of PICA. В There is late filling of the single draining dilated inferior vermian vein. С Frontal view of vertebral angiography shows a midline AVM of the posterior fossa. D CT depicted the location of the AVM within the inferior vermis and its relation to the IVth ventricle. E CT after succesful removal of the AVM.

References p. 394

with an AVM include: acute and old hemorrhage, areas of recent and chronic infarction, gliosis, dystrophic calcification, edema, local or diffuse atrophy, hydrocephalus, and various causes of mass effect. , The appearance of an AVM on computed tomography depends mainly on the presence or absence of a recent hematoma. AVMs, uncomplicated by recent massive hemorrhage, exhibit a rather characteristic though variabJe appearance on computed tomography. On non-contrast scans they usually appear as mixed-density lesions. The lowdensity areas may be caused by infarction, small old hemorrhagic foci or parenchymal damage due to steal phenomena. The high-density areas may be caused by areas of small, recent hemorrhages, calcifications occurring either within the nidus of the AVM or in the wall of feeding arteries and draining veins or by thrombus formation within venous vascular spaces of the AVM. In some cases of large AVMs the feeding arteries, the dilated veins and even the nidus of the lesion may be seen on non-contrast scans as slightly hyperdense structures. This is due to the significant increase in their blood content. However, in approximately one-third of cases of unruptured AVMs, noncontrast computed tomography will be normal. Detectability of AVMs on non-contrast computed tomography depends mainly on the size of the lesion. Those that remain invisible belong, as a rule, to the group of small lesions. Almost all unruptured AVMs exhibit intense enhancement after intravenous administration of iodinated contrast material which is due primarily to the intravascular accumulation of the contrast material. There is also evidence of additional interstitial accumulation of contrast material within the nidus of the lesion due to a defective bloodbrain barrier at the level of the arteriolo-venular shunts (Norman 1984). The pattern of contrast enhancement of AVMs is more or less characteristic and consists of tubular, serpiginous and round or oval areas of intense enhancement. Frequently it is also possible to localize the nidus and to identify the main feeding arteries as well as the main draining veins. Generally, two types of niduses can be seen on computed tomography. One consists of an area of intense but nonhomogeneous, plexiform enhancement and the other of an enhancing homogeneous compact area. In small AVMs, as well as in large AVMs with a significant A-V-fistulous component, it may be difficult or even impossible to identify a nidus. In these cases, only tortuous, curvilinear enhancing vessels are seen in the region of the AVM.

Computed Tomography

253

As a rule, veins draining the AVM have a larger diameter than feeding arteries. Furthermore, draining veins may exhibit varicose or aneurysma-tic dilatations. Superficial draining veins are located on the surface of the brain immediately beneath the calvarium and appear as round enhancing nodules seen to join the superior sagittal sinus on higher sections. In contrast, superficial arteries leading to the AVM may be followed in the depths of sulci. They have a curvilinear appearance and are usually of a smaller size than the veins. Based on these criteria, it is usually possible to predict, by computed tomography, the main arteries supplying the AVM and the venous system(s) involved in its drainage. If the deep galenic system participates in the drainage of the AVM, then dilated ipsilateral internal cerebral, thalamostriate, other subependymal and/or basal cerebral veins are easily identified. This information is helpful in planning the selective angio-graphic investigation. AVMs draining into the galenic system may also cause obstructive hydrocephalus. In such cases it is usually not the AVM mass itself which causes obstruction of the ventricular system, but rather dilated veins. A dilated thalamostriate vein draining a deeply located AVM may, for example, compress the ipsilateral foramen of Monro and thus produce dilatation of the ipsilateral lateral ventricle. Also, a varicously dilated vein of Galen, draining a so called vein of Galen AVM or a thalamic AVM, typically compresses and obliterates the posterior portion of the third ventricle, resulting in symmetric obstructive hydrocephalus of the third ventricle and both lateral ventricles. Extensive, symmetrical, bilateral calcifications within the subcortical and paraventricular white matter may be observed in some cases of AVM of the vein of Galen. The etiology of such calcifications is not known, but is has been suggested that they represent areas of calcified leucomalacia (Diebler et al. 1981) (Figs 6.4, 6.5).

254

6. Neuroradiological Evaluation

Fig 6.4A-J AVM of the vein of Galen in a 6 year old girl. CT (A-B) showed diffuse bilateral and symmetric calcifications within the periventricular white matter. C-Е CT 2 years later after surgical elimination of the AVM (1981).

References p. 394

References p. 394

Computed Tomography

255

Fig 6.4 Postoperative course was uneventful. Normal physical and mental development up to present time. Preoperative vertebral (FG) and carotid (H) angiography show the mixed, fistulous and plexiform type AVM of the vein of Galen. Note also the dilated tentorial branch of the internal carotid artery contributing to the supply of the AVM (H). The venous phase of vertebral angiography (I-J) shows absence of the straight sinus (?), filling of accessory straight sinus (arrow) as well as of both sigmoid sinuses (J) with redistribution of venous flow. Postoperative angiography was refused by family.

256

6. Neuroradiological Evaluation

References p. 394

Fig 6.5A-J Pre- (A), and postoperative (4 years later) (B-C) CT showed calcifications in the basal ganglia and frontal white matter in a 4 year old boy, who had a plexi-form and fistulous type AVM of vein of Galen. D-G Vertebral angiography showed almost identical finding as in Fig 6.4J. There is absence of the straight sinus and redistribution of venous flow through accessory straight sinus and accessory torcula (arrows). ?-sign means that the straight sinus was angiographically not visualized, which may be stenotic or occluded. Frontal view of vertebral (E), right carotid (F) and left carotid (G) angiography showed the extensive arterial supply to the AVM from both posterior cerebral arteries as well as from perforating posterior communicating and posterior cerebral branches.

References p. 394

Fig 6.5H Postoperative lateral carotid angiography with retrograde filling of the vertebrobasilar system, through the poste^ rior communicating artery. I Postoperative frontal vertebral angiogra^ phy with filling of both middle cerebral arteries through posterior communicating arteries. J Postoperative lateral carotid angiography, venous phase. Note the continued absence of the straight sinus. The postoperative course was uneventful.

Computed Tomography

257

258

6. Neuroradiological Evaluation

AVMs, especially those of the cerebral convexities, have been described as having a typical pyramidal or triangular shape with the base located at the brain surface and the tip at the ventricular wall. Experience with computed tomography has shown, however, that less than 50% of cortical and subcortical AVMs exhibit a classic pyramidal shape. In fact, many of the superficially located AVMs and most of the deep and of the infratentorial AVMs exhibit an irregular, or oval shape on computed tomography. In the pre-computed tomography era, angiographic demonstration of mass effect in association with an AVM was taken to be definite evidence that rupture, with hematoma formation, had occurred within the lesion. Experience with computed tomography has shown that rupture is not a requirement for mass effect and that unruptured cerebral AVMs do cause a mass effect in a significant proportion of cases (Kumar et al. 1985). Local or remote mass effects are evidenced by COT^C&m 01 displacement of the ventricular system, displacement oi the pineal g\and, obliteration of adjacent cortical sulci, distortion of basal cisterns, uncal herniation and erosion of the inner taMe of the skull. Factors contributing to mass effect in AVMs are, in decreasing order of fre-quency: the size of AVMs, the presence of venous sacs or ectatic veins and edema of white matter (Kumar et al. 1985). In rare instances, an unruptured AVM causing mass effect may simulate a neoplasm on computed tomography (Britt et al. 1980). Occasionally, the pattern of contrast enhancement may simulate that of subacute cerebral infarction. Dilated vascular structures adjacent to the area of abnormal enhancement and on the surface of the brain, which represent feeding arteries and/or draining veins, do not occur with infarction or tumor and therefore help to distinguish between the two conditions. In cases of recently ruptured AVM, computed tomography is the neuroradiologic method of choice for establishing the presence of hemorrhage. For identification of hematoma and assessment of its size and location, a non-contrast study is performed first and is usually sufficient. Acute hemorrhage appears as a homogeneous high-density lesion with a small, peripheral, low-density rim representing perifocal edema. Depending on the location of the hematoma and on the clinical condition of the patient, a contrast-enhanced study may then be performed in order to detect the underlying cause of bleeding. However, in patients with massive hemorrhage and poor clinical condition, administration of contrast material

References p. 394

may occasionally cause further clinical deterioration. It is therefore advisable that the neuroradiologist performing the computed tomographic study be fully oriented about the clinical condition of the patient and make the decision to perform a contrast-enhanced scan after consultation with the neurosurgeon. In most cases of ruptured AVM the hematoma is located in the brain parenchyma, but rupture of an AVM may also be associated with subarachnoid or intraventricular hemorrhage. Frequently, an intraparenchymal hematoma may extend into the subarachnoid space or more rarely into the ventricular system. Isolated subarachnoid hemorrhage is rare in cases of AVM. Isolated intraventricular hemorrhage may indicate a corpus cal-losum AVM (Cone et al. 1979). Hematoma in the corpus callosum itself may also occur with an AVM of the corpus callosum but is most likely to arise from rupture of an anterior communicating aneurysm, especially if there is also hemorrhage into the suprasellar cistern (Norman 1984). Occasional^ \t ma\/ "be dffiicuYi \o (Mm^ p^dsdv the location of hematoma. This applies especially for the sylvianinsular and the thalamic areas. A hemorrhage appearing on CT to be intraparenchv-niaj1 mar m?tea<3 i>
394

References p. 394

obliterates the AVM. Furthermore, small AVMs which may be visible when not associated with hematoma may become invisible when located within the high-density, acute hematoma (Norman 1984). The detection rate of AVMs increases steadily with progressive resolution of the hematoma. As the hematoma undergoes resolution it may become isodense, later hypodense and show a ring-shaped pattern of enhancement. This might then be misinterpreted as tumor or abscess (see Fig 6.6A-B). In the early postoperative period, CT may be use-

Magnetic Resonance Imaging (MRI)

259

ful in monitoring complications including hematoma, swelling, hydrocephalus, infarction and later infection. Probably the most important application of computed tomography in the early postoperative period is identification of hemorrhage, which may necessitate emergency craniotomy. Although computed tomography is very sensitive in detecting intraparenchymal hemorrhage, it is not always accurate in assessing the presence of small or medium-sized postoperative epidural and subdur-al hematomas, especially in the posterior fossa.

Magnetic Resonance Imaging (MRI) Magnetic resonance represents the latest develop ment in the field of noninvasive imaging. Unlike CT, it does not require ionizing radiation and is based on the interaction between radiowaves and \VYixc^^dd\u^ <& Ъ strong magnetic field. Advantages of MRI over computed tomography include the absence of bone artifact, superior sensitivity in detecting small lesions and the ability to perform direct sagittal and coronal images without the need to reposition the patient. Furthermore, MRI has the unique ability to noninvasively visualize flowing blood within vessels. Initial experience gained from the application of MRI in the investigation of cerebral vascular malformations indicates that this method is as sensitive as computed tomography when detecting and further characterizing such lesions (Lee et al. 1985). Rapidly flowing blood does not generate an MR-signal. Therefore, the feeding arteries, the nidus and the draining veins of AVMs exhibit a characteristic low-intensity on MRI. The MRmorphology of AVMs is otherwise similar to that displayed by computed tomography. However, delineation of the nidus and assessment of the neural tissue within it, seem to be more accurate with MRI than with computed tomography. Gliotic, old hemorrhagic and ischemic tissue produce a high-signal intensity on MRI and this contrasts dramatically with the low-intensity of nearby vessels. MRI is able to depict such changes, not only in the tissue surrounding the AVM, but also within the nidus itself. The ability to perform direct axial, coronal and sagittal sections without loss of image quality, allows a more precise topographical analysis of the AVM, with

regard to the surface sulci and the deep cerebral structures, than is currently possible when using computed tomography. MRI is also sensitive in detecting acute intracere-

tion of hematomas. It also seems probable that small AVMs associated with hematoma may be detected by MRI more frequently than by CT. Initial experience also indicates that MRI may also be employed for the diagnosis of vascular malformations other than AVMs. Cavernous angiomas, venous angiomas and occult cerebral vascular malformations have already been demonstrated by MRI and appear to exhibit a rather specific morphology such that they can be distinguished from each other. Despite these encouraging initial conclusions, further experience is required before the definite role of MRI in the evaluation of cerebral vascular malformations can be more clearly defined.

260

6. Neuroradiological Evaluation

References p. 394

Cerebral Angiography Despite significant progress in imaging modalities, such as occurred with technical refinements of computed tomography and the introduction of magnetic resonance imaging, cerebral angiography remains the pretherapeutic procedure of choice for detailed angioarchitectural evaluation and precise hemodynamic analysis of cerebral AVMs. Before the advent of computed tomography, the primary scope of cerebral angiography, in patients suspected clinically to harbour an AVM, was to detect the lesion. Today, in most patients coming to angiography, an AVM has been previously demonstrated by computed tomography and/or magnetic resonance imaging. The primary purpose of angiography is, therefore, a precise delineation of the lesion including detailed demonstration of its arterial supply, venous drainage, composition of its nidus and determination of its hemodynamic characteristics.

Technique Cerebral angiography should be performed by a percutaneous, transfemoral approach. This approach has several advantages compared to other angiographic techniques: 1. only one arterial puncture is needed to investigate multiple vessels, 2. the arterial puncture occurs at a site remote from the craniocerebral vessels, reducing the risk of neurological complications, and 3. with this technique, less sedation is required and general anesthesia is only rarely used. For adequate angiographic evaluation of AVMs, rapid serial angiography, with at least 3 films per second as well as the ability to perform magnifications and subtractions are essential. The usefulness of stereoscopic views has been limited by the advent of computed tomography and magnetic resonance imaging. However, stereoscopic angiography is still beneficial in displaying the three-dimensional relationships of vessels composing the AVM. A significant technical improvement in cerebral angiography was the introduction of digital subtraction. Selective intra-arterial digital subtraction angiography is now routinely used in Zurich for investigation of patients with AVM. It provides excellent contrast resolution and requires a smaller amount of contrast medium. Furthermore, the subtracted images are immediately available on the fluoroscopic screen, so that any decisions regarding catheterization of additional

vessels can be made immediately. This reduces the procedure time significantly and therefore contributes to further reduction of the complication rate. Standard frontal and lateral projections are usually sufficient for adequate visualization of an AVM. For identification of perforating feeding: arteries in certain deeply located supratentorum AVMs, however, additional oblique projectionmay be useful. The angiographic appearance of an AVM is quite characteristic and consists of dilated, tortuous arteries, a tangle of abnormal, convoluted vesse.and early appearing, dilated draining veins. The circulation time of the contrast material througr the AVM is usually decreased but is more prolonged in AVMs associated with acute hematoma.. In these cases the AVM, including some of its feeding arteries and/or draining veins, may be compressed by the hematoma. This could result in the erroneous impression that the nidus is smaller or that the feeders are fewer than they actually are.

Erroneous Findings While the majority of cerebral AVMs can be correctly localized by angiography, certain AVMs may pose problems. This applies especially to AVMs located along the tentorial incisura, such as hippocampal or superior cerebellar AVMs (see figures in Vol. Ill B) (Figs 6.6-6.8).

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261

Fig 6.6A-B This 42 year old male with slowly progressive mental deterioration had a differential diagnosis of tumor vs AVM. A A contrast enhanced CT showed a right frontal non-enhancing hyperdense area adjacent to a hypodense lesion exhibiting faint ring enhancement. This appearance suggested intratumoral hemorrhage. В Right carotid angiogram appeared normal. At exploration ahematomaand a small AVM were found and removed. Histological examination verified an AVM.

Fig 6.7A-E A 19 year old student presented with epileptic seizures. A On CT a right frontal hyperdense lesion was seen to display discrete eccentric enhancement. В Postoperative CT. Fig 6.7C, D, E >•

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References p. 394 Fig 6.7C Lateral view of right carotid angiography showed displacement of frontal opercular branches of the middle cerebral artery but no abnormal vascularity. D-E In the venous phase of lateral carotid angiography (D) a pathological dilated parastriate vein could not be easily recognized, whereas in the frontal view (E) this abnormal vein was clearly seen. At surgical exploration a hematoma was found and removed. Histology verified the presence of an AVM.

394

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Erroneous Findings

263

Fig 6.8A-D This 64 year old female presented with epileptic seizures and mental deterioration. A CT showed a left paramedian frontobasal inhomogeneously enhancing lesion with scattered, mostly peripheral, calcifications. В Postoperative CT. C-D Left lateral (C) and frontal (D) preoperative carotid angiograms showed a left frontal space occupying lesion with abnormal vascularity and early draining veins suggesting a highly vascular tumor with a-v shunting (meningioma!). At surgical exploration an AVM was found and removed. Postoperative improvement was gradual.

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6. Neuroradiological Evaluation

Although arteriovenous shunting with early appearance of veins is characteristic of AVMs, it does not occur exclusively with this condition. The angiographic appearance of certain tumors, such as glioblastoma multiforme, angioblastic meningioma, hemangioblastoma and metastases may closely resemble the appearance of an AVM (Fig 6.9). The terminal arteries supplying gliomas and metastases are, however, usually straight and only slightly dilated or may even have a normal caliber, while AVM feeders are typically tortuous and definitely dilated (Goree and Dukes 1963). Most

References p. 394

hemangioblastomas are cystic with a mural nodule of varying size, have a rounded contour and are usually found in the cerebellum. They may occasionally be virtually indistinguishable from an AVM on angiography, particularly when they are large and noncystic and have dilated feeding arteries and rapid arteriovenous shunting. Early appearing veins may also be observed in inflammatory conditions, trauma, encephalopathy, cerebral infarction with luxury perfusion and epilepto-genic foci (Newton et al. 1984). Computed tomography and magnetic resonance imaging will distinguish between most of these lesions.

Fig 6.9A-B A 21 year old female student presented with subarachnoid hemorrhage. A Lateral view of vertebral angiography showed a vascular space occupying lesion in the superior vermis which was supplied by slightly dilated branches of the superior cerebellar artery. Note the early appearing dilated draining ver-mian vein. This angiographic appearance suggested the diagnosis of hemangioblastoma. At surgical exploration an AVM was found, removed and confirmed histologically. В Postoperative vertebral angiography confirmed complete removal of this lesion. The postoperative course was uneventful.

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A small AVM with a varix nodule may even simulate an arterial aneurysm on one angiographic

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projection, while another projection may help to clarify the erroneous situation (Fig 6.10).

Fig6.10A-C

A The frontal view of a right carotid angiogram showed findings resembling an aneurysm (arrow) of the A1 segment of the anterior cerebral artery. There was associated displacement of the pericallosal artery. В Lateral view of carotid angiography showed an entirely different situation with the lesion being more distally located. С In the venous phase a draining vein was seen. On exploration an AVM associated with a large hematoma was found and removed. The postoperative course was uneventful in this 7 year old girl.

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6. Neuroradiological Evaluation

In the frontal projection of vertebral angiography during the arterial phase, one may frequently observe a faint blush or a more or less circumscribed tangle of small vessels appearing above the bifurcation of the basilar artery. This blush is caused by the interpeduncular thalamoperforating branches (Margolis et al. 1974) and should not be

References p. 394

confused with a small midline AVM (Figs 6.11 and 6.12). In cases of totally thrombosed, and therefore angiographically occult AVMs, CT will usually detect a high-density, non-enhancing lesion. In these cases definite diagnosis can only be made at operation (Kramer and Wing 1977). Fig 6 . 1 1 This frontal view from a vertebral angiogram of a patient presenting with subarachnoid hemorrhage showed a vascular tangle located in the midline above the basilar bifurcation (arrow), suggesting a small mesence-phalic AVM. Note the spasm of the right P1 segment of the posterior cerebral artery. The lateral view (not shown) failed to confirm the presence of an AVM.

Fig 6.12A-B Frontal view of vertebral angiography in a 48 year old patient (A) showed an abnormal vascular tangle located above the basilar bifurcation (arrow). It was similar in appearance to that described in Fig 6 . 1 1 . Lateral view (B) of vertebral angiography in this case confirmed the presence of a small AVM. Surgery refused. No follow-up available.

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Angiographic Classification Depending on the origins of arterial supply, Newton and Cronqvist (1969) classified intracranial AVMs into three major types: a. pure pial AVMs, supplied exclusively by cerebral or cerebellar arteries b. mixed pial-dural AVMs, supplied by both cerebral or cerebellar and meningeal arteries and c. pure dural AVMs, supplied exclusively by meningeal arteries. Mixed pial-dural AVMs are intraparenchymal lesions with a dural component. This type includes certain AVMs exhibiting a close topographical relationship to the dural covers, such as hemispheric AVM's reaching the surface of the brain, certain midline AVMs in close relationship to the falx and certain posterior fossa AVMs in close relationship to the undersurface of the tentorium. Demonstration of a dural component requires selective injection into the external carotid arteries. Injection into the common carotid artery and selective injection into only the internal carotid artery are insufficient to demonstrate dural supply to AVMs. In the series reported by Newton and Cronqvist, 73% of supratentorial and 50% of infratentorial lesions were supplied exclusively by pial arteries. The remainder were at least partially supplied (partially dural 5.5%, purely dural 11.5%) by the external carotid artery and by meningeal branches of the internal carotid and

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vertebral arteries. Depending on the location of the AVM as determined by computed tomography, the neuroradiologist may predict a possible participation of dural vessels in the supply of an AVM and thus include injection of the external carotid artery in his angiographic protocol. Meningeal branches of the external carotid artery may occasionally supply normal or functionally ischemic brain parenchyma adjacent to an AVM through transdural anastomoses (Russell and Berenstein 1981, Lasjaunias 1983) (Fig 6.13). In rare instances, a portion of the nidus or some of the feeders of a cortical-pure pial AVM may be supplied by a dural branch of the external carotid artery (Manelfe and Lasjaunias 1985). Therefore, four types of participation of dural arteries in pial AVMs can be differentiated: 1) Supply of a dural component of the AVM, 2) Supply of normal brain adjacent to an AVM, 3) Supply of some pial feeders, 4) Supply of a portion of the nidus of a pial AVM. There is no doubt that if selective external carotid angiography would be performed systematically in each case of cerebral AVM the incidence of participation of dural arteries would be higher than reported in the literature. In our experience dural participation occurs more frequently in cases of temporal, parietooccipital and cerebellar AVMs.

Fig 6.13A-E Right insular opercular AVM. A Right lateral carotid angiogram showed dilated middle cerebral artery branches terminating in the AVM. The anterior cerebral artery was not visualized. В Vertebral angiography showed an additional supply to the AVM by posterior cerebral artery branches.

Fig6.13C-E

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6. Neuroradiological Evaluation

Fig 6.13C This frontal view of a contralateral carotid angiogram showed significant dilatation of the left A1 segment and reduced flow into the left MCA. The AVM is also supplied by leptomeningeal collaterals. D Venous phase of carotid angiography showed a huge single draining vein dividing on the surface into several branches. Absence of the straight sinus. E Selective middle meningeal artery injection. The anterior and posterior branches of the middle meningeal artery are dilated and supply normal middle cerebral artery branches distal to the AVM. The 55 year old mentally changed male refused surgery. He is not working.

References p. 394

Angiographic Investigation Angiographic investigation of AVMs should be complete, however, not every case of AVM needs to be routinely subjected to four-vessel angiogra-phy. Instead, a protocol for injection of different vessels should be developed for each individual case. This should be based on the location and the size of the AVM, as determined by previous computed tomography and/or magnetic resonance imaging. For example, in cases of small AVMs of the frontal lobe and insular area, ipsilateral internal carotid angiography should be performed. Unilateral vertebral angiography should be performed in cases of small or medium-sized occipitopolar and dorsal mesencephalic cases. Bilateral carotid angiography is required in cases of large frontal and anterior callosal AVMs. In cases of AVMs of the occipital, parietal or temporal lobes, ipsilateral internal carotid and vertebral angiography is necessary. A four-vessel angiographic study is essential in AVMs of the vein of Galen (see Vol. Ill B, Figs 4.160-4.173). Angiographically, three types of so-called arteriovenous malformations of the vein of Galen may be distinguished, depending on the pure fistulous or plexiform composition of the nidus: - Pure A-V-fistulous type, - Mixed type, composed of pure A-V fistulae and plexiform nidus, - Plexiform type. The plexiform type nidus may occur within the mesencephalon, the thalamus or the superior portion of the cerebellum. Four-vessel angiograpy should also be performed in cases of AVM of the lentiform nucleus, of the thalamus and of the splenium of the corpus callosum. Bilateral vertebral angiography is necessary in cases of cerebellar AVMs. As mentioned previously, in certain types of AVM additional selective angiography of the external carotid artery is necessary to detect a dural component. Identification of the feeding arteries is not only essential for planning the surgical approach, it is also helpful in accurately localizing the nidus of the AVM with reference to the adjacent surface of the brain and the deep sulci. Feeding arteries may arise from one major cerebral artery or may originate from two or more arteries depending primarily on the vascular territory in which the nidus is located and to some extent on the size of the malformation. The original classification of the 3 major cerebral arteries into 5 segments by Fischer (1938) is pro-

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vided here in a slightly modified manner in order to help the reader to correlate the vascular territory of an AVM with its corresponding arterial feeders, as illustrated in this chapter (Fig 6.14AD) and in further descriptions in this book. The anterior cerebral artery supplies AVMs of the genu and body of corpus callosum as well as AVMs of the medial parasagittal cortex (Fig 6.15 A). The middle cerebral artery participates in the supply of AVMs of the frontal, temporal, parietal and occipital hemispheric convexity as well as of hemispheric subcortical AVMs located within the paraventricular white matter (Fig 6.15B). The posterior cerebral artery supplies exclusively, or participates in, the supply of medial occipital, parietal, temporal AVMs and of AVMs of the thalamus and splenium of corpus callosum (Fig 6.15C). The anterior choroidal artery supplies AVMs located near or in the wall of the temporal horn, in or around the trigone of the lateral ventricle and in the choroid plexus. The perforating branches of the Ml and Al segments of the middle and anterior cerebral arteries supply AVMs of the lenticular nucleus, anterior limb of the internal capsule and head of caudate nucleus. Perforating Ml branches may also participate in the supply of the inferomedial portion of large hemispheric AVMs. The distal pericallosal artery, the posterior choroidal arteries, the thalamoperforating branches, the anterior temporal and anterior choroidal arteries participate in the supply of AVMs of the posterior thalamus, the hippocampus and the inferomedial temporal lobe. The superior cerebellar artery supplies AVMs of the superior and superomedial cerebellar hemisphere. The AICA supplies AVMs of the lateral cerebellar hemisphere and of the cerebellopontine angle. The PICA provides supply to AVMs of the posteromedial cerebellar hemisphere including the inferior vermis and the tonsils (Fig 6.15D). Large cerebellar AVMs are usually supplied by all three major cerebellar arterial systems. Perforating branches of the basilar trunk participate in the supply of AVMs intrinsic to the brain stem. In the present series it was found angiographi-cally, that the anterior cerebral artery was involved in the supply of 178 cases, the middle cerebral artery in 194 cases, the posterior cerebral artery in 196 cases, the anterior choroidal artery in 22 cases.

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6. Neuroradiological Evaluation

In the group of posterior fossa AVMs, the superior cerebellar artery participated in the supply of the lesion in 56 cases, the anterior inferior cerebellar artery in 34 cases and the posterior inferior cerebellar artery in 49 cases. The relatively high incidence of participation of the posterior cerebral artery in the present series as compared to other reports (Newton 1984) is explained by the fact that a proportionately large number of cases with parahippocampal and para-splenial AVMs supplied by posterior cerebral artery branches have been referred for operation. In the present series of AVMs 158 cases were predominantly supplied by one major cerebral artery.

References p. 394

The most frequent combination of two arteries was anterior and middle cerebral arteries in 49 cases, followed by middle and posterior cerebral arteries in 38 cases, other combinations being far less frequent. It must be emphasized, however, that calculation of the percentage of participation of different major cerebral arteries in the supply of AVMs does not provide significant or essential information to the neurosurgeon. Instead, information concerning the topography of distal arteries entering the nidus and the composition of the nidus itself and the proximal venous channels exiting from the nidus should be provided preoperatively.

Fig 6.14A-D Modified drawing of the original schema of Fischer (1938) displaying the segmental classification of the 3 major cerebral arteries.

References p. 394

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271

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6. Neuroradiological Evaluation

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Fig 6.15A-D

A Demonstration of main and accessory blood supply of cerebral and cerebellar AVMs depending on vascular territory 1 Frontoorbital: supplied only by A1-brancnes or 4 Frontoopercular: M 1 - a n d MS-branches, collateral fror A1-branches and Heubner artery or A 1 - and M1-branA3. ches, 5 Frontodorsal pararnedian: A4- and M4-branches. 2 Frontal pol: supplied by A2-branches. 6 Frontoprecentral: A5-, M5- and P5-branches. 3 Frontal deep (head of caudate nc.): Heubner artery and 7 Callosal + cingular: A2- and A3-branches. 1 A1-branches. 8 Splenial and parasplenial: A3- and P5- (posterior ca losal} branches.

References p. 394

B MCA-territory. 1 Frontoorbital lateral: supplied by M 1 - and M2-branches. 2 Frontoopercular: M2- and A3-branches. 3 Insular: M2-branches. 4 Frontodorsal paramedian: M4- and A4-branches. 5. parietal M5 and A5 branches

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6 Parieto-temporo-occipital dorsal: M5-. A5- and PSbranches. 7 Temporal pol: supplied by M1-. M2- and P2-3-branches. 8 Temporal lateral: supplied by M3-. M4- and P4-branches.

9 Temporo-medial-basal(hipocamppy) sapplied by ante-rior choroidal artery, M3, P2-3-branches.

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References p. 394

Fig 6.15C-D

С РСА territory. 1 Temporolateral posterior: supplied by M3- and PSbranches. 2 Temporooccipital: supplied by M3-4 and РЗ-branches. 3 Occipital: supplied by M5-, PS-branches.

4 Occipital-paramedian (parasplenial): supplied by M5-, P5and A5-branches. 5 Occipital-median: supplied by P5- and A5-branches. 6 Vein of Galen AVM: supplied by A5- and P1-. P2-, P4branches (not shown in figure).

7 Parieto-occipito-ternporal (mediobasal parasplenial): supplied by P3- and P4-branches. 8 Thalamic: supplied by P1-, P2-branches. 9 Lentiform nucleus and internal capsula: supplied by anterior choroidal artery, M1- and A1-branches. r 10 Hippocampal, plexus choroideus: supplied by anterio choroidal artery, P2-, РЗ-branches. 11 Mesencephalic: supplied by branches of P1 and superior cerebellar artery.

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D PICA, AICA, SCA territory. 1 Anterior and posterior quadrangular lobuli: supplied by lateral and paramedial branches of superior cere-bellar artery. 1a Superior vermian: supplied by median branches of superior cerebellar artery. 2 Paravermian: SCA- and PICA-branches.

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2a Inferior vermian: SCA- and PICA-branches. 3-4 Semilunar lobuli, paramedian and lateral: SCA-, PICAand AlCA-branches. 5 Biventer-tonsillar: supplied by PICA-branches, also by AlCA-branches. 6 Cerebellopontine: supplied by AICA-, PICA- and SCAbranches.

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Limitations of Conventional Selective Angiography Unfortunately, precise determination of the construction of AVMs is not possible with the current conventional selective angiographic techniques. Advances in interventional neuroradiologic techniques, especially the introduction of calibrat-edleak microballoon catheters, allow superselec-tive catheterization of intracerebral vessels. With this technique, catheterization of cortical branches as well as deep perforating arteries became possi-

References p. 394

ble. Systematic application of this technique in the angiographic investigation of AVMs (mapping or staging angiography) in the near future may enhance our knowledge concerning the angioarchitecture and the hemodynamics of AVMs. Superselective injection of the individual, terminal feeders of the AVM, may identify the compartments composing the nidus of the lesion and any communications between them. This method might also establish which arteries are terminal arteries, ultimately ending in the nidus, and which are transit arteries, either participating or not participating in the supply of the AVM (Fig 6.16).

M,

Fig 6.16 Schematic representation of the composition and supply of a large multicompartmental AVM. Each compartment may, in the future, be angiographically visualized by superselective catheterization of each individual feeding artery. Improved demonstration of each compartment may be achieved by temporarily occluding feeders (black dots) while injecting superselectively into another single feeder.

394

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Limitations of Conventional Selective Angiography

The currently available angiographic techniques permit full assessment of the morphology and, in some cases, of the flow dynamics of simply constructed AVMs. These techniques are, however, rather insufficient in assisting the understanding of the composition and the hemodynamics of complexly constructed AVMs. In such cases, the angiographically demonstrated AVM may only represent the peak of the iceberg with its flow dynamics remaining only partially understood. Often the surgeon has had to confess that the flow dynamics of certain complex AVMs remained poorly understood or were confusing during, and even after their removal. Superselective investigation not infrequently detects unexpected dural feeders of an AVM as well as meningeal collaterals of the normal pial arterial system. Superselective catheterization followed by embolization of some feeding arteries may help to better visualize other potential feeders, but not to understand the flow dynamics of the lesion. After embolization of a feeding artery it may become

Fig 6.17A-C An understanding of the differential hemodynamics of AVMs may only be achieved by Superselective injection of contrast medium into each individual feeder while temporarily occluding all other feeders. Conventional angiography (A), temporary occlusion of a branch (B), temporary occlusion of a and b branches (C) would give precise information of vascular pattern of the AVM.

277

evident that this vessel represented an important artery for the supply of normal brain tissue adjacent to the AVM however, after permanent occlusion, there is no "return". For these reasons the authors followed a critical and restrictive attitude regarding embolization of cerebral AVMs. As long as the dominant feeding artery (a) controls the blood flow to the AVM, there is no possibility of investigating the role of other potential, hitherto hidden or incompletely visualized feeders (b,c or more). Alternating Superselective injection of certain feeders combined with simultaneous temporary occlusion of other feeders (a,b,c, etc.) may provide in the future a full and active angiographic study of AVMs (Figs 6.17-6.20). From this point of view, angiographic evaluation may be subdivided historically into three phases: 1. 1930—1970: passive phase, 2. 1970-1986: partially active phase, 3. Future: fully active phase.

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6. Neuroradiological Evaluation

Fig6.18A-D

A A frontal dorsolateral AVM may be filled from cortical and perforating branches of MCA. Because of the high flow towards the AVM, and also by compression of controlateral carotid artery, the ipsilateral АСА may be poorly filled or not filled at all. В Contralateral carotid angiography shows filling of both ACAs but the right АСА does not participate in the supply of the AVM. This does not prove that there are no feeders arising from the right АСА. Therefore the sign (?) is put. С Contralateral angiography with ipsilateral carotid compression or balloon occlusion may show a clear participation in the supply of the nidus of the dorsolateral AVM. D Contralateral angiography may also reveal an additional nidus in the paramedian area, but not always the entire AVM (therefore ?-sign).

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Limitations of Conventional Selective Angiography

279

Fig 6.19 Both compartments of a bicompartmental temporal AVM will be visualized only if separate and adequate carotid and vertebral angiography is performed.

Fig 6.20A-B A multicompartmental parietooccipital AVM may be supplied from the ipsilateral MCA and PCA. If the ipsi-lateral АСА is not visualized (A), contralateral carotid angiography may demonstrate a further compartment located in the paramedian area (B).

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References p. 3S

Venous Phase It is most important that angiography be carried out well through the venous phase in order to provide adequate assessment of the draining veins and their relationship to the sinuses and of the dural sinuses themselves. The venous drainage seems to depend primarily on the location and the size of the AVM. Most commonly involved is the superficial venous system. Deep venous drainage is observed in approximately 30% of supratentor-ial, mainly deep located AVMs (Newton et al. 1984). An infrequent occurrence is the exclusive participation of the deep venous system in superficially located AVMs (Newton et al. 1984). In 254 cases of this series the final venous drainage was into the superior sagittal sinus, in 64 cases into the inferior sagittal sinus, in 176 cases into the galenic system, in 62 cases into the transverse sinus, in 15 cases into the sigmoid sinus, in 31 cases into the petrosal sinuses, in 33 cases into the sphenoparietal sinus, and in 19 cases into the cavernous sinus. It must, however, be emphasized that these data do not provide essential or practical information. In fact, more attention should be paid to the frequently occurring absence, aplasia and anomalous course of veins and to the associated redistribution and reversal of venous blood flow. Usually, the venous drainage of an AVM reflects the normal regional venous anatomy, with the veins draining into adjacent sinuses or into superficial and deep veins in the area. In some cases, various anomalies of the draining veins and of the dural sinuses are observed. The draining veins may assume an aberrant sometimes bizarre course, or the drainage may occur through persistent embryonic veins such as the marginal sinus or the ventral and diencephalic veins (Vidyasagar 1979). The vein draining a frontal AVM may be seen coursing posteriorly to the transverse or sigmoid sinus and a draining vein from an occipital AVM may course in an anterior direction towards the frontal area. Veins arising from a frontal cortical AVM may drain into the deep venous system and a deeply located AVM may drain outward to the cortex and subsequently to the superior sagittal sinus. Occasionally a cerebral AVM may drain via a dilated superior ophthalmic vein extracranially into the supraorbital, frontal and facial veins. This may cause variable degrees of exophthalmus and dilatation of periorbital veins. Such rare situations have been reported be Cecile et al. (1971) in a case with a frontoparietal AVM, by Huang et al. (1984) in a case with a juxtapineal AVM and by Dobbelaere et al. (1979) who had 4 such cases.

vermis drain primarily towards the vein of Galen.l In AVMs of the lateral cerebellar hemisphere, drainage is into the transverse sinus and into the petrosal venous system. AVMs of the cerebello-, pontine angle and lateral brain stem drain pre-l dominantly into the pontomesencephalic veins.

Associated Aneurysms In approximately 5 to 10% of cases with AVM. angiography reveals the presence of an arterial aneurysm (Hayashi et al. 1981, Ferret and Nishioka 1966, Suzuki and Onuma 19791. Approximately 1-2% of aneurysms detected in patients with AVMs are located on arteries which do not participate in the supply of the lesion (peripherally unrelated, see Chapter 3).

Spasm Spasm of cerebral vessels is rarely observed in cases with recently ruptured AVMs (London and Enzmann 1981). In only one of the 500 cases in the present series was spasm evident on preoperath e angiography (Fig 6.21). While it has been suggested that it is more difficult to detect spasm angiographically in cases with AVMs than in cases with aneurysms, because reduction in the caliber of the dilated feeding arteries may not be apparent (Newton 1984), one would expect to observe vasospasm of the basal arteries of the brain in cases of AVM with severe subarachnoid hemorrhage. However, this is usually not the case and the basal cerebral arteries appear to be normal in cases of severe subarachnoid hemorrhage.

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Venous Phase It is most important that angiography be carried out well through the venous phase in order to provide adequate assessment of the draining veins and their relationship to the sinuses and of the dural sinuses themselves. The venous drainage seems to depend primarily on the location and the size of the AVM. Most commonly involved is the superficial venous system. Deep venous drainage is observed in approximately 30% of supratentor-ial, mainly deep located AVMs (Newton et al. 1984). An infrequent occurrence is the exclusive participation of the deep venous system in superficially located AVMs (Newton et al. 1984). In 254 cases of this series the final venous drainage was into the superior sagittal sinus, in 64 cases into the inferior sagittal sinus, in 176 cases into the galenic system, in 62 cases into the transverse sinus, in 15 cases into the sigmoid sinus, in 31 cases into the petrosal sinuses, in 33 cases into the sphenoparietal sinus, and in 19 cases into the cavernous sinus. It must, however, be emphasized that these data do not provide essential or practical information. In fact, more attention should be paid to the frequently occurring absence, aplasia and anomalous course of veins and to the associated redistribution and reversal of venous blood flow. Usually, the venous drainage of an AVM reflects the normal regional venous anatomy, with the veins draining into adjacent sinuses or into superficial and deep veins in the area. In some cases, various anomalies of the draining veins and of the dural sinuses are observed. The draining veins may assume an aberrant sometimes bizarre course, or the drainage may occur through persistent embryonic veins such as the marginal sinus or the ventral and diencephalic veins (Vidyasagar 1979). The vein draining a frontal AVM may be seen coursing posteriorly to the transverse or sigmoid sinus and a draining vein from an occipital AVM may course in an anterior direction towards the frontal area. Veins arising from a frontal cortical AVM may drain into the deep venous system and a deeply located AVM may drain outward to the cortex and subsequently to the superior sagittal sinus. Occasionally a cerebral AVM may drain via a dilated superior ophthalmic vein extracranially into the supra-orbital, frontal and facial veins. This may cause variable degrees of exophthalmus and dilatation of periorbital veins. Such rare situations have been reported be Cecile et al. (1971) in a case with a frontoparietal AVM, by Huang et al. (1984) in a case with a juxtapineal AVM and by Dobbelaere et al. (1979) who had 4 such cases.

References p. 394

For the anomalies of the great veins and dural sinuses see Chapter: Pathological Considerations, pages 193-194, 224-226). AVMs of the posterior fossa usually have a more variable and complex venous drainage than those which are supratentorial. AVMs of the superior portions of the cerebellar hemispheres and of the vermis drain primarily towards the vein of Galen In AVMs of the lateral cerebellar hemisphere, drainage is into the transverse sinus and into the petrosal venous system. AVMs of the cerebello-pontine angle and lateral brain stem drain predominantly into the pontomesencephalic veins.

Associated Aneurysms In approximately 5 to 10% of cases with AVM. angiography reveals the presence of an arterial aneurysm (Hayashi et al. 1981, Ferret and Nishioka 1966, Suzuki and Onuma 1979). Approximately 12% of aneurysms detected in patients with AVMs are located on arteries which do not participate in the supply of the lesion (peripherally unrelated, see Chapter 3).

Spasm Spasm of cerebral vessels is rarely observed in cases with recently ruptured AVMs (London and Enzmann 1981). In only one of the 500 cases in the present series was spasm evident on preoperative angiography (Fig 6.21). While it has been suggested that it is more difficult to detect spasm angiographically in cases with AVMs than in cases with aneurysms, because reduction in the caliber of the dilated feeding arteries may not be apparent (Newton 1984), one would expect to observe vasospasm of the basal arteries of the brain in cases of AVM with severe subarachnoid hemorrhage. However, this is usually not the case and the basal cerebral arteries appear to be normal in cases of severe subarachnoid hemorrhage.

References p. 394

Spasm

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Fig 6.21A-J An 18 year old girl presented with acute right hemiparesis, hemianopia and aphasia. A CT showed a left capsulothalamic hematoma with intraventricular extension. В After remarkable neurological recovery a repeat contrast-enhanced CT performed 7 months later demonstrated resolution of the hematoma and a walnut sized malformation in the left para-thalamic area. С CT, one week after removal of the AVM shows a small residual hematoma. D Left lateral carotid angiography performed one week after the acute onset of symptoms showed mass effect due to hematoma and partial filling of an AVM in the capsulothalamic area. It is supplied by thalamic branches of the anterior choroidal artery. Note severe segmental spasm of the supraclinoid internal carotid artery (long arrow) as well as of the feeding arteries (short arrow). E Repeat angiography performed 4 weeks later demonstrated disappearance of spasm and complete filling of the malformation. Fig 6.21 F-J

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Fig 6.21F Left frontal carotid angiography showed the course of the dilated anterior choroidal artery, feeders arising from the M1 segment of the middle cerebral artery and the parathalamic-capsular location of the lesion. G Left frontal vertebral angiography shows slightly dilated feeding arteries arising from P3 segment of the posterior cerebral artery.

Fig 6.21H-J Postoperative angiography performed 4 weeks after removal of the AVM showed elimination of the feeders arising from the anterior choroidal artery and posterior cerebral artery (left lateral carotid angiogram [H], left frontal carotid angiogram [I]).

Summary

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283

Fig6.21J Left frontal vertebral angiogram (J). At surgical exploration it was found that the malformation did not have any relation to the choroid plexus and that it was not intraven-tricular but entirely subependymal in location. Postoperative course was uneventful with full recovery from hemipa-resis and aphasia within 6 months. Only quadrantanopia remained.

Summary While it is unlikely that newer diagnostic methods will make angiography obsolete, it is nevertheless important that the angiogram be tailored to answer the questions important to the management of the AVM and not simply to confirm the diagnosis. In this respect it is appropriate for angiography of these lesions to be performed at a facility where neurosurgeons and neuroradiologists work closely together so the proper studies and sequences can be determined in order to maximize the usefulness of the technique. Too often it is necessary to subject the patient to repeat angiography because the initial investigation did not have a clear plan as to what would be needed. When the diagnosis is reasonably clear by CT or MRI transfer to a hospital that has experience in angiography and the evaluation and treatment of these patients is appropriate.

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Supratentorial Sulci and Fissures The cerebral hemispheres are frequently depicted as representing two halves of a sliced apple. They would be better thought of as two halves of an orange which has large segments and multiple smaller facets divided by fibrous tissue. The entire surface of the brain is folded massively (Fig 7.1A—C) and over two thirds of its surface area is located deep within the sulci and fissures. _Many of the sulci are both very long and very deep. The same basic pattern is followed in the cerebellum although the more obvious and exaggerated folding of the cerebral hemispheres often obscures this fact (Fig 7.2A-G). Sulci are formed through folding produced by the differential growth rate of various parts of the embryonic brain (Fig 7.HA). Anatomical texts describe various types of sulci — limiting, axial, operculated, and complete. These major or primary sulci may have smaller sulci arising from them produced by further folding in a different plane.__________________________ A limiting sulcus is one in which distinct functional areas are separated by its floor (for example the central sulcus). An_axial sulcus is a longitudinal fold in a homogeneous area (for example the posterior calcarine sulcus in the striatum of the visual cortex). An operculated sulcus is one which separates distinct functional areas at its entrance but not its floor, often a third functional area presents in the walls of the sulcus without reaching the surface (for example the lunate sulcus, separating at the surface the striate and peristriate areas and containing the parastriate area). The lateral and parietooccipital sulci are termed secondary sulci, being formed as a result of submersion of the insular cortex by adjoining cortical regions and the development of the corpus callosum respectively.

Some sulci (for example the calcarine and collateral sulci) are so deep that they produce corresponding elevations in the walls of the lateral ventricles. These are termed complete sulci.

Fig7.1A-C A Dorsal view of gyri and sulci. (From Ludwig, E.. J. Klingler: Atlas cerebri humani. Karger, Basel 1956.)

Supratentorial Sulci and Fissures

References p. 396

285

В Dorsolateral view of the left hemispheric surface to show the garland shaped gyri. Two thirds of the gyral surface are buried in the depths of the suici and are therefore invisible. С Complexity and richness of the sulcal system of the cerebral hemisphere as seen after removal of the cortex. By courtesy of Prof. S. Kubik, Institute of Anatomy, University Zurich. 1 Central sulcus 2 Precentral sulcus

3 Postcentral sulcus 5 4 Superior frontal sulcus 6

Inferior frontal sulcus Lateral sulcus

7 Superior temporal sulcus 8 Inferior temporal sulcus

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References p. 396

Fig 7.2A-G Horizontal section through both cerebral hemispheres showing the complexity and depth of sulcal system in the central parietal area.

It is not our intention to present a highly detailed account of sulcal anatomy but show the general arrangement of the lobes, gyri, sulci, and fissures and emphasize a few points. One can see from the Fig 7.2A-G just how deeply many of the major sulci run and it is impor-

tant to remember that normal vascular channels follow these sulci in regular (albeit with individual variations) patterns and that AVMs will be found to lie predominantly within the sulci. The individual variation in morphology of even well known primary sulci, such as the calcarine

References p. 396

may be enormous, as has been shown by the work of Prof. Kubik described on p. 350-368. Further studies should be undertaken to detail these anatomical patterns and irregularities. Studying the basal aspects of the cerebral hemispheres (Fig 7.4A-C) one can see the potential

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importance of the olfactory and collateral sulci in the dissection of orbitofrontal and medial basal temporal AVMs. Both these sulci have been rather neglected in anatomical study, yet each has its own structural and vascular relationships, of importance to the surgeon.

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References p. 396

Fig 7.2C Horizontal section at a lower level showing interhemispheric (frontal, parietal, occipital) fissure and indentations of the cingulate sulcus containing arteries.

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289

I

Fig 7.2D Horizontal section at the ventricular level showing suici in the frontal, temporal and occipital lobes, Sylvian fissure and occipital interhemispheric fissure. We would recommend that our younger colleagues consult the atlas of Nieuwenhuys, Voogd and van Huijzen (Das Zentralnervensystem des Menschen, Springer. Berlin 1980) for a detailed description of the basal ganglia.

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Fig 7.2E fissure.

References p. 396

Note complexity of calcarine sulcus and close relationship between the trigone and posterior end of the Sy vian

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291

Fig 7.2F Horizontal section at the level of the optic chiasrn showing the interpeduncular and ambient cisterns with their arteries. The collateral suici are seen (arrows). The central position of the upper cerebellum is also displayed.

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References p. 396

Fig 7.2G Horizontal section at the level of the olfactory sulcus. (These section series were prepared by M. P. Lusk, M. D and T. Orbay. M. D., in the Neurosurgical Department of the University of Zurich.)

References p. 399 Fig7.3A-D Artist's drawing of the deep surfaces of the central sulcus (cent) and the superior temporal sulcus (ts) with its ascending part (ts-asc) seen in a lateral view (A). Note the oblique infolded surfaces. Superior frontal (fs), precentral (prc) and intra-parietal (ip), postcentral (рос) suici (B). (From Szikla, G., G. Bouvier, T. Hori, V. Petrov: Atlas of Vascular Pattern and Stereo-tactic Cortical Localization. Springer, Berlin 1977.)

C-D Deep surface of superior precentral (prc[s]) and inferior precentral (prc[i]( suici (C) frontal view. Deep surface ol central G., G. Bouvier, T. Hori, V. Petrov. Atlas of Vascular Pattern and Stereotactic Corti ca\ LocaU-zation. Springer, Berlin 1977.)

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Fig 7.4A-C

A-B Left olfactory sulcus before and after removal of the olfactory tract. Note looping of arteries into the sulcus (arrows).

Fig 7.4C Anteroposterior extent of the left collateral sulcus, opened by pins from the left temporal pole to the occipital pole with temporooccipital arteries arising from P2 and P3 segments.

References p. 396

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295

Fig 7.5A-D Artistic drawing of the medial frontal, parietal and occipital suici of the right cerebral hemisphere seen from a posterior medial perspective. The horizontal fissures of the left cerebellar hemisphere are also depicted.

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References p. 396

Fig 7.5B-D Clear visualization of the callosal, cingular, parietooccipital and calcarine sulci on MRI sagittal sections. (Courtesy of Th. Naidich, M. D., Chicago, USA.)

Fissures There are three important supratentorial fissures which are detailed in pictorial form in Fig 7.9 (see page 303).

Interhemispheric (Longitudinal) Fissure The longitudinal fissure divides the cerebral hemispheres and extends from frontal to occipital poles in the median plane. It is divided longitudinally by the falx cerebri - a flat structure but one which may contain gaps (windows) of varying size. The falx cerebri frequently fails to reach the cor-

pus callosum and stops short at the sulcus cinguli. This means that the cingulate gyri (or even more superficial structures) may be joined across the midline and the surgeon will then have to exercise care to not damage cortical structures when approching the corpus callosum. The cingulate gyrus is an important structure which is not, as is so frequently depicted in anatomical texts, featureless and homogeneous. It overlaps the lateral aspect of the corpus callosum and both its superior and inferior surfaces contain interdigitations (rather like a comb) in which vessels are organized. These features are now increasingly well demonstrated on CT and MRI scans (Figs 7.5, 7.6A-B, see also Fig 7.2C).

References p. 396

/nterhemispher/c (Longitudinal) Fissure

297

Fig 7.6A-C A The course of АСА and PCA as seen on the medial surface of the cerebral hemisphere and their relation to the sulci. В Note the course of A2 segments and their branches within the callo-sal, cingular (arrow), median frontal and parietal sulci. (Both photos courtesy of Prof. S. Kubik.

Fig7.6C

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References p. 398

Fig 7.6C Complete visualization of cerebral cortical and subcortical arteries. Note the A2 segments and their branches within the cingular sulci. (From Salamon, G.: Atlas of the Arteries of the Human Brain. Sandoz, Paris 1970.)

Sylvian Fissure The anatomical relations of this major fissure (the most posterior ramus of the lateral sulcus) have been well documented, but not always appreciated are the depth, irregularity, and length of the fissure such that it might be better termed a fossa. It is conveniently divided into anterior, middle, and posterior sections corresponding to the major division of the middle cerebral vessels. The vascular relationships in the anterior part have been described in Volume I (Fig 7.7A-C). The fissure contains not only the insula with its short and long gyri but also short and long gyri of the temporal lobe and deep parts of the frontoparieto-opercular gyri. The surgeon must therefore pay attention to the sulci of the frontal and temporal opercular regions within the Sylvian fissure.

The fissure is not a straight anterior to posterior structure, it runs at the surface as a long diagonal line. After opening the superficial membranes, side branches are found on both the temporal and frontal aspects. When dissecting deep in the Sylvian fissure the surgeon should constantly bear in mind the position of the circular and central insular sulci and their vascular relations (Fig 7.7B) and the proximity of the brain stem (see Fig 7.2D—E). Entering the Sylvian fissure to a depth of around 6 cm one is jbutting the brain stem, an important fact to remember as insular AVMs often extend in this direction. In the anterior part of the Sylvian fissure there lies the Ml segment of the MCA with its temporal branches and perforators, and in the middle portion (limen) are the superior and inferior trunks,

References p. 396

both of which may run deeply and be quite tortuous. The real problems in orientation with respect to vascular anatomy occur in the posterior third of the fissure where the candelabra of frontoparietal and temporal branches loop around the opercula. These vessels may be extremely difficult to identify and may be recognized sometimes only by following far more peripheral branches from them to either parietal or temporal regions. Because of this crowding together at the posterior end of the fissure of vessels distributed to disparate regions, far more precise anatomical studies are necessary. Fig 7.7A-C Deepening of the Sylvian fissure from the fetus (A) to the adult (B). Note its anteroposterior extent of the insula (B). The relation of the end of the Sylvian fissure to the trigone (C).

Sylvian Fissure

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References p. 396 Fig7.8A-C

A-B Position of MCA and its branches in the insular fissure. Note particularly their course around Heschl's gyrus. Note the depth of insular sulcus under the frontal opercular region.

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Fig 7.8C Depth of Heschl's gyri (transverse temporal gyrus) which may be 5-6 cm deep.

Transverse Fissure The transverse fissure is well known to every neuroradiologist and neurosurgeon but not, perhaps, under this anatomical term. It is more generally considered as part of the tentorial incisural region. Clear anatomical description of this fissure is also lacking, yet it is of extreme importance as it represents the natural plane of entry to the subsplenial and thalamic areas, the dorsal mesencephalon, ambient cistern, crural cistern, pineal cistern, quadrigeminal cistern, the vein of Galen and the roof of the Illrd ventricle. Dissection in this plane enables the surgeon to recognize many of the major vascular relations of AVMs in these areas (Fig 7.9). The fissure has the same three-dimensional image as is formed by the internal cerebral veins and basilar veins being shaped as two paired semicircles, one pair superior in the vertical plane and the other lateral in the horizontal plane, rather like the antennae and jjincers of a lobstery (Fig 7.9). From the surgeons view, the fissure may be described as originating at the quadrigeminal cistern. The superior median limb of the fissure runs then between the splenium of the corpus callosum infe-

riorly and superiorly the pineal body as the cistern of the velum interpositum. From this cistern a potential space runs forward between the tela choroidea in the roof of the Illrd ventricle, under the fornix and between the superomedial aspects of the thalamus on each side to reach the posterior border of the foramen of Monro. The superior and inferior walls of the space are formed by the two layers of the tela with the upper layer attached to the undersurface of the fornix and hippocampal commissure and the lower abutting the superior medial thalamus and superior surface of the pineal body. This potential channel (velum interpositum) contains the internal cerebral veins as they run posteriorly from their origin near the foramen of Monro to reach the great vein of Galen. The extent of the lateral wings of the transverse fissure may~be best described in terms of the basal cisternal communications in the region of the tentorial incisura (see Vol. I)| The interpeduncular cistern lies between the cerebral peduncles and the dorsum sellae, being separated from the chiasmatic cistern by Liliequist's membrane and communicating laterally with the Sylvian cistern below the anterior perforated substance. Posterolaterally the interpeduncular cistern is extended to form

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the crural cistern between the cerebral peduncle and uncus and this opens further posteriorly into the ambient cistern, bounded medially by the midbrain, above by the pulvinar and laterally by the dentate gyrus and fimbria of the fornix. The ambient cistern continues posteriorly to the quadrigeminal cistern. It also runs below the free edge of the tentorium to the more superior part of the cerebellomesencephalic fissure. We can thus see that starting at the quadrigeminal cistern there is potential space for the surgeon to work anterolaterally and superiorly around^the site of the midbrahiiand of the pons (cerebral peduncle and tegmentum) and medial to the dentate gyrus, parahippocampus, and uncus. The space is bounded inferolaterally by the pulvinar and fimbria hippocampi. The choroid plexus of the temporal horn runs in the choroidal fissure between the fimbria and pulvinar and is also a superior lateral relation to the transverse fissure. The lateral ventricles are superior to the fissure and separated by the thalamus. Just as the superior limb of this transverse fissure contains the internal cerebral veins so the transverse limbs contain the basal veins. Other draining veins in this region are the mesencephalic, pontomesencephalic, hippocampal and uncal veins and cortical veins from the inferomedial aspect of the temporal lobe. The most important arterial structures running in the fissure are the P3 and P4 segments of the posterior cerebral arteries and most posteriorly, branches of the superior cerebellar artery (Fig 7.10A-B). Important branches of these vessels lying in relation to the fissure are the posterior medial and posterior lateral choroidal arteries, hippocampal and posterior temporal arteries, thalamogeniculate arteries and collicular arteries. The superior cerebellar artery ultimately provides hemispheric and vermian branches. The fissure will also contain the IVth and Vth cranial nerves. One can thus see that on reaching this plane apparently inaccessible structures such as the pulvinar take on the characteristics of a juxtamedul-lary structure. As will be described below, AVMs in various parts of this deep mediobasal region may thus be approached from several directions. One may approach from the proximal Sylvian fissure through the amygdala and hippocampus to reach the sulcus choroidalis. A second approach is from a laterotemporobasal direction via the ambient and crural cisterns and then transventric-ularly through the temporal horn. A third median parietooccipital (interhemispher-ic) approach may be made along the precuneus into the trigone and thence through the base of the ventricle.

References p. 396

Two further approaches to this area may be made: parietooccipital interhemispheric, subsplenial and parasplenial and infratentorial-supracerebellar. In these few brief paragraphs and pictures the topographical anatomy of various regions particularly important in AVM surgery has been deliberately oversimplified to try and improve the basic understanding necessary for means of approaching these lesions. More precise details may be obtained from the works of Margolis et al. 1972. 1974, Saeki and Rhoton (1977), Ono et al. (1984). Huang (1965-1984) and Seeger (1978, 1980). Yamamoto and Kageyama (1980). Special surgical considerations, Vol. Ill B, Chapter 4: Deep Central AVMs.

References p. 396

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303

Fig 7.9 Artist's drawing of the perplexing configuration of the transverse fissure (A), Sylvian fissure (B), cerebellar interhemispheric fissure (C) and interhemispheric fissure (D). Note how the subarachnoid space of the Sylvian fissure connects directly to the transverse fissure around the uncus hippocampus, which surrounds the lateral and third ventricles and extends interiorly over dorsal mesencephalon.

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References p. 396 Fig7.10A-B Posterior part of the interhemispheric fissure showing the course of the parietooccipital and calcarine arter-ies within the corresponding sulci. (Courtesy of Prof. S. Kubik.) A P2 and P3 segments are seen in the ambient cistern as well as the inferior temporooccipital arteries, whereas the parietooc-cipital and calcarine arteries are hidden by the sulci. B After separating the sulci the courses of the parietooccipital (Par. occ.) and calcarine (Cal.i arteries are well seen.

Vascular Patterns Relating to Supratentorial Sulci The general relationships of arterial distribution of supratentorial sulci have been elegantly demonstrated by Szikla et al. (1977) and Waddington (1974) who have also linked this relationship to development in terms of infolding of the cerebral cortex. The various patterns of sulcal/arterial relations are illustrated in Fig 7.11. On the whole, definite and more constant arterial patterns are seen in relation to sulci whereas the veins show more constant arrangement in relation to the major fissures of the brain. While a knowledge of the exact topography of vessels within sulci and fissures is important, it is probably better to gain

an understanding of the areas of supply and drainage of these vessels which are very regular, even if the vessels themselves are variable (Waddington 1974). Several arterial patterns are seen; vessels loop deep into sulci without branching, loop in giving vessels to one or both walls of a sulcus or simply dip in the sulcus as end arteries. Such different arterial distributions necessitate careful sulcal dissection even in the treatment of relatively superficial cortical AVMs (Figs 7.12A-B, 7.13A-B, 7.14A-C).

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305

Fig7.11A-B

A Diagram of the embryonic formation of the deep vascular pattern in the central region: arteries cross the suici obliquely, the pressure of neighboring developing areas leads to typical secondary deformations: a retrograde obliquity in depth (postcentral gyrus covers part of the precentral) and the formation of the genu inferior within the originally straight central sulcus, continuing the process of lower frontal infolding.

В

Fig 7 . 1 1 B The angiographic appearance of deep vascular segments results from their position in relation to the direction of the X-ray beam and the orientation of the film. Some typical forms are illustrated on this plate: a Loop of an ascending branch in the inferior frontal (fi) sulcus: lateral, oblique, and a-p projections, b Loop in the posterior intraparietal (ip) sulcus: lateral and ap views. с Terminal loops of arterial branches coming from behind and in front into the upper precentral (prc) sulcus (lateral and a-p). d A branch crossing the central (centfaj) sulcus (lateral and a-p). e A temporal branch coming from the sylvian fissure and crossing the superior temporal (ts) sulcus (lateral, oblique, and a-p projections). f A branch of the anterior cerebral artery coming from the mesial surface, crossing over F1 and entering the superior frontal (fs) sulcus (lateral and a-p projections). g A superficial vein descending into the rolandic region collects smaller branches coming from the central and precentral (cent[v]) sulci. Straight intrasulcal segments bend upon arriving at the surface (lateral and a-p views). (FromSzikla, G., G. Bouvier.T. Hori, V. Petrov: Atlas of Vascular Pattern and Stereotactic Cortical Localization. Springer, Berlin 1977.)

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References p. 396

Fig 7.12A-B Artist's drawing of the anterior cerebral artery and its branches (A2-A5) as seen on angiography (A) and at surgery (B).

References p. 396

Fig7.l2B

Vascular Patterns Relating of Supratentorial Suici

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30&

7. M'lcrosurg'ica) Anatomy of foe Brain

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Fig 7.13A-B Artist's drawing of the middle cerebral artery and its branches (M1-M5) as seen on angiography (A) and at surgery (B). 1 Prefrontal artery 5 Anterior parietal artery 9 Polar temporal artery 2 Frontoopercular artery 6 Posterior parietal artery 10 Anterior temporal artery 3 Precentral artery 7 Angular artery ' 11 Middle temporal artery 4 Central artery 8 Frontoorbital artery 12 Posterior temporal artery 13 Temporooccipital artery

References p. 396

Fig7.13B

Vascular Patterns Relating of Supratentorial Suici

309

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Fig 7.14A-C Artist's drawing of the posterior cerebral artery and its branches (P1-P5) as seen on angiographv (A) and at surgery (B). Posterior interhemispheric approach.

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Fig7.14B

Fig7.14C

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Fig 7.14C Complete visualization of the calcarine arteries within the calcarine sulci. Note the other arteries and their branches, especially the anterior and posterolateral choroidal arteries and their branches. (From Salamon, G.: Atlas of Arteries of the Human Brain. Sandoz, Paris 1970.)

Infratentorial Sulci and Fissures The sulcal pattern of the cerebellum is less immediately obvious than that of the cerebral hemispheres, but none the less is important both in terms of evincing functional subdivision and of directing surgical approach. The pattern of subdivision of cerebellar function, in relation to the chief fissures and lobes can be appreciated by study of a simplified representation of the embryological development of the cerebellum. The morphological and functional subdivisions in the adult cerebellum are diagram-matically represented in ¥ig "7.15. The morphological features of the cerebellar surfaces and fissures most relevant to the surgeon have been accurately and comprehensively described by Matsushima et al. (1982). This article, detailing the microsurgery of the IVth ventricle,

emphasizes the relations also of the superior portion of the roof of the IVth ventricle to the cerebellomesencephalic fissure, the inferior portion of the roof to the cerebellomedullary fissure, and the relation of the lateral recesses of the IVth ventricle to the cerebellopontine fissures. Briefly, the cerebellar surface may be divided, from the surgical point of view, into three parts -the tentorial or most superior surface, the inferior or suboccipital surface and the ventral or petrosal surface. On each of the first two surfaces the ver-mis lies in the midline and the ceiebellar hemispheres laterally on either side, and each surface is divided by a main fissure: the tentorial, petrosal. and suboccipital fissures respectively. The other principle fissures related to the cerebellum are those running between the cerebellum itself and

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313

the brain stem. Since the perforators from SCA, PICA and AICA are arising in those areas, these fissures are of great importance to the ncurosurgeon. On the tentorial surface, we see the simplest pattern of sulci running in more or less symmetrical parallel lines in separating the various folia. The vermis merges smoothly with the hemispheres. The vermis is divided into a central lobule and oilmen, declive, and folium and the hemispheres are divided into quadrangular, simplex and superior semilunar lobules (see Fig 7.15). The single, large fissure in the tentorial aspect is the primary or tentorial fissure separating the quadrangular and simplex lobules and the culmen and declive of the vermis. The SCA runs over this fissure to enter and finally disappear in the great horizontal fissure (see below). The lobular and the fissure pattern in the inferior or suboccipital surface is more simple. The posterior cerebellar incisura containing the falx cere-bclli provides a deep vertical indentation, in front of which lies the vermis. The vermis is separated from the hemispheres by paiaveimicm fissures. The vermis is divided into the upper pyramid and lower uvula. The posterior cerebellar incisura continues interiorly to communicate with the foramen of Magendie between the cerebellar tonsils. The anterior aspect of the tonsils is separated from the medulla by the cerebcllomedullary fissure, their medial aspects face onto the vallecula leading into the IVth ventricle, their ventral aspects face the inferior portion of the roof of the IVth ventricle and their superior parts are separated from the remainder of the cerebellum by the posterior part of the cerebellomedullary fissure. These fissures are closely related to the proximal parts of PICA and Fig 7.15 Diagram showing morphological and functional its perforating branches. The cerebellar anatomy of the cerebellum. hemispheres on this surface comprise the superior Blue: archicerebellum. and inferior semilunar lobules, the biventral Green: paleocerebellum. lobules and the tonsil. The vermis in this region is Yellow: neocerebellum. Williams, P. L, R. Warwick: Functional Neuroanatdivided into the folium, tuber, pyramid and uvula, (From omy of Man. Gray's Anatomy, 35th ed. Williams & Wilkins, from above downwards. The sub-occipital fissure Baltimore. Churchill, Livingstone, Edinburgh 1975). separates the biventral and inferior semilunar A = ala, lobules and the tuber and the pyramid of the vevm\s. Bl = biventral lobule, Ce = central lobule, The most complex fissural pattern is seen in the Cul = culmen, petrosal aspect owing to the tendency of the lobuli to converge in the direction of the foramen of Luschka. Here also, the vermis is not continuous but is divided into superior and inferior parts by the IVth ventricle. Rostral to the TVth ventricle the vermis comprises the lingula, the central lobule and the culmen. Caudally it comprises the nodule and uvula. The hemispheres comprise the ala of the central lobule and the anterior aspects of

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the quadrangular, simplex and biventral together with the superior and inferior semilunar lobules and the tonsils and floccuVi. The horizontal fissure over the brachium pontis divides the petrosal sur-face into superior and inferior components and reaches to the inferior surface between the superior and inferior semilunar lobules. From the point of view of AVM surgery, the most important fissure dividing the cercbellar hemispheres and vermis is the great horizontal fissure. Essentially, this runs in a semicircle on each side from the foramen of Luschka, horizontal to the midline and at the level of the fastigium, dividing both the hemisphere and vermis into superior and inferior portions. The importance of this division is that there is also here a division of the three

Fig 7 .1 6A - D Artist's drawing of PICA seen from a lateral view (A), medial view (B) and dorsal (C). A Lateral view. Cerebellomesencephalic ( 1 ) . cerebellopontine (2), cerebellomedullary (3), and pontomedullary (4) fissures.

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Fig 7.16B Medial view.

Fig 7.16C-D

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Fig 7.16C Dorsal view.

Fig 7.16D Schematic drawing of PICA and its branches. 1 Anterior medial segment and lateral medial segment {caudal loop). (Perforators to posterior lateral medulla, also to dentate nucleus.) 2 Posterior medial segment (superior pole of tonsil). Supratonsillar segment (tonsil and plexus). (From Huang, Y. P., B. S. Wolf: Amer, J. Roentgenol. 107: 543, 1969.)

References p. 397

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Small clusters of vessels run on the walls within the sulci but since no deep loops of the main vessels are to be found witYvm the clefts the removal of surface AVMs of the cerebellar hemispheres is made easier (Figs 7.18, 7.19). The superior cerebellar artery reaches the cerebellomesencephalic fissure in its third part looping deeply into the fissure and giving many branches, which are characteristically also deeply and tightly looped. The anterior inferior cerebellar artery in its third part reaches the cerebellopontine fissure usually as two trunks, a rostral and a caudal. The rostral trunk sends branches to the middle cerebellar peduncle, to the superior aspect of the cerebellopontine fissure and to the petrosal surface of the cerebellum, whereas the caudal trunk supplies the lateral parts of the IVth ventricle. The PICA is the artery of supply to the inferior part of the roof of the IVth ventricle, the inferior cerebellar peduncle and the suboccipital surface of the cerebellum. It is closely applied to cerebellomedullary fissure. It is also related to the fissures between the tonsil, vermis and hemisphere and gives rise to perforating branches to the medulla, tela choroidea and choroid plexus and cortical arteries to the suboccipital surface and to the dentate nucleus.

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References p. 396

Fig7.17A-B

A Artist's drawing of AICA seen from an anterolateral view. В Schematic drawing of AICA and its segments. a Anteropontine segment. b Lateropontine segment. с Flocculopeduncular segment. d Hemispheric segment.

References p. 396

Infratentorial Sulci and Fissures

Fig7.18A-C A Artist's drawing of SCA seen from superior view. B-C Schematic drawing of SCA and its branches. Perforators to 1 Ant. pontomesenc. segment. 3 Cerebell. mesenc. segment, dentate nc., roof nuclei,

2 Lat. pontomesenc. segment. 4 Cortical segments.

middle cerebel. peduncles

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References p.

Fig 7.19 Complete visualization of the SCA and its branches. (From Salamon, G.: Atlas of the Arteries of the Hur Brain. Sandoz, Paris 1970.)

Organization of the Cerebral Microcirculation A thorough working knowledge of the anatomy of the cerebral circulation and of the principal variations and developmental anomalies of the major vessels is of obvious importance to every practising neurosurgeon. Since the early descriptions of Thomas Willis (1664) there have been innumerable studies detailing all aspects of this field using a great variety of techniques. These have ranged from simple visual inspection of the gross cadaveric anatomy to live radiographic examinations, radiographic tissue microscopy, and, most recently, sophisticated examination of minute cerebral vessels using the scanning electron microscope.

Over recent years, some of the most useful detailed demonstrations of regional (and microf surgical) anatomy have been those of Rhoton and his associates and the radiographic studies of Huang, Salamon and Newton and associates. These publications are essential for neuroradio logical and neurosurgical developments. In order to pursue a precise, reasoned and atrau-matic excision of any cerebral AVM, however, one needs also a knowledge of the microvascula-ture of the brain, or at least, of the general patterns which the perforating vessels most commonly adopt on entering the brain substance.

References p. 396

Organization of the Cerebral Microcirculation

Since the pioneerwork of Heubner (1872) and Duret (1874), smaller cerebral vessels and their networks have also been studied by a variety of means including direct light microscopy, radiography, vascular perfusion and tissue staining followed by microdissection or tissue cleaning, and x-ray microscopy. Notable in these areas have been the studies of: Heubner 1872, Duret 1873, 1874, Beevor 1907, Cerletti 1910/11, Stopford 1916, Craigie 1920-1940, Foix and Hillemand 1925a, Bonne 1927, Shellshear 1927, 1933, Pfeifer 1928-1940, Uchimura 1929, Campbell 1938, Wolff 1938, Altschul 1938, Finley 1940, Perria 1941, Kaplan 1953-1966, Vander Eecken 1959, Saunders 1959-1971, Gillilan 1969, 1974, Rowbotham and Little 1963, 1965, Van den Bergh 19591969, Plets 1969, 1970, Lierse 1963, Hager 1963ab, Huang 1964-1984, Majno 1965, Hase-gawa et al. 1967, Hassler 1967, Stephens and Still-well 1969, Duvernoy 1969-1983, Jones 1970, Salamon 1973, Dahl 1973, Fang 1974, Lazorthes 1976. Schlesinger 1976, Hammersen 1977, bang 1977. Bar 1980, Braak 1980, and Briggs et al. 1985. The cerebral angioarchitecture maintains its pattern in all developmental stages of the embryonal brain. The central parts are supplied by the paramedian arteries, the ventrolateral by the short circumflex arteries, and the dorsolateral and dorsal by the long circumflex arteries. Development of the cerebral and cerebellar hemispheres causes a corresponding regrouping and lengthening of the long circumflex arteries, which finally evolve into anterior, middle, and posterior cerebral arteries and into the inferior and superior cerebellar arteries. Diagrammatic illustrations of the distribution of these vessels give only a general outline of the areas supplied by them (Fig 7.20). But the diagrams are useful for general orientation, especially in the presence of collaterals.

Fig 7.20A-E Schematic drawing of the arterial supply of the central nervous system. (From Krayenbuhl, H., M. G. Ya§argil: Cerebral Angiography, 2nd ed. Butterworth, London 1968.) A Spinal cord. В Medulla oblongata.

С Metencephalon.

D Mesencephalon. E Prosencephalon (diencephalon and telencephalon). 1 Distribution area of paramedian arteries (aa. paramedianae) 2 Distribution area of short circumflex arteries (aa. circumflexae brevis). 3 Distribution area of long circumflex arteries (aa. circumflexae longae).

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7. Microsurgical Anatomy of the Brain

Cerebral arteries are located throughout their course partially on the surface of gyri and sulci and/or deep within the sulci. Along their route they give small side branches running at right angles to the sulcus to the banks of the adjacent gyri. Sometimes a vessel will run right over a gyrus to dive into a sulcus on the other side, giving side branches throughout its course. Leptomeningeal arteries are by no means all terminal arteries and many anastomoses exist. Anastomoses occur frequently in the depths of sulci between branches derived from different main cerebral *arteries. The infratentorial leptomeningeal vessels display frequent anastomoses, often between vessels derived from the same main cerebellar vessel. Van den Bergh describes the intracerebral circulation in terms of supply and drainage of a thick walled tube. Perforating branches from the outer coat of leptomeningeal arteries run radially and centripetally toward the ventricular lumen and in turn, some of these vessels have side branches running into the parenchyma. In the cerebrum and cerebellum, a secondary set of vessels of "ventricular" origin complements this system (Fig 7.21A-B). Short cortical arteries run from the pial network to the superficial cortex where they form a palisade and supply the cortical capillary bed (Fig 7.22). They are of varying length and some continue to supply also the middle and deep layers of the cortex and occasionally the superficial white matter. There is no sharp division between the cortical capillary bed and white matter. Long cortical vessels run from the pial network converging radially towards the nearest aspect of the ventricle. They are gently curving vessels (transcerebral arteries; rami medullaris, perforantes, striati) which supply the white matter, thalamus and central grey nuclei. They are usually of larger caliber than the short arteries and terminate in the periventricular vascular plexus. The ventricular arteries, derived predominantly from branches of the anterior choroidal arteries, splay out into the parenchyma to supply the periventricular white matter and paraventricular areas of the grey nuclei. There is no demonstrable anastomosis between these vessels and those perforators derived from the peripheral leptomeningeal arteries (Fig 7.23A-C). In the cerebellum, the same basic pattern of arterial supply persists, taking the IVth ventricle as the center of the radial vascular supply, but the ventricular-derived afferents are relatively more extensive. The peripherally derived vessels supply principally the cortex and superficial white matter.

References p. 399

The centrally derived vessels (from the proximal segments of the major cerebellar arteries) run with the cerebellar peduncles to supply the central grey nuclei (see pages 345-349). Van den Bergh describes a crown of radial arteries in the brain stem which converge toward the aqueduct and IVth ventricle and are divided into an anterior, anterolateral, lateral, and posterior group. The angioarchitecture of brain is perfectly shown in the plate of Salamon (Fig 7.24A-B).

Fig7.21A-B Schematic representation of cerebral circulation (after Van den Bergh, R., H. Vender Eecken). A Classical concept: the brain is encircled by an anasto-motic network which penetrates transcortically in a ventri-culopetal direction. В Concept of Van den Bergh and Vander Eecken: Ventriculofugal arteries meet ventriculopetal arteries at a periventricular demarcation line.

References p. 398

Organization of the Cerebral Microcirculation

Fig7.22A-B A Microangiogram of the middle frontal gyrus showing the vessels of the cortical palisade. The "bush-like" appearance of the cortical veins (C) distinguishes them from the slender short cortical arteries. Several ruptured vessels can be seen. (J.35:M.82 yr). Chromopaque arterial and venous injection. Coronal section. x10. (From Saunders, R. L, W. H. Feindel, V. R. Carvalho: Med. biol. III. 15:235, 1965.)

В Modified scheme from Pfeiffer demonstrating the differ-nt types of cortical and subcortical arteries. ' Cortical artery. 2-4 Medullary arteries. 2 Sickle naped artery. 3 Tap root artery. 4 Scythe shaped artery.

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References p. 398 Fig 7.23A-C A Artist's drawing of cortical-subcortical a-: deep gray matter arteries in frontal view.

B Schematic drawing of a sagittal section through the thalamus, (From Plets, C., J. De Reuck, H. Vander Eecken. R. Van den Bergh: Acta neural, belg. 70; 688, 1970.) 1 Premamillary arteries. 2 Th alamo perforate arteries. 3 Posteromedial choroidal artery. 4 Choroidal arteries. 5 Lateroventral branches of anterior choroidal artery. 6 Thalamogeniculate artery. A Nucleus anterior. B Nucleus posterior. C Pulvinar.

References p. 396

Organization of the Cerebral Microcirculation

Fig 7.23C Perforating arteries to the brain stem and the corpus callosum.

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References p. 398

Fig 7.24A-B

A Perforating arteries of the carotid system in a frontal section through the basal ganglia. B Perforating arteries of the basilar and carotid systems in a lateral view. (From Salamon, G.: Atlas of the Arteries of the Human Brain. Sandoz, Paris 1970.)

References p. 396

The Venous System of the Brain

327

The Venous System of the Brain The venous system of the brain is superbly described in Huang's publications (1964-1985), the deep venous system by Hassler (1966) and the microsurgical aspects displayed by Rhoton and his

associates (1976-1985); the superficial veins by Oka et al. (1985) and the deep venous system by Ono et al. (1984b) (Tables 7.1 and 7.2).

Table 7.1 Outline of the superficial cortical veins (from Oka, K., A. L. Rhoton jr., M. Barry, R. Rodriguez: Neurosurgery 1 7 : 7 1 1 , 1985) Frontal lobe A. Lateral frontal surface 1. Ascending group a. Frontopolar vein b. Anterior frontal vein c. Middle frontal vein d. Posterior frontal vein e. Precentral vein f. Central vein (rolandic vein) 2. Descending group-frontosylvian veins B. Medial frontal surface 1. Ascending group a. Anteromedial frontal vein b. Centromedial frontal vein c. Posteromedial frontal vein d. Paracentral vein 2. Descending group a. Anterior pericallosal vein b. Paraterminal vein c. Anterior cerebral vein C. Inferior frontal surface 1. Anterior group a. Anterior frontoorbital vein b. Frontopolar vein 2. Posterior group a Olfactory vein b. Posterior frontoorbital veins

III. Temporal lobe A. Lateral temporal surface 1. Ascending group-temporosylvian veins 2. Descending group a. Anterior temporal vein b. Middle temporal vein c. Posterior temporal vein B. Inferior temporal surface 1. Lateral group a. Anterior temporobasal vein b. Middle temporobasal vein c. Posterior temporobasal vein 2. Medial group a. Uncal veins b. Anterior hippocampal vein c. Medial temporal veins IV. Occipital lobe

A. Lateral occipital surface-occipital veins B. Medial occipital surface 1. Anterior calcarine vein

2. Posterior calcarine vein C Inferior occipital surface -occipitobasal vein A. Vein of Trolard (superior anastomotic vein) B. Vein of Labbe (inferior anastomotic vein)

Parietal lobe A. Lateral parietal surface 1. Ascending group a. Central vein b. Postcentral vein c. Anterior parietal vein d. Posterior parietal vein 2. Descending group-parietosylvian veins B. Medial parietal surface 1. Ascending group a. Paracentral vein b. Anteromedial parietal vein c. Posteromedial parietal vein 2. Descending group-posterior pericallosal veins

C. Superficial sylvian vein (superficial middle cerebral vein)

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References p. 398

Table 7.2 Deep cerebral veins (from Ono, M., A. L. Rhoton jr., D. Peace, R. J. Rodriguez: Neurosurgery 1 5 : 621, 1984 I. Ventricular veins A. Frontal horn 1. Anterior caudate veins 2. Anterior septal veins B. Body of the lateral ventricle 1. Thalamostriate vein 2. Thalamocaudate vein 3. Posterior caudate veins 4. Posterior septal veins C. Atrium and occipital horn 1. Medial atrial veins 2. Lateral atrial veins D. Temporal horn 1. Inferior ventricular vein 2. Amygdalar vein 3. Transverse hippocampal veins E. Choroidal veins 1. Superior choroidal vein 2. Inferior choroidal vein F. Thalamic veins 1. Deep thalamic veins a) Anterior thalamic vein b) Superior thalamic vein 2. Superficial thalamic veins a) Anterior superficial thalamic veins b) Superior superficial thalamic veins c) Posterior superficial thalamic veins

II. Cisternal veins A. Anterior group 1Л Basal vein (anterior segment) 2. Deep middle cerebral vein 3. Insular veins 4. Anterior cerebral vein 5. Olfactory vein 6. Inferior striate veins 7. Frontoorbital veins 8. Peduncular vein 9. Temporal cortical veins B. Middle group 1. Basal vein (middle segment) 2. Inferior ventricular vein 3. Anterior hippocampal veins 4. Anterior longitudinal hippocampal veins 5. Lateral mesencephalic vein 6. Temporal cortical veins C. Posterior group 1. Great vein 2. Basal vein (posterior segment) 3. Posterior longitudinal hippocampal vein 4. Posterior pericallosal veins 5. Superior vermian vein 6. Tectal veins 7. Epiphyseal veins 8. Temporal and occipital cortical veins D. Thalamic veins (deep) 1. Inferior thalamic veins 2. Posterior thalamic veins

The figures summarize and j^mglify the intracranial veins and sinuses (Figs 7.25-7.28). The venous system reflects the arterial system in general, although medullary veins (those draining the territory supplied by the transcerebral or long perforating arteries) are subdivided into superficial and deep vessels. The superficial veins are short and run out of the cortex in a perpendicular fashion to join the superficial cortical veins. The deep medullary veins are larger and converge upon and join subependymal veins at the corners

of the lateral ventricle. The situation is well demonstrated in the drawing of Huang (Fig 7.26). Veins which drain the central grey matter run either superiorly (superior striate veins) to join subependymal or thalamic veins, inferiorly to join the inferior striate or basal cerebral veins, or posteriorly - usually to the posterior thalamic veins or inferior ventricular vein. The transcerebral and paraventricular veins are superbly demonstrated with the technique of micropaque injection by Saunders (Fig 7.27).

References p. 398 Fig7.25A-B Schematic drawing of the superficial and deep venous systems as seen in lateral (A) and superoposterior (B) views. 1 Superior sagittal sinus. 2 Inferior sagittal sinus. 3 Great cerebral vein (vein of Galen). 4 Straight sinus. 5 Confluence of sinuses (torcular Herophili). 6 Transverse sinus. 7 Sigmoid sinus. 8a Inferior petrosus sinus. 8b Superior petrosus sinus. 9 Cavernous sinus. 10 Frontal ascending veins. 11 Vein of Troland. 12 Vein of Rolando. 13 Parietal and occipital ascending veins. 14a Veins of sylvian fossa. 1 4b Sphenoparietal sinus. 15 Vein of septum pellucidum. 16 Thalamostriate veins. 17 Venous angle. 18 Internal cerebral vein. 19 Basal vein (vein of Rosenthal). 20 Inferior ventricular vein. 21 Posterior pericallosal vein (v. corporis callosi dorsalis). 2 1 a Internal occipital vein.

The Venous System of the Brain

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7. Microsurgical Anatomy of the Brain

References p. 3r:

Fig 7.26 Organization of the veins of the brain. (From Salamon, G., Y. P. Huang: Radiologic Anatomy of the Springer, Berlin 1976.)

References p. 398 Fig 7.27 Microangiogram of the precentral region showing the venous delta formed by the convergence of the transcerebral veins (T) on the paraventricular veins (f) near the outer angle of the lateral ventricle. Note that the former (T) drain the elongated capillary network of the white matter. Superior lenticular veins (L) can be seen entering the v. terminalis. Human brain (J.21:M.76 yr). Coronal section. Micro-paque injection of a segment of the superficial middle cerebral vein. x10. (From Saunders, R. L., W. H. Feindel, V. R. Carvalho: Med. biol. III. 15: 234, 1965; courtesy of Dr. W. Feindel.)

Fig 7.28 Diagrammatic cross section through the brain of a Rhesus monkey showing the connections between the galenic system and the veins on the surface of the brain: 1 Great vein of Galen. 2 Small veins of Galen. 3 Transverse caudate vein. 4 Longitudinal caudate vein. 5 Venous channels connecting the great vein of Galen with the superior longitudinal sinus and the superficial sylvian vein. 6 and 7 Superior external and internal lenticular veins. 8 and 9 Inferior external and internal lenticular veins. 10 Superficial sylvian vein. 11 Deep sylvian vein. 12 Superior sagittal sinus. (From Schlesinger, В.: Brain 62: 274, 1939.)

The Venous System of the Brain

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7. Microsurgical Anatomy of the Brain

The Veins of the Posterior Fossa The veins of the cerebellomesencephalic fissure and superior cerebellar peduncle drain the lateral structures and the superior part of the roof of the IVth ventricle. Those within the cerebellomedullary fissure drain the inferior half of the roof of the

References p. 398

IVth ventricle and the veins of the cerebellopontine fissure drain the region of the middle cere' bellar peduncle, the lateral wall of the IVth ventricle and that part of the cerebellopontine angle around the lateral recess (Fig 7.29). The detailed venous anatomy of this region has been described very completely by Huang and by Rhoton and his coworkers.

Int. cerebral vein Vein of Galen Sup. vermian vein

Precentr. cerebellar vein Straight sinus

References p. 399 продолжение

The Collateral Circulation

333

The Collateral Circulation Thomas Willis (1664) has described the collateral circulation between the carotid and vertebral arteries, which is not infrequently developed in an imperfect manner. When we speak of the collateral circulation of the brain, we are thinking primarily of the circle of Willis and of the meningeal anastomoses (Fig

Fig 7.30 Schematic drawing of "meningeal anastomoses" between the three major cerebral arteries (after Sedlar, in: Tonnis, W., W. Schiefer: Zirkulationsstorungen des Gehirns im Serienangiogramm. Springer, Berlin 1959).

Fig 7.31 Artist's drawing of the collateral system between the three major cerebellar arteries.

7.30). The continuous collateral supply of blood to the supratentorial and brainstem regions is ensured by the annular formation between both carotid and the basilar arteries. The union of both vertebral arteries into a basilar artery ensures a good supply of blood to each side subtentorially (Fig 7.31).

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7. Microsurgical Anatomy of the Brain

References p '-'^

The vascularization of the head and of the brain, however, also shows other complex systems of annular formations fitted one inside the other which intercommunicate at different points. We have schematically assembled these annular formations to aid in the understanding of the physiological and pathophysiological processes (Figs 7.32, 7.33 A-B). The following annular structures can be distinguished: I. Extracranial arterial circle, II. Dural arterial circle, III. Basal cerebral arterial circle of Willis, IV. Cerebral interhemispherical and intrahemisphericaj arterial circle, V. Cerebellar arterial circle, VI. Transcranial arterial circle, VII. Spinal arterial circle, VIII. Vertebrocervical arterial circle, I.. Primitive arterial circle.

I Extracranial Arterial Circle The outermost ring is formed by the external carotid artery, whose branches show many recurrent anastomoses even across the midline (1).

II Dural Arterial Circle Connections of the branches of the middle meningeal artery with the branches of other meningeal vessels and with the branches of the external and internal carotid arteries (2).

Ill Basal Cerebral Arterial Circle of Willis Connections between both internal carotid arteries via the anterior communicating artery (3) and with the basilar artery via the posterior communicating arteries (4).

IV Cortical Interhemispherical and Intrahemispherical Arterial Circle 1) Connections between the frontopolar, callosomarginal and pericallosal arteries and also from them to the different branches of the middle cerebral artery (5). 2) Connections between the branches of the middle cerebral artery with the branches of the posterior cerebral artery (6). 3) Connections of the pericallosal artery with the callosodorsal artery and with the parietooccipital artery (7).

Fig 7.32 Diagram to show the possible collate-;; between the intracranial and extracranial arteries = - : their connection to the spinal medullary arteries - es:e-

cially to the aorta. A = ascending cervical artery, • D = deep cervical artery, • E. occ. = external occipital artery, 1 i = internal thoracic artery, • i. s. = supreme intercostal artery, su = supraclavicular artery, Th = thyreocervical truncus, Tr. c. = transverse colli artery, See further explanation of legend in text pages 334-336. ®See Fig 7.33A-B.

fig 7J

References p. 396

The Collateral Circulation

Tr. c.

Tr. c.

Fig 7.32

335

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7. Microsurgical Anatomy of the Brain

References p. 396

VII Spinal Arterial Circle Connections between the anterior spinal artery and the posterior spinal artery also form a network (18). These also anastomose with the spinal branches of the vertebral artery, which arise caudally from the vertebral artery (19), and with the spinal branches of the aorta (20).

VIM Vertebrocervical Arterial Circle Connections between the muscular branches of the vertebral artery and the muscular branches of the external carotid artery and the branches of the subclavian artery (21).

IX Primitive Arterial Circle (not shown on diagram) Rare anastomoses, which are based on a persistence of the embryonic connections, constitute the rete mirabile in which vessels join the meningeal arteries from the external carotid artery with the leptomeningeal arteries on the surface of the brain (Kraus and Mark 1963). The circulatory rings communicate with one another at different points. 1) The cerebral arterial circle is connected via the ophthalmic artery with the extracranial and dural arterial circle. a) Via the dorsal nasal artery: infraorbital branch from the maxillary artery. b) Via the frontal medial artery: angular branch from the facial artery, medial branch of the frontal branch of the superficial temporal artery. c) Via the frontal lateral artery: lateral branch of the frontal branch of the superficial temporal artery. d) Via the lacrimal artery: meningeal frontal branch of the middle meningeal artery; zygomatic orbital branch from the superficial temporal artery. e) Via the anterior and posterior ethmoidal arteries: pteriopalatinal artery. 2) Connections between the very fine branches of the maxillary artery and internal carotid artery in the petrous bone. a) Carotid tympanic branch with the anterior and inferior tympanic artery. b) Branch of the pterygoid canal. c) Branch of the clivus over the midline. 3) Connection between the vertebral artery and external occipital artery in the sulcus vertebralis atlantis.

Fig 7.33A-B

A Schematic drawing of the arteries of the spinal area (after Krueger). 1 Aorta. 2 Intercostal (or lumbar, or iliolumbar) artery. 3 Ventral branch. 4 Dorsal branch. 5 Muscular branch. 6 Spinomedullary branch. 7 Branch of the posterior canal. 8 Branch of the anterior canal. 9 Anterior radicular artery. 10 Posterior radicular artery. 11 Anterior spinal artery. 12 Posterolateral spinal artery. В Schematic drawing of the arteries of the spinal cord. 1 Anterior spinal artery. 2 Anterior sulcal artery. 3 Sulcocommissural (paracentral) artery. 4 Posterolateral artery. 5 Dorsal fissural and interfunicular arteries.

Pathology of Collateral System

References p. 396

337

Pathology of Collateral System The anomalies, namely hypoplasia and aplasia of vessels, must be considered. Riggs and Griffith (1938) have shown that in a sample of 1647 brains, the circle of Willis is normal in only 18% of cases. In cases with cerebral vascular occlusive disease, other collateral arterial circles (II, III, IV, V, VI, VIII, even VII and IX) are also present and are provided by the inherent dynamic of brain circulation. However, the existence and the quality of collateral circulation cannot be precisely evaluated by conventional angiographic techniques. Neuropathological research shows that children possess many more collateral pathways than adults. With advancing age and the appearance of diseases such as hypertension, atherosclerosis, etc., the number of collateral vessels progressively decreases. The observation that patients with occlusive vascular disease of the brain may have

optimal, and therefore sufficient, extra-intracranial and meningeal collaterals remains unexplained. The mechanism of development and the rate of establishment of certain patterns of collateral flow are poorly understood. In cases with ruptured aneurysms visualization of vessels and collateral channels may be difficult, due to associated spasm and cerebral edema. In contrast, in cases with AVM the collateral pathways through all circles (I-VIII) seem to be wide open, this occurring throughout all age groups. Even the hypoplasias or aplasias known to occur in the circle of Willis are not observed in patients with intracranial AVMs. With the help of modern angiographic techniques, both the intactness and the quality of possible collateral channels in the case of an AVM, can be precisely investigated.

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8

Cortical Blood Vessels of the Human Brain Н. М. Duvernoy

Blood Vessels of the Cerebral Cortex I Pial Vessels The Pial Arterial Network (Fig 8.1) Description Arterioles reaching the cortical surface arise from cerebral arteries in two ways: some arise directly from the principal trunk at the sulcal surface and their entire course is visible, whereas the majority of arterioles reaching the gyral surface have a hidden origin deep within the sulcus. There are, in general, four characteristic branchings of the pial arteries: 1) Frequently a central artery reaches the center of the gyral surface where a shallow depression may be formed. The central artery divides into numerous, highly sinuous branches. Thus, a high density of arterioles and venules is found at the level of this depression. 2) The peripheral arteries covering the rest of the gyrus have an angular course as noted by Wolff (1938), Steegman (1960) and Ruckes (1967). They consist of a succession of straight segments and angles. 3) In rare cases an arteriole arises from the concavity of an arterial trunk and after a short course divides into numerous, often fine branches. These diverge like the bristles of a brush and vascularize the entire surface of a lobule. 4) Another type of cortical arteriole greatly reduced in diameter can be seen with complete injections. These small arterioles may have a long course at the cortical surface; they end in the vascular network of the molecular layer of the cortex. Terminal branches of the arterial network often penetrate the cortex at right angles. In our opinion, except for the small arterioles described

above ending in the molecular or superficial layer of the cortex, the oblique penetration described by certain authors appears to be an exception. Superficial Arterial Anastomoses Numerous arterial anastomoses exist at the cortical surface. There are several inter-anastomosing arterial sources for each gyrus. Two types of anastomoses are found: numerous large diameter anastomoses joining certain arterial branches end to end and extremely small diameter anastomoses joining two adjacent arteries by a straight course. Cortical Artery Diameters Central arteries of the lobule always have a large diameter of 250 |i to 280 ц at their origin. Peripheral arteries have an average diameter of 150 to 180 (x. At the cortical surface, all arterioles of 50 u or less, penetrate the cortex or form anastomoses. The diameter of most of these penetrating arteries is approximately 40 |я. The diameter of the largest anastomoses which join two arterioles end to end varies considerably from 25 to 90 \i. Relationships Between Arteries and Arachnoid As noted by Dahl (1973), the arachnoid observed under the stereoscopic microscope appears to be composed of a homogeneous superficial layer in contact with the dura mater and a deep layer of delicate connective tissue trabeculae which connect the pia mater. The superficial arterioles are firmly attached to these trabeculae which must be cut to free the vessels. Venules underlying the arteries are generally free of arachnoid trabeculae. In contrast to the arterioles, large arterial trunks within the sulcus often appear free with respect to the arachnoid.

References p. 399

Rial Vessels

339

Fig 8.1 Secondary occipital gyrus (SEM) Bar = 800 urn. Male, 54 years. General arrangement of pial arteries and veins. 1 Marginal vein of the gyrus. 2 Large diameter arterial anastomosis. 3 Central vein of the gyrus. 4 Hidden junction of a principal intracortical vein and a pial vein. Note increase in diameter of the pial vein. 5 Peripheral veins. 6 Venous anastomosis.

The Pial Venous Network (Fig 8.1) Description Veins are described from their junction at large cortical venous trunks to their emergence at the cortical surface. In contrast to large cerebral arterial trunks usually found within the sulcus, collecting venous trunks remain at the surface and are visible for their entire course until flowing into the venous sinus. Therefore superficial cortical veins which generally pass over the sulcus, directly join principal collecting trunks without entering the sulcus. In general, the pial venous network is quite dense and composed of veins larger than corresponding arteries (Florey 1925, Hakim and Fisher 1957); the veins have a slightly angular pathway and receive many highly ramified branches along their

entire course like a tree with its trunk and branches. Superficial veins have two main aspects: 1) The cortical venous network may merge into a single trunk at the gyrus center: the central vein of the gyrus. The entire structure has a star-like appearance. 2) Also observed are peripheral veins which are parallel with respect to each other and flow into a marginal collecting vein along the gyral edge. In most cases, both peripheral and central dispositions are present on the same gyrus. According to the aspect of their emergence at the cortical surface, intracortical veins can be divided into large and small diameter veins: Large diameter intracortical veins sometimes flow into the inner surface of a superficial vein. The junction-point, therefore, is often hidden. It is,

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8. Cortical Blood Vessels

however, possible to locate the junction since, at this point, there is a sudden increase in diameter of the superficial vein. Intracortical veins may flow into a superficial vein at its extremity and in this case the emergence is clearly visible. At their emergence, large diameter intracortical veins are few and uniformly distributed. Small diameter intracortical veins, however, are quite numerous. These venules are only visible at the surface following a perfect injection. Often, after a short superficial course, these small veins drain into a large vein at its point of emergence. Venous Anastomoses In most cases the superficial venous network is anastomotic and by their anastomoses the veins form large meshes at the cortical surface; however, certain venous branchings may remain independent of neighbouring systems; in particular, peripheral or parallel veins often visible on elongated gyri may be separated from veins at the opposite side by an avascular zone. Thus, certain lobules are devoid of notable venous anastomoses. Superficial venous anastomoses, then, are fewer than arterial anastomoses. Superficial Cortical Vein Diameters In general, the average diameter of pial veins is larger than that of arteries. Central veins have an average diameter of 280 to 380 ц and peripheral veins average 130 ц; even though few in number, venous anastomoses often have a large diameter which may reach 180 u.._______________ Relationships Between Veins and the Arachnoid There are two types of relationship between superficial cortical veins and the arachnoid: branchings at the cortex surface are found under the arterial network and in close contact with the cortex; there is little contact with the arachnoidal layer. However, in order to join the large collecting trunks, superficial veins separate from the nervous tissue and adhere to the inner surface of the arachnoid; they often have a sinuous pathway as they cross the sulci.

Pial Vessels: Discussion At gyral surfaces the arterial network covers the venous network. Pial cortical veins are characterized by their large diameters and numerous branches; pial cortical arteries are generally small in diameter and form a network characterized by right-angled branches and large meshes. Narrowing of arteriole diameters at their point of origin

References p. 399

on the principal trunk was noted by Florey (1925), Wolff (1938) and Rowbotham and Little (1962). The localized decrease in the arteriole diameter may be due to the presence of muscular sphincters regulating the cortical arterial flow. In contrast to arteries, veins show no change in diameter; however, arterioles crossing over veins compress and form a groove in the venous walls which may slow the blood flow (Fig 8.2). Annular thickenings of the arachnoid forming ring-like structures at the junction of cortical veins and the collecting trunk may also decrease the blood flow. Generally, arteries penetrate and veins emerge from the cortex at right angles. Penetrating arteries are clearly more numerous than veins. Due to the absence of arteriovenous anastomoses and of a capillary network at the cortical surface, blood must flow through the intracortical vascular 1 network before being drained by superficial veins. Relationships Between Arteries and Veins and the Arachnoid It may be important for the neurosurgeon to know the position of superficial cortical vessels in relation to the arachnoid. There are distinctly different positions for arteries and veins. Superficial arterioles are linked to the arachnoid by numerous bridges whereas the venous network situated under the arterial network is relatively free of these bridges; inversely, veins draining the venous network separate from the pia mater and clearly adhere to the arachnoid. This adherence and the fact that any tension applied to the arachnoid may damage their walls makes the dissection of these veins difficult. Satellite veins of the arachnoid cross over the sulci to flow into collecting veins: they are in contact with the cerebrospinal fluid and may participate in its resorption (Takahashi 1968). Satellite veins of the arachnoid appear distended and deformed in the case of cerebral edema; furthermore, in this instance the entire pial arterial and venous networks of the cortex seem equally deformed and have a characteristic irregular appearance. Another pathological aspect sometimes present concerns cortical arterioles which are curled like glomular loop formations, particularly in the occipital lobe.

Intracortical Vessels In the literature, cortical vessels are usually divided into three groups: short, intermediate and long. However, examination of our specimes led

References p. 399

Fig 8.2 Rial vascular network (SEM) Bar = 200 цт. Male, 66 years. 1 Rial marginal vein. Arrows indicate arteries crossing over the vein leaving grooves in the venous wall (x100).

Fig 8.3 Degrees of intracortical blood vessel penetration into the cortex are schematically shown. 1, 2, 3, 4 and 5 represent five groups of intracortical arteries and veins. The disposition of cortical cellular layers is shown on the left from the pial surface inwards. I = molecular layer (outer part la, inner part Ib), II = external granular layer, III = pyramidal layer (outer part Ilia, b, inner part Illc), IV = internal granular layer, V = ganglionic layer (outer part Va, inner part Vb), VI = multiform layer.

Intracortical Vessels

341

342

8. Cortical Blood Vessels

References p. 399

Fig 8.4 Drawing of typical intracortical artery and vein. A4: typical intracortical artery. 1, 2, and 3 Superficial, intermediate, and deep branches. 4 Terminal arterial trunk. The intermediate or recurrent branches (2) give tributaries to superficial cortical layers (these branches may have a sinuous path) (2'), and to middle layers (2"). V4 = typical intracortical vein. ( 1 . 2, and 3) Superficial, intermediate and deep branches. - Superficial branches may flow into the venous trunk at the cortex surface ( 1) or within the molecular layer (V). - Intermediate branches (2) reach the parent vessel at an acute angle. - Deep branches increase in fength in the innermost cortical layers (3, 3', 3"). The disposition of cortical cellular layers (I-IV) is shown on the left.

us to divide the cortical arteries and veins into 5 groups (group 6 consists of large arteries which pass through the cortex without branching and only vascularize the white matter). A schematic representation in Fig 8.3 shows their degree of penetration. Fig 8.4 describes the typical appearance of an artery and a vein; Fig 8.5 indicates the morphological features of each intracortical arterial or venous group of vessels and Fig 8.6 shows the vascular aspect of the cortex. The Vascular Network of the Cortex Is Not Homogeneous in Appearance

There are differences in vascular density in the tangential plane parallel to the surface due to differences in vascular density according to the cellular layers (layers IIIc and TV are the most vascularized). The vascular density is also not homogeneous in the vertical plane perpendicular

to the surface; probably due to physiological and pathological conditions. It is possible to find vertically congested bands of the capillary network. The nonhomogeneous aspect of the capillary network may also be explained by the presence of a capillary-free space surrounding each artery and vein. This capillary-free space was described by Pfeifer in 1930 (Zirkumvasaler kapillarfreier Raum) and later cited by Lierse (1963) and Saunders and Bell (1971). It is a circular zone of nervous tissue devoid of capillaries around each artery and vein. However, this space, which we recommend be called the Pfeifer space, is more pronounced around arteries than veins. The diameter of the Pfeifer space varies according to the vessel diameter and is greatest around large arteries (A6 and A5). Our observations show it may reach a diameter of 225 u, for an artery of 75 (A, and 170 [A for an artery of 40 (Я.

References p. 399

Intracortical Vessels

343

Fig 8.5 This drawing indicates the morphological features of intracortical arteries and veins. Arteries are divided into 6 groups, (A1-A6) and veins into 5, (V1 -V5). V5 = principal intracortical vein. V4 which is described in Fig 8.4, is not shown on the drawing. Black circles indicate the site of probable precapillary arteriovenous anastomosis. I, II, III, IV, V, VI = cortical cellular layers. SC = subcortical white matter. Note vascular deformities of an artery (A5) whose branches in the cortex coil like a rope (Fig 8.7). Moreover, this artery presents a sinuous appearance (glomerular loop formation) in the subcortical region. These vascular features seem to be due to aging.

Fig 8.6 Temporal pole (SEM). Bar - 500 urn. Male, 66 years. General view of the cortical vessels. 1 Cortical arteries. 2 Cortical vein. 3 Medullary artery (type A6}.

4 Subcortical white matter.

344

8. Cortical Blood Vessels

References p. Fig 8.7 Temporal po'e (SEM). Bar = 50 цт. Mae. 66 years. Coiling of recj-rent branches arounc ~« arterial trunk (1).

Pfeifer space composed of nervous tissue should not be confused with classic perivascular space which surrounds cortical vessels and forms leptomeningeal expansions within the cortex. Anastomoses of Cortical Vessels and Intracortical Shunts Conheim's (1872) classic conception of totally independent intracortical arteries (end arteries) had been accepted without reservation for many years; however, more and more researchers believe the theory of end arteries is too restrictive. There may be several types of anastomoses among f different parts of the cortical vascular bed: capillary, arterial, venous and arteriovenous anastomoses. Capillary Anastomoses Since the work of Wislocki and Campbell (1937), followed by the observations of Scharrer (1940), Craigie (1945) and Lewis (1957), the vascular network of nervous tissue is divided into two types: a continuous and anastomosed capillary network in most mammals (network type) and a particular vascular structure composed of capillary loops uniting arteries and veins which form independent units (loop type).

References p. 399 Arteriovenous Anastomoses and Intracortical Shunts It must be noted at this point that large arteriovenous anastomoses joining an intracortical arterial trunk to an adjacent vein have only rarely been found in the cortex (Ravens 1974). Our observations concerning vascular anastomoses, in general, have the following results and we insist, as Saunders and Bell (1971), on the difficulty in proving the existence of an anastomosis: numerous false interpretations are due to the superimposition of vessels and can only be avoided by a detailed examination of thick sections (500 [i) cleared by Spalteholz solution; with this method, the vascular bed is completely visible.

Blood Vessels of the Cerebellar Cortex

345

In our preparations, no large diameter arterial or venous anastomoses were discovered. Therefore, the only possible anastomoses are at the precapillary level (Fig 8.5). In this case, it is difficult to distinguish a precapillary anastomosis from a simple cortical capillary since they are only slightly different in diameter: the capillary diameter may reach 6 (A and the preferential channel is about 8 |.i. Only a study of the vessel walls will distinguish between capillary and preferential channel. Many aspects of the vascularization of the cerebral cortex remain obscure. The reader is recommended to study some approaches to them which have recently been published by Duvernoy et al. (1981).

Blood Vessels of the Cerebellar Cortex The vascularization of the cerebellar cortex has not inspired much recent research. The characteristics of these blood vessels, however, and their relationship to the Purkinje cells present several interesting features already demonstrated decades ago, by the works of Conighi (1922), Perria (1941), Fazzari (1924) and Uchimura (1929), and described in a recent paper by Duvernoy et al. (1983).

I Pial Vessels The pial vessels may be divided into two groups: those situated at the cerebellar surface and those located within the sulci. Due to the considerable folding of the cortex, the majority of pial vessels are situated within the sulci. Pial Vessels on the Cerebellar Surface The anatomy of the cerebellar arteries and veins is well established (Lazorthes et al. 1976). The fine pial network at the cerebellar surface, however, is rarely described. The superficial pial vessels are relatively few in number and arranged perpendicularly to the axis of the folia. The superficial pial arteries have an irregular course and give off two types of branches: large diameter branches (200 \a on the average) which penetrate the sulci (the diameter of these branches depends upon the depth of the sulci) and branches much smaller in diameter (8 to 20 u.) which remain at the cerebellar surface. The superficial pial veins run a course just as irregular as that of the superficial arteries. They

f

receive two types of branches: large diameter branches (200 n on the average) which drain the pial network situated within the sulci and branches of smaller diameter. These small diameter veins (50 to 140 \i), sligthly larger in diameter than the corresponding arteries, often emerge at the center of the folia in more or less regular order (Fig 8.8). In certain cases these superficial veins, which run parallel to each other, flow into a collecting vein which overlies the sulcus (superficial venous arch, Fig 8.8). The relationship between pial arteries and veins on the cerebellar surface is similar to that of the cerebral cortex and of the brainstem: the large collecting veins often cross over the corresponding arteries whereas, for the finer network, the veins lie deep to the arteries. Deep Pial Vessels Deep pial vessels form considerably dense vascular laminae which are situated in the sulci separating the folia. The dense vascular laminae (principal laminae) give offshoots (secondary laminae) which penetrate the secondary furrows situated on the lateral side of the folium. To simplify the description, only the arteries and the veins of the secondary laminae will be studied. The deep pial arteries often run a rectilinear course towards the bottom of the furrow and each principal arterial trunk gives off parallel secondary branches. These secondary branches penetrate the cortex in one or two ways: some bend at right angles and enter the cortex; others, continuing

346

8. Cortical Blood Vessels

their rectilinear course, arrive at the bottom of the furrow where they divide into numerous small branches upon entering the cortex. In elderly persons, on the contrary, the pial arteries trace a sinuous course; their secondary branches stem from irregular dilatations of the main trunk; before entering the cortex these arteries present either a simple loop or several loops in rapid succession giving a corkscrew appearance. The deep pial veins have a characteristic appearance: a venous arch (from 100 to 170 ц in diameter) is situated at the beginning of each secondary fold of the folium and is drained by voluminous

References p. 399

veins (200 \i or more) situated in the sulci. Еасh arch collects the blood from the secondary vascular lamina. The veins of the secondary vascular lamina are generally larger than the corresponding arteries. They originate at the bottom of the furrow receiving, as they progress, numerous srn.il parallel branches (of an average diameter of 10) from the nervous tissue. The arteries and veins, which run parallel to each other, are often grouped in bundle-like formations having a voluminous pial vein in the center surrounded by several arteries. Fig 8.8 Diagram depicting aspects of pial vessels on the cerebellar surface The superficial pial arteries give off two types of branches: 1 Large diameter branches penetrating the sulci. 2 Small diameter branches penetrating the cortical surface. 3 Pial veins emerging from the cerebellar surface at the center of the folia. 4 Superficial venous arch. Black circles indicate the site of arterial or venous anastomoses.

References p. 399 Concluding Remarks Concerning the Anatomy of Rial Vessels At the surface of the cerebellum the pial vessels are extremely rare. Within the sulci, and the secondary furrows, however, the complexity of the pial vascular network is by far superior to that of the cerebral cortex; this may be due to the fact that within the furrows each vascular lamina vascularizes two adjacent cortical layers.

Blood Vessels of the Cerebellar Cortex

347

2 3,

II Intracortical Vessels Fig 8.9 and 8.10 show the general organization of intracortical cerebellar arteries and veins which will be studied in comparison with that of the cerebral cortex. The short arteries and veins (Al and VI) which reach the external granular layer of the cerebral cortex are absent in the cerebellar cortex which is devoid of this external layer. Note the special aspect of middle arteries (A3) whose branches run parallel to the cerebellar surface in the Purkinje cell layer (parallel arteries). Three Vascular Layers are Present within the Cerebellar Cortex: Superficial, Middle and Deep (Fig 8.10) — The superficial intracortical vascular layer which coincides with almost all the molecular layer is about 280 [i in size. A marginal zone about 80 fi in thickness, entirely devoid of capillaries, separates the superficial layer from the cortical surface (a marginal zone of this type is equally encountered in the cerebral cortex). The superficial vascular layer is composed of a loose network formed by the ramifications of short arteries (A2), recurrent branches of parallel arteries - short veins (V2) and capillaries. — The middle intracortical vascular layer is centered by the band of the Purkinje cells. Its average thickness is about 90 \i. Its vascular organization is completely different from that of adjacent layers because its vascular components are arranged parallel to the surface. These components mainly include the parallel arteries which are terminal branches of middle arteries (A3) and collateral branches of deep arteries (A4 and A5). The parallel arteries are in close contact with the Purkinje cells; due to the paucity of capillaries in the middle vascular layer it seems that the parallel arteries vascularize the Purkinje cell bodies in the human. — The deep intracortical vascular layer, situated within the granular layer, is conjointly vascularized by the branches of the parallel arteries and

Fig 8.9 Diagram showing the different types of cerebellar intracortical vessels in comparison with those of the cerebral cortex. 2, 3, 4, 5 Four types of cortical cerebellar arteries and veins. 1 Arteries and veins of type 1, present in the cerebral cortex, are absent in the cerebellar cortex. I = molecular layer, II = Purkinje cell layer, III = granular layer, SC = subcortical white matter.

the long arteries (A4 and A5); it is the most vascularized layer. Cortical Cerebellar Blood Flow According to Conighi (1922), blood circulates within the cerebellar cortex in only one direction: superficial arterial supply and deep venous return. Our observations, however, based on the anatomy of intracortical arteries and veins, suggest the existence of two major types of circulation within the cerebellar cortex (Fig 8.11): — The deep circulation concerns the granular layer. Ramifications of parallel arteries provide the main arterial supply and the branches of long veins (V5) constitute the principal mode of venous return; the direction of the blood flow is thus orientated towards the deepest regions of the cortex. — The superficial circulation concerns the molecular layer and is orientated, on the contrary, towards the cortical surface. The main arterial supply is provided by the recurrent branches of the parallel arteries and numerous V2 venules are responsible for the venous return.

348

8. Cortical Blood Vessels

References p.

Fig 8 . 1 0 Diagram illustrating the anatomy of intracortical cerebellar arteries and veins (A2 to A6 and V2 to V5). a Parallel arteries (parallel to cerebellar surface), branches of middle cerebellar arteries (A3). b Branches of parallel arteries reaching the granular layer. с Secondary arterial network. d Branches of parallel arteries reaching the molecular layer (recurrent branches). The left-hand column indicates the three vascular layers ( 1 , 2, 3). The right-hand column indicates the molecular (I). Purkinje cell (II) and granular (III) layers. SC = subcortical white matter, m = Marginal zone. Black circles indicate the site of probable arterial and arteriovenous anastomoses.

References p. 399 продолжение

Blood Vessels of the Cerebellar Cortex

349

Fig 8.11 Diagram showing the principal aspects of the cerebellar cortical blood flow. A Superficial circulation: main arterial supply by recurrent branches of parallel arteries (p) and venous drainage by short V2 veins. B Deep circulation: main arterial supply by branches of parallel arteries (p) and drainage by a long V5 principal vein. 1, 2, 3 Superficial, middle and deep cerebellar vascular layers. SC = subcortical white matter, m: marginal zone.

There are only a few arterial and venous anastomoses in the fine pial network (Fig 8.8). In the cerebellar cortex arterial, venous or arteriovenous anastomoses of large diameter vessels are absent, as is the case within the cerebral cortex. The question of precapillary anastomoses is very difficult to resolve. This difficulty stems from the fact that no differentiating characteristic feature permits one to distinguish between true capillaries and precapillary arteriole or postcapillary venule. Nevertheless, there seems to exist precapillary anastomoses within the molecular layer (Fig 8.10). These anastomoses probably correspond to the "preferential channels" referred to by Chambers and Zweifach (1944) concerning structures outside the brain. It seems that the arterial pathology of the cerebellar cortex concerns essentially parallel arteries,

since other cortical arteries present little or no abnormalities. It is exceptional, for example, to encounter arterial coiling or glomerular loop-formation as is the case in the cerebral cortex. The absence of these alterations may be explained by the fact that the cerebellar cortex does not atrophy during the process of aging (Hassler 1965, Naritomi et al. 1979, Ravens 1978). In conclusion, we note that the vascularization of the cerebellar cortex closely resembles that of the cerebral cortex. The vascularization of the former is much easier to understand due to the relative simplicity of its cellular structure. The special relationships between Purkinje cells and parallel arteries may be used as a model in the study of exchanges between nervous tissue and blood vessels.

350

9

Anatomy of the Calcarine Sulcus S. Kubik and B. Szarvas

The calcarine sulcus is easily recognized as being a primary fissure appearing early in embryological development. It lies close to the border of the medial and basal aspects of the cerebral hemispheres and forms a horizontal Y with the parie-_ tooccipital sulcus, the common trunk of which forms the stalk of the fissure. Between the two branches of the Y lies the cuneus. The apex of the cuneus marks the meeting point of the sulcus calcarinus and the sulcus parietooccipitalis (Fig 9.1A). The literature regarding detailed description and nomenclature is very heterogenous. Beninghoff and Goertler (1979), Braus (1932), Clara (1953), Forssmann and Heym (1982), Krieg (1949), Rauber and Kopsch (1943) and Spalteholz (1922)

mention only the names of the sulcus and its junction with the parietooccipital sulcus. Crosby et al. (1962), Lenhossek (1924), Paturet (1964) and Testut (1929) describe the shape and the parts; Lang (1979) and Donges (1983) provide the measurements of depth and length, Smith and Richardson (1966) and Jensen (1926) give only the depth. Detailed information regarding shape, variations of the terminal portion and inner structure, supplemented by references to comparative anatomy may be found in the papers by Broca (1888), Cunningham, Elliot-Smith (1903, 1904), Giacomini (1884), von Hallerstein (1934), Kuhlenbeck (1928), von Monakow (1892), Filimonoff (1932) and Zuckerkandl (1906).

Fig9.1A-E

A Parts of the calcarine sulcus. Calcarine sulcus. a) Anterior part. b) Posterior part. 2 Cuneus. 3 Apex of cuneus. 4 Parietooccipital sulcus.

B-E Various positions of the junction point of the parietooccipital sulcus and the calcarine sulcus. 5 Cingulate gyrus. 6 Isthmus of the fornicate gyrus with the infundibulum of the calcarine sulcus. Dotted: upper calcarine lip. Grey: lower calcarine lip.

References p. 400

Nomenclature of the Various Parts

351

Development According to Clara (1953) the calcarine sulcus appears in the 5th to the 6th month of fetal development, but according to Braus (1932) in the 6th to the 7th month and to Corning (1925) in the 7th to 8th month. Cunningham (1892) states that three successive linearly disposed parts of the fissure appear. The stalk of the fissure develops first, followed by the middle, and then the posterior part. The middle section fuses with the stalk in the 7th fetal month and with the posterior portion in the 8th to the 9th month. The various parts of the fissure are interrupted by vertically directed so-

called cuneolingual transitional convolutions (gyrus cuneolingualis anterior, posterior). The deepening of the main fissure, causes the transitional convolutions to sink more and more deeply. i. e. they are operculated. If one of the transitional convolutions remains superficial, as is usually the case in the posterior convolution, the sulcus calcarinus is divided into two parts, namely the stem or trunk and the so-called forking branches. These branches which are separated from the main fissure may form a sulcus calcarinus externus or a sulcus extremus.

Nomenclature of the Various Parts of the Calcarine Sulcus Most authors consider the calcarine sulcus as a uniform structure which runs from the occipital pole towards the isthmus gyri fornicati and unites with the sulcus parietooccipitalis at the apex cunei. Jensen (1926) designated the sulcus calcarinus as being the fissura horizontalis and the sulcus parietooccipitalis as the fissura perpendicularis. The anterior part of the sulcus which is united with the sulcus parietooccipitalis has been named by Cunningham (1892) as the stem of the fissure, by Tandler (1929) as the truncus communis and by Lenhossek (1924) as the truncus fissurae calcarini. Zuckerkandl (1906) considered the whole sulcus to be the stem and described the end-branches as the "forking branches" (the sulcus extremus of Schwalbe [1881]). Broca (1888), Crosby et al. (1962), Paturet (1964) and Testut (1929) divide the sulcus calcarinus into a pars anterior and a pars posterior. Paturet calls the anterior section the pars precuneata and the posterior section the pars infracuneata. Cunningham (1892), ElliotSmith (1903, 1904) and Kuhlenbeck (1928) separate three parts of the sulcus. Cunningham calls them the fissura calcarina anterior, posterior and externa, Kuhlenbeck names them the pars anterior, intermedia and posterior. Elliot-Smith uses different synonyms for each section. The first section he designates the sulcus calcarinus proprius or sulcus jjrestriatus, the second the sulcus calcarinus posterior or sulcus retrocalcarinus or sometimes the sulcus intrastriatus medius and the third part the sulcus calcarinus externus, sulcus occipitalis latcralis or sulcus intrastriatus lateralis.

We differentiate two parts in the sulcus calcarinus: a pars anterior and a pars posterior. The border of the two parts can be defined by the meeting point of the sulcus calcarinus and the sulcus parietooccipitalis (junctio calcarino-parietooccipitalis) or by the apex cunei (Fig 9.1A). Paturet described the pars posterior as ascending, the pars anterior as descending and compared the shape of the fissure to an "accent circonflexe". Testut gives a similar description of the position of the two parts and calls the bending point "coude de la calcarine". We name it the knee of the calcarine sulcus (genu sulci calcarini) and maintain that it lies only in the junctio calcarino-parietooccipitalis when the pars posterior runs in a straight line (23%) (Fig 9.2, 136). If the pars posterior makes a curved, inverted V or Sshaped configuration (76%). the first section forms the extension of the pars anterior. Consequently, the genu does not lie at the border of the two sections, i.e. at the junction point with the sulcus parietooccipitalis, but in the region of the pars posterior (Fig 9.2. 128. 112). For this reason we defined the border between the two sections by means of the apex cunei but not the genu.

352

9. Anatomy of the Calcarine Sulcus

References p. 400

The Location of the Meeting Point The location of the meeting point of the sulcus calcarinus and the sulcus parietooccipitalis is almost symmetrical on both sides. It is about 2 cm from the splenium of the corpus callosum and lies above the lower rim of the splenium in 40% of cases, above the upper border of the splenium in 29%, in between in 22%, below the splenium in 6% and completely above it in 3% (Fig 9.1B-E). From the literature it would appear that nearly all

Anatomical Variations of the Pars Posterior The pars posterior of the calcarine sulcus runs somewhat above the border between the medial and basal surfaces of the hemispheres from the apex cunei towards the occipital pole. It represents the border between the cuneus and the gyrus lingualis. Its upper contour-line is formed by the lower margin of the cuneus and the lower one by the upper margin of the gyrus lingualis. Both the border zones are called the lips of the calcarine fissure by Crosby et al. (1962) and by Benninghoff and Goertler (1979) (Fig 9.1A). Braus (1932) calls them the gyrus calcarinus superior and inferior. In 18% of cases the pars posterior lies basal to the border between the facies medialis and basalis. In two cases it has formed a very high arch, which causes the cuneus to be very small and to lie in a high position (Fig 9.3). In another case the similarly small cuneus was displaced basally because of the deep position of the sulcus parietooccipitalis (Fig 9.3). In two cases (1%) we found an accessory calcarine sulcus bilaterally (Fig 9.3).

Table 9.1 Pattern of combination of different sulc types on the left and right hemisphere. Symmetry: 24% (framed numbers), asymmetry: 76%

The configuration of the pars posterior shows seven variations. Descriptions of any single type and the statistics regarding occurrence are summarized in Fig 9.2. Because of the great variability, the types described are represented in simplified forms with subgroups of each of these types. However, we have not considered minimal and unimportant differences. Braus has pointed out that the diversity in the unique arrangement of the human brain is as variable as that of the single individual. No brain is quite the same as another, not even in monozygous twins, nor are the right and left sides of the brain the same. These statements also apply to the sulcus calcarinus in which a symmetrical pattern was found only in 24% of cases. The frequency and variability of possible bilateral combinations are given in Table 9.1.

Variations in the Terminal Part of the Pars Posterior On the average the pars posterior of the calcarine sulcus terminates at the occipital pole in 54%, at the medial aspect in 25.5%, on the convexity in 18.5% and on the basal hemispheric surface in 5% of cases. In 59.5% of the cases the terminal section is ramified. In 39% the ramification is T-shaped (Fig 9.2), in 16% V-shaped (Fig 9.2), and in 2% there are three branches (triradiate type, Fig 9.3, 71). The unbranched terminal part is rectilinear in 15% (Fig 9.4, 30); it ascends (Fig 9.2, 112) or descends (Fig 9.2, 190) in a hooklike manner in 25% of cases. In 43% of cases the forked branches were separated from the posterior end of the main fissure,

References p. 400

Variations in the Terminal Part

TypE

353

Relative distribution Left

Right

Mean values

Straight line

17%

29%

23 %

II. ARC-shaped

22%

19%

20.5%

III. Waved

20%

23%

21.5%

IV. Roof-shaped

22%

11%

16.5%

V. Wing-shaped

3%

6%

4.5%

VI. S-shaped

15%

11%

13 %

VII. M-shaped

1%

1%

1 %

I.

Fig 9.2 Variations in shape of the posterior part of the calcarine sulcus. 1 Torus of the cingulate gyri. 2 Infundibulum of the calcarine sulcus.

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9. Anatomy of the Calcarine Sulcus

References p. 400 Fig 9.3 1 3 1 High position of the calcarine sulcus (1). 193 Deep position of the parietooccipital sulcus (2). Both specimens have a small cuneus (3). 96 Accessory calcarine sulcus (4). 71 Triradiate branching (5) of the calcarine sulcus.

1 1 6 External calcarine sulcus (6). 1 5 2 Extreme sulcus (7). Both specimens have a superficial posterior cuneolingual gyrus (8). Infundibulum of the calcarine sulcus (9).

References p. 400

Side-Branches and Connections

355

Fig 9.4 127 An apparent superficial union simulates a triradiate branching ( 1 ) of the calcarine sulcus (2). In reality the calcarine sulcus terminates in front of an extreme sulcus (3) and is separated from this by a partly oper-culated posterior cuneolingual gyrus (4). 30 Union of the calcarine sulcus (2) with a vertical fissure of the cuneus (5). 1 4 1 Union of the calcarine sulcus (2) with the occipitotemporal sulcus (6). 7 Parietooccipital sulcus. 8 Vascular grooves. 9 Funnel like endings of the anterior part of the isthmus of the fornicate gyri.

in 19% they represented a horizontal fissure (Fig 9.3, 116) and in 24% a simple vertical or Y-shaped ramified fissure (Fig 9.3, 152). The horizontal fissure was called by Cunningham and Elliot-Smith the sulcus calcarinus externus, and the vertical one was named by Schwalbe and Zuckerkandl the sulcus extremus. In 34.5% of cases both variations of the fissure were separated from the main fissure by a superficially lying gyrus cuneolingualis posterior (Fig 9.3, 116, 152). In 8.5% this transitional convolution was operculated to a greater or lesser degree and thus arose as an apparent union with the main fissure. An example of such a case is shown in Fig 9.4. The superficial view looked deceptively like a triradiate branching main fissure. However, the deep aspect showed that this terminated without ramification and was separated from the closely annexed sulcus extremus.

Side-Branches and Connections The pars posterior formed in 41.5% of cases a simple linear fissure, in 58.5% was more complex, sidebranches (18%), indentations (35.5%) or both (5%). They were more frequently directed upwards than downwards. The side-branches represent the surface end of the deep fissures (Fig 9.10, 162), the indentations the ends of shallower sulci, which separate the transversely running internal convolutions (Fig 9.10. 13, 66, 152). Apart from the true branches which indent the whole width of the roof and floor of the sulcus, there are so-called pseudo branches in 18.5% of cases. These appear only in the upper or lower lips of the calcarine sulcus and form the "intrinsic fissures" of the internal transverse convolutions (Fig 9.7A, 13b). When the lips of the sulcus are closed, they appear to be side-branches of the calcarine sulcus (Fig 9.7, 13a).

356

9. Anatomy of the Calcarine Sulcus

References p. 400

In isolated cases an ascending side-branch joins terior end of the gyrus lingualis (Fig 9.4, 141). the fissural system of the cuneus (3%, Fig 9.4, 30) All the identified variations of the fissures and or a descending branch sulcus occipitotemporalis. their frequency of occurrence are summarized in The latter connection is considered by Zucker- Table 9.2. kandl as the result of the operculization of the posTable 9.2 Summary of different characteristic features of the posterior part of the calcarine sulcus in 200 hemispheres Characteristic features

Relative distribution Left

Right

Average

on the occipital pole

44%

64%

54%

on the medial brain surface

23%

22%

22.5%

on the convex brain surface

27%

10%

18.5%

on the basal brain surface

6%

4%

5%

unbranched

straight line

19%

hooklike upwards

7%

5%

6%

hooklike downwards

23%

16%

19.5%

T-shaped

31%

V-Shaped

18%

triradiate

Termination

branched

11%

52%

15%

41.5%

14%

16%

2%

2%

2%

Side-branches

20%

17%

18.5%

Indentations

41%

30%

Side-branches and indentations

7%

3%

of the medial brain surface

3%

-

of the basal brain surface

2%

2%

2%

Apparent connections

13%

24%

18.5%

Accessory calcarine sulcus

2%

2%

2%

Connection with grooves

Pars Anterior of the Calcarine Sulcus

The pars anterior of the calcarine sulcus begins at the calcarine-parietooccipital junction und runs obliquely downwards onto the basal surface of the hemisphere. Its funnel-shaped enlarged ending narrows the gyrus fornicatus. The narrowed point, the isthmus gyri fornicati, separates the upper part of the gyrus (gyrus cinguli) from the lower component (gyrus parahippocampalis) (Figs 9.1 A and

35.5% 5% 1.5%

9.4, 30). As the pars anterior forms the common stem of the sulcus calcarinus and the sulcus parietooccipitalis, its upper lips are formed by the lower end of the sulcus parietooccipitalis and its lower lips by the sulcus calcarinus (Fig 9.1A). Due to the divergence of the two lips the terminal portion of the fissure is widened into a funnel-shape (infundibulum sulci calcarini Fig 9.4, 30, 141).

References p. 400

Inner Structure of the Calcarinus

Fig 9.5 Variation in shape of the anterior part of the sulcus calcarinus. I Straight course. IV Sshaped. V Scythe-shaped. VI Bayonet-shaped. VII Undulating course.

Variations in Course The variations in the course of the pars anterior are similar to the pars posterior in that 7 types are found. Most frequent (41%) is a straight line (Fig 9.3, 131), or a crookedly ascending arch shape (20%) (Fig 9.3, 96). The individual variations and the frequency of their occurrence are shown in Fig 9.5. Unlike to the pars posterior, the pars anterior is symmetrical in about 50% of cases.

Connections and Side-Branches The upwardly arched end of the upper lips of the sulcus may join with the sulcus cinguli (1.5%, Fig 9.3, 102) or with the sulcus corporis callosi (1.5%). In the latter case it forms the tortuously indented end of the gyms cinguli (Fig 9.2, 136, 190). In 93.5% of cases the lower lip ends in a downwardly directed bow-shape in the vicinity of the

357

I Arc-shaped. Ill Angled.

sulcus hippocampi under the splenium of the corpus callosum (Fig 9.3, 96). In 5.5% it is strikingly long and runs parallel and very close to the sulcus hippocampi. Although previous literature strongly emphasizes that the sulcus calcarinus never joins the sulcus hippocampi, we found in one case out of 200 (0.5%) a union of the sulcus calcarinus and the sulcus hippocampi (Fig 9.6, 124). In another case the pars anterior did not constrict the gyms fornicatus but became continuous with the sulcus collateralis (Fig 9.6, 118). In 26% of cases side-branches of the sulcus intralingualis and collateralis appeared to anastomose with the pars anterior (Fig 9.6, 124]. These anastomoses, however, are not real. The side-branches simply formed indentations in the edges of the lower lip and were produced by the "intrinsic fissures" of the transverse and omega-shaped convolutions (Fig 9.8, 32, 162). In about 20% of cases there were small so-called vascular grooves on both sides of the sulcus calcarinus produced by branches of the medial occipital artery (Fig 9.6, ; 102, 115).

Inner Structure of the Sulcus Calcarinus The sulcus calcarinus is a deep fissure and has correspondingly broad upper and lower walls. In the region of the pars posterior the upper wall, the roof, and the lower wall or floor are formed by the lower surface of the cuneus and the gyrus Linguah's respectively. In the pars anterior the floor is similarly formed by the gyrus lingualis and the roof by the gyrus cinguli (Figs 9.1A, 9.7A-B)7_____ Cunningham described the so-called cuneolingual transitional convolutions as intrinsic structures of the calcarine sulcus. By means of the development he observed two such convolutions, the anterior and posterior cuneolingual gyrus. Both of them lie primarily superficially and divide the sulcus calca-

rinus into 3 sections. Later they become operculated and form deep convolutions. If they remain on the surface the sulcus calcarinus is interrupted, as in the early stage of its development. Because of the cogged wheel form of the interlocked components of the convolutions many lie either on the floor or in the roof (Figs 9.7 and 9.8). With the exception of the pillar-shaped unions, it is therefore difficult to differentiate exactly between convolutions belonging to the roof and to the floor. For this reason we studied the two structures separately and found great variability on both sides. Both sulcal surfaces exhibit major or minor transverse convolutions and straight or

358

9. Anatomy of the Calcarine Sulcus

References p. 400 1 2 3 4 5 6 7 8 9

Calcarine sulcus. Hippocampal sulcus. Parietooccipital sulcus. Cingulate gyrus. Collateral sulcus. Intralingual sulcus. Cingulate sulcus. Anterior part. Branching fissure.

Fig 9.6 Connection of the calcarine sulcus with theJTjppocampal sulcus (124), the collateral sulcus ( 1 1 8 ) and the^cjrv gulate sulcus (102). Undulating course of anterior part ( 1 1 5 ) .

S-shaped unions. There are approximately three times as many transverse convolutions as pillars. Contrary to previous publications we found two convolutions on the floor of the sulcus (Fig 9.8, 21) in only 44% of cases. In 41% there were 2 to 5 convolutions (3 convolutions in 28%, 4 in 12%, 5 in 1%) and in 11% only a single convolution. In 4% there was also a marked longitudinal convolution apart from transverse convolutions (Fig 9.8, 10). It is interesting that the number of convolutions varies greatly between right and left. On the left there were 2 convolutions in 58%, on the right only in 30%. On the other hand 3 or more convolutions appeared more frequently on the right (56%) than on the left (24%). Zuckerkandl (1906) examined 50 hemispheres and illustrated only the

left side. This could be the reason why he only mentions two transitional convolutions. We have named the most proximal convolution the gyrus cuneolingualis anterior, the most distal the gyrus cuneolingualis posterior and those between them the gyri cuneolinguales intermedii (Fig 9.8, 20). Besides the horizontal transverse convolutions of the floor and roof there is also a frontal transverse convolution at the end of the fissure. At the T—Y-or hooklike end of the sulcus calcarinus there are not only horizontal convolutions but also a frontal transversal convolution. We have named this the terminal convolution (Fig 9.7, 68, 13). Cunningham (1892) found a gyrus cuneolingualis anterior in 92% and a gyrus cuneolingualis posterior in 90% of cases. Our own material showed the

References p. 400

former in 25%, but the latter in 93% of cases. According to Cunningham the gyrus cuneolingualis anterior lies superficially in 31%, but according to Retzius (1896) only in 3%. We found the gyrus cuneolingualis to be lying superficially in only one case, i. e. 0.5% (Fig 9.9, 168). The superficial position of the gyrus cuneolingualis posterior was found by Cunningham in 31.5% of cases. We found this to be the case in 34.5%. The posterior section of the sulcus calcarinus separated by this convolution forms the sulcus calcarinus externus in 17% (Fig 9.3, 116) and a sulcus extremus in 17.5% (Fig 9.3). In a single case the lower part of the gyrus cuneolingualis posterior lay superficially whereas the upper part was operculated. Only the lower calcarine lip was interrupted, the sulcus calcarinus remained intact (Fig 9.9, 88). Fig 9.10 shows a few examples of the variability of shape, arrangement and quantity of the "roof-convolutions" lying on the lower surface of the cuneus. In 98% of cases the plane of the parieto-occipital sulcus is directed obliquely to the front, therefore the deep part of the apex cunei extends into the angle between the parietooccipital and calcarine sulcus like a tongue (Fig 9.7A, 68a,b). This socalled lingula cunei is always operculated in man (Zuckerkandl 1906). It was absent in only 2% of cases when the plane of the sulcus parietooccipitalis was transversely directed (Fig 9.7B, 8, 13). In 85% of cases the JinguJa ended blindJy and allowed communication between the sulcus parietooccipitalis and calcarinus. In 15.5% of cases the apex continued in a U or S-shaped crooked convofution. fn tne first case it ran info tfie anterior wai/ ot the, s\yk,v& рэд\йХоосс\р\Ы\ъ (¥\% 9.11, \Ж], in. the latter the prolonged S-shaped process formed the roof of the pars anterior sulci calcarini (Fig 9.11, 186). Cunningham designated this latter structure as the peduncle of the cuneus (gyrus cunei). It bridges the sulcus parietooccipitalis and closes off its deep part. In one case the peduncle of the cuneus joined the gyrus lingualis and closed off the sulcus calcarinus in its deeper part (Fig 9.11. 69). The floor of the pars anterior is formed by the gyrus lingualis and in 14% of cases remains flat and structureless throughout its whole length (Fig 9.12. 89, 104). In the remaining cases only the anterior half is flat, the posterior aspect contains convolutions in varying numbers and shapes. One transverse convolution was found in 21% (Fig 9.8, 151), two transverse convolutions in 4% (Fig 9.8, 21), a protuberance in 20% and an omega-shaped convolution in 20% (Fig 9.8, 32, 162). All these structures are closely related to the gyrus cuneolingualis anterior. There is a single longitudinal

Inner Structure of the Calcarinus

359

convolution in 2% and two in 6% of cases. They begin near the infundibulum sulci calcarini and run along the whole length of the floor of the pars anterior. The roof of the pars anterior sulci calcarini is usually formed by the lower end of the anterior wall of the sulcus parietooccipitalis and the gyrus cin-guli (Fig 9.1A, 9.7A-B). It can exhibit one or two obliquely ascending convolutions. In the above mentioned cases in which there is a peduncle of cuneus this forms the roof of the sulcus. Generally, the peduncle of the cuneus is operculated. However, it can sometimes lie superficially (pithecoid form) (Fig 9.11, 186). A superficial position was found by Lenhossek (1924) in 2.9%, but we found this only in 1% of cases (Fig 9.11, 186). Zuckerkandl's general assertion that the form of the calcarine fissure is essentially influenced by the shape and size of the deeply lying convolutions, could not be confirmed by our own findings. Our experience has shown that only defined curvatures (wave-, roofM-shaped) point to inner structures and these only to a limited extent. As an example the pars posterior in cases 89, 104 and 153 in Fig 9.12 shows an S-shaped curvature on the surface but in each case the inner structures differ. Side branches or indentations of the calcarine sulcus generally point to the existence of transverse convolutions or pillars (Figs 9.9, 88, 9.12, 89).

360

9. Anatomy of the Calcarine Sulcus

References p. 400

Fig 9.7A Shape of the apex of the cuneus in the presence of obliquely (A, 68) and transversely oriented parietooccipital sulcus (B, 13). 68a and 1 3 a surface view, 68b, 1 3 b cuneus removed. 1 Calcarine sulcus. 8 Apex of the cuneus. 2 Parietooccipital sulcus. 9 Lingula of the cuneus. 3 Roof of posterior part. 10 Transverse convolutions of sulcal floor. 4 Floor of posterior part. . 11 Terminal convolution. 5 Roof of anterior part. 12 Indentation of the end of an inner transverse fissure. 6_Floor of anterior part. 13 Pseudo branching of an intrinsic fissure of the transverse convolution. 7 Infundibulum of the calcarine sulcus.

References p. 400

Inner Structure of the Calcarinus

За

Fig 9.7B Inner structures of the parietooccipital and the posterior part of the calcarine sulcus. Cuneus removed. 1 Parietooccipital sulcus. 3/a Anterior cuneolingual gyrus. 2 Lingula of the cuneus. 3/b Posterior cuneolingual gyrus. 3 Floor of the posterior part of the calcarine sulcus. 4 Lower calcarine lip. 5 Anterior part of the calcarine sulcus.

361

362

9. Anatomy of the Calcarine Sulcus

References p. 400 Fig 9.8 Transitional convolutions of the floor of the calcarine sulcus. 1 Lingula of the cuneus. 2 Transverse convolution of posterior part. 3 Transverse convolution of anterior part. 4 Terminal convolution. 5 Longitudinal convolution. 6 Omega-shaped convolution of anterior part. 7 Pillar. 8 Parietooccipital sulcus.

Fig 9.10 Transitional convolutions in the roof of the posterior part. 1 Apex of the cuneus. 2 Lingula of the cuneus. 3 Indentation (end of a shallow inner transverse fissure). 4 Transverse convolution. 5 Pseudo side-branch (end of a deep inner fissure). 6 Pseudo side-branch (intrinsic fissure of a transverse convolution). 7 Pillar. Dotted line: Course of the calcarine sulcus. Similar configurations of the calcarine sulcus with different inner structures (162, 169).

References p. 400

Fig 9.9 168 Calcarine sulcus interrupted by a superficial anterior cuneolingual gyrus. 88 Partially superficial posterior cuneolingual gyrus. 1 Calcarine sulcus. 2 Parietooccipital sulcus.

Fig 9.10

Inner Structure of the Calcarinus

363

3 Superficial anterior cuneolingual gyrus. 4 Partial superficial posterior cuneolingual gyrus. 5 Floor of posterior part. 6 Cuneus-dotted line indicates the margin of the lip; i.e. the position of the calcarine sulcus on the surface of the brain.

364

9. Anatomy of the Calcarine Sulcus

References p. 400

Fig 9.11 130 U-shaped cuneate gyrus closing off the parietooccipital sulcus. 169 Cuneate gyrus closing off the deep aspect of the calcarine sulcus. 186 S-shaped cuneate gyrus closing off the parietooccipital sulcus. The end of the gyrus is not operculated.

References p. 400

Inner Structure of the Calcarinus

Fig 9.12 Different inner structures in similar configurations of the posterior part: 1 Calcarine sulcus (anterior part). 4 Transverse convolution. 2 Parietooccipital sulcus. 5 Cuneate gyrus (operculated). 3 Side branched fissure separating the transverse 6 Anterior part, convolutions. 7 Pillar.

365

366

9. Anatomy of the Calcarine Sulcus

Measurements The length and depth of the sulcus calcarinus was measured in 200 hemispheres. The average total length was 87 mm, of which the pars anterior accounted for 29 mm and the pars posterior for 58 mm. According to Donges (1983) the posterior part measures 37 mm. The discrepancy between his data and ours results from the different method of measurement. Donges measured the straight length, we however, took into consideration the shape dependent length and also that of the forking branches (13 mm). It is interesting that the different length of the right and left pars posterior (right 57 mm, left 59 mm) is compensated for by the opposite proportions of the pars anterior (right 30 mm and left 28 mm) and therefore the total length of the sulcus calcarinus is 87 mm on both sides. The depth of the sulcus calcarinus in our measurements was on average 15 mm. Smith and Richardson (1966) found a depth of 14.9 mm,

References p. 400

Lang (1979) 16.7 mm and Jensen (1926) 20 mm. The deepest point lay close to the junction with the sulcus parietooccipitalis. Here we found it to be 19 mm; Lang gives a depth of 21.5 mm. The extent of the inner surface of the sulcus is important because of the size of the area striata. Smith and Richardson (1966) found an average surface of 20.4-45 cm2, Zvorykin and SkolnikJarros (1953) of 26.3 cm2 and Economo (1926) of 24.25 cm2. As shown in Fig 9.13, the area striata occupies both halves of the sulcus in the pars posterior and only the lower portion in the pars anterior. Taking these three areas into consideration, we calculated an average surface area of 22 cm2. Our own calculations suggest that the size of the surfaces of the sulcus measures 22 cm2. If a strip about 0.5 cm along the exterior surface of the lips of the sulcus is taken into account the total size of the area striata is about 29 cm2. The length and width of the sulcus calcarinus are about equal on both sides and therefore the surface area too. Extent of the stripe of Fig 9.13 Gennari. 1 Upper lip of the posterior part. 2 Lower lip of the posterior part. 3 Lower lip of the anterior part. 4 Calcarine sulcus. 5 Parietooccipital sulcus. 6 Cuneus. 7 Lingual gyrus. 8 Cingulate gyrus. 9 Stripe of Gennari.

The Relationship Between the Sulcus Calcarinus and the Calcar Avis, Posterior Horn and Optic Radiation Most authors consider that because of its depth the sulcus calcarinus produces a dome, the calcar avis, in the posterior horn. Only Kuhlenbeck 71928) and Lenhossek (1924) suggest that the calcar avis is formed by the pars anterior sulci cal-carini (Fig 9.14A). Horizontal sections confirm this finding and show that the junction of the sulcus calcarinus and parietooccipitalis is largely responsible for the formation of the calcar avis (Fig 9.14C). At this point depth measurement revealed

maximum values (19 respectively 21.5 mm). The posterior horn exceeds this point only in exceptional cases. In such cases the pars posterior can also contribute to the formation of the calcar avis (Fig 9.14B). According to Lenhossek the calvar avis is absent in 5%. This finding can be explained by the individually varying depth of the sulcus (10—28 mm). A calcar is only formed at greater depths.

References p. 400

Relationship Sulcus Calcarinus and Optic Radiation

367

Fig 9.14 The relationship of the calcarine sulcus to the calcar avis, the posterior horn and the optic radiation. 1 Anterior part. 6 Calcar avis. 2 Posterior part. 7 Optic radiation. 3 Splenium of the corpus callosum. 8 Junction point of the calcarine sulcus with the pari4 Posterior forceps. etooccipital sulcus. 5 Posterior horn. 9 Boundary between anterior part and posterior part.

368

9. Anatomy of the Calcarine Sulcus

As Fig 9.14 shows the cortex in the floor of the sulcus borders on the radiation of the corpus callosum, the forceps posterior and the tapetum of the posterior horn. The optic radiation lies at the lower end of the sulcus parietooccipitalis, very close to the base of the sulcus, separated from this only by the forceps posterior (Figs 9.14B-C and 9.15). This position is also retained in the region

References p. 400

of the pars posterior sulci calcarini. The distance between the floor of the sulcus and the optic radiation measures on average 0.5 cm. Exceptions are those cases with an elongated posterior horn. In these cases the posterior horn lies close to the floor of the sulcus and separates it from the optic radiation (Fig 9.14B left side). Fig 9.15 Horizontal section of the right hemisphere. The calcar avis is formed only by the deep anterior part of the calcarine sulcus. 1 Head of the caudate nucleus. 2 Insula. 3 Internal capsule. 4 Thalamus. 5 Choroid plexus. 6 Hippocampus. 7 Collateral trigone (posterior horn). 8 Calcar avis. 9 Optic radiation. 10 Floor of the posterior part of the calcarine sulcus. 11 Cuneolingual convolutions. 12 Anterior part of the calcarine sulcus. 13 Posterior forceps.

369

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продолжение

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AVM Associated with Other Pathological Entities Fine, R. D., A. Paterson, J. B. Gaylor: Recurrent attacks of subarachnoid hemorrhage in the presence of a cerebral angioma and an intraventricular oligodendroglioma. Scot. med. J. 5: 324-345, 1966 Fischer, E. G., A. Sotrel, K. Welch: Cerebral hemangioma with glial neoplasia (angioglioma?). J. Neurosurg. 56: 430-434, 1982 Hettner jr.,R., R. S. Porro,M. D. V. Deck: Benign astrocytoma associated with arteriovenous ma/rbrmarion. Case report. J. Neurosurg. 35: 229-233, 1971 McCormick, W. F.: The pathology of angiomas. In Fein, J. M., E. S. Flamm: Cerebrovascular Surgery,' vol. IV/1. Springer, New York 1985 (pp. 1073-1095)

Chapter 4: Hemodynamics

•' ' v"r"

Aarabi, В., D. M. Long: Dynamics of cerebral edema. J. Neurosurg. 51: 779-784, 1979

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Chapter 6: Neuroradiological Evaluation Britt, R. H., G. D. Silverbcrg, D. R. Enzmann, J. W. Hanbery: Third ventricular choroid plexus arteriovenous malformation simulating a colloid cyst. J. Neurosurg. 52: 246-250, 1980 Cecile, J. P., A. Fournier, E. Laine, J. Cousin, M. Jomin, P. H. Duthilleux: Malformations artero-veineuses cerebrales re"ve"l£es par des varices peri-orbitaires chez une enfant de 3 ans. J. Radiol. Electrol. 52: 451-456, 1971 Cone, J. D., K. R. Maravilla, P. R. Cooper, J T. Diehl, W. K. Clark: Computed tomography findings in ruptured arteriovenous malformations of the corpus callosum. J. Comput. assist. Tomogr. 3: 478-482, 1979 Daniels, D. L., V. M. Haughton, A. L. Williams et al.: Arteriovenous malformation simulating a cyst on computed tomography. Radiology 133: 393-394, 1979 Decker, K.: Rontgendiagnostische Betrachtungen supratentorieller arteriovenoser GefaSmiBbildungen. ler Congr. Int. Neurochir., Bruxelles. Acta med. bclg. 57: 237-248, 1957 Diebler, C., O. Dulac, D. Renier, C. Ernest, G. Lalande: Aneurysms of the vein of Galen in infants aged 2 to 15 months. Diagnosis and natural evolution. Neuroradiology 21: 185-197, 1981 Dobbelaerc, P., M. lomin, J. Clarisse, E. Laine: Interet pronostique de I'etude du drainage veincux des anevrysmes arterio-veineux cerebraux. Neuro-chirurgie 25: 178-184, 1979 Faria jr., M. A.: External carotid component of AVMs. (Letter). J. Neurosurg. 56: 740, 1982 Fischer, E.: Die Lageabweichungen der vorderen Hirnartcrien im GefaBbild. Zbl. Neurochir. 3: 300-312, 1938

Foy, P. M., L. Lozada, M. D. Shaw: Vascular malformation simulating a glioma on computerized tomography. Case report. J. Neurosurg. 54: 125-127, 1981 Gardeur, D., M. Seurot, C. Fonda, A. Raynaud, J. C. Gaux: Digital intravenous subtraction angiography of intracranial arteriovenous malformations. Neuroradiology 25: 307-313, 1983 Goree, J. A., H. T. Dukes: The angiographic differential diagnosis between the vascularized malignant glioma and the intracranial arteriovenous malformation. Amer. J. Roentgenol. 90: 512-521, 1963 Harwood-Nash, D. C., C. R. Fitz: Neuroradiology in Infants and Children, vol. III. Mosby, St. Louis 1976 (pp. 913-929) Hayashi, S., T. Arimoto, T. Itakura et al.: The association of intracranial aneurysms and arteriovenous malformation of the brain. Case report. J. Neurosurg. 55: 971-975, 1981 Hayman, L. A., A. J. Fox, R. A. Evans: Effectiveness of contrast regiments in CT detection of vascular malformations of the brain. Amer. J. Neuroradiol. 2: 421-425, 1981 Hayward, R. D.: Intracranial arteriovenous malformations. Observations after experience with computerized tomography. J. Neurol. Neurosurg. Psychiat. 39: 1027-1033, 1976 Holmegren, B. S.: Radiographic changes by intracranial arteriovenous aneurysms. Acta psychiat. scand., Suppl. 46: 145-155, 1947 Huang, Y. P., T. Ohta, T. Okudera, A. Robbins: Anatomic variations of the dural venous sinuses. In Kapp, J. P., H. H. Schmidek: The Cerebral Venous System and its Disorders. Grune & Stratton, Orlando 1984 (pp. 109-167) Jensen, H. P., H. Klinge, J. Lemke, U. Muhtaroglu, M. Rautenberg: Computerized tomography in vascular malformations of the brain. Neurosurg. Rev. 3: 119-127, 1980 Kamrin, R. В.. H. W. Buchsbaum: Large vascular malformation of the brain not visualized by serial angiography. Arch. Neurol. (Chic.) 13: 413-420, 1965 Kendall, B. E., L. E. Claveria: The use of computed axial tomography (СТА) for the diagnosis and management of intracranial angiomas. Neuroradiology 12: 141-160, 1976 Kramer, R. A., S. R. Wing: Computed tomography of angiographically occult cerebral vascular malformations. Radiology 123: 649—652, 1977 Kumar, A. J.,F. Vinuela, A. J. Fox, A. E. Rosenbaum: Unrupturedintracranial arteriovenous malformations do cause mass effect. Amer. J. Neuroradiol. 6: 29-32, 1985 Lasjaunias, P.: Craniofacial and Upper Cervical Arteries. Collateral Circulation and Angiographic Protocols. Williams & Wilkins, Baltimore 1983 Lazar, M. L., C. C. Watts, B. Kilgore, K. Clark: Cerebral angiography during operation for intracranial aneurysms and arteriovenous malformations. Technical note. J. Neurosurg. 34: 706—708, 1971 Leban, M., U. Bergvall, M. Jiddane, F. Gelbert, E. di Geronimo, J. F. Landou, G. Salamon: Interet de la stereoangiographie dans 1'approche diagnostique et therapeutique des angiomes cerebraux. Value of stereoangiography for the diagnosis and treatment of cerebral angiomas. J. Neuroradiol. 12: 260-270, 1985 Leblanc, R., R. Ethier: The computerized tomographic appearance of angiographically occult arteriovenous malformations of the brain. Canad. J. neurol. Sci. 8: 7-13, 1981 Leblanc, R., R. Ethier, J. R. Little: Computerized tomography findings in arteriovenous malformations of the brain. J. Neurosurg. 51: 765-772, 1979 Lee, B. C. P., L. Herzberg, R. D. Zimmermann, M. D. F. Deck: MR imaging of cerebral vascular malformations. Amer. J. Neuroradiol. 6: 863-870, 1985 Leo, I. S., J. P. Lin, 1.1. Kricheff: Pseudoaneurysm formation secondary to spontaneous thrombosis of a massive cerebral arteriovenous malformation. Neuroradiology 17: 115-119, 1979 Lindgren, E.: Rontgenologic. In Olivecrona, H., W. Tennis: Handbuch der Neurochirurgie, vol. II. Springer, Berlin 1954 (pp. 198-207) London, D , D. Enzmann: The changing angiographic appearance of an arteriovenous malformation after subarachnoid hemorrhage. Neuroradiology 21: 281-284, 1981 McCallum, S. E., D. LoDolce, M. Boehnke: CT scan in intraventricular hemorrhage. Correlation of clinical findings with computerized tomographic scans of the brain. Neurosurgery 3: 22-25, 1978 McRae, D. L., V. Valentine: Pneumographic findings in angiomata of the brain. Acta radiol. (Stockh.) 50: 18-24, 1958 Manelfe, C., P. Lasjaunias: Endovascular treatment of cerebral AVMs. Cortical and posterior fossa AVMs. Book of abstracts. XHIrd Congress of the European Society of Neuroradiology 1985 (p. 45) *

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Lazorthes, G., A. Gouaze, G. Salamon: Vascularisation et Circulation de 1'Encephale, vol. I. Masson, Paris 1976 Lewis, O. J.: The form and development of the blood vessels of the mammalian cerebral cortex. J. Anat. (Lond.) 91: 40-48, 1957 Lierse, W.: Uber die Beeinflussung der Hirnangioarchitektur durch die Morphogenese. Acta anat. (Basel) 53: 1-54, 1963 Naritomi, H., J. S. Meyer, F. Sakai, F. Yamaguchi, T. Shaw: Effects of advancing age on regional cerebral blood flow. Arch. Neurol. (Chic.) 36: 410-416, 1979 Perria, L.: La vascolarizzazione del cervelletto dell'uomo. L'angioarchitettonica e i suoi rapporti con la citomielo-architettonica. Riv. Pat. nerv. ment. 58: 1-68, 1941 Pfeifer, R. A.: Grundlegende Untersuchungen fur die Angioarchitekto-nik des menschlichen Gehirns. Springer, Berlin 1930 (p. 220) Ravens, J. R.: Anastomoses in the vascular bed of the human cerebrum. In Cervos-Navarro, J.: Pathology of Cerebral Microcirculation. De Gruyter, Berlin 1974 (pp. 26-38) Ravens, i. R.: Vascular changes in the human senile brain. Advanc. Neurol. 20: 487-501, 1978 Rowbotham, G. F., E. Little: The circulations and reservoir of the brain. Brit. J. Surg. 50: 244-250, 1962 Ruckes, J.: Die arterielle Vascularisation der Pia mater des Neugeborenen. Frankf. Z. Path. 76: 227-234, 1967 Saunders,R. L. deC. H.,M. A. Bell: X-ray microscopy and histochemistry of the human cerebral bloodvessels. J. Neurosurg. 35: 128-140, 1971 Scharrer, E.: Arteries and veins in the mammalian brain. Anat. Rec. 78: 173-196, 1940 Steegman, А. Т.: A note on the anatomy of the meningeal blood vessels. Acta anat. (Basel) 40: 323-335, 1960 Sunderland, S.: The production of cortical lesions by devascularization of cortical areas. J. Anat. (Lond.) 73: 120-129, 1948 Takahashi, M.: Fine structure of the rat intracranial veins. Acta anat. nippon. 43: 238-254, 1968 Uchimura, Y.: Uber die Blutversorgung der Kleinhirnrinde und ihre Bedeutung fiir die Pathologic des Kleinhirns. Z. ges. Neurol. Psychiat. 120: 774-783, 1929 Wislocki, G. В., A. C. P. Campbell: The unusual manner of vascularization of the brain of the opossum (Didelphys virginiana). Anat. Rec. 67: 177-191, 1937 Wolff, J. A.: The cerebral blood vessels. Anatomical principles. Proc. Ass. Res. nerv. ment. Dis. 18: 29-67, 1938

Chapter 9: Anatomy of the Calcarine Sulcus Benninghoff, A., K. Goerttler: Lehrbuch der Anatomie des Menschen. Makroskopische und mikroskopische Anatomie unter funktionellen Gesichtspunkten, ll/12th ed. by H. Ferner; vol. Ill: Nervensystem, Haul und Sinnesorgane. Urban & Schwarzenberg, Munchen 1979 Braus, H.: Anatomie des Menschen, vol. III. Springer, Berlin 1932 Broca, P.: Descript. element des Circumvol. cerebr. de l'homme. Mem. f. Cerveau de l'homme et des primates, Paris 1888 Clara, M.: Das Nervensystem des Menschen, 2nd ed. Barth, Leipzig 1953 Corning, H. K.: Lehrbuch der Entwicklungsgeschichte des Menschen. Bergmann, Munchen 1925 Crosby, E. C., T. Humphrey, E. W. Lauer: Correlative Anatomy of the Nervous System. Macmiuan, New York 1962 (p. 731) Cunningham, D. J.: Contribut to the surface anatomy of the cerebral hemisph. Roy. irish Acad. 1892 Donges, C.: Befunde zur Fossa cranialis posterior. Diss., Wiirzburg 1983 Ecker, A.: Zur Entwicklung der Furchen und Windungen der GroQhirnhemispharen. Arch. Anthropol. 1868 Economo, C. V.: Die Bedeutung der Hirnwindungen. Allg. Z. Psychiat. psych.-gerichtl. Med. 84: 123-132, 1926 Elliot-Smith, G.: The so-called "Affenspalte" in the human (Egyptian) brain. Anat. Anz. 24: 74-83, 1903 Ellioth-Smith, G.: The morphology of the occipital region of the cerebral hemisphere in man and the apes. Anat. Anz. 24: 436-451,1904a Elliot-Smith, G.: The morphology of the retrocalcarin region of the cortex cerebri. Proc. roy. Soc. 73/1904b Filimonoff, I. N.: Uber die Variabilitat der GroBhirnrindenstruktur. Mitt. II. Regio occipitalis beim envachsenen Menschen. J. Psychol. Neurol. (Lpz.). 44: 1-96, 1932 Flatau, E., L. Jacobsohn: Handb. der Anat. und vergleichende Anat. des Zentralnervensystems der Saugetiere. Karger, Berlin 1899

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