Surgical Disorders of the Peripheral Nerves, Second Edition

Surgical Disorders of the Peripheral Nerves Second Edition

Rolfe Birch

Surgical Disorders of the Peripheral Nerves Second Edition

Author Rolfe Birch M. Chir, FRCP&S (Glas), FRCS (Edin), FRCS (Eng) by election Professor in Neurological Orthopaedic Surgery, University College, London and Visiting Professor, Department of Academic Neurology, Imperial College, London and Honorary Orthopaedic Consultant, Hospital for Sick Children Great Ormond Street, London and The National Hospital for Nervous Diseases, Queen Square, London and Raigmore Hospital, Inverness and Honorary Orthopaedic Surgeon to the Royal Navy and Consultant in Charge, War Nerve Injuries Clinic at the Defence Medical Rehabilitation Centre, Headley Court, Leatherhead, Surrey

ISBN  978-1-84882-107-1 e-ISBN  978-1-84882-108-8 DOI  10.1007/978-1-84882-108-8 Springer London Dordrecht Heidelberg New York British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library Library of Congress Control Number: 2010933604 © Springer-Verlag London Limited 2011 1st edition by R. Birch, G. Bonney and C.B. Wynn Parry published in 1998 by Churchill Livingstone, ISBN 978-0-443-04443-4 Apart from any fair dealing for the purposes of research or private study, or criticism or review, as permitted under the Copyright, Designs and Patents Act 1988, this publication may only be reproduced, stored or transmitted, in any form or by any means, with the prior permission in writing of the publishers, or in the case of reprographic reproduction in accordance with the terms of licenses issued by the Copyright Licensing Agency. Enquiries concerning reproduction outside those terms should be sent to the publishers. The use of registered names, trademarks, etc., in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant laws and regulations and therefore free for general use. Product liability: The publisher can give no guarantee for information about drug dosage and application thereof contained in this book. In every individual case the respective user must check its accuracy by consulting other pharmaceutical literature. Cover design: xxxxxx Printed on acid-free paper Springer is part of Springer Science+Business Media (www.springer.com)

In memoriam George Bonney

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Preface to the First Edition

“Opportunity comes to the mind prepared.” Opportunity came in full measure to H.J. Seddon with his appointment as surgeon in charge of the Medical Research Coucil’s (MRC) Peripheral Nerve Injury Unit in Oxford during the Second World War (1939–1945). It was after all in the Oxford of those days that J.Z. Young was doing the work on the nervous system that was to be the beginning of so many of the later developments in neuroanatomy and neurophysiology. The rewards of the MRC’s far sighted planning were abundant: to Seddon in particular was due that happy result. He was, however, the first to acknowledge the fortunate circumstances that enabled him to undertake the work in the company of so many doctors and scientists distinguished in the fields of anatomy, physiology and pathology of the peripheral nerves. He acknowledged too his debt to two great colleagues in clinical medicine: Hugh Cairns and George Riddoch. It was also fortunate that the Oxford unit was not allowed to die away at the end of the War, and that Seddon was able to continue at the Royal National Orthopaedic Hospital and the Institute of Orthopaedics the work that had begun and flourished at Oxford. After Seddon’s retirement his close colleague Donal Brooks and others developed and extended his work in London, while in other centres those who had worked with these men made their own contributions. Sadly, the bright hope that with introduction of the National Health Service the planning that contributed so much to the earlier success would be continued, has withered and died. Seddon’s belief that “the necessity for this segregation, this concentration of cases” would be recognised has been proved wrong. The hope may finally have been extinguished in this country by the introduction through the National Health Service Act of 1990 of an artificial internal market in health care, with competition between “providers of health care” and by the necessary corollary of the forced Gleichschaltung of the medical profession. Seddon’s firmness of purpose, clarity of thought, immense capacity for sustained hard work and powers of organisation were shown in “Peripheral Nerve Injuries” (1954) presented by the Nerve Injuries Committee of the Medical Research Council under his chairmanship. These characteristics were complemented by the qualities of those who collaborated in the work at Oxford. In the preface to the first edition of Surgical Disorders, Seddon paid generous tribute to J.Z. Young, P.B. Medawar, Graham Weddell and others. A special prominence was accorded to the contribution made by Donal Brooks. One who knew and worked with both has recorded the view that even that recognition was inadequate. He has made the disrespectful comparison of Brooks and Seddon with Jeeves and Wooster, and others who shared that experience may recognise the origins of the impious thought. Seddon’s character was of course the antithesis of that of Wooster, but those who saw these men at work cannot doubt that the calm guidance from the Irish Jeeves greatly influenced Seddon’s work and actions. Both editions of Surgical Disorders bear the mark of Seddon’s personality: the ordered thought; the meticulous observation and recording; the awareness of the ambient scientific field; the occasional dogmatic assertion; the love of tabulation. No one can read the book and vii

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not admire its depth and scope; no one can read it without astonishment at the comprehensive manner in which the subject is treated. One finds in it flashes of insight which, thought by the reader to have originated with him or her, turn out to be the subliminal origins of that thought. Some may consider it too bold an undertaking to attempt the revision of a work which is a classic of British clinical science and an abiding monument to Seddon’s work and leadership. However, things have moved on since 1975. Advances have been made in this country. In the field of disorders of peripheral nerves by Eames, Fullerton, Gamble, Gilliatt, Thomas, Urich and others. In continental Europe the work of Brunelli, Carlstedt, Gilbert, Hagbarth, Landi, Lundborg, Millesi, Morelli, Narakas, Slooff, Torebjörk, Wallin and others has opened new possibilities and destroyed old certainties. In the USA, Gelberman, Kline, Leffert, Omer, Spinner, Terzis, Wilbourn and many others have made massive contributions. In Canada, Hudson and Mackinnon have made great clinical and experimental contributions. In Australia, the doctrine of primary repair of injuries in the upper limb and hand was developed by Rank, O’Brien and others. In China, where the feasibility of “replantation” was first demonstrated, Professor Gu of Shanghai has made and continues to make advances in the field. The development of neurotisation was largely due to work in Japan, where Nagano and Sugioka and many others continue that and other work. In particular, ideas about all types of lesion of the brachial plexus have changed; conceptions of pain mechanisms have developed, and much enlightenment has come to the understanding of the pathology of tumours. Lastly, and most sadly the incidence of “iatrogenic” lesions has greatly increased, though in this connection great advances have been made in the treatment of birth injuries of the brachial plexus. The authors of the present work hope that they may have succeeded in restoring Surgical Disorders to its place as the British text on the present state of affairs in the field. George Bonney had the privilege and pleasure and occasional pain, of working with Seddon; Christopher Wynn Parry came to the Royal National Orthopaedic Hospital at the time of its Renaissance under the leadership of Lipmann Kessel when new fields in neurophysiology, in the treatment of pain and in the surgery of the brachial plexus were being explored; Rolfe Birch came to the field at St Mary’s and the Royal National Orthopaedic Hospitals armed with experience in microsurgery, and in histological and electron-microscopic techniques. Most of the work on the results of which we have drawn was done at St Mary’s and the Royal National Orthoapaedic Hospitals. The original layout of the book has largely been retained, but the text has been entirely rewritten. Chapters on “iatrogenic” lesions, on birth injuries of the brachial plexus and on recovery of sensibility after repair have been added. The subjects of pain and of tumours are considered in more depth than formerly. The subject of electrophysiological examination is considered by an expert in the field, Dr. Shelagh Smith. Rather more attention is given to anatomical considerations than was formerly the case. As Last (1949) remarked with some asperity “restatement of the facts appears to be warranted by the misconceptions shown by many postgraduate students.” Not just by students. Evidently, we have tried to keep abreast of continuing advances in this developing field, but we shall inevitably be overtaken by the march of events. One does what one can. As was shown by his magisterial reorganization of a then famous London medical library, Seddon saw a clear separation between “medicine” and “surgery.” As the title of this book suggests, we have aimed to deal mainly with disorders which are generally amenable to treatment by operation, and with the appropriate techniques of operation. However, we maintain a belief in the unity of medicine. The book is aimed at surgeons in training and in practice, at physicians in general and at neurologists in particular. We even hope that undergraduates will come to no great harm through reading it. The aim has been determined by observation over the years in the clinic and in the courts of a general lack of knowledge and want of interest in conditions of peripheral nerves. These defects in medical education have generally been unhelpful to patients: injuries of nerves have been “missed” in accident departments; the delay so

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produced is compounded by a lack of appreciation of the urgency of the situation and of the possibilities of repair; tumours of nerves too often go unrecognised until at operation a junior practitioner is confronted by a tumour occupying, or in close proiximity to, a major nerve. We hope that this book may help in stimulating interest in conditions affecting peripheral nerves, that it may aid in enhancing the quality of treatment of such lesions, and that it may bring the field of study to the notice of clinicians highly placed in surviving teaching institutions. Lesions of peripheral nerves are indeed very useful in teaching the interpretation of physical signs, which is after all the main business of the clinician. It has not been possible to treat exhaustively every aspect of the now large subject, but we hope that sufficient and sufficiently well chosen references have been given to open avenues for further reading. We had hoped to include a chapter on disorders of selected cranial nerves, and in particular of the facial nerve. That hope was, alas, born to die: we have in the event restricted the cranial nerve study to one which is really a spinal nerve – the spinal accessory – and to some aspects of damage to the fifth, seventh, tenth and twelfth nerves. Rashly, perhaps, we have proposed one or two new terms for varieties of nerve injury and for pain arising from the nerve injury. We have also revived an old suggestion for a term to replace that commonly used to designate injury inflicted by doctors. We do not hope to escape criticism for this presumption, but we hope that, at least, our derivations will be found by classicists to be correct. We hope that those derivations do no discredit to the august institution where their principles were imparted. All who work in this field owe a debt of gratitude to the late Sir Herbert Seddon, and to the late Sir Sydney Sunderland. The extent of their contribution is overwhelming: no list of references, however long, can indicate its magnitude. Any book on this subject must draw heavily on Peripheral Neuropathy, and in particular on the third edition (1993). We are glad to acknowledge our debt to the editors and authors contributing to that majestic work. The late Professor Roger Gilliatt was foremost amongst those who after the Second World War made advances in the field and stimulated the interest of his colleagues and juniors at Queen Square and in other centres. No-one contributed more to the study and treatment of lesions of the brachial plexus than did the late Professor Algimàntas Narakas of Lausanne. We gratefully acknowledge the contribution of these two men and the lasting influence of their work. 

Rolfe Birch George Bonney† Christopher Wynn Parry

Preface to the Second Edition

This work is dedicated to George Bonney who began preparation of the second edition of Surgical Disorders of the Peripheral Nerves shortly after the publication of the first. The structure of the book was well advanced by the time of his death. One main reason for undertaking this task was the rising tide of iatrogenous injuries. It became clear that it was no longer reasonable to assume that modern medical education provides graduates with a sound grasp of the anatomical and physiological principles of the peripheral nervous system. The work has been almost entirely rewritten with much greater emphasis upon the causes and manifestations of injuries to nerves, particularly iatrogenous injuries and the effects of ischaemia. Shelagh Smith and Ravi Knight have rewritten the chapter on electrodiagnosis which now takes its proper place in the central part of the book rather than at the end. Tara Renton has provided a welcome addition about the risks to the branches of the trigeminal nerve during facio-maxillary and dental work. The field of entrapment neuropathy has been reduced to a discussion about how to avoid error in diagnosis and in execution. With considerable reluctance the field of tumours of peripheral nerves has been approached in the same way. Information about cause, course and outcome in more than 6000 nerve injuries are summarised. The immense task of collation of data was undertaken by the staff of the Peripheral Nerve Injury Unit under the direction of the research coordinator, Margaret Taggart. Sanjay Patel provided exceptional skills in the development of different data bases and he analysed the extensive material about the birth lesion of the brachial plexus. Dirk de Camp, photographer of the Institute of Orthopaedics undertook all of the photographic work and developed an archive of several thousand images with particular precision. This involved the retrieval of much earlier material and he showed extraordinary patience in preparing the final order of the photographs for the different chapters. All of the drawings in this edition were done by Philip Wilson, who took on the constant revision and alteration without demur. We have indeed been fortunate in the close collaboration with distinguished colleagues in two other Institutions. Praveen Anand, now at the Hammersmith Hospital (Imperial College), has, with his team, provided extensive information from investigations of tissues obtained from patients with nerve injuries or suffering from neuropathic pain and these findings have been matched with those drawn from clinical examination and quantitative sensory testing performed in the Joint Clinics held with him, and with Peter Misra, at the Hammersmith Hospital. Uma Anand provided beautiful illustrations from the successful culture of neurones from human dorsal root ganglia. Nicholas Murray, Shelagh Smith, Peter Misra, and Carla Cordivari of the Department of Neurophysiology at the National Hospital for Nervous Diseases, Queen Square examined more than 1000 patients seen in our Joint Diagnostic Clinics. Susan Standring provided a great deal of her own original material and, through her good offices, Martyn Cooke curator and John Carr photographer, went to great lengths to provide photographs of specimens held in the Wellcome Museum of the Royal College of Surgeons of England. xi

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A number of colleagues undertook the laborious task of reading the manuscripts. The first four chapters were read by Susan Standring, Praveen Anand and Peter Misra who made many cogent suggestions and important corrections. Frank Horan, Editor Emeritus of the Journal of Bone and Joint Surgery, and Michael Laurence of the Editorial Board of that Journal undertook the arduous task of reading the entire work. Their contribution went far beyond the detection of innumerable blemishes. Their highly informed and meticulous criticism strengthened the structure and concept of the work. The responsibility for errors remains with the author. Margaret Taggart indexed and catalogued all references and transcribed the entire manuscript as well as developing and implementing methods within the Peripheral Nerve Injury Unit for the prospective collection of data for all patients. Thomas Carlstedt joined us in 1995, transferring his work from the Karolinska Institute, Stockholm and he shared his thoughts and work in the fields of injuries to the lumbo sacral plexus, reconnection between the central and the peripheral nervous systems in cases of avulsion of spinal nerves, entrapment of the pudendal nerve and in aspects of nerve tumours. Marco Sinisi, who joined us five years ago generously provided material from his experience with peripheral nerve tumours, neuropathic pain and prolonged conduction block. For many years our house surgeons and registrars have made important contributions by reviewing both case notes and patients and going to great lengths to retrieve classical references. We have been extremely fortunate in our many visiting colleagues, who brought with them new ideas and who undertook much original work. Without their contributions the work could not have gone forward and wherever possible those contributions have been acknowledged in the text. Particular thanks are due to the many hundreds of colleagues, for the most part orthopaedic surgeons, by whose acumen and professional authority so many patients have been sent to us with a clear and accurate diagnosis at the best possible time for their treatment. Particular thanks too go to our editors, Melissa Morton and Denise Roland of Springer. They provided so much encouragement and interest throughout but also offered highly critical reviews of earlier drafts which ensured some clarity of purpose. Rolfe Birch

Contents

1  The Peripheral Nervous System: Gross Anatomy . . . . . . . . . . . . . . . . . . . . . . . . . 1.1 The Cranial Nerves. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2 The Spinal Nerves. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.1 The Anterior Primary Rami. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.2 Thoracic Anterior Primary Rami. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.3 Lumbar and Sacral Anterior Primary Rami. . . . . . . . . . . . . . . . . . . . . . . . 1.2.4 The Posterior Primary Rami. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3 The Autonomic Nervous System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3.1 The Sympathetic System. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3.2 The Parasympathetic Nervous System. . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3.3 Afferent Autonomic Pathways. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.4 Nerves at Risk from Musculo Skeletal Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1 4 7 7 18 18 32 33 34 36 37 37 41

2  The Microscopic Structure of the Nervous System: Its Function . . . . . . . . . . . . . 2.1 The Neurotrophins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.1 Nerve Growth Factor. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 The Peripheral Nerve Fibres. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.1 Conduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.2 The Basis of the Action Potential: Ion Channels. . . . . . . . . . . . . . . . . . . . 2.2.3 Axonal Transport. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.4 The Blood Supply of Nerves. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.5 The Nervi Nervorum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.6 Changes in Nerves with Ageing. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 The Somatic Motor System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4 The Somatic Sensory System. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.1 Cutaneous Sensibility. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.2 The Skin. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.3 Cutaneous Sensory Receptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.4 Deep Sensibility. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.5 The Muscle Spindles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.6 The Golgi Tendon Organs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.7 Central Connections. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.8 Visceral Afferents. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5 Cortical Maps. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.6 Synaptic Activity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

43 44 44 46 54 56 57 58 59 59 61 62 62 64 65 66 66 68 69 70 71 72 72

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Contents

3  Reactions to Injury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Axonotmesis – Neurotmesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 The Cell Body and Proximal Stump. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.1 Wounds of the Perineurium. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.2 Contralateral Effects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 The Distal Stump . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4 Types of Lesion Produced by Different Physical Agents. . . . . . . . . . . . . . . . . . . 3.4.1 Acute Ischaemia. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.2 Ischaemia from Tamponade. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.3 Ischaemia and Acute Compression Within Neurovascular Fascial Compartments. . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.4 Ischaemia by Acute Compression from Swollen Muscle . . . . . . . . . . . . . 3.4.5 Ischaemia Caused by Traction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.6 Reperfusion Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.7 Chronic Ischaemia. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.8 Crush . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.9 Compression – Acute. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.10 Chronic Nerve Compression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.11 Traction or Stretch Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.12 Thermal Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.13 Electric Shock . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.14 Percussion Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.15 Injection Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.16 Vibration Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5 The Perineurium and Neoplasm or Infiltration. . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6 Radiation and Peripheral Nerves. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.7 Envenomation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.8 The Peripheral Effects of Denervation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.9 Changes at the Higher Levels: The Phantom Limb . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

90 92 95 96 97 97 98 99 100 103 104 106 106 107 107 108 108 109 110 111

4  Regeneration and Recovery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1 The Response of the Nerve and Axon to Transection. . . . . . . . . . . . . . . . . . . . . . 4.2 The Repair of Large Gaps. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.1 Other, Non Neural, Material for Grafts: Entubation . . . . . . . . . . . . . . . . . 4.3 Nerve Transfer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.1 Recovery of Cutaneous Sensation after Nerve Transfer . . . . . . . . . . . . . . 4.3.2 Recovery of the Deep Afferent Pathways after Nerve Transfer. . . . . . . . . 4.3.3 Complications of Regeneration. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4 Regeneration after Intradural Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5 Recovery of Function after Nerve Repair. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5.1 Methods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.6 Factors in Prognosis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.7 Severity of Injury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.8 Delay. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

115 116 123 126 128 130 130 132 135 137 138 139 140 140 140

5  Clinical Aspects of Nerve Injury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1 Associated Symptoms and Signs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2 Recognition of the Level and the Depth of Injury . . . . . . . . . . . . . . . . . . . . . . . . 5.3 Signs. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4 Tinel’s Sign. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5 Eliciting the Tinel Sign in Closed Lesions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

145 148 151 154 156 159

77 81 82 84 85 85 87 87 89

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5.6 5.7 5.8 5.9

Tinel’s Sign and Recovery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Examination of Sensibility. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Quantitative Sensory Testing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Examination of Muscles. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.9.1 Some Pitfalls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.9.2 Our Methods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.9.3 Clinical Examination. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.9.4 The Lower Limb. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.9.5 Late Signs of Nerve Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.9.6 Signs of Reinnervation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.10 Records. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.11 Aids to Diagnosis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

161 161 163 166 166 168 168 174 177 180 182 185 188

6  Clinical Neurophysiology in Peripheral Nerve Injuries . . . . . . . . . . . . . . . . . . . . Shelagh Smith and Ravi Knight 6.1 Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2 Electrodiagnostic Techniques. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2.1 Glossary of Electrodiagnostic Procedures. . . . . . . . . . . . . . . . . . . . . . . . . 6.2.2 Intra-operative Neurophysiological Procedures. . . . . . . . . . . . . . . . . . . . . 6.2.3 Electrodiagnostic Techniques and Localisation. . . . . . . . . . . . . . . . . . . . . 6.3 Limitations and Pitfalls of Electrodiagnostic Investigation . . . . . . . . . . . . . . . . . 6.4 Safety Aspects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.5 Pathophysiological Correlates. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.5.1 Types of Nerve Lesion: the Electrophysiological Consequences . . . . . . . 6.5.2 Regeneration and Reinnervation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.6 Clinical Applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.6.1 Upper Limb Neuropathies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.6.2 Lower Limb Neuropathies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.6.3 Diffuse Problems. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

191

7  Operating on Peripheral Nerves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1 Indications and Objects of Intervention . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1.1 Special Units: Their Role. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2 General Principles of Operation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2.1 Control of Bleeding. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.3 Apparatus and Instruments. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.4 Methods of Repair. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.4.1 The Vascular Repair. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.4.2 The Nerve Operations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.5 The Nerve Repair . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.5.1 Methods of Suture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.5.2 Grafting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.5.3 Indications For and Methods of Nerve Transfer . . . . . . . . . . . . . . . . . . . . 7.5.4 Immobilisation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.6 Approaches to Individual Nerves. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.6.1 The Transverse Supraclavicular Approach: (Anterior, or Anterolateral). . 7.6.2 The Transclavicular Exposure. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.6.3 The Postero-Lateral Route. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.7 Repair of the Roots of the Spinal Nerves in an Avulsion Lesion. . . . . . . . . . . . . 7.7.1 The Spinal Accessory Nerve. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.7.2 The Suprascapular Nerve. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.7.3 The Infraclavicular Part of the Brachial Plexus. . . . . . . . . . . . . . . . . . . . .

231 231 232 233 233 234 239 239 241 244 245 247 249 252 254 254 256 259 262 264 265 265

191 191 192 197 199 199 201 201 202 205 206 206 219 223 225

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7.7.4 7.7.5 7.7.6 7.7.7 7.7.8 7.7.9 7.7.10 7.7.11 7.7.12

The Circumflex Nerve . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Median and Ulnar Nerves in the Arm and the Axilla. . . . . . . . . . . . . . . . The Radial Nerve. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The Posterior Interosseous Nerve. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The Lower Part of the Median Nerve. . . . . . . . . . . . . . . . . . . . . . . . . . . . The Lower Part of the Ulnar Nerve . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nerves in the Abdomen and Pelvis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The Sciatic Nerve. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The Tibial and Common Peroneal Nerves in the Popliteal Fossa and Below. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  7.7.13 The Lower Tibial Nerve and the Plantar Nerves . . . . . . . . . . . . . . . . . . . 7.8 Entrapment Neuropathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.8.1 The Thoracic Outlet Syndromes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.8.2 The Suprapleural Membrane (Sibson’s Fascia). . . . . . . . . . . . . . . . . . . . 7.8.3 The First Rib. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.8.4 The Seventh Cervical Rib. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.8.5 Considerations About Operation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.8.6 Carpal Tunnel Syndrome. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.8.7 Technique of Operation (Open Method) . . . . . . . . . . . . . . . . . . . . . . . . . 7.8.8 Operations for Ulnar Neuropathy at the Elbow. . . . . . . . . . . . . . . . . . . . 7.8.9 The Less Common Entrapment Syndromes – Upper Limb. . . . . . . . . . . 7.8.10 Some Entrapment Neuropathies in the Lower Limb . . . . . . . . . . . . . . . . 7.8.11 Meralgia paraesthetica. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.8.12 Entrapment of the Pudendal Nerve. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.8.13 The Piriformis Syndrome. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.8.14 The Tarsal Tunnel Syndrome. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.8.15 “Morton’s Metatarsalgia”. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.9 Pitfalls in Operating on Tumours of Peripheral Nerves. . . . . . . . . . . . . . . . . . . . 7.9.1 The Solitary Benign Schwannoma (Neurolemmoma, Neurinoma). . . . . 7.9.2 The Intraneural Ganglion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.9.3 The Solitary Neurofibroma. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.9.4 Malignant Peripheral Nerve Sheath Tumours (MPNST). . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

266 266 266 267 267 269 270 271

8  Compound Nerve Injury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.1 The Wound. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.1.1 War Wounds: Current Practice. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.2 The Vascular Lesion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.2.1 The Shoulder . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.2.2 The Elbow. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.2.3 The Knee . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.2.4 The False Aneurysm and Arteriovenous Fistulae. . . . . . . . . . . . . . . . . . . 8.2.5 Ischaemia and the Nerve. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.2.6 Iatrogenous Ischaemic Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.3 Skin. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.4 Penetrating Missile Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.4.1 Suture and Grafting During World War Two: The MRCR Evidence. . . . 8.4.2 Grafts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.4.3 Experience from St Mary’s and the Royal National Orthopaedic Hospitals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  8.4.4 The Brachial Plexus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.4.5 Pain. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.4.6 The Peripheral Nerves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.4.7 Recent Experience . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

303 304 305 306 309 312 312 313 316 319 320 322 323 324

272 273 273 275 276 276 276 280 282 282 284 284 285 285 285 286 286 287 287 287 289 290 293 298

326 326 328 328 330

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8.5 Neurovascular Injuries: Amputation Revascularisation. . . . . . . . . . . . . . . . . . . . 332 8.5.1 The Brachial Plexus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 333 8.5.2 The Closed Infraclavicular Lesion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 334 8.6 Nerves and Bone and Joint Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 339 8.6.1 The Nerve and the Pattern of Fracture. . . . . . . . . . . . . . . . . . . . . . . . . . . 341 8.6.2 The Shoulder Girdle and Gleno-Humeral Joints. . . . . . . . . . . . . . . . . . . 343 8.6.3 The Clavicle. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 344 8.6.4 Dislocation of the Gleno-Humeral Joint . . . . . . . . . . . . . . . . . . . . . . . . . 345 8.6.5 The Radial Nerve and Fractures of the Humerus. . . . . . . . . . . . . . . . . . . 351 8.6.6 Incidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 351 8.6.7 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 355 8.6.8 The Musculocutaneous Nerve. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 355 8.6.9 Elbow. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356 8.6.10 Iatrogenous Injuries in the Adult. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 359 8.6.11 The Forearm. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  359 8.7 The Lower Limb. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 360 8.7.1 The Femoral Nerve . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 360 8.7.2 The Lumbo Sacral Plexus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 361 8.7.3 The Hip. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 363 8.7.4 The Common Peroneal and Tibial Nerves. . . . . . . . . . . . . . . . . . . . . . . . 365 8.7.5 More Recent Experience at the Royal National Orthopaedic Hospital. . 367 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 369 9  The Closed Supraclavicular Lesion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.1 Mechanisms of Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.2 Anatomy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.2.1 Course in the Neck. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.2.2 Micro Anatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.2.3 Functional Distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.3 Lesions of the Spinal Cord. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.4 The Evolution of Our Policy of Treatment of Closed Traction Lesions of the Brachial Plexus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.5 The Definition of Pre and Postganglionic Lesion: Prognosis for Recovery. . . . . 9.6 Epidemiology. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.7 Diagnosis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.7.1 Conduction studies: The Current Situation . . . . . . . . . . . . . . . . . . . . . . . 9.7.2 The Operation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.8 Some of the Techniques Used for Repair. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.9 Strategies of Repair. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.9.1 The Upper Lesion: Rupture or Avulsion of C5, C6 (C7) with Intact (C7) C8, T1. . . . . . . . . . . . . . . . . . . . . . . . . . 9.9.2 The Lower Lesion: Intact C5, C6 (C7), Rupture or Avulsion C8, T1. . . 9.9.3 The Middle Group. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.9.4 The Complete Lesion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.9.5 Free Functioning Muscle Transfer (FFMT). . . . . . . . . . . . . . . . . . . . . . . 9.9.6 The Bilateral Lesion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.10 Results. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.10.1 Methods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.10.2 Definitions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.10.3 Conventional Nerve Transfers. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.10.4 Repair of Avulsed Ventral Roots. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.11 Recovery of Function by Patients. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.11.1 Age. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

375 376 378 378 379 379 380 384 385 388 389 392 398 398 399 399 404 404 404 406 407 409 409 409 410 410 411 415

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9.12 Relief of Pain by Repair. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 416 9.12.1 Return to Work. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 420 9.13 Reimplantation of Avulsed Spinal Nerves. . . . . . . . . . . . . . . . . . . . . . . . . . . . 421 9.13.1 The First Clinical Case – George Bonney, 1977 (from the first edition of this work) . . . . . . . . . . . . . . . . . . . . . . . . . . 421 9.13.2 Subsequent Work by Thomas Carlstedt. . . . . . . . . . . . . . . . . . . . . . . 423 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425 10  Birth Lesions of the Brachial Plexus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 429 10.1 The Lesion of the Spinal Nerve in Birth Lesion of the Brachial Plexus (BLBP)����������������������������������������������������������������������������������������430 10.1.1 The Central Affect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 431 10.2 Methods of Study. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 432 10.2.1 Diagnosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 432 10.3 Epidemiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 436 10.3.1 Incidence. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 436 10.3.2 Risk Factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 437 10.4 Recovery in the Complete Lesion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 444 10.4.1 Group 3. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 445 10.4.2 Group 4. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 445 10.5 Treatment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 447 10.6 Supplementary Investigations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 448 10.6.1 Neurophysiological Investigations (NPI). . . . . . . . . . . . . . . . . . . . . . 448 10.6.2 Imaging. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 453 10.7 Nerve Operations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 453 10.8 The Indications for Operation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 453 10.8.1 The Incomplete Lesion: Groups 1 and 2 . . . . . . . . . . . . . . . . . . . . . . 454 10.9 The Operation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 454 10.9.1 Methods of Repair . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 456 10.9.2 Post-operative Care. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 456 10.10  Results of Nerve Operations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 457 10.10.1  Experience at St Mary’s – Royal National Orthopaedic Hospital . . . 458 10.10.2  Late Reinnervation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 462 10.10.3  Cocontraction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 463 10.11  Deformities. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 463 10.12  Posterior Subluxation (PS) and Posterior Dislocation (PD) of the Gleno-humeral Joint with Related Contractures . . . . . . . . . . . . . . . . . . 466 10.12.1  Onset and Progression of the Secondary Deformities. . . . . . . . . . . . 467 10.12.2  Diagnosis and Classification. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 469 10.12.3  Medial Rotation Contracture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 470 10.12.4 The Development of Our Preferred Operation for Posterior Subluxation or Dislocation of the Gleno-Humeral Joint. . . . . . . . . . 471 10.12.5 The Operation for Reduction of the Posterior Subluxation and Dislocation of the Gleno-Humeral Joint. . . . . . . . . .  473 10.12.6  Deformities at the Elbow and Forearm. . . . . . . . . . . . . . . . . . . . . . . . 478 10.13  Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 479 References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 479 11  Iatrogenous Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Part 1: General Considerations Rolfe Birch 11.1 Incidence and Audit. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.2 Causes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.2.1 Generalised Disorders. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.2.2 Alcohol. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

483

485 486 486 487

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11.2.3 Diabetes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.2.4 Connective Tissue Disease. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.2.5 Warning and consent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.2.6 Teaching and Training. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.2.7 Specialisation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.2.8 Continuity of Care: Timing of Operation. . . . . . . . . . . . . . . . . . . . . . . 11.3 Nerve Lesions in Total Hip Arthroplasty. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.3.1 The Nerve Lesion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.3.2 Findings in the 110 Patients Seen Between 2001 and 2007. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.3.3 Indications for Urgent Reexploration . . . . . . . . . . . . . . . . . . . . . . . . . 11.4 Radiation Neuropathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.4.1 The Place of Operation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.5 Prevention of Iatrogenous Lesions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.5.1   Teaching and Training. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.5.2   Audit and Consent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.5.3   Conduct of Affairs. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.5.4   Recognition and Action. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

487 488 490 492 493 493 494 494

Iatrogenous Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  Part 2: Minimising and Managing Iatrogenous Trigeminal Nerve Injuries in Relation to Dental Procedures Tara Renton 11.6 Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.6.1   Signs and Symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7 Mechanisms of Nerve Injuries. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7.1   Local Analgesic Related Trigeminal Nerve Injuries . . . . . . . . . . . . . . 11.7.2 Implant Related Nerve Injuries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7.3   Management of Implant Related Nerve Injuries . . . . . . . . . . . . . . . . . 11.7.4   Endodontic Related Nerve Injury. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7.5   Third Molar Surgery. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7.6   Dental Extraction of Other Teeth Proximal to IAN Canal. . . . . . . . . . 11.7.7   Socket Medications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7.8   Post Operative Infection Related Nerve Injuries. . . . . . . . . . . . . . . . . 11.7.9   Management of Trigeminal Nerve Injuries . . . . . . . . . . . . . . . . . . . . . 11.7.10  Evaluation of Trigeminal Nerve Injuries. . . . . . . . . . . . . . . . . . . . . . . 11.7.11  Possible Interventions and Timing. . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7.12  Possible Management Tools. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7.13  Reassurance Counselling/Cognitive Behavioural Therapy. . . . . . . . . 11.7.14  Medical Intervention . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7.15  Surgical Intervention . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7.16  Reasoning for Early Nerve Repair. . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7.17  Surgical Technique. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7.18  Medico Legal Issues. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7.19  Improved Consent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.7.20  Improved Management of These Injuries . . . . . . . . . . . . . . . . . . . . . . 11.7.21  Can We Prevent These Injuries? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

501

12  Pain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12.1 Nocicipient. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12.1.1 The Gate Theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12.1.2 Events After Nerve Injury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12.1.3 Central Pain: The Preganglionic Injury of the Brachial Plexus. . . . . . 12.1.4 The Sympathetic Nervous System and Pain . . . . . . . . . . . . . . . . . . . .

527 528 530 530 533 534

494 496 497 498 499 499 499 499 500

501 503 503 503 504 505 507 509 513 513 513 513 513 515 515 515 516 516 517 517 518 521 521 521 521

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12.2 Complex Regional Pain Syndrome (CRPS) Type 1 and (CRPS) Type 2. . . . . . 534 12.2.1 CRPS Type 2 (Causalgia). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 535 12.2.2   The Painful, Stiff, Swollen Part After Fracture or Soft Tissue Injury (CRPS Type I, Reflex Sympathetic Dystrophy). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  536 12.3 Diagnosis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 538 12.3.1 Drugs and Other Measures Short of Operation. . . . . . . . . . . . . . . . . . 538 12.3.2 Indications for Operation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 542 12.3.3 Causalgia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 542 12.3.4 Neurostenalgia. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 549 12.3.5 Post Traumatic Neuralgia. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 551 12.4 Interventions upon the Central Nervous System. . . . . . . . . . . . . . . . . . . . . . . . 555 12.4.1 Interventions on the Central Nervous System: Stimulation. . . . . . . . . 556 12.4.2 Interventions upon the Central Nervous System: Ablation. . . . . . . . . 557 12.5 Summary. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 558 References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 558 13  Reconstruction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.1 Requirements. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.1.1 The Tension of Transfer. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.1.2 Fixed Deformity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.1.3 Correction of Fixed Deformity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.2 Principles of Operation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.2.1 The Equino-varus Deformity of Ankle and Foot. . . . . . . . . . . . . . . . . 13.2.2 Flexor Muscle Slide, by the Technique of Books . . . . . . . . . . . . . . . . 13.2.3 Fixed Extension at the Metacarpo-phalangeal Joints. . . . . . . . . . . . . . 13.2.4 Release of Contracted Small Muscles of the Hand. . . . . . . . . . . . . . . 13.3 Methods of Reconstruction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.3.1 The Shoulder Girdle. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.3.2 Extension of the Elbow . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.3.3 Flexion of Elbow. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.3.4 The Operations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.4 Paralysis of the Extensors to the Wrist and Fingers, and of the Abductors and Extensors to the Thumb. . . . . . . . . . . . . . . . . . . . . . . 13.4.1 Pre and Post-operative Care. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.4.2 The Operations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.5 The High Median Palsy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.5.1 Abduction and Opposition of the Thumb. . . . . . . . . . . . . . . . . . . . . . . 13.6 The High Ulnar Palsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.7 Combined Nerve Lesions and the Hand. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.8 The Lower Limb. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.8.1 The Insensate Foot. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.8.2 Abduction and Flexion at the Hip . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.8.3 The Knee . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.8.4 Foot and Ankle: The Drop Foot from Common Peroneal Palsy. . . . . 13.9 Vascularized Bone and Muscle Transfer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.10 Amputation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.11 Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

563 565 568 569 571 572 573 573 574 575 576 576 580 580 582 584 586 587 589 589 591 593 594 596 596 597 598 601 601 602 603

14  Rehabilitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 607 14.1 Communication. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 608 14.2 History. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 609

Contents

xxi

14.3 The Rehabilitation Team. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.4 The Method of Work. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.5 Some Technical Aspects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.6 Motivation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.7 Rehabilitation in Progressive Neurological Disease. . . . . . . . . . . . . . . . . . . . . 14.8 The Choice of Intervention. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.9 Patients with Neuropathic Pain. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.10 Paralysis not Physically Determined. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.10.1 Conversion Paralysis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.10.2 The Munchausen Syndrome. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.10.3 Malingering. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.11 Rehabilitation in the War Wounded . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  14.11.1 Outcomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.12 The Future. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

610 611 612 616 624 624 625 626 626 627 628 628 629 630 630

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 631

Contributors

Ravi Knight, MB BS MD MRCPCH   Department of Clinical Neurophysiology, John Radcliffe Hospital, Oxford, UK Tara Renton, PhD MDSc BDS FRACDS(OMS) FDSRCS MHEA  Oral Surgery Department, King’s College London, London, UK Shelagh Smith, BSc MBChB FRCP  Department of Clinical Neurophysiology, National Hospital for Neurology and Neurosurgery, London, UK

xxiii

1

The Peripheral Nervous System: Gross Anatomy

Restatement of the facts appears to be warranted by the misconceptions shown by many post graduate students (Last 1949). Definition of the nervous system; separation of the central and peripheral nervous system; gross anatomy of the peripheral nervous system, including cranial and spinal nerves and the autonomic nervous system; nerves particularly at risk from skeletal injury and bleeding. The nervous system is the mechanism through which the organism is kept in touch with its internal structures and external environments and reacts to changes in them. The central nervous system – the brain and its caudal prolongation the spinal cord – is connected to the periphery by the peripheral nervous system. The latter includes the cranial nerves, the spinal nerves with their roots and rami, the peripheral nerves and the peripheral components of the autonomic nervous system, the sympathetic, parasympathetic and enteric divisions (Gardner and Bunge 2005). The peripheral nerves contain motor fibres (to end plates in skeletal muscle), sensory fibres (from organs and endings in skin, muscle, tendon, periosteum, and bone and joint), efferent autonomic fibres (to blood vessels, sweat glands and arrectores pilarum muscle), and visceral afferent fibres. In no other system is so much functional and relay capacity concentrated in so small a volume of tissue. The cervical spinal cord, with a width of about 2 cm and a depth of about 1.5 cm, contains all the apparatus transmitting control of somatic function from the neck down, together with that of control of much visceral function. Because of their greater content of connective tissue, the peripheral nerves have proportionately a lesser functional content, yet severance in an adult’s arm of the median nerve of 5 mm diameter effectively ruins the function of the hand and forearm (Fig. 1.1).

Phrenic n.

Dorsal root ganglion C5 Dorsal root ganglion C6

Fig. 1.1  The fifth, sixth cervical nerves avulsed from the spinal cord. The ventral root is easily distinguishable from the dorsal rootlets. Note the dorsal root ganglion, the dural sleeve merging into the epineurium and the spinal nerve itself. The small pieces of tissue on the proximal ends of the dorsal rootlets (below) are probably portions of the spinal cord.

Ventral root C5 Ventral root C6 Dorsal roots C5

R. Birch, Surgical Disorders of the Peripheral Nerves, DOI: 10.1007/978-1-84882-108-8_1, © Springer-Verlag London Limited 2011

Dorsal roots C6

1

2

Surgical Disorders of the Peripheral Nerves

The cranial and spinal nerves: Twelve pairs of cranial nerves arise from the brain and brain stem. The second of these, the optic nerves, are in fact prolongations of the central nervous system. Thirty-one pairs of spinal nerves – 8 cervical, 12 thoracic, 5 lumbar, 5 sacral and 1 coccygeal – arise from the spinal cord. Each spinal nerve leaves or enters the cord by a ventral, largely motor, root, and a dorsal sensory root (Figs. 1.2 and 1.3). Each sensory root splits into several rootlets as it approaches the spinal cord; these enter the cord along the line of the postero lateral sulcus. The division of the anterior roots into rootlets is less obvious and takes place nearer the cord. Because in the adult the spinal cord extends caudally only so far as the first lumbar vertebral level, the obliquity of the emerging and entering roots in the theca increases from above downwards (Figs. 1.4 and 1.5). The theca below the first lumbar level is occupied by the lumbar, sacral and coccygeal roots forming a leash whose appearance has been likened to that of a horse’s tail (cauda equina). The cell bodies of the fibres forming the anterior roots are mostly situated in the anterior horn of the grey matter of the spinal cord; those of the fibres of the dorsal root are in the dorsal root ganglion, situated in or near the intervertebral foramen. As they approach the foramen, the two roots join to form the spinal nerve, which outside the foramen divides into anterior and posterior primary rami (Fig. 1.6). The autonomic nervous system: Three divisions of the autonomic nervous system – the sympathetic, the parasympathetic and the enteric – are usually described. In each, pre-ganglionic fibres arise from cells in the brain stem or spinal cord. These relay in ganglia to post-ganglionic fibres innervating cardiac muscle, smooth muscle and glands. Most viscera are supplied by both sympathetic and parasympathetic divisions; the cell bodies of the enteric system are confined to the wall of the bowel (Gardner and Bunge 2005). Dorsal root

Dura mater Arachnoid Pia mater

Dorsal root ganglion

Fig. 1.2  The origin of the roots from the cord, their junction just distal to the dorsal root ganglion, and the emergence of the nerve from the spinal cord.

Ventral root

Posterior primary ramus

Fig. 1.3  The division of the spinal nerve (cervical region) into anterior and posterior primary rami.

Anterior primary ramus

Dorsal root ganglion

Spinal cord Dura mater

The Peripheral Nervous System: Gross Anatomy Fig. 1.4  The spine and spinal cord, seen from the front (a) and behind (b). Some of the dorsal bone has been excised. There is increasing obliquity of the roots in relation to the spinal cord from above down. Below the first lumbar level the spinal canal is occupied by the cauda equina. The dorsal root ganglia lie within the intervertebral foramina. The posterior primary rami are generally smaller than the anterior primary rami. The thoracic sympathetic chain is seen (a). The formation of the sacral plexus and the origin of the sciatic nerve is shown (b).

a

Fig. 1.5  The left side of the spinal cord exposed by hemilaminectomy. The cord has temporarily been rotated by stays passed through the denticulate ligaments. The upper most roots (left) are those of the fifth cervical nerve: they emerge at an angle of about 45° to the cord. The lowest roots (right) are those of the seventh cervical nerve, emerging at a very oblique angle to the cord.

3

b

4

Surgical Disorders of the Peripheral Nerves

1.1 The Cranial Nerves (Figs. 1.6–1.9, 1.12 and 1.14–1.16) The first, olfactory, mediates the sense of smell; the second, optic, mediates that of sight. The latter nerve is a prolongation of the central nervous system. The third, fourth and sixth nerves control the muscles concerned with movement of the eye. The fifth, (trigeminal) nerve has an extensive motor and sensory function, controlling the muscles of the jaw and conveying sensation from the skin of the face and the mucosa of the mouth and nose, and probably from the superficial muscles of the face. The lingual branch which conveys sensation from the tongue and buccal mucosa is, with the inferior alveolar nerve, particularly at risk during operations upon the mouth and jaws. Compression of the trigeminal sensory root by branches from the superior cerebellar artery is a common cause of trigeminal neuralgia (Hughes 2005). The seventh (facial) nerve innervates the superficial muscles of the face and neck. It is remarkable for its vulnerability to damage in each of the three parts of its course – intra-cranial, intra-osseous (in the petrous part of the temporal bone) and extra-temporal. The eighth (auditory) nerve mediates the senses of hearing and of balance. The ninth (glosso-pharyngeal) nerve conveys sensibility from the pharynx and from the back of the tongue and has a small motor function. The tenth (vagus) nerve has, as its name suggests, wide ranging branches and functions, most of the latter being parasympathetic. Motor branches innervate the muscles of the larynx, and sensory branches convey sensation from it. Its recurrent laryngeal branch is in the ascending part of its course in close relationship with the trachea and oesophagus and with the thyroid and parathyroid glands (Fig. 1.16a and b).

Spinal accessory n.

Vertebral a.

Dorsal roots C3, C4 and C5 Superior cervical sympathetic ganglion Vagus n. Dorsal root ganglia C5 and C6

Posterior primary ramus of C7

Fig. 1.6  The brainstem and cervical cord exposed by laminectomy. The spinal accessory nerve passes anterior to the dorsal roots, and emerges through the jugular foramen accompanied by the vagus and glosso-pharyngeal nerves. The vertebral artery courses anteriorly to the spinal nerves.

The Peripheral Nervous System: Gross Anatomy Fig. 1.7  The formation of the 11th cranial (cranial and spinal accessory) nerve. Note the temporary “cranialisation” of the spinal component of the nerve.

5

Pons

Vagus n.

Abducens n.

Jugular foramen

Cranial root

Spinal root C1

Accessory n. Foramen magnum

C2

C3 Spinal cord C4

C5

Trigeminal (V) n. Facial (VII) and vestibulocochlear (VIII) n.n. Glossopharyngeal (IX), vagus (X) and accessory (XI) n.n. Spinal part of accessory n.

Vertebral a. Posterior primary ramus C2 Anterior primary ramus C2 Dura Dorsal root ganglion C3

Fig. 1.8  The junction between the spinal cord and the brain stem shown by excision of a posterior bony element. The first cervical nerve passes away from the spinal cord at almost a right angle.

6 Fig. 1.9  (a) The terminal branches of the facial nerve emerging from deep to the parotid gland. The greater auricular nerve courses obliquely across the sternocleidomastoid. (b) The deeper course of the facial nerve is shown after excision of parotid, the spinal accessory nerve is seen crossing the floor of the posterior triangle.

Surgical Disorders of the Peripheral Nerves

a

Greater occipital n. Lesser occipital n. Parotid gland and facial n. branches at anterior border

Great auricular n. External jugular v. Transverse cervical n.

Marginal mandibular branch of facial n. Cervical branch of facial n.

b

Spinal accessory n.

The Peripheral Nervous System: Gross Anatomy

7

The spinal part of the eleventh (accessory) nerve arises from cells in the accessory nucleus, “a column of cells of the somatic efferent type, extending from the second to the fifth and sixth cervical segments of the cord” (Brodal 1981). These cells are in the dorsolateral part of the anterior horn of the grey matter. The fibres emerge segmentally from each side of the cord, to unite to form on each side a nerve which passes rostrally, posterior to the denticulate ligament, into the cranial cavity through the foramen magnum. In the cranial cavity the nerve unites briefly with its cranial part, derived mainly from the cells in nucleus ambiguus, before passing out of the skull with it through the jugular foramen. Outside the skull the two parts separate, the cranial portion going to join the vagus nerve and the spinal part passing obliquely down the neck to innervate the sternocleidomastoid and trapezius muscles. The spinal accessory nerve is particularly at risk to the activities of surgeons in the posterior triangle of the neck yet its course here is consistent. It emerges from beneath the sternocleidomastoid muscle at about 5 mm cephalad to the point where the greater auricular nerve begins its upward course over the anterior face of the muscle. The course of the nerve distal to the posterior triangle has been described by Pereira and Williams (1999). The innervation of the trapezius has been described by Brown (2002) and by Kierner et al. (2001) who showed that the middle and lower parts of the muscle may be partially supplied by branches from the cervical plexus whereas the upper one-third is innervated solely by the spinal accessory nerve. Although Bremner-Smith et al. (1999) thought that 60% of the individual nerve fibres were unmyelinated or finely myelinated, and that many of these were afferent fibres, this observation was not confirmed by Bunting and Standring (2000), who did not detect unmyelinated axons in immunofluorescence light microscopic studies. The 12th (hypoglossal) nerve leaves the skull through the hypoglossal canal in the occipital bone to supply the intrinsic and all but one of the extrinsic muscles of the tongue. Although there are receptor organs in the muscles of the human tongue (Cooper 1953), it is likely that most of the impulses from them travel in the lingual nerve (Weddell et al. 1940). The sensation of taste is mediated by fibres in the facial nerve (anterior two-thirds of the tongue) and by fibres in the glossopharyngeal nerve (posterior one-third of the tongue). In the upper part of the neck the hypoglossal nerve is joined by fibres from the anterior rami of the uppermost two cervical nerves. These soon leave the nerve to form the ansa hypoglossi from which the infrahyoid muscles are supplied.

1.2 The Spinal Nerves 1.2.1 The Anterior Primary Rami The anterior primary rami of the uppermost four cervical nerves unite and branch to form the cervical plexus, through which the skin of the neck and part of the face and some of the muscles of the neck are innervated. A branch of the fourth cervical anterior ramus, with contributions from the third and fifth rami, passes caudally into the thorax as the phrenic nerve, to supply motor fibres to the diaphragm and sensory fibres to the related pleura, fibrous pericardium and peritoneum (Figs. 1.10–1.12). The anterior primary rami of the lowest four cervical nerves and most of that of the first thoracic nerve unite and branch to form the brachial plexus in the lower part of the neck and behind the clavicle (Figs. 1.13–1.16). The upper limb receives its innervation through the branches of this important plexus. The most proximal muscles are supplied by branches from the rami; the intermediate muscles by branches from the trunks and cords; the muscles of the limb itself by branches from the main terminal nerves – the median, ulnar, musculo-cutaneous, radial and circumflex (axillary). There is a segmental pattern to this innervation: the most proximal muscles are supplied by branches of the uppermost rami; the most distal muscles are supplied by branches derived from the eighth cervical and first thoracic nerves. The segmental pattern of innervation is shown more clearly in the cutaneous supply (Figs. 1.17 and 1.18). The cervical root supply has been, as it were, extruded from the supply to the trunk. Thus, in the transition of innervation from the skin of the neck to that of the trunk there is anteriorly a change from the fourth cervical to the second thoracic segment; posteriorly, from the fifth cervical to the first thoracic segment. An important anatomical and functional differentiation of the plexus takes place with the division of the trunks into anterior and posterior divisions. From the anterior divisions the lateral and medial cords are formed; from the posterior divisions the posterior cord is formed. The lateral and medial cords innervate pre-axial (flexor) musculature; the posterior cord innervates post-axial (extensor) musculature. The plexus and the distribution of its nerves vary considerably from one individual to another: the contributions made by the component nerves vary; the origin and method of formation of the main nerves vary; in some cases the contribution of the fifth nerve is large and that of the first thoracic nerve is small, while in others the reverse is the case. The truly autonomous area of cutaneous supply of each main component nerve is small and variable in extent and location. The contributions made

8

Surgical Disorders of the Peripheral Nerves

Fig. 1.10  The right cervical plexus and its (mainly sensory) branches.

C1 Hypoglossal (XII n.) Lesser occipital

C2

Great auricular Transverse cervical

C3

Superior root of ansa cervicalis Inferior root of ansa cervicalis

C4

C5

Supraclavicular n.n.

Phrenic

Ramus to n. to serratus anterior

by the fourth cervical and second thoracic nerves vary: usually their contributions are small, but occasionally the fourth cervical nerve makes an important contribution to the innervation of scapulo-humeral muscles (Figs. 1.19–1.29). The supply of the skin and of the hand is divided between the median, ulnar and radial nerves. The first two supply the palmar aspect; all supply the dorsal aspect. The median nerve supplies the skin of the radial side of the palm, the palmar aspects of the thumb, index and middle fingers and of the radial part of the ring finger, and the terminal parts of the dorsal aspect of these digits. The ulnar nerve supplies the skin of the ulnar side of the palm, the palmar aspects of the little finger and the ulnar part of the ring finger, the dorsal aspect of the ulnar half of the hand, the little and ring fingers and the ulnar side of the proximal part of the middle finger. The radial nerve supplies the radial side of the dorsum of the hand, of the proximal parts of the thumb and index fingers and of the radial side of the middle finger. Damage to the terminal branches of these nerves of cutaneous sensation, which is usually caused by a needle or scalpel, often leads to pain which is quite out of proportion to the functional importance of the nerve. Mok et al. (2006) studied the cutaneous innervation of the dorsum of the wrist and of the hand; Tindall et al (2006) describe a “safe zone” which avoids damage to the dorsal cutaneous branch of the ulnar nerve; Beldner et al. (2005) studied the relations between the lateral cutaneous nerve of the forearm and the superficial radial nerve and MacAvoy et al. (2006) offer practical advice about avoiding damage to the posterior cutaneous nerve of the forearm (Fig. 1.29). Gruber (1870) having dissected the forearm of 125 cadavers, reported an incidence of 15.2% of branches between the median and ulnar nerves in the forearm . Most commonly, a branch runs from the anterior interosseous branch of the median nerve to the ulnar nerve, but Srinivasan and Rhodes (1981) recognize six varieties of this anomaly, the “Martin-Gruber” anastomosis. Bhadra et al. (1999) displayed, by dissection, important variations in the innervation of the flexor digitorum profundus, whilst Branovovacki et al. (1998) and Mahakkanukrauh and Somsarp (2002) reveal different patterns of distribution of the radial nerve. Whilst the variations of the distribution of the peripheral nerves are significant we have found that the variations in the distribution of the spinal nerves forming the brachial plexus are much more important. At least one-third of patients with complete lesions of C5, C6 and C7 retain powerful extension of the digits and this is seen in some patients in whom only the first thoracic nerve has survived.

The Peripheral Nervous System: Gross Anatomy

9

Fig. 1.11  The course of the phrenic nerve. Note the small branch to the pericardium.

Great auricular n. Transverse cervical n. Spinal accessory n. Cervical n. passing to accessory Supraclavicular n.n.

Omohyoid m. Internal jugular v. Nerve to serratus anterior Phrenic n. Lateral pectoral n.

Fig. 1.12  The cervical and brachial plexus. The right supraclavicular nerves are shown. The left brachial plexus is exposed after excision of sternocleidomastoid and the clavicular head of pectoralis major.

10

Surgical Disorders of the Peripheral Nerves

Fig. 1.13  The right brachial plexus. Note the sequence: the anterior primary rami; trunk; divisions; cord; nerves. Note that the trunks are upper, middle and lower, and that the cords are lateral, medial and posterior from their position in relation to the axillary artery which is, in fact, variable.

C3 C4 C5

Supraclavicular n.

C6

Upper trunk

Lateral cord Posterior cord Medial cord Lateral pectoral n. Circumflex n.

C7

Dorsal scapular n. Middle trunk Suprascapular n. Lower trunk

C8 T1 Phrenic n. Nerve to serratus anterior Medial pectoral n.

Axillary a. Thoracodorsal n. Medial cutaneous n. of forearm Radial n. Musculocutaneous n. Median n. Ulnar n.

Vagus n. Transverse cervical a. Suprascapular a. Thoraco-acromial a.

Phrenic n. Suprascapular n.

Fig. 1.14  The brachial plexus revealed by excision of both clavicles. The right subclavian vein has been removed, both left subclavian vessels have been excised.

The Peripheral Nervous System: Gross Anatomy

11

a

b Stellate ganglion Vertebral a.

Suprascapular n. Phrenic n. Vagus n. Recurrent laryngeal n.

Suprascapular a. Subclavian a.

Subclavian a. Common carotid a.

Subclavian v.

Brachiocephalic v.

Fig.  1.15  The right brachial plexus and the great vessels. (a) Left: showing the relations of the brachiocephalic vein and its branches. (b) Right: the subclavian vein has been excised, revealing the subclavian artery passing deep to scalenus anterior.

a

b

Internal carotid a. Vagus n.

Phrenic n. Thyrocervical a.

Superior cervical sympathetic ganglion

Spinal accessory n. Internal jugular v.

Subclavian a. Vagus n. Recurrent laryngeal n.

Thoracic duct

Common carotid a.

Common carotid a.

Thoracic duct

Subclavian a. Recurrent laryngeal n.

Fig. 1.16  The left brachial plexus. (a) Left: sternocleidomastoid has been excised. (b) Right: the clavicle and part of pectoralis major has been removed.

12

Surgical Disorders of the Peripheral Nerves

C3

C3

C4

C4 T2 T3 T4 T5 T6 T7

T3 T4 T2

T2

T10 T11

T5 T6

T8 T9

T2

C5

C5

T1

C6

C6

T7 T1

T8 T9

T12

C6

L1

T10

C6

T11 T12 L1

C8

C7

Fig.  1.17  Approximate distribution of dermatomes on the posterior aspect of the right upper limb (From Aids to the Examination of the Peripheral Nervous System, 4th edition. By kind permission of Dr. Michael O’Brian and Elsevier Ltd).

C7

C8

Fig.  1.18  Approximate distribution of dermatomes on the anterior aspect of the right upper limb (From Aids to the Examination of the Peripheral Nervous System, 4th edition. By kind permission of Dr. Michael O’Brian and Elsevier Ltd).

Upper subscapular n.

Musculocutaneous n.

Circumflex n. Lower subscapular n. Thoracodorsal n.

Latissimus dorsi tendon Median n.

Nerves to triceps

Ulnar n. Nerve to brachialis

Lateral cutaneous n. forearm

Fig. 1.19  The main nerves in the right axilla and arm.

Nerve to medial head triceps

The Peripheral Nervous System: Gross Anatomy Fig. 1.20  The right circumflex (axillary) and suprascapular nerves.

13

Suprascapular n.

Superior transverse scapular ligament

Supraspinatus

Suprascapular n. Joint capsule Infraspinatus

Deltoid Circumflex n.

Teres minor Branches of radial n. to triceps Teres major

Radial n.

Triceps brachii

Suprascapular a. Suprascapular n.

Acromioclavicular joint

Medial head Long head Lateral head

CIRCUMFLEX (AXILLARY) NERVE

Deltoid RADIAL NERVE UPPER CUTANEOUS NERVE OF THE ARM

Posterior circumflex humeral a.

Teres minor

Circumflex n.

Fig. 1.21  The posterior aspect of the right shoulder after excision of trapezius and most of deltoid showing the course of the suprascapular and the circumflex nerves and their vessels.

Fig. 1.22  The right (axillary) circumflex nerve (From Aids to the Examination of the Peripheral Nervous System, 4th edition. By kind permission of Dr. Michael O’Brian and Elsevier Ltd).

14

Coracobrachialis MUSCULOCUTANEOUS NERVE

Surgical Disorders of the Peripheral Nerves

CIRCUMFLEX (AXILLARY) NERVE Triceps, long head Triceps, lateral head

Biceps Triceps, medial head Brachialis

Brachioradialis

RADIAL NERVE

Extensor carpi radialis longus Extensor carpi radialis brevis Supinator

POSTERIOR INTEROSSEOUS NERVE (deep branch)

Extensor carpi ulnaris Extensor digitorum Lateral cutaneous nerve of the forearm

Extensor digiti minimi Abductor pollicis longus Extensor pollicis longus Extensor pollicis brevis Extensor indicis

Fig.  1.23  The right musculocutaneous nerve (From Aids to the Examination of the Peripheral Nervous System, 4th edition. By kind permission of Dr. Michael O’Brian and Elsevier Ltd).

SUPERFICIAL RADIAL NERVE

Fig. 1.24  The right radial nerve (From Aids to the Examination of the Peripheral Nervous System, 4th edition. By kind permission of Dr. Michael O’Brian and Elsevier Ltd).

The Peripheral Nervous System: Gross Anatomy

15

Fig. 1.25  The anterior aspect of the right elbow. Lateral cutaneous n. of the forearm

Brachioradialis m. Posterior interosseous n.

Superficial radial n. Flexor digitorum superficialis m. (radial head cut) Anterior interosseous n. Nerve to flexor pollicis longus

Ulnar n. Brachial a. Median n. Nerve to pronator teres Nerve to palmaris longus, flexor dig. sublimis and flexor carpi radialis Nerve to flexor carpi ulnaris Nerve to flexor digitorum profundus Nerves to flexor digitorum sublimis

Nerve to flexor digitorum profundus Ulnar n. and a.

Flexor pollicis longus

Flexor carpi ulnaris Flexor digitorum profundus

16

Surgical Disorders of the Peripheral Nerves

Sensory Dorsal cutaneous branch

MEDIAN NERVE

ANTERIOR INTEROSSEOUS NERVE

Flexor carpi radialis Palmaris longus Flexor digitorum superficialis

Deep motor branch Superficial terminal branches

Flexor digitorum profundus I & II Flexor pollicis longus

Flexor pollicis brevis Opponens pollicis

Flexor carpi ulnaris Flexor digitorum profundus III & IV MEDIAL CUTANEOUS NERVE OF THE FOREARM

Motor Abductor pollicis brevis

MEDIAL CUTANEOUS NERVE OF THE ARM

Palmar cutaneous branch

Pronator teres

Pronator quadratus

ULNAR NERVE

Palmar branch Motor

Flexor retinaculum

Adductor pollicis Flexor pollicis brevis

Abductor Opponens digiti Flexor minimi

1st Dorsal interosseous

First lumbrical

1st Palmar interosseous

Second lumbrical

Third lumbrical

Fourth lumbrical

Sensory

Fig. 1.26  The right median nerve (From Aids to the Examination of the Peripheral Nervous System, 4th edition. By kind permission of Dr. Michael O’Brian and Elsevier Ltd).

Fig. 1.27  The right ulnar nerve (From Aids to the Examination of the Peripheral Nervous System, 4th edition. By kind permission of Dr. Michael O’Brian and Elsevier Ltd).

The Peripheral Nervous System: Gross Anatomy

17

Fig. 1.28  The median and ulnar nerves in the left hand. Inset shows the normal course of median nerve at the wrist and also the palmar cutaneous nerve.

Common palmar digital n. Median n. dividing into common palmar digital branches Recurrent branch of median n. Flexor carpi radialis m. Radial a.

Superficial palmar arch Nerve to hypothenar m.m. Deep branch of ulnar n. Superficial branch of ulnar n. Ulnar n. Ulnar a. Flexor carpi ulnaris m.

Median n.

Recurrent branch of median n.

Flexor retinaculum

Palmar cutaneous branch of median n. Median n. Flexor carpi radialis m. Flexor digitorum superficialis m.

18 Fig. 1.29  The terminal branches of the superficial radial and lateral cutaneous nerves of forearm seen during operation at the right wrist.

Surgical Disorders of the Peripheral Nerves Superficial radial n.

Extensor carpi radialis longus

Lateral cutaneous n. forearm

Extensor carpi radialis brevis

1.2.2 Thoracic Anterior Primary Rami The second to the sixth thoracic anterior primary rami innervate the intercostal muscles and the skin of the anterior and lateral chest wall. Most of the first nerve goes to join the brachial plexus; most of the second goes as the intercosto-brachial nerve to innervate the skin of the axilla and of the medial side of the arm. The lower six thoracic anterior rami continue from the intercostal spaces to the anterior wall of the abdomen, innervating its skin and muscles. The lowest nerves supply sensory fibres to the lateral part of the diaphragm. The lowest (12th) thoracic ventral ramus, sometimes called the subcostal nerve, is larger than the others and connects with the ilio-hypogastric branch of the first lumbar nerve.

1.2.3 Lumbar and Sacral Anterior Primary Rami (Fig. 1.30) The first lumbar anterior primary ramus gives rise to two mainly cutaneous nerves and part of a third. The iliohypogastric, iloinguinal and genitofemoral nerves supply respectively the skin of part of the buttock, of the groin and the greater part of the external genitalia. The second, third and fourth lumbar anterior rami unite and branch to form the lumbar plexus from which arise the nerves innervating the skin of the thigh and its anterior and medial muscles. The plexus is formed in the anterior part of the psoas major muscle, in the posterior wall of the abdomen. Its terminal branches lie under the parietal peritoneum. Some of these emerge lateral and some medial to the psoas major. The most important terminal branch is the femoral nerve, which passes, lateral to the psoas major and femoral vessels, under the inguinal ligament to reach the upper part of the thigh (Figs. 1.31 1.32 and 1.39). Through its anterior and posterior divisions it supplies the skin of the anterior surface of the thigh and the quadriceps and sartorius muscles. The saphenous branch of the posterior division descends with the femoral artery to emerge from the femoral canal above the knee and supply the skin of the medial side of the leg and foot. The obturator nerve emerges medial to the psoas major and, passing along the lateral wall of the pelvis, emerges into the thigh through the obturator foramen. Through anterior and posterior branches the adductor muscles and the skin of the medial side of the thigh are supplied. Part of the fourth lumbar ramus and all the fifth ventral ramus join to form the lumbo-sacral trunk, which emerges medial to the psoas major to enter the pelvis and join the first, second and third sacral nerves to form the sacral plexus on the posterolateral wall of the pelvis (Figs. 1.33 and 1.34).

The Peripheral Nervous System: Gross Anatomy

19

Ganglionated chain

L1

L1

L2

L2

Iliohypogastric n. L3

L3

Ilioinguinal n. L4

L4

Genitofemoral n. Psoas muscle

L5

L5

Femoral n. Lumbosacral trunk

S1

Lateral cutaneous n. thigh Femoral n.

S2

Obturator n.

S3 S4

Pudendal n.

Fig. 1.30  The femoral and sacral plexuses and the ganglionated sympathetic chain.

Sciatic n.

20

Surgical Disorders of the Peripheral Nerves

Fig. 1.31  The left femoral nerve. Lateral cutaneous n. of thigh

Femoral n. Femoral a. Medial circumflex femoral a. Lateral circumflex femoral a. Anterior branch of obturator n. Medial cutaneous nerve of thigh 2nd perforating a. 3rd perforating a. Saphenous n. Femoral a. (cut)

Femoral a. (cut) Ascending branch of lateral circumflex femoral a. Profunda femoris 1st perforating a. Intermediate cutaneous nerve of thigh Descending branch of lateral circumflex femoral a.

The Peripheral Nervous System: Gross Anatomy

21

Fig. 1.32  The left femoral nerve.

Femoral n.

Nerves to iliacus

External iliac a. External iliac v. Obturator n.

a

1st sacral n.

Lumbosacral trunk Genitofemoral n.

Sympathetic trunk 2nd sacral n. 3rd sacral n.

Femoral n.

4th sacral n. Pudendal n.

Fig. 1.33  The relations of the left sacral plexus. (a) The female pelvis. (b) The male pelvis.

Obturator n.

22 Fig. 1.33  (continued)

Surgical Disorders of the Peripheral Nerves

b

1st sacral n.

Lumbosacral trunk Genitofemoral n.

Sympathetic trunk 2nd sacral n. Femoral n.

3rd sacral n. 4th sacral n.

Obturator n.

Pudendal n.

Union of ventral rami of S2 and S3

Ventral ramus of S1

Ventral ramus of S4

Fig. 1.34  The left sacral plexus.

Sacrospinous ligament

Lumbosacral trunk

The Peripheral Nervous System: Gross Anatomy

23

The innervation of the perineum and most of the lower limb is derived from the branches of this plexus (Figs. 1.37 and 1.38). The sciatic nerve, the largest in the body, leaves the pelvis through the greater sciatic foramen and passes behind the hip joint into the back of the thigh. This great trunk has two main components, which are functionally and often anatomically quite distinct (Figs. 1.35, 1.36, 1.39 and 1.40). The tibial nerve innervates the medial hamstrings, it descends in the midline through the popliteal fossa into the back of the leg, to supply its superficial and deep muscles. It has an important and frequently useful branch, the sural

Gluteus maximus (reflected) Superior gluteal n. Inferior gluteal n. Pudendal n. Sciatic n. Posterior cutaneous n. of thigh

Tibial n. Common peroneal n. Nerves to lateral and medial gastrocnemius Nerve to popliteus Nerves to soleus Sural n.

Sural communicating branch

Tibial n.

Medial calcaneal n.

Fig. 1.35  The right sciatic nerve and its major components in the lower limb.

24

Surgical Disorders of the Peripheral Nerves

Superior gluteal n.

T10

Common peroneal division of sciatic trunk

L1 T11

L2 T12

Inferior gluteal n.

L1

S5

S4

S3

S3

Pudendal n.

S4

Posterior cutaneous n. of thigh

L2

L2 S2

L3

L3

Tibial division of sciatic trunk

S2 L4

Fig. 1.36  The right sciatic nerve and its two main components, the common peroneal and tibial nerves. The CPN is quite distinct and in this specimen it passes separately through piriformis muscle, a not uncommon variation.

L5 L4 L5

S1

L3

L3

S2

S1 L5

S2

S1 L5

S4 S3

S3 S5

L2

L2

L2

L2

Fig.  1.38  Approximate distribution of dermatomes on the perineum (From Aids to the Examination of the Peripheral Nervous System, 4th edition. By kind permission of Dr. Michael O’Brian and Elsevier Ltd).

Fig. 1.37  Approximate distribution of dermatomes on the right lower limb (From Aids to the Examination of the Peripheral Nervous System, 4th edition. By kind permission of Dr. Michael O’Brian and Elsevier Ltd).

The Peripheral Nervous System: Gross Anatomy Fig. 1.39  The nerves on the anterior aspect of the right lower limb (From Aids to the Examination of the Peripheral Nervous System, 4th edition. By kind permission of Dr. Michael O’Brian and Elsevier Ltd).

25

Iliacus FEMORAL NERVE

LATERAL CUTANEOUS NERVE OF THE THIGH

OBTURATOR NERVE

Cutaneous branch Adductor brevis MEDIAL CUTANEOUS NERVE OF THE THIGH

Rectus femoris Quadriceps Vastus lateralis femoris Vastus intermedius Vastus medialis INTERMEDIATE CUTANEOUS NERVE OF THE THIGH

Adductor longus Gracilis

Adductor magnus

COMMON PERONEAL NERVE SUPERFICIAL PERONEAL NERVE Peroneus longus Peroneus brevis LATERAL CUTANEOUS NERVE OF THE CALF Peroneus tertius

Extensor digitorum brevis

DEEP PERONEAL NERVE Tibialis anterior Extensor digitorum longus Extensor hallucis longus SAPHENOUS NERVE

26 Fig. 1.40  The nerves on the posterior aspect of the right limb (From Aids to the Examination of the Peripheral Nervous System, 4th edition. By kind permission of Dr. Michael O’Brian and Elsevier Ltd).

Surgical Disorders of the Peripheral Nerves

Gluteus medius Gluteus minimus SUPERIOR GLUTEAL NERVE Piriformis

SCIATIC NERVE

Tensor fasciae latae INFERIOR GLUTEAL NERVE Gluteus maximus

Semitendinosus Semimembranosus Adductor magnus

TIBIAL NERVE

POSTERIOR CUTANEOUS NERVE OF THE THIGH Biceps, long head Biceps, short head

COMMON PERONEAL NERVE

Gastrocnemius, medial head Soleus

Gastrocnemius, lateral head

Tibialis posterior Flexor digitorum longus

Flexor hallucis longus

TIBIAL NERVE SURAL NERVE CALCANEAL BRANCH

MEDIAL PLANTAR NERVE to: Abductor hallucis Flexor digitorum brevis Flexor hallucis brevis Cutaneous branches

LATERAL PLANTAR NERVE to: Abductor digiti minimi Flexor digiti minimi Adductor hallucis Interossei Cutaneous branches

The Peripheral Nervous System: Gross Anatomy

27

nerve, which arises in the upper part of the popliteal fossa, descends between the two heads of gastrocnemius and pierces the deep fascia in the proximal part of the leg (Figs. 1.41 and 1.42). Usually, a branch from the common peroneal (or fibular) nerve joins the sural nerve; at times, it is larger than the contribution from the tibial nerve. Rarely, the sural nerve arises wholly from the common peroneal division. The nerve then descends to pass lateral to the tendo Achilles to supply the skin on the lateral side of the foot. The tibial nerve continues into the foot behind the medial, tibial, mallelous and through its terminal medial and lateral plantar branches supplies the intrinsic muscles of the foot and the skin of the sole (Fig. 1.44a). The common peroneal nerve innervates the lateral hamstring muscles in the thigh. It diverges laterally from the mid line to pass behind the head of the fibula and lateral to its neck. Here it divides into deep and superficial peroneal nerves. The former passes into the anterior compartment of the leg to innervate the anterior muscles and finally to supply the extensor digitorum brevis and the skin of the dorsum of the first interdigital space (Figs. 1.43 and 1.44b). The superficial peroneal (musculocutaneous) nerve passes deep to the upper part of the peroneus longus muscle to supply both peronei. Its continuation pierces the deep fascia in the distal part of the leg to supply the skin of the dorsum of the foot and anterolateral part of the ankle.

Popliteal a.

Sciatic n.

Tibial n. Common peroneal n. Superior lateral genicular a. Superior medial genicular a. Saphenous n. Inferior medial genicular a.

Sural communicating branch Inferior lateral genicular a. Nerve to popliteus

Tibial n.

Sural n.

Fig. 1.41  The right popliteal fossa.

28

Surgical Disorders of the Peripheral Nerves

Fig. 1.42  The right popliteal fossa.

Tibial n. Sartorius m. Gracilis m. Semitendinosus m. Nerve to medial gastrocnemius m.

Common peroneal n. Plantaris m. Lateral head of gastrocnemius m.

Semimembranosus m. Popliteal a.

Medial head of gastrocnemius m.

Sural n.

The more proximal branches of the sacral plexus supply the gluteal muscles and the skin and muscles of the perineum (Figs. 1.35, 1.36 and 1.38). The superior gluteal nerve, emerging above the piriformis muscle supplies the short gluteus medius and minimus and the tensor fasciae latae. The inferior gluteal nerve, emerging below the piriformis muscle, supplies the gluteus maximus muscle. Kampa et al. (2007) have described an internervous “safe zone” for exposure of the capsule of the hip. The pudendal nerve leaves the pelvis through the greater sciatic foramen and, entering the pudendal canal through the lesser sciatic foramen, passes into the perineum to innervate its skin and muscles. As in the case of the upper limb, there is a segmental innervation of the muscles and, more easily seen, of the skin. Again, the segments innervating the limb have been extruded from the innervation of the trunk and perineum, so that in the transition from trunk to perineum there is posteriorly a segmental change from the third lumbar to the third sacral dermatome. The skin of the foot is supplied by all the main nerves of the lower limb save the obturator (Figs. 1.44–1.46). The plantar surface is supplied by the tibial nerve through its plantar branches; the medial side by the saphenous branch of the femoral nerve; the lateral side by the sural branch of the tibial nerve, and the dorsum by the superficial and deep divisions of the common peroneal nerve. Apparently trivial injuries to the terminal branches of the nerves of cutaneous sensation sometimes cause even more trouble in the lower than in the upper limbs. Tennent et  al. (1998) describe painful neuromas of the infrapatellar branch of the saphenous nerve whilst MacNicol and Kelly (2002) provide an ingenious method for preventing this by transillumination during arthroscopic work. Solan et  al. (2001) advise against the conventional dorsal incision over the hallux because of the constant dorso medial branch which arises from the superficial peroneal nerve.

The Peripheral Nervous System: Gross Anatomy

29

Fig. 1.43  The course relations and branches of the right common peroneal nerve.

Lateral sural cutaneous n. Common peroneal n. Lateral sural cutaneous n.

Deep peroneal n. Superficial peroneal n.

Sural n. Deep peroneal n. Superficial peroneal n.

Fascia of the leg

Lateral calcaneal branches

Dorsal branch of plantar digital n. of great toe

Deep peroneal n., cutaneous branch

30 Fig. 1.44  (a) Above: the medial aspect of the right ankle. (b) Below: the lateral aspect of the left ankle and heel.

Surgical Disorders of the Peripheral Nerves

a Posterior tibial a. Medial calcaneal n.n.

Tibialis posterior m. Flexor digitorum longus m. Flexor hallucis longus m. Medial plantar n.

Lateral plantar n.

b Short saphenous v. Sural n.

Superficial peroneal n.

Peroneus longus m. Anterior tibial a. and deep peroneal n.

Peroneus brevis m.

The Peripheral Nervous System: Gross Anatomy

Dorsal branch of plantar digital n. of great toe

31

Proper plantar digital n.n.

Common plantar digital n.n. Flexor hallucis longus Flexor digitorum longus

Medial plantar n.

Lateral plantar n., superficial branch Lateral plantar n., deep branch

Lateral plantar n.

Dorsal branches of plantar digital n. great toe

Flexor hallucis longus Flexor digitorum longus

Medial plantar n. Lateral plantar n. Flexor digitorum brevis Tibial n.

Fig. 1.45  The sole of the left foot.

Plantar aponeurosis

Fig. 1.46  The sole of the left foot.

32

Surgical Disorders of the Peripheral Nerves

1.2.4 The Posterior Primary Rami The posterior primary rami are usually smaller than the anterior. Most divide into medial and lateral branches to supply the muscles and skin of the posterior part of the neck and trunk. They do not enter the limbs. The posterior primary rami of the uppermost three spinal nerves differ from those of the lowest five in extending their supply to the back of the head (Fig. 1.47). The posterior ramus of the first nerve, actually larger than the anterior ramus, chiefly supplies muscles between the atlas and occiput. The posterior ramus of the second cervical nerve is the largest of the cervical posterior rami and larger than its anterior ramus. Emerging between the posterior arch of the atlas and the lamina of the axis, it divides into a large medial and a smaller lateral branch. The former goes on as the greater occipital nerve to innervate the skin of the back of the scalp. At its beginning, it is in close relationship with the back of the atlanto-axial joint. The third cervical posterior ramus provides a third occipital branch. The posterior rami of the lowest five cervical nerves innervate the posterior vertebral muscles; the medial branches of the fourth and fifth rami also innervate the skin. The thoracic posterior primary rami similarly pass posteriorly close to the posterolateral (zygapophyseal) intervertebral joints to supply posterior vertebral muscles and the skin of the back of the chest. The lumbar posterior rami are similarly disposed, but only the uppermost three reach the skin. The sacral posterior rami are small, having a small distribution to muscle and to the skin over the sacrum.

Vertebral a.

Atlantoaxial facetal joint

Greater occipital n.

Fig. 1.47  The uppermost right three cervical vertebrae and the greater occipital nerve.

Lower articular process of C3

Vertebral a.

The Peripheral Nervous System: Gross Anatomy

33

1.3 The Autonomic Nervous System Conventionally, the autonomic nervous system is divided into two parts – the sympathetic and the parasympathetic nervous systems. Langley (1903, 1926) proposed the enteric nervous system as a third component. Indeed, the complexity and extent of the innervation of the viscera are such as to make this further division attractive (Furness and Costa 1980). Both systems are characterized by having relays between their cells of origin and their terminations: in the case of the sympathetic system the relays are in paravertebral or axial ganglia; in the case of the parasympathetic system they are in or near the organs innervated (Fig. 1.48).

Afferent Dorsal root Sympathetic chain Dorsal horn (sensory neurone) ganglion and ganglion

Blood vessel

Ventral horn Fig. 1.48  Efferent (red) and afferent (green) autonomic paths in the spinal cord and ganglionic chain.

Ventral Efferent (motor neurone) root

Grey ramus

Skin

Intestine

Splanchnic ganglion (coeliac) White ramus

34

Surgical Disorders of the Peripheral Nerves

1.3.1 The Sympathetic System The pre-ganglionic cells of the efferent fibres of the sympathetic system are in the lateral horn of the grey matter of the spinal cord from the first thoracic to the second lumbar level. Most of the ganglia are in the paravertebral sympathetic chains extending from the top to the bottom of the spinal column; others lie in autonomic plexi in the abdominal cavity. Usually there are on each side 2 cervical, 1 cervico-thoracic (stellate), 11 thoracic, 4 lumbar and 5 sacral or pelvic ganglia. Preganglionic myelinated fibres enter the cervico-thoracic, thoracic and upper two lumbar ganglia in white rami from the first thoracic to the second lumbar spinal nerve. These fibres relay in the corresponding ganglia or proceed up or down the chain to relay in other ganglia of the chain or in one of the ganglia of the autonomic plexi. The distribution to the spinal nerves is by way of grey rami, which contain unmyelinated fibres, from the corresponding paravertebral ganglia. Fibres pass directly from the autonomic plexi to their destinations. Afferent fibres have their cells in the posterior root ganglia; their sites of relay are not clearly identified. The sympathetic supply to the head and neck arises mainly from the uppermost three thoracic segments, passes cranially, and relays in the cervical ganglia to be distributed to vessels and sweat glands and in particular to the dilator of the pupil, and the smooth muscle fibres in orbitales and levator palpebrae superioris muscles. Most of the supply to these muscles of the eye arises from the first thoracic segment. The sympathetic supply to the upper limb arises principally from the second to the sixth thoracic segments. Fibres pass up the chain to the middle cervical and cervicothoracic stellate ganglia, where they relay to be distributed by grey rami to the nerves of origin of the brachial plexus (Figs. 1.49 and 1.50). The sympathetic supply to the lower limbs arises from the lowest three thoracic and uppermost two lumbar segments. Fibres enter the first and second lumbar ganglia by white rami, descend in the chain, relay in the lumbar and sacral ganglia and are distributed by grey rami to the lumbar and sacral nerves (Figs. 1.51 and 1.52).

Stellate ganglion

8th cervical n. Lower trunk of plexus

C7

1st intercostal n. 1st posterior intercostal vessels

T1

Kuntz n. Rib 1 T2

T3

Ventral ramus T1

Rib 2

Ventral ramus C8

Rib 3

Lower trunk

Sympathetic chain and ganglion

T4 Rib 4 Superior intercostal v.

Superior costotransverse ligament

Fig. 1.49  The relations of the cervico thoracic (stellate) ganglion.

Unusually large communication between T2 and T1

Fig. 1.50  The relations of the cervico thoracic (stellate) ganglion.

The Peripheral Nervous System: Gross Anatomy Fig. 1.51  The autonomic nerves in the chest and abdomen.

35

Common carotid a. Internal jugular v. Vagus n. Thoracic duct Subclavian v. Intercostal n.n.

Arch of aorta

Azygos v. Sympathetic trunk and ganglia Branches from sympathetic trunk to the greater splanchnic n.

Thoracic duct

Aorta

Greater splanchnic n.

Coeliac plexus Superior mesenteric plexus

Inferior mesenteric plexus

Superior hypogastric plexus

36

Surgical Disorders of the Peripheral Nerves Coeliac plexus

Superior mesenteric plexus Subcostal n. Iliohypogastric n. Inferior mesenteric plexus

Ilioinguinal n. Genitofemoral n.

Superior hypogastric plexus

Inferior hypogastric plexus and pelvic splanchnic n.

Fig. 1.52  The autonomic nerves in the abdomen and pelvis.

1.3.2 The Parasympathetic Nervous System The efferent outflow of the parasympathetic nervous system arises from nuclei in the mid-brain and part of the hind brain and the sacral part of the spinal cord. The pre-ganglionic fibres are distributed by the third, seventh, ninth and tenth cranial nerves and by the second to the fourth sacral spinal nerves. From the last arise the pelvic splanchnic nerves (nervi evigentes) which supply the ganglia in which the pre-ganglionic fibres relay are in or near the organs supplied. The effect of parasympathetic activity is inhibitory in the heart, motor to the muscle of the bladder and bowel and dilator in small vessels. The central control of both sympathetic and parasympathetic function is exercised from nuclei in the hypothalamus which themselves receive input from higher centres. The fibres from the hypothalamus almost certainly descend in a column in the lateral part of the white matter of the spinal cord (Nathan and Smith 1987). Parasympathetic fibres to the papillary and ciliary muscles pass with the oculomotor (III) cranial nerve via the ciliary ganglion, those to the lacrimal, submandibular and sublingual salivary glands travel with the facial (VII) cranial nerve via the submandibular ganglion. Those to the parotid gland are conveyed by the glossopharyngeal (IX) cranial nerve. The main visceral plexi are the cardiac, pulmonary oesophageal, coeliac, mesenteric and hypogastric (Fig. 1.52). They are fed from the cervical and cervico-thoracic ganglia, from the middle and lower thoracic ganglia (the thoracic splanchnic nerves), from the lumbar ganglia (the lumbar splanchnic nerves) and from the sacral ganglia. Both sympathetic and parasympathetic systems contribute to these plexi, the vagus (tenth cranial) nerve being the principal source of parasympathetic fibres to the chest and abdomen, and the second, third and fourth sacral nerves to the pelvis. The effect of efferent sympathetic activity is to cause sweating, to constrict small vessels and to cause contraction of the arrectores pilarum muscle. The visceral actions are to stimulate the action of the heart and to cause sphincteric contraction.

The Peripheral Nervous System: Gross Anatomy

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1.3.3 Afferent Autonomic Pathways Autonomic afferent fibres have their cells of origin in the dorsal root ganglia and in some cranial ganglia. Their peripheral processes run with efferent fibres, terminating in receptor endings in the walls of viscera and vessels. Impulses from these endings do not necessarily obtrude on consciousness, but evidently mediate sensations such as hunger, distension of the bladder and perhaps pain. Most, presumably, are concerned with the initiation of visceral reflexes. Schott (1994) re-examined the role of afferent autonomic pathways in the transmission of painful impulses, and has proposed a return to Langley’s (1903) concept of the unitary nature of the sensory system. In particular, he proposes the inclusion of autonomic afferents from the peripheral organs such as blood vessels with those from organs in the head, neck, thorax and abdomen under the general head “visceral afferents.” Edgar (2007) reviewed the considerable evidence showing that there is dual innervation to the lumbar intervertebral disc. The somatic afferent pathway enters the adjacent dorsal root segmentally via the sinu-vertebral nerves. The other pathway is non segmental and sends fibres through the paravertebral sympathetic chain which re enter through the thoraco lumbar white rami communicantes (Suseki et al. 1998). The nociceptor terminals from the spine have been mapped by Bucknill et al. (2002) by detecting sodium channels Nav 1.8 and Nav 1.9 which are associated with pain fibres. The afferent component of the enteric division is described by Furness (2006).

1.4 Nerves at Risk from Musculo Skeletal Injury The anatomical arrangements of some of the peripheral nerves make them particularly vulnerable to damage from skeletal injury. The sacral nerves are particularly at risk in fractures involving the sacral foramina. The proximity to bone of the main nerves at the elbow render all three vulnerable to skeletal injury (Fig. 1.53). The sciatic trunk is damaged by the posterior displaced head of the femur. Fleming et al. (2004) showed, by “video extensometry” that strain on the sciatic nerve was increased by 26% with the hip flexed to 45° and the knee extended. The course of the circumflex nerve is described by Coene (1985) “in the axillary region the nerve has a free course in loose fatty tissue, but when it turns around the subscapularis muscle, it is captured in a tunnel formed by the fascia of the subscapularis muscle cranially, the teres major muscle caudally and the coraco-brachialis muscle laterally. The fascii of these muscles join at the entrance to the quadrilateral tunnel, where they firmly surround the hitherto independent axillary nerve and posterior circumflex vessels which meet the nerve at this point. This neurovascular complex turns around the inferior border of the subscapular tendon, it passes cranially over the superior border of the teres major tendon, and enters a horizontal ‘tube’.” This arrangement puts the nerve at risk by forward displacement of the head of humerus and bleeding from the posterior circumflex vessels strangles the nerve. The radial nerve is at risk from fractures of the shaft of the humerus between the two relatively fixed points of the nerves to the lateral head of triceps and the tunnel through the inter muscular septum (Lambert 2005). The common peroneal nerve, which passes above or through the piriformis in as many as 30% of cases, is tethered above in relationship to the piriformis and below at the neck of the fibula. The fascia surrounding the biceps femoris muscle and tendon sweeps around to embrace the nerve. The deep peroneal nerve passes rather acutely forward to enter the anterior compartment of the leg. Sleeves of fascia surround main nerves and main vessels in some regions, an arrangement which predisposes the nerve to injury from ischaemia or compression or both, from bleeding. The anterior primary rami of C7, C8, and T1 are enclosed in quite a rigid space after they enter the posterior triangle of the neck. This is bounded, posteriorly, by the dorsal part of the first rib, the transverse processes of the cervical vertebrae and by the fascia of the levator scapulae muscle. The nerves are embraced by the scalenus anterior and scalenus medius muscles, both of which are invested in an unyielding fascia. This is one envelope of the prevertebral fascia which also serves to bind the phrenic nerve down to the anterior face of scalenus anterior. The prevertebral fascia is particularly well developed in front of the vertebral column and also at the base of the posterior triangle where it envelops C7, C8, and T1, the phrenic nerve, the cervical sympathetic chain, and the subclavian and vertebral arteries. Infusion of relatively large volumes of fluid, from 10 to 20 mL, deep to the prevertebral fascia for the

38

Surgical Disorders of the Peripheral Nerves

purpose of inducing regional block may cause tamponade of the radicular vessels which enter the spinal canal and contribute to the anterior spinal artery. Wilbourn (2005) has described the medial brachial fascial compartment which extends from the axilla to the elbow, and is bounded by the tough medial intermuscular septum and the axillary sheath. Wilbourn suggests that bleeding into this compartment is responsible for the majority of infraclavicular plexopathies following regional block and possibly for many of the neurovascular injuries which result from closed or penetrating missile injuries into this region. The anterior interosseous nerve and its accompanying artery may be damaged by compression because of swelling in the deepest part of the flexor compartment of the forearm. The ulnar nerve is accompanied by the ulnar artery, in a discrete fascial compartment in the distal two-thirds of the forearm. Donaghy (2005) suggests that the femoral nerve is more seriously damaged by haematoma where it passes deep to the thick fascia over the iliacus muscle. The nerve is especially at risk from bleeding into the femoral triangle (Fig. 1.54). The deep peroneal nerve is accompanied by the anterior tibial artery, an end artery, throughout most of the anterior compartment of the leg. The tibial nerve is accompanied by the posterior tibial artery in the distal one-half of the leg in a sheath of fascia similar to the arrangements for the ulnar vessels and nerve. The collateral circulation at the knee is particularly poor (Figs. 1.55 and 1.56).

Superior ulnar collateral a.

Brachial a.

Radial recurrent a.

Common interosseous a.

Anterior ulnar recurrent a.

Radial a.

Ulnar a.

Fig. 1.53  The collateral vessels at the elbow accompany the nerves. They must be compromised if the nerves are injured. The specimen is the left elbow.

Anterior interosseous a.

The Peripheral Nervous System: Gross Anatomy

39

Fig. 1.54  The femoral nerve and vessels deep to the inguinal ligament. The drawing shows the left inguinal region.

Lateral femoral cutaneous nerve Inguinal ligament Femoral nerve Femoral branch of genitofemoral nerve Iliacus m. Femoral artery Femoral vein Femoral canal Pectineus m. Psoas major m.

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Surgical Disorders of the Peripheral Nerves

Fig. 1.55  The collateral circulation about the knee is poor. The drawing shows the left knee.

Descending genicular a. Articular branch of descending genicular a. Saphenous branch of descending genicular a. Medial superior genicular a.

Descending branch of lateral circumflex femoral a.

Lateral superior genicular a.

Common peroneal n.

Patellar tendon

Lateral inferior genicular n.

Medial inferior genicular a.

Circumflex fibular a.

Anterior tibial a.

Anterior tibial recurrent a. Deep peroneal n. Superficial peroneal n.

a

Superior lateral genicular a.

b

Superior medial genicular a. Popliteal a. Popliteal a.

Superior lateral genicular a. Inferior lateral genicular a.

Anterior tibial a. Anterior tibial a.

Inferior lateral genicular a.

Tibiofibular trunk

Inferior medial genicular a.

Fig. 1.56  The popliteal and the anterior tibial arteries. Lateral view (a) (left) posterior view (b) (right). In this specimen the anterior tibial artery passes above the popliteus muscle. Other variations are common. The specimen is the right knee.

The Peripheral Nervous System: Gross Anatomy

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References Beldner S, Zlotolow DA, Melone CP, Agnes AM, Jones MH (2005) Anatomy of the lateral antebrachial cutaneous and superficial radial nerves in the forearm: a cadaveric and clinical study. J Hand Surg 30A:1226–1230 Bhadra N, Keith MW, Peckham PH (1999) Variation of innervation of flexor digitorum profundus muscle. J Hand Surg 24A:700–703 Branovovacki G, Hanson M, Cash R, Gonzalez M (1998) The innervation pattern of the radial nerve at the elbow and in the forearm. J Hand Surg 23B:167–169 Bremner-Smith AT, Unwin AJ, Williams WW (1999) Sensory pathways in the spinal accessory nerve. J Bone Joint Surg 81B:226–228 Brodal A (1981) The spinal accessory nerve. In: Neurological anatomy. Oxford University Press, New York/Oxford, p 458 Brown H (2002) Anatomy of spinal accessory nerve plexus: relevance to head and neck cancer and atherosclerosis. Exp Biol Med 227:570–578 Bucknill AT, Coward K, Plumpton C, Tate S, Bountra C, Birch R, Sandison A, Hughes SP, Anand P (2002) Nerve fibres in lumbar spine structures and injured spinal roots express the sensory neurones specific sodium channels SNS/PN3 NaN/SNS2. Spine 27:135–140 Coene LNJEM (1985) Axillary nerve lesions and associated injuries. Thesis, University of Leiden Cooper S (1953) Muscle spindles in the intrinsic muscles of the human tongue. J Physiol 67:1–13 Donaghy M (2005) Lumbosacral plexus lesions. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy. 4th edn. Philadelphia, Elsevier, Chapter 56. pp 1375–1390 Edgar MA (2007) The nerve supply of the lumbar intervertebral disc. J Bone Joint Surg 89B:1135–1139 Fleming P, Lenehan B, Sankar J, Folan-Curran P, Curtin W (2004) One third, two thirds: relationship of the radial nerve to the lateral intermuscular septum in the arm. Clin Anat 17:26–29 Furness JB (2006) Novel gut afferents: intrinsic afferent neurones and intestinofugal neurones. Auton Neurosci 125:81–85 Furness JB, Costa M (1980) Types of nerves in the enteric nervous system. Neuroscience 5:1–20 Gardner E, Bunge RP (2005) Gross anatomy of the peripheral nervous system. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Saunders Elsevier, Philadelphia, pp 11–34 Gruber W (1870) Über die Verbindung des Nervus medianus mit dem Nervus ulnaris am Unterarme der Menschen und der Säugethiere. Archive Anatomie Physiologie Medizin (Leipzig) 37:501–522 Hughes RAC (2005) Disease of the fifth cranial nerve. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier Saunders, Philadelphia, pp 1207–1218, Chapter 49 Kampa RJ, Prasthofer A, Lawrence-Watt DJ, Pattison RM (2007) The internervous safe zone for incision of the capsule of the hip. J Bone Joint Surg 89B:971–976 Kierner AC, Zelenka I, Burian M (2001) How do the cervical plexus and the spinal accessory nerve contribute to the innervation of the trapezius muscle? Arch Otolaryngol Head Neck Surg 127:1230–1232 Lambert SM (2005) Further opinion: radial nerve palsy associated with fractures of the shaft of the humerus. Doi: 10.1302/0301-620X. 87B12.17720 Langley JN (1903) The autonomic nervous system. Brain 26:1–26 Langley JN (1926) The autonomic nervous system. Part 1. Heffer, Cambridge Last RJ (1949) Innervation of the limbs. J Bone Joint Surg 31B:452–464 MacAvoy MC, Rust SS, Green DP (2006) Anatomy of the posterior antebrachial cutaneous nerve: practical information for the surgeon operating on the lateral aspect of the elbow. J Hand Surg 31A:908–911 MacNicol MF, Kelly M (2002) Identification of the saphenous nerve at arthroscopy. Arthroscopy 14:312–314 Mahakkanukrauh P, Somsarp V (2002) Dual innervation of the brachialis muscle. Clin Anat 15:206–209 Mok D, Nikolis A, Harris PG (2006) The cutaneous innervation of the dorsal hand: detailed anatomy with clinical implications. J Hand Surg 31A:563–574 Nathan PW, Smith MC (1987) The location of descending fibres to sympathetic pre-ganglionic vasomotor and sudomotor neurones in man. J Neurol Neurosurg Psychiatry 50:1257–1262 Pereira MT, Williams WW (1999) The spinal accessory nerve distal to the posterior triangle. J Hand Surg 24B(3):368–369 Schott GD (1994) Visceral afferents: their contribution to “sympathetic-dependent” pain. Brain 117:397–413 Solan MC, Lemon M, Bendall SP (2001) The surgical anatomy of the dorsomedial cutaneous nerve at the hallux. J Bone Joint Surg 83B:250–252 Srinivasan R, Rhodes J (1981) The median-ulnar anastomosis (Martin Gruber) in normal and congenitally abnormal fetuses. Arch Neurol 38:418–419 Standring SM, Bunting S (2000) The fibre content of the spinal accessory nerve. Personal Communication Suseki K, Takahishi Y, Takahishi K, Chiba T, Yamagata M, Moriya H (1998) Sensory nerve fibres from lumbar intervertebral discs pass through rami communicates. J Bone Joint Surg 80B:737–742 Tennent TD, Birch NC, Holmes MJ, Birch R, Goddard NJ (1998) Knee pain and the infrapatellar branch of the saphenous nerve. J R Soc Med 91:573–575 Tindall MA, Patel M, Frost A, Parkin I, Shetty A, Compson J (2006) The anatomy of the dorsal cutaneous branch of the ulnar nerve – a safe zone for positioning of the 6R portal in wrist arthroscopy. J Hand Surg 31B:203–205 Weddell G, Harpman JA, Lambley DG, Young L (1940) The innervation of the musculature of the tongue. J Anat 74:255–267 Wilbourn AJ (2005) Brachial plexus injuries. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier Saunders, Philadelphia, Chapter 55. pp 1339–1373

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The Microscopic Structure of the Nervous System: Its Function

The neurone and neurotrophins; transitional zone and roots; the Schwann cell and myelin; the connective tissue sheaths; conduction; axonal transport; blood supply; nervi nervorum; changes with aging; motor path with central and peripheral connections; sympathetic outflow; sensory path with superficial and deep peripheral connections and with central connections; the role of visceral afferents; neurotransmitters. The essential component of the system is the nerve cell with its dendrites and its prolongation, the axon (Figs.  2.1–2.3). Young (1945) characterized the axon as “a very long cylinder of a semi fluid nature.” It is a column of neuronal cytoplasm, the axoplasm enclosed by a cell membrane, the axolemma. Thomas et  al. (1993a) described the axoplasm as a “fluid cytosol in which are suspended formed elements.” The most conspicuous of the latter is the cytoskeleton consisting of neurotubules, neurofilaments and matrix. In addition, there are mitochondria, axoplasmic reticulum, lamellar and multivesicular bodies, and membranous cisterns, tubes and vesicles. It is the cytoskeleton that provides the apparatus for axoplasmic transport. Berthold et al. (2005) describe the axolemma as a three-layered unit membrane about 8  nm thick and consider that it: “conveys signals between the neurone and its Schwann cells that control the proliferative and myelin

producing functions of the Schwann cells and partly regulate axon size.” The glial cells of the peripheral nervous system are essential for the development, maturation, survival and regeneration of the neurone. The relationship between the axon and the Schwann cell is lifelong. The myelinating and non myelinating Schwann cells are the main peripheral glial cells. There are others, which include the satellite cells surrounding cell bodies in the dorsal root and autonomic ganglia, the glia of the enteric system; the teloglia (terminal Schwann cells) at the terminals of somatic motor axons and the glia associated with sensory terminals such as the Pacinian corpuscle. Mirsky and Jessen (2005) observe: “evidence to date suggests that the molecular and morphological differences between these various cells depend on the specific location and cellular environment in which they are found and that the glial cells of the PNS retain unusual plasticity throughout

Fig. 2.1  Cultured human dorsal root ganglion neurone immunostained for Gap 43 (growth associated protein) showing the cell body and neurites arising from the cell body, x40 (Courtesy of Dr. Uma Anand).

Fig. 2.2  Phase contrast image of a single DRG neurone showing the large rounded cell body, x63 (Courtesy of Dr. Uma Anand).

R. Birch, Surgical Disorders of the Peripheral Nerves, DOI: 10.1007/978-1-84882-108-8_2, © Springer-Verlag London Limited 2011

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Surgical Disorders of the Peripheral Nerves

2.1 The Neurotrophins 2.1.1 Nerve Growth Factor

Fig.  2.3  Cultured human DRG neurones immunostained for Gap 43 (green) and for the vanilloid receptor TRPV1 (red), the nuclei of satellite cells are stained blue (DAPI). Bar = 25 mm (Courtesy of Dr. Uma Anand).

life.” King (Berthold et al. 2005) estimated that about 10% of nuclei within the endoneurium of a normal peripheral or spinal nerve root are fibroblasts, and that endogenous macrophages account for between 2% and 9%. Most of the remainder are Schwann cells. Whilst mast cells are also seen their function is not well understood. “Neuron theory” Cajal (1954) asserts that “the neuron, a nerve cell with its processes, is the structural unit of nervous tissue, and the neurons are the only elements in the nervous system which conduct nervous impulses” (Brodal (1981b)). There is no continuity between nerve cells: the termination of the axon on a cell is no more than a contact, a contact to which Sherrington (1897) gave the name, synapse. Brodal (1981b) goes on: “not only is the neuron a structural unit; it also, in most cases, behaves as a trophic unit”; but the neurone itself requires trophic support during maturation and for survival after injury to the axon (Fig. 2.4).

Fig. 2.4  NGF immuno reactivity in neurones in a human dorsal root ganglion which was avulsed from spinal cord six weeks earlier. Immuno reactivity, identified by green fluorescence staining, is localized to cells of the small type. The yellow intracellular granules are lipofucsin deposits which exhibit auto fluorescence. Indirect immunofluorescence method, x50 (Courtesy of Professor Praveen Anand).

Cajal (1928) proposed that there was no autogenous regeneration of the peripheral stump. His belief in the presence of some neurotrophic factor in the distal stump is expressed in the phrase “The penetration into the peripheral stump implies a neurotrophic action, or the exercise of electrical influence by the latter.” He named contact guidance “tactile adhesion.” Young (1942) seemed to conclude that “successful nervous regeneration must depend mainly on the chances provided for adequate numbers of outgrowing fibers to establish connections resembling their original ones.” A hint of belief in neurotrophins had, however, been given in his work with Holmes (Young and Holmes 1940). It was during the 1940s that Hamburger and his colleagues (Hamburger and Keefe 1944) showed that the removal of a limb bud from a chick embryo led to a reduction in the number and size of the neurones destined for that limb whereas addition of extra target tissue during embryonic development was followed by an increase in the number and the size of the relevant neurones. “These observations led directly to the discovery of nerve growth factor (NGF)” (Windebank and McDonald 2005). Levi-Montalcini et  al. (1954) and Cohen et  al. (1954), described an agent found in mouse sarcomata which markedly promoted growth in the sympathetic and posterior root ganglia of chick embryos. They found that treatment with snake venom enhanced the activities of this agent, and that snake venom itself contained a potent growth promoting agent. The results of partial purification and characterisation of this nerve growth factor (NGF) were presented and suggested that the active material was a protein or bound to a protein. Levi-Montalcini and Angeletti (1968) indicated the specific action of NGF on sensory and sympathetic nerve cells: “the control exerted by the NGF on sensory and sympathetic nerve cells stands out by virtue of the magnitude of its effects, its target specificity, and the plurality of its actions.” Windebank and McDonald (2005) defined growth factors as “soluble extracellular macromolecules that influence the proliferation, growth and differentiation of target cells by a cell surface receptor mediated mechanism.” Most neurotrophins are polypeptides which are produced in ­tissues such as skin or muscle from whence they are transported to the neuronal cell body by the fast centripetal component of axonal transport. Three major families of growth factors are recognized. 1. The classic neurotrophins include nerve growth factor (NGF), brain derived nerve factor (BDNF) and the neurotrophins 3–7 (NT3, 4, 5, 6, 7). NGF is produced by cells including keratinocytes, melanocytes, vascular and smooth muscle cells, testis and ovarian cells, and endocrine and exocrine tissue. NGF interacts with the high

The Microscopic Structure of the Nervous System: Its Function

affinity ­receptor p140 tyrosine receptor kinase (TrkA) which is expressed by sympathetic neurones and by small diameter neurones in the dorsal root ganglia. After nerve injury, cells in other tissues, including Schwann cells and fibroblasts, synthesize and release NGF. Mice experimentally engineered to be deficient in TrkA do not develop thermoceptive or nociceptive neurones. BDNF apparently supports the development of motor neurones and their survival after axonotomy. After nerve transection, BDNF messenger RNA increases in muscle and the messenger RNA of one of the receptors to this nerve growth factor, tyrosine receptor kinase B (TrkB) increases in motor neurones. Neurotrophin 3(NT3) is mainly expressed in muscle spindles, Merkel cells and the Golgi tendon organs. This neurotrophin specifically binds to tyrosine receptor kinase C (TrkC). Mice which have been genetically engineered to lose this receptor lack proprioceptive organs. 2. Other neurotrophins are synthesized by the glial cells. It is likely that these factors support the embryonic midbrain and motor neurones in the spinal cord. The glial derived nerve factor (GDNF) binds with its high affinity receptor, also the tyrosine kinase receptor c-Ret. The ciliary neurotrophic factor (CNTF) first binds to its receptor and also the leukemia inhibitory factor receptor beta (LIFR ß). CNTF supports neurones in the ciliary ganglion, dopaminergic neurones, retinal rods and sympathetic and motor neurones. 3. The third family include the insulin growth factor (Igf) which structurally resembles insulin and binds with the tyrosine kinase IGF-I receptor, which is itself homologous to the insulin receptor. This receptor is expressed throughout the nervous system. Nerve growth factors are synthesized by the target organs of the nerves and are conveyed centrally to the neuronal cell bodies. This transport ceases after axonotomy. The interruption of this flow contributes to cell death amongst central neurones, an effect which is more severe in the immature nervous system and after axonotomy close to the neuronal cell bodies (Figs. 2.5 and 2.6). Anand and his colleagues have extensively investigated neurotrophic factors and their receptors in the normal human nerve, and in nerves affected by diabetes, leprosy, and injury. These studies have been extended to neurones from human dorsal root ganglia, (Anand et  al. 1996, Bar et  al. 1998,Saldanha et al. 2000, Yiangou et al. 2000, Durrenberger et  al. 2004, Chessell et  al. 2005, Facer et  al. 2007). More recently, Uma Anand and her colleagues have perfected methods in vitro for the study of living neurones from human dorsal root ganglia and this has permitted close study of the effects of neurotrophins and molecular mechanisms. (Anand et al. 2006, Sanchez et al. 2007, Anand et al. 2008a, Anand et al. 2008b, Anand et al. 2008c) Anand et al. (2006) summarize the effect of neurotrophin factors on the morphology and expression of some receptors in cultured human dorsal

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Fig. 2.5  Brain derived neurotrophic factor (BDNF) immunoreactivity in medium sized neuronal cell bodies and associated axons in human dorsal root ganglion 6  weeks after avulsion of spinal nerves, x40 (Courtesy of Professor Praveen Anand).

Fig. 2.6  Glial derived nerve factor (GDNF) receptor Cret immunoreactivity in neuronal cell bodies of human dorsal root ganglion two weeks after avulsion of spinal roots, x40 (Courtesy of Professor Praveen Anand).

root ganglion sensory neurones: the factors NGF, NT3 and GDNF are produced by peripheral target tissues such as epidermal keratinocytes and affect the phenotype of cultured sensory neurones. In the mature nervous system neurotrophins switch from providing trophic support for neuronal survival to maintenance of a specific neuronal phenotype thereby facilitating modality specific sensory function. For example GDNF and NGF regulate the normal function of two distinct classes of nociceptors via their receptors Ret and TrkA respectively. The levels of these factors are altered by injury. Administration of NGF induces thermal and mechanical hyperalgesia, it is upregulated by inflammation and plays a key role in the pathophysiology of nociception (Figs. 2.7–2.10). Evidently, important questions regarding the role of neurotrophic factors both in regeneration of peripheral nerves and in causation of pain and cutaneous hyperaesthesia and

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Fig. 2.7  Neurotrophin 3 (NT3) immunostaining in suprabasal epithelial cells of human glabrous arm skin, x40 (Courtesy of Professor Praveen Anand).

Surgical Disorders of the Peripheral Nerves

Fig. 2.10  Subepithelial fascicles of NGF positive axons in the tongue of patient with burning mouth syndrome (BMS), x40 (Courtesy of Professor Praveen Anand).

hyperalgesia are raised by the continuing work in this field. Although trials using factors for the treatment of amyotrophic lateral sclerosis and diabetic neuropathy failed, their therapeutic roles continue to be explored and developed.

2.2 The Peripheral Nerve Fibres

Fig. 2.8  Nerve growth factor (NGF) immunostaining of basal epithelial cells in human glabrous arm skin, x40 (Courtesy of Professor Praveen Anand).

Fig. 2.9  GDNF immunoreactivity in Schwann cells of healthy human sural nerve, x150 (Courtesy of Professor Praveen Anand).

In the central nervous system the neurones are supported in a network of oligodendrocyte and astrocyte processes, with very little extracellular space. The structure of peripheral nervous tissue is one of nerve fibres (axons – Schwann cell units) suspended in a collagen rich extra cellular space (Berthold et al. 1984, 1993). The transition from central to peripheral nervous structures takes place in the rootlets or less often in the roots of the spinal nerves. This is the transitional region or transitional zone (TZ). The development of the transitional region in dorsal rootlets was described by Carlstedt in 1981. The extension of CNS structure into the base of the rootlet is cone-shaped. Thus, “each transitional region can be subdivided into an axial CNS compartment and a surrounding PNS compartment” (Berthold et al. 1993) (Figs. 2.11 and 2.12). The myelin sheath distal to the transitional zone is formed by the transitional Schwann cell and that central to it by the transitional oligendendrocyte. The basal lamina of the axon remains continuous through the TZ. Some myelinated nerve fibres become nonmyelinated centrally. Fraher (2005) states that during development: “the CNS-PNS interface oscillates and continually changes its form and position as the two tissue classes establish their mutually exclusive territories.” The astrocyte barrier, which is at first flush with the glia limitans becomes pushed

The Microscopic Structure of the Nervous System: Its Function

peripherally by the central tissue process. Myelination is delayed in the transitional zone and that in the proximal rootlet segment lags behind the rest of the root. The ventral root

47

of the rat has a rich blood supply unlike the dorsal root; in the cat the blood vessels do not accompany the axons in the dorsal root, instead they deviate from the endoneurial space and join vessels on the surface of the cord. Fraher suggests that this arrangement causes the dorsal roots to be more susceptible to ischemia than ventral roots. His findings that the mechanical arrangements lead to rupture at the rootlet rather than in the transitional zone has been confirmed in the human by Schenker (Schenker and Birch 2001) who examined biopsies of the tips of avulsed roots in 12 patients by light and by transmission electron microscopy. Of the ten biopsies taken within 4 weeks of injury the level of rupture was central to the TZ in two of the roots and peripheral to it in the remaining eight (Figs.  2.13 and 2.14). Schenker also studied the corpora amylacea (CA), round homogenously staining

Fig. 2.11  Morphology of the normal human spinal cord. A transverse light microscopic section at C7 showing a ventral root. A single large root in transition is demonstrated with central islands of autolysed glia. Numerous corpora amylacea are seen on the central side of the transitional zone. Toluidine blue, x100 (Courtesy of Editor Journal of Bone and Joint Surgery [British]).

Fig. 2.13  Transverse section of the tip of an avulsed dorsal root at C6 4 days after injury showing a central avulsion. The tissue in the centre of the section is CNS tissue in which glial cells show post traumatic lytic changes. Corpora amylacea are indicated by arrows. Toluidine blue, x100 (Courtesy of Editor Journal of Bone and Joint Surgery [British]).

Fig. 2.12  Normal anatomy of the transitional zone. Schwann cell processes are seen above, astrocyte processes lie closely to an unmyelinated axon (arrows) which is surrounded by a basal lamina(arrow head) Electron microscopy by Michael Kayser, Institute of Orthopaedics (Courtesy Michael Schenker).

Fig.  2.14  Avulsed ventral root of C6 4 days after injury showing a peripheral intradural rupture. The nerve tissue at the site of the rupture showed no CNS features. The tip is covered by organized blood clot and erythrocytes which interweave with fibrin strands. The myelinated fibres show early signs of Wallerian degeneration. Toluidine blue, x200.

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Surgical Disorders of the Peripheral Nerves

bodies 15–50 mm in diameter, which are found in the subpial zone of the spinal cord in post mortem material. The CA mark the watershed between the central and the peripheral nervous systems. The basal lamina surrounding the Schwann cell – axon unit extends into the spinal cord and cannot be used as a reliable indicator of peripheral nervous tissue. Most of the fibres of the ventral roots have their cells in the ventral horn of the grey matter. They can, perhaps, be regarded as outposts of the peripheral system in the central system. The fibres of the dorsal roots have their cells in the dorsal root ganglion: possibly, outposts of the central in the peripheral nervous system? These neurones are “unipolar in form with a single axon and no true dendrites” (Thomas et  al. 1993b). Each axon bifurcates into peripherally and centrally directed axons after leaving the cell body at a variable distance from the cell. The centrally directed branch is of smaller caliber than the peripheral one. The central processes enter the spinal cord along the posterolateral sulcus. In the cord the fibres bifurcate into ascending and descending branches. The branches of the smaller fibres in the lateral part of the root reach the dorsal horn of the grey matter, where both soon terminate having traversed between three and five segments. The branches of the larger fibres in the medial part of the root, mostly myelinated, similarly bifurcate after entering the white matter just medial to the dorsal horn. Some ascending fibres reach as high as the gracile and cuneate nuclei in the caudal part of the medulla. Other fibres of this group have short ascending and descending branches which enter the grey matter of the dorsal horn to establish synapses with nerve cells in its different laminae (Fig. 2.15). Sherrington (1894) showed that ventral roots of cats and monkeys contained intact myelinated nerve fibres after

transection of both the ventral and dorsal roots and he concluded that some afferents reached the spinal cord the “wrong way” through the ventral roots. Unmyelinated afferent fibres certainly enter the spinal cord in the ventral roots (Coggeshall et al. 1974). They may be concerned with the transmission of painful impulses (Clifton et  al. 1976) though White and Sweet (1969) failed to produce pain in man by stimulation of ventral roots. On the other hand, Brindley (1986) described three paraplegic patients who experienced pain whilst stimulating the ventral roots of S2 and S3 or of S3 and S4 to induce micturition by an implanted stimulator. Brindley says: “the Bell-Magendie law is certainly nearly true, but on published evidence it seems likely that it is not exactly true,” pointing out that pain could be evoked by antidromic impulses in efferent fibres. We were able to take advantage of the opportunity offered by intradural damage to nerves of the brachial plexus to demonstrate the presence of afferent fibres in the ventral roots of man. Stephen Gschmeissner examined by electron microscopy the ventral root of the eighth cervical nerve avulsed with its dorsal root and found with it at operation for exploration of the plexus in the posterior triangle of the neck. He found several surviving small myelinated and unmyelinated axons (Fig. 2.16). Clearly, the cell bodies of these axons must have been in the nerve or in the dorsal root ganglion; the fibres must have belonged to the afferent system. These findings were confirmed by Schenker (Schenker and Birch 2000) who examined biopsies from the tip of the avulsed rootlets in nine patients. The tips of the dorsal and of the ventral rootlets of 5 spinal nerves were examined within 8 days of injury, the other patients were operated at intervals ranging between 4 and 50 weeks from injury. Schenker found intact myelinated fibres in all ventral root specimens. The majority of those Direct ascending tract Lissauer’s tract I

Lateral corticospinal tract

X

II III IV V VI VII VIII

Fig. 2.15  The paths of the afferent fibres entering and efferent fibres leaving the spinal cord. Note (right) the laminae of the grey matter.

IX

Crossed ascending tract

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Fig. 2.16  Afferent and efferent fibres in the ventral root. Large healthy myelinated axons in the ventral root of the 8th cervical nerve avulsed from the spinal cord 6 weeks previously. The myelinated efferent fibres have undergone Wallerian degeneration and there is much collagenisation (Electron microscopic study by Mr. Stephen Gshmeissner, x5000).

identified in the later biopsies were regenerating, perhaps signifying collateral sprouting from the intact cell bodies of the adjacent avulsed dorsal root ganglion. There were a small number of intact fibres in the early specimens and Schenker suggests that: “it is therefore likely that these few fibers of the ventral root represent afferent fibers in continuity with the cell body in the DRG.” Less than 5% of the central processes of all dorsal afferents survive the traction injury and it was assumed that “wrong way” ventral afferents do just the same so that the few surviving ventral root afferents that were observed may represent only a very small proportion of the population. Based on this assumption Schenker proposed that the proportion of afferent fibres in the ventral root of man is similar to that found by Loeb (1976) who, by microelectrode recordings in cats, calculated that 3.9% of all afferent fibres reached the cord through the ventral root (Fig. 2.17). In the peripheral nervous system the axons are closely associated with the Schwann cells (Schwann 1839). Sanders (1942) established the central role of Schwann cells in regeneration through grafts: “autografts remain alive and myelin fragmentation and Schwann multiplication go on very much as in a normal peripheral stump.” Sanders rejected methods of repair which do not enrich the environment with Schwann cells. Schwann cells arise from the neural crest, from the same cells that differentiate into peripheral neurones; they provide essential trophic support to the neurone during development and also during regeneration. Our present understanding of the part played by these cells in repair owes a

great deal to the work of Susan Hall of Guy’s Hospital, and now editor of Gray’s Anatomy. (Hall 1997, 1999, 2001, 2005, Li et al. 1998) (Fig. 2.18). Mirsky and Jessen (2005) described how two important growth factors, neuregulin 1 and endothelin regulate early Schwann cell development. The Schwann cell separated from its axon survives for rather longer in the mature than in the immature nervous system. The most important component of the basal lamina is laminin which interacts with receptors in the plasma membrane of the Schwann cell which include the integrins and alphadystroglycan. Laboratory mice which have been genetically engineered to produce defective laminin or a defective receptor for laminin, develop profound nerve pathology and muscle dystrophy (Uziyel et al. 2000). Schwann cells provide another important protein, the tumor suppressor protein, Merlin (schwannomin), which links membrane proteins to the actin cytoskeleton in epithelia and other cell types. Mutations in the gene controlling Merlin lead to an increased frequency of schwannomas. In leprosy, components of the cell wall of M.leprae interact with laminin 2, the major isoform of laminin, and this interferes with the normal interaction between laminin and alphadystroglycan leading to demyelination and to axonal degeneration. During myelination Schwann cells radically transform their phenotype in response to signals from the larger axons; as Mirsky and Jessen (2005) say: “this response represents one of the most striking examples of cell-cell interaction that is known.”

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Surgical Disorders of the Peripheral Nerves

Fig. 2.19  A large myelinated nerve fibre within the posterior root of a 7th cervical nerve which had been avulsed from the spinal cord six weeks previously. The axoplasm contains neurofilaments and a few microtubules. The Schwann cell cytoplasm it is enveloped by a well defined basal lamina. There are processes from fibroblasts from within the endoneurium, x16,200. Fig. 2.17  Rupture of the ventral root of C5 peripheral to the transitional zone examined 5 months after avulsion. Two thinly myelinated axons are seen. x 17,000 (Electron microscopic study by Mr. Michael Kayser, Institute of Orthopaedics. By courtesy editor Journal of Anatomy).

Fig. 2.18  In vitro cultures of mouse DRG neurones and Schwann cells. The Schwann cells are immunostained for S100 (red) the neurones for nerve growth factor (green), x50 (Courtesy of Professor Susan Standring).

Scherer and Arroyo (2002) provide an extensive review of the molecular organisation of myelinated axons. The larger axons are enwrapped along their length by a continuous series of contiguous Schwann cells into which they are invaginated. The nodes of Ranvier represent the points of contiguity of adjacent Schwann cells (Fig. 2.19). The fibre is contained within a basal lamina. The basal lamina separates nerve fibres from the endoneurial space and it runs without interruption from the central nervous system to the termination of the axon. Thomas (1963) defined this structure in an electron microscope study. Schwann cells are surrounded by a basal lamina approximately 250 Å in thickness which is separated from the plasma membrane of the Schwann cell by a gap of 250 Å. The endoneurium is organized in two layers which surround the basal lamina. The inner layer is composed of collagen fibres of smaller diameter than those in the outer layer which run longitudinally, circularly and obliquely. This layer is inflected at the nodes with the basement membrane. The outer layer consists solely of longitudinal collagen fibres and it is not inflected at the node. Bunge et  al. (1986) considered the basal lamina essential in the linkage

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51

Fig. 2.20  Clusters of unmyelinated axons (long arrows), enveloped by Schwann cell cytoplasm. Short arrows indicate basal lamina, x26,220.

between the Schwann cell and the axon and with the extracellular matrix. The smaller fibres are contained in bundles by columns of Schwann cells. Eames and Gamble (1970) showed the ensheathing arrangement of successive Schwann cells which overlapped and interdigitated: the Schwann cells of unmyelinated axons in these nerves give off multiple cytoplasmic processes, which form close relationships with axons, with other processes, and with bundles of collagen. A ramifying “network” system of Schwann processes is thereby present throughout the endoneurium.

Eames and Gamble recognize areas of specialisation of the Schwann membranes which consisted of “a short length of increased plasma membrane thickness and electron density.” Later studies using scanning electron microscopy and freeze fracture replication have generally confirmed these earlier observations (Stolinski and Breathnach 1982). It is at times very difficult to distinguish between a nonmyelinated axon and a Schwann cell process in histological sections of regenerating peripheral nerves! (Fig. 2.20). The diameter of the axon is one important factor which determines whether the Schwann cells will lay down a myelin sheath around it. Webster (1993) proposes that the sheath is laid down in spiral layers by the Schwann cell, or part of its surface, moving around the axon (Webster 1993). The multilamellar sheath has a high lipid content and some protein components. Suter and Martini (2005) say that the major component of the protein components of myelin is Po myelin protein zero (MPZ), which accounts for 50–60% of all myelin protein. Peripheral myelin protein 22 (PMP 22) comprises from 2% to 5% of myelin proteins and mutations of the controlling gene lead to inherited myelin disorders. Suter and Martini comment that mutation of this gene was: “the first identified culprit gene for inherited neuropathies of Charcot-Marie Tooth (CMT) type.” Myelin basic protein

(MBP) accounts for 5–15% of myelinated proteins. The myelin associated glycoprotein (MAG), which forms no more than 0.1% of the myelin proteins, may play a pivotal role during myelination because of its early expression and because of its location to the axon-Schwann cell interface. Mice genetically engineered to be deficient in MAG showed extensive axonopathy and degeneration of myelin in motor fibres. The myelin sheath is traversed by cytoplasmic channels – the incisures of Schmidt-Lanterman (Hall and Williams 1970) (Fig.  2.21). The meeting points of consecutive Schwann cells are the nodes of Ranvier. These are short, about 1 micron in length and the axon here is constricted,

Fig. 2.21  A widened Schmidt-Lanterman incisure in a teased mouse sciatic nerve. Normal saline in vitro, x100 (Courtesy of Professor Susan Standring).

52

free of myelin but enveloped by projections of Schwann cytoplasm. The node is bordered by an adjacent paranode, which is dilated and which contains an increasing amount of mitochondrial rich Schwann cell cytoplasm outside a more or less crenated myelin sheath. Berthold et al. (2005) characterize the node thus: “these parts of the myelinated nerve fibers, the paranode-node-paranode (PMP) regions, constitute, structurally as well as functionally, the most spectacular parts of a myelinated nerve fiber.” The PMP regions are responsible for the generating and propagation of the action potential and they are the centers for activity in the early phases of Wallerian degeneration and collateral sprouting (Figs. 2.22–2.24). The axon-myelin sheath–Schwann cell complexes are arranged in bundles otherwise known as fascicles or funiculi. In so small a nerve as the fourth cranial there may be as many as 3,400 fibres. In the roots inside the spinal canal endoneurial collagen is scanty in contrast with the abundant content in the nerves outside the foramen (Gamble 1964; Eames and Gamble 1964) The surgeon who has had dealings with nerves inside and outside the spinal canal will appreciate the distinction: the spinal roots and rootlets are fine and fragile and very susceptible to trauma; the peripheral nerves are strong and have much greater resistance to handling. Outside the intervertebral foramina the three supporting structures, epi, peri, and endoneurium are clearly established. The epineurium, in effect the prolongation of the dural sleeve of the nerve roots, is composed of longitudinally directed collagen fibres, fibroblasts and fat cells. (Gamble and Eames 1964). The perineurium, which ensheaths the bundles, is composed of flattened cell processes alternating with layers of collagen. It provides a barrier to diffusion (Thomas 1963). The perineurium is strong; the intrafascicular pressure can be raised to more than 300  mmHg before it ruptures (Selander and Sjostrand 1978). The contents of the perineurium are under tension so that when it is cut they are extruded, rather like

Fig. 2.22  Node of Ranvier, mouse sciatic nerve in vivo, oblique incident illumination, x400(Courtesy of Professor Susan Standring).

Surgical Disorders of the Peripheral Nerves

toothpaste. This is most clearly seen on the day of injury in nerves which have been transected or ruptured and it is one of the indications that the level of section of the stump is adequate. The outflow rapidly diminishes over the course of several days. In the endoneurium, supporting the fibres

Fig. 2.23  Longitudinal section through a node of Ranvier, showing a remyelinated heminode (left) adjacent to a normal heminode (right). Compare the complexity of the paranodal fingers of the normal myelin sheath with the simple arrangement of the paranodal loops of the thinner, remyelinated sheath, x5,000 (Courtesy of Professor Susan Standring).

Fig.  2.24  Double immunostaining of sural nerve showing nodes of Ranvier (black) stained with antibodies to junction adhesion molecule (JAM – c) and axons (red) stained with antibodies to neurofilaments, x40 (Courtesy of Professor Praveen Anand).

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53

themselves, there is a return to longitudinal direction of cells and fibres; there are abundant collagen fibrils (Thomas 1963; Gamble and Eames 1964). Stolinski (1995) describes the epineurium as an outer layer of alveolar connective tissue and a more compact inner layer containing collagen and elastic fibres which are arranged in a wavy pattern. Perineurial cells are also arranged in a wavy manner and Stolinski suggested that the spiral bands of Fonata represent the wavy or zig zag organisation of nerve fibres. These arrangements provide a degree of protection to the nerve against traction. The nerve can be stretched by as much as 20% before the wavy arrangement is converted into a linear array. Tillett and her colleagues (2004) offer the concept of a distinct core and sheath in the rat sciatic nerve, and proposed that the interactions between the core and the sheath involve physical connections rather than a viscous fluid interface. The anatomical features of this interface were characterized using transmission electron microscopy and it appeared that the sheath was derived from the epineurium and most of the perineurium, whilst the core consisted of the endoneurium and a small proportion of perineurium: the plane of cleavage involved the innermost perineurial cell layer. A normal peripheral nerve trunk exposed at operation is enveloped in a well defined translucent envelope. This is the external epineurium (Fig.  2.25). Normal nerve trunks are easily distinguished from other longitudinal structures by the appearance of white spiral bands on their surface, the spiral bands of Fontana (Clarke and Bearn 1972, Stolinski 1995). The individual bundles or fascicles are seen within. These are enclosed by the perineurium with some condensation of the innermost epineurium forming a white, opaque layer (Fig.  2.26). The tissues surrounding the bundle form the epineurium, rather loose in texture, and rich in blood vessels which pass longitudinally along the axis of the nerve. However, the observer will see adventitial material outside the epineurium which is more clearly defined in some nerves

than in others and in different locations within the limb. There are, for example, translucent connective tissue arcades accompanying the median nerve in the forearm where it passes between the superficial and the deep flexor muscles of the fingers. Such vessels provide an alternative collateral pathway to the part; they also supply the nerve trunk so permitting the use, for example, of the ulnar nerve as a free vascularized graft. This tissue plane not only conveys vessels to the nerve but it also permits gliding of that nerve across joints and against the adjacent tissues. Thomas (1963) has estimated that 45% of nuclei seen in transverse sections of nerves are those of fibroblasts. Sunderland (1968) mapped the arrangement of bundles along the course of nerve trunks, showing branching, fusion and changes in number. He further showed that the cross-sectional area of the nerve occupied by connective tissue was variable, ranging from 60% to 85% (Fig. 2.27). These findings, especially those concerning re-arrangement of bundles, have been used to cast doubt on the feasibility of achieving accurate co-aptation of the ends of divided nerves. However topographical organisation is one essential quality of the nervous system and this is shown by the considerable topographical segregation of neurones involved in the somatic afferent pathways in the dorsal root ganglia, dorsal horn of the spinal cord, the thalamus and the sensory cortex. Perhaps predictably injury anywhere in the nervous system provokes considerable reorganisation. Sunderland himself recognized that there was a degree of topographical segregation of nerve fibres according to function over considerable lengths of the median and ulnar nerves. Micro­neurographic studies (Torebjörk and Ochoa 1980) confirmed these findings. Specific organisation (aggregation) of sensory and motor fibres occurs in the median nerve in the arm, so it does in all peripheral nerves. This segregation permits transfers such as that of Oberlin et  al. (1995), in which one bundle of the ulnar nerve

Fig. 2.25  The extrinsic epineurial vessels of the ulnar nerve, x40.

Fig. 2.26  The bundles and epineurial vessels of the ulnar nerve after displacing the adventitia, x40.

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Surgical Disorders of the Peripheral Nerves

Fig. 2.27  Sural nerve undergoing Wallerian degeneration 4 days after a proximally sited crush lesion showing macrophages stained positively for ED1, x100 (Courtesy of Professor Susan Standring).

is anastomosed to the nerve to the biceps. Stimulation of individual bundles, whose number ranges from 6 to 12, permits separation of those passing to the flexor muscles of the wrist and fingers from those passing to the small muscles of the hand. The ability to “map” the stump of a divided nerve allied to the ease of matching individual bundles by their size and disposition is but one of the great advantages of urgent repair of nerves (Fig. 2.28).

2.2.1 Conduction The special property of the nerve fibre is that of conducting a signal in the form of a propagated action potential (Landon 1985). Rasminsky (1985) opens the subject thus: “Nerve fibres are specialized processes of nerve cells that have the unique property to propagate action potentials, the currency of information in the nervous system.” The action potential is a brief, self propagating reversal of membrane polarity and it depends on an initial influx of sodium ions which cause a reversal of polarity to about +40  mV followed by a rapid return towards the resting potential as potassium ions flow out. In the unmyelinated fibre, a wave of depolarisation spreads continuously along the axon, attenuated by the large capacitance of the axolemma, which limits the velocity of conduction to about 1m/s. Standring (2008) likens this to: a flame moving along a fuse. Just as each segment of the fuse is ignited by its upstream neighbor, each segment of axon membrane is driven to threshold by the depolarization of neighboring membrane. Sodium channels within the newly depolarized ­segment

open and positively charged sodium ions enter, driving the local potential inside the axon towards positive values. This inward current in turn depolarizes the neighboring, downstream, non depolarized membrane, and the cyclic propagation of the action potential is completed.

The action potential is evoked by a stimulus which exceeds threshold by the all or nothing law of Adrian (1928); the cell body, on the other hand, responds in a graduated manner to stimuli transmitted across synapses which either inhibit or facilitate by raising or lowering the threshold respectively. In the myelinated fibre the myelin sheath acts as a capacitor and limits radial resistance at the internode, so that most of the current flows axially along the fibre. It is, says Bostock (1993) “powered by inward ‘kicks’ of inward membrane current at the nodes of Ranvier.” This method of “saltatory” conduction was so named by Tasaki and Takeuchi (1941; 1942), and further confirmed by Huxley and Stämpfli (1949). The myelin sheath thus enables the fibre to conduct rapidly without the necessity for a very large increase in axonal diameter. The caliber of unmyelinated axons varies from 0.4 to 1.25 mm (Gasser 1955); that of myelinated fibres from 2 to 22 mm (Ranson 1915; Greenfield and Carmichael 1935; Sunderland et al. 1949). The largest, fastest conducting elements are the myelinated fibres of around 20 mm diameter concerned with somatic afferent and efferent activity; the smallest and slowest conducting are the fibres of around 1 mm diameter that subserve autonomic activity and delayed pain sensibility (Galbraith and Myers 1991). Conduction velocity ranges from about 0.7 m/s in small unmyelinated fibres to about 80 m/s in the largest

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Fig. 2.28  Fascicular arrangement of nerve fibres and their supporting structures, the vascular systems of the peripheral nerve.

Epineurium Extrinsic vessel

Perineurium

Endoneurium Regional feeding vessel

Unmyelinated fibres

Node of Ranvier

Schwann cell nucleus

Myelin sheath

Axon

Myelinated fibre

56

myelinated fibres. Omer (1980) gives a range of 40–75 m/s in large myelinated fibres. The electrical changes associated with the wave of depolarisation can be measured through electrodes placed on the skin over the nerve, on the nerve, in the nerve or in individual fibres. These reactions form the basis for electrophysiological examination and for microneurography.

2.2.2 The Basis of the Action Potential: Ion Channels Hodgkin and Huxley (1939) made the first intracellular measurements of the resting potential across the cell membrane in the unmyelinated giant axon of the squid. In 1952 Hodgkin and Huxley described the cycle of depolarisation and repolarisation which underlies the high speed transmission of nerve action potentials and showed that the reversal of polarity was brought about by the influx and efflux of sodium and potassium ions across the axon membrane through individual parallel pathways which are controlled by independent gating particles or charges. Conduction of an action potential was blocked by pressure or by cold (Hodgkin 1937a, 1937b) Chiu (2005) defines the ion pathways, now known as channels: “voltage gated ion channels are like membrane lodged proteins that mediate rapid ion flux (106 ions/s) across cell membranes.” Chiu describes some of the methods that have been developed to define these entities. The patch clamp technique permitted study of the electrical events associated with the opening and the closing of a single ion channel. Later came the cloning of ion channels which permitted the recognition of 50 potassium channel genes and 10 sodium channel genes (by 2005). Later still the pore structure of potassium channels was studied by x-ray crystallography at a resolution of between 2.4 and 3.2 Å. Scholz, Reid, Vogel and Bostock (1993) were amongst the first to study, by patch clamping, sodium and potassium channels in the human nerve. The voltage-gated sodium ion channels are uniformly distributed along the membrane of nonmyelinated axons but they are densely concentrated at the nodes of Ranvier in the myelinated nerve axons. The potassium channels, on the other hand, are concentrated in the membrane at the juxta paranode. Ion channel function is energy dependent, it is ATP driven and this function is curtailed or altogether blocked by anoxia. Distortion of the myelin sheath adjacent to the node of Ranvier may unmask the potassium ion channels to such an extent that prolonged conduction block ensues. Evidently, demyelination is bound to lead to decrease of conduction velocity (McDonald 1963; McDonald and

Surgical Disorders of the Peripheral Nerves

Sears 1970) and eventually to conduction block. These facts will not escape the attention of the clinician faced with an ischaemic limb or with a deepening nerve lesion caused by expanding haematoma or entrapment. Once again we are indebted to Praveen Anand and his colleagues who have provided us with illustrations of sodium and potassium channels in the normal and in the injured nerve. Their extensive studies on the behavior of the ion channels in the injured nerve and in painful lesions of nerves are described in Chaps. 3 and 12. One of their observations reveals an important difference between the immature and the mature peripheral nerve in the human. Two voltage-gated sodium channels, Nav 1.8 and Nav 1.9 play a key role in neuropathic pain. The sodium channel Nav 1.9 could not be demonstrated in the nerves of infants (Yiangou et al. 2000) (Figs. 2.29 and 2.30).

Fig. 2.29  Sodium channel staining normal sural nerve, x40 (Courtesy of Professor Praveen Anand).

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Fig. 2.30  Nerve fibres within the mucosa and submucous plexus in human rectum stained with antibody to Protein Gene Product 9.5 (PGP9.5), a pan neuronal marker, x10 (Courtesy of Professor Praveen Anand).

2.2.3 Axonal Transport The axon functions as part of the neurone as a whole in transporting materials to and from the cell body. Lasek (1982) goes further than this: neurones exhibit a remarkable form of locomotion when they extend axons over great distances without moving the cell body. This capacity of neurones to extend axons independently of the movement of the perikaryon is one of the distinctive properties of the neuronal linkage because it distinguishes neurones from other migratory cell types.

Lasek (1982) further proposes that the unusual feature of neurones – their ability to translocate the axonal skeleton independently of the perikaryon – is accomplished by the continuous addition of cytoskeletal proteins at the proximal end of the cytoskeleton in the perikaryon. So, the neurone is able to extend its process “without towing the cell body along.” Ochs and Brimijoin (1993) define axonal transport as: “a system of intra cellular motility enabling nerve cells to deliver essential proteins and membrane components to the periphery, and to receive from these chemical signals and materials for disposal.” Two forms of transport, fast and slow, are recognized (Brimijoin 2005). The former may be orthograde (centrifugal) or retrograde (centripetal). The fast retrograde (centripetal) component conveys material to the cell body in microvesicles at the rate of 150– 300  mm/day. The fast orthograde (centrifugal) component

transports proteins, peptides, and neurotransmitters from the cell body at a rate of 200–400 mm/day. All systems are ATP dependant, and the microtubules are critical for fast axonal transport. Landon (1985) puts it this way: fast transport “is concerned with the orthograde transport of particular constituents of the axoplasm and materials such as some transmitter synthesizing enzymes, glycoproteins and membrane components, and the retrograde transport of membranous prelysosomal structures, and extra cellular materials such as nerve growth factor ingested at the axon terminal.” The process is sensitive to temperature; it is sensitive to deprivation of oxygen. Slow transport is uni-directional, orthograde (centrifugal). Rates of transport are from 1 to 4 mm daily; it is concerned with the transport of the neurotubule-neurofilament network of the cytoskeleton. Brimijoin recognizes two distant components: 1. Slow component A (SCa averaging about 1 mm/day) 2. Slow component B (SCb averaging 2–10 mm/day) The rate of transport of the SCa component is of course about the same as the rate of peripheral regeneration after axonotomy. The significance of axonal transport in disorders of peripheral nerves is plain: interference with the centrifugal process is likely to lead to defect or cessation of conduction; interference with the centripetal process will ultimately lead to degeneration of the nerve cell.

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2.2.4 The Blood Supply of Nerves Nerves have a very good blood supply: they need it. The surgeon notes the segmental blood supply from without and the axial vessels within the nerve. There are indeed (Lundborg 1979,1988) intrinsic epineurial perineurial and endoneurial plexuses, and extrinsic regional vessels in the “paraneurium.” These form “separate but extensively interconnected microvascular systems” providing a wide margin of safety. As McManis and colleagues (1993) remark: “these anastomotic vessels confer a resistance to ischemia in peripheral nerves so that nerve suffers functional or structural changes only when there is widespread vascular or microvascular damage.” Dyck et al. (2005) show that arterioles and small arteries are detectable only in the epi- and perineurium, and that these vessels may range in diameter from 50 to 400 mm. The arteries penetrating the perineurium are small, only rarely do they exceed 15  mm in diameter and small arteries are rarely detectable within the endoneurium. Lymphatics have not been detected within the perineurium. The endothelial junctions of the endoneurial vessels are tight, unlike those in the epineurium (Low 1976). Some nerves are better supplied than others. Kadiyala and his colleagues (2005) showed that the common peroneal nerve at the knee has far fewer extrinsic vessels than the tibial nerve at that level. Seddon (1975) commented on the extent to which it was permissible to mobilize the nerve in order to facilitate suture. His rather sanguine views of the effect on the blood supply are not confirmed by the later injection studies of Bell and Weddell (1984); indeed, later clinical experience has shown that it is preferable to bridge a gap by interposition than by mobilisation.

Surgical Disorders of the Peripheral Nerves

Weerasuriya (2005) proposed the concept of a “bloodnerve interface” instead of the “blood-nerve barrier.” Weerasuriya comments: “the structure of the perineurium combines features of the dura mater in terms of mechanical strength and the arachnoid with respect to impermiance.” Endoneurial fluid is in contact with the cerebro-spinal fluid through the subarachnoid angle. Flow is proximal to distal, the hydrostatic pressure of cerebro-spinal fluid is 10 mmHg, it is 3.5  mmHg in the dorsal root ganglion and it drops to between 1 and 2  mmHg within the peripheral nerves. Endoneurial hydrostatic pressure (EHP) rises in the aged nerve and it is possible that external pressure increases EHP by obstructing flow. This may be one factor underlying the effect of entrapment or compression. Hill and Hall (1999) suggest that the aggregation of Renaut bodies at sites of potential entrapment represents a response to local injury to the endoneurial capillaries. The blood supply to the roots of the spinal nerves is much less robust (Figs.  2.31a–c and 2.32). Two distinguished Cambridge anatomists, Woollam and Millen (1958), considered that: “man has just as much nervous system as he can supply with oxygen and no more.” The most important spinal vessel, the anterior spinal artery, was studied in the fetus and in the guinea pig and rat. Relatively few radicular arteries survived into adult life, the average number of those so doing was eight. Two of these seemed to be particularly important: a cervical vessel, arising from the vertebral artery and entering into and sustaining the anterior spinal artery at C6, C7 or C8, and the artery of Adamkiewicz 1881a,b, in the upper lumbar region. Figure 1 in Woollam and Millen’s paper shows, in a 24 week human fetus, that the radicular vessel adjacent to

Fig. 2.31  The dorsal vessels to the spinal cord and cauda equina: (a) upper thoracic segment (b) thoraco lumbar junction, (c) cauda equina.

The Microscopic Structure of the Nervous System: Its Function

a

59

b

Fig. 2.32  Resin cast of the blood vessels of the neck, seen from the front (a) and from the side (b). The arteries are shown red, the veins blue showing the segmental arrangement of vessels. The anterior spinal artery is shown (arrow) with an important segmental feeder vessel.

the seventh cervical nerve was the major supplier for the anterior spinal artery (Fig.  2.33). Dommisse (1974, 1975) confirmed that the number of radicular arteries (which he termed the medullary feeders) reinforcing the anterior longitudinal arterial channel was eight and that those reinforcing the dorsal arterial columns were 17. Only 8% of those passing to the cervical spinal cord arose from the vertebral artery. The pattern was variable: “but the principle of a rich supply for the cervical and lumbar enlargements was confirmed” (Dommisse 1975). In the 6 drawings from cadaver dissections a total of 12 vessels are described, 4 of these at the level C6, C7 and 4 more at C4. The anterior spinal artery is the most important of the longitudinal channels. Its central branches, which are end arteries, supply about two-thirds of the cross-sectional area of the cord. The rest of the dorsal grey and the white columns are supplied by branches arising from the dorsal arterial system. Occlusion of the anterior spinal artery leads to the catastrophe of infarction of the anterior cord, the anterior spinal cord syndrome. The significance of damage to major feeder arteries is emphasized by the work of Svensson (2005) who addressed the risk of severe cord lesion after aortic surgery. Svensson achieved a rate of paralysis of 3.8% on patients most at risk, those with complex thoracoabdominal aneurysms, by a number of measures which included: “sequential segmental repair with repositioning and moving the clamp upon the grafts sequentially downwards

and reattaching intercostal and lumbar arteries.” Disruption of the radicular arteries entering the spinal canal with the spinal nerves which form the brachial plexus probably underlies the partial Brown Séquard syndromes which are seen in cases of avulsion. Occlusion of flow through those vessels by tamponade explains the catastrophe of spinal cord infarction or even death complicating spinal nerve or interscalene block.

2.2.5 The Nervi Nervorum Curiously but perhaps predictably, nerves have their own nerve supply in the shape of the nervi nervorum, derived from their own fibres. There are free endings in the epi-, peri- and endoneurium, and some encapsulated endings of Pacinian type in the endoneurium. (Hromada 1963). These are probably one factor underlying the exquisite sensitivity of nerves trapped in fibrosis after operations for “entrapment” neuropathy.

2.2.6 Changes in Nerves with Ageing Corbin and Gardner (1937) examined the dorsal and ventral roots of the eighth and ninth thoracic spinal nerves of 34

60

Surgical Disorders of the Peripheral Nerves Posterior spinal aa.

Posterior segmental medullary a. Spinal branch Anterior segmental medullary a.

Posterior segmental medullary a. Spinal branch Anterior segmental medullary a.

Anterior spinal a.

Fig. 2.33  The segmental medullary (radicular) arteries and the anterior spinal artery in the lower cervical cord (after Woollam and Millen 1958).

cadavers whose ages ranged from 1 day to 89  years. The highest number of myelinated fibres, found in persons in their second and third decades, was 187% larger than that found in the nerves of a 1 day old infant. They found that after the third decade there was a gradual loss of myelinated fibres, up to 32% for the person of 89 years. Cottrell (1940) examined the median, femoral, sciatic and common peroneal nerves of 30 persons coming to necropsy at ages ranging from 3 h to 81 years. She found changes in the vessels and the connective tissue, with “alteration and loss of the nerve fibers.” Ochoa and Mair (1969) examined portions of the sural nerves of seven volunteers aged 5–59, and were the first to show that active destruction of unmyelinated fibres started early in life, whereas loss of myelinated fibres was found only in the 59-year-old. Tohgi and colleagues (1977) examined the sural nerves of 79 persons coming to necropsy after “acute death,” whose ages ranged from 1 week to 88 years. The average density of small myelinated fibres decreased rapidly from the age of 1 week (26,300/mm2) to the second decade (9,560/mm2), and continued to decrease gradually with age, to reach at the eighth decade an average of 74% of that at the second decade. There seems to be an error in the printing of the figure for the eighth decade. Large myelinated fibres appeared first in an infant aged 3 months. Their density increased rapidly, to reach at 3 years the level found in the young adult. The average of the

third decade was 6,480/mm2; at the ninth decade it was 3,480/ mm2. In this extensive study there is mention of the ageing changes in the vasa nervorum and the perineurium. Jacobs and Love (1985) made a qualitative and quantitative study of 27 sural nerves obtained within 24 h of death from human subjects without history of disease or of ingestion of drugs known to affect peripheral nerve. Densities of myelinated and unmyelinated fibres decreased from birth to the end of the eighth decade, because of increasing size and separation of fibres during the first decade, and an increase in endoneurial collagen in the older persons. Also, the slope of the internodal length-fibre diameter increased progressively during the first decade, but then remained virtually constant until the age of 60. Then, degeneration, regeneration, demyelination and remyelination caused increasing variation in internodal length. Thomas et al. (1993b), summarising previous findings, refer to “mild peripheral neuropathy” of older humans. Norris and colleagues (1953) examined age changes in the maximum conduction velocity of motor fibres of the ulnar nerves of 175 ambulatory male patients, employees and staff members of the Baltimore City Hospitals. There was steady reduction in conduction velocity from the third to the ninth decade. They canvassed possible causes for this regression. Taylor (1984) studied the effects of age on conduction and amplitude in motor and sensory fibres of adult nerves. He indicated that tables of normal data of the rise and

The Microscopic Structure of the Nervous System: Its Function

fall of conduction and amplitude could be constructed for use in clinical investigation. Kimura (1993) stated that: “nerve conduction velocities are roughly half the adult value in fullterm infants, but increase rapidly, reflecting the process of myelination, to the adult value at age 3–5 years.” He noted the slow decline of conduction velocity after the fourth decade, and drew attention to the contemporaneous increase of the latencies of the F wave and somatosensory evoked potentials. Cowen et al. (2005) describe the greater vulnerability with increasing age of large, long, myelinated nerve fibres, and of larger sensory neurones. There also appears to be selective vulnerability of some autonomic neurones, notably within the enteric system. Evidence is provided to support the proposal that “interactions between sensory neurones and their receptor targets are crucial initiators of an age related nervous deterioration.” These changes must evidently concern clinicians treating the very young and the rather old: in the former, they may have a bearing on diagnosis; in the latter, they may be relevant to the susceptibility of a nerve or nerves to damage by pressure or traction.

61 V

Re

V

C Re Ru

2.3 The Somatic Motor System The motor pathway begins in the neurones in the pre-central gyrus of the cerebral cortex. Their axons pass by the internal capsule to the mid-brain and to the pyramids of the medulla. From each side most fibres cross the mid line at the decussation of the pyramids to descend in the lateral part of the white matter of the cord as the lateral corticospinal tract. At various segmental levels impulses from this tract activate, through internuncial neurones, the motor cells in the anterior part of the grey matter (Fig. 2.34). “Extrapyramidal” tracts from the red nucleus, the vestibular nuclei and the reticular formation also influence the activity of the ventral horn neurones. Brodal (1981c) prefers to discard the designation “extrapyramidal,” on the grounds that “those cortical regions which give rise to fibers in the pyramidal tract also give rise to fibers to a number of nuclei which project further caudally….” The cell bodies of the motor neurones are in Lamina IX (Rexed 1954) of the ventral horn of the grey matter. There are large (alpha) and small (gamma) cells (Fig. 2.35). They are acted on by primary sensory fibres and by fibres descending from the cortex and from nuclei in the brain stem. The axons from the large cells are destined for the extrafusal fibres. By correlating the distribution of paralysis with the sites of loss of cells in the ventral horn, Sharrard (1955) was able to show how the cells were grouped in the grey matter. Broadly, the medial group supply the muscles of the trunk and neck; the lateral group supply the muscles of the limbs.

Fig. 2.34  The major descending tracts in the spinal cord and their overlapping zones of termination in the grey matter. C corticospinal, V vestibulospinal, Re reticulospinal, Ru rubrospinal.

Thus, cells of the latter group are present chiefly in the cervical and lumbar enlargements, whereas those of the medial group are found throughout the length of the cord. Nathan and Smith (1958) studied the spinal cord in patients who had earlier undergone cordotomy, and defined the descending

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Fig. 2.35  Motor neurone cell bodies in the ventral horn of human spinal cord stained with antibodies to TRPV 4, a novel ion channel, x40 (Courtesy of Professor Praveen Anand).

pathways for the control of the bladder: “in man, the majority of descending fibers concerned with micturition lie in the lateral column, on an equatorial plane passing through the central canal. This location remains the same in the cervical, thoracic, lumbar and sacral segments.” The distribution of nerves within the muscles of the upper limb has been described by Lim and his colleagues (2004). The staining technique of Sihler was used which renders muscle translucent and stains the myelin in the nerves a dark blue. The intramuscular distribution of the nerves was then mapped by photographing the superficial and deep surfaces of the muscle using a back light technique. In flat, triangular or trapezoid muscles (class 1) the main nerve runs perpendicular to the muscle fibres giving off side branches that run parallel with them. The spindle shaped or fusiform muscles (class 2) were subdivided into unipennate or bipennate muscles. In the bipennate muscles the aponeurosis of the tendon splits the muscle into two compartments and in these the primary nerve divided into two secondary branches passing each side of the tendon. In muscles with more than one head of origin (class 3) the pattern of innervation is more complex. The pattern of innervation is determined by three factors: “the shape of the muscle, its position and orientation in relation to the passage of the nerve, and the muscle tendon morphology.” These findings support the idea of transfer of part of a muscle and they emphasize the requirement for the repair of intramuscular nerves in lacerated muscles. Contact with, and transmission to muscle is effected through the motor end-plates (see Fig. 2.42). There are two components of each end plate: neural and muscular. They are separated by a cleft of about 30 nm. The muscular soleplate contains a number of muscle cell nuclei; it is not itself

Surgical Disorders of the Peripheral Nerves

contractile. There are two types of neural endings: the en plaque terminal on extrafusal (alpha nerve fibre) muscle fibre, and the plate endings on intrafusal (gamma nerve fibre) muscle fibres. Transmission at en plaque endings initiates action potentials which are rapidly conducted to all parts of the muscle fibres, whereas transmission at plate endings of “trail” and “en grappe” types excites the fibres at several points. Acetylcholine released at the nerve ending interacts with receptors to produce depolarisation of the muscle membrane and trigger the action potential in the muscle. The ventral roots from the first thoracic to the second lumbar segments of the spinal cord contain also the efferent pre-ganglionic fibres of the sympathetic nervous system: those of the second to fourth sacral nerves contain the efferent pelvic parasympathetic outflow.

2.4 The Somatic Sensory System The afferent pathways of the peripheral nervous system considerably exceed the efferent pathways in numbers and in complexity of organisation. By no means all lead to conscious sensation. Amongst the somatic afferents the Golgi organs and the muscle spindles are examples; the whole array of the visceral afferents is one more.

2.4.1 Cutaneous Sensibility The long debate about the mechanism of cutaneous sensibility begun by Blix (1884) and Goldscheider (1884) and continued by von Frey (1894, 1896), Head et  al. (1905), Head and Sherrin (1905), Head (1920),Adrian and Zotterman (1926), Adrian (1928), Zotterman (1939), Weddell (1941), Sinclair (1955) and many others is now drawing to its close: as Iggo (1985) remarks “the long-standing argument of ‘specificity’ versus ‘pattern’ in the operation of cutaneous receptors has been settled in favor of the ‘specificity’ hypothesis.” Iggo also states that: “it is now clear that no cutaneous receptors have an absolute specificity; they have a high degree of selective sensitivity, that is, a much reduced threshold to one form of stimulation” (Fig.  2.36). Adrian pioneered methods in Cambridge in the 1920s (Adrian and Zotterman 1926) which enabled electrophysiological studies of single afferent units. This led to work with microelectrodes and with intraneural microstimulation done by, among others, Hallin and Torebjörk (1973), Torebjörk and Ochoa (1980), Vallbo and Hulliger (1981) Hagbarth et  al. (1993), and Torebjörk Schmelz (2005). However, as Wall

Fig. 2.36  Cutaneous sensory receptors: glabrous skin (left) and hairy skin (right). Aα Aδ C

‘G’ unit ‘D’ unit Cutaneous (C) unit

Aδ/C

Aα

Field receptor

Thermoceptors

Aα

Lanceolate

Aδ/C

Aα

Aα

Aα

Aα

Paciniform

Type II (Ruffini)

Type I (Merkel)

Vibrissa

Nociceptors

Rapidly adapting mechanoreceptors

Slowly adapting mechanoreceptors

Hairless skin

Aα

Aδ/C

Aα

Meissner

Thermoceptors

Aα

Pacinian

Aδ/C

Aα

Type II (Ruffini)

Nociceptors

Aα

Type of ending: Type I (Merkel)

Type of fibre:

Rapidly adapting mechanoreceptors

Slowly adapting mechanoreceptors

The Microscopic Structure of the Nervous System: Its Function 63

Hairy skin Guard hair Down hair

Touch dome

64

(1961) pointed out: “specific modality and patterning theories are supplementary. The recognition of receptor specialisation for transduction of particular kinds and ranges of cutaneous stimulation does not preclude acceptance of the concept that information is coded in a pattern of impulses.” Mountcastle (1980) assigns to the specialized receptors a role as transducers responsible for amplification. He points out that in areas of skin subjected to sensory testing and later marked and excised, histological examination has shown only free nerve endings. No specialized mechanosensor transducers transmitting through unmyelinated fibres have been identified yet; the same is not so for nociceptors and most thermoreceptors, where the transient receptor potential (TRP) channels have been identified as transducing specific ranges of temperature. All these receptors seem to be represented in fine branching unmyelinated nerve endings in the cell layers of the epidermis (Fig. 2.37). The basis of stereognosis is a combination of stimuli from skin, tendons, muscles and joints relaying sensory information centrally where comparison is made from memories of movement. The role of movement is vital: a blindfolded person cannot identify the nature of a material if it is simply placed on the finger. Identification is aided if the material is drawn across the finger tip. Recognition is, however, immediate if the subject is allowed to create temporal and spatial patterns by feeling the texture between the moving finger and thumb (Melzack and Wall 1962). The fibres of afferent neurones are classed by their conduction velocity. Afferent fibres from the skin are divided into A-ab, A-d and C; muscle afferents are classed I, II, III and IV (Light and Perl 1993, Lawson 2005). There is some correlation between fibre diameter and the characteristics of the soma within the dorsal root ganglion. These are classed as large light (neurofilament rich) and small dark (neurofilament poor) neurones.

Surgical Disorders of the Peripheral Nerves

Fig. 2.38  Small diameter nociceptor cell bodies from a human dorsal root ganglion 2 weeks after avulsion stained with antibodies for prostaglandin receptor sub type EP1, x40 (Courtesy of Professor Praveen Anand).

Fig. 2.39  Small diameter nociceptor cell bodies and axons in the human dorsal root ganglion immunoreactive for the heat and capcaicin receptor TRPV1 2  weeks after avulsion injury, x20 (Courtesy of Professor Praveen Anand).

The neurones of C-fibres are small; those with Ad fibres are small to medium size; those with A-ab fibres are medium to large (Lawson 2005) (Figs. 2.38 and 2.39).

2.4.2 The Skin The introduction of immunohistochemical staining of nerve antigens has provided new insights into innervation of the skin (Kennedy et al. 2005). Kennedy says: Fig.  2.37  PGP9.5 immunoreactive somatic nerves in skin of patient with small fibre neuropathy, x 40 (Courtesy of Professor Praveen Anand).

bundles of nerves enter the skin deep in the dermis and course towards the skin surface, giving off axons to innervate the associated end organs. Unmyelinated nerve fibers comprise the vast

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morphologically unidentified receptors responding to very slow displacement of hair or skin are innervated by small slowly conducting C fibres. The principal mechano-sensor in hairy skin is the hair follicle receptor; in hairless (glabrous) skin the two principal types are the Meissner corpuscle, rapidly adapting, and the Merkel receptor, slowly adapting. Beneath the skin the rapidly adapting organ is the Pacinian corpuscle; the slowly reacting organ is the Ruffini’s corpuscle which is found in deep dermal layers and is characterized by large diffuse receptive fields. The Ruffini corpuscles provide information about finger position by responding to stretching of the skin (Lundborg 2004b). Stark et al. (1998) studied the distribution of Pacinian corpuscles in the hand: the total number identified was around 300 and most were located in the pulp skin of the fingers. Fig. 2.40  PGP9.5 immunoreactive autonomic nerve fibres surrounding sweat glands in the skin of a patient with small fibre neuropathy, x40 (Courtesy of Professor Praveen Anand).

majority of cutaneous innervation to the above dermal structures. The few myelinated nerve fibers terminate at hair follicles, Meissner corpuscles and Merkel complexes. The vertically orientated nerve bundles form a horizontal sub epidermal neural plexus. Epidermal nerve fibers branch from this plexus and, while penetrating the dermal-epidermal basement membrane to enter the epidermis, they lose their Schwann cells ensheathment and collagen collar.

The sweat glands are carpeted by a dense pattern of autonomic nerves (Fig. 2.40). Fine unmyelinated nerve endings form a network covering larger arteries in the deep dermis. The density of innervation of the epidermis is greatest in the proximal segment of the limb. There is little change between the 20th and 80th year.

2.4.3 Cutaneous Sensory Receptors

2.4.3.2 Thermoreceptors So long ago as 1884 Blix postulated that there were two types of thermoreceptor in the human skin: one for cooling and one for warming. Cooling receptors are served by unmyelinated and fine myelinated fibres, usually serving receptor fields about 100 mm in diameter (Light and Perl 1993). They are very sensitive to decrease in skin temperature from the normal or “neutral” level of 30–35°C. Fowler and colleagues (1988) indicate a conduction velocity of up to 2.1 m/s. Davis and Pope (2002) found that the sensation of cooling is replaced by an ache below 17.5°C and by pain below 14°C. Warming receptors, less common than cooling receptors, have receptive fields of less than a millimetre in diameter. Warm sense is a function of unmyelinated fibres within the epidermis; as we have seen the TRP channels transduce specific ranges of temperature. Temperatures above 43°C induce firing in C-fibre polynociceptors. Temperatures above 53°C evoke responses in fast conducting myelinated mechano-heat fibres (Light and Perl 1993, Lawson 2005).

Three types of cutaneous receptor are defined: low threshold mechano-sensors; thermoreceptors; nociceptors. 2.4.3.3 Nociceptors 2.4.3.1 Low Threshold Mechanosensors The distinction is made between slowly adapting receptors responding to sustained displacement such as continuous pressure; rapidly adapting receptors responding to the beginning or withdrawal of a stimulus or by a moving stimulus, and receptors responding to brief mechanical disturbances such as vibration and tapping. The first group includes the Merkel cells; the second includes the Meissner corpuscles and the third, the Pacinian corpuscles. Most are innervated by large and medium sized fibres conducting at rates of from 20 to 90  m/s. A few

The term is applied to primary afferent units which “uniquely signal stimuli intense enough to threaten physical damage to the tissue” (Light and Perl 1993). Some respond to intense mechanical stimuli; some to strong thermal stimulation, and some are polymodal. Impulses travel in myelinated fibres in the Ad to Aab ranges and in unmyelinated C fibres. Nociceptor fibres are widely distributed in the skin, muscle, joints, the epineurium of trunk nerves and the wall of blood vessels as an extensive plexus of free nerve endings. These pass to fine myelinated and non myelinated fibres and also to the largest (Aab) fibres (Light and Perl 1993, Lawson 2005). Ad nociceptors are high threshold mechano-sensors.

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Some respond to damaging heat. They conduct impulses from receptive fields of about 5 mm2 at about 20 ms. Many of the C-fibres are polymodal, responding to a range of noxious stimuli including histamine and other chemicals, heat, cutting and crushing. C-fibres are responsible for the triple response of Lewis and they are the basis of the axon reflex. They are less than 2 mm in diameter and conduct at between 0.5 and 2  m/s from fields which range from 1 to 10  mm2. Microneurography has clarified the physiological characteristics of the nociceptors in humans. Sharp, well localized pain follows stimulation of Ad afferents. Stimulation of single C-afferents induces dull, burning, poor localized and delayed pain (Torebjörk and Ochoa 1980). Head (with Rivers and Sherrin in 1905) observed two types of pain after the division and suture of his own superficial radial and lateral cutaneous nerves of the forearm. There was epicritic pain which was sharp and localized and protopathic pain which was dull, burning, delayed and unpleasant. It is tempting to relate these two pain types to the now proven characteristics of the two main groups of nociceptors. The reader can experience the two modalities of pain by stimulating the skin on the front of the wrist with a sharp pin. First, and almost immediately, a sharp, well localized pain is experienced. A little later the delayed response–slightly unpleasant, a little longer lasting and a little diffuse – is felt. The A-ß and A-d nociceptors have punctate superficial receptive fields and respond to noxious mechanical or noxious mechanical and thermal stimuli (Mechano-heat units) (Lawson 2005).

2.4.4 Deep Sensibility Sensation is conveyed from muscles, ligaments and tendons from specialized receptors and from free nerve endings in those structures. The receptor organs are: in muscle, muscle spindles and free nerve endings; in tendons, the Golgi organs, and in capsules and ligaments various endings, some similar to Ruffini endings, Pacinian corpuscles and Golgi organs. There are also plexuses of unmyelinated fibres (Fig. 2.41). Joints are innervated by a network of rapidly conducting myelinated fibres some of which are associated with encapsulated mechanosensors and by high threshold, slowly conducting fibres many of which are perhaps nociceptors (Takebayashi et  al. 1997, Petrie et  al. 1997, Hogervorst and Brand 1998, Chen et al. 2000). Takebayashi et al. (2006) recognized sympathetic afferents innervating the lumbar intervertebral discs. Tomita et al. (2007) investigated the distribution of nerve endings in the human dorsal radio-carpal ligament by fluorescence immunohistochemistry, with confocal laser microscopy and by Kontron image analysis “to rebuild” the endings, so providing data about morphological characteristics as well as incidence, density and distribution.

Surgical Disorders of the Peripheral Nerves

2.4.5 The Muscle Spindles It is over a 100 years since Sherrington (1894) demonstrated by ventral root section that “in a muscular nerve-trunk from one-third to one-half of the myelinated fibers are from cells of the spinal root-ganglion.” The size of these fibres was from 1.5 to 20 mm; they were not the largest fibres in the nerve; the largest came from the ventral root. On the other hand, the largest of these fibers were larger than any fibres in the cutaneous nerves. “It was shown that about two-thirds of all the afferent fibers measure above 7 mm. Of these I imagine that considerably more than one-half may be apportioned to the muscle spindles, the majority of the rest belonging to Golgi’s tendon organs.” Sherrington found too that “the smallest myelinated fibers in the muscular nerve are for the most part, perhaps entirely, root ganglion fibers.” Sherrington further showed that there were “recurrent” (afferent) fibres in the ventral roots. He identified the special end-organs of the afferent fibres in the muscle-spindles (muskel-spindel) of Kühne (1864). Ruffini (1897), in his observations on sensory nerve endings in muscles, defined the “sensorial” end organs of muscle as (1) the muscle spindles; (2) the tendon organs (Golgi organs) and (3) the Pacinian corpuscles. He concluded: “in my opinion it is upon these three levels of sense organ that physiology must turn its attention if it will resolve the problem of the muscular sense.” Batten (1897) further examined the muscle spindle and its behavior in various pathological conditions including injury to the brachial plexus. Horsley (1897) noted their “preservation in conditions of extreme muscular atrophy.” Since Sherrington’s time, a very great deal of work has been done on the structure and function of the muscle spindles (Banks et al. 1982; Boyd 1962, 1966, Boyd and Smith 1984; Goodwin and colleagues 1972; Cooper and Daniel 1963; Matthews 1981). Their behavior after nerve injury and on their regeneration is described in Chaps. 3 and 4. Boyd and Smith (1984) state that “The whole human body must contain about 20,000 spindles, each of them a marvel of micro-engineering.” Most spindles lie deep in muscle near branches of its nerve or blood vessels. Each contains small muscle fibres (intrafusal fibres) within a cellular and connective tissue capsule. Banks (2005) says: “there are two principle kinds of encapsulated sense organs in skeletal muscle.… the tendon organ, which senses the force of contraction and the muscle spindle which responds to muscle length.” Both have a copious innervation by large afferent fibres and the muscle spindle and the Golgi tendon organ account for nearly all group 1 afferent axons from muscles. There are three types of specialized intrafusal muscle fibres: the nuclear bag fibres (bag 1, bag 2), with a central accumulation of nuclei, and nuclear chain fibres, smaller and with a single row of nuclei. The spindles vary in length from a few millimeters to a centimeter. Each spindle receives up to 25 terminal branches

The Microscopic Structure of the Nervous System: Its Function

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Ib afferent

Golgi tendon organ

Primary (annulospiral) Ia afferent

Secondary (flower spray) II afferent

Aα efferent Muscle sole plate

Aγ efferent Motor end-plate with synaptic vesicles Muscle spindle

Fig. 2.41  The afferent and efferent innervation of skeletal muscle.

Motor end-plate

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of motor and sensory axons, together with autonomic innervation. The motor axons are the b and g axons of the ventral root; the sensory axons are myelinated fibres of groups I and II. The combination of motor and sensory innervation is reflected in the complexity of the function of the spindles. The conception of a servo action is evidently too simple; rather, it is evident that the spindles play several roles in the “feedback” mechanism for regulating muscle contraction and for appreciation of body position. Stacey (1969) reckoned that in a “motor” nerve of the cat the distribution of fibres was one-third myelinated motor, one-third myelinated sensory and one-third unmyelinated sensory. Banks (2005) studied the nerve to the soleus muscle of the cat. The nerve contains 180 myelinated sensory and 270 myelinated motor fibres. Most of the myelinated afferents arose from 56 spindles and 45 tendon organs. There were 115 fusimotor gamma efferent fibres, which means that the 25,000 extrafusal skeletal muscle fibres are innervated by only one-third of the total of myelinated nerve fibres. The human longissimus capitis is the most densely spindled muscle and the density of muscle spindles is 25 times more in the lumbrical muscles than in the gastrocnemius (Cooper and Daniel 1963). The other afferent endings in skeletal muscle are free endings innervated by unmyelinated and small myelinated fibres. Iggo (1961) found that these responded to sustained pressure but not to stretch or contraction. They responded to hypertonic saline, but that stimulus was sufficient to excite the spindles too. Other studies of these organs and their afferent fibres were made by Mense and Schmidt (1974) and by Mense (1977) who studied the response to chemical noxious stimulation by single fibre recording. Pomeranz and colleagues (1968) traced fine myelinated afferents from viscera, muscle and skin to Lamina V of the dorsal horn of the spinal cord.

2.4.6 The Golgi Tendon Organs Scott (2005) characterizes the second of the two encapsulated mechano-sensors in muscle. The Golgi organ senses length of muscle and impulses project from it to the cerebellum and cortex. Stimulation of the fibres from the Golgi apparatus in hand muscles causes cortical potentials and “illusions of muscle stretch.” The Golgi organ is about 0.1 mm in diameter and between 0.2 and 1.5 mm in length. It contains collagen strands which continue into muscle fibres at one end and into the tendon at the other. There are between 3 and 50 of these organelles in each muscle, and Scott says that the ratio of Golgi organs to spindles is less than 0.3. The myelinated afferent fibre is a little smaller than the largest afferent from the muscle spindle, and in the cat it conducts at the rate of 60–110 m/s. The terminals interweave amongst the collagen strands as sprays or spirals. The capsule contains capsular cells which

Surgical Disorders of the Peripheral Nerves

are continuous with the Schwann cells. The receptor is slowly adapting; it responds to the whole range of muscle contraction and the firing rate is proportionate to active tension. In humans the fibres are silent at physiological rest and there are progressive steps in the firing rate with increasing steps in muscle contraction. Recovery is virtually complete after a crush lesion inducing axonotmesis, it is very much worse after repair of divided nerves. The poor recovery of the two main encapsulated mechano-sensors in muscle after repair of divided nerves may account for the common complaints of weakness, lack of stamina, and poor coordination and also for the failure of musculotendinous transfer using reinnervated muscles. As MacQuillan (2006) says: “the normal function of muscles is dependent on their sensory apparatus.” Up to now, most clinical work on sensation and on recovery of sensibility after nerve injury and repair has been directed to cutaneous sensibility. Yet function such as stereognosis and proprioception must depend principally on signals from endings in muscle, tendons and ligaments. It is perhaps inadequately appreciated that there may be good recovery of sensory function of the hand with very imperfect cutaneous reinnervation, and that pain is just as likely to follow damage to a “purely motor” nerve as it is to follow damage to a “mixed” or “sensory” nerve. There is in fact no such entity as a “purely motor” nerve, except perhaps for the hypoglossal or facial. The signals from the muscles supplied by those nerves probably proceed by other cranial nerves: the lingual in the case of the hypoglossal nerve and the trigeminal and the auricular branch of the vagus in the case of the facial nerve. There are indeed a few peripheral nerves without a cutaneous sensory component: the spinal accessory; the phrenic; the anterior and posterior interosseous; the deep branch of the ulnar; the suprascapular. The content of afferent fibres in all such nerves is about 30%. Laviano (1992/93) in his thesis on “transfer of the spinal accessory nerve for the suprascapular in avulsions of the brachial plexus” shows EM photographs of portions of the suprascapular nerve taken at operation as long as 94  days after injury (Fig.  2.42). There are numerous medium-sized and small myelinated fibres in good condition: evidently, the distal processes of dorsal root ganglia. Our work along the same lines also suggests a proportion of myelinated afferent fibres for the “motor” nerve of around 30%. Laviano’s work confirms the earlier supposition (Bonney 1959) that the dorsal root ganglion cells survive for a long time the interruption of their central processes. As to the last: in a case of extensive intradural damage to the plexus we examined a specimen of suprascapular nerve taken at the time of “neurotisation” well after the period required for degeneration, and found that it contained not less than 30% of myelinated fibres. It is perhaps best to drop the terms “purely motor” and “purely sensory,” and even drop the term “mixed” applied to nerves with both motor and cutaneous sensory components. The terms

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2.4.7 Central Connections

Fig. 2.42  Intact (afferent) myelinated and unmyelinated fibres in the suprascapular nerve after avulsion lesion of the brachial plexus. Specimen taken 6 weeks after injury, when efferent fibres had degenerated, x6,600(Electron microscopic study by Mr Stephen Gshmeissner).

“nerves with motor and cutaneous sensory components” and “nerves without somatic motor components” are, unfortunately, cumbersome, but they do say what they mean.

The great array of sensory receptors in the skin and deep tissues sends back to the centre the signals of the stimuli received. Most afferent fibres, with their cell bodies in the dorsal root ganglia, enter the cord by the dorsal roots. Others, with cell bodies in the dorsal root ganglia or actually in the ventral roots, enter the cord by the latter (Fig. 2.43). The first analysis of incoming signals takes place in the spinal cord and medulla where all fibres terminate. Most of the large myelinated fibres ascending in the dorsal columns terminate in the gracile and cuneate nuclei in the medulla. Some smaller fibres of the dorsal columns terminate and relay in the cord: these are the propriospinal fibres. Although the classical view of the function of the dorsal column has been challenged (Wall 1970) it is broadly true that, as Brodal (1981d) states, they “mediate sensory signals necessary for rather complex discrimination tasks” (Nathan et al. 1986). Other afferent fibres terminate and relay in the grey matter of the dorsal horn. Each lamina (Rexed 1952, 1954; Price and Meyer 1974) of the grey matter receives afferents of specific functional modalities; each has a particular neuronal structure. Small myelinated nociceptor and thermoreceptor fibres terminate in lamina I; C fibres, nocithermo- and mechanosensors, in lamina II (substantia gelatinosa). Larger mechano-sensor fibres terminate in laminae III and IV. These relay to cells whose axons either ascend in the dorsal columns or reach the dorsal column nuclei by the dorsolateral fasciculus. Some fibres pass through the dorsal horn to relay with the large cells in the motor apparatus in lamina IX. Some unmyelinated and small myelinated fibres enter the dorsolateral fasciculus (Lissauer’s tract) just lateral to the tip of the dorsal horn to join fibres from cells in the substantia gelatinosa. Direct ascending tract

Lissauer’s tract Lateral corticospinal tract

III IV V VI

II

Dorsal root ganglion

I

X VII VIII

Fig. 2.43  The laminae of the grey matter with direct ascending, crossed ascending and internuncial tracts.

Crossed ascending tract

IX

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Surgical Disorders of the Peripheral Nerves

Fig. 2.44  Ascending tracts in the cord, brain stem and cortex. Note the relay of the directly ascending tracts in the gracile and cuneate nuclei in the medulla (after Brodal 1981a).

Leg

Trunk

Gyrus post. centr. Arm Caps. int. Face

Pes. pedunculi Nucl. ruber Subst. nigra Nucl. sens. princ. n. v.

Nucl. vent. post. lat. thalami (VPL) Mesencephalon

Pons Lemn.med.

Nucl. fun. gracil. Nucl. fun. cun. N. tract. spin. n. v. Tr. sp. cereb. dors. Tr. sp. cereb. ventr.

Med. obl. Tr. spinothal.

Med. spin.

Some fibres cross the midline to terminate in laminae I and V of the contralateral dorsal horn. There is a complex network of interconnecting fibres in the dorsal horn and in the substantia gelatinosa in particular. Sensory input is first analyzed and modified here. Secondary neurones in the dorsal horn give rise to fibres which ascend or descend for a few segments in the cord. They give rise principally to the fibres that, crossing the midline, ascend in the long tracts in the anterolateral segment of the spinal cord (Fig. 2.44). The transmission of impulses from the nuclei of the dorsal column is influenced by fibres descending from the sensory motor cortex (Gordon and Jukes 1964). This influence is predominantly inhibitory. The ascending fibres of those nuclei form the medial lemniscus of the brainstem, crossing the midline in the medulla to end in the thalamus. The final resolution of sensory impulses takes place in the somatosensory areas of the cerebral cortex (Mountcastle 1957). Not

even in this last analysis are afferent functions separated completely from motor function: stimulation of any of these areas produces motor effect (Woolsey 1964).

2.4.8 Visceral Afferents Schott’s (1994) principal proposition was that “sympathetically determined” pain was so determined because the afferent pathways were in the autonomic nerves. He noted the finding by Varro and colleagues (1988) of calcitonin generelated peptide (CGRP) in visceral afferents, admitting that selective histochemical markers for specifically pain-serving afferents were not, at that time, available. In developing his thesis Schott reverted to the conception of a system of visceral afferents which comprised not only fibres from organs

The Microscopic Structure of the Nervous System: Its Function

Fig. 2.45  Afferent fibres in the enteric division of the autonomic system. Nerve fibres within the mucosa and submucous plexus of human rectum stained with antibodies to sensory sodium channel (Nav1.7), x10 (Courtesy of Professor Praveen Anand).

generally classed as “viscera” but also afferents from blood vessels (Fig. 2.45) The evidence for the presence of a system for conveying from all viscera sensations both perceived and unperceived rests largely on indirect observations: the truly autonomic functioning of viscera: the production of pain by mechanical stimulation of peripheral arteries and veins; the operation of “referred pain” mechanisms; pain after operations on the sympathetic chain; the lack of “visceral sensibility” when the function of visceral afferents is impaired by age. There is evidence from the work of Sugiura and colleagues (1989) that visceral afferents terminate in laminae IV, V and X of the dorsal horn as well as in laminae I and II. They were also traced up and down in the cord and crossing the midline. In their final “conclusion,” Sugiura and colleagues (1989) proposed that their morphological observations suggested that “the somato-visceral convergence could occur in the superficial dorsal horn of the spinal cord,” and that “the scattered and extensive distribution of the terminal fields of single visceral C-afferent fibres may be one basis for the poor localisation of visceral sensation.”

2.5 Cortical Maps The fact that individual movements were controlled by specific areas of the cerebral cortex was recognized in the latter part of the nineteenth century and a “body map” of the sensory cortex was developed by Penfield and Boldrey (1937). The extensive observations made by these early workers do not support the notion of a rigid motor and sensory homunculus. Graham Brown and Sherrington (1912) and Sherrington and Leyton (1917) recognized the functional instability of

71

cortical motor points. A motor response might be elicited by stimulation of the post central cortex after preliminary stimulation of the precentral gyrus, a process that they termed facilitation. Repeated stimulation of the face area of the motor cortex in chimpanzees was followed by swift expansion of the region to embrace the territory originally representing the hand. Repeated stimulation sometimes induced a change from flexion to extension, a phenomena that they termed “reversal.” A third phenomenon, of “deviation of response” was recognized: “a cortical point can also influence the motor response of another whose response is neither diametrically opposed to nor identical with or very closely similar to its own” (Graham Brown and Sherrington 1912). Penfield and Boldrey (1937) mapped the areas of motor function by direct stimulation of the cerebral cortex during operations in 163 patients which were conducted under local anesthetic for the purpose of removing tumor or epileptogenic foci. Localisation was sharply defined for finger movements but very much less so for movements of the tongue and the jaws. Stimulation of the post central gyrus usually evoked a sensory response but this was by no means sharply defined. Even in the best defined map of finger sensation over one-sixth of the 158 points of stimulation actually lay in the pre central gyrus (Fig. 13 in the original paper). On 11 occasions stimulation of the cortex evoked a sensation of pain and in 13 more a sensation of cold. Patrick Wall (Wall 1977) provided clear evidence of plasticity within the adult somatosensory system by recording from single neurones and dorsal column nuclei and finding striking changes in the size of the receptive fields soon after partial deafferentation. Wall suggested that these changes might be caused by the unmasking of synapses normally ineffective or silent. The concepts of brain plasticity are reviewed by Lundborg (2004a) in his excellent monograph . Lundborg says that: brain plasticity implies the capacity of cortical synapses to change their function as circumstances require. In a short term perspective, they may rapidly alter their function, as a result of unmasking or potentiation of already existing synapses. In a more extended perspective, the synapses may increase or decrease in actual numbers and new dendrites may be formed.

(Lundborg 2004c). He continues: “cells that fire together, wire together i.e. neurones become involved in accomplishing the same function and learn to work together efficiently. This phenomenon is named Hebbian learning. Conversely, cells that fire apart, wire apart – i.e. neurones that are not involved in accomplishing the same function learn to ignore each other.” (Hebb 1947) We touch upon other aspects of brain “plasticity” in later chapters but should not forget the salutary observations of Ramachandran and Hirstein (1998): “it is an embarrassing fact that despite five decades of single unit physiology in animals, studied in excruciating detail, we still have no clear idea of how the brain works or why cortical maps exist.”

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2.6 Synaptic Activity The transmission of impulses at synapses is chemical, by the release of neurotransmitters causing a change in the permeability and hence the electrical polarisation of the post-synaptic membrane. Such changes may be excitatory or inhibitory; they are usually short-lived, because of early inactivation of the neurotransmitter. This is not of course the whole process: the effect of some neurotransmitters may be more prolonged or even permanent. In addition, some substances released at synapses may simply modify the response of the post-synaptic membrane to neurotransmitters. The general term “neuromediators” has been applied to substances released at synaptic endings; “neurotransmission” implies a direct effect on post-synaptic membrane; “neuromodulation” implies alteration of its response to a neuromediator ( Wigley et al. 2008). The best-known mediator and the one that has longest been known, is of course acetylcholine, synthesized by motor neurones and released at the motor terminals in skeletal muscle and at the synapses in sympathetic and parasympathetic ganglia. The other well-known mediators belong to the monoamine group: they are noradrenaline, adrenaline, dopamine, serotonin and histamine. Noradrenaline is the chief transmitter at the endings of sympathetic ganglionic neurones. Adrenaline too is present in peripheral neural pathways. Nitric oxide (NO) mediates smooth muscle relaxation at autonomic synapses. The other monoamines are chiefly present in the central nervous system. Gamma amino butyric acid (GABA) is a major inhibitory transmitter which is released at the terminal of such local circuit neurone systems as the inhibitory Renshaw loop. Glycine is another example of an inhibitory transmitter which is particularly prominent in the lower brain stem and spinal cord. Glutamate and aspartate are widely distributed excitatory transmitters. The range of neuropeptide modulators is very wide, including those associated with the function of the hypothalamus and hypophysis, corticotrophin, beta-endorphin, the enkephalins, calcitonin-related gene peptide and nerve growth factors. In the field of peripheral nerves, the last is of great and growing importance; the beta-­endorphins and enkephalins are important in the consideration of the mechanism and treatment of pain.

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The Microscopic Structure of the Nervous System: Its Function Omer G (1980) Range of conduction velocities. In: Omer GE, Spinner M (eds) Management of peripheral nerve problem. WB Saunders, Philadelphia, pp 6–7 Penfield W, Boldrey E (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:389–443 Petrie S, Collins J, Solomonow M, Wink C, Chuinard R (1997) Mechano receptors in the palmar wrist ligaments. J Bone Joint Surg 79B: 494–496 Pomeranz B, Wall PD, Weber WV (1968) Cord cells responding to fine myelinated afferents from viscera, muscle and skin. J Physiol (Lond) 199:511–532 Price DD, Meyer DJ (1974) Physiological laminar organisation of the dorsal horn of M. Mulatta. Brain Res 79:321–325 Ramachandran VS, Hirstein W (1998) The perception of phantom limbs. The DO Hebb lecture. Brain 9(121):1603–1630 Ranson SW (1915) Unmyelinated nerve fibres as conductors of protopathic sensation. Brain 38:381–389 Rasminsky M (1985) Conduction in normal and pathological nerve fibres. In: Swash M, Kennard C (eds) Scientific basis of clinical neurology, vol 28. Churchill Livingstone, Edinburgh, pp 390–399 Rexed B (1952) The cytoarchitectonic organisation of the spinal cord in the cat. J Comp Neurol 96:415–495 Rexed B (1954) A cytoarchitectonic organisation of the spinal cord in the cat. J Comp Neurol 100:297–379 Ruffini A (1897) Observations on sensory nerve-endings in voluntary muscle. Brain 20:367–374 Saldanha G, Bar K, Yiangou Y, Anand P, Birch R, Carlstedt T, Burrin JM (2000) Marked increase of interleukin – 6 in injured human nerves and dorsal root ganglia. J Neurol Neurosurg Psychiatry 69:693–694 Sanchez D, Anand V, Gorelik J, Benham CD, Bountra C, Lab M, Klenerman D, Birch R, Anand P, Korchev Y (2007) Localized and non-contact mechanical stimulation of dorsal root ganglion sensory neurons using scanning ion conductance microscopy. J Neurosci Methods 159:26–34 Sanders FK (1942) The repair of large gaps in the peripheral nerves. Brain 65:281–337 Schenker M, Birch R (2000) Intact myelinated fibres in biopsies of ventral spinal roots after preganglionic traction injury to the brachial plexus. A proof that Sherrington’s “wrong way afferents” exist in man? J Anat 197:383–391 Schenker M, Birch R (2001) Diagnosis of level of intradural ruptures of the rootlets in traction lesions of the brachial plexus. J Bone Joint Surg 83B:916–920 Scherer SS, Arroyo EJ (2002) Recent progress on the molecular organisation of myelinated axons. 3 rd Bunge Memorial lecture. J Peripher Nerv Syst 7:1–12 Scholz A, Reid G, Vogel W, Bostock H (1993) Ion channels in human axons. J Neurophysiol 70:1274–1279 Schott GD (1994) Visceral afferents: their contribution to “sympatheticdependent” pain. Brain 117:397–413 Schwann T (1839) Mikroskopiche Untersuchungen über die Übereinstimmung in der Strukter und dem Wachstum der Tiere und Pflanzen. Sander, Berlin Scott JJA (2005) The Golgi tendon organ. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier Saunders, Philadelphia, Chapter 7, pp 151–161 Seddon HJ (1975) Surgical disorders of peripheral nerves. Churchill Livingstone, 2nd edn. Edinburgh, London/New York, pp 267–270 Selander D, Sjostrand J (1978) Longitudinal spread of intraneurally injected local anaesthetics. An experimental study of the initial distribution following intraneural injections. Acta Anaesthesiol Scand 22:622–634 Sharrard WJW (1955) The distribution of the permanent paralysis in the lower limb in poliomyelitis. J Bone Joint Surg 37B:540–558

75 Sherrington CS (1894) On the anatomical constitution of nerves of skeletal muscles: with remarks on recurrent fibres in the ventral spinal nerve-root. J Physiol 17:211–258 Sherrington CS (1897) The synapse in: the central nervous system. In: Foster M, Sherrington CS A textbook of physiology, vol 3, 7th edn. Macmillan, London, p 929 Sherrington CS, Leyton ASF (1917) Observations on the excitable cortex of the chimpanzee, orang-utan and gorilla. Quart J Exp Physiol 11:135–222 Sinclair DC (1955) Cutaneous sensation and the doctrine of specific energy. Brain 78:584–614 Stacey MJ (1969) Free nerve endings in the skeletal muscle of the cat. J Anat 105:231–254 Standring S (2008) Conduction of nervous impulses. In: Standring S (ed in chief) Gray’s anatomy, 40th edn. Churchill Living stone, Elsevier, pp 63–64 Stark B, Carlstedt T, Hallin RG (1998) Distribution of human pacinian corpuscles in the hand. J Hand Surg 25B:370–372 Stolinski C (1995) Structure and composition of the outer connective tissue sheaths of peripheral nerve. J Anat 186:123–130 Stolinski C, Breathnach AS (1982) Freeze-fracture replication of mammalian peripheral nerve – a review. J Neurol Sci 57:1–28 Sugiura Y, Terui N, Hosoya Y (1989) Difference in distribution of central terminals between visceral and somatic unmyelinated (C) primary afferent fibres. J Neurophysiol 62:834–840 Sunderland S (1968) Intraneural topography. In: Sunderland S Nerve and nerve injuries. E & S Livingstone Edinburgh, London. … Median nerve pp 758–769; ulnar nerve pp 816–825; radial nerve pp 905–914; sciatic nerve pp 1029–1046 Sunderland S, Lavarack JO, Ray LJ (1949) The caliber of nerve fibers in human cutaneous nerves. J Comp Neurol 91:87–101 Suter U, Martini R (2005) Myelination. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier Saunders, Philadelphia, Chapter19, pp 411–431 Svensson LG (2005) Paralysis after aortic surgery: in search of lost cord function. The James IV lecture. Surgeon 3:396–405 Takebayashi T, Yamashita T, Minakiy, Ushii S (1997) Mechano sensitive afferent units in the lateral ligament of the ankle. J Bone Joint Surg 79B:490–493 Takebayashi T, Cavanagh JM, Kallukuri S, Chen C, Yamashita T (2006) Sympathetic afferents from lumbar intervertebral discs. J Bone Joint Surg 88B:554–557 Tasaki I, Takeuchi T (1941) Der am Ranvierschen Knoten entstehende Aktionström und seine bedeutung für die Erregungsleitung. Pflügers Archiv 244:696–711 Tasaki I, Takeuchi T (1942) Weiters Studien über den Aktionsstrom der markhältigen Nervenfäser und über die elektrosaltatorische. Uberträgung des Nervenimpulses. Pflügers Archiv 245:764–782 Taylor PK (1984) Non-linear effects of age on nerve conduction in adults. J Neurol Sci 66:223–234 Thomas PK (1963) The connective tissue of peripheral nerve; an electron microscope study. J Anat 97:35–42 Thomas PK, Berthold C-H, Ochoa J (1993a) Microscopic anatomy of the peripheral nervous system. In: Dyck PJ, Thomas PK, Griffin JW, Low PA, Poduslo JF (eds) Peripheral neuropathy, 3rd edn. WB Saunders, Philadelphia, Chapter 3, pp 28–92 Thomas PK, Scaravilli J, Belai A (1993b) Pathological alterations in cell bodies of peripheral neurons in neuropathy. In: Dyck PJ, Thomas PK, Griffin JW, Low PA, Poduslo JF (eds) Peripheral neuropathy, 3rd edn. WB Saunders, Philadelphia, Chapter 29, pp 476–513 Tillett RL, Afoke A, Hall SM, Brown RA, Phillips JB (2004) Investigating mechanical behaviour at a core-sheath interface in peripheral nerve. J Peripher Nerve Syst 9:255–262 Tohgi H, Tsukagoshi H, Toyokura Y (1977) Quantitative changes with age in normal sural nerves. Acta Neuropathol (Berlin) 38: 213–220

76 Tomita K, Berger EJ, Berger RA, Kraisarin J, An KN (2007) Distribution of nerve endings in the human dorsal radio carpal ligament. J Hand Surg 32A:466–473 Torebjörk HE, Ochoa JL (1980) Specific sensations evoked by activity in single identified sensory units in man. Acta Physiol Scand 110:445–447 Torebjörk E, Schmelz M (2005) Single-unit recordings of afferent human peripheral nerves by microneurography. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. WB Saunders, London, Chapter 38, pp 1003–1014 Uziyel Y, Hall S, Cohen J (2000) Influence of laminin-2 on Schwann cell-axon interactions. Glia 32:109–121 Vallbo AB, Hulliger M (1981) Independence of skeletomotor and fusimotor activity. Brain Res 223:176–180 Varro A, Green T, Holmes S, Dockray GJ (1988) Calcitonin generelated peptide in visceral afferent nerve fibres: quantification by radio immunoassay and determination of axonal transport rated. Neuroscience 26:927–932 Von Frey M (1894) Beitrage zur Physiologie der Schmerzsinns. Berichte der Königliche Sächsiche Gesellschaft der Wissenschaften 46:185–196 Von Frey M (1896) Untersuchungen uber die Sinnesfunktionen der menschlichen Haut. 1. 1. Druckempfindung und Schmertz. Berichte der Köningliche Sächsiche Gesellschaft der Wissenschaften 48:175–264 Wall PD (1961) Two transmission systems for skin sensation. In: Roseblith WA (ed) Sensory communication. MIT press, Cambridge, pp 475–496 Wall PD (1970) The sensory and motor role of impulses travelling in the dorsal columns towards the cerebral cortex. Brain 93:505–524 Wall PD (1977) The presence of ineffective synapses and the circumstances which unmask them. Philos Trans R Soc Lond B278: 361–372 Webster HdeF (1993) Development of peripheral nerve fibers. In: Dyck PJ, Thomas PK, Griffin JW, Low PA, Poduslo JF (eds)

Surgical Disorders of the Peripheral Nerves Peripheral neuropathy, 3rd edn. WB Saunders, Philadelphia, pp 243–266 Weddell G (1941) The pattern of cutaneous innervation in relation to cutaneous sensibility. J Anat 75:346–366 Weerasuriya A (2005) Blood-nerve interface and endoneurial homeostasis. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier Saunders, Philadelphia, Chapter 29, pp 651–665 White JC, Sweet WH (1969) Pain and the neurosurgeon: a forty year experience. Charles C Thomas, Springfield, pp 895–896 Wigley C, Felts P, Standring S (2008) Mechanism of synaptic activity. In: Standring S (ed in Chief) Grays anatomy, 40th edn. Churchill Livingstone, Elsevier, pp 46–48 Windebank AJ, McDonald ES (2005) Neurotrophic factors in the peripheral nervous system. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier Saunders, Philadelphia, Chapter 17, pp 377–386 Woollam DHM, Millen JW (1958) Discussion on vascular disease of the spinal cord. Proc R Soc Med 51:540–543 Woolsey CN (1964) Cortical localization as defined by evoked potential and electrical stimulation studies. In: Scaltenbrand G, Woolsey CN (eds) Cerebral localization and organisation. University of Wisconsin Press, Madison, pp 17–32 Yiangou Y, Birch R, Sangeswaram L, Eglen R, Anand P (2000) SNS/PN3 and SNS2/NaN sodium channel like immunoreactivity in human adult and neonate injuries of sensory nerves. FEBS Lett 467:249–252 Young JZ (1942) Functional repair of nervous tissue. Physiol Rev 22:318–374 Young JZ (1945) The history of the shape of a nerve fibre. In: Le Gros Clark WE, Medawar PB (eds) Essays on growth and form. Oxford University Press, Oxford, p 41 Young JZ, Holmes W (1940) Nerve regeneration. Lancet 2:128–130 Zotterman Y (1939) Touch, pain and tickling: an electrophysiological investigation on cutaneous sensory nerves. J Physiol 95: 1–28

3

Reactions to Injury

Reactions to injury: the reaction of the nerve cell and myelin/Schwann cell complex; differential reaction of fibres of different sizes; two main types of nerve injury, degenerative and non-degenerative; Wallerian degeneration; the special case of the brachial plexus; reactions to various physical agents; the effects of denervation. Nerves can be damaged in a number of ways: (1) ischaemia; (2) physical agents such as traction or stretching which may be sudden, intermittent or prolonged, pressure, distortion, cold, heat, severance, electric shock, injection of noxious substances, ionising radiation; (3) infection and inflammatory processes; (4) ingestion of drugs and metals; (5) infiltration by or pressure from tumours; (6) the effects of systemic disease. The damage to the nerve may be “closed,” or “open” through a wound of the skin. Damage may be acute or chronic; single, repeated or continuing. The lesion may affect the whole nerve or only part of it. The depth of affection may vary from fibre to fibre or from one part of the nerve to another. The nerve affected may be entirely healthy or may be the subject of a neuropathy from hereditary or systemic causes or from a more proximal affection. Nerve injury may be associated with damage to one or more important structures: artery, vein, viscus, bone, muscle or ligament. It is helpful to the clinician to bear in mind two facts: (1) a nerve which has been transected or ruptured cannot recover until it is repaired; (2) a lesion of a peripheral nerve which remains in continuity but which continues to be subjected to the cause of that lesion will deepen until the cause is removed (Fig. 3.1a, b). The speed of that deepening is related to the cause. A nerve crushed by a plate or by an encircling suture may recover if that cause is removed within a minute or two. It is unlikely to recover if it is not relieved for more than 2 or 3 h. A nerve subjected to continuing traction and ischaemia from an expanding haematoma will recover if the situation is corrected within 6–8 h. After that recovery will probably be imperfect and may not occur at all. The nerve subjected to compression and ischaemia within a swollen ischaemic limb will almost certainly recover if the cause is corrected within 4 h; the chances of full spontaneous recovery diminish with the passage of every hour after that time. It may be years before the situation becomes irretrievable for a nerve subjected to radiotherapy or exposed to continuing traction from a malunited fracture. The cardinal symptom of the persistence of a noxious agent is pain (Fig. 3.2).

a

b

Fig. 3.1  Deepening of lesion. (a) Median nerve extricated from supracondylar fracture in a 9 year old girl at 3 days from injury. There was complete recovery. (b) Median nerve extricated from supracondylar fracture in a 13 year old girl 8 weeks after injury. There was no recovery.

In the mildest form of damage – that produced by transient ischaemia – there is transient failure of conduction affecting principally the large myelinated fibres. Lewis et al. (1931) described this form of centripetal paralysis produced by the application round the arm of a cuff inflated to suprasystolic pressure. First, there is loss of superficial sensibility. This is succeeded by a gradual loss of motor power. The first

R. Birch, Surgical Disorders of the Peripheral Nerves, DOI: 10.1007/978-1-84882-108-8_3, © Springer-Verlag London Limited 2011

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Fig. 3.2  Conduction block. The radial nerve shown tented over the tip of the screw 10 days after operation for fracture. There was a painful deep radial palsy. Conduction in the distal segment was preserved but there was no conduction across the lesion. Conduction in the nerve to brachioradialis (left hand sling) was preserved. Stimulation of the radial nerve above the level of lesion did not evoke response through the nerve to extensor carpi radialis longus (right hand sling). The screw was shortened. Recovery was complete by 24 h.

pain response is lost soon after superficial sensibility fails, but the delayed pain response can still be elicited after 40 min of ischaemia. Pilomotor and vasomotor functions are scarcely affected. This differential paralysis reflects, of course, the differing reactions of the fibres of different sizes. Large myelinated fibres are first affected; C fibres and autonomic fibres escape. Recovery of all modalities occurs within a few minutes of release of the cuff. By a simple but ingenious method Lewis and his colleagues demonstrated that the lesion was caused by ischaemia of the segments of the nerves underlying the cuff. MacKinnon and Dellon (1988) rightly suggest that all those intending to take up peripheral nerve work should try this experiment on themselves. The experience gives a very clear indication of what is meant by the depth of a nerve injury. That knowledge is certain to be important in clinical practice. Further, the experience of the unpleasant quality of the residual delayed pain sensation gives a good insight into the feelings of patients affected by dysaesthesia. It is interesting to note Merrington and Nathan’s (1949) observation that the paraesthsiae occurring during recovery arise not from the periphery but from the nerve trunks recovering from ischaemia. The effect of temporary ischaemia is particularly well illustrated by the behaviour of the main nerves during emergency repair of a main artery. Conduction persists for about an hour whilst the artery is being controlled and repaired. Then, conduction diminishes before altogether ceasing. Conduction returns within a few minutes after removal of clamps and restoration of flow. The conduction block caused by the penetrating missile wounds of war was recognised by Mitchell et al. 1864: “this condition of local shock is very curious. A man is shot in the thigh, the ball passes near the sciatic nerve, and instantly the

Surgical Disorders of the Peripheral Nerves

limb is paralysed; within a few minutes or at the close of a day or a week the volitional control in part returns, but finally they may be left with some single group of muscles permanently paralysed.” Seddon (1943) observed the characteristic features: paralysis exceeds loss of sensation; the nerves responsible for proprioception are more deeply affected than those conveying light touch sensation; vasomotor and sudomotor function is least affected. It is likely that this lesion is provoked by a momentary displacement, or stretching, of the nerve trunks. This explanation cannot account for the conduction block of blast injuries in which the patient is exposed, at close range, to the shock wave of an explosion without any wound, or fracture and with no signs of significant injury to the soft tissues. Case Report: A rocket propelled grenade landed 5 ft from an infantryman who was thrown through the air by the blast, landing heavily on his left side. He immediately noted loss of sensation of the whole of the left forequarter including the skin of the neck and of the chest wall. There was complete paralysis of the whole of the left upper limb. There was no local injury to the posterior triangle, the shoulder or to the cervical spine. Sensation started to recover after 3 days, the muscles started to work after 5 days. Recovery was nearly complete by about 3 weeks although subsequent QST revealed elevated warm thresholds. The mechanism underlying this increasingly common form of conduction block is now under investigation. It is possible that the shock wave causes distortion of the paranodal myelin and the membrane of the axon at the node of Ranvier. As Lewis et al. (1931) noted, the differential response of nerve fibres is reversed in the conduction block produced by infiltration of local anaesthetic agent. Here, the first sign of developing paralysis is the drying and warming of the extremity. It is probable that here conduction block is caused by interference with axonal conduction: so, the small unmyelinated fibres are the most susceptible and the first to succumb. By contrast compression of nerves by haematoma or aneurysm produces a characteristic pattern: autonomic paralysis is early and deep; loss of power extends over hours or days; deep position sense and limited joint position sense persist. With severe and prolonged pressure there is local demyelination and more prolonged conduction block (Fowler et al. 1972; Gilliatt 1981) (Fig. 3.3). The pressures used by

Proximal

Cuff

Distal

Axon

Fig. 3.3  Effect of pressure on nerve: squeezing of myelin with invagination at the node of Ranvier. Narrowing of axon with extrusion of its contents (After Ochoa J et al.1972).

Reactions to Injury

Gilliatt could not reasonably be used in experiments on human subjects. The myelin is squeezed proximally and distally from underneath the tourniquet so as to invaginate into the proximal and distal sheaths of the nodes of Ranvier. The structural affects of focal compression were analysed by Dyck et al. (2005a) in a series of experiments on the peroneal nerve of the rat. The nerve was subjected to a compression force of 300 mmHg for periods ranging from 2 min to 2 h, after which the nerve was rapidly stabilised by perfusion fixation. There was a sequence of events deep to the cuff: (1) the endoneurial fluid was squeezed out so that the nerve fibres and cells became more closely apposed; (2) fluid was squeezed from out of the axon leading initially to compaction of the formed elements and later to their being expressed from out of the axon at the margins of the zone of compression, and (3) the internodes were lengthened with shearing between the lamellae of the myelin sheath. Additional changes occurred at the edges of the cuff, at the intersection between the compressed and the non compressed nerve fibres. Here the area of the endoneurium increased, the axons became distended, especially at the nodes of Ranvier because of the increase of axonal fluid and loops of myelin which had been sheared off and came to overlap the nodes. The structural alterations revealed by this method cannot be caused by ischaemia, for these take several hours to develop and are, in appearance, quite different. A conduction block which may last for weeks or months results. If, in the clinical situation, the cause of the local demyelination persists in the form of (say) a bony projection causing pressure and distortion or of external pressure by haematoma, the block persists. This was so in the three cases reported by Birch and St Clair Strange (1990): in these, removal of the external pressure was rapidly followed by recovery in lesions which had persisted for up to 3 years. The bestowal of the name axonamonosis on this type of lesion by Birch and St Clair Strange, abetted by Bonney, was sharply criticised by Gilliatt in a communication which he was kind enough to keep private. In the experimental situation conduction recovers and motor and sensory functions are restored, though not necessarily in an orderly manner. In this type of paralysis, the autonomic fibres are usually spared, though not necessarily so. We have seen lesions of the median, the tibial and the common peroneal nerves produced by prolonged pressure in which there was prolonged vasomotor and sudomotor paralysis. All these forms of paralysis are examples of neurapraxia (Seddon 1943); all are examples of the non-degenerative lesion. Seddon gave the credit for the naming of his three types of nerve lesion to Sir Henry Cohen, later Lord Cohen of Birkenhead. “Neurapraxia” is perhaps the most admirable but potentially the most misleading of the three: derived from neuron (neuron – nerve or tendon) and apraxia (apraxia – non function), it signifies loss of nerve function – no more and no less. It will not do as a diagnosis unless the clinician using it is aware that it never signifies a degenerative lesion.

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The use of the negating a (alpha) is or should be familiar to clinicians, since it occurs in terms in common use such as aphasia, aphonia, astigmatism, anorexia, amyotrophy and so on. It is all the sadder that declining standards of literacy have combined with rising looseness of thought to render the use of the term neuropraxia a commonplace even in formerly reputable Journals and text books. Punishment should be reserved for clinicians using this meaningless neologism; lawyers using it should lose their fees; classicists using it should suffer an appropriate loss. The situation is wholly different when the lesion is serious enough to cause interruption of the axon. Then follow the changes of a degenerative lesion, caused by the damage to the neurone itself. The changes were first described by Waller (1850) and have since that time been known as those of Wallerian degeneration. We know now that they affect not only the axon but also the cell body; not only the neurone but also its Schwann cell ensheathment and its myelin sheath. There are changes too in the endoneurial cells and, over longer periods of time, in the motor and sensory end-organs. Distal to the site of injury the axon degenerates; there is a granular disintegration of the cytoskeleton and axoplasm, which are converted over succeeding days into amorphous debris (Figs. 3.4a–c and 3.5). Although Adrian (1916, 1917) and Pollock et al. (1946) thought that peripheral neural conduction might survive for up to a month after nerve section in man, Landau (1953) found that the motor response after section persisted for a much shorter period. The interval between injury and the last observation of a neuromuscular response ranged from 66 to 121 h. Gilliatt and Taylor (1959) investigated motor response after section of the facial nerve in man, and found that visible twitch in response to stimulation disappeared within 3–4 days; though an electrical response persisted for a further 48–72 h. Our own observations on motor conductivity after pre-ganglionic injury to the brachial plexus suggest that the motor response ceases about 3 days after injury. In one case stimulation of the ventral roots of spinal nerves which had been avulsed from the spinal cord evoked a motor response 132 h after the injury. The detection of persisting conduction in the distal segment of a nerve which has been ruptured or detached from the spinal cord excludes a more distal lesion of the nerve and excludes ischaemia of the nerve in cases where the axial artery has been damaged. Conduction may cease first in the most proximal part of the fibres. Gilliatt and Hjorth (1972) studied the matter in baboons. The motor response to stimulation disappeared after 4–5 days, but ascending nerve potentials could be recorded for a further 2 or 3 days. Evidently, failure of transmission at the neuromuscular junction precedes failure of conduction along the degenerating axon. Landau (1953) made the perceptive comment that “the distinction between complete Wallerian degeneration and less severe injury can be made on the basis of the disappearance of excitability in the peripheral nerve segment at this

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a

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b

c

Fig. 3.4  Changes in the distal stump of ulnar nerve transected 3 weeks previously. The gap between the proximal and distal stumps was 5 cm. (Electronmicroscopic studies prepared by Mr Stephen Gshmeissner.) (a) Disintegration of the axon and the myelin sheath. Axoplasm and

neurofilaments are seen in the lower fibre ×2,210. (b) Another part of the same specimen. Myelin debris within a macrophage (asterisk), probable Schwann cell processes (arrows) ×5,525. (c) Another part of the same specimen. Many Schwann cells, some with active nuclei ×5,525.

time,” that is, the time of disappearance of neuromuscular function. Many misdiagnoses of “neurapraxia” could have been and could be avoided if this simple procedure were more widely used. The essential difference between neurapraxia and the different types of degenerative lesion is the persistence of conduction in the distal segment of the nerve in the former and

its disappearance in the latter. Conduction disappears within 1 h of an ischaemic lesion but persists for hours or even days after transection or rupture. The early disappearance of conduction is, of course, the hall mark of impending or actual “critical” ischaemia. It is unwise to make a diagnosis of neurapraxia in the presence of persisting pain for that pain signifies that the

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Node of Ranvier

Fig. 3.5  Wallerian degeneration in the distal stump of fifth cervical nerve ruptured 3 weeks previously. The axon is collapsing and it is surrounded by a macrophage although the myelin sheath appears intact x 1,100.

noxious agent is continuing to act. A diagnosis of neurapraxia should not be made in the presence of a strong Tinel sign for this indicates that axons have been ruptured. A diagnosis of neurapraxia should never be made in limb rendered pulseless by injury: conduction block may prove to be but the first step towards something much worse.

3.1 Axonotmesis – Neurotmesis So long as the lesion is not severe enough to interrupt the continuity of the Schwann cell basal laminae from proximal to distal segment the original pathways for re-growth of axons remain (Young 1949; Causey and Palmer 1952; Thomas 1964; Haftek and Thomas 1967) (Fig.  3.6). As Gutmann and Sanders (1943) noted in their experimental work, “only after crushing (as opposed to section) was the nerve fully reconstituted.” Seddon (1943) described the appearance of axonotmesis in rabbits following firm squeezing of a nerve with fine smooth bladed forceps: “the immediate lesion is of striking appearance: the central and peripheral parts are united only by a fine ribbon of translucent connective tissue. The main substance of the nerve is broken and separated by an appreciable interval. Within a few minutes it flows together again, and the fine connecting ribbon is filled out so that the gap is no longer visible.” Seddon described similar experiments, which were performed with JZ Young, in patients in whom part of a limb required amputation: “on several occasions patients have allowed us to crush or divide a nerve, in the part to be sacrificed, at an appropriate interval before the final operation.” The general pattern of the nerve was retained: “the axons were completely interrupted and the conjugating tissue

Basal lamina

Schwann cell nucleus

Myelin sheath

Axon

Fig. 3.6  Axonotmesis (centre) and neurotmesis (bottom) at the moment of injury. Note the preservation of the Schwann cell basal lamina in axonotmesis.

appeared to consist of collapsed endoneurial tubes. In all but one case the lesion had been allowed to proceed to some measure of regeneration; there was a noticeable absence of the axonal branching and crisscrossing that are always found after suture. As Fig.  3.4b shows, the fibres have grown without hindrance into their old paths, exactly as described by Stroebe, Cajal and Langley.” Seddon and Young recognised that the integrity of the Schwann tubes provided important support for regeneration: “if, as we believe, the process of regeneration is a protoplasmic outflow from the central stump (Holmes and Young 1942) progress will be faster when the flow is confined to one main channel and not dissipated in many separate protoplasmic streams.” (Seddon 1975). It is the difference between preservation and destruction of continuity that underlies the division of degenerative lesions between those with the potential for spontaneous recovery and those that will not recover unless action is taken. Seddon (1943) named the first axonotmesis, from azwnw (axono – shaft, or axon) and TmhsiV (tmesis, cutting). That term is still valuable, indicating as it does the vital element of the degenerative lesion: the interruption of the axon and the consequent damage to the neurone. Seddon (1943) named lesions in which interruption of the axon was associated with interruption of the basal lamina, neurotmesis. He, of course derived the term from neuron (neurone, nerve or tendon) and TmhsiV (tmesis, cutting). It rightly indicates interruption of continuity of all elements of the nerve. As our colleague Gereis (2005) points out it is never easy to distinguish between paralysis (par lnsiV) an unrecoverable nerve lesion, and a palsy or paresis (paaresiV), a lesion which may recover spontaneously.

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Table 3.1  Classification of focal mechanical nerve injury. I. Focal conduction block Transient Ischaemic Other More persistent Demyelinating Axonal constriction II. Axonal degeneration With preservation of basal laminal sheaths of nerve fibers With partial section of nerve With complete transection of nerve From Thomas and Holdorff (1993). With permission.

Sunderland (1951) introduced a rather more elaborate system of classifying injury. Five degrees of severity were named, ranging from simple conduction block to loss of continuity. The views of this pioneer in the field command respect; it may well be, that some clinicians find Sunderland’s classification an improvement on Seddon’s and of more practical use than the earlier method. We, on the contrary, have tended towards a further simplification: to classification as “degenerative” and “non-degenerative.” This, we think, is the manner in which clinicians should regard nerve injuries: the first question to be asked is “is this lesion degenerative or non degenerative?” Thomas and Holdorff (1993) elaborate this conception of “degenerative” and “non-degenerative” lesions in a manner helpful to clinicians and experimentalists. We reproduce by permission their table  52–1, in which the subdivisions of “focal conduction block” and “axonal degeneration” are set out Table 3.1. We think that the question mark placed against “axonal constriction” is removed by the case shown to one of us by Campbell Semple (personal communication) (Fig. 3.7). In that case of hour-glass constriction of a main nerve trunk external neurolysis and decompression was followed by early and complete recovery, there must have been axonal constriction. Nagano et al. (1996) and Nagano (2003) studied “spontaneous” paralysis of the anterior interosseous nerve. They found during interfascicular neurolysis of the median nerve that there was “hourglass” constriction of the fascicles belonging to the anterior interosseous nerve. There was no external compression. Recovery after interfascicular neurolysis alone was “generally good.” Akira Nagano has summarised his experience in a personal communication (Nagano 2008). He has identified “hourglass” like fascicular constriction involving the median nerve near the elbow in 24 patients. Five of these presented with symptoms and signs suggestive of a diagnosis of neuralgic amyotrophy. Oberlin et al. (2006) describe a similar lesion involving the circumflex nerve. The possibility that this represents a twisting or torsion of the bundles is raised. Dyck et al. (2005a) show that

Fig.  3.7  Hour glass “constriction” of the lateral root of the median nerve, the result of traction injury. There was full spontaneous recovery (Mr Campbell Semple’s case).

the axon itself may be damaged or even transected by infolded loops of the myelin sheath thrust in by external pressure or other processes. Is it possible that this occurs in cases of “hour glass” constriction? In clinical practice, most injuries of nerves short of transection inflict damage of all three grades of severity. The lesion is pure only in cases of transient ischemia or complete transection. Seddon based his classification on a study of 650 nerve lesions. The injury was in continuity in 537 of these amongst which only 117 cases of “pure” lesions could be indentified; the rest were mixed. This is the usual pattern for the sciatic nerve stretched but not ruptured by dislocation of the femoral head and for the cords of the brachial plexus stretched but not ruptured by anterior dislocation of the head of the humerus. The decision about exploration in cases such as these is never easy but the difficulties may be eased if the clinician bears in mind the possibility that removal of the cause of the lesion may prevent deepening or deterioration and that it may convert a situation inimical to spontaneous recovery to one that is more favourable. The persistence of pain is an important indication for exploration of the nerve.

3.2 The Cell Body and Proximal Stump The central and the peripheral effects of Wallerian degeneration are profound and they are ultimately irreversible. The cell body is separated from the supply of neurotrophins and it may be drained or exhausted by the process of regeneration. The sooner the cell body is reconnected with the periphery the better. Proximal to the lesion changes occur in the axon, the myelin sheath, and in the nerve cells. Within a few days there is a reduction in the calibre of the proximal axon; there may be atrophy of the whole axonal “shaft.” Gutmann and Sanders (1943) thought that this might be caused by the

Reactions to Injury

outflow of axoplasm during regeneration. Aitken and Thomas (1962) showed that the reduction in the diameter of the fibre was still evident 300  days after suture of the nerve. Cragg and Thomas (1961) found that nerve conduction velocity in the proximal segment fell to between 60% and 70% of normal by 200 days and it did not improve in nerves which had not been repaired. Hoffer et al. (1979) recorded nerve conduction potentials in the roots of spinal nerves in cats whose leg nerves had been cut and prevented from regrowing. A progressive decline in nerve conduction velocity from the dorsal root fibres was demonstrated; the decline for the motor fibres stabilised. A clear correlation between the reduction in the calibre in the larger myelinated nerve fibres and a drop in the peak to peak amplitude of the nerve compound action current was demonstrated by Walbeehm et al. (2003). In the cell body itself there may be chromatolysis, a process characterised by Groves and Scaravilli (2005) as one associated with a regenerative and not a degenerative response to an insult. Curiously enough, transection of the central branches going to the central nervous system does not produce such clear cut changes in the cell bodies in the dorsal root ganglia. Lawson (2005) describes changes in the behaviour and in the expression of ion channels in the dorsal root ganglion (DRG) cell bodies which can be detected within a few minutes of an injury to the nerve. Anand and his colleagues (Rabert et al. 2004) studied the expression of genes in the neurones within adult human dorsal root ganglia in cases of avulsion lesions of the brachial plexus, taken at intervals ranging from 1 to 100  days after injury. There was a clear alteration in the expression of 91 genes particularly for those known to be involved in neurotransmission, trophism, cytokine function, signal transduction, myelination, transcription regulation and apoptosis. In other studies of the behaviour of human DRG neurones Boettger et al. (2002) measured the changes in potassium channel behaviour and the influence of neurotrophic factors, Bar et  al. (1998) recorded significantly higher levels of GDNF and Saldhana et al. (2000) found a remarkable increase in interleukin-6 (IL-6), which is a member of the neuropoietic cytokine family (Fig. 3.8). The chromatolysis following axonotomy1 may continue to actual dissolution of the cell body: “the nucleus becomes unidentifiable, all basophilia has disappeared and what remains is a seemingly empty sac containing the condensed remnants of neuronal DNA, a so-called ghost cell” (Groves and Scaravilli 2005). On the other hand rhizotomy scarcely affects the neurone, it “does not produce any observable morphological change in the perikarya of the affected neurones.” Chromatolysis does not occur in newborn mammals, instead the affected neurones become smaller, more intensely stained and many die. Groves and Scaravilli go on to define apoptosis

1

 he common usage is of course axotomy, but we believe that axonotomy T is the more correct term

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Fig. 3.8  TRPV1 (the heat and capsaicin receptor) in a human dorsal root ganglion 6 weeks after avulsion showing immunostaining in small diameter neuronal cell bodies and axons ×40 (Courtesy of Professor Praveen Anand).

as a controlled and deliberate form of neurone destruction that is largely a secondary effect of an insult. The loss of cells is more severe in more proximal axonotomy; axonotomy in the neonate produces a more rapid and much greater incidence of sensory and motor neurone death than in the adult and it is particularly severe after avulsion of the ventral root: “ventral root avulsion being the most severe and acute form of injury, because of the significant trophic support being supplied by surrounding glia and neurones in the adult spinal cord which is disrupted in avulsion” (Fig. 3.9a, b). The loss of sensory neurones was studied in the rat by Ygge (1989a,1989b) and by Schmalbruch (1987). Romanes (1946) observed the changes in the anterior horn cells of mice after permanent axonotomy by amputation. Dyck et al. (1984) were able to study the effect of permanent axonotomy on the spinal cords of two patients who had undergone respectively, partial and total amputation of a lower limb. They found that “loss of target tissue by axotomy leads to atrophy and then loss of motor neurones.” Suzuki et  al. (1993) examined the cervical cord and the roots and ganglia of the spinal nerves in a patient who died 38  years after amputation of the upper limb. They demonstrated a loss of neurones in the DRG, in the anterior horn, and a diminution of the large myelinated nerve fibres in the ventral and dorsal roots. Perhaps the electrophysiological findings in a cohort of old polio survivors described by Sorenson et  al. (2006) represent an attrition of surviving neurones in the anterior horn. Carlstedt (2007) says that: “motor neurones are rapidly killed by ventral root avulsions. Disconnection from the periphery means that interrupted supply of neurotrophic factors, together with vascular trauma leading to cytotoxicity drastically reduces the number of motor neurones up to about 90% of the normal population.” Carlstedt reckons that about one half of all motor neurones in the affected spinal cord segment have disappeared by 2 weeks after avulsion of the ventral root and he suggests that “a swift intervention to re

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a

b

Fig. 3.9  Delay: the proximal stump of C5 ruptured at the same level, 1 cm distal to the foramen, but exposed at operation at different intervals. (a) Six weeks after injury. Clusters of myelinated and unmyelinated nerve fibres forming minifascicles. Bar = 20 mm, (b) Eight months

after injury. Some unmyelinated axons lie within debris laden Schwann cell cytoplasm. There is extensive fibrosis. Fibroblast processes surround the Schwann cell- axon units ×3,000.

establish contact between the injured nerve cells and the periphery with its supply of neurotrophic substances would counteract nerve cell loss in these injuries.” The same phenomenon, of central cell death, follows more peripheral axonotomy although not to the same degree. One example of the depletion of neurotrophins is provided by Anand et  al. (1997) who showed, in human nerves, depletion of NGF proximally and rapid depletion of CNTF both proximally and distally after section of a nerve. As long ago as 1913 Cajal (1928) noted

intradural damage to the roots of the brachial plexus. At delayed operation (hemi laminectomy) the ipsilateral cord is seen to be atrophic, doubtless from the damage to the motor and sensory pathways. Further, magnetic resonance imaging plainly shows atrophy of the cord after birth injury of the brachial plexus. It is a matter of interest that, despite the degeneration of the proximal process of the cells of the dorsal root ganglion, those cells appear to retain for a long time their ability to sustain their distal processes, apparently without serious functional impairment (Bonney and Gilliatt 1958) (Fig. 3.10).

as shown by the older observations of Dickinson (1868) and by the more modern ones of Gadden, Ford and Monakow (1882), there are cases where the neuron whose axon is mutilated or even functionally isolated shows morbid changes, and may even die.

In the words of McComas et al. (1978) “the periphery is essential for the functional integrity of motor and sensory nerve axons.” Further evidence about the changes in proximal neural structures is available from studies of the spinal cord after

3.2.1 Wounds of the Perineurium Wounding of the perineurium causes demyelination and Wallerian degeneration (Thomas and Jones 1967). Spencer et  al. (1975) studied the process of demyelination and

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3.2.2 Contralateral Effects

Fig. 3.10  Right side of the spinal cord at the level C5 to C8 seen at hemilaminectomy 6 months after intradural lesion of the plexus. Note the shrinking of the middle part of the cord at the level of the emergence of the seventh cervical root and the mouths of the pseudo meningocoele.

For some years it has been our impression that the regenerative capacity of the central nervous system is diminished by the most severe injuries to the brachial plexus and we attributed this to an affect extending beyond the injured segments of the spinal cord. A dramatic example of the involvement of regions beyond the area of injury is provided by Suzuki et al. (1993) who, in addition to the ipsilateral effects already described, also demonstrated atrophy of the contralateral anterior horn, where there was a loss of the medium size cells and a reduction in the numbers of the medium and small myelinated nerve fibres in the contralateral ventral roots. This phenomenon has been closely examined by Oaklander and Brown (2004) who used the pan neuronal marker protein (PGP9.5) to measure the density of innervation in the skin of the paws of the rat after transecting one tibial nerve. There was almost complete loss of innervation within the plantar skin in the injured limb. However, a persisting loss of innervation, in excess of 50%, was noted in the skin of the contralateral hind paw. The significance of these findings will not be lost on the clinicians treating patients with nerve injuries.

3.3 The Distal Stump

Fig. 3.11  Injection injury. The tip of the needle lacerated the lateral part of median nerve at the elbow and a neuroma occupied about four of the bundles. Small fascicles of thinly myelinated axons and Schwann cells occupy the proximal stump of one bundle ×2,000.

subsequent remyelination induced by making a window in the perineurium and Thomas and Bhagat (1978) scrutinised the effects of performing a window in the perineurium and extracting its contents at that level. The perineurial cells separated from one another and also from their basal lamina and came to resemble fibroblasts. Regrowth occurred by bundles of axons and Schwann cells which became surrounded by fibroblasts which later developed into perineurial cells leading to the formation of many small fascicles, otherwise known as mini fascicles. This process may occur when the perineurium is lacerated by the tip of a needle and it leads to the formation of a small neuroma within the nerve trunk. The initiation of degeneration is inevitable after lacerating the perineurium which is, of course, deliberately incised during “end to side” repair or during transfer of one bundle from one undamaged nerve to the distal stump of another (Fig. 3.11).

Waller (1850) described the microscopical changes in the hypoglossal and glossopharyngeal nerves of the frog following division. He noted no change for the first 4 days but then progressive varicosity and irregularity of the myelin sheath. About the twentieth day the medullary particles are completely reduced to a granular state…. where we found a presence of the nervous element indicated by numerous black granules, generally arranged in a row like the beads of a necklace. In their arrangement it is easy to detect the wavy direction characteristic of the nerve.

Hall (2005) conceives Wallerian degeneration as an active process in which the environment of a normal nerve so inimical to regeneration of axons is transformed into one which is actively receptive to that regeneration, at least for a limited period. The earliest changes affect the cytoskeleton: “the earliest evidence of fibre alteration is the dissolution and clumping of the neurofilaments and microtubules of axons” (Dyck et al. 2005a). Schwann cells in the distal nerves, both in myelinated and unmyelinated fibres, begin a process of proliferation and the fact that the Schwann cells of undamaged unmyelinated fibres seem to share the proliferation of Schwann cells of damaged myelinated fibres suggest that diffusible, trophic factors are the stimulants for this proliferation(Archer and Griffin 1993, Griffin and Hoffman 1993). Within 48 h of injury, denervated

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myelinating Schwann cells down regulate expression of those genes encoding myelin associated proteins and other proteins which are important for maintaining the organisation of nodes, paranodes, and incisures (Hall 2005). The denervated Schwann cell columns lie within the original basal lamina forming Schwann tubes, formerly known as bands of Büngner. There is proliferation too of endoneurial fibroblasts in the distal nerve. The last important feature is the increase of macrophages; some derived from “resident” cells, others “recruited from the circulation” (Stoll et  al. 1989, Griffin and Hoffman 1993). Omura et  al. (2005a) estimated that the increase in macrophages reached a peak of 150-fold by day 14 after breaking down of the blood brain barrier. Macrophages clear the debris of myelin and axoplasm during which process a Schwann cell mitogen is liberated from the debris. Significantly, they remove proteins such as the myelin associated glycoprotein (MAG) which normally inhibit axonal growth (Hall 2005). Omura et al. (2005b) measured the changes in expression of BDNF, NT3 and NT4 in muscle and nerve after different types of injuries to the peripheral nerves. The significant changes occurred only after transection of the nerve. By 7 days there was a dramatic increase in the expression of messenger RNA for BDNF in muscle and the distal nerve. The messenger RNA for NT-4 decreased. Durrenberger et al. (2004, 2006) measured increase in the expression of chemical mediators of inflammation by macrophages and glial cells after injury to human nerves. Thomas (1964) examined by electronmicroscopy the distal stumps of nerves transected 7 days earlier and found that cords of Schwann cells, often several cells thick and surrounded by a common basal lamina, extended from the distal stump into the outgrowth by about 2  mm. The endoneurial tubes shrink, more collagen is deposited within the endoneurium and there is progressive fibrosis within the distal stump (Holmes and Young 1942). As time passes the number of Schwann cells in the distal stump diminishes and they become less receptive to regenerating axons because of the decrease in the expression of receptors which are normally important in Schwann cell-axon signalling (Li et al. 1997, 1998, Hall 1999, 2005). Calder and his colleagues (Terenghi et  al. 1998) examined the distal stumps from ten patients in whom the delay before repair ranged from 8 to 53  months: “denervated S-100 positive Schwann cells remained within the distal stumps for at least 53 months, organised into typical bands of Büngner, i.e. delicate processes of densely staining Schwann cell cytoplasm enclosed by a basal lamina.” Axons were demonstrated in all specimens; some of these were myelinated (Fig.  3.12). The effects of delay on the behaviour of the Schwann cell is summarised by Niels et  al. (2007) who write: “the reduced capacity to regenerate seems to be

Surgical Disorders of the Peripheral Nerves

Fig. 3.12  Distal stump of median nerve in a 25 year old man, transected 6 months previously by bullet from military rifle. Numerous pale processes of Schwann cell cytoplasm and occasional axonal sprouts. Extensive endoneurial collagenisation ×3,245 (Electronmicroscopic studies by Mr Michael Kayser).

linked to progressive inability of chronically denervated Schwann cells to respond to axonally-derived signals, a response that has been shown to decrease significantly after only two months of denervation” (Li et al. 1998). It is now established that delay before repair is harmful not only because of the effects upon the target organs, not only because of the effects upon the neurones themselves but also because of the falling away of the capacity of the Schwann cells, the essential supporting cells of peripheral nerves, to support regeneration. These facts will not escape the attention of clinicians (Fig. 3.13a–c). The special case of the brachial plexus – A wholly different system of thought has to be employed in lesions of the brachial plexus, or for that matter of the lumbo-sacral plexus, in which there is intradural damage to the roots (Fig. 3.14). In spite of the damage to the proximal branches, the axons, whose cells of origin are outside the cord in the posterior root ganglion, remain healthy for a long time when they are avulsed from the cord or ruptured intradurally. Such axons include all those in the dorsal root; also, of course, many

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a

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b

c

Fig.  3.13  The results of rupture complicated by sepsis. Electron­ microsopic study of serial (2 cm interval) biopsies of proximal stump of sciatic nerve of 34  year old man examined 8 months after rupture

c­ omplicated by fracture and subsequent sepsis. (a) 2 cm from the tip of the proximal stump ×2,340. (b) 4  cm from the tip of the proximal stump ×3,000. (c) 6 cm from the tip of the proximal stump ×1,500.

“recurrent” fibres in the anterior root whose cells of origin are in the dorsal root ganglion. These axons, their Schwann cells and myelin sheaths remain intact and functional, detached not only from central connection but also from Seddon’s, Sunderland’s, Thomas and Holdorff’s and even our systems of classification (Figs.  3.15–3.17). This is in fact, so far as afferent neurones are concerned, a lesion of the central nervous system. Somatic efferent fibres undergo degeneration, being separated from their cells; post ganglionic autonomic efferent fibres also degenerate, because of damage to their grey rami communicantes. We did think of applying the term neuradetosis (from neuron: neurone; nerve and a etoV : adetos; unbound, loose, free) to the lesion of the afferent fibres in avulsion of the plexus. However, we suffered so severe a mauling from the late Roger Gilliatt in connection with our previous attempt at naming that we have decided not to press the point.

3.4 Types of Lesion Produced by Different Physical Agents 3.4.1 Acute Ischaemia The first effect of ischaemia upon peripheral nerves is the loss of conduction caused by anoxic block of fast axoplasmic transport systems and the paralysis of ion channel function. We have seen the effect of transient ischaemia from a short period of pressure from a suprasystolic cuff and this can be observed during exposure of limb nerves with an inflated cuff in position. For about the first 20 min stimulation of the nerve evokes a brisk muscular response by transmission through the neuromuscular junction. This response diminishes and disappears after about 30 min. Conduction within the nerve itself can still be detected for up to another 20 min.

88 Fig. 3.14  The nerve and roots detached from the spinal cord. Note the intact dorsal root ganglion cell, with healthy axons in the detached parts of the roots, the degeneration of the efferent fibre in the ventral root and of the central projections of the afferent fibres.

Surgical Disorders of the Peripheral Nerves Direct ascending tracts

Dorsal root ganglion

Dorsal root ganglion

Cells and sensory nerves

Degenerate efferent Ventral horn cell and axon

Fig. 3.15  Dorsal root ganglion 6 months after avulsion from the spinal cord. The two neuronal cell bodies appear healthy and there are numerous myelinated fibres. Solochrome cyanin ×960.

On the other hand direct stimulation of the muscle provokes a twitch which can be elicited for up to several hours. Indeed, it is the loss of that direct response which signifies impending death of the muscle, and with it, the death of the limb. Whilst it is hard to separate the effects of acute ischaemia from those of other physical agents there are examples of the effects of ischaemia alone upon conducting tissue. Harriman (1977) examined the lower limb soon after amputation in a case where femoral embolectomy successfully restored flow but failed to relieve severe pain. There were areas of muscle infarction but these were confined to the thigh, the muscles below the knee were normal in colour. The nerves in the leg were infarcted. The stump of the sciatic nerve appeared normal but as the nerves passed distally they became soft and

Afferent fibre in ventral root

grey and sections showed swelling of the myelin sheaths and axons with only a scanty cellular reaction in the epineurium. Case report: In October 1993 a man then aged 73 underwent an injection of steroid into the right forearm. There was instant severe pain and loss of function in the distribution of the right ulnar nerve. Persistence of pain and alteration of sensibility combined with failure to detect sensory nerve action potentials led to exploration (August 1995). There were slight localised changes in the flexor carpi ulnaris muscle. The ulnar nerve appeared healthy, but the ulnar artery was tortuous, calcified and distally occluded. Evidently, steroid had been injected into the ulnar artery which at this point was the principal nutrient of the ulnar nerve. An ischaemic nerve lesion had followed, chiefly affecting the larger myelin fibres with very little and much circumscribed affection of muscle. The necrotising angiopathy which complicates disorders such as rheumatoid arthritis and polyarteritis nodosa illustrate the effects of occlusion of smaller vessels in the epineurium. Dyck et al. (2005b) show that many of the epineurial arterioles become occluded and this leads to: “quite dramatic multifocal fibre degeneration, fibre loss and regeneration, extending to involve the perineurium.” Sander (1999) described the case of a diver returning from a depth of 195 ft who developed a lesion of the deep peroneal nerve affecting the sensory fibres and suggested that there had been an infarction of part of the nerve by gas bubbles within the vasa nervorum. The cases of cranial nerve palsies reviewed by Greer (1997) were thought to be caused by compression of the facial and the trigeminal nerves by gas bubbles within the osseous canals.

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89

Fig. 3.16  Rupture and avulsion of the spinal nerves forming the brachial plexus: response to intradermal injection of histamine. (left) There is a flare, mediated by the axon reflex in the territory of the avulsed first thoracic nerve. (right) There is a wheal but no flare in the dermatome of C7 which was ruptured.

Fig. 3.17  Wallerian degeneration in the ventral root of the eighth cervical nerve 6  weeks after avulsion from the spinal cord. A degenerate efferent myelinated fibre (right) compared with a non degenerated myelinated afferent fibre (left) ×11,115 (Electron microscopic studies by Mr Stephen Gshmeissner).

3.4.2 Ischaemia from Tamponade The most dramatic examples of this are provided by the catastrophic cases of infarction of the spinal cord and the roots of the spinal nerves by the injection of local anaesthetic and other agents into the invertebral foramina. Flow through radicular vessels passing into the spinal canal to the anterior

spinal artery is occluded. One such case (Brouwers et  al. 2001) was caused by a diagnostic block of the right sixth cervical nerve in a 58 year old man. Under radiological control a 22 gauge needle was positioned in the posterior caudal corner of the foramen of C6 so that the tip of the needle lay well within the foramen. No cerebrospinal fluid was aspirated and radio contrast medium showed spreading alongside the nerve root. A mixture of 0.5 ml of bupivicaine and 0.5 ml triamcinolone was injected around the nerve root over a 1 min period. At about 1 min after this the patient suddenly developed flaccid paralysis and severe breathing difficulties. It soon became clear that there was a complete lesion of the cord from C3. An MR scan at 6 h showed increased signal intensity from C2 to T1 and a further MR scan at 24 h confirmed infarction of the spinal cord. There was, later, some recovery in the function of dorsal column but little else. The patient later died. In an informed and extensive comment on this paper Nash (2001) describes other cases of severe cord ischaemia following radiofrequency lesioning of dorsal root ganglia and root sleeve injection and he emphasised the importance of the blood vessels passing with the spinal nerves through the intervertebral foramina. “The intervertebral foraminae are of critical value in the blood supply of the cord, as the feeder vessels pass through the foraminae alongside the nerve root.” Similar cases of infarction mainly of the anterior part of the cord but without a fatal outcome, are described by Houten and Errico (2002) and Somayaji et al. (2005). These cases are thoroughly presented and it seems more likely that ischaemia was caused by tamponade of the radicular vessels rather than by direct damage. We believe that a

90

similar mechanism underlies the cases of anterior cord infarction following interscalene block in which the infusion of relatively large volumes of fluid deep to the unyielding prevertebral fascia disturbs flow within the radicular vessels accompanying the spinal nerves. The permanent defects in eight patients are set out in Table 3.2. We are aware of five more cases. Case Report: A 48 year old woman underwent arthroscopic decompression for her painful left shoulder. An interscalene block was performed after induction of anaesthetic using 20  ml of 0.5% bupivicaine under stimulator control. She developed hypotension and was slow to breathe spontaneously. On awakening she had numbness and weakness in all four limbs. There was flaccid paralysis in the left upper limb and of the C5/6 and C7 muscles in the right upper limb. There were severe defects in light touch and temperature sense in the left forequarter with lesser abnormalities in the right hand. Joint position and vibration sense were maintained. There was vasomotor and sudomotor paralysis in the right hand. There was no Bernard Horner syndrome. There was some affection of both lower limbs with weakness of the muscles about the hip and defects in light touch and temperature sense in the right lower limb. Her reflexes were brisk but there was no clonus. A dissociated sensory loss was evident on the right side of the trunk, the level for light touch was T4, that for pinprick sense was T6. An MR scan done on the day after injury was reported as normal but when this was repeated at 5 days bilateral linear patchy areas of high signal were seen, extending from C3 to T5. Somatosensory evoked potentials (SSEPs) at 11 days were normal; sensory action potentials were maintained in all four limbs and motor conduction in both lower limbs was preserved. Motor conduction was absent in the median and ulnar nerves in both upper limbs. By 6 months the lower limbs had recovered. There was complete paralysis of C8 and T1 muscles on the right and of C7,C8 and T1 muscles on the left. By now she experienced severe burning pain in the shoulder girdles and chest. Quantitative sensory testing revealed normal vibration sense in all four limbs, a marked elevation of thermal thresholds especially so in the left forequarter and reduced sweating in both hands. It seems that motor neurones in the anterior horns of the segment C7, C8 and T1 were infarcted, that there was some involvement of the sympathetic outflow to both of the upper limbs and that there was a primary spinothalamic syndrome. She remains in severe pain. Case Report: a previously fit 4 year old boy fell 3 or 4 ft from the steps of a slide sustaining a fracture through the extreme lateral end of the right clavicle. There was no loss of consciousness. The clavicular fragments were markedly displaced with dropping of the forequarter, but there was no evidence of neural affection. Six days after injury, operative reduction and internal fixation were done. The distal clavicular fragments had pierced the trapezius and platysma; after

Surgical Disorders of the Peripheral Nerves

reduction the fragments were united by two sutures. A right interscalene injection of 10  ml of 0.5% bupivicaine was done. It was clear early that there was a lesion of the cord and brain stem with palsies of right cranial nerves III, IV, V, VI, VII, VIII, IX, X, XI, XII, right phrenic palsy and right sided Claude Bernard Horner syndrome. There was flaccid paralysis in the right upper limb but sweating was present in the hand. Light touch sensation was present. Magnetic resonance imaging 2 days after operation showed swelling of the right side of the brain stem and cervical spinal cord. Vertebral angiography showed no abnormality. Neurophysiological investigations were done at 16 days after the operation and showed sensory conduction in the nerves of the upper limbs whilst motor conduction was absent in the right median and ulnar nerves. Somatosensory evoked potentials were recorded at Erb’s point and also from electrodes placed over the lower cervical vertebrae by stimulating the median and ulnar nerves but the higher cervical potentials and all cortical responses were absent, suggesting a lesion at the root entry level of the cervical cord (Dr. Steven Jones, Queen Square). By 5 months the cranial nerves and the phrenic nerve had recovered but the Bernard Horner sign persisted. There was complete paralysis of the muscles innervated by the right eighth cervical and first thoracic nerves. Quantitative sensory testing 1 year after the event revealed preservation of dorsal column function and of light touch and cotton wool sensation in both upper limbs but the thresholds for cooling and warming were very elevated in the right upper limb and also in the contralateral T3 and T4 dermatomes. Sweating in both palms was normal. It seems likely, in view of the absence of abnormal findings on angiography, that the responsible lesion here was a true spasm of the right vertebral artery, causing ipsilateral lesion of the cervical cord and brain stem and that there was also occlusion of flow through the radicular artery accompanying C8. The state of this boy’s hands, 7 years after the event, is illustrated in Fig. 3.18. Evidently, interscalene block is not lightly to be undertaken: the price of avoidance of general anaesthesia or relief of pain after operation may be too high. The increasing use of ultrasonography is likely to reduce the risk to the vertebral artery but it is unlikely to remove altogether the risk of tamponade of critical radicular vessels. The blocks were given with the patient awake in two of our cases.

3.4.3 Ischaemia and Acute Compression Within Neurovascular Fascial Compartments This is caused by bleeding or infusion of fluid into a fascial compartment which encloses the nerve and axial vessels but not muscle. Nerves especially at risk include the femoral

F

F

F

M

F

55

46

46

60

4a

48

R

L

R

R

L

R

L

No

No

Yes

Yes

No

No

Yes

a

The bulbar palsy had recovered by 5 months in case 4.

F

F

60

C7,8, T1

C7,8, T1

C7,8,T1

C5,6,7,8,T1

C7,8

C5,6,7,8,T1

C5,6,7,8,T1

C4,5,6

C8,T1

T1

–

–

–

C6,7

C5

No

Yes

No

No

No

Yes

No

No

Bilateral

No

Bilateral

No

No

Bilateral

No

No

Yes

M

52

R

Upper limb sympathetic

Table 3.2  Permanent defects in eight patients after interscalene block, followed for at least 3 years. Age Sex Side Phrenic palsy Lower motor neurone Cervical sympathetic Ipsilateral Contralateral

C5,6,7,8,T1

C5,6,7,8,T1

C5,6,7,8,T1

–

–

C6,7,8,T1

C7,8,T1

C5,6,7

C7,8,T1

T3,T4

Upper limb C7,8,T1 Lower limb

–

–

Upper and lower limbs

Lower limb

Spinothalamic tract Ipsilateral Contralateral

PNI3:VAS8 Shoulders and neck

No

PNI3: VAS 8 Neck. Shoulders and right hand

PNI 3: VAS 8 neck and shoulder

No

PNI 3: VAS 8 neck and shoulders

Resolved by day 7

Neck and shoulders PNI 3; VAS 8

Pain

Reactions to Injury 91

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Surgical Disorders of the Peripheral Nerves

Fig. 3.18  The hands of an 11 year old boy 7 years after anterior cord infarction caused by interscalene block.

nerve in the groin, the ulnar nerve in the forearm and the tibial nerve in the leg (Fig. 3.19). The syndrome is a common complication of skeletal injury, of nerve blocks and of vessel puncture. The anatomical arrangements putting certain nerves at risk are outlined in Chap. 1 and examples are described in Chap. 8. The medial brachial fascial compartment syndrome (Tsao and Wilbourn 2003) is an important example, for as Wilbourn (2005) suggests it is responsible for the majority of infraclavicular plexopathies following axillary regional block and also for many of the neurovascular injuries which result from closed or penetrating injuries in this region. The progression of the lesion is characteristic: there is, almost always, pain accompanied by dysaesthesiae; loss of sensation soon follows and then, over the next 2–3 h, paralysis ensues. Wilbourne’s comment bears repeating: “distal pulses are normal as they are with most compartment syndromes because the elevated pressure, although sufficient to collapse the vasae nervori, is far below mean arterial pressure. Ultrasound, MR and CT may reveal the vascular lesion, but, considering the very brief time available for surgical decompression before irreversible nerve damage occurs, obtaining these is rarely justified.” The 16 patients described by Stenning et  al. (2005) probably fall into the syndrome described by Wilbourn. There was, in all of these cases, an injury to the axillary artery or one of its offsets caused by dislocation of the shoulder or fracture of the proximal humerus. The diagnosis of continuing bleeding into the axillary sheath was made by the delayed onset of nerve palsy or the deepening of the lesion whilst under observation. There were 87 nerve palsies. A favourable outcome was seen in all cases where urgent repair of the artery and decompression of the axillary sheath was performed (see Table  8.5). The

Fig. 3.19  Recovering femoral palsy from haematoma in the femoral triangle in a 69 year old farmer who was taking warfarin after aortic valve replacement. Two months previously he had injured his thigh whilst vaulting a gate. He experienced severe pain for 24 h but this recovered spontaneously. The area of sensory loss is outlined and the site of the Tinel sign marked. Recovery was good but not complete by 6 months.

outcome for function within the hand in another patient in whom the diagnosis was delayed by 8 weeks is shown in Fig. 3.20.

3.4.4 Ischaemia by Acute Compression from Swollen Muscle The effect upon the nerves is at least as rapid as it is in cases of compression within a neurovascular sheath. The response to correction within 3 hours is almost always gratifying and the consequences of delay before that correction are particularly severe. The vascular arrangements of nerves are such that injuries of main arteries are more likely to produce infarction of muscle than necrosis of nerve trunks. Even when ischaemic degeneration of myelinated fibres was produced by multiple arterial ligation (Hess et al. 1979) Schwann cells and their lamina tubes and fibroblasts survived and provided conditions for recovery. The evidence is distorted by

Reactions to Injury

93

Fig. 3.21  Volkmann’s ischaemic contracture. Below: the ulnar nerve exposed during flexor muscle slide 8 weeks after supracondylar fracture. The epineurial vessels and also the ulnar recurrent collateral vessels are occluded and the nerve is compressed by the swollen infarcted muscle. Above: the appearance of the hand 14 years later.

Fig.  3.20  Fracture of left proximal humerus was complicated by expanding haematoma in a 63 year old man. Two attempts to occlude the torn posterior circumflex artery by interventional radiology failed. He was seen at 8 weeks by which time he was in right heart failure, in great pain and he had a complete infraclavicular plexopathy on the left side. Six litres of altered blood were removed from the axilla. His pain was relieved. Recovery was particularly poor in the radial and median nerves. (a) MR angiogram before operation. (b) The left hand 4 years after operation.

the circumstance that ischaemia is rarely complete. Even nerves which have been seriously ischaemic for 36 h have been seen to recover adequate function. In one case of ischaemia after supracondylar fracture of the humerus complicated by thrombosis of the brachial artery, the median nerve was seen at operation to lack all vascular pedicles from elbow to wrist. It lay in the middle of the completely infarcted flexor muscles of the forearm. Three years later there was recovery of sweating and of impaired sensation in its area of distribution. The effect of increasing pressure within the osseo-fascial compartment upon the vessels running with the nerves at the elbow is illustrated in Fig.  3.21. These vessels provide the main pathway for collateral circulation at the elbow after cessation of flow through the axial artery; the consequences

of neglect are especially severe. We shall return to this serious, and as it seems, increasingly common problem in Chap. 8. It is somewhat reassuring that adequate decompression, even when delayed for some months, usually leads to relief of pain and considerable improvement in sensation. Leonard (1967) described five such cases and he observed that: “ the vasa nervorum were seen to fill upon release of the tourniquet” (Fig. 3.22). Case Report: A 33  year old man suffered injury to the popliteal artery in the course of arthroscopic meniscectomy. We saw him 5 months later when he complained of severe pain. There was a vicious equino varus deformity of the ankle and foot. Below knee amputation had been recommended. The deep flexor compartment was exposed and wide step elongation of the heel cord and the flexor tendons brought the foot into a plantigrade position. The tibial nerve and posterior tibial artery were strangled within a thickened sheath. Both were narrowed to less than one half their normal diameter, the artery was not pulsatile and was there was no flow through the epineurial vessels. They were widely decompressed. Pulsatile flow returned at the end of the procedure. The patient reported relief of his pain and a sensation of warmth in the sole of his foot on the first post operative day. Over the next

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Surgical Disorders of the Peripheral Nerves

Fig. 3.22  The popliteal artery was lacerated during arthroscopic reconstruction of the posterior cruciate ligament. There was 24 h delay before the vessel was repaired. This was followed by rhabdomyolysis and acute renal failure. Most of the muscle in the leg was excised. Nine months later step elongation of the flexor tendons improved the posture of the foot and the decompression of the tibial nerve was followed by considerable recovery of sensation and some recovery into the small muscles of the foot.

few days he regained cutaneous sensibility in the skin of the sole of the foot. Recovery into the small muscles of the foot was apparent by 6 months and some recovery of vasomotor and sudomotor function in the plantar skin was observed 2 months later. Some nerve fibres were affected by conduction block; the greater number sustained a degenerative lesion. The strangulation of nerves by scar tissue is a common occurrence in war wounds, especially when damaged or repaired nerves are covered by split skin graft. “Nothing less than a full thickness flap or tune-pedicle graft will suffice since it is important that the nerve graft should lie, a far as possible, in healthy, well vascularised tissue” (Seddon 1954). Case Report: A 38 year old soldier sustained severe soft tissue damage to the right posterior triangle from bomb fragments. The wound was closed with split skin graft. He experienced significant pain and much loss of function from a deep palsy of the spinal accessory nerve. Operation was performed 4 years later in the hope of easing his pain. The scar was excised then the cervical plexus and the spinal accessory nerves were exposed. The spinal accessory nerve appeared as a narrowed cord from the posterior margin of the sternocleidomastoid to three fingers breadth above the clavicle. The epineurial circulation was almost nonexistent. Stimulation of the nerve above, when it was first exposed, evoked no distal response. After the nerve had been liberated from scar stimulation evoked an increasingly powerful muscular response in the fibres of the upper trapezius. A free full thickness skin flap was used to cover the defect (Roderick Dunn, Salisbury).

On the day after operation the patient demonstrated powerful activity in his right trapezius (Fig. 3.23). This case is by no means exceptional. It seems there must have been prolonged conduction block involving a significant number of the efferent fibres in the spinal accessory nerve. This type of lesion is common in nerves strangled in scar. Phang et al. (2009) described the case of a 26 year old woman who developed pain in her left hip. This was attributed to previously undiagnosed bilateral hip dysplasia. Pelvic osteotomy of both hips was done. The pain in the left hip became much worse and both hips were resurfaced 6 years later. The pain in her left hip deepened so that she could walk only with crutches. When she was reviewed 10 years after the onset of her symptoms it was clear that there was a focal lesion of the left femoral nerve. There was a strong and painful Tinel sign over the nerve at the groin crease, motor and sensory conduction was impaired and electromyography confirmed a mild degree of degenerative lesion of the fibres to the quadriceps muscle. The femoral nerve was exposed (Marco Sinisi RNOH). It was tethered and sharply compressed by scar tissue over a 4 cm segment. The nerve was liberated. Her pain was improved, there was, later, improvement in the range of movement at the hip and improvement to the power of extension of the knee. By 1 year she was able to walk freely without any aid. Hindsight is always easy but it does seem that the lesion of the nerve occurred during the operation of pelvic osteotomy and her description of the new symptoms which occurred after that operation indicated neuropathic pain.

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95

Fig.  3.23  The spinal accessory nerve after excision of scar during operation 4 years after missile injury. The transverse cervical nerve (1) and the proximal accessory (2) and distal accessory (3) are exposed. A full thickness skin flap was inserted. Recovery of function was evident on the day after operation (Courtesy of Mr Roderick Dunn, Salisbury).

Fig.  3.25  A 20  year old man developed staphylococcal septicaemia after an operation for pilonidal sinus. Rhabdomyolysis led to multiple organ failure. Early fasciotomy and wide excision of the muscles of the anterior compartment of both legs was performed. There was recovery of sensation and sympathetic function in the foot: the small muscles also recovered.

Fig. 3.24  An 18 year old man with Marfan’s syndrome suffered severe and extensive rhabdomyolysis with organ failure after an operation for aortic valve replacement. Urgent and extensive fasciotomies were performed. There was considerable recovery in the peripheral nerves of both lower limbs so that he was able to walk independently by 3 years after operation.

“Critical illness neuropathy” may develop in patients who develop multi organ failure or sepsis. (Donaghy 2009a). It is possible that the intense compression of nerve trunks within oedematous and swollen limbs contributes to this disorder (Figs. 3.24 and 3.25).

3.4.5 Ischaemia Caused by Traction Lundborg and Rydevik (1973) showed that 8% elongation of a segment of a nerve could cause impairment to vascular flow and that an elongation of 10–15% could arrest all blood

flow. Relaxation within 30 min would, in most cases, lead to restoration of flow and conductivity. Nerves which are stretched over an expanding haematoma sustain the most severe lesions, especially so when the false aneurysm is pulsatile. This type of injury is associated with causalgia. Recovery for nerves embedded within the wall of the sac is generally poor (Stewart and Birch 2001). Gardiner et  al. (2006) reported a fatal outcome in a 71 year old man with a 3 month history of “sciatica.” The pain increased in severity and it was attended by rapidly deteriorating function in the lumbar plexus. The underlying cause was an aneurysm of the common iliac artery (Fig. 3.26). Ischaemia is the common factor in many of the lesions inflicted upon nerves in continuity. The situation can usually be retrieved by urgent and accurate action. The recovery of some function through nerves strangled by fibrosis for months or even years, provides an indication of their resilience: on the other hand relief of the cause within 3 or 4 h offers the only real prospect for complete recovery. The

96

Fig.  3.26  A 68  year old woman developed an intensely painful and rapidly deepening lesion of the sciatic nerve on the evening of operation for total hip arthroplasty. The nerve was exposed 3 months later and it was found stretched over an organised haematoma. Her pain improved but the nerve did not recover.

different responses evoked by acute compression of a nerve trunk within a fascial sheath versus the insidious effect of a haematoma is illustrated by the following example. Case report: A healthy 28 year old woman suffered a fracture of her left tibia and fibula. This was treated by open reduction, internal fixation and bone graft from the ipsilateral iliac crest 7 days later. A femoral nerve block was given before induction of general anaesthesia. In spite of her complaints of intense searing, shooting pain radiating down the front of her thigh and leg the anaesthetist persisted with the infusion of local anaesthetic into the groin crease. Upon awakening the patient continued to experience intense pain which required high doses of morphine during the next 3 days. She became aware that she could not feel the sole of her foot and could not move her ankle. Her haemoglobin was measured at less than 8 g per dL on the third post operative day but the significance of this was not grasped. By 7 months it was appreciated that she had developed not only a significant femoral neuropathy but also a profound sacral plexopathy. The femoral neuropathy remained very painful and she continued to experience dynamic mechanical allodynia to stimulation of the skin of the front of the thigh. She was unable to walk because of pain, weakness and loss of position sense throughout the left lower limb. NPI were performed 9 months after her injury. Sensory and motor conduction studies were normal. Electromyo­ graphy revealed a few small polyphasic motor units in the right vastus medialis, otherwise the motor units were normal. QST found that joint position sense was very poor throughout the left lower limb, indeed it could not be detected for the hip. On the other hand vibration thresholds at the left great toe were within normal limits. The thresholds to monofilament stimulation and warm sensation were

Surgical Disorders of the Peripheral Nerves

increased throughout the left lower limb and there was a rather patchy loss of pinprick sense. The pain was exacerbated by extension at the hip. The femoral nerve was explored 11 months after her injury. The fascia surrounding the nerve was greatly thickened. The nerve was narrowed, and inflamed with a much diminished epineurial circulation. There was no sign of injury to any of the individual bundles within the trunk. The nerve was decompressed over some 10 cm. A tissue catheter was placed for the infusion of local anaesthetic about the proximal part of the femoral nerve for 48 h. There was considerable improvement in her pain and in her ability to walk. By 9 months after operation the muscles about both hips and knees were graded 5 by the MRC system but she still had extremely poor joint position sense throughout the left lower limb. It seems likely that the injury to the femoral nerve was provoked by injection of bupivicaine into the epineurium but not, in all likelihood, into the perineurium and that the nerve became strangled within its fascial sheath. The chief effect of this injury was pain, a pain so severe that the more insidious and painless lesion of the sacral plexus caused by continuing bleeding from the donor site at the ipsilateral iliac crest escaped attention. The effect of the haematoma was particularly severe for the largest myelinated afferent fibres: some never recovered. The myelinated efferent fibres and the smaller myelinated afferent fibres recovered over the course of 3 months: in these the lesion was one of conduction block. The experience of severe pain at the beginning of the femoral nerve block should have led to instant cessation of the injection.

3.4.6 Reperfusion Injury Bywaters et al. (1941) described the fatal outcome after freeing people whose limbs had been crushed for some hours by the debris of bombed houses. The renal failure was caused by the release of myoglobin from ischaemic muscle. The effects upon the nerves of reperfusion are of lesser consequence than the systemic effects but as McManis et  al. (2005)point out reperfusion aggravates the ischaemic injury to the nerve fibre. Nukada et al. (1997) described the stages of reperfusion injury of nerves. The blood nerve barrier (BNB) breaks down at about 3 h; then follows oedema, demyelination and axonal degeneration. There is an infiltration of polymorphonuclear leucocytes which peaks at about 24 h. This is followed by an increase in macrophages which invade the Schwann cell and the myelin sheaths. McManis et al. (2005) consider the function of the BNB as a physiological index of oxidative injury, which causes microvascular permeability and an environment in which there is generation of oxygen free radicals.

Reactions to Injury

3.4.7 Chronic Ischaemia Eames and Lange (1967) studied clinically and by light and electron microscopy of biopsy specimens, the effect of chronic ischaemia on the sural nerves of 30 patients with arteriosclerotic obliterative disease and two with Buerger’s disease. There was a good correlation between the severity of the arterial disease and the incidence of neuropathy. The incidence of neuropathy was high: 87.5%. There was found extensive segmental demyelination and remyelination in addition to Wallerian degeneration and regeneration. The unmyelinated fibres were least affected. In all cases – not only in those with Buerger’s disease – there were marked occlusive changes in the small arterial vessels of the epineurium. The relation of these changes to “ischaemic pain” and “trophic” changes in the skin was canvassed.

3.4.8 Crush Crush injuries stand with inadvertent transection, traction or neglected ischaemia as one of the four main causes of iatrogenous lesions. Although a crush injury might be considered as an extreme form of compression the clinical evidence suggests that it is rather more than that. Unless the cause is relieved swiftly the lesion of the nerve rapidly becomes a neurotmesis. The most extreme examples of this of course is when a nerve is encircled by a suture. Much depends on the material used and the tightness of the strangulation. We have seen nerves divided by stainless steel wire used for the fixation of displaced fragments of bone. Whilst recovery might be anticipated after removal of a braided suture, within an hour or two, nerves do not recover after this time (Fig. 3.27).

Fig. 3.27  A 48 year old woman experienced severe pain and an incomplete lesion of the sciatic nerve after operation of total hip arthroplasty. The nerve was exposed 8 weeks later. It had been transfixed by a braided suture. There was some moderation in her pain but little recovery for the nerve.

97

Not only do catgut sutures crush, they also provoke a brisk inflammatory response. Not only does an encircling suture strangle a nerve it also tethers it so that there is the added element of stretch. Severe pain is usual and it is often related to posture. Attempted stretching of the limb against the tethered nerve provokes intense pain (Fig. 3.28). We have seen more than 40 patients in whom main nerves had become inadvertently strangled by a suture passed around, or through, the nerve. When the suture was removed within hours of the operation there was instant relief of pain and a high level of recovery. Relief of pain was usual after removal of the suture up to about 2 weeks. In these cases recovery was always incomplete and when the ligature was removed later there was very little useful recovery. Hindsight suggests that that the better course might have been resection and suture of the relatively short damaged segment. Nerves entrapped within fractures or joints certainly pass through a period of ischaemic conduction block which may last for as long as 2 or 3 days. After that there is demyelination but recovery may be anticipated if the nerve is set free within 7–10 days. The situation is made very much worse if a compression plate or tension band is applied to the fracture without extricating the nerve. The resected material in such cases shows transection of normal structures with an interposed zone of dense fibrosis. The effect of compression between the bone and the plate is illustrated by a case treated by an alert surgeon who, drawing to the close of a difficult operation of internal fixation of a fractured shaft of humerus, realised that the hitherto protected radial nerve had inadvertently slipped between the plate and the bone. The nerve was

Fig. 3.28  A 38 year old woman experienced intense pain and a partial lesion of the ulnar nerve after repair of the capsule of the joint using an arthroscope. Her pain was worsened by attempted extension at the elbow. The nerve was exposed 4 days later, it had been caught by a clip. The clip was removed and her pain was relieved. There was considerable recovery in the ulnar nerve but she did not recover vasomotor and sudomotor control and there was lasting weakness of the small muscles.

98

Fig.  3.29  The appearance of a radial nerve after extrication from beneath a compression plate 48 h after first operation. There was relief of pain but only incomplete recovery so that later flexor to extensor transfer was necessary (Courtesy of Marco Sinisi, RNOH).

at once extricated. The duration of compression was, at the most, 5 min. The nerve was re-explored at that surgeon’s insistence some 6 weeks later even though an advancing Tinel sign offered the prospect of spontaneous recovery. The nerve had reconstituted, the epineurium was thickened but the epineurial vessels were patent and the bundles within had not been severed. Recovery proceeded uneventfully as an axonotmesis. Other examples of a good outcome after urgent correction of the situation are outlined in Chap. 8. Nerves extricated from within a fracture 2 or 3 days of the injury usually recover. There is certainly some narrowing of the nerve trunk in these cases but the perineurium is not breached. All may not be well within the perineurium: the lesion is mixed with elements of ischaemic and demyelinating conduction block interspersed with varying degrees of axonal degeneration (Fig. 3.29).

3.4.9 Compression – Acute Thomas and Holdorff (1993) consider crush and compression separately. It is likely that in the latter type of injury the lesion is localised – a mixture of demyelination and axonal interruption (Richardson and Thomas 1979). Certainly, with more severe pressure there is axonal interruption but that interruption is within the Schwann cell basal lamina tubes. Thomas and Holdorff show a figure which well illustrates this point. Dyck, Dyck and Engelstad (2005a) reserve the term compression for a “monophasic application of force exerted to the nerve from the outside so that it is compressed against a rigid underlying structure. Acute compression may also occur repeatedly.” They rightly point out that “entrapment” should be reserved for a nerve passing through an opening that is too small for it. This effectively tethers the

Surgical Disorders of the Peripheral Nerves

nerve so that it becomes subject to stretch. Platt (1928) described precisely this lesion in relation to the radial nerve stretched over an ununited fracture of the humeral shaft. Closed compression lesion, in which an external force is applied to the limb of a conscious patient usually leads to a conduction block. Such is the event in radial palsy caused by a badly applied plaster of Paris splint or the older style of crutch favoured by the cook in Treasure Island. Case report: A fit 23 year old woman fell deeply asleep lying on her left side for about 2 h and awoke with a complete left sided radial palsy. She had no pain, there was no Tinel sign and there was some preservation of cutaneous sensibility within the distribution of the nerve. She was fitted with a dynamic extension splint and at 6 weeks the first evidence of recovery into the extensor muscles of the wrist was apparent. Neurophysiological investigations were performed 9 weeks later which revealed normal conduction and a normal recruitment to a full pattern of motor units of normal appearance. Her recovery was complete by 12 weeks from the incident. The lesion was one of pure conduction block. More sustained compression leads to deeper lesions (Tait and Danton 1991). Case Report: A slim healthy 22 year old woman sustained a mid shaft right femoral fracture through an area of fibrous dysplasia. The operation of internal fixation was difficult and lasted for 7 h during which time the contralateral left leg was kept in a flexed abducted position to permit the use of an image intensifier. A muscle relaxant (Rocuronium) was used. She awoke with a complete left sciatic palsy. There was no bruising in the left thigh or the buttock. NPI at 2 months after operation showed a complete degenerative lesion of the nerves and muscles of the leg and foot with extensive denervation in the hamstring muscles. She was examined again 8 months after the incident, when she reported increasingly severe pain but some recovery of feeling into her foot. Recovery of power of the knee flexor muscles was measured at MRC Grade 4 and there was perceptible activity in the flexor muscles of the heel. There was complete vasomotor and sudomotor paralysis in the foot. There were strong Tinel signs for both divisions of the sciatic nerve in the leg indicating a rate of regeneration of a little more than 2 mm per day. By 14 months all muscle groups in the leg and foot were recovering and she could localise light touch to the skin of the foot. There was still sympathetic paralysis in the sole of the foot and she still had pain. NPI were repeated. No sensory conduction could be demonstrated in the nerves of the leg nor was motor conduction demonstrable for the tibial nerve. Motor conduction in the common peroneal nerve was reduced and slowed. Electromyography of the leg muscles revealed persisting denervation with reinnervation by collateral sprouting with many wide polyphasic units and irregular recruitment. By 18 months she showed further recovery and some improvement of her pain. Quantitative sensory testing (Praveen Anand Imperial College) showed elevated thermal

Reactions to Injury

thresholds in the plantar skin but the threshold to cooling fell within normal limits. The threshold to monofilament sensation was elevated and pinprick was felt as an unpleasantly sharp sensation from the mid calf down. Sweating in the left sole was reduced to about one half of that on the right. The threshold to vibration was markedly elevated. It seems that the largest and the smallest fibres suffered most. Such lesions can prove very serious in the growing child because of the disturbance of growth. Case Report: A 12 year old boy fell from a swing and experienced much pain. There was deep bruising in the left buttock and he presented with a high sciatic palsy which involved the superior gluteal nerve. The common peroneal nerve was more severely affected, NPI at 6 weeks revealing loss of conduction and denervation of all of the muscles innervated by that nerve. Sensory conduction was diminished in the tibial division and there were signs of partial denervation of all tibial muscles. There was considerable muscular recovery by 1 year. Sensory conduction in the tibial nerve had recovered. There was no sensory conduction in the common peroneal nerve and motor conduction was slowed and reduced in amplitude to just under 10% of the uninjured side. At 2 years the nerve had recovered but the left lower limb was shorter by 1.5 cm and the heel was fixed in equino varus deformity. The lesion in the more severe compression injuries is usually much more than a conduction block. The tempo of recovery varies from one population of nerve fibres to another

Fig. 3.30  A 50 year old man who required crutches developed “carpal tunnel syndrome” in his right hand. Two operations were performed with no lasting relief of his symptoms. His symptoms were improved after modification of his crutches and by the use of a silicone pad.

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and it is not unusual to see poor recovery for somatic unmyelinated fibres. As a rule, the sympathetic efferent fibres suffer least. Some nerves never recover.

3.4.10 Chronic Nerve Compression Entrapment syndromes provide most of the examples of chronic nerve compression, though the latter is one of the causes of neuropathy after ionising radiation and in other conditions in which a nerve is deformed over a tumour or bony abnormality (Fig. 3.30). Clearly, there are a number of mechanisms. Episodic ischaemia accounts for the nocturnal paraesthesiae in “carpal tunnel syndrome,” and possibly continued ischaemia accounts for the continuous symptoms (Hongell and Mattson 1971). Evidence about the size of fibres affected comes from Thomas and Fullerton (1963), and of segmental demyelination from Neary and Eames (1975). The systematic studies of MacKinnon and her colleagues (MacKinnon et al. 1985; Dellon and MacKinnon 1988; MacKinnon and Dellon 1986) showed that the earliest changes occurred in the small vessels of the endo- and perineurium. The presence of numerous Renaut corpuscles (Renaut 1881; Jefferson et al. 1981) was also observed, consistent with the observation made by Hill and Hall (1999) that these aggregate at sites of entrapment, and represent a response to local injury to the endoneurial

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Fig. 3.31  Intraneural ganglion of the common peroneal nerve. Top left: the patient presented with a painful foot drop of 9 months duration. The area of sensory loss is shown. Top right: magnetic resonance scan

shows the extent of the lesion and the communication with the proximal tibio-fibular joint. Below left: the ganglion is shown at operation. Below right: the resected specimen includes the articular branch.

capillaries. Later, there is perineurial and epineurial fibrosis, followed by loss of fibres and thinning of myelin sheaths. At the end of the process there is damage to unmyelinated fibres. Compression may be intermittent as it was in the case described by Mannan et al. (2008). A 25 year old woman experienced intense but intermittent sciatica which was closely related to the menstrual cycle. She endured this for many months and became dependent upon crutches and even a wheel chair. Her pain was relieved by removal of a focus of endometrial cysts which had infiltrated the sciatic nerve in the upper thigh. Bendszus et al.(2003) described two cases of severe but intermittent sciatica, provoked by sitting or lying and eased by standing or walking, which were caused by varicose veins enveloping the sciatic nerve. Pain was relieved by excision of the varicosities. The perineurium and the intraneurial ganglion. This rather mysterious disorder is often a source of needless maiming. Spinner et  al. (2003), Spinner et  al. 2006) have shown that the pedicle of the ganglion is, in fact, the articular branch of the nerve and that this is a pathway for synovial

fluid passing from an adjacent joint into the trunk of the nerve. It seems that the pathway is epineurial, and the perineurium acts as a barrier between the endoneurium and the increasing volume of synovial fluid. The perineurium, with its contents, is subjected to prolonged and varying compression. This may explain the high success following successfully conducted operations which involve not only decompression of the nerve but also excision of the articular branch through which synovial fluid tracks. The early recovery after months or even years of pain and weakness is remarkable indicating that the lesion of the nerve fibres is predominantly one of conduction block (Fig. 3.31).

3.4.11 Traction or Stretch Injury Peripheral nerves outside the spinal canal have considerable tensile strength, but their function is damaged by an elongation of 12% or more, the extent of damage varying with the

Reactions to Injury

suddenness and the length of time during which that elongation is maintained. Lundborg and Rydevik (1973) showed that venous flow was blocked when a nerve was stretched by 8% of its resting length, and that stretching by 15% produced ischaemia. At first, elongation is permitted by the elongation of the epineurium and the straightening of the irregular course of the fibres within the fascicles (Haftek 1970; Clarke and Bearn 1972). The latter drew attention to the significance of the “spiral bands of Fontana,” confirming his conclusion that the banding appearance of the peripheral nerve is due to the wave-like alignment of its individual nerve fibres. As the fibres are straightened the banding disappears. It is difficult to separate the effects of stretch upon the conducting tissue from those imposed upon the vessels. Ochs et al. (2000) studied the effects of stretch upon isolated segments of nerve placed within an oxygen chamber. A very light stretch straightened out the zig zag disposition of the nerve fibres. The spiral bands of Fontana were erased when the nerve was elongated to about 15%. This effect was achieved with an applied tension of less than 0.1 g. An applied tension of 2 g or more induced beading of the nerve fibres which was maximal at 4–5 g of tension. The change in the nerve was rapid and it was also rapidly reversible. The compound nerve action potential was actually augmented in the earliest stages before it fell away. Haftek (1970) added the observation that “before rupture of the perineurium the damage to the nerve fibres is either neurapraxia or axonotmesis, because the endoneurial sheaths and Schwann fibres remain intact.” Next, the calibre of the fibres is diminished, the endoneurial space is diminished and myelin is disrupted (Chalk and Dyck 1993). Then rupture starts: first the epineurium and lastly the nerve fibres. The longitudinal extent of damage is considerable. The process of damage by a bullet passing through soft tissue near a nerve is comparable. Such lesions are usually conduction blocks. Seddon (1975) illustrates one such case, where the epineurium was split by the passage of a bullet but the bundles were intact. It is usual, in closed traction lesion, to see that the epineurium has ruptured but the perineurium within remains intact, albeit stretched. These injuries are usually complicated by bleeding into the epineurium, extending over many centimetres. However we have encountered cases where the perineurium was ruptured even though the epineurium remained intact in nerves sharply angulated over a fragment of bone. It is much easier to recognise this pattern when the nerve is explored within 24 h of the injury (Figs.  3.32a–c). In the extreme traction injury the nerve is ruptured or avulsed from muscle. The wide recoil of the stumps be reduced only by urgent operation. We have seen nerves destroyed over a length of 15 cm by the action of a drill during operation. The manipulation of any joint which has been fixed for some time in a position of deformity always carries the risk of damage to nerves and vessels passing across it and accustomed to the position of deformity. In one case of attempted correction of long standing flexion deformity of both knees

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in an adult with cerebral palsy loss of pulses at the ankles was recognised by the staff of the recovery ward. No action was taken and above knee amputation of one lower limb proved necessary. Aspden and Porter (1994) reported a case in which the sciatic nerve was damaged by straightening knees that had long been flexed because of spastic diplegia. Birch et  al. (1991) described three cases in which the brachial plexus was damaged during manipulation of the shoulder for “frozen shoulder.” In one of these cases, manipulation had caused anterior dislocation. The plexus was explored in this case; there was no interruption of continuity, and recovery followed. Case report: A fit man, in age 64 years, developed severe osteoarthritis in his right knee complicated by severe fixed flexion deformity. Capsulotomy was done to regain extension as the first step in total arthroplasty of the joint. The surgeon avoided a suprasystolic cuff because of anticipated difficulties. A complete lesion of the tibial and common peroneal nerves was recognised on the evening of operation. Neurophysiological investigations at 22 months revealed no sensory or motor conduction. Considerable reinnervation of the tibial muscles was demonstrated and the distal muscles of the anterior compartment were also recovering (EHL, EDC) However, tibialis anterior was fibrosed, the muscle was silent and the concentric needle met with the characteristic, gritty resistance. In addition to the traction injury of the nerves it is likely that flow through the anterior tibial artery was interrupted. The patient had been discharged from the first hospital in spite of severe disability and continuing pain. Case report: A 13 year old girl with severe cerebral palsy was treated by anterior transfer of the hamstring muscles of the left knee with the object of correcting flexion deformity. On the day of operation she developed intense pain in the leg and foot. This did not respond to opiates and neither the child nor her mother were able to sleep for 8 weeks. The child lost a good deal of weight. We saw her at 8 weeks when it was clear that the nerve lesion, although deep, was not complete. The child had causalgia. The extent of discoloured skin matched the areas of intense mechanical allodynia. At operation both tibial and common peroneal nerves were found stretched and compressed, indeed strangled, by fascia and by scar in the popliteal fossa. The common peroneal nerve was reduced to about one half of normal diameter and the epineurial vessels were obliterated. The tibial nerve was inflamed and embedded in vascular adhesions. An external neurolysis was done, and a tissue catheter placed to permit infusion of local anaesthetic for 48 h after operation. The pain from the tibial nerve was improved, the pain from the common peroneal nerve persisted. Both nerves recovered. By about 9 months the child was able to tolerate shoes and weight bearing. Her mother described how vasomotor and sudomotor disturbance in the foot persisted even after pain had improved. In this case stretching of the nerves damaged the epineurial vessels, the myelin sheath and the axons, and this was compounded by compression from

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a

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b

c

Fig.  3.32  Traction injury. (a) The circumflex nerve exposed 4  days after anterior dislocation of shoulder. The bundles had ruptured and retracted within the intact epineurium. (b) Traction injury of the common peroneal nerve from varus injury at the knee. There was extensive recovery over the course of 9 months (axonotmesis). (c) A more violent

traction injury of the right upper limb. The median nerve was elongated by more than 100%. Over the course of the next 3 years there was recovery of cutaneous sensation in the hand, and some recovery of the flexor muscles of the forearm. The sympathetic fibres never recovered.

bleeding and by the persistence of inflammation induced by haematoma. A wide range of drugs had been used in an attempt to control the pain without considering the possibility of a persisting focal noxious agent at work. There may be a case, not only for monitoring of nerve conduction, but also the flow through adjacent main arteries before, during and after operations for the correction of severe flexion deformity at the knee and other joints as recommended by Martin et al. (2006). Somewhat similar circumstances obtain in limb lengthening operations, even though it is usual to effect a change slowly, over a period of weeks. It has been argued that, if during the process, signs or symptoms of actual or impending neural damage appear, the process can be stopped to permit recovery. Galardi et al. (1990) are less reassuring: they studied events in the limbs of five patients whose tibiae were lengthened at the rate of 1  mm per day over a period of 53–107  days. The ages of the patients ranged from 3 to 24 years. The conduction velocity of nerves and the electrical activity in muscles during lengthening were examined

and evidence of damage to myelin sheaths and axons was found in all cases. These findings evidently raise the question of whether nerve function should always be monitored during correction of major deformities of long standing. This concept was used by Nogueira et al. (2003) who used a pressure sense monitoring device during 814 limb lengthening procedures. Seventy-six (9.3%) nerve lesions occurred. Nerves were most at risk in double level lengthening of the tibia and in skeletal dysplasia. Most of the affected nerves were decompressed; 74 of the 76 recovered. Clear conclusions are drawn from this admirable work: the rate of lengthening should be slow; affected nerves should be decompressed as soon as possible; monitoring of nerve function by a pressure sense device is more sensitive than clinical examination and the largest myelinated fibres are the most vulnerable. Paley (1990) provides sound advice about prevention. Analysis of the deformity provides information about the potential distortion of neurovascular bundles; the drill hole for the frame screws should be made opposite to the bundle and neuromuscular blocking agents should not be used.

Reactions to Injury

Severe pain indicates damage to a nerve or vessel or both. If a Tinel sign is evoked by tapping the transfixion wire then it has certainly passed through, or close to, a trunk nerve. Polo et al. (1997) lengthened the lower limbs in 14 patients with achondroplasia and found that the common peroneal nerve was most vulnerable and that the lesion was detectible in the first days of elongation. The prognosis for nerves injured during correction of deformity or limb elongation is poor. Case report: A 12 year old child with Stüve-Weidemann syndrome had osteotomy of the femur for flexion deformity of the lower limb. The operation was done under epidural anaesthetic and a suprasystolic cuff was placed about the upper part of the thigh. There was a complete, but painless, sciatic palsy. NPI confirmed deep axonopathy without any evidence of generalised neuropathy. The tibial and common peroneal nerves were exposed 5 months later. They were unblemished. The amplitude of CNAP’s across the presumed level of lesion was diminished. At 36  months, there was some recovery for the tibial nerve but very little for the common peroneal nerve. Case report: A 35 year old woman with severe deformity at the knee and in the leg after operations for Blount’s disease, was treated by two level osteotomy of the tibia and fibula stabilised by an Ilizarov frame. This was followed by a deep, but painless, palsy of the tibial and common peroneal nerves. The nerves were exposed at 14 days to exclude the possibility of haematoma. They were unblemished. There was little recovery for either nerve at 18 months.

3.4.12 Thermal Injury The effects of cold have been studied extensively (Franz and Iggo 1968; Lundberg 1948; Douglas and Malcolm 1955; Dodt 1953; Denny Brown et  al. 1945). Bickford (1939)), cooling the ulnar nerve, found a sequential loss of the different modalities of sensation: first, appreciation of cold, and last, sensibility to pain, touch and warmth. As Thomas and Holdorff (1993) remark “observations on non freezing cold injury of nerve have largely stemmed from the exigencies of war”.

In the First World War “trench foot” was a common cause of disablement; in the Second World War “immersion foot” was a more common occurrence (Ungley et al. 1945). Donaghy (2009b) describes the freezing injury of frost bite, in which there is tissue necrosis often with a clear demarcation between living and dead tissue. Wallerian degeneration is an early feature of these injuries. One of us experienced this injury to a relatively minor degree and noted the loss of sensation in the affected toes which persisted for more than 10 years, a

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sensory loss which increased and became painful when the foot was exposed to mild cooling. The terrible pain which often complicates more severe frost bite is described by Maurice Herzog from his experience with the French expedition to Annapurna. The second type of cold injury recognised by Donaghy follows prolonged immersion in cold water or prolonged exposure to cold around freezing point. Irwin et al. (1997) had the opportunity of investigating the neural damage in a case of “trench foot” or “non freezing cold injury.” A 40 year old Asian man, homeless in the UK through the operation of free market principles, was subjected to exposure lasting 19 days, during 8 of which the ambient temperature was below 0°c. He lost all function and sensibility in his feet, and, ultimately, several toes. Sensory nerve function was carefully measured and recorded; at the time of removal of dead tissue, 4 weeks after admission, a biopsy of viable tissue was taken from the plantar surface of the right great toe. There was evidence of damage to both myelinated and unmyelinated nerve fibres, possibly, the authors’ speculate, “in a cycle of ischaemia and reperfusion.” In civil practice at the present time, it is rather the effects of heat that concern the clinician, principally because of damage to the sciatic nerve by the heat of polymerising cement during arthroplasty of the hip. The effects of heat seem to have received little attention. Nerves can be destroyed by extremes of heat, or by diathermy during operation. Hoogeveen et al. (1991) investigated the effect of heating a 5 mm segment of the sciatic nerve of the rat for 30 min at 45°C. They found that this produced swelling of the endothelium of the neural blood vessels and Wallerian degeneration of all the nerve fibres. There was of course total loss of motor function. The process in the nerves was, however, reversible: regeneration occurred over 4–5 weeks. The vascular changes were not apparently reversible. Xu and Pollock (1994) examined physiologically and morphologically the effect of heat ranging from 47°C to 58°C on rat sciatic nerve. Unmyelinated fibres showed a greater direct vulnerability to hyperthermia, first manifest as a reversible conduction block and at higher temperatures by immediate and selective axonal degeneration. Lower grade thermal injury caused a delayed selective loss of myelinated fibres. Xu and Pollock remark in relation to the latter effect: “Evidence from this study suggests that this is secondary to a heat-induced angiopathy, immediately and diffusely manifest in the vasa nervorum and giving rise to a progressive and ultimately severe reduction in nerve blood flow.” The relative sparing of unmyelinated fibres was attributed to their greater resistance to ischaemia. It is necessary in considering risk to the sciatic nerve in operation for hip replacement, to recall that the temperature of polymerising cement rises to 95°C about 15 min after mixing, and remains above 70°C for another 12 min. Birch et al. (1992) had the opportunity of examining a length of sciatic nerve damaged by the heat of polymerising cement. They later took the

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a

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a

b b

Fig. 3.33  A case of damage to the sciatic nerve by cement during operation for arthroplasty of the hip. (a) The sciatic nerve seen at operation a year after initial operation. The extruded cement can be seen in relation to the nerve. (b) The severely damaged common peroneal component was resected and grafted. The proximal stump appeared to be relatively healthy at 1 cm proximal to the cement. Toluidine blue ×100.

opportunity of studying the effect of the heat of polymerising cement on the median nerve of an arm recently amputated because of a complete pre-ganglionic injury of the brachial plexus. The remarkable feature was the localised nature of the lesion: although at the site of burning there was destruction of axoplasm and disruption of myelin, a normal pattern of myelinated and unmyelinated fibres was found 10  mm from the margin of the cement (Figs. 3.33a, b and 3.34 a, b). Wilkinson and Clarke (1992) reported two cases of burns to the brachial plexus in patients who fell asleep with their arms draped over the back of heated towel rails. Later decompression was performed in one case, revealing extensive fibrosis of the nerves and adjacent tissues. Recovery was poor in both these cases. Tubiana (1988) made rather sombre observations on the evolution of the treatment of these injuries during a long and illustrious career, noting little significant improvement. Salisbury and Dingeldein (1988) and Salzberg and Salisbury (1991) provide extensive reviews emphasising the necessity for early incision of the encircling eschar (Fig. 3.35). A clear description of the technique, with

Fig.  3.34  Thermal damage to the median nerve after exposure to the heat of setting cement, showing the limited longitudinal extent of the neural lesion. (Electronmicroscopic studies by Mr Stephen Gschmeissner.) (a) Virtual destruction of axoplasm and cellular elements at the site of the lesion ×3,600. (b) Healthy axons and collagen 10 mm from site of injury ×3,000.

emphasis on avoiding damage to underlying nerves, is given. Chalain and Clarke(2000) review the field of thermal injuries, their pathophysiology and the treatment of the consequences in children. Bonney (2002) describes the tragic consequences of the flash burns incurred during the Battle of Jutland which affected the face and the hands and were caused by the momentary flame of high explosives.

3.4.13 Electric Shock Hobby and Laing (1988) recognised four groups of electrical injury in 169 cases from a total of 3,300 patients: true electrical injury, from current passing from the conductor through

Reactions to Injury

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Fig. 3.35  Urgent and extensive division of the skin and fascia in a full thickness burn from petrol fire (Courtesy of Major K Brown RAMC).

the skin to the tissues; “arc” burn, where a current passes external to the body to the ground; secondary flame burn, from ignited clothing; and direct burn, from a hot electrical element. Reasonable spontaneous recovery occurred in those cases where the blood supply to the adjacent tissues was not destroyed. Di Vincenti et al. (1969) reported 69 cases of electrical burns, mostly from high tension injuries. The median and ulnar nerves were the most frequently damaged and the lesions were often severe and irreparable. Because nerves are good conductors the neurovascular bundles may be destroyed. Clifton et al. (2000) advise immediate repair of trunk nerves charred in electrical burns using nerve grafts which are covered by free full thickness skin flaps or by a vascularised nerve graft, such as the lateral cutaneous nerve of forearm within a free lateral arm flap. When electrical contact is brief there may be little burning but the passage of electrical current causes break down of the cell membranes. Clifton and colleagues describe this process of electroporation which is caused: “by polar water molecules being driven into molecular scale defects in the lipid bilayer component of the cell membrane, causing the defects to enlarge, with an increase in permeability, and the membrane to rupture.” Muscle and nerve cells are particularly susceptible to this injury which is responsible for some of the immediate clinical signs such as muscle spasms and episthotonus. The case described by Thaventhiran et al. (2001) provides one example of this phenomenon. The patient was injured by contact with a 20,000 voltage AC supply, the current entering at the right arm and exiting through the left elbow. He was completely paralysed below the neck but over

the subsequent 5 years there was extensive recovery although he remained doubly incontinent: “the remarkable degree of peripheral nerve regeneration and recovery seen in this patient suggests that the axons were selectively injured, leaving the surrounding tissue including the Schwann cells intact to enable subsequent regeneration.” The recovery of the very severe and generalised sensory motor polyneuropathy unmasked the extent of the myelopathy. There are some similarities between this case that of a 34 year old man who was struck by lightning. He suffered immediate loss of consciousness and cardiac arrest but was successfully revived. He was wearing a heavy gold chain at the time and a deep entry burn was seen on the right side of his neck with an exit burn on the left side. There were second degree flash burns to the chest, groin, upper and lower legs and there were superficial burns over the whole of his torso which formed a feathery or fern leaf pattern. He had a C5 tetraplegia with both urinary and faecal incontinence. His rehabilitation was directed by Dr Lal Landham (Rochester) and we were given the opportunity to examine him on several occasions. By 2 years after injury he had regained considerable recovery of power in all four limbs so that he could walk and he had regained urinary and faecal control. Quantitative sensory testing showed normal sensory thresholds for all modalities in all four limbs except for an elevated vibration threshold in the right lower limb. Neurophysiological investigations confirmed normal sensory and motor conduction but persisting denervation of the C5 and C6 myotomes. He had sustained a severe, diffuse sensory motor neuropathy. The permanent defect lay with the anterior horn cells at C5

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findings did nothing to explain the transient interruption of nerve function after percussive injury described by DennyBrown and Brenner (1944).

3.4.15 Injection Injury

Fig.  3.36  Function in the upper limbs 2 years after lightning strike. Note the atrophy of the muscles of the shoulder and in the arm.

and C6 and it seems likely that the site of the entry and exit burns in the neck is relevant. Perhaps these neurones were destroyed by electroporation? (Fig. 3.36). Quantitative sensory testing may reveal abnormalities which cannot be detected by classical neurophysiological investigations. A 40 year old man was electrocuted (AC current), by a faulty fuse in his house. The current passed through his right ear down to his right hand. He experienced very considerable pain and was unable to use his right upper limb. NPI were performed, first, 1 month after the injury and then again after 6 months which showed no disturbance either of sensory or motor conduction. Electromyography showed a pattern consistent with conduction block. However, QST at 6 months revealed diminished pinprick sensation in the right forearm and hand but also in the right trunk. Thermal thresholds were elevated in the right thenar eminence, with paradoxical burning on cooling by 7.2°C. There was also a suggestion of elevated thresholds in his right T2 region. Vibration thresholds were elevated at the right thumb and middle finger. In the same area there was elevation of monofilament threshold. Cotton wool sensation was reduced in the same distribution as pinprick sense. His sweating was preserved.

3.4.14 Percussion Injury Richardson and Thomas (1979) studied the effects of percussion injury. The clinical application in the peripheral nerve field is perhaps slight, but the authors indicate that their results could give some indication of events in injury of the spinal cord, in spite of the difference in structure between central and peripheral nervous tissue. The lesion appears principally to be a localised axonal interruption with later degeneration. Richardson and Thomas noted that their

The perineurium may be lacerated by the point of a needle an event which causes severe pain in the conscious patient. If that complaint of pain is ignored and through an injection into the nerve, the consequences may be severe. The damaging substances commonly injected into nerves are: steroid preparations; anaesthetic agents for intravenous use such as thiopentone; non steroidal anti-inflammatory drugs; anxiolytic agents such as diazepam; antibiotics; and local anaesthetics. The nerves most commonly affected are the brachial plexus in the neck and axilla, the radial nerve in the arm, the median at the elbow and the sciatic in the buttock. Usually, the occurrence of severe local and radiated pain makes it plain that the drug has been injected into the nerve. The onset of later and sensory paralysis may, however, be delayed for some hours. Although Hudson (1984) suggested that the ill effects arise from intraneural injection rather than from injecting near the nerve and later diffusion, it is hard to resist the speculation that the latter must sometimes be the responsible mechanism, a suggestion which is supported by Kline and Hudson (1995). The response of the nerve to the needle and to the substances injected is illustrated by some cases that we have treated. 1. A 40 year old man of slender physique came to operation which required exposure of the common peroneal nerve at the knee. After induction of general anaesthesia the line of incision was infiltrated with 0.25% bupivicaine. This provoked a twitch in the extensor muscles of the ankle indicating that the needle had been passed too deeply. The nerve was then exposed and the epineurium was greatly distended by the injected fluid. The bundles within were intact but the epineurial circulation had disappeared over a segment of some 4 cm. The epineurium was incised to decompress the nerve; the operation was then completed. On awakening he had a foot drop with sensory loss but no pain. By 6 h, sensation had recovered and there was the first evidence of recovery into the dorsiflexor muscles. Recovery was complete by 36 h. 2. A 45 year old woman with rheumatoid arthritis, for which she was taking prednisolone, experienced sudden severe shooting pain into her hand during venepuncture at the elbow. Pain persisted and sensation remained abnormal in the index and middle fingers whereas muscle power and sympathetic function remained intact. At 24 months the amplitude and velocity of sensory conduction from the affected digits was reduced to less than one half of

Reactions to Injury

normal. The median nerve was explored at the level of lesion which was marked by a strong Tinel sign. The epineurium was thickened and adherent to adjacent structures; epineurotomy revealed a neuroma of two bundles. After external neurolysis local anaesthetic was infused about the nerve by catheter for 24 h. Her pain was greatly improved. 3. The sciatic nerve of a 60 year old woman was blocked by 30 ml of 0.5% bupivicaine during operation for total knee replacement. Numbness and weakness were apparent within a few minutes but pain did not develop until 7 days had passed, increasing in intensity for the next 14 days. This was expressed as burning pins and needles in the sole of the foot and as shooting or electrical pain to the dorsum of the foot. The common peroneal nerve recovered by 6 weeks but the lesion of the tibial nerve remained dense. NPI at 14 weeks confirmed loss of conduction for the tibial nerve but recovery of motor conduction in the common peroneal nerve. Normal motor units were demonstrated in gastrocnemius but there were fibrillations in the abductor hallucis. Pain resolved spontaneously by 16 weeks, recovery was extensive by 36 weeks and by this time conduction was now detectable in the sural nerve, but the tibial nerve action potential was still absent and sympathetic paralysis persisted. It seems that recovery was better for the larger myelinated fibres than it was for the finely myelinated and non myelinated fibres. 4. A 6 year old boy was given an injection of antibiotics into the buttock and he experienced instantaneous and severe pain. When he was seen 2 years later there was a severe equinovarus deformity with shortening of the femur, the tibia and the foot on the ipsilateral side. Neurophysiological investigations at that time revealed an extensive degenerative lesion. There was no motor or sensory conduction in the common peroneal nerve, sensory conduction was preserved in the sural nerve. Denervation of the muscles was widespread, but rather deeper for the common peroneal nerve than it was for the tibial divisions. The posture of the foot was improved by an extensive operation which included elongation of the tendo Achillis, slide of the plantar muscles, shortening of the lateral column of the foot, calcaneal osteotomy and anterior transfer of tibialis posterior (Mr Fergal Monsell, RNOH). Experience with injection injuries in human beings does not always match with that of injection into the nerves of rats, just as the behaviour of the former is not regularly matched by that of the latter. Full recovery is by no means invariable; noxious injection is often followed by epineurial fibrosis and sometimes by dense intraneural scarring. Persistence of pain following an injection of steroid for carpal tunnel syndrome led to exploration of the median nerve in four patients at intervals ranging from 2 weeks to 8 weeks after injection. The nerves were found inflamed and swollen over a length of some 3 cm and they were surrounded by filmy adhesions, but

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there were no signs of penetration of the trunk by the needle. Injection of steroids into the buttock of a 64 year old man with psoriasis and scleroderma was followed, at about 1 hour, by complete common peroneal palsy and a painful partial lesion of the tibial nerve. The pain resolved spontaneously at about 3 months. Neurophysiological investigations at 1 year showed extensive demyelination with some axonopathy. Sensory conduction was absent: motor conduction was reduced in amplitude and in velocity. Polyphasic potentials were widespread in the muscles sampled but there were no fibrillations. It is possible that diffusion of the agent provoked vasculitis within and about the nerve in this case. The prognosis is not at all good. Pandian et al. (2006) followed 65 lesions of sciatic nerve and radial nerves caused by intramuscular injections of various drugs. Axonopathy was confirmed in all cases, and reinnervation was demonstrated in only one third. Pain was usual. The consequences for the growing limb were particularly severe.

3.4.16 Vibration Injury Extensive studies from the Department of Hand Surgery in Malmo have improved understanding of this difficult and controversial field (Stromberg 1997). The regular use of hand held vibrating tools may lead to a complex of symptoms, the hand–arm vibration syndrome. Stromberg defines three groups of symptoms: sensory-neural; vasospastic, and a combination of both. Cold intolerance presents as a significant symptom in one half of the patients with sensoryneural symptoms. There was impairment of nerve conduction, vibro tactile sense, and temperature sense in all patients, changes which were more strongly expressed in the median nerve. Biopsies of the dorsal interosseous nerve revealed demyelination, endoneurial and perineurial fibrosis, and loss of axons.

3.5 The Perineurium and Neoplasm or Infiltration Tumours arising from cells within the endoneurium are contained within the perineurium which acts as a compartment. The tumour may be a benign schwannoma but malignant peripheral nerve sheath tumours whose cell of origin is the Schwann cell, are contained within the perineurium, at least initially, and spread within it. We have seen intraneural spread of malignant tumours extending up to 18 cm from the main tumour (Fig.  3.37). The brachial and lumbo sacral plexus are common sites for malignant invasion by direct spread or by metastases through the lymphatics. However

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3.6 Radiation and Peripheral Nerves

Fig. 3.37  Malignant peripheral nerve sheath tumour in the medial cord of the brachial plexus in a patient with NF1. A biopsy of C8, 15  cm proximal to the main tumour mass, shows one bundle replaced by tumour and some degenerative changes in adjacent bundles. Haemotoxylin and eosin ×160 (Courtesy of Dr Jean Pringle).

there are no lymphatics within the endoneurium and the two cases of lumbosacral radiculoplexopathy in prostate cancer, described by Ladha et al. (2006a) at the Mayo Clinic, represent, in all likelihood, direct extension of the tumour within nerves from the prostate. Both patients had experienced worsening pain with a deepening sensory motor loss for a number of years. In one case this led to an increasing defect of bladder and bowel control. Biopsy of the affected nerves showed tumour cells organised into a glandular appearance, surrounded by S-100 positive cells which were contained within the perineurium. These workers comment that magnetic resonance imaging is extremely helpful in localising the disease and defining its extent and they observe that: “the clinician should always consider the entity of neoplastic radiculoplexopathy in the differential diagnosis of progressive, painful, lower extremity weakness as treatments such as radiotherapy may be palliative and spare further neurological decline.” Ladha et  al. (2006b) described two cases of isolated amyloidosis presenting as lumbosacral radiculoplexopathy. The first patient experienced a painless progressing sensory and motor loss. There was no systemic disease. Biopsy revealed diffuse infiltration of the endoneurium and perineurium. The MR scan in this case showed enlargement of the sciatic nerve with a denervation signal in the gluteal muscles. In the second case the lesion was more severe, with incontinence of bladder and bowel. This patient had successfully been treated for a lymphoma some years previously and there were no signs of active disease when he presented to the Mayo Clinic. Biopsy of the cauda equina was performed which revealed replacement by amyloid, and his neurological state was stabilised by excision of an “amyloidoma” from L3. The neurological effects of generalised amyloidosis are protean, the subject is reviewed by Kyle et al. (2005).

The statement by Janzen and Warren (1942) that “nerve tissue is extremely resistant to radiation” is, alas, true only so far as the function of conducting an impulse is concerned, and in so far as doses up to 10,000R (100 Gy) “do not cause overt damage to this normally static cell population” Vujaskovic (1997) found that peripheral nerves were damaged by exposure exceeding 20 Gy. The more deeply seated larger fibres were worst affected: the first changes occurred within the axon, where there was increased density of microtubules and neurofilaments. The lesion is perhaps best considered as (1) a lesion from external compression exerted by fibrosis of soft tissue and (2) an intrinsic lesion of the nerve. The latter affects the axon, the Schwann cells and the myelin sheath; it is associated with vasculitis, which leads eventually to fibrosis (Spiess 1972) (Fig.  3.38a, b). The affection may extend to the main vessel (Fig. 3.39). It seems likely that the dose of radiation tolerated by neural tissue depends broadly on the total dose and the period of time over which it is given, but evidently there are individual variations and there may indeed be individual susceptibilities.

3.7 Envenomation In the singular case reported by Laing and Harrison (1991) a young man’s right ulnar nerve was affected by the venom expressed from the tentacle of a box jellyfish (Chironex fleckeri) and presumably conveyed transcutaneously. The nerve was explored and found to be oedematous, but the period elapsing between injury and exploration is not related. There was spontaneous recovery. The case evokes echoes of that of the Lion’s Mane (1909), though because of the absence of Dr Watson from the latter we are condemned to remain in the dark about the presence of neuropathy in the surviving victim of Cyanea capillata. The fascinating field of poisons and evanomation is reviewed by Donaghy (2009a). The active agents cause death by interfering with ion channel function, by blocking the neuromuscular junction and by blocking synaptic transmission within the central nervous system. Cicutoxin, the agent in water hemlock, blocks ion channels and also receptors to gamma amino butyric acid (GABA) in the brain and the symptoms bear little relation to those attributed to Socrates in the Phaedo. The Puffer fish contains tetradotoxin which blocks sodium channels, a phenomenon which has enabled the analysis of these channels. The Krait injects bungarotoxins which block the post synaptic acetyl choline receptors at the neuromuscular junction; whereas the venom injected by the Mamba and the Taipan block pre synaptic nerve endings.

Reactions to Injury

109

a

Fig. 3.39  Radiation induced thrombosis of the third part of subclavian artery. A 38 year old woman developed severe pain, swelling and paralysis 6 weeks after completing a course of radiotherapy for breast cancer. She lost all sensation in the tips of her fingers. She could recognise light touch but could not localise it in the palm of the hand. Sensation was normal proximal to the wrist crease. There was no recovery of skeletal muscle or of smooth muscle function in her forearm and hand.

b

Fig. 3.38  Radiation neuropathy. Electron microphotographs of specimens from biopsy of the lateral trunk of the brachial plexus taken two and a half years after radiotherapy for cancer of the breast. (a) Extensive collagenisation, loss of axons and myelin ×4,125. (b) Extensive demyelination and Schwann cell loss ×4,125 (Electron micrographs prepared by Mr Michael Kayser).

3.8 The Peripheral Effects of Denervation These effects follow degenerative lesions in which recovery fails or is long delayed. If regeneration of axons into the distal stump fails, changes, which over time become

irreversible, develop in the target organs and in the proximal neurone. Motor end-plates atrophy and disappear (Bowden and Gutmann 1944); the denervated muscles undergo fibrosis. Bowden and Gutmann (1944) recorded that after 3 months denervation it became increasingly difficult to identify the end plates. From 3 years on they found fragmentation of structures, and reckoned that this represented irreversible change. Luco and Eyzaguirre (1955) found that the nearer the lesion was to the point of denervation the more rapidly did the changes in the end plates appear. Cutaneous sensory end-organs atrophy more slowly. Dellon (1981) found that they degenerate and eventually atrophy. The reaction of muscle spindles to denervation has been studied extensively. Sherrington (1894) found the spindles “very obvious amid atrophied extrafusal muscle fibres five months after denervation.” Batten (1897) found in a case of complete paralysis after a lesion of the brachial plexus that atrophy of spindles occurred but took place much later than was the case in ordinary muscle fibres. Tower (1932) found that the nuclear bag fibres showed only a slight reduction in diameter after denervation, whereas the chain fibres atrophied almost as rapidly as did the extrafusal fibres. Tower noted in particular the thickening of the capsule. De Reuck (1974) reported rather similar findings. Swash and Fox (1974) noted capsular thickening and atrophy of intrafusal fibres after sensorimotor denervation and Myles and Glasby (1992) conclusively showed that atrophy of muscle spindles followed uncorrected denervation. Loss of nervous control of the small peripheral blood vessels leads to defects of nutrition and atrophy in the subcutaneous tissues. This is compounded by unnoted injury, which can lead to the loss of part or the whole of the limb or even death as is seen in congenital insensitivity to pain, in leprosy

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or in septicaemia from an unnoted sore in neglected cases of sciatic palsy. The effects of denervation are particularly severe in the growing child especially so where there is persisting imbalance of muscle forces acting across a joint (Fig.  3.40). It is our impression that the shortening of the limb is more severe after complete lesions of main trunk nerves such as the sciatic than it is in cases of poliomyelitis.

3.9 Changes at the Higher Levels: The Phantom Limb

Fig. 3.40  Atrophy of the left foot in an 11 year old boy 4 years after transection of the tibial and common peroneal nerves at the knee. The repair of the common peroneal nerve was successful, that of the tibial nerve failed.

The changes in the functional organisation of the somatosensory cortex are rapid and extensive. Structural or, at least, synaptic reorganisation at a subcortical level was probably shown by Banati et al. (2001) who demonstrated changes in the activity of glial cells in the thalamus in patients with intractable pain after injury to the brachial plexus or peripheral nerves (Fig. 3.41). Ramachandran and Hirstein (1998) described their findings in a patient (DS) who had his arm amputated 1 year after an avulsion lesion of the brachial plexus. Stimulating the skin of the face evoked a sensation which was referred to the amputated digits: “when the cotton swab was moved continuously from the angle of the mandible to the symphysis menti, the referred sensation felt as if ‘it was moving from the ball of the thumb to the tip in an arc like motion’. This observation was replicated several times.” Ramnachandran and Hirstein suggest that the sensory input from the face is being received in two different cortical areas: the original face area and the area that previously only received information from the arm. Kew et al. (1997) studied

Fig. 3.41  Positron emission tomographic scan showing an in vitro marker of increased glial cell activity indicating synaptic reorganisation in the thalamus in a patient with persisting pain 4 years after brachial plexus lesion (Courtesy of Professor Praveen Anand).

Reactions to Injury

two patients with avulsion lesions of the brachial plexus using positron emission tomographic (PET) scanning. Both of these patients had referred sensations on the anterior and posterior chest wall where stimulation evoked a response in the amputated hand. PET scans showed a precise correlation between the finger where the referred sensation was felt and the disposition of the cortical maps. The phenomena of the “phantom” limb provides opportunities for analysis of the changes in the somatosensory cortex after injury. Mitchell (1872) wrote: “nearly every man who loses a limb carries about with him a constant or inconstant phantom of the missing member, a sensory ghost of that much of himself and sometimes a most inconvenient presence, faintly felt at times, but ready to be called up to his perception by a blow, a touch or a change of wind.” To Lord Nelson the severe phantom limb pain which he experienced in his right arm, lost during the attack at Santa Cruz provided a “direct proof of the existence of the soul” (Riddoch 1941). One extraordinary example of the persistence of a painful phantom is provided by a patient treated by our colleague, Christopher Wynn Parry, in the Rehabilitation Unit of the Royal National Orthopaedic Hospital. A 33 year old woman presented with persistent and severe phantom pain following amputation of her right arm in a road traffic accident at the age of 11 years. She described her clenched fist tightly holding a florin, for she had been going shopping at the time of her accident. There was a dramatic response to transcutaneous nerve stimulation and she described that, as the pain diminished, she felt the fingers of her clenched fist open and the coin dropped from her hand. The transcutaneous nerve stimulator was used on several occasions, ultimately with lasting relief. On the last occasion she described how she “saw” the coin disappearing down a drain. There are a number of possible explanations for this result; we might add that Christopher Wynn Parry often succeeded in relieving pain in patients otherwise abandoned.

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112 Denny Brown D, Adams RD, Brenner G, Doherty MM (1945) The pathology of injury to nerve induced by cold. J Neuropathol Exp Neurol 4:305–323 Denny-Brown D, Brenner C (1944) The effect of percussion on nerve. J Neurol Neurosurg Psychiatry 7:76–95 Di Vincenti FC, Moncrieff JA, Pruitt BA (1969) Electrical injuries: a review of 65 cases. J Trauma 9:497–507 Dodt E (1953) Differential sensitivity of mammalian nerve fibres. Acta Physiol Scand 29:91–108 Donaghy M (2009a) Polyneuropathy. In: Donaghy M (ed) Brain’s diseases of the nervous system, 12th edn, Oxford University Press, Oxford Chapter 21, pp 541–602 Donaghy M (2009b) Toxic and environmental disorders. In: Donaghy M (ed) Brain’s diseases of the nervous system, 12th edn, Oxford University Press, Chapter 5, pp 141–164 Douglas WW, Malcolm JL (1955) The effect of localized cooling on conduction in cat nerves. J Physiol 130:63–71 Durrenberger PF, Facer P, Gray RA, Chessell IP, Naylor A, Bountra C, Banati RB, Birch R, Anand P (2004) Cyclooxygenase – 2 (COX-2) in injured human nerve and a rat model of nerve injury. J Peripher Nerv Syst 9:15–24 Durrenberger PF, Facer P, Casula MA, Yiangou MY, Gray RA, Chessell IP, Day NC, Collins SD, Birnham S, Wilson AW, Elliot D, Birch R, Anand P (2006) Prostanoid receptor EP1 and COX-Z in injured human nerves and a rat model of nerve injury: a time course study. BMC Neurol 6:1 Dyck PJ, Nukada H, Lais CA, Karnes J (1984) Permanent axotomy: a model of chronic neuronal degeneration produced by axonal atrophy, myelin remodelling and regeneration. In: Dyck PJ, Thomas PK, Lambert EH, Bunge R (eds) Peripheral neuropathy, 2nd edn. WB Saunders, Philadelphia, pp 660–690 Dyck PJ, Dyck J, Engelstad PJB (2005a) Pathological alterations of nerves. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier Saunders, Philadelphia, pp 733–829, Chapter 32 Dyck PJB, Engelstad J, Dyck PJ (2005b) Microvasculitis. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier Saunders, Philadelphia, pp 2405–2414, Chapter 106 Eames R, Lange LS (1967) Clinical and pathological study of ischaemic neuropathy. J Neurol Neurosurg Psychiatry 30:215–236 Fowler TJ, Danta G, Gilliatt RW (1972) Recovery of nerve conduction after a pneumatic tourniquet: observations in the hind limb of a baboon. J Neurol Neurosurg Psychiatry 35:638–647 Franz DN, Iggo A (1968) Conduction failure in myelinated and nonmyelinated axons at low temperatures. J Physiol 199:319–345 Galardi G, Comi G, Lozza L, Marchettini P, Novarina M, Facchini R, Paronzini A (1990) Peripheral nerve damage during limb lengthening. J Bone Joint Surg 72B:121–124 Gardiner MD, Mangwani J, Williams WW (2006) Aneurysm of the common iliac artery presenting as a lumbosacral plexopathy. J Bone Joint Surg 88B:1524–1526 Gereis V (2005) Paresis and paralysis, pers com Gilliatt RW (1981) Physical injury to peripheral nerves. Mayo Clin Proc 56:361–370 Gilliatt RW, Hjorth RJ (1972) Nerve conduction during Wallerian degeneration in the baboon. J Neurol Neurosurg Psychiatry 35:335–341 Gilliatt RW, Taylor JC (1959) Electrical changes following section of the facial nerve. Proc Royal Soc Med 52:1080–1083 Greer HD (1997) Neurological consequences of diving. In: Bove AA, Davis JC (eds) Diving medicine. WB Saunders, Philadelphia, pp 258–269 Griffin JW, Hoffman PN (1993) Degeneration and regeneration in the peripheral nervous system. In: Dyck PJ, Thomas PK, Lambert EH, Bunge R (eds) Peripheral neuropathy, 3rd edn. WB Saunders Company, Philadelphia, pp 361–376 Groves MJ, Scaravilli F (2005) Pathology of peripheral neurone cell bodies. In: Dyke PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier Saunders, Philadelphia, pp 683–732, Chapter 31

Surgical Disorders of the Peripheral Nerves Gutmann E, Sanders FK (1943) Recovery of fibre numbers and diameters in the regeneration of peripheral nerves. J Physiol 101:489–518 Haftek J (1970) Stretch injury of peripheral nerve. J Bone Joint Surg 52B:354–365 Haftek J, Thomas PK (1967) An electron-microscopic study of crush injuries to peripheral nerves. J Anat 102:154–155 Hall S (1999) The biology of chronically denervated Schwann cells. Ann NY Acad Sci 883:215–233 Hall S (2005) The response to injury in the peripheral nervous system. J Bone Joint Surg 87B:1309–1319 Harriman DGF (1977) Ischaemia of peripheral nerve and muscle. J Clin Pathol 30(supplII):94–99 Hess K, Eames RA, Darveniza P, Gilliatt RW (1979) Acute ischaemic neuropathy in the rabbit. J Neurolog Sci 44:19–43 Hill S, Hall S (1999) Microscopic anatomy of the posterior interosseous and median nerves at sites of potential entrapment in the forearm J Hand Surg 24B: 170–176 Hobby JAE, Laing JE (1988) Electrical injuries of the upper limb. In: Tubiana R (ed) The hand, vol III. WB Saunders Company, Philadelphia, pp 779–787 Hoffer JA, Stein RB, Gordon T (1979) Differential atrophy of sensory and motor fibres following section of cat peripheral nerves. Brain Res 178:347–361 Holmes W, Young JZ (1942) Nerve regeneration after immediate and delayed suture. J Anat 77:63–96 Hongell A, Mattson HS (1971) Neurographic studies before, after and during operation for median nerve compression in the carpal tunnel. Scand J Plast Reconstr Surg 5:103–109 Hoogeveen JF, Wondergem J, Troost D, van der Kracht AHW, Haveman O (1991) Blood vessel damage followed by Wallerian degeneration in the rat sciatic nerve after local hyperthermia. Neuropathol Appl Neurobiol 17:250–251 Houten JK, Errico TJ (2002) Paraplegia after lumbosacral nerve root block: report of three cases. Spine 2:70–75 Hudson AR (1984) Injection injuries of nerves. In: Dyck PJ, Thomas PK, Lambert EH, Burge R (eds) Peripheral neuropathy, 2nd edn. WB Saunders, Philadelphia. pp 429–431 Irwin MS, Gilbert SEA, Terenghi G, Smith RW, Green CJ (1997) Cold intolerance following peripheral nerve injury. Brit J Hand Surg 22:308–316 Janzen AH, Warren S (1942) Effect of roentgen rays on peripheral nerves of rats. Radiology 38:333–337 Jefferson D, Neary D, Eames RA (1981) Renaut body distribution at sites of human peripheral nerve entrapment. J Neurolog Sci 49:19–29 Kew JJ, Halligan PW, Marshall JC, Passingham RE, Rothwell JC, Ridding MC et  al (1997) Abnormal access of axial vibrotactile input to deafferented somatosensory cortex in human upper limb amputees. J Neurophysiol 77:2753–2764 Kline DG, Hudson AR (1995) Nerve injuries,WB Saunders, Philadelphia Injection injury p 46–50 Kyle RA, Kelly JJ, Dyck PJ (2005) Amyloidosis and neuropathy. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. WB Saunders, Philadelphia. Chapter 108, pp 2427–2452 Ladha SS, Spinner RJ, Suarez GA, Amrami KK, Dyck PJB (2006a) Neoplastic lumbosacral radiculoplexopathy in prostate cancer by direct perineurial spread: An unusual entity. Muscle Nerve 34: 659–665 Ladha SS, Dyck PJB, Spinner RJ, Perez DG, Zeldenrust SR, Amrami KK, Solomon A, Klein CJ (2006b) Isolated amyloidosis presenting with lumbosacral radiculopathy: description of two cases and pathogenic review. J Peripher Nerv Syst 11:346–352 Laing JHE, Harrison DH (1991) Envenomation by the box-jellyfish - an unusual cause of ulnar nerve palsy. J Royal Soc Med 64:115–116 Landau WM (1953) The duration of neuromuscular function after nerve section. Neurosurgery 10:64–68 Lawson SN (2005) The peripheral sensory nervous system: dorsal root ganglion neurones. In: Dyck PJ, Thomas PK (eds) Peripheral

Reactions to Injury neuropathy (in two volumes), 4th edn. Elsevier Saunders, Philadelphia, pp 163–202, Chapter 8 Leonard MH (1967) Immediate improvement of sensation on relief of extraneural compression. J Bone Joint Surg 51A:1282–1284 Lewis T, Pickering GW, Rothschild P (1931) Centripetal paralysis arising out of arrested bloodflow to the limb. Heart 16:1–32 Li H, Terenghi G, Hall SM (1997) Effects of delayed reinnervation on the expression of C-er6B receptors by chronically denervated rat Scwann cells in vitro. Glia 20:333–347 Li H, Wigley C, Hall SM (1998) Chronically denervated rat Schwann cells respond to GGF in vitro. Glia 21:1–14 Luco JV, Eyzaguirre C (1955) Fibrillation and hypersensitivity to ach in denervated muscle: effects of length on degenerated nerve fibers. J Neurophysiol 18:65–73 Lundberg A (1948) Potassium and the differential thermosensitivity of membrane potential, spike and negative after potential in mammalian A and C fibres. Acta Physiol Scand Suppl 50(15):1–67 Lundborg G, Rydevik B (1973) Effects of stretching the tibial nerve of the rabbit: preliminary study of the intraneural circulation of the barrier function of the perineurium. J Bone Joint Surg 55B:390–401 MacKinnon SE, Dellon Al (1986) Experimental study of chronic nerve compression. Hand Clin 2:639–650 MacKinnon SE, Dellon AL (1988) Ischaemia of nerve: loss of vibration sensibility. In: Surgery of the peripheral nerve. Thieme Medical, New York, Georg Thieme Verlag Stuttgart New York p 57 MacKinnon SE, Dellon AL, Hudson AR, Hunter DA (1985) A primate model for chronic nerve compression. J Reconstr Surg Microsurg 1:185–195 Mannan K, Altaf F, Maniar S, Tirabosco R, Sinisi M, Carlstedt T (2008) Cyclical sciatica. J Bone Joint Surg 90B:98–101 Martin JN, Vialle R, Denormande P, Sorriaux G, Gad H, Harding I, Dizien O, Judet T (2006) Treatment of knee flexion in contracture due to central nervous system disorders in adults. J Bone Joint Surg 88A:840–845 McComas AJ, Sica REP, Banarjee S (1978) Long term effects of partial limb amputation in man. J Neurol Neurosurg Psychiatry 41: 425–432 McManis PG, Low PA, Lagerlund TD (2005) Nerve blood flow and microenvironment. In: Dyke PJ, Thomas PK (eds) Peripheral neuropathy. Elsevier Saunders, Philadelphia, pp 671–680, Chapter 30 Merrington WR, Nathan PW (1949) A study of post-ischaemic paraesthesiae. J Neurol Neurosurg Psychiatry 12:1–18 Mitchell SW (1872) Injuries of nerves and their consequences. JB Lippincott, Philadelphia Mitchell SW, Morehouse GR, Keen WW (1864) Gunshot wounds and other injuries to nerves. JB Lippincott, Philadelphia Myles M, Glasby MA (1992) The fate of muscle spindles after various methods of nerve repair in the rat. Neuroorthopaedics 13:15–23 Nagano A (2003) Spontaneous anterior interosseous nerve palsy review article. J Bone Joint Surg Br 85B:313–318 Nagano A (2008) “Hour glass” like fascicular constriction. Pers com Nagano A, Shibata K, Tokimura H, Yamamoto S, Tajiri Y (1996) Spontaneous anterior interosseous nerve palsy with hourglass-like fascicular constriction within the main trunk of the median nerve. Hand Surg 21A:266–270 Nash TP (2001) Comment on: “A cervical anterior spinal artery syndrome after diagnostic blockade of the right C6-nerve root” Browers PJAM et al. Pain 91:397–399 Neary D, Eames RA (1975) The pathology of ulnar nerve compression in man. Neuropathol Appl Neurobiol 1:69–88 Niels OB, Thomsen, Lars Dahlin B (2007) Injury to the radial nerve caused by fracture of the humeral shaft: timing and neurobiological aspects related to treatment and diagnosis. Scand J Plast Reconstr Surg Hand Surg 41:153–157 Nogueira MP, Paley D, Nave A, Herbert A, Nolente C, Herzenburg JE (2003) Nerve lesions associated with limb lengthening. J Bone Joint Surg 85A:1502–1510

113 Nukada H, Anderson GM, McMorran PD (1997) Reperfusion nerve injury: pathology due to reflow and prolonged ischaemia. J Peripher Nerv Syst 2:60–69 Oaklander AL, Brown JM (2004) Unilateral nerve injury produces bilateral loss of distal innervation. Ann Neurol 55:639–644 Oberlin C, Shafi M, Diverres JP, Silberman O, Adle H, Belkheyar Z (2006) Hourglass like constriction of the axillary nerve. J Hand Surg 31A:1100–1104 Ochoa J, Fowler TJ, Gilliatt RW (1972) Anatomical Changes in peripheral nerves compressed by pneumatic tourniquet. J Anat 113:433–455 Ochs S, Pourmand R, Si K, Friedman RN (2000) Stretch of mammalian nerve in  vitro: effect on compound action potentials. J Peripher Nerv Syst 5:227–235 Omura T, Omura K, Sano M, Sawada T, Hasegawa T, Nagano A (2005a) Spatio temporal quantification of recruit and resident macrophages after crush nerve injury utilizing immuno-histo chemistry. Brain Res 1057:29–36 Omura T, Sano M, Omura K, Hasegawa T, Doi M, Sawada T, Nagano A (2005b) Different expressions of BDNF, NT3 and NT4 in muscle and nerve after various types of peripheral nerve injuries. J Peripher Nerv Syst 10:293–300 Paley D (1990) Problems, obstacles and complications of limb lengthening by the Ilizarov technique. Clin Orth Rel Res 250:81–104 Pandian JD, Bose S, Daniel V, Singh Y, Abraham AP (2006) Nerve injuries following intramuscular injections: a clinical and neurophysiological study from North West India. J Periph Nerve Syst 11:165–171 Phang IS,Biant LC, Jones TS (2009) Neurostenalgia of the femoral nerve A treatable cause of intractable hip pain in a young adult. J Arthroplasty. PMID: 19577882 Platt H (1928) On the peripheral nerve complications of certain fractures. J Bone Joint Surg 10:403–414 Pollock LJ, Golseth JG, Arieff AJ (1946) The response of muscle to electrical stimuli during degeneration, denervation and regeneration. Military Neurophysiol 25:236–257 Polo A, Aldegheri R, Zambito A (1997) Lower limb lengthening in short stature. J Bone Joint Surg 79B:1014–1018 Rabert D, Xiao Y, Yiangou Y, Kreder D, Sangameswaran L, Segal MR, Hunt CA, Birch R, Anand P (2004) Plasticity of gene expression in injured human dorsal root ganglia revealed by gene chip oligonucleotide microarrays. J Clin Neuroscience 11:289–299 Ramachandran VS, Hirstein W (1998) The perception of phantom limbs. The DO Hebb lecture. Brain 9(121):1603–1630 Renaut J (1881) Systéme hyalin de souténement des centres nerveux et de quelques organes de sens. Archives de Physiologie Normale et Pathologique 8:845–860 Richardson PM, Thomas PK (1979) Percussive injury to peripheral nerve in rats. J Neurosurg 51:178–187 Riddoch G (1941) Phantom limbs and body shape. Brain 64:197–222 Romanes GJ (1946) Motor localization and the effects of nerve injury on the ventral horn cells of the spinal cord. J Anat 80:117–131 Saldhana G, Bar K, Yiangou Y, Anand P, Birch R, CarlstedT T, Burrin JM (2000) Marked increase of interleukin – 6 in injured human nerves and dorsal root ganglia. J Neurol Neurosurg, Psychiatr 69:693–694 Salisbury RE, Dingeldein GP (1988) The burnt hand and upper extremity. In: Green DP (ed) Operative hand surgery, vol II, 2nd edn. Churchill Livingstone, New York, pp 2135–2164 Salzberg CA, Salisbury RE (1991) Thermal injury of peripheral nerve. In: Gelberman RH (ed) Operative nerve repair and reconstruction. JB Lippincott, Philadelphia, pp 671–677 Sander HW (1999) Mononeuropathy of the medial branch of the deep peroneal nerve in a scuba diver. J Periph Nerv Syst 4:134–137 Schmalbruch H (1987) Loss of sensory neurones after sciatic nerve section in the rat. Anat Rec 219:323–329 Seddon HJ (1943) Three types of nerve injury. Brain 66:237–288 Seddon HJ (1954) Nerve grafting. In: Peripheral nerve injuries by the Nerve Injury Committee of the Medical Research Council MRC Special Report Series 282. London HMSO, pp 402–403

114 Seddon HJ (1975) Surgical disorders of peripheral nerves, 2nd edn. Churchill Livingstone, Edinburgh, pp 67–88 Sherrington CS (1894) On the anatomical constitution of nerves of skeletal muscles: with remarks on recurrent fibres in the ventral spinal nerve-root. J Physiol 17:211–258 Somayaji HS, Saifuddin A, Casey ATH, Briggs TWR (2005) Spinal cord infarction following therapeutic computed tomography-guided left L2 nerve root injection. Spine 30:E106–E108 Sorenson J, Daube JR, Windebank AJ (2006) Electrophysiological findings in a cohort of old polio survivors. J Peripher Nerv Syst 11:241–246 Spencer PS, Weinberg HJ, Raine CS, Prineas JW (1975) The perineurial window – a new model of focal demyelination and remyelination. Brain Res 96:323–329 Spiess H (1972) Schädigungen am peripheren Nervensystem durch iioniserende Strahlen. In: Schriftenreihe neurologie, Band 10. Springer Verlag, New York Spinner RJ, Atkinson JLD, Teil RL, Birch R et al (2003) Peroneal intraneural ganglia: the importance of the articular branch. A unifying theory. J Neurosurg 99:330–343 Spinner RJ, Amrami KK, Kliot M, Johnston SP, Casanas J (2006) Suprascapular intraneural ganglia and glenohumeral joint attachments. J Neurosurg 104:551–557 Stenning M, Drew S, Birch R (2005) Low energy arterial injury at the shoulder with progressive or delayed nerve palsy. J Bone Joint Surg 87B:1102–1106 Stewart M, Birch R (2001) Penetrating missile injuries. J Bone Joint Surg 83B:517–524 Stoll G, Griffin JW, Li CY, Trapp BD (1989) Wallerian degeneration in the peripheral nervous system: participation of both Schwann cells and macrophages in myelin degeneration. J Neurocytol 18:671–683 Stromberg T (1997) Vibration induced neuropathy in the hand. Doctoral thesis. Wallin and Dalholm Boktryckeri AB ISBN. 91-628-2539-9 Sunderland S (1951) A classification of peripheral nerve injuries producing loss of function. Brain 74:491–516 Suzuki H, Oyanagi K, Takahishi H, Kono H, Yokoyama M, Ikjta F (1993) A quantitative pathological investigation of the cervical cord, roots and ganglia after long term amputation of the unilateral upper arm. Acta Neuropathol (Berl) 85:666–673 Swash M, Fox P (1974) The pathology of the human muscle spindle: effect of denervation. J Neurol Sci 22:1–24 Tait GR, Danton M (1991) Contralateral sciatic nerve palsy following femoral nailing. J Bone Joint Surg 73B:689–690 Terenghi G, Calder JS, Birch R, Hall SM (1998) A morphological study of Schwann cells and axonal regeneration in chronically transected human peripheral nerve. J Hand Surg 23B:583–587 Thaventhiran J, O’leary MJ, Coakley JH, Rose M, Nagendran K, Greenwood R (2001) Pathogenesis and recovery of tetraplegia after electrical injury. J Neurol Neurosurg Psychiatry 71:535–537

Surgical Disorders of the Peripheral Nerves Thomas PK (1964) Changes in the endoneurial sheaths of peripheral myelinated nerve fibres during Wallerian degeneration. J Anat 98:175–182 Thomas PK, Bhagat S (1978) The effect of extraction of the interfascicular contents of peripheral nerve trunks in perineurial structure. Acta Neuropathol (Berl) 43:135–141 Thomas PK, Fullerton PM (1963) Nerve fibre size in the carpal tunnel syndrome. J Neurol Neurosurg Psychiatry 26:520–527 Thomas PK, Holdorff B (1993) Neuropathy due to physical agents. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 3rd edn. WB Saunders, Philadelphia, pp 990–1014 Thomas PK, Jones DG (1967) The cellular response to nerve injury. 2. Regeneration of the perineurium after nerve section. J Anat 101:45–55 Tower SS (1932) Atrophy and degeneration in the muscle spindles. Brain 55:77–90 Tsao BE, Wilbourn AJ (2003) The medial brachial fascial compartment syndrome following axillary arteriography. Neurology 61:1037 Tubiana R (1988) Burns. In: Tubiana R (ed) The hand, 3rd edn. WB Saunders, Philadelphia Ungley CC, Channell GB, Richards RL (1945) The immersion foot syndrome. Br J Surg 33:17–31 Vujaskovic Z (1997) Structural and physiological properties of peripheral nerves after intra-operative irradiation. J Peripher Nerv Syst 2:343–349 Walbeehm ET, von Heel EBM, Kuypers PDL, Terenghi G, Hovius SER (2003) Nerve compound action current (NCAC) measurements and morphometric analysis in the proximal segment after nerve transection and repair in a rabbit model. J Peripher Nerv Syst 8:108–115 Waller A (1850) Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of their primitive fibres. Philos Trans R Soc Lond 140:423–429 Wilbourn AJ (2005) Brachial plexus injuries. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier Saunders, Philadelphia, pp 1339–1373, Chapter 55 Wilkinson M, Clarke J (1992) Thermal Injuries to the brachial plexus. Injury 23:342–343 Xu D, Pollock M (1994) Experimental nerve thermal injury. Brain 117:375–384 Ygge J (1989a) Neuronal loss in lumbar dorsal root ganglia after proximal compared to distal sciatic nerve resection: a quantitative study in the rat. Brain Res 47B:193–195 Ygge J (1989b) Central projections of the rat radial nerve investigated with transganglionic degeneration and transganglionic transport of horse radish peroxidase. J Com Neurol 279:199–211 Young JZ (1949) Factors influencing the regeneration of nerves. Adv Surg 1:165–220

4

Regeneration and Recovery

Regeneration: the cellular proliferation; importance of integrity of the basal lamina; neurotropins and neurotrophins; regeneration after intradural injury; regeneration of end organs; predictors of recovery. But the journey of the axon tip to an end organ is only the most dramatic of the phases in the process of regeneration, and its arrival is alone no guarantee of the return of useful function. J.Z. Young 1942

Much of what is now known about the regeneration of nerves is based on the work of Ramon Y. Cajal (1928) who developed concepts about the regrowth of divided axons, the formation of growth cones, the re-ordering of growing axons into new fascicles (Cajal 1928a, Cajal 1928b), and the guidance of new axons to their target tissues. He postulated the existence of “allowing or attracting substances” (Cajal 1928c) and gave credit to Forsmann (1900) for introducing the term neurotropism. Cajal described neurotropism as an effect which was initially one of general attraction emanating from the distal stump which later became more individual and specific as the new axon approached its end organ and in particular, the muscle spindle or the Golgi tendon organ. He also outlined the likelihood of a neurotrophic influence provided by the Schwann cells: “the nutritive and tutorial functions of the cells of Schwann had already been recognized by the embryologists, many of whom believed that the success of the thickening of young fibres and the development of the medullary sheath were the principal functions of these cells. We may especially cite Graham Kerr (1904) who studied the behaviour of these cells in the normal development of nerves, and Mott and Halliburton (1901), who attributed to the bands of Büngner of the peripheral stump of cut nerves the function of feeding and protecting recently arrived sprouts. There is only a step between the recognition of these cells as a nutritive placenta and the admission in them of secretions capable of stimulating and orientating the sprouts that are wandering in the scar.”(Cajal 1928c) These concepts have, in effect, been confirmed by later work. Early in the Second World War a Nerve Injuries Committee was again appointed by the Medical Research Council. George Riddoch was appointed chairman and Hugh Cairns, then Professor of Surgery in Oxford, was placed in charge of injuries to the nervous system. Five hospitals were designated for the treatment of nerve injuries. A team was set up in the Zoology Department of Oxford University which included,

amongst others, Young, Medawar, Holmes, Sanders, Gutmann, Guttmann and Ruth Bowden. Young (1993) summarized some of this work. Nerve grafting in all its forms was studied. The first evidence of axonal transport was revealed. The rate of nerve regeneration, the effects of disuse, the regeneration of proprioceptors, the maturation of regenerated fibres and the significance of retrograde influence were amongst the fields of enquiry. Collectively this work marked a most important stage in improving understanding of regeneration and of applying those lessons to clinical practice: here is an example of what has become known, in fashionable circles, as “translational research.” The decades since the appearance of the MRC report in 1954 have seen extensive advances in understanding cellular and molecular mechanisms. These include the role of neurotrophic factors; the dramatic and urgent changes in the expression of genes which transform, at least in the early days, an environment from one which inhibits new axonal growth to one which protects the cell body and facilitates new growth. The functions of the Schwann cell and its basal lamina, and the mechanisms of guidance, selection, and discarding of new axons have been illustrated. Much of this new work is reviewed in the comprehensive and excellent works of Hall (2005a, b), and of Lundborg (2003, 2004). For an authoritative description of the cellular and molecular events which underlie the process of Wallerian degeneration and regeneration the reader is referred to Dyck and Thomas (2005). It is important to remember the differences between the laboratory investigation, in which a controlled, precise and limited lesion is inflicted upon a nerve and the situation faced by the clinician presented with a patient with a massive wound involving the soft tissues, the skeleton, the vessels and sometimes by other injuries which threaten life and limb. The demonstration of regenerating axons across a lesion of a nerve inflicted in the laboratory does not necessarily translate

R. Birch, Surgical Disorders of the Peripheral Nerves, DOI: 10.1007/978-1-84882-108-8_4, © Springer-Verlag London Limited 2011

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to the recovery of function in the human. The phenomena of pain and recovery of sensation are rather poorly revealed by experiments upon small mammals or for that matter by barely justifiable experimentation upon primates. “The proper study of man is man.” We have been singularly fortunate over the years in the work of colleagues who meticulously examined tissues removed from injured nerves in more than 1,000 patients. At St Mary’s Hospital all biopsies were examined by Dr Arthur Boylston, later Professor Boylston at Leeds and at the Royal National Orthopaedic Hospital material was examined by Dr Jean Pringle. Dr Yusuf Ali, of the Institute of Orthopedics actively encouraged study of material by transmission electronmicroscopy in investigations performed by Mr Stephen Gshmeissner and by Mr Michael Keyser. The work of the joint diagnostic clinic in the Department of Neurophysiology at Queen Square is related in Chaps. 5 and 6. From 1990 Professor Praveen Anand and his colleagues at the Royal London Hospital and then later at Imperial College investigated, by novel techniques, changes in expression of nerve growth factors and of ion channels, correlating these with the measurement of small and large fibre function using methods which are described in Chap. 5. There is no doubt that the fundamental cellular processes which underlie regeneration are similar in the laboratory, in the injuries of civilian practice and in the wounds of war, but they are modified by the violence of the injury, by the effects of injury on associated tissues and in particular by ischemia and by delay before repair. We offer some general conclusions which are based on our clinical and laboratory investigations. 1. The extent of longitudinal damage of the nerve is greater in a rupture caused by traction that it is in “tidy” transections caused by knife or glass and this effect rapidly worsens with increasing delay before repair. If healing has been complicated by sepsis then it is often necessary in a late repair to resect 3 cm or more from both proximal and distal stumps of the divided nerve before reaching a recognizable architecture and even then microscopic examination reveals considerable abnormality. The concept of retrograde degeneration of the axon extending to the first internode applies only to the most benign lesions, that of crushing the nerve between the tips of a jeweller’s forceps. 2. As time goes by the cellular response in both stumps changes from one friendly to regeneration to one less favorable. Dense collagenisation and a profusion of fibroblasts are characteristics of the distal stump in late cases. 3. The normal architecture of the nerve is most closely restored to normal in a well executed primary suture (Birch 1989). 4. It seems that regeneration through a graft falls away along its length and not solely at the suture lines. 5. Delay before repair leads to increasing fibrosis and to shrinking of the distal segment so that it becomes impossible to ensure an accurate topographical match.

Surgical Disorders of the Peripheral Nerves

4.1 The Response of the Nerve and Axon to Transection The cellular response. The cellular process of regeneration involves both proximal and distal stumps and any gap between them. Wallerian degeneration is an essential preliminary to regeneration in peripheral nerves for it is a process which transforms the environment of the peripheral nerve from one which is actively hostile to the sprouting and growth of axons into one which actively supports that process. The disappearance of the distal axon is more than a withering away, rather it is an active self destructive process, “triggered by events which occur before any morphological or electrophysiological changes can be detected” (Hall 2005a). These very early events, which lead to cytoskeletal disintegration, were likened to the lighting of a fuse by Tsao et al. (1999). Within a few hours the transected axon seals off. The proximal end is transformed into a growth cone which has been defined by Lundborg (2004a) as: “a swelling at the tip of the regenerating axon and possesses multiple needlelike extensions, filopodia and broader sheet like extensions, lamellopodia.” The filpodia are rich in actin, and they may extend or retract within a matter of minutes. The axon forms new branches or sprouts: collateral sprouts arise from nodes of Ranvier at levels at which the axons are still intact; terminal sprouts arise from the tip of the surviving axon. Seddon (1975a) described this process: “the individual outgrowing streams of axoplasm – even when confined, as they may sometimes be, within one Schwann tube – have been referred to as fibers or even axons. They are, in fact, only parts of the axon or nerve fibres. The Nile is still the Nile even when the body of water, diversified by rocks or islands, breaks up into many streams.” The axon response is followed, within a few days, by a dramatic increase in the numbers of supporting cells. The influx of haematogenous macrophages into the endoneurium is accompanied by intense mitotic activity within the Schwann cells and the fibroblasts so that the number of nuclei increases by as much as six times or more (Griffin and Hoffman 1993, Dyck et al. 2005) (Figs. 4.1–4.4). The beautiful work of Mirsky and Jessen (2005) describes the development of Schwann cells from the neural crest to Schwann cell precursors, then to immature Schwann cells and finally to myelinating and nonmyelinating cells. This work provides important insights into the behaviour of the Schwann cell after nerve transection. A remarkable feature of the Schwann cell is the rapid reversibility of the last stage of differentiation following separation of the Schwann cells from the axon. This “can be achieved either by injuring nerves in vivo or by dissociating cells from adult nerves and placing them in culture without neurons. Both in  vivo and in vitro, the process entails the developmental regression and dedifferentiation of individual Schwann cells and myelin

Regeneration and Recovery

Fig. 4.1  Wallerian degeneration in the ulnar nerve at 3 weeks after section. (Electronmicroscopic study by Stephen Gshmeissner) Distal stump. Macrophage (top left) clears myelin debris. A degenerating large myelinated axon (bottom left). Schwann cells x 2880.

Fig. 4.2  Distal stump. Degenerating large myelinated axons with proliferating Schwann cells x 11340.

breakdown. The characteristic molecular markers and structural features of myelinating and nonmyelinating cells are lost and the cells reenter the cell cycle and regress to a phenotype similar to that of immature Schwann cells. Such denervated Schwann cells redifferentiate readily on reassociation with axons during nerve regeneration” (Mirsky and Jessen 2005). This redifferentiation is associated with the renewed expression of phenotypes which are specific to myelinated and non myelinated axons and also to motor and sensory axons (Hall 2009, Höke et al. 2006). The proliferation, indeed the survival, of Schwann cells is modified by the severity of

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Fig. 4.3  Proximal stump. Retrograde degeneration of one large myelinated axon, proliferating Schwann cells and sprouting axons, forming a regenerating unit x 6960.

Fig. 4.4  Wallerian degeneration in the ulnar nerve at 3 weeks after section (Electronmicroscopic study by Stephen Gshmeissner). Distal stump. Schwann cell proliferation x 6840.

the injury to the distal trunk. Examination of biopsies taken during late repairs, especially when the injury was complicated by arterial injury or by sepsis, often show remarkably few Schwann cells. Instead it seems that the cellular population is largely composed of fibroblasts, surrounded by much collagen. Myelin fragments are detectable in such cases many months after the injury (Figs. 4.5 and 4.6). Transection of neonatal sciatic nerves in the rat results in the death of teloglia at the neuromuscular junction (Tra­ chtenburg and Thompson 1996). Mirsky and Jessen (2005) point out that there is no comparable Schwann cell death

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Fig. 4.5  The proximal stump of the median nerve 3 months after rupture of the nerve and of the axillary artery, which was not repaired 8 mm from the tip of the neuroma. Disintegration of axon and of myelin with very scanty evidence of regeneration activity. x 4880.

following nerve transection after the first post natal week. In adult animals Schwann cells survive in the distal stumps for several months although their numbers slowly decrease and they respond less well to extrinsic signals: “although most Schwann cells within the main nerve trunks survive, there is also increased Schwann cell death within the nerve, indicating a partial dependence on axonal signals. Since the cells can be rescued by application of exogenous neuregulin-1, it is likely that the death is caused, at least in part, by loss of contact with axon associated neuregulin as axons degenerate after transection.” These findings provide further evidence about the harmfulness of delay before repair of divided nerves an also offer a possible explanation for the rather poor recovery of muscle function in the neonate (Anand and Birch 2002). The axon. The axon sprouts form clusters which are surrounded by the cytoplasm of one Schwann cell and its basal lamina: “the regenerating units” of Morris et al. (1972a, b). Dyck et al. (2005) say: “sometimes in abortive regeneration many, (as many as 25–20 or more) neurites will be found in a cluster - regenerative nerve fibre clusters.” The sprouts within one regenerating unit represent the regenerative effort of one

Surgical Disorders of the Peripheral Nerves

Fig. 4.6  The proximal stump of the median nerve 3 months after rupture of the nerve and of the axillary artery, which was not repaired 2 cm proximal to the rupture. One surviving myelinated axon embedded within dense collagen. x 3400.

neurone and its axon (Figs. 4.7–4.9). The proximal segments of regenerating axons become ensheathed by Schwann cells. Enlargement of the diameter of the axon is one important signal for myelination. The regenerating sprouts of unmyelinated fibres remain so. The ensheathment of the growing axon is brought about by complex interactions involving the laminin component of the basal lamina and receptors such as the integrins in the plasma membrane of the Schwann cell and also between the adjacent plasma membranes of the axon and the Schwann cell (Mirsky and Jessen 2005). Reorganisation of regenerating nerve fibres by compartmentation. Cajal (1928b) described the process called “compartmentation” by Morris et al. (1972c) in which the proximal stump becomes divided into “mini fascicles,” replacing the original large bundles (Cabaud et  al. 1982). Griffin and Hoffman (1993) described the process by which endoneurial fibroblasts proliferate, migrate, and form a partial basal lamina: “adopting the appearance of perineurial cells; in extreme cases they divide into “mini fascicles”.” We have seen this pattern in many grafts in small mammals and in failed grafts coming to revision in the human. Even after an ideal

Regeneration and Recovery

Fig. 4.7  Regenerating units. Proximal stump of ulnar nerve at 3 weeks after section. (Electronmicroscopic study by Stephen Gshmeissner) Numerous axon sprouts, Schwann cell processes, commencing remyelination with some retrograde degeneration. x 2784.

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Fig. 4.9  Regenerating units. Proximal stump of ulnar nerve at 3 weeks after section. (Electronmicroscopic study by Stephen Gshmeissner) Axonal sprouts adjacent to a Schwann cell nucleus x 3190.

Fig. 4.8  Regenerating units. Proximal stump of ulnar nerve at 3 weeks after section. (Electronmicroscopic study by Stephen Gshmeissner) Axonal sprouts and Schwann cells x 17980.

laboratory repair, immediate suture after clean transection, regenerating nerve fibres burst out from the perineurium at the suture line and form mini fascicles in the epineurium. Perhaps the process of compartmentation into mini fascicles should be seen as an aberrant or incomplete form of regeneration? (Figs. 4.10–4.13). Guidance and selection. In a carefully performed crush by jeweller’s forceps only the axon is interrupted and growth cones elongate along former Schwann tubes, “the cluster of axonal sprouts Schwann cells and macrophages enclosed in a Schwann cell basal lamina tube are the counterpart of what light microscopists call bands of Büngner” (Dyck et al. 2005). Unfortunately this most favorable situation is rarely

Fig. 4.10  Compartmentation or mini fascicle formation in the proximal stump of the common peroneal nerve ruptured 9 weeks previously in an 8 year old boy. Myelinated and unmyelinated axons and their ensheathing Schwann cells are loosely associated with perineurial like fibroblasts. x 3400.

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Surgical Disorders of the Peripheral Nerves

Fig.  4.11  Failure of regeneration through a graft inserted 3 years p­ reviously to bridge a gap in the median nerve. The proximal suture line. Many small bundles (minifascicles) of regenerating myelinated fibres. Scale bar: 100 mm.

Fig. 4.12  The middle of the graft. Increasing fibrosis and loss of neural elements. Scale bar: 100 mm.

encountered in clinical practice. Other mechanisms become important in the control of the exuberant but chaotic regeneration which occurs after nerve repair. Witte and Bradke (2005) describe the guidance of the growth cone: “guidance cues act either by direct contact (e.g., between the axonal growth cone and a repelling environment) or as diffusible factors that are secreted by the target regions. Thus they act as short range or long range cues.” If the “growth cone” encounters non neural tissue, axonal elongation still occurs and may even be followed by myelination. Witzel and Brushart (2003) studied the behaviour of axons traversing a gap. Some projected directly into distal Schwann tubes even though they meandered about in the gap and continued to produce collateral sprouts. Others “arborized,” sampling a number of distal tubes, whilst still others ended in the gap whilst sending out minute sprouts with multiple growth cones. Lundborg (1991) helpfully defines the terms neurotrophic and neurotropic. “A neurotrophic factor (nemron (neurone)

Fig. 4.13  Failure of regeneration through a graft inserted 3 years previously to bridge a gap in the median nerve. Distal segment of graft. Poor regeneration. Scale bar: 100 mm.

and trofh (trophe): nutrition) is a substance influencing survival and growth of nerve cells. A neurotropic factor (nemron (neurone) and tropoV (tropos): way, conduct) is a substance exerting an attraction, at a distance, on growing axons.” He later refined this view (Lundborg 2004a) because neurotrophic factors such as nerve growth factor (NGF) also exert a tropic influence. Trophic and tropic influences are preferable terms. Experiments were undertaken in which axons growing from the proximal stump were “offered” a choice between nerve, tendon and granulation tissue as distal targets. Nerves almost exclusively grew towards nerves (Lundborg et  al. 1986, MacKinnon et  al. 1986a). An even further degree of specificity may lead motor axons to motor endings and sensory axons to sensory endings (Brushart 1988). Brushart and Seiler (1987) studied regeneration in the rat femoral nerve using retrograde labeling techniques and demonstrated that motor axons entering sensory pathways were “pruned” whilst those entering motor pathways were

Regeneration and Recovery

maintained. Redundant axon sprouts atrophy (Bennett et al. 1986, MacKinnon et al. 1986b, Brushart 1993). There are limits to neurotropism: in experimental repairs where the stumps were deliberately malaligned axonal dispersion was determined by fascicular size, not by fascicular identity (Brushart et al. 1995). Hall (2005a) puts it thus: “there is no doubt that, providing the gap length does not exceed 1 cm, adult rat axons and their associated cells behave as though they are responding to “tropic” signals emanating from a distal stump. The extent to which specificity exists at the fascicular or nerve trunk level has been difficult to establish, perhaps because it is only unmasked in particular experimental protocols, and cannot be demonstrated when axons are challenged to enter grafts rather than intact distal stumps.” Clinicians must strive for accurate topographical alignment during repair whether by suture or by graft, and must accept the limitations of neurotropism exerted by a cutaneous nerve graft. Maturation. Initially, there are more axonal sprouts than there were axons in the intact nerve, but only those that establish connections with end organs survive (Sanders and Young 1946, Aitken et al. 1947). This can cause difficulty in estimating recovery by the numbers of myelinated nerve fibres (MNF) crossing a lesion. In a series of experiments, the sciatic nerve of the rat was transected and repaired by immediate (primary) or delayed suture at 2 weeks, or by immediate grafting or delayed grafting. Predegenerate grafts were also tested. (Birch 1989). The nerves were examined 1 year later. Even at this interval the numbers of MNF at the suture line and in the proximal segment of grafts were increased by about one third more than the number in the proximal trunk or in control nerves. The numbers of MNF in the distal trunk were reduced by about 25% in the primary sutures, by 33% in the secondary sutures and primary grafts and by 40% in the delayed and predegenerate grafts. These differences corresponded to such functional measures of outcome as power and weight of the reinnervated muscles. As connections are established and the regenerating nerve matures, the original profusion of Schwann cells gives way to the more orderly arrangement characteristic of the healthy nerve. Sanders and Young (1946) and Vizoso and Young (1948) studied internodal length and fibre diameter in the developing and regenerating nerves of rabbits. In the adult the former relationship between fibre length and internodal length did not reappear: internodal lengths were always shorter in the regenerated than in the healthy nerve. Griffin and Hoffman (1993) suggest that this is because longitudinal growth in regeneration occurs at the growing tip, whereas the internodal length increases by true longitudinal elongation during growth after birth. The production of nerve growth factors in the distal nerve by endoneurial fibroblasts, macrophages, Schwann cells and by muscle and skin provide an environment friendly to regenerating axons. Indeed, Griffin and Hoffman (1993) remark

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“given the environment of the distal stump, it is perhaps surprising that functional restoration is so seldom the consequence of nerve injury in humans.” The perspective of most clinicians is perhaps rather different: they think that the results they obtain are not all that bad considering the natural difficulty encountered by regenerating nerve fibres in reaching their targets. When there is a lesion “in continuity” or when healthy nerve end has been opposed to healthy nerve end, the elongating axon enters the environment most favorable to it: the denervated distal stump. Early and accurate suture of a divided nerve is followed by reconstitution of the trunk which is closest to normal. On two occasions the suture lines of the median and ulnar nerves 12 months after reattachment of the amputated hand were inspected during operations of tenolysis. The perineurium surrounding the bundles had reformed, there was only slight thickening of the epineurium and there was no visible neuroma. One indication about the accuracy of repairs completed within 3 or 4 h of the injury is the temporary restoration of conduction. On several occasions we have evoked the appropriate muscular response by stimulating the nerve trunk proximal to the repair. After even the most careful primary suture of a cleanly divided nerve it seems that there is: (1) a diminution in the number of nerve fibres which have made successful reconnection with their target tissues; (2) reduction in the calibre of those nerve fibres; (3) shortening of the internode and (4) slowing of conduction. These facts should not permit any sense of therapeutic nihilism: the best chance for the restoration of useful function rests on following the fundamental principles in the treatment of wounds by prevention of sepsis, restoration of flow through an injured axial artery, restoration of perfusion of the tissues, stabilisation of any fracture and providing full thickness skin cover over the repair. The nerve itself should be repaired as soon as reasonably possible. Whilst there may be a limit to technique much more needs to be done to improve the organisation of the handling of severe nerve injuries. The neuroma. Neuroma is a common example of the fate of the regenerating axons which are unable to form any connections with original targets. Griffin and Hoffman (1993) describe the behaviour of the growth cones when they enter “trackless regions of connective tissue or other foreign tissue even in this setting, the impulse to growth and extend continues; it may result in a meandering elongation followed by at least partial axonal maturation and myelination, culminating a neuroma near the site of the injury, or fronds of regenerating fibres extending over connective tissue planes.” A neuroma is an expression of the vitality of the neurones producing new axons. After amputations of the lower limb it is common to find neuromas of the main nerves 3  cm or more in length, which contain abundant myelinated nerve fibres rather chaotically organised into mini fascicles. Barnes et  al. (1945) revealed the capacity for robust regeneration many months

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after injury. An ulnar nerve was exposed more than 600 days after it had been divided. It could not be repaired. A piece of the distal stump of the nerve was removed and sutured to the proximal stump after the neuroma had been resected. It was a predegenerate graft. This segment was later removed and examined. The graft was reinnervated throughout but there was no myelination of the fibres. Barnes and his colleagues thought that this lack of myelination was due to endoneurial collagenisation, with consequent narrowing of the Schwann tubes, a suggestion made earlier by Holmes and Young (1942). Another reason is provided by Li et al. (1998) who showed that Schwann cells separated from axons for a long time lose their capacity to support regeneration and remyelination. The only way to avoid inflicting neuromas upon patients during the course of treatment is to avoid cutting nerves. Sometimes neuromas are responsible for severe and debilitating pain particularly so when the nerve is only partially injured. It seems strange that wounding a terminal branch of a cutaneous nerve so often leads to severe pain whilst the planned and deliberate section of that nerve at its origin very rarely does so. (Fig. 4.14) It is usual to find numerous axons, some of them myelinated, in the tissues bridging nerve stumps in the human: so it was in the cases studied by Terenghi et al. (1998). These findings illustrate the difference between regeneration and recovery. The extent of reinnervation of the skin by collateral sprouting after resection of a cutaneous nerve was examined by Healy et al. (1996). Twenty patients were studied in whom upper limb nerves had been used as grafts. The area of donor nerve sensory defect shrank by rather small amounts: 6  mm for light touch, 7  mm for sharp pain, and 11.5 mm for heat pain. There was no change in the area of loss for warming and cooling sense. Healy and his colleagues

Fig.  4.14  NGF immunoreactive fibres in a human painful neuroma, x 40 (Courtesy of Professor Praveen Anand).

Surgical Disorders of the Peripheral Nerves

found that sweating did recover, and caution against using this as an indication of nerve recovery (Figs. 4.15–4.17). The rate of regeneration. The rate of peripheral outgrowth of regenerating fibres is reckoned at about 1 mm a day in the human adult: that is about the rate of slow axoplasmic transport. The rate is substantially faster in children, as indeed it is in young experimental animals. It is almost certainly faster after primary than after secondary repair (Birch and Raji 1991) and is faster proximally than distally. We suggest a rate of 2 mm a day after suture of clean wounds of nerves at clavicular level and in the proximal part of the lower limb. Indeed, we have seen a rate of 3 mm a day after suture, or even after graft of ruptures performed within 24 h of injury, a rate similar to that recorded by Holmes and Young (1942) in their experiments on rabbit nerves. Why not? Such wounds are nearer to the nerve cell than are more distal injuries. Case report. A 24 year old soldier sustained a missile injury to the upper thigh which caused an extensive comminuted fracture of the sub trochanteric region of the femur. The fracture was stabilised and the sciatic defect, which measured more than 5  cm, was grafted 5 days after injury by Wing Commander Ian Sargent and Mr Garth Titley, Birmingham. By 180 days there were strong Tinel signs for both divisions

Fig. 4.15  Useless regeneration. Failure of recovery in a median nerve sutured 3 years previously. Proximal to the suture line. Clusters of myelinated axons extensive endoneurial collagenisation x 4300.

Regeneration and Recovery

Fig. 4.16  Useless regeneration. Failure of recovery in a median nerve sutured 3 years previously distal to the suture line. There was no recovery of function in spite of the presence of regenerating well myelinated axons x 4300.

of the sciatic nerve in the upper third of the leg at a distance of 44 cm from the proximal suture line. Flexion of the heel was powerful and there was early recovery into tibialis anterior suggesting that motor axons had traversed at least 35 cm (2 mm a day) of the length of the limb. The patient had no pain. This example of strong regeneration after urgent repair is by no means unusual, indeed we consider it the rule.

4.2 The Repair of Large Gaps Direct apposition may be impossible because of the fixed retraction of stumps in delayed cases or because so much of the nerve has been destroyed by the injury. Methods of bridging this gap have been extensively studied for more than 100 years. They include: 1. Autogenous grafts of cutaneous nerves 2. Autogenous grafts of main nerves. These may be vascularised as a pedicle or as a free graft 3. Homografts or allografts 4. Non neural material

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Fig. 4.17  Useless regeneration. Failure of recovery in a median nerve sutured 3 years previously. Biopsy of the skin of the index finger. Schwann cell processes and some unmyelinated axons x 18000.

Sanders (1942) recognized the essential role of Schwann cells when he classed operations for the repair of large gaps in the peripheral nerves into two groups: those which provide orientated live Schwann cell columns, down which large numbers of fibres can grow and become mature,........ and those which provide some form of artificial scaffolding down which....... the new fibres and Schwann cells can grow in a regular manner.

The Schwann cells promote, sustain and guide regenerating axons. Regeneration in the peripheral nervous system is possible only because of the interaction between the Schwann cell and the axon (Hall 2005a,Hall 2005b). Some of these methods are now considered. The technical aspects are set out in Chap. 7 and results in Chaps. 8–10. Regeneration through grafts. Tinel (1917) wrote: “when the distance between the segments of the nerve trunk is too great to permit direct suture the only legitimate operation is nerve grafting as recommended by J and A Déjerine and Mouzon.” He further added “nothing but nerve tissue can serve as a conductor for regenerating axis cylinders” and roundly castigated “mischievous” operations such as lateral implantation, transplantation of a motor nerve into a sensory one and isolation of nerve by foreign body. Only the

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interposition of a “muscular- or better still, a fatty-layer” between a nerve and callus or bony projection is permitted. It seems difficult to add to this. Sanders (1942) thought that the earliest adequately studied case of repair by fresh autograft was that performed by Dean in 1896 and reported by Sherren (1906), and he commended the series of Foerster (1929), Bunnell and Boyes (1939) and Joyce (1919) for their thoroughness. Sanders (1942) confirmed and extended observations made by workers in the first decades of the 20th century in concluding that: “autografts remain alive and myelin fragmentation and Schwann multiplication go on in them much as in a normal peripheral stump.” Human cutaneous nerve grafts could be fully reinnervated, presenting an appearance barely distinguishable from normal (Seddon et al. 1942, Gutmann and Sanders 1942, Seddon 1954. The ulnar nerve could be used with success but nerves of larger caliber were much less successful; a grafted segment of the common peroneal nerve simply necrosed (Seddon 1947). These observations stimulated the development of the vascularised ulnar nerve as a pedicle graft (Strange 1947) and a similar method for the common peroneal nerve MacCarty (1951). Millesi (1973) provides further evidence about the ill effects of tension and also about the necessity of accurate topographical disposition of the grafts. It is often said that grafting is the “gold standard” in the repair of nerves with defects but adherence to the gold standard led to severe financial difficulties for more than one nation and a considerable set back in Churchill’s career whilst he was Chancellor of the Exchequer in the 1920s. We have seen a high rate of failure amongst the more than 4,000 grafts of trunk nerves carried out since 1965. We are not alone in recording a success rate for repair of the more severe injuries to nerves which is little better than that set out in the Medical Research Council Special Report Series No. 282 (1954). The chief advantage of grafting is that it overcomes tension, which, as Highet and Sanders (1943) demonstrated, leads to a slow traction injury and ischaemia of the nerve after removing protecting splints. Seddon (1975b) commented that: “suture under tension… is not practiced by any knowledgeable surgeon today” and he referred to the normal elasticity of nerve which is not a negligible factor. Wide retraction of the stumps in closed traction lesion is usual and it is a simple matter to draw the nerves back to their normal position during operation performed within the first 1 or 2 days. It is always easy to be wise after the event but it now seems that suture would have been the better way forward in some of our cases particularly for nerves injured at the elbow, the knee and the wrist. In an earlier study of repair of the median and ulnar nerves at the wrist and forearm (Birch and Raji 1991) there was no detectable difference in the results between the 25 sutures and the 35 grafts. The gap after resection of the neuroma was measured with the elbow extended and the wrist at 20° dorsi flexion. The average gap was 2.5 cm in the sutures and 5.5 cm in the grafts. Trumble (1991) provides sound advice about reasonable methods of diminishing

Surgical Disorders of the Peripheral Nerves

the gap between nerve stumps by careful mobilisation and by positioning of adjacent joints and he emphasizes that the gap is always longer in delayed repairs. Wherever possible the stumps of transected or ruptured nerves should be approximated at the first operation in cases where circumstances prevent primary repair. The shortage of available donor graft means that the sciatic nerve should be sutured wherever possible, even though the patient must endure a hip spica with gradual release for some weeks. Clinicians must never forget that nerve grafts obtain their blood supply from the bed in which they lie. The admonitions of Tinel and Delorme were restated by Seddon (1947): “since the wounds of nerves that call for repair by grafting are usually extensive the need for the replacement of skin scars by healthy tissue arises with corresponding frequency. Nothing less than a full thickness flap or tube pedicle graft will suffice since it is important the graft should lie, so far as is possible, in healthy well vascularised tissue.” Leaving a nerve graft within scarred muscle or underneath split skin graft just will not do. The limitations of conventional grafting. 1. There is only a limited amount of cutaneous nerve available. In an adult with a complete lesion of the brachial plexus it is possible to collect about 180 cm of nerve by using both sural nerves with the cutaneous nerves of sensation from the injured limb. 2. The added defect imposed upon the patient may be too severe. The lateral cutaneous nerve of forearm and the superficial radial nerve provide significant innervation to the skin of the thumb, the thenar eminence and the palm of the hand. We use them only when the parent nerve is irreparably damaged. The supraclavicular nerves provide important sensation from the skin above the clavicle, over the shoulder and the upper part of the chest. The sural nerve innervates the heel and it should not be used for repair of low lesions of the tibial nerve. Pain is a common complication after deliberate wounding of the terminal branches of the nerves of cutaneous sensation and it is advisable always to section the donor nerve proximally, deep to the deep fascia. We agree with Seddon (1975c) in favoring the medial cutaneous nerve of forearm over other cutaneous nerves. 3. The architecture of a cutaneous nerve bears little resemblance to that of a main nerve trunk. The fifth cervical nerve contains between four and eight bundles. The largest of these requires one strand of cutaneous nerve which may contain between 8 and 20 such bundles. Dyck et al. (2005) examined the cross sectional area occupied by myelinated nerve fibres (MNF) in the roots of the spinal nerves, in the spinal nerves and more peripheral nerves. Myelinated fibres accounted for between 46% and 70% of the cross sectional areas of the ventral root of L5; the area fell to between 23.8% and 34.5% in the proximal sural nerve. The area occupied by MNF in the dorsal roots of

Regeneration and Recovery

L5 lay between 35.8% and 50.1%. In equally painstaking studies Dyck et al. (2005) showed that the median diameter of MNF in the ventral root of L5 was 12 mm. It was about 5 mm in the tibial nerve and just under 4 mm in the sural nerve. The median diameters in the fibres of the dorsal root resembled those found in the peripheral nerves. These findings suggest that there are serious defects in cutaneous nerve grafts particularly when they are used for repair of the ventral roots of the brachial plexus or the most proximal parts of the spinal nerves because of the disproportion in the volumes occupied by conducting tissue and the calibre of nerve fibres. Seddon (1975c) had this to say about the possible effects of fibre size: “it might therefore be thought that motor recovery through the cutaneous nerve graft would be appreciably inferior to the sensory recovery. The evidence presented by our series of cases shows that this possible objection has little substance; and Simpson and Young (1945) have shown that large fibres in the proximal stump have no difficulty in inflating rather smaller distal Schwann tubes, and so attaining a diameter sufficient for their effective function.” However Young (1942) recognized the limitations of experimentation on small mammals and in particular, the robust regeneration characteristic of the rat and the rabbit. The problem resurfaces when regenerating axons having traversed the graft reach the distal trunk of the nerve for here, particularly in late or neglected cases, the Schwann tubes are embedded in dense collagen. 4. The recognition that Schwann cells may be specific either to motor or to sensory axons casts a shadow over the use of cutaneous nerves for the repair of main nerves (Hall 2009, Höke et al. 2006). Nichols et al. (2004) and Lago et al. (2007) showed that the regeneration of motor axons is better promoted by a graft of a “motor” nerve whilst the regeneration of sensory axons is better through a graft from a cutaneous nerve. Whilst there is no such thing as a purely motor or sensory nerve within the peripheral nervous system these findings may account for the relative success of vascularized main nerve grafts. We reproduce a section through such a graft showing numerous myelinated and unmyelinated fibres but, perhaps disappointingly, we show sections through a failed vascularised sural nerve graft in which the vascular anastomosis remained patent and yet regeneration failed (Figs. 4.18–4.22). 5. The nerve pedicle operations remain extremely useful in the most severe cases especially so in otherwise irreparable injury of the sciatic nerve. It is strange that these innovative techniques seem to have been forgotten by so many clinicians. 6. The most elaborate method of nerve repair cannot overcome the baleful effect of delay. Allografts. The advantages of the autogenous cable graft are now so well known that we tend to forget that earlier last

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Fig. 4.18  Regeneration through a vascularised ulnar nerve graft (fifth cervical nerve to lateral cord). Although the biceps muscle recovered well, the appearance of the hand led the patient to demand amputation. Note the numerous myelinated and unmyelinated fibres without excess of collagenisation x 2142.

century surgeons obtained what we would now consider remarkably good results with grafts which would now not be used. Thus, Mayo-Robson (1917) reported a good result after repair of a lesion of the median nerve with an allograft of median nerve, and another good result after repair of another lesion of the median nerve with a length of the spinal cord of a rabbit. Barton (2005) has provided us with details of the use of calf’s nerve for repair of a war wound to the right (dominant) median nerve, in 1917. The operation was done at Baschurch Military Hospital (in Shropshire). The patient lived to the age of 90 years and recovery was good enough for him to act as organist to various churches and chapels. The method was thoroughly and extensively reviewed by Sanders (1942), and by Sunderland (1978). Seddon (1975d) pointed out that the immune reaction may be avoided either by reducing the antigenicity of the graft or by suppression of the response in the host: “it must be remembered that repair of a nerve is not a life saving operation.” A number of methods were used including treating the graft with alcohol or with other agents, freeze drying and irradiation. The results were generally very poor but there was the occasional success. The introduction of newer methods of immuno suppression

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Fig.  4.19  Failure of regeneration through a vascularised sural nerve graft used to repair a long defect in the median nerve. At re-exploration two years after operation the vascular anastomosis was found to be patent. (Electronmicroscopic study by Michael Kayser) Just distal to the proximal suture line. Mini fascicles (arrows) of myelinated and unmyelinated nerve fibres x 2108.

allowed MacKinnon (1996) to give a qualified recommendation: “In the carefully selected patient with an otherwise irreparable nerve injury, consideration for nerve transplantation should be given.” Hand transplantation provides one dramatic example of allograft. Schuind et al. (2006) described the first Belgian patient at 37 months after operation, showing very impressive recovery for motor, sensory and sympathetic functions. Larsen et al. (2007) sound a warning note in reporting Epstein Barr virus infection complicating transplantation of a nerve allograft from a living donor.

4.2.1 Other, Non Neural, Material for Grafts: Entubation Surgeons have for many years sought a source of material for graft to supplement or to replace the rather meagre stock provided by dispensable cutaneous nerves.

Surgical Disorders of the Peripheral Nerves

Fig. 4.20  Just distal to the proximal suture line. A mini fascicle (small arrows) of myelinated and unmyelinated nerve fibres lie just outside the perineurium of one of the vascularised strands (large arrows) x 6270.

The freeze thawed muscle graft (FTMG) introduced by Glasby et al. 1986 is a method which has been used extensively in laboratory and clinical studies. Hall (1997) showed that axonal regrowth through short acellular muscle grafts requires a sustained supply of Schwann cells, perineurial cells, and fibroblasts. Schwann cells may migrate from the stumps of the nerve on either side of the acellular graft or which may be “seeded” in that graft (Calder and Green 1996). Thomas et al. (1994) defined a particular role for FTMG in the repair of damaged cutaneous nerves, in the treatment of the painful states arising from such damage. Although in such cases an adequate supply of nerve is available for grafting it seems perverse to inflict a lesion on a cutaneous nerve in a patient suffering from the results of damage to another. A paper of importance appeared from Pereira et al. (2008) who treated the leprotic hand and foot by replacing the damaged segment of the median or tibial nerve with FTMG. Most patients recovered protective sensation; their ulcers healed. Doubtless, a number of amputations were prevented. One

Regeneration and Recovery

Fig.  4.21  The middle part of the graft. Endoneurial fibrosis; myelinated and unmyelinated axons; a suggestion of new perineurium formed from fibroblasts (arrows). x 1770.

intriguing finding was the improvement in the condition of the skin in one third of the contralateral feet. Entubation. In 1997 Lundborg and colleagues (Lundborg et al. 1997) published a significant paper describing a prospective randomized trial comparing silicone entubution and suture of median and ulnar nerves in the forearms of 18 patients. Recovery was studied most thoroughly and no significant difference in outcome between the two groups was noticed. They wrote “in one case, the tube was removed at 11 weeks. Upon opening the tube, it was found that the former empty space was now occupied by newly formed nerve tissue in direct continuity with the proximal and distal ends..... it was not possible to define the exact level of the previous nerve injury.” The proposed advantages following placing of nerve stumps within a silicone tube, so providing a “chamber” separate from the surrounding tissues, include: the local accumulation of neurotrophic factors; the longitudinal orientation of fibrin matrix within the tube; and the possibility for the regenerating axons to be better guided into distal Schwann tubes across the gap. The tube must not be too tight. Silicone entubation may cause constriction and fibrosis of a sutured nerve (Birch 1979).

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Fig.  4.22  Failure of regeneration through a vascularised sural nerve graft used to repair a long defect in the median nerve. At re-exploration 2 years after operation the vascular anastomosis was found to be patent (Electronmicroscopic study by Michael Kayser). The distal portion of the graft. This shows one of the few surviving clusters of neural elements. Several myelinated and unmyelinated axons lie within the perineurium x 4408.

With the exception of some cases using the freeze-thawed muscle graft, it seems that the upper limit of a defect reparable by these methods is 3 cm. Repair of the long gap by means other than autogenous graft remains elusive. De Ruiter et  al. (2009) conclude that there is, as yet, little evidence demonstrating the superiority of empty, hollow biodegradable nerve tubes over suture or autografting and that: “the repair of all sorts of nerve lesions may lead to unnecessary failures and, again, a discontinuation of interest in the concept of the nerve tube. The extensions of the applications, especially in a repair of larger mixed or motor nerves, should be carefully evaluated.” Hall (2005b) defines the ideal conduit which should have: “walls that are biologically bio compatible and resorbable, sufficiently robust to resist collapse, and yet not so rigid that they compress the structures which they surround, and a lumen whose contents…. facilitate orientated and sustained axonal elongation. It goes without saying that it must also be easy to handle and to suture. It also goes without saying that

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such a device does not currently exist.” Some show promise: one such is the bioresorbable glass fibre technique investigated by Bunting et  al. (2005) in nerves of the rat. Axonal regeneration was indistinguishable from that seen in autografts. Hall’s more recent essay (2009) reviews the use of such natural polymers as collagen and various polysaccharides and a wide range of synthetic polymers. One essential requirement of the biodegradable conduit is that the degradation products must not be cytotoxic. Manipulating the behaviour of the growth cone will determine the path of the regrowing axon “since wherever the growth cone goes, the rest of the attached axon must surely follow.” Hall (2009) goes on: “given that axons and Schwann cells comigrate, it is perhaps surprising that little or no attention has thus far been paid to manipulating Schwann cell outgrowth from the nerve stumps.” The work of Caddick et al. (2006) opens the possibility of encouraging the differentiation of mesenchymal stem cells along a Schwann cell lineage. Cells were removed from the marrow of long bones of rates and cultured. Those cells cultured with glial growth factor (GGF) increasingly expressed such Schwann cell markers as S-100, p75, and glial fibrillary acidic protein (GFAP). The cells were then co cultured with neurones from the dorsal root ganglion and those which expressed Schwann cell markers enhanced neurite outgrowth from the sensory neurones to the same level as that produced by Schwann cells. This work represents a potentially important advance because the culture of autologous Schwann cells in the adult human is such a lengthy process. The development of micro-machined sieve electrodes may prove to be extremely important. These are made from silicone (Wallman et  al. 2001) or polyimide (Zhao et  al. 1997, Navarro et al. 1998) and are inserted into conduits to create a neural interface which can be used to control a limb prosthesis. Is it possible that these developments might enable the reconnection of stumps of the spinal nerves within the spinal canal, a concept put forward by Bonney (1977).

4.3 Nerve Transfer Nerve transfer, also known as neurotisation, or nerve crossing, involves the passing of nerve fibres from a healthy nerve to the distal stump of an injured nerve and this principle can be applied in a number of ways. 1. End to side transfer by suture of the distal stump of the injured nerve onto or within the epineurium of the healthy donor. 2. Transection of a healthy donor nerve and transfer onto the distal stump of the injured nerve. 3. Transfer of one or more healthy bundles within an uninjured donor to the recipient. This important technique was studied and used by Oberlin et al. (1994) and it rests on

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the functional segregation and topographical organisation of nerve fibres within the donor nerve trunk so that it is possible to take one bundle from the ulnar nerve to reinnervate the nerve to biceps without inflicting any significant loss of function within the hand. The method has been extended to the transfer of intact bundles from C7 or C8 to the suprascapular nerve or to the avulsed ventral root of an adjacent spinal nerve. 4. Transfer of the proximal stump of a divided nerve onto the distal stump of another divided nerve. 5. Direct muscular neurotisation. Sometimes a nerve is avulsed from the muscle. The musculocutaneous and the circumflex nerves are most commonly affected. Sorbie and Porter (1969) took the nerve to the flexor carpi ulnaris muscle in dogs and implanted it into flexor carpi radialis. Muscle volume was restored and the twitch strength of the reinnervated muscle reached 50% of normal by 40 weeks. Brunelli and Monini (1985) developed a concept of implantation of a working nerve directly into the paralyzed muscle, calling this method “direct muscular neurotization.” Narakas (1988) described considerable experience with the method. The extent of afferent reinnervation of the muscle offers a fruitful field of study. End-to-side repair. Insertion of the stumps of damaged nerves into adjacent undamaged nerves is amongst the earliest of methods tested for bridging large defects. Sanders (1942) pointed out that the operation of “double lateral implantation” could be performed in one of two ways. The prepared stumps might be implanted into longitudinal slits between the bundles of the host nerve; or, some bundles within the host nerve could be cut at two levels and the prepared stumps sutured to these. In the first operation, axons from the implanted central stump might grow down through the epineurium: “an environment which contains no Schwann cells.” Kilvington (1907) investigated the second method, where bundles of the undamaged nerve were sectioned to act as a bridging graft and showed that there was histological evidence of reinnervation of the distal part of the damaged nerve. Ballance and Ballance (1903) used the technique in repair of the facial nerve. Kettle (2003) provides an extensive review and a careful analysis of the method using nerves in the sheep as a model. She demonstrated that end-to-side nerve repair “did support nerve regeneration” but her findings “do not support the view that this technique is associated with a functional outcome.” Carlstedt (2007a) sets out important objections to the technique. The internal environment of an uninjured nerve is not conducive to new axonal growth. It is only after injury to the donor nerve, by opening the perineurium that changes are induced in the Schwann cell phenotype more favorable to axonal growth. Regeneration is now end to end. One carefully studied clinical example comes from Irwin et al. (2006) whose patient sustained severe injuries to both legs. A below knee amputation proved necessary on the

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right side but the undamaged plantar skin of the right foot was used to successfully resurface the left foot in which the plantar skin had been avulsed. The right tibial nerve was transferred to the intact left tibial nerve by an end-to-side method without incision of the epineurium. Quantitative sensory testing (QST) at 9 months revealed that the patient could localize pressure but was not able to feel cotton wool or pinprick over the sole. She could perceive a graded monofilament of 7.5 g on the sole (normal, less than 0.08 g). Vibration sense was present but the threshold was elevated. She could not detect warm or cool sensations but sweating was close to normal. By 16 months there was clear improvement in the thresholds to vibration and light touch. Vibration thresholds now lay within normal limits and the monofilament threshold had improved to 1.66 g. She could not recognize cotton wool and a pin prick was felt as a touch. There was no change in the thermal threshold. She recovered some large sensory fibre function (vibration sense and touch) and autonomic function; there was no evidence of recovery of small sensory fibre function. Nerve transfer. When, as happens with serious injuries of the brachial plexus, nerves are so badly damaged that no repair is possible and no recovery can be expected, the question of “neurotizing” or reinnervating the distal stump with the proximal stump of an intact nerve or nerves is raised. Warren Low, working at St Mary’s Hospital, Paddington with Wilfred Harris, was probably the first to suggest this expedient and to put the suggestion into practice (Harris and Low 1903). The validity of the method was, however, open to question. The matter was raised again by Tuttle (1913), who reported on the use of the spinal accessory nerve as a donor. Transfer of the hypoglossal nerve to the facial nerve became a well recognized remedy for facial paralysis in the early years of the last century (Ballance and Ballance 1903) before it was superceded by grafting (Ballance and Duel 1932, Bunnell and Boyes 1939, Collier 1940). Probably the first recorded success from nerve transfers in the brachial plexus was that of Seddon (1975c), who with Yeoman transferred intercostal nerves into the musculocutaneous nerve. Seddon acknowledged an earlier contribution: “in a case of traumatic tetraplegia extending up to the fifth cervical segment Benassy and Robart (1966) helped the patient very considerably by severing an intact musculocutaneous nerve and uniting it to the neighbouring totally paralysed median.” Tsuyama and Hara (1973) adopted intercostal nerve transfer for patients with complete avulsion injury in 1965 and Nagano et al. (1989) described the results in 179 patients More than 80% of their patients regained functional flexion of the elbow. Kotani et al. (1972) and Allieu (1989) described the use of the distal part of the spinal accessory nerve in re-innervation of the upper limb preserving rami to the upper fibres of trapezius. A great deal of detailed and important work towards the study of potential nerves

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available for transfer is set out in the volumes published by the Groupe d’Étude de la Main which were brought together by Alnot and Narakas (1989, 1996). Nerve transfer has developed as an essential part of the treatment of severe intradural lesions of the brachial plexus, and until the place of intradural re-attachment or repair is established, it is likely to remain so. It is also valuable in some peripheral lesions. Gore (1978) restored powerful wrist extension by transferring a nerve to the medial head of triceps to the radial nerve, 15 months after the injury. Gousheh (2002, personal communication) transfers the nerve to the lateral head of gastrocnemius to the deep division of the common peroneal nerve in severe lesions. The superficial division, which is usually more amenable to repair, can be grafted at the same time. Carlstedt (2007b) recommends the technique “in cases where intra spinal repair of a lumbosacral plexus lesion is impossible, eg. when there is no proximal, ventral root stump to use for reconstruction, it is possible to perform nerve transfers.” One example is described in the important paper from Lang et  al. (2004). The patient, a 5 year old girl, presented with bilateral, asymmetric injuries to the lumbo-sacral plexus. Paralysis of the abductors of the hip on one side was treated by placing a graft between the superior gluteal nerve and two bundles within the femoral nerve. Paralysis of the extensor muscles of the knee on the other side was treated by transfer of intercostal nerves 10 and 11 to the femoral nerve. 18 months later the child was able to walk independently. Brunelli and Brunelli (1999) enabled a paraplegic patient to walk by transfer of the ulnar nerve to the superior gluteal and femoral nerves. The deficit in the hand was remedied by musculo-tendinous transfer. Contra-lateral transfer. A more daring idea comes from Gu and his colleagues in Shanghai. The contra-lateral seventh cervical nerve is used to re-innervate the upper limb after a complete lesion of the brachial plexus. A vascularized ulnar nerve is used as an interposed graft. The first operations were performed in 1986 and Gu and his colleagues described promising results in ten patients with adequate follow up in 1992 (Gu et al. 1992). The method is supported by a considerable amount of experimental work (Chen and Gu 1994). One of us was able to examine some of the patients operated by Professor Gu and his colleagues in Shanghai, and some details of one of these follows. Case report. The patient, a male aged 27, sustained a complete preganglionic lesion of the right brachial plexus in a motor cycle accident on the 18th June 1993. At 3 months accessory to suprascapular and phrenic to muculocutaneous transfers were performed. At four and a half months intercostal nerves were transferred to the thoracodorsal nerve and the contralateral C7 was sutured to the ulnar nerve from the damaged limb. Eight months later the distal stump of this vascularised graft was sutured to the median nerve. The patient was examined 18 months after re-innervation of the

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median nerve. Power in the long digital and wrist flexors was MRC grade 4. There was some activity in abductor pollicis brevis and the patient was able accurately to localize touch to the thumb, the index and middle fingers. This patient had regained true hand function which could have come only from contralateral C7. Those of us examining him were unable to find any significant deficit of power or sensation in the donor limb. Closely scrutinized series have been reported by Waikakul et al. (1999) and Songcharoen et al. (2001). Our own experience of the transfer of contra-lateral spinal nerves is confined to two cases of bilateral and complete lesions of the brachial plexus. All available post ganglionic ruptures were used to reinnervate the less severely damaged upper limb. (Chap. 9). Limitations of nerve transfer: 1. There are far fewer MNF in the donor nerves than in the main trunks. The number of MNF in the spinal accessory nerve at the base of the posterior triangle is about 1,500; that number in C5, usually the smallest of the spinal nerves forming the brachial plexus, is at least 25,000. 2. The deficit imposed on the patient must not be too severe. No nerve of vital function should be used for the sake of regaining a non vital function. Phrenic nerve palsy at birth is life threatening. Some adults experience serious ventilatory impairment following injury to the phrenic nerve complicating lesions of the brachial plexus. Blaauw et al. (2006) condemn transfer of the hypoglossal nerve because of the high morbidity and disturbance of speech. We have seen one adult patient where both hypoglossal nerves were used in whom there was very serious disturbance of speech and swallowing for as long as 6 months after operation.

4.3.1 Recovery of Cutaneous Sensation after Nerve Transfer The infant. The recovery of sensation within the hand in children after repair of the brachial plexus in infancy is remarkably good. Anand and Birch (2002) studied 24 patients with severe birth lesions of the brachial plexus, in 20 of whom the plexus had been repaired. The recovery of sensation was far better than that of skeletal muscle and sympathetic function. Sensation was normal in all dermatomes for at least one modality in 16 examined hands and there was accurate localisation in the dermatomes of avulsed spinal nerves which had been reinnervated by intercostal nerves transferred from remote spinal segments. These findings are described in more detail in Chap. 10: there too are described the results of sensory recovery after nerve transfer in children and young adolescents. The reason for this difference has been sought in the better adaptation of the child’s central receptor mechanisms. The poor recovery of muscle function in these

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children may reflect the greater vulnerability of the immature nervous system to avulsion or proximal axonotomy. The adult. Özkan et al. (2001) treated 20 cases of irreparable lesions of ulnar or median nerves by transfer of the digital nerve from the inner to the outer side of the appropriate digit. Extensive sensory retraining was used in all patients and accurate localisation was restored in 18. Battiston and Blanzetta(1999) reported useful recovery into six of seven cases of high ulnar lesion by transfer of the distal part of the anterior interosseous nerve and the palmar cutaneous branch of the median nerve to the ulnar nerve at the wrist. We have transferred the dorsal branch of the ulnar nerve or the medial cutaneous nerve of forearm to the median nerve with modest success. Whilst transfer of the intercostal nerves to the lateral or medial cords often improves the trophic state of the skin of the hand in adults with severe injuries to the brachial plexus it is usual to find that stimulation of the reinnervated skin is referred to the chest wall. Appropriate referral and accurate localisation has been seen in only nine cases and these were patients with substantial muscle recovery through the transfer. Htut et al. (2006) studied 76 patients with severe injuries to the brachial plexus repaired by conventional graft, nerve transfer or reimplantation. Stimuli were appreciated in the reinnervated skin of the hand in only a few patients. More than one half of patients experienced “wrong way” sensations such as pins and needles in the affected arm or hand while shaving, touching or tapping the ipsilateral cheek or lip. In some patients these sensations were evoked by warming or cooling or by transcutaneous nerve stimulation. Two patients experienced sensations in the affected arm or hand when the ipsilateral leg was stimulated. These referred sensations could be unpleasant, with a painful or gripping quality and in one patient coughing produced a squeezing or gripping feeling at the wrist. This “wrong way” sensation generally occurred within 2 months of the operation, some months before the development of “right way” sensation which followed regeneration from the donor nerve into its new territory. In the “right way” sensation stimulation of the hand evoked feelings in the chest wall, the territory of the donor nerve.

4.3.2 Recovery of the Deep Afferent Pathways after Nerve Transfer The capacity of the child’s central nervous system to adapt to a new peripheral situation is illustrated by the case of a 13 year old boy who suffered avulsion of C5, C6 and C7 in a road traffic accident (Fig. 4.23). It seems likely that there was some reinnervation of the deep afferent pathway from the muscle spindles and the tendon sensory organs so that an appropriate pattern of inhibition and facilitation was restored within the spinal cord.

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Fig. 4.23  A 13 year old boy. Right sided lesion. Avulsion of C5, C6 and C7.Repair at 2 months: accessory to suprascapular transfer, and one bundle of the ulnar nerve to the nerve to biceps and the nerve to the medial head of triceps; the medial cutaneous nerve of the forearm was transferred to the lateral root of the median nerve. Results at 18 months: full range of lateral rotation; abduction to 60°; power of elbow flexion MRC grade 4; and power of elbow extension, MRC Grade 3+. There was a full range of active flexion and extension without obvious cocontraction.

There is considerable adaptation of the central receptor and effector mechanisms in adults after nerve transfer. The association between activity in biceps with clenching of the fist after ulnar to biceps transfer is useful in the early stages of rehabilitation. Independent flexion of the elbow without associated activity in the flexor muscles of the forearm is usual by 24 months after operation. Kanamura et al. (1993) studied 14 patients after intercostal to musculocutaneous nerve transfer. Percussing the biceps tendon induced sensory evoked potentials in four cases and appropriate reflex activity was demonstrated by electromyography. These workers concluded that: “muscle afferent fibres in the intercostal nerves reinnervated mechano-sensors in the biceps, and these evoked both cortical sensory activity and muscle activity which represents the classical stretch reflex” Sai et al. (1996) confirmed these findings in a study of 15 patients. Recovery of the elbow flexion reflex was confirmed by electromyography in nine cases and in five “tapping at various frequencies induced gradual augmentation of the integrated electromyogram of reinnervated biceps,” implying reinnervation of the muscle spindles by 1a and 2 fibres. Mano et al. (1995) demonstrated remapping within the cortical motor cortex by magnetic stimulation in 44 patients. At intervals ranging from 4 to 33 months after the nerve transfer a change from the intercostal area to that of the arm was found, and this was associated with a clear separation between ventilatory effort and that of elbow flexion. Further observations about the changes within the central nervous system following intercostal nerve transfer were made by Malessy et al. (1998) and by Malessy et al. (2003) who used functional magnetic resonance imaging (FMRI) and cortical magnetic stimulation.

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Voluntary elbow flexion became independent of breathing. In those patients who regained a powerful biceps the distribution of cortical activity did not materially differ between the injured and the uninjured arms. Regeneration of end-organs. There is, evidently, a limit to the period during which an end-organ can be denervated and yet recover after reinnervation. All end-organs have been studied: the earliest were perhaps the motor end-plates. Bowden and Gutmann (1944) did an extensive study of the response of the motor end-plates to denervation, finding that after 3 months it became increasingly difficult to identify the organs. Denervation for up to 3 years produced no degeneration nor disruption of the muscle fibres themselves. However, “shrinkage and increase of connective tissue may be too advanced to allow recovery after reinnervation.” After 3 years, disruptive changes occurred in the muscle fibres. Gutmann and Young (1944) investigated the reinnervation of muscle in rabbits and found that when muscles were kept denervated for increasing periods the proportion of old end-plates which became reinnervated was progressively reduced: “Most of the nerve fibres escape and run along between the muscle fibres, ultimately making contact with the sarcoplasm and forming new plates.” They had the opportunity of examining the extensor carpi radialis muscle of a patient whose radial nerve was repaired 5 years earlier after it had been interrupted. There was no recovery of motor power. Examination of a piece of this muscle showed that “although abundant nerve fibres were present they had failed to make connexions with the muchatrophied muscle fibres.” The regeneration of muscle spindles has been extensively studied by, amongst others, Barker et al. (1986), Barker et al. (1990), and Banks (2005). After crush injury (axonotmesis) regeneration and recovery of function is good although there is a reduction in the number of primary endings in the terminal bands coiled around nuclear bag fibres. This is related to the duration of denervation. Regeneration after repair of the nerve is much more variable. A muscle spindle may become reinnervated by afferents normally destined for the tendon organ although Barker et al. (1990) indicated that delaying repair for up to 8 weeks “did not give rise to any significant detrimental effect on such reinnervation.” The behaviour of the Golgi tendon organ has been investigated by Scott (1995, 2005). It appears that the tendon organ is relatively resistant to denervation atrophy: “after crush injury there is usually successful restoration of the 1b afferent ending, although it is reduced in extent” (Scott 2005). The pattern of recovery is worse following nerve repair. Many tendon organs remain uninnervated and the regenerated endings are frequently abnormal in appearance. Scott identified three deleterious factors: (1) the effects of denervation on the afferent axon; (2) the consequences of reinnervation by inappropriate axons, and (3) the effects caused by the reorganisation of the motor units after repair causing

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s­ ignificant alterations in the mechanical input to an individual tendon organ. Changes in the number and distribution of muscle afferent neurons in the dorsal root ganglion of the rat following transection and repair of the sciatic nerve were investigated by Myles et al. (1992). The cell bodies were labeled by injecting horse radish peroxidase into the extensor digitorum longus 300 days after the first operation. The number of labeled cells was diminished, the cell size was reduced and the somatotopic organisation of neurones within the dorsal root ganglion was altered. Michael Glasby and his colleagues investigated recovery in the deep afferent pathway in the new born and 1 year old sheep (Fullerton et al. 2001). In the first experiment the sixth cervical nerve was ruptured and immediately grafted and in the second experiment the ventral root of C6 was avulsed from the spinal cord and immediately repaired by autologous coaxial freeze thawed skeletal muscle graft. The nerves were examined 1 year later, by electrophysiological and morphometric methods. Regeneration of the largest, fastest conducting nerve fibres was defective in both the new born and in the 1 year old sheep. The maximum conduction velocity never reached normal levels and the diameter of the fibres, the axons and the thickness of the myelin sheath were all reduced. These workers found: “a selective failure of regeneration of the largest diameter fibres..... it seems more likely that the failure of recovery of fine movements is due to the fact that the proprioceptive pathway involving 1a, 1b and group 2 fibres on the afferent side and the process of a and g coactivation on the efferent side, is lost.” The changes are not confined to the end-organs of the motor apparatus: the cutaneous sensory receptors similarly undergo a slow degenerative change after denervation. After 3 years they may in fact disappear. Reinnervation tends to reverse these changes, though the longer the period of denervation has been, the less complete will be the regeneration. It is not too surprising that correlation of histological evidence of regeneration of cutaneous nerves with clinical evidence of recovery is often imperfect. Thus, Jabaley et  al. (1976) attempted to correlate sensory function with evidence of cutaneous reinnervation after section and repair of the median nerve. They found that there was no such correlation. Indeed, in one case, after division and repair of the median and ulnar nerves, two point discrimination was seriously defective in the thumb; yet, blindfold identification of objects was regularly correct and the pickup test of Moberg (1958) was performed in 1950s. Histological examination of the skin of the index and little fingers showed only an occasional nerve fibre and a few Meissner corpuscles. In contrast, a woman whose median nerve had been repaired by fascicular suture regained plentiful cutaneous innervation, but was unable to pick up objects because she could not feel them. On the other hand, Dellon and Munger (1983), using the partially denervated finger tips of three patients to correlate observations of sensibility with the presence of reinnervated

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sensory corpuscles as seen by light and electron microscopy, found that in all cases the reinnervated receptors identified were appropriate to provide the neurophysiological basis for the observed results of quality of sensibility.

4.3.3 Complications of Regeneration Recovery of function after repair of nerves is often marred by cocontraction and pain, reflecting imperfect regeneration of both the afferent and the efferent pathways. Cocontraction. The normal movement of joints is brought about by the smoothly coordinated and controlled activity in muscles and precise and delicate regulation by inhibition and facilitation of the motor neurones. Beevor (1904) showed that the sensory motor cortex controls movements rather than individual muscles. The conversion of an antagonist to an agonist is the basis of musculotendinous transfer and it is common to see patients actively extending the knee or the ankle and toes as soon as the post operative splint is removed after hamstring to quadriceps transfer or anterior transfer of tibialis posterior. This control is damaged in lesions in continuity, especially of the brachial plexus; the joints of the shoulder girdle are especially vulnerable. It is possible that some of this is caused by the reinnervation of muscle units in antagonists by the same parent motor neuron but this explanation cannot account for the initial association between ventilatory and elbow flexion effort after intercostal transfer nor for the later separation of these functions. Muscles reinnervated by nerve repair or through a serious lesion in continuity usually fail to convert after muscle transfer irrespective of their power. Perhaps the defective reinnervation of the deep afferent pathways from the muscle spindles and the tendon receptors blinds muscles, which are, after all, sensory as well as effector organs. Cocontraction is common after reimplantation of the avulsed ventral root. Hallin et al. (1999) showed, in experiments on primates, that the motor neurones reinnervating the biceps were both abundant and scattered about in the anterior horn but that: “in double labeling experiments, simultaneous links to both antagonistic and agonistic muscles from the same neurone could not be demonstrated.” Carlstedt (2007c) thinks that: “the structural basis for deficient performance such as synkinesis or cocontraction was not due to the same neurones innervating antagonistic muscles, but rather was the effect of an unspecific reinnervation by inappropriate neurones under inappropriate supraspinal control.” Another possible mechanism is described by Camp and Allen (2008) who reported cocontraction between the trapezius and the swallowing muscles in a 27 year old woman who had sustained a basal skull fracture (Fig. 4.24). There was a severe but incomplete lesion of the spinal accessory nerve at or close to the jugular foramen and involuntary activity in

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Fig. 4.25  A 25 year old man. Penetrating missile wound to the shoulder, the exit wound close to the upper medial border of the scapula damaging the spinal accessory nerve at the level of the spine of the scapula. There was cocontraction between trapezius, levator scapulae and the rhomboid muscles.

Fig. 4.24  Cocontraction between platysma, trapezius, and other neck muscles (Courtesy of Camp and Allen).

sternocleidomastoid and trapezius with swallowing. There was abnormal synchronous activity between fibres within the spinal accessory the glossopharyngeal and vagus nerves. Camp and Allen suggest that there was aberrant reinnervation by motor fibres from the cranial root of the accessory nerve, or by motor fibres from the vagus, or glosso pharyngeal nerves. Other patients have been seen in whom a partial lesion of the peripheral nerve incited abnormal activity in motor fibres within adjacent peripheral nerves (Fig.  4.25). It is possible that disturbance at a spinal or supraspinal level underlies the abnormal muscle patterning seen in some cases of recurrent or habitual dislocation of the glenohumeral joint. Regeneration and Pain. Pain is, of course, a common feature of nerve injury particularly when the agent remains active but nerve regeneration itself may be associated with pain, particularly in adults. Anand (pers comm, 2009) has pointed out that there is a lifelong need for regeneration in the autonomic nerves to the smooth muscle of the skin and viscera and also in the somatic nerves of the skin. In traumatic

neuropathy the event is usually an isolated episode involving one nerve. The neuropathy induced by chemotherapy is cyclical, so that there are repeated sequences of axonopathy followed by regeneration. In diabetic neuropathy pain is usually associated with regeneration and in this disease the process is a lifelong event (Figs. 4.26a–d and 4.27a–d). Many patients experience flitting, deep, cramping pain in muscle, months after repair of the brachial plexus or high lesions of the sciatic nerve and shortly before obvious recovery of muscle function. We consider this a reassuring symptom and often suggest to patients that this is perhaps the only “good” form of neuropathic pain. The mechanism is obscure but the close relation to return of muscle activity suggests some reintegration of the deep afferent pathway. Anand and his colleagues have carried out extensive investigations in human nerve tissue and these provide some understanding about the mechanisms underlying pain associated with regeneration. In one study neurones from the dorsal root ganglion, which had been avulsed from the spinal cord, were cultured with a variety of neurotrophins including nerve growth factor (NGF), glial derived nerve factor (GDNF) and neurotrophin 3 (NT3) (Anand et al. 2006). The neurotrophins induced an increase in cell size and an increase in the proportion of cells exhibiting the receptor TRPV1, characteristic of nociceptor fibres. TRPV1 is the receptor for capsaicin, a potent nociceptor, and is expressed in DRG neurones, in painful neuromas and in the nerves of hypersensitive skin. The increase in this receptor was most marked in the larger cell bodies. Neurotrophin production is increased after nerve injury, indeed it is essential for the survival of the cell body and the regenerating axon. This finding provides one possible explanation for the mechanical sensitivity, at times so severe as to merit the term mechanical allodynia, which so often disturbs sensory recovery (Fig. 4.28). Durrenberger et al. (2004) studied the production of prostanoids, which are potent chemical mediators of inflammation

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Fig. 4.26  A 26 year old woman developed back pain radiating to the left foot and an ankle a sprain whilst training for a run. Over a few weeks she developed allodynia to touch, changes in colour and sweating and an abnormal foot posture. Clinical examination and quantitative sensory testing revealed a mechanical allodynia, elevated cold threshold and reduced heat pain threshold over the affected limb. Below knee amputation was performed. Examples of various nerve markers in the skin of the

calf close to the ankle. (a) Preserved sub-epithelial nerve fibres stained with the marker PGP9.5 (arrowed) x 40. (b) Unusually dense PGP9.5 fibres around blood vessels in the skin (arrowed) x 40. (c) Increased intra-epithelial transient receptor potential TRPV1 (heat receptor) fibres (arrowed) x 40. (d) A few sub-epithelial TRPM8 (cool receptor) fibres, (arrowed) x 40 (Courtesy of Professor Praveen Anand).

associated with nerve injury, in the human and the rat. Prostanoids sensitise nerve terminals. The enzymes responsible for prostanoid production are the cyclooxygenases (Cox-1 and Cox-2). The immunoreactivity for Cox 2 increased in cells resembling macrophages especially in the nerve proximal to the injury. The number of cells labeled for the enzyme reached a peak at between 4 or 6 weeks after injury. Anand et al. (2008) studied cannabinoid receptors in human nerves and neurones cultured from avulsed dorsal root ganglia. The cannabinoid receptor 2 (CB2) inhibits nociception and reduces pain, possibly by inhibiting inflammatory cell action or by inducing the release of the endogenous opiate b endorphine and it does this without inducing effects on the central nervous system which are associated with activation of a cannabinoid

receptor 1 (CB1). It was shown that agonists to CB2 block the action of capsaicin by impeding the activation of inward cation currents and preventing the increase in intracytoplasmic Ca++. Anand and her colleagues concluded that: “CB2 receptor agonists functionally inhibited nociceptive signaling in human primary sensory neurones.” Studies of the sodium channels Nav1.9 and Nav1.8 by Yiangou et  al. (2000) provides some understanding of the phenomenon of the “irritable” healing nerve and of the painful quality sometimes seen with Tinel’s sign. The channel Nav1.8 accumulated at the site of the injury in the proximal part of the nerve. One form of the channel Nav1.9 was not expressed at all in the infant nerves. Whilst much more needs to be done to explain the mechanisms underlying neuropathic pain and also the pain

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Fig. 4.27  Further examples of skin staining with various nerve markers in the patient illustrated in Fig.  4.26. (a) Sub-epithelial TRPM8 (cool and menthol receptor) fibres (arrowed) x 40. (b) PGP9.5 ­(structural marker) staining of injured nerve showing ovoid typical of Wallerian

degeneration. (c) Increased intra-epithelial (arrowed) and sub-epithelial TRPV1 (heat and capcaisin receptor) fibres x 40. (d) Basal keratinocytes (arrow head) and sub-epithelial NGF immunoreactive fibres (arrowed) x 40 (Courtesy of Professor Praveen Anand).

of regeneration these investigations of the cellular and molecular level in human tissue undoubtedly opens important lines of enquiry.

central nervous system. Although as long ago as 1907 Kilvington demonstrated the ability of the axons of the anterior horn cells to regenerate, and Tower (1943) showed the same, the matter was not systematically pursued. The latter indeed stated that the object of her work was “to prove unfounded the prevailing assumption that ventral nerve roots cannot regenerate if avulsed from the spinal cord.” She did just that in experiments on cats. Freeman (1952) used plasma clot suture for intradural transplantation of anterior spinal nerve roots in immature male guinea baboons. He reported functional restoration of a spinal reflex pattern of activity, and drew the conclusion that regeneration had occurred. Ochs and Barnes (1969) showed regeneration of ventral root fibres into dorsal roots in the cat, as shown by axoplasmic flow of radio-labeled leucine. Sanjuanbenito et al. (1976) demonstrated axonal regeneration in the ventral roots of the cat.

4.4 Regeneration after Intradural Injury The intradural, preganglionic lesions of the brachial plexus and to a lesser extent the similar lesions of the lumbosacral plexus have to be discussed separately in the matter of regeneration. It has for some time been clear that repair of such lesions offered the best chance of restoration of function and avoidance of pain, but the formidable technical difficulties of this have for years deterred most aspirants. There was, in addition, the discouraging thought that even if repair could be achieved, success required regeneration in the

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Fig. 4.28  Small to medium sized neuronal cell bodies and nerve fibres from a human dorsal root ganglion 3 weeks after avulsion immunostained with antibody to TRPV1 (heat and capsaicin receptor, black). The cell bodies of large diameter neurones are weakly stained. x 40 (Courtesy of Professor Praveen Anand).

The demonstration of Nathaniel and Nathaniel (1973) that in adult rats the dorsal root fibres could regenerate into the spinal cord after crushing seemed to indicate that the proximal limb of the axon of the sensory cell could make its way into the substantia gelatinosa and posterior funiculi. Bonney and Jamieson (1979) achieved reattachment of dorsal roots in the case of a man with a severe traction lesion of the brachial plexus. That was followed by recovery of proximal muscle function. Then Jamieson and Eames (1980) studied in adult dogs the regeneration of motor and sensory axons after avulsion and reimplantation. They found that, whereas there was significant regeneration of motor axons across the zone of repair, there was no regeneration of sensory axons. It appeared that whereas the motor axons behaved as part of the peripheral nervous system, the central process of the axon of the sensory cell behaved as part of the central system. Regeneration through the ventral root. Carlstedt and his colleagues have taken the matter far forward in extensive experimental studies which confirmed the reinnervation of skeletal muscle after ventral root implantation into the spinal cord. It was not even necessary to re-implant the roots along the anterolateral sulcus; sub-pial implantation near the sulcus was all that was necessary. This far reaching work is outlined by Carlstedt (1991, 2007d). Carlstedt et  al. (1995) reported the results of repair in man, of one root by direct implantation and of another by an intervening graft. There was secure evidence of functional reinnervation (Fig. 4.29). Regeneration through the dorsal root. The difference in behaviour of the nerve fibres within the dorsal and the ventral roots has been extensively studied by Carlstedt and his colleagues. Avulsion of the dorsal root causes proliferation of the asytrocytes which form a glial scar: “the astrocyte

Fig. 4.29  A horse radish peroxidase (HRP) filled motor neurone regenerated into an avulsed and implanted ventral root. (Above) Scale bar 20 mm. (Below). Scale bar 200 mm (Courtesy of Thomas Carlstedt).

barrier, developed as a response to nerve fibre degeneration, is most effective in preventing regeneration” (Carlstedt 1997, Carlstedt 2007d). However regeneration is possible in the immature animal before the establishment of the astrocyte population (Carlstedt 1988). It became clear that regeneration is enhanced if the transitional zone is bypassed by implanting the dorsal root directly into the spinal cord. This is followed by a substantial outgrowth of axons of the dorsal horn neurones to the injured dorsal root. Outgrowth from the secondary sensory neurones in the dorsal horn is further enhanced by excision of the dorsal root ganglion (Carlstedt 1997). Other methods have been used to enhance dorsal root fibre regeneration including glial cell transplants (Kliot et al. 1990), inflicting a preliminary or conditioning lesioning of the nerve before the implantation (Chong et al. 1999), and by transplanting olfactory ensheathing cells (Ramon-Cueto and Nieto-Sampedro 1994). Carlstedt and his colleagues applied olfactory ensheathing cells to reattached dorsal roots: the interposition enabled a “bridging channel” between the Schwann cells and the atrocytes, that is, between the peripheral and the central nervous systems (Li et al. 2004) (Fig. 4.30).

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avulsion of the ventral root. Nor can it, any longer, be a matter of doubt that this regeneration is capable of restoring useful function within the upper limb.

4.5 Recovery of Function after Nerve Repair a rule that a biologist, at any rate, finds useful is to suspect both those who lay down that results must be quantitative, and those who deny that they can be, but particularly to suspect the latter. (Young 1993)

Fig. 4.30  Regeneration through a reimplanted dorsal root. Olfactory ensheathing cells (green) in the proximal part of the dorsal root. Red stained regenerating nerve fibres passing between the root and the spinal cord. Original magnification x 180. Courtesy of Thomas Carlstedt.

Avulsion of the roots has a devastating effect on cells within the dorsal and ventral horns. It seems that the motor neurones can be rescued by reconnection with the periphery. Bergerot et  al. (2004) combined reimplantation with intrathecal delivery of glial derived neurotrophic factor (GDNF), and the intraperitoneal injection of a neuroprotective agent, riluzole. The population of the anterior horn neurones was maintained at 80% of the contra lateral side. Hart et  al. (2004) showed that dorsal horn neurones were protected by repair of the nerve within 24 h combined with the administration of acetyl-l-carbitine (ALCAR) or N-acetylcytseine (NAC). “As work in this field expands, it will be necessary to examine the effect of a solely motor innervation of muscles on their function. Doubtless, the search for sensory reinnervation will have to continue” (Birch and Bonney 1998a). Since that time we have confirmed the existence of myelinated afferent fibres in the ventral root of the human; their role awaits study. It is difficult to explain the level of function that has been seen in some successful cases after reimplantation without some elements of recovery of the muscle afferent pathway. In one case, which was demonstrated at the 7th International Brachial Plexus Meeting in London in 2008 the restoration of the biceps tendon reflex was demonstrated in a man who had undergone reimplantation of the ventral root of C6 six years previously. There can be no doubt that the motor neurones in the anterior horn are capable of regenerating new axons through the scar caused by

In clinical practice, most injuries of nerves short of transection inflict damage of all three grades of severity. The quality of reinnervation and hence of recovery depends first on the extent of damage causing degeneration and in particular loss of continuity of the basal lamina. A nerve fibre recovers completely after conduction block (neurapraxia), so long as the causative factor ceases to operate. Since this recovery does not have to be determined by axonal regrowth, it occurs over minutes, hours, days, weeks or – rarely– months. A nerve fibre will regenerate to its correct target after axonotomy so long as the basal lamina is preserved and the causative factor is removed. But recovery will take as long as it takes for the axon to re-innervate its target. Thus, recovery is the rule after “axonotmesis.” A nerve fibre will only regenerate to its correct target after axonotomy with interruption of the basal lamina if it is correctly directed to its target field or is drawn there by the operation of growth factors and other guiding mechanisms. Thus, in the case of individual nerves when the promptitude and quality of primary treatment is equal, the quality of recovery will depend on (1) the nature of the lesion: (2) the incidence of axonotomy: (3) the incidence of interruption of the basal lamina: (4) the obstacles posed to correct targeting by the complexity of functional representation in the nerve and the consequent liability to axon/target confusion; (5) the distance of the lesion from the target organs. We have already indicated that there are in effect no “purely motor” or “purely sensory” nerves, but the liability to axon/target confusion is plainly greater in a nerve such as the median with an extensive motor and cutaneous sensory distribution than it is in the posterior interosseous nerve, with no cutaneous sensory distribution. It is not doubted that full maturation of the regenerating nerve fibre depends on the establishment of the connection with its end-organ. The quality of recovery after neurotmesis and repair depends chiefly on the number of axons reaching their correct targets and on the later development and myelination of those axons. Factors influencing such re-innervation are: (1) the promptitude of repair; (2) the quality and viability of the opposed nerve ends; (3)The quality and accuracy of fascicular matching; (4) the degree of damage to the nerve ends

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during suture; (5) the length of gap after resection; (6) the number of channels provided by the interposed graft for the regenerating columns; (7)the extent of fibroblastic infiltration of the stumps and of the interposed grafts.

4.5.1 Methods The methods used for measurement of power, of cutaneous sensibility and sympathetic function are set out in the following Chap. 5. We have made only slender progress towards measuremt of recovery in the deep afferent pathways. The documents which have been developed to record progress are illustrated in Chaps. 5 and 10. Recall. Recovery of nerves after suture is a prolonged business. Omer (1998) described recovery of the small muscles of the hand 8 years after nerve repair and he pointed out: “these well documented late returns of neurological function to the intrinsic muscles of the hand are contrary to all results previously reported.” Case report. Primary repair of median and ulnar nerves was performed in a 22 year old staff nurse. Recovery was quite good, but marred by cold sensitivity, so that her result was considered only fair at 3 years after operation. She came to see us 7 years after operation to report a striking improvement during the previous few months. Over-sensitivity had disappeared, the final result for the ulnar nerve was considered excellent – and it was very good for the median. Case report. A 39  year old nursing sister wounded the digital nerves to little and ring fingers. Recovery was marred by cold sensitivity, and overreaction to light touch, until there was quite sudden resolution, over a few weeks, of these difficulties 6 years after operation. Zachary (1954) analyzed the duration of followup in patients with nerves repaired in the five Medical Research Council Nerve Injury Centres. More than 70% of them were seen at 60 months. Most of the failed repairs of the radial nerve were subsequently treated by flexor to extensor muscle transfer and after excluding these the rate of recall at 5 years was close to 80%. It has always been difficult to match this in civilian practice, indeed, clinicians, now, may find it impossible to do so as they find themselves working in an over politicized, management led and target driven health service. We must do what we can. Adequate assessment of outcome after severe injuries to the brachial and lumbosacral plexus in the adult requires at least 5 years of study. In some patients even this is inadequate (Chap. 9). The length of the follow up must be longer still in children with birth lesions of the brachial plexus (BLBP) or in those with severe injuries to the main nerves of the lower limb because of the ever present risk of secondary deformity from muscular imbalance or impaired

Surgical Disorders of the Peripheral Nerves

growth and because of the high incidence of posterior dislocation at the shoulder in BLPP. As it is our follow up is adequate in 1,060 repairs of closed traction lesion of the supraclavicular brachial plexus in the adult, in 1,128 (250 repairs) cases of BLPP and in around 1,800 repairs of main nerves. The results are related in later chapters. Grading of results. The results for nerves as a whole are graded by systems based on those developed by Seddon (1975e) which were drawn from those used in the five Specialist Nerve Injury Units (Zachary 1954). In some nerves muscular function is a good deal more important than recovery of sensation and for the circumflex, musculocutaneous, radial, femoral and common peroneal nerves, little significance is attributed to return of cutaneous sensation except when recovery is complicated by significant pain when the result is considered poor. Recovery of sensation has been given equal importance to muscle function in describing results of repairs of median and ulnar nerves and of the tibial division of the sciatic nerve. One could argue that sensibility is the most important function of the median and tibial nerves. Three grades are used (Birch, Bonney 1998): 1. Good, which means that recovery of function is substantial, that it enables the patient to use the part and to lead a normal life without difficulty and that they are not troubled by pain or over reaction. 2. Fair, implies recovery of function which is useful but which falls far short of normal. The patient is sufficiently aware of the hand or the foot that they do not damage it. Muscle power of MRC grade 2 or 3 restores some balance across a joint and it may be possible to supplement this with the appropriate muscle transfer to enhance, for example, flexion of the elbow or extension of the wrist. 3. Poor, means no or insignificant recovery and this grade is used in all cases with persisting spontaneous neuropathic pain, hypersensitivity or over reaction. The criteria used for grading results in individual nerves are set out in Chap 8. All systems of measurement have their defects and it seems the more closely one looks at the result of a nerve repair the more defects are revealed. Birch and Raji (1991) and Kline and Hudson (1995) introduced an “excellent” result, a result which we have given to a small number of repairs of the median and ulnar nerves nerve in the forearm and to some cases of repair of the spinal accessory nerve. The outcome is set out according to the cause of injury: the “tidy” wound from knife, glass or scalpel; the “untidy” wound from axes, saw, penetrating missile, open fracture or dislocation or burn; and the closed traction lesion. The effects of associated arterial injury are severe: such cases are considered separately in each of the three main groups. This reflects our view that the two factors of overwhelming significance on outcome are first, the violence of the injury and the extent

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of damage to the nerve and adjacent tissues and second, delay before repair. Other factors which are important in prognosis were clearly defined in the Medical Research Council Special Report Series No. 282 (1954), by Seddon (1975c), Sunderland (1978), and Kline and Hudson (1995), Kline and Hudson (2008, 2008) amongst others. We shall examine these.

4.6 Factors in Prognosis Age. Recovery of function after repair of a nerve in a child is, on the whole, better than in the adult, but it is not as good as has sometimes been assumed. This comes as no surprise if we take into consideration the increased vulnerability of the immature nervous system to axonotomy. Some of the most difficult problems in reconstruction follow failure of recovery of either of the divisions of the sciatic nerve in the growing child. The unpredictability and the limitations of outcome after repair of the plexus in birth lesions are related in Chap. 10. The recovery of skeletal muscle and of sympathetic efferent function after injuries to the brachial or lumbosacral plexus in the growing child is generally inferior to that seen following urgent repair in adults. There is often severe shortening of the limb and atrophy of the hand or foot. On the other hand the recovery of cutaneous sensation in the infant or child is often remarkably good. The results after repair of digital nerves provides one example of the difference between the adult and the child (Table 4.1). Goldie et  al. (1992) made a detailed study of 27 adult patients. Thirty nerves were repaired, all but one by primary repair using sutures for we did not have access to fibrin clot glue at that time. The digital artery was repaired if that had been damaged. Examination for sensation was thorough and it was helped by using weighted pins designed for us by Professor Ruth Bowden. The results were surprisingly disappointing, an indication perhaps that the more scrupulously that one examines outcome from a nerve repair the more one will find wrong. Thirty-seven per cent of fingers regained normal two-point discrimination but

only 27% of patients graded their overall result as “excellent” and 40% complained of persistent hyperaesthesia up to 2 years. Goldie and Coates concluded: “following repair of the divided digital nerve, normal sensation will never be regained. Hyperaesthesia may be present for months or years but will ultimately resolve. The final result will take two or three years to achieve.” Fortunately results do seem to be a good deal better in children. It does seem odd that recovery of sensation after a well executed primary repair of the median nerve at the wrist is regularly better than that from repair of digital nerves more distally. It is only fair to add that a number of patients reported striking improvement in sensation, with sudden loss of cold sensitivity and hypersensitivity to touch, some years after repair. There seems a trend towards neglecting nerve injuries in patients of a certain age, a policy for which we find a remarkable absence of supporting evidence. Indeed, the changes in the peripheral nerves with aging (Chap. 2) suggest that the older patient may in fact be more likely to develop severe pain after injury to a nerve. Some striking results have been seen after repair of the brachial plexus in patients aged over 65 years. In several of these the relief of pain and with it the improvement in the patient’s mental well being, were remarkable. It may be administratively convenient to ignore the elderly but they are, after all, still human beings and the risk of losing independence calls for a far more rational and vigorous approach than is often, too often, seen. Level of injury. This is undoubtedly important for the median, ulnar and radial nerves but it seems to be much less important for the sciatic nerve and its divisions. Only rarely is extension of the digits regained after injuries to the brachial plexus, the posterior cord or the radial nerve in the axilla. Urgent repair of lesions of C5 and C6 is often followed by recovery to a level far higher than that seen after repair of combined lesions of the circumflex, the suprascapular and the musculocutaneous nerves. There seems little doubt, however, that repair of the recurrent motor branch of the median nerve at the wrist, of the posterior interosseous nerve and of the deep branch of the ulnar nerve is followed by a return of function which is scarcely ever seen after high repairs of main nerves. On the other hand lesions of the distal

Table 4.1  Recovery of sensation after repair of 129 digital nerves. Grade Adults Repair within 48 h of injury Repair 2 weeks or more after injury Excellent

1

0

Children (aged 1 years or less) Repair at varying intervals after injury 17

18

Good

33

9

8

50

Fair

24

11

2

37

Poor

16

74 17 digital arteries repaired at primary operation. 20 flexor tendons repaired at primary operation.

8

0

24

28

27

129

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branches of such cutaneous nerves as the sural, the medial cutaneous of forearm and the superficial radial nerve have deservedly gained an ill reputation. The nerve. Whilst there is no such thing as a purely “motor” or “sensory” nerve in the peripheral nervous system, it appears that recovery after repair of nerves which have no cutaneous distribution is generally better than after repair of main nerves. The spinal accessory and the nerve to serratus anterior generally recover well after repair. The suprascapular fares better than the circumflex. It is more than 50 years since Zachary established that recovery for the common peroneal nerve is far inferior than for the tibial nerve, an observation which has been repeatedly confirmed. The blood supply to the most proximal segment of the radial nerve and to the common peroneal nerve is rather poor, so that transection of these nerves is likely to enhance ischaemic changes in the distal segment.

4.7 Severity of Injury Useful recovery in function cannot be expected if the fundamental principles of treatment of a wound are neglected. Arteries must be repaired, the tissues of the limb must be perfused, the skeleton must be stabilized and repaired nerves and vessels must be covered by full thickness skin. Michael Glasby and his colleagues used the freeze-thawed muscle graft (FTMG) in a series of experiments which showed that recovery is worsened by delay, by arterial injury, by fractures, by cavitation and by haematoma (Fullerton et al. 1998, Glasby et al. 1997, Glasby et al. (1998).

Surgical Disorders of the Peripheral Nerves

inevitable.” Zachary and Holmes (1946) compared 55 cases of primary sutures of nerves referred to the Peripheral Nerve Injury Centre, at the Wingfield-Morris Hospital, Oxford, during the years 1940–1944 with 36 “early” secondary sutures. The results of secondary suture were distinctly better. The primary repair was resected and the nerve re-sutured in 16 patients. Histological examination of the resected material revealed a number of causes for the failure of the first operation: poor matching of the proximal and distal stumps; coarse suture material lodged between the stumps; separation of the stumps; and dense scar between or within the stumps. Zachary and Holmes concluded that “Formal nerve suture should be undertaken at the earliest moment when it is possible to recognise the extent of damage to the nerve, excise the injured segment, and bring together the mobilised nerve ends without the prospect of undue post operative tension.” These are painful but important findings: the lesson is that the results of operating on peripheral nerves depend to an extent hardly matched in any other branch of surgery on the skill of the surgeon and the quality of the technique. The clinician must always bear in mind that the sooner the distal segment is connected to the cell body and proximal segment the better the result will be. The quality of treatment of the wound at first operation and the timing of repair of the nerves are factors within the control of clinicians. The last 20 years has seen extensive laboratory work which confirms the view, long held by many clinicians, that the central nervous system suffers after interruption of a peripheral nerve. The rapidity and the severity of that response to violent proximal nerve injury is the over arching biological imperative which must guide action.

4.8 Delay References Sherren (1908) examined 50 cases of primary suture performed at the London Hospital. Pain sensibility recovered before touch; tactile localisation continued to improve for more than 2 years. Recovery of power was rather slower. There was no recovery in only one patient, whose wound had become infected. Sherren recommended primary suture “because the prognosis after secondary suture is more unfavourable.” Platt and Bristow (1924) reviewed the late results of nerve injuries treated in the First World War, and noted the “extreme perfection attained after so-called primary suture,” acknowledging that the more severe gunshot wounds of nerves were treated by secondary suture. Platt (1937) wrote “in primary sutures performed under ideal conditions, complete recovery of motor power and recovery of protopathic sensibility at least, is to be expected.....however, in more extensive wounds with widespread bruising and multiple tendon injuries, and in wounds in which infection had already secured a hold, partial or complete failure after primary suture is almost

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141 Brushart TM, Mather V, Sood R, Koschorke G-M (1995) Dispersion of regenerating axons across enclosed neural gaps. J Hand Surg Am 20:557–564 Bunnell S, Boyes JH (1939) Nerve grafts. Am J Surg 44:64–75 Bunting S, Di Silvio L, Deb S, Hall S (2005) Bioresorbable glass fibres facilitate peripheral nerve regeneration. J Hand Surg Br 30: 242–247 Cabaud HE, Rodky G, Nemeth TJ (1982) Progressive ultrastructural changes after peripheral nerve transection and repair. J Hand Surg Am 7:353–365 Caddick J, Kingham PJ, Gardiner NJ, Wyburg M, Terenghi G (2006) Phenotypic and functional characteristics of mesenchymal stem cells differentiated along a Schwann cell lineage. Glia 54:840–849 Cajal SRY (1928a) A regenerative process of the central stump. In: Degeneration and regeneration of the nervous system. Oxford University Press, London, Chapter 7, pp 141–166 (Trans ed: May RM) Cajal SRY (1928b) Late conditions shown by the nerve sprouts of the central stump and of the scar. In: Degeneration and regeneration of the nervous system. Oxford University Press, London, Chapter 9, pp 198–222 (Trans ed: May RM) Cajal SRY (1928c) Experiments dealing with the transplantation of nerves or their products, designed to prove especially an attractive or neurotropic action on nerve sprouts. In: Degeneration and regeneration of the nervous system. Oxford University Press, London, Chapter 15, pp 329–361 (Trans ed: May RM) Calder JS, Green CJ (1996) Nerve-muscle sandwich grafts: the importance of Schwann cells in peripheral nerve regeneration through muscle basal lamina conduits. J Hand Surg Br 20:423–428 Camp SJ, Allen D (2008) Cocontraction of swallowing musculature and trapezius following basal skull fracture. Injury Extra 39:95–97 Carlstedt T (1988) Reinnervation of the mammalian spinal cord after neonatal dorsal root crush. J Neurocytol 17:335–350 Carlstedt T (1991) Experimental studies on surgical treatment of avulsed spinal nerve roots in brachial plexus injury. J Hand Surg Br 16:477–482 Carlstedt T (1997) Nerve fibre regeneration across the peripheral-central transitional zone. J Anat 190:51–56 Carlstedt T (2007a) End to side or termino-lateral neurorrhaphy. In: Central nerve plexus injury. Imperial College Press, London, pp 70–71 Carlstedt T (2007b) Outcome of nerve transfer. In: Central nerve plexus injury. Imperial College Press, London, pp 71–74 Carlstedt T (2007c) Cocontraction. In: Central nerve plexus injury. Imperial College Press, London, pp 144–150 Carlstedt T (2007d) Basic science of experimental root injuries. In: Central nerve plexus injury, Chap 6. Imperial College Press, London, pp 78–111 Carlstedt T, Crane P, Hallin RG, Noren G (1995) Return of function after spinal cord implantation of avulsed spinal nerve roots. Lancet 346:1323–1325 Chen L, Gu YD (1994) An experimental study of contralateral C7 root transfer with vascularised nerve grafting to treat brachial plexus root avulsion. J Hand Surg Br 19:60–66 Chong MS, Woolf CJ, Haque NS, Anderson PM (1999) Axonal regeneration from injured dorsal roots into the spinal cord of adult rats. J Comp Neurol 410:42–54 Collier J (1940) Facial paralysis and its operative treatment. Lancet 1:91 Dellon AL, Munger BL (1983) Correlation of histology and sensibility after nerve repair. J Hand Surg Am 8:871–875 Durrenberger PF, Facer P, Gray RA, Chessell IP, Naylor A, Bountra C, Banati RB, Birch R, Anand P (2004) Cyclooxygenase – 2 (Cox-2) in injured human nerve and a rat model of nerve injury. J Peripher Nerv Syst 9:15–24 Dyck PJ, Thomas PK (2005) Peripheral neuropathy, 4th edn. Elsevier, Philadelphia

142 Dyck PJ, Dyck PJB, Engelstad J (2005) Pathological alterations of nerves. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier, Philadelphia, pp 733–829 Foerster O (1929) Die therapie der Schussverletzungen der peripheren nerven, resultate der plexus operationen. In: Foerster BO (ed) Handbuch der neurologie von lewandowski, vol 2. Springer, Berlin, pp 1676–1691 Forsmann J (1900) Zur kenntnis des neurotropismus. Ziegler’s Beiträge Zur Pathol Anat 27:407 Freeman LW (1952) Observations on spinal nerve root transplantation in the male guinea baboon. Ann Surg 136:206–210 Fullerton AC, Glasby MA, Lawson GM (1998) Immediate and delayed nerve repair using freeze-thawed muscle autografts in complex nerve injuries. Associated long bone fracture. J Hand Surg Br 23:360–364 Fullerton AC, Myles LM, Lenihan DV, Hems TEJ, Glasb M (2001) Obstetric brachial plexus palsy: a comparison of the degree of recovery after repair of 16 ventral root avulsions in newborn and adult sheep. Br J Plas Surg 54:697–704 Glasby MA, Gschmeissner SE, Huang CL, De Souza BA (1986) Degenerated muscle grafts used for peripheral nerve repair in primates. J Hand Surg Br 11:347–351 Glasby MA, Fullerton AC, Lawson GM (1997) Immediate and delayed nerve repair using freeze-thawed muscle autografts in complex nerve injuries. Cavitation, fibrosis and haematoma. J Hand Surg Br 22:479–485 Glasby MA, Fullerton AC, Lawson GM (1998) Immediate and delayed nerve repair using freeze-thawed muscle autografts in complex nerve injuries Associated arterial injury. J Hand Surg Br 23(3):354–359 Goldie BS, Coates CJ, Birch R (1992) The long term results of digital nerve repair in no man’s land. J Hand Surg Br 12:75–77 Gore RV (1978) A new method of nerve repair: repair of a lesion of the radial nerve with a branch to the triceps muscle. Br J Surg 65: 352–353 Griffin JW, Hoffman PN (1993) Degeneration and regeneration in the peripheral nervous system. In: Dyck PJ, Thomas PK, Lambert EH, Bunge R (eds) Peripheral neuropathy, 3rd edn. WB Saunders, Philadelphia, Chapter 22, pp 361–376 Gu YD, Zhang GM, Chen DS, Yan JG, Cheng XM, Chen L (1992) Seventh cervical nerve root transfer from the contralateral healthy side for treatment of brachial plexus root avulsion. J Hand Surg Br 17:518–521 Gutmann E, Sanders FK (1942) Functional recovery following nerve grafts and other types of nerve bridges. Brain 65:373–408 Gutmann E, Young JZ (1944) The reinnervation of muscle after various periods of atrophy. J Anat 78:15–43 Hall S (1997) Axonal regeneration through acellular muscle grafts. J Anat 190:57–71 Hall S (2005a) Mechanisms of repair after traumatic injury. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier Saunders, Philadelphia, Chapter 58, pp 1403–1434 Hall S (2005b) The response to injury in the peripheral nervous system. J Bone Joint Surg Br 87:1309–1319 Hall SM (2009) Biomaterials for the repair of peripheral nerves. In: di Silvio L (ed) Cellular response to biomaterials, Chap. 11. Woodhead, Cambridge, pp 252–290 Hallin R, Carlstedt T, Nilsson-Remahl IA, Risling M (1999) Spinal cord implantation of avulsed ventral roots in primates: correlation between restored motor function and morphology. Exp Brain Res 124(3):304–310 Harris W, Low VW (1903) On the importance of accurate muscular analysis in lesions of the brachial plexus and the treatment of Erb’s palsy and infantile paralysis of the upper extremity by cross-union of nerve roots. Br Med J 2:1035–1038 Hart AM, Terenghi G, Kellerth JO, Wiberg M (2004) Sensory neuroprotection, mitochondrial preservation and therapeutic potential of N-acetyl-cysteine after nerve injury. Neuroscience 125:91–101

Surgical Disorders of the Peripheral Nerves Healy C, Lequesne PM, Lynn B (1996) Collateral sprouting of cutaneous nerves in man. Brain 119:2063–2072 Highet WB, Sanders FK (1943) The effects of stretching nerves after suture. Br J Surg 30:355–369 Höke A, Redett R, Hameed H, Jari R, Zhou C, LI ZB, Griffin JW, Brushart TM (2006) Schwann cells express motor and sensory phenotypes that regulate axon regeneration. J Neurosci 26:9646–9655 Holmes W, Young JZ (1942) Nerve regeneration after immediate and delayed suture. J Anat 77:63–96 Htut M, Misra P, Anand P, Birch R, Carlstedt T (2006) Pain phenomena and sensory recovery following brachial plexus avulsion injury and surgical repair. J Hand Surg Br 31:596–605 Irwin MS, Abhilash J, Anand P, Manchahal J (2006) Free innervated sole of foot transfer for contralateral lower limb salvage. Plast Recon Surg 118:93e–97e Jabaley ME, Burns JE, Orcutt BS, Bryant WM (1976) Comparison of histologic and functional recovery after peripheral nerve transection and repair. J Hand Surg 1:119–130 Jamieson A, Eames RA (1980) Reimplantation of avulsed brachial plexus roots: an experimental study in dogs. Int J Microsurg 2:75–80 Joyce JL (1919) Nerve suture. Br J Surg 6:418 Kanamura A, Suzuki S, Sibuya M, Homma I, Sai K, Hara T (1993) Sensory reinnervation of muscle receptor in human. Neuroscience 161:27–29 Graham K (1904) On somepoints in the early development of motor nerve trunks, etc. in lepidosiren. Trans Roy Soc Edin 41:121–128 Kettle S (2003) The use of end to side repair of peripheral nerves for neurotization after loss of nerve tissue in a large tissue model. MD Thesis. University of Edinburgh Kilvington B (1907) An investigation on the regeneration of nerves, with regard to surgical treatment of certain paralysies. Br Med J 1:988–990 Kline DG, Hudson AR (1995) Nerve injuries. WB Saunders, Philadelphia Kline DG, Hudson AR (2008) Nerve injuries, 2nd edn. Saunders Elsevier, Philadelphia (with Kim DH, Midha R, Murovic JA, Spinner RJ) Kliot M, Smith GM, Siegal JD, Silver J (1990) Astrocyte-polymer implants promote regeneration of dorsal root fibres into the mammalian spinal cord. Exp Neurol 109:57–69 Kotani PT, Matsuda H, Suzuki T (1972) Trial surgical procedures of nerve transfers to avulsion injuries of the plexus brachialis. Excerpta Medica International Congress Series Number 291 (1973). Proceedings of the 12th Congress of S.I.C.O.T. Tel Aviv, October 9–12 1972, pp 348–351 Lago N, Ceballos D, Rodriguez FJ, Stieglitz T, Navarro X (2007) Effects of motor and sensory nerve transplants on amount and specificity of sciatic nerve regeneration. J Neurosci Res 85:2800–2812 Lang EM, Borges J, Carlstedt T (2004) Surgical treatment of lumbosacral plexus injuries. J Neurosurg Spine 1:64–71 Larsen M, Habermann TM, Bishop AT, Shin AY, Spinner RJ (2007) Epstein-Barr virus infection as a complication of transplantation of a nerve allograft from a living related donor. J Neurosurg 106: 924–928 Li H, Wigley C, Hall SM (1998) Chronically denervated rat Schwann cells respond to Ggf in vitro. Glia 21:1–14 Li Y, Carlstedt T, Berthold CH, Raisman G (2004) Interaction of transplanted olfactory ensheathing cells and host astrocyte processes provides a bridge for axons to regenerate across dorsal root entry zone. Exp Neurol 188:300–308 Lundborg G (1991) Neurotropism, frozen muscle grafts and other conduits. J Hand Surg Br 16:473–476 Lundborg G (2003) Nerve injury and repair. A challenge to the plastic brain. The Bunge Memorial Lecture. J Peripher Nerv Syst 8:209–226 Lundborg G (2004a) The growth cone. In: Nerve injury and repair, 2nd edn. Elsevier/Churchill Livingstone, Philadelphia, p 13

Regeneration and Recovery Lundborg G, Dahlin LB, Danielsen N, Nachemson AK (1986) Tissue specificity in nerve regeneration. Scand J Plast Reconstr Surg 6:265–281 Lundborg G, Dahlin L, Dohi D, Kanje M, Terad N (1997) A new type of “bioartificial” nerve graft for bridging extended defects in nerves. J Hand Surg Br 22:299–303 MacCarty CS (1951) Two-stage autograft for repair of extensive damage to sciatic nerve. J Neurosurg 8:319 MacKinnon SE (1996) Nerve allotransplantation following severe tibial nerve injury. J Neurosurg 84:671–676 MacKinnon S, Dellon L, O’brian J (1986a) Changes in nerve fibre numbers distal to a nerve repair in the rat sciatic model. Muscle Nerve 14:1116–1122 MacKinnon SE, Dellon AL, Lundborg G, Hudson AR, Hunter D (1986b) A study of neurotropism in a primate model. J Hand Surg Am 11:888–894 Malessy MJ, Thomeer RT, Van Dijk JG (1998) Changing central nervous system control following intercostal nerve transfer. J Neurosurg 89:568–574 Malessy MJ, Bakker D, Dekker AJ, Van Dijk JG, Thomeer RT (2003) Functional magnetic resonance imaging and control over the biceps muscle after intercostal-musculocutaneous nerve transfer. J Neurosurg 98:261–268 Mano Y, Nakamuro T, Tamara R, Takayang T, Kawanishi K, Tamai S, Mayer RF (1995) Central Motor re-organisation after anastamosis of the musculocutaneous and intercostal nerves following clinical root avulsion. Ann Neurol 38:15–20 Mayo-Robson AW (1917) Nerve grafting as a means of restoring function in limbs paralysed by gunshot or other injuries. Br Med J 1:117–118 Medical Research Council Special Report Series No. 282. (1954). Peripheral nerve injuries. Seddon HJ (ed). HSMO London. Millesi H (1973) Microsurgery of peripheral nerves. Hand 5:157–160 Mirsky R, Jessen KR (2005) Molecular signalling in Schwann cell development. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier Saunders, Philadelphia, Chapter 16, pp 341–376 Moberg E (1958) Objective methods for determining the functional value of sensibility in the hand. J Bone Joint Surg Br 40:454–476 Morris JH, Hudson AH, Weddell G (1972a) A study of degeneration and regeneration in the divided rat sciatic nerve based on electron microscopy ii the development of the “regenerating unit”. Zeitschrift für Zellforschumg 124:103–130 Morris JH, Hudson AH, Weddell G (1972b) Changes in the axons of the proximal stump. Zeitschrift für Zellforschumg 124:131–164 Morris JH, Hudson AH, Weddell G (1972c) Changes in fascicular microtopography. The perineurium and endoneurial fibroblasts. Zeitschrift für Zellforschumg 124:165–203 Mott FW, Halliburton WD (1901) The chemistry of nerve-degeneration. Phil Trans R Soc Lond B 194:437–466 Myles LM, Gilmour JA, Glasby M (1992) Effects of different methods of peripheral nerve repair in the number and distribution of muscle afferent neurons in the rat dorsal root ganglion. J Neurosurg 77:457–462 Nagano A, Tsuyama N, Ochiai N, Hara T (1989) Direct nerve crossing with the intercostal nerve to treat avulsion injuries of the brachial plexus. J Hand Surg Am 14(6):980–985 Narakas AO (1988) Neurotization or nerve transfer in traumatic brachial plexus lesions. In: Tubiana R (ed) The hand III. WB Saunders, Philadelphia, Chapter 62, pp 656–683 Nathaniel EJM, Nathaniel DR (1973) Regeneration of dorsal root fibers into the adult rat spinal cord. Exp Neurol 40:333–350 Navarro X, Calvet S, Rodriguez FJ, Stieglitz T, Blau T, Buti M, Valderrama E, Meyer JU (1998) Stimulation and recording from regenerated peripheral nerves through polyimide sieve electrodes. J Peripher Nerv Syst 3:91–101 Nichols CM, Brenner MJ, Fox IK, Tung TH, Hunter DA, Rickman SR, MacKinnon SE (2004) Effects of motor versus sensory nerve grafts on peripheral nerve regeneration. Exp Neurol 190:347–355

143 Oberlin C, Beal D, Leechavengvongs S, Salon A, Dauge MC, Sarly JJ (1994) Nerve transfers to biceps muscle using part of ulnar nerve for C5-C6 avulsion of the brachial plexus: anatomical study and report of four cases. J Hand Surg Am 19:232–237 Ochs S, Barnes CD (1969) Regeneration of ventral root fibers into dorsal roots shown by axoplasmic flow. Brain Res 15:600–603 Omer GE (1998) Peripheral nerve injuries and gunshot wounds. In: Omer GE, Spinner M, Van Beek AL (eds) Peripheral nerve problems, 2nd edn. WB Saunders, Philadelphia, Chapter 41, pp 398–405 Őzkan T, Őzer K, Gülgőnen A (2001) Restoration of sensibility in irreparable ulnar and median nerve lesions with use of sensory nerve transfer: long-term follow up of 20 cases. J Hand Surg Am 26:44–51 Pereira JH, Palande DD, Narayanakumar TS, Subramian AS, Gschmeissner S, Wilkinson M (2008) Nerve repair of denatured muscle autografts promotes sustained sensory recovery in leprosy. J Bone Joint Surg Br 90:220–224 Platt H (1937) Discussion on injuries to peripheral nerves. Proc R Soc Med Lond 30:863 Platt H, Bristow WR (1924) The remote results of operations for injuries of the peripheral nerves. J Br J Surg 11:535–567 Ramon-Cueto A, Nieto-Sampedro M (1994) Regeneration into the spinal cord of transected dorsal root axons is promoted by ensheathing glial transplants. Exp Neurol 127:232–244 De Ruiter GCW, Spinner RJ, Yaszmenski MJ, Windebank AJ, Malessy MJA (2009) Nerve tubes for peripheral nerve repair. Neurosurg Clin North Am 20:91–106 Sai K, Kanamura A, Sibuya M, Homma I, Hara T (1996) Reconstruction of tonic vibration reflex in the biceps brachii reinnervated by transferred intercostals nerves in patients with brachial plexus injury. Neurosci Lett 206:1–4 Sanders FK (1942) The repair of large gaps in the peripheral nerves. Brain 65:281–337 Sanders FK, Young JZ (1946) The influence of peripheral connections on the diameter of regenerating nerve fibres. J Exper Biol 22:203–212 Sanjuanbenito L, Esteban A, Gonzalez-Martinez E (1976) Regeneration of the spinal ventral roots. Acta Neurochir 34:203–214 Schuind F, Van Holder C, Mouraux D, Robert CH, Meyer A, Saliva P, Vermeylen N, Abramowicz D (2006) The first Belgian hand transplantation – 37 months results. J Hand Surg Br 31:371–376 Scott JJ (1995) The functional recovery of muscle proprioception after peripheral nerve lesions. J Peripher Nerv Syst 1:19–27 Scott JJA (2005) The Golgi tendon organ. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy (in two volumes), 4th edn. Elsevier Saunders, Philadelphia, Chapter 7, pp 151–161 Seddon HJ (1947) The use of autogenous grafts for the repair of large gaps in peripheral nerves. Br J Surg 35:151–167 Seddon HJ (1954) Nerve grafting. In: Peripheral nerve injuries by the Nerve Injury Committee of the Medical Research Council MRC Special Report Series 282. Hmso, London, pp 402–403 Seddon HJ (1975a) Degeneration and regeneration. In: Surgical disorders of peripheral nerves, Chap. 2, 2nd edn. Churchill Livingstone, Edinburgh, pp 9–31 Seddon HJ (1975b) Repair and tension. In: Surgical disorders of peripheral nerves, 2nd edn. Churchill Livingstone, Edinburgh, pp 298–299 Seddon HJ (1975c) Nerve Grafting and kindred procedures. In: Surgical disorders of peripheral nerves, 2nd edn. Churchill Livingstone, Edinburgh, pp 287–302 Seddon HJ (1975d) Homografts. In: Surgical disorders of peripheral nerves, 2nd edn. Churchill Livingstone, Edinburgh, p 299 Seddon HJ (1975e) Results of repair of the nerves. In: Surgical disorders of peripheral nerves, 2nd edn. Churchill Livingstone, Edinburgh, pp 303–314 Seddon HJ, Young JZ, Holmes W (1942) The histological condition of a nerve autograft in man. Br J Surg 29:378–384 Sherren J (1906) Some points in the surgery of the peripheral nerves. Edin Med J 20:217–231

144 Sherren J (1908) Injuries of nerves and their treatment. James Nisbet, London Simpson SA, Young JZ (1945) Regeneration of fibre diameter after cross-unions of visceral and somatic nerves. J Anat 79:48 Songcharoen P, Wongtrakul S, Mahrisavariya B, Spinner RJ (2001) Hemi-contralateral C7 transfer to median nerve in the treatment of root avulsion brachial plexus injury. J Hand Surg Am 26:1058–1064 Sorbie C, Porter TL (1969) Reinnervation of paralysed muscles by direct motor nerve implantation: an experimental study in a dog. J Bone Joint Surg Br 51:156–164 Strange FGS (1947) An operation for pedicle nerve grafting. Br J Surg 34:423–425 Sunderland S (1978) Nerve and nerve injuries, 2nd edn. Churchill Livingstone, Edinburgh Terenghi G, Calder JS, Birch R, Hall SM (1998) A morphological study of Schwann cells and axonal regeneration in chronically transected human peripheral nerve. J Hand Surg Br 23:583–587 Thomas M, Stirratt A, Birch R, Glasby M (1994) Freeze thawed muscle grafting for painful cutaneous neuromas. J Bone Joint Surg Br 76:474–476 Tinel J (1917) Nerve wounds (Revised and edited by Joll CA). Ballière Tindall and Cox, London Tower SS (1943) Regenerative capacity of ventral roots after avulsion from the spinal cord. Arch Neurol Psychiatry 49:1–12 Trachtenburg JT, Thompson WJ (1996) Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factor. Nature 379:174 Trumble TE (1991) Overcoming defects in peripheral nerves. In: Gelberman RH (ed) Operative nerve repair and reconstruction. JB Lippincott, Philadelphia, Chapter 36, pp 507–524 Tsao JW, George EB, Griffin W (1999) Temperature modulation reveals three distinct stages of Wallerian degeneration. J Neurosci 19: 4718–4726 Tsuyama N, Hara T (1973) Intercostal nerve transfer in the treatment of brachial plexus injury of root-avulsion type. Proceedings of the

Surgical Disorders of the Peripheral Nerves S.I.C.O.T. Tel Aviv Oct. 9–12 1972. Excerpta Medical International Congress Series No. 291: 348–351 Tuttle H (1913) Exposure of the brachial plexus with nerve transplantation. JAMA 61:15–17 Vizoso AD, Young JZ (1948) Internode length and fibre diameter in developing and regenerating nerves. J Anat 82:110–134 Waikakul S, Orapin S, Vanadurongwan V (1999) Clinical results and contralateral C7 root neurotization to the median nerve in brachial plexus injuries with total root avulsions. J Hand Surg Br 24:556–560 Wallman L, Zhang Y, Laurell T, Danielson N (2001) The geometric design of micromachined silicon sieve electrodes influences functional nerve regeneration. Biomaterials 22:1187–1193 Witte H, Bradke F (2005) Guidance of axons to targets in development and in disease. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier Saunders, Philadelphia, Chapter 21, pp 447–481 Witzel C, Brushart T (2003) Morphology of peripheral axon regeneration. J Peripher Nerv Syst 8:75–76 Yiangou Y, Birch R, Sangeswaram L, Eglen R, Anand P (2000) Sns/ PN3 and SNS2/NaN sodium channel like immunoreactivity in human adult and neonate injuries of sensory nerves. FEBS Lett 467:249–252 Young JZ (1942) Functional repair of nervous tissue. Physiol Rev 22:318–374 Young JZ (1993) First evidence of axonal transport. In: DyckPJ TPK, Griffin JW, Low PA, Poduslo JF (eds) Peripheral neuropathy, 3rd edn. WB Saunders, Philadelphia, p 2 Zachary RB (1954) Results of nerve sutures. In: Seddon HJ (ed) Peripheral nerve injuries. Medical Research Council. Special report series No. 282, pp 354–387 Zachary RB, Holmes W (1946) Primary suture of nerves. Surg Gynaecol Obstet 82:632–651 Zhao Q, Drott J, Laurell T, Wallman L, Lundstrom K, Bjursten LM, Lundborg G, Montelius L, Danielson N (1997) Rat sciatic nerve regeneration through a micromachined silicone chip. Biomaterials 18:75–80

5

Clinical Aspects of Nerve Injury

Clinical aspects: acute injury; penetrating missile wounds; symptoms and signs; importance of recognition of differential affection of fibres of different sizes; recognition of level and depth of lesion; significance of Tinel’s sign; examination of sensibility; quantitative sensory testing; the motor pathways; examination of muscles; late signs of nerve injury; records; signs of regeneration; aids to diagnosis. “Few surgeons see their patients from the beginning to the end. One could well wish that there was no evil in this. But there is much of evil, and not least is the fact that the orthopaedic surgeons work has enormously increased” (Keogh 1917).

In the acute injury the object of the clinician must be to recognise the fact of injury as soon as possible after the event, and later to go on to determine the nerve or nerves affected, the level or levels of injury and the extent and depth of the lesion or lesions. That this is not always easy nor always appreciated is apparent to anyone who has been able to study the records of the medical defense organisations. The history is important: high velocity injury, compound fracture and wounding, accidental, criminal, surgical or all three, are likely to mean that there has been a serious lesion. The use of a knife, often enough in the hand of a surgeon, is an indication that a nerve is likely to have been partly or completely severed. Advice from witnesses or emergency paramedical staff is always valuable. Potentially life or limb threatening injuries complicate closed traction lesion of the supraclavicular brachial plexus in at least 20% of cases. Even more patients with injuries to the lumbo-sacral plexus are so threatened. The subclavian artery is ruptured in 10% of complete lesions of the brachial plexus and in as many as 30% of cases of violent traction injury of the infraclavicular portion of the brachial plexus. The incidence of arterial lesion is high after fracture dislocations of the shoulder and elbow, higher still after fracture dislocations of the knee. It is important always to search with diligence for occult injuries to the head, the spine, the chest, the abdomen and pelvis before embarking upon treatment of the nerve lesion, both at the first hospital but also after transfer to another Unit (Fig. 5.1). The site and nature of the wound or wounds must be observed. In closed injuries the presence of swelling and bruising may give some indication of severity (Novak and Baratz 2006). In all cases of limb injury the adequacy of perfusion as judged by the state of the pulses, by colour and by temperature must be observed. Indications of associated

fracture must be sought (Fig. 5.2). In cases of serious injury, special attention has to be given to the patient’s general condition as shown by colour, pulse, blood pressure, respiration and other indicators. We follow Rank et al. (1973) in distinguishing between “tidy” wounds as from a knife and “untidy” wounds, such as those seen in open fracture. Soft tissue damage is worse in the latter; nerves and vessels are often

Fig. 5.1  This motor cyclist struck his shoulder against a traffic bollard. There is bruising and swelling of the left shoulder, neck and upper arm. Total avulsion.

R. Birch, Surgical Disorders of the Peripheral Nerves, DOI: 10.1007/978-1-84882-108-8_5, © Springer-Verlag London Limited 2011

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Fig. 5.2  The Platt lesion. A 64 year old woman avulsed the fibular styloid standing up from a chair. The common peroneal nerve was ruptured.

Fig. 5.3  Bullet wound of divisions of the sciatic nerve in the thigh. The common peroneal nerve (above) was transected and repaired (neurotmesis). The tibial nerve (below, sling) recovered spontaneously (axonotmesis).

subjected to traction. In penetrating missile wounds it is important to distinguish between the shot gun, the hand gun or rifle and the fragment (Fig.  5.3–5.5). The immensely destructive effect of a close range shotgun injury is much more than that of wounds from more distant discharge. This fact was recognised by Stewart (Stewart and Birch 2001) who classed penetrating missile wounds of the brachial plexus into high energy transfer (HET) and massive energy

Fig. 5.4  Close range shot gun blast to the posterior triangle of the neck. There was rupture of the first part of the subclavian artery.

transfer (MET) injuries. Wounds from bomb fragments and shell splinters have some of the characteristics of shotgun injury, though on a larger scale and with a higher velocity. The International Committee of the Red Cross (ICRC) wound classification, described by Coupland (1993), has enhanced the understanding of the treatment of war wounds. Coupland writes “the surgical task presented by any wound

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147

Fig. 5.5  Penetrating missile wound. A military rifle bullet entered in the front of the shoulder, passed through the quadrilateral tunnel, destroying the circumflex nerve and posterior circumflex artery and exited posteriorly destroying the infraspinatus and much of the overlying skin.

depends on the wound severity i.e. the degree of tissue damage, and also the structure (s) that may have been injured. Recognition of this demands a clinical classification of wounds that is based on the features of the wound and not on the weaponry or the presumed velocity of the missile.” The system scores certain features of a wound: the maximum diameter, in centimeter, of the entry (E) and of the exit(X) wounds; the presence and the size of the cavity (C); the presence of a fracture (F) and the extent of comminution of that fracture; injury to a vital structure which may be the dura, the

pleura, the peritoneum, or a major vessel; and the retention of metallic fragments (Tables 5.1 and 5.2). The wounds are graded according to the amount of tissue damage by the E, X, C, and F scores into low energy transfer, high energy transfer and massive wounds, and then typed according to the structures injured. The wound is then placed in 1 of 12 categories by grade and type. We are indebted to Colonel Michael Stewart FRCS and his colleagues in the RAMC, Major K Brown, Major W Eardley FRCS, Major A Ramasamy FRCS, and for their extensive advice about the

Table 5.1  The red cross wound classification (Drawn from Coupland 1993). 1. The Field Wound Score

2. Subsequent Analysis. (A) Extent of Tissue Damage

E

Entry

diameter of entry wound, in centimeter

Grade 1

E + X < 10: CO, F0 or F1

Low energy transfer

X

Exit

diameter of exit wound, in centimeter

Grade 2

E + X < 10: c0 or F2

High energy transfer

C

Cavity

Grade 3

E + X > 10: c0 or F2

Massive energy transfer

F

V

M

Fracture

Vital Structure Metallic body

0

wound cavity too small to take two fingers

1

Wound cavity admits two or more fingers

0

No fracture

1

Simple fracture

2

Comminuted fracture

0

No injury to brain, vessels or viscera

1

Injury to the above

0

No metal fragment seen on radiograph

(B) Type Of Wound According To Structure Injured

ST

F0 and V0

F

F1 or F2 and V0

1

One fragment

V

F0 and V1

2

More than one fragment

VF

F1 or F2 and V1

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Surgical Disorders of the Peripheral Nerves

Table 5.2  The 12 categories of wounds (Drawn from Coupland 1993). Grade I Grade II Grade III ST

Small simple wounds

2ST

3ST

F

1F

2F

3F

V

1V

2V

3V

VF

1VF

2VF

3VF Large wounds threatening life or limb

Fig. 5.6  Military rifle bullet, before debridement (above) and after debridement (below). Type 3F wound: E3, X8, C2, F2. The common peroneal nerve recovered (axonotmesis) (Courtesy of Major K Brown RAMC).

use of the IRCR classification in battle casualties and also for their providing numerous examples. They point out that the classification is somewhat defective in the analysis of severe blast injuries (Figs. 5.6 and 5.7).

5.1 Associated Symptoms and Signs The early symptoms of acute nerve injury are abnormal sensations, alteration or loss of sensibility, weakness, motor paralysis, impairment of function and sometimes pain.

Sometimes the patient is aware of warming and dryness of all or part of an extremity. Abnormal sensations or paraesthesiae, most often “pins and needles,” are usually associated with continuing noxious process. They are of course commonly associated with recovery of a transient conduction block. Their mechanism in that process was ingeniously explored by Merrington and Nathan (1949). Increasing pain and deepening of the nerve lesion signifies continuing noxious process. The patient’s failure to observe warming and anhidrosis is, regrettably, often shared by the examining clinician (Fig. 5.8). Pain, though not always present, is a most important symptom. It may be immediate or delayed; episodic or continuous; of all grades of severity. Its occurrence after injury often means that the noxious process is continuing, as when a nerve is stretched over a bony projection, compressed by a hard object or constricted by, for instance, a suture. It is a regular feature of injury caused by critical ischaemia. Such pain is neurostenalgia. It indicates not only that the noxious process is continuing but also that the lesion of the nerve may be deepening and it is an important indication for operation. Neuropathic pain is never easy to recognise in the injured patient who is probably confused, distressed and in pain. It can be distinguished from the pain of fracture or dislocation by loss of sensation, by painful, spontaneous sensory symptoms, (dysaesthesiae), expressed in the territory of the nerve, and by lancinating or shooting pain radiating into the distribution of that nerve. In some patients neuropathic pain is so severe that it overwhelms the pain from a fracture. Mothers may advise the clinician that the pain is worse than that of child birth. A constant crushing, bursting or burning pain in the otherwise undamaged hand or foot indicates serious and continuing injury to major trunk nerves. Progression of sensory loss with a deep bursting or crushing pain within the muscles of the limb, often accompanied by allodynia indicates impending critical ischaemia until proven otherwise. Two rare and easily recognizable forms of severe pain quite often begin soon after injury: they are (1) the pain associated with intradural damage to nerve roots, particularly in traction lesions of the brachial plexus, and (2) causalgia. These, and related matters are discussed in Chaps. 9 and 12. Examination should enable the clinician to extend the knowledge afforded by the history and the narrative of symptoms to permit accurate diagnosis to be made. All findings should be recorded in such a manner that the record will be intelligible later not only to the examiner but also to others. Unfortunately, the signs of acute nerve injury have to be sought at a time when the patient may be the least able to co-operate in an examination; soon after wounding, when there is likely to be distress and when the general condition may be affected by loss of blood and other injuries. The examination often has to be done in the often unfavorable

Clinical Aspects of Nerve Injury Fig. 5.7  A massive blast injury to the buttock and thigh. E more than 20, X0, C1, F0, V0. The profunda femoris artery was intact, the sciatic nerve recovered (axonotmesis) (Courtesy of Major K Brown RAMC).

Fig. 5.8  Sympathetic paralysis seen within a few days of transection of (left) the median nerve at the elbow and (right) the tibial nerve in the thigh.

149

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Surgical Disorders of the Peripheral Nerves

Figures 5.9–5.32 show the sensory loss after transection, rupture, or avulsion of spinal and peripheral nerves Fig. 5.9   Complete avulsion of C4–T1 in two patients.

surroundings of an accident department. The patient may be a distressed child; an older child, an adolescent or an adult patient who may be affected by drink or drugs or by both. When the lesion has been inflicted by a surgeon or anesthetist, the patient’s response is likely to be distorted by post operative pain, by the effects of recent general anaesthesia or by sedative or analgesic drugs. The patient’s ignorance of medical process and even his or her trust in “the doctor” may lead him or her to think that pain and paralysis after operation is just something to be expected. That faith or even deference may inhibit him or her from voicing a complaint. These are no conditions for a quiet and comprehensive “neurological examination,” yet this is the time when the fact of nerve injury must at least be recognised if the best result is to be obtained from treatment. The examiner should at all times bear in mind that if there is a wound over the line of a main nerve and if there is any suggestion of loss of sensibility or impairment of motor function in the distribution of that nerve, it must be regarded as having been cut until and unless it is proved otherwise. Sensory loss is determined by response to light touch and pin prick and if circumstances permit, the patient outlines the area of sensory loss which is marked by a black skin marker pen. The surrounding zone of incomplete sensory loss can be similarly marked in red, and the limb then photographed (Figs. 5.9–5.32). Selected muscles are examined. The patient lying supine is usually able to demonstrate

Fig. 5.10  Sensory loss in avulsion of C5-T1. C4 innervates the skin of the outer aspect of the shoulder; T2 innervates the skin of the inner aspect of the arm.

Clinical Aspects of Nerve Injury

151

Fig. 5.11  Avulsion of C4, C5, C6, C7.

Fig. 5.13  Avulsion of C5. The area of sensory loss is usually larger than that seen after rupture of the circumflex nerve (see Fig. 5.19).

Fig.  5.12  In this patient with T6 spinal cord lesion and on clinical examination, C5 and C6 lesion, operation showed avulsion of C5, C6 and C7.

activity in serratus anterior by lifting the shoulders away from the couch, by “forward shrugging.” A radiograph of the chest will detect, inter alia, elevation of the hemi diaphragm. It is usually possible to observe the presence of flexion and abduction at the shoulder, flexion and extension of the elbow and wrist and flexion and extension of the fingers. The radial, median and ulnar nerves are tested by asking the patient to form an “O” between the thumb and little finger, to give the “thumbs up,” and to open and close the fingers like a fan. It should be possible, by gentle persuasion, to observe active flexion and abduction at the hip,

extension at the knee, and extension and flexion at the heel and toes. The palmar and plantar skin is scrutinised for changes in colour and in sweating. Although this may be more difficult in pigmented skin such changes are detectable. The standard tendon reflexes are examined. A more detailed examination is possible when the patient’s condition is stable, and when pain has been controlled. Limb dominance, occupation, marital status, underlying disease or continuing medication are recorded if this has not already been done. Neuropathic pain is by now somewhat easier to recognise, for this is less responsive to analgesics than is pain from skeletal injury.

5.2 Recognition of the Level and the Depth of Injury In the absence of wounding clinicians should be able to arrive at an accurate diagnosis of the level and depth of a lesion by clinical examination. A sound grasp of the level of the branches of the trunk nerves and of the contribution to those nerves coming from individual spinal nerves is a prerequisite. “Aids to Examination of the Peripheral Nervous System,” originally produced by the Medical Research Council and now in its

152

Surgical Disorders of the Peripheral Nerves

Fig. 5.14  Rupture of C5 and C6. Sensory loss does not extend to the thumb and the index finger.

Fig. 5.16  The area of sensory abnormality after section of the lateral cord in the axilla. As in Fig.  5.15, there was no complete loss of sensation. Fig. 5.15  Transection of C8 and T1. The area of sensory disturbance extends into the arm (medial cutaneous nerve of arm).

fourth edition under the direction of Michael O’Brian (2000), is essential reading. This slim volume should be in the possession of all doctors engaged in injury work. It easily fits into a pocket, but now that white coats have been abolished perhaps nurses and therapists who, of course, continue to wear their uniforms, might be invited to carry the volume.

To take one example, the level of injury to the posterior cord and the radial nerve can be determined by examining teres major (inferior subscapular nerve), latissimus dorsi (thoraco dorsal nerve), and deltoid (circumflex nerve). The nerves to the long head of triceps leave the main trunk proximal to the spiral groove. Those innervating the medial head of triceps pass away from the radial nerve at the entrance to and in the first part of the spiral groove whereas those innervating the lateral head of the muscle leave the main nerve

Clinical Aspects of Nerve Injury

still more distally. Paradoxically, the contribution from the spinal nerves is in reverse order: the medial head is usually innervated by the eighth cervical nerve, the long head by the seventh cervical nerve and the lateral head by the sixth cervical nerve. The nerve to brachioradialis consistently passes away from the trunk about three finger breadths above the lateral epicondyle; the nerve to extensor carpi radialis longus

Fig. 5.17  Rupture of the posterior divisions of the trunks of the brachial plexus deep to the clavicle.

Fig. 5.18  Rupture of the medial cord in the axilla. Loss of sensation was confined to the forearm and hand. There is sympathetic paralysis in the ulnar three fingers.

153

comes off about a centimeter more distally. One nerve to extensor carpi radialis brevis leaves the main nerve about 1 cm above the lateral epicondyle and another at the level of the branching into superficial radial and posterior interosseous nerves. Lesions of the sciatic nerve are often, incorrectly, placed at the knee, to the common peroneal nerve. These errors are prevented by examining gluteus medius, gluteus maximus and biceps femoris. Some of the most serious mistakes in the diagnosis and treatment of patients with injured nerves are made because the examiner fails accurately to assess the depth of injury, failing to distinguish between degenerative and non-degenerative injury and to estimate the extent in the nerve of each type of lesion. Some atavistic urge seems to cause clinicians to play down the severity of nerve injury. Perhaps beneath this urge there is a feeling that if there is a serious injury, much hard and possibly unrewarding work is going to be required. The tendency is of course particularly marked in cases of closed injury and of injury during operation. Too often the mantra “Neuropraxia” is pronounced: too often the soothing words “just some bruising of the nerve” are uttered. The diagnosis of the depth of the injury depends on the history and signs and on the simplest electrical examination. Serious injuries are likely to cause serious lesions of nerves. Severance of a nerve with a cutaneous sensory component will lead to well-defined loss of sensibility and to complete motor, sudomotor and vasomotor paralysis in the distribution of the nerve. Simple conduction block is likely to produce a patchy loss of sensibility and a patchy motor loss.

154

Surgical Disorders of the Peripheral Nerves

Fig. 5.20  Rupture of circumflex and musculocutaneous nerves. Fig. 5.19  Rupture of the circumflex nerve.

Further, it is likely to bear more heavily on the large axons than on the small ones: vibration sense and sensibility to light touch are likely to be impaired, whereas pain sensibility may be unaffected. If the axons are damaged (degenerative lesion), stimulation of the nerve below the level of the lesion 6 days after injury will not elicit a motor response. (Landau 1953, Gilliatt and Taylor 1959). If the axons are intact (conduction block) stimulation will evoke a motor response. It will, equally, be possible to stimulate and record from the nerve below the level of the lesion. This simple but rarely used test can permit the early recognition of the depth of the lesion. A firm diagnosis of neurapraxia should never be made unless 1 week after the injury stimulation of the nerve below the level of the lesion produces a motor response.

5.3 Signs The early signs of nerve injury are alteration or loss of sensibility, weakness or paralysis of muscles; vasomotor and sudomotor paralysis in the distribution of the affected nerve or nerves, and abnormal sensitivity over the nerve at the point of injury. For the reasons given, testing of sensibility is often difficult soon after wounding, or when nerve injury is associated with fracture of a long bone. In addition, it may even be

that for a few hours there is conduction across a clean transection without retraction of nerve ends (Smith and Mott 1986). The actions of some muscles can be simulated by the actions of others, so that the fact of paralysis can be missed in the early stages after nerve injury. However, one almost infallible sign is always present in the first 48 h after deep injury of a nerve with a cutaneous sensory component: because of the affection of small as well as of large fibres, the skin in the distribution of the affected nerve is warm and dry. (Bonney 1983, Birch 1986) In the small child, there may be an abnormal posture of the denervated digits (Fig. 5.33). Canale et al. (2000) describe a sign for anterior interosseous palsy in children. When the child is asked to bend the index finger they do it with the other hand. Other early signs which indicate a deep injury to a nerve include changes in texture of the skin rather like “goose pimples” development of a skin rash, and hypersensitivity surrounding the area of anaesthesia. Another good test for nerve injury in small infants is the “immersion test”: the injured hand or foot is placed, for a few minutes, in warm water. The skin of the denervated digits fails to wrinkle. When there is no breach of the skin and the injury of the nerve is caused by pressure or distortion, there is usually differential affection of fibres. Szabo et  al. (1984), working with volunteer human subjects on the effects of an acute rise of pressure on the median nerve in the carpal tunnel, plainly showed that vibratory thresholds were the earliest measure of a decrease in nerve function. The largest fibres were the most susceptible to pressure. The use of vibratory, or

Clinical Aspects of Nerve Injury

155

Fig. 5.21  Sensory loss in two cases of rupture of the musculocutaneous nerve. Both patients were able to supinate the forearm fully; the power of elbow flexion was around 30%.

Fig. 5.22  Two examples of high lesion of the radial nerve. Right: there is early recovery into the wrist extensors after repair.

pressure stimuli as a non-invasive diagnostic test may, as the authors suggest, have a significant role in clinical work and in research. The smaller ones are spared, so that there is rarely any sudomotor or vasomotor paralysis, and delayed pain sensibility is preserved. We have however seen cases in which pressure paralysis was deep enough to affect the autonomic fibres. In one young girl whose attempt at suicide with narcotic drugs led to prolonged pressure on the tibial and

common peroneal nerves, there was prolonged vasomotor and sudomotor paralysis of the foot. In the case of intraneural hemorrhage or injection the situation is different: small fibres are early affected, sometimes, as with injection of local anaesthetic, before the large fibres. When the injected fluid is itself noxious there is early affection of all sizes of fibre. Peripheral ischaemia is usually signalled by pain, but in cases in which the vascular injury is

156

Surgical Disorders of the Peripheral Nerves

Fig. 5.25  Section of the median and the palmar cutaneous nerve at wrist. Fig. 5.23  Transection of median, ulnar, medial cutaneous nerve of forearm, and brachial artery in the arm of a 14 year old boy. Note the extent of skin innervation provided by the superficial radial and lateral cutaneous nerves of forearm. The intact radial nerve permits a sort of grasp.

associated with fracture, the significance of that pain may not be recognised. Ischaemia affects first the large fibres: discriminative sensibility and vibration sense are first affected (MacKinnon and Dellon 1988) It is not easy to test these modalities when ischaemia is developing because of damage to a main vessel associated with a fracture of a long bone, but if action is not taken until superficial sensibility is lost, it will come too late.

5.4 Tinel’s Sign

Fig.  5.24  High median nerve injury: no active flexion of the index finger and thumb.

Tinel (1915, 1917) was probably the first to draw attention to the indication of the “growing point” of the regenerating axons signalled by the production of paraesthesiae by tapping over the course of the nerve. Buck-Gramcko and Lubahn (1993) remind us that Tinel made the observation at about the same time that Hoffman working on the other side of the Western Front, made a similar discovery (Hoffman 1915a, b). Properly, the sign should be called the “Hoffman-Tinel sign.” Tapping the skin over the course of a recovering nerve reveals the presence of regenerating axons by the production of paraesthesiae in the sensory distribution of the nerve. Rothwell’s translation of Tinel (1917) says: “When compression or percussion is lightly applied to the injured nerve trunk, we often find, in the cutaneous region of the nerve, a creeping sensation usually compared by the patient to that caused by

Clinical Aspects of Nerve Injury

157

Fig. 5.26  A typical area of loss of sensibility after division of the median nerve at the wrist, sparing the palmar cutaneous branch.

Fig. 5.27  The area of sensory loss and “clawing” of little and ring fingers after division of ulnar nerve in the forearm.

electricity.... The “formication sign” is thus of supreme importance since it enables us to see whether the nerve is interrupted, or in the course of regeneration; whether a nerve suture has succeeded or failed, or whether regeneration is rapid and satisfactory, or reduced to a few insignificant fibres. All clinicians will recognise this sign. The element of unreliability is introduced by the fact that some of those regenerating axons are not on their way to any target. However, these

points can be stated: (1) a strongly positive Tinel sign over a lesion soon after injury indicates rupture of axons or severance of the nerve; (2) in favorable degenerative lesions (axonotmesis) or after repair which is going to be successful, the centrifugally moving Tinel sign is persistently stronger than that at the suture line; (3) after repair which is going to fail, the Tinel sign at the suture line remains stronger than that at the growing point; (4) failure of distal progression of

158

Surgical Disorders of the Peripheral Nerves

Fig. 5.28  The area of loss of sensibility in two cases of injury to the femoral nerve at, or proximal to the groin crease.

Fig.  5.29  Cutaneous distribution of the sacral plexus. Left showing area of sensory loss after closed fracture/dislocation of sacro-iliac joint. Right showing area of loss of sensibility after open fracture/dislocation of the pelvis. The muscles of the buttock are wasted.

Fig.  5.30  The area of sensory loss after transection of sciatic nerve in the thigh is confined to the leg and foot.

Clinical Aspects of Nerve Injury

159

Fig. 5.33  Infant’s hand 24 h after section of the palmar nerves to the index finger and thumb. Note that the anaesthetic digits are held out from the others. There was no tendon injury.

Fig. 5.31  Area of sensory loss after high division of common peroneal nerve. Note the pressure sore caused by a conventional ankle-foot orthosis.

conduction block for, at least, a significant number of axons within the nerve. It is important always to remember Tinel’s own advice that a positive sign should not be confused with the “hypersensitivity seen in some cases of neuralgia” (Tinel 1917). The Tinel-like sign elicited by percussion over schwannoma or over nerves in the early stages of entrapment neuropathy, such as the ulnar nerve at the elbow or the median nerve at the wrist, does not indicate that axons have been ruptured, rather that nerve fibres have become sensitised because of focal demyelination and changes in the expression of voltage gated ion channels at the level of lesion.

5.5 Eliciting the Tinel Sign in Closed Lesions

Fig. 5.32  Area of sensory loss after interruption of the deep division of the common peroneal nerve. Left, showing the leg of a 29 year old man in whom severe “compartment syndrome” was overlooked after intramedullary nailing of closed fracture of tibial shaft. The anterior compartment was infarcted and it was excised. Right, showing the area of sensory loss after transection of the deep division of the common peroneal nerve by a knife.

the Tinel sign in a closed lesion indicates rupture or other injury not susceptible of recovery by natural process; (5) a positive Tinel sign means the lesion is degenerative, not a

The examiner’s finger percusses along the course of the nerve from distal to proximal starting well below the presumed level of lesion. The patient is asked to say when the advancing finger elicits a wave or a surge of pins and needles or abnormal sensations, which may be painful, into the distribution of the nerve which must be clearly indicated by the examiner. A positive Tinel sign indicates that axons are ruptured at that level. The sign can be regularly elicited on the day of injury in a conscious patient. The level of the sign should be measured from a fixed point and the distance entered into the records. In the upper limb, we use the tip of the coracoid, the medial or lateral epicondyle and the styloid process of the radius and in the lower limb, the tip of the greater trochanter, the tip of the styloid process of the fibula and the lower points of the medial and the lateral malleoli, whichever is appropriate. At times the examination is painful and patients need to be warned about that. Percussion over the swollen posterior triangle of the neck in cases of multiple

160

Surgical Disorders of the Peripheral Nerves

Fig. 5.34  Static and progressing Tinel’s signs. A 43 year old woman sustained a complete and very painful, lesion of the common peroneal nerve from the kick of a horse. There was a strong, painful, Tinel sign at the level of lesion at the time of exploration 10 weeks after injury. The nerve was deeply compressed by scar from which it was removed. Her pain was abolished. The rate of progress of the Tinel sign for the superficial and the deep divisions of the nerve was about 2 mm a day. There was complete recovery.

avulsion usually elicits painful sensory phenomena which do not radiate into the dermatomes of the injured nerves. A strongly positive Tinel sign indicates to the clinician the level of lesion, and also the depth of lesion. Axons are ruptured where the percussing finger evokes radiation of sensations into the distribution of the nerve under examination. Subsequent examinations may provide evidence that the lesion is regenerating by demonstrating centrifugal progression of the sign which becomes progressively stronger at the distal rather than at the proximal level of sign (Fig. 5.34). Kato (Kato and Birch 2006) examined the evolution of Tinel’s sign in 137 nerves injured by closed fracture or dislocation. Recovery was good in 69 of the 86 nerves where the Tinel sign progressed. or where no Tinel sign was present. A static Tinel sign was one of the indications for operation in 43 of 51 nerves. Thirty-two were repaired and the other 19, which were embedded in callus or caught within a fracture or joint, could not have recovered spontaneously. Table 5.3 shows the

value of a static or advancing Tinel sign in predicting recovery in degenerative lesions after closed injury to the common peroneal, the radial and tibial nerves. An advancing sign proved misleading in 18 nerves. In most of these the distal muscles had been damaged by ischaemia so that the regenerating axons arrived at target organs which were irredeemably fibrosed. One case, of a radial nerve damaged by closed fracture of the humeral shaft was initially seen by one of us (RB) who predicted recovery because the Tinel sign was advancing. Marco Sinisi noted that there was discrepancy between the advancing sign and the failure of recovery of brachio radialis and when he exposed the nerve he found that about three quarters of it was embedded in the fracture; the surviving portion was destined for the superficial radial nerve. Tinel’s sign is particularly valuable in the diagnosis of post ganglionic rupture of the spinal nerves of the brachial plexus (Landi and Copeland 1979). If percussion in the posterior triangle induces radiation as far as the elbow then rupture of C5 is likely; rupture of C6 is anticipated when radiation extends to the lateral forearm and thumb and when radiation extends to the whole hand, especially to the dorsum, then rupture of C7 is expected. Table 5.4 summarises the role of Tinel’s sign in the early diagnosis of rupture of the spinal nerves in 100 consecutive cases of closed traction lesions of the supraclavicular brachial plexus. Most patients were examined within 14 days of injury: a positive sign was found in nine cases of lesion to C5 and C6 yet these nerves were found avulsed. Irradiation into the territory of the supraclavicular nerve (C4) was sometimes wrongly ascribed to a rupture of C5 and irradiation from percussion over a rupture of C5 sometimes extends to the forearm suggesting rupture of C6. Nineteen spinal nerves were found to be ruptured even though no Tinel sign was detected. These stumps were concealed by torn muscle or haematoma, and the level of rupture was close to the foramen. Absence of the sign over a peripheral nerve which is not working, suggests conduction block. The absence of the sign in closed traction lesion of the supraclavicular brachial plexus indicates one of two things: that the nerve has been avulsed or the lesion is conduction block. The distinction between these two is usually straight forward.

Table  5.3  Tinel’s sign as a guide to prognosis in 339 consecutive cases of degenerative lesions in closed injuries to the common peroneal (171 cases), the radial (139 cases) and the tibial (29 cases) nerves examined 2000–2007. Tinel Sign – Progressing Tinel Sign – Static Spontaneous Misleading – no, or poor, Spontaneous recovery Rupture or other lesion not suscepRecovery spontaneous recovery tible to recovery by natural process Common peroneal nerve with divisions

84

12

0

75

Radial nerve

103

5

0

31

Tibial nerve

16

1

0

12

TOTAL

203

18

0

118

Clinical Aspects of Nerve Injury

161

Table 5.4  Tinel’s sign in closed traction lesions of the brachial plexus in 100 adult patients examined and operated 2004–2005. Tinel sign absent Spinal Tinel sign present (358 nerves). Findings nerves (142 nerves). Findings at operation at operation Intact

Rupture

Avulsion Intact

Rupture Avulsion

C5

1

58

4

0

10

27

C6

0

41

5

10

6

38

C7

0

24

0

40

2

34

C8

0

4

0

45

0

51

T1

0

TOTAL 1

4

1

52

1

42

131

10

147

19

192

5.6 Tinel’s Sign and Recovery Henderson (1948) made serial observations on Tinel’s sign in 400 cases of nerve injury in his fellow prisoners of war. Henderson thought that the behaviour of the sign provided certain indications of satisfactory, or unsatisfactory, spontaneous regeneration by 4 months after the injury so that “a strongly positive sign at the level of the lesion, which gradually diminished as the sensitivity of the distal part of the nerve increased, progress peripherally, and faded centrally, was a certain indication that satisfactory spontaneous regeneration was in progressed. Poor recovery, attributed to great axonal confusion at the site of injury, was observed in cases where the sciatic lesion remained sensitive and a positive sign developed in the most proximal muscles within the distribution of the damaged nerve.” The situation is much more straightforward for the clinician examining main nerves damaged by closed fractures or dislocations in civilian practice and it is usually possible to distinguish between axonotmesis and neurotmesis by between 4 and 6 weeks from the day of the injury in closed lesions of the radial, median, ulnar, common peroneal and tibial nerves. Ruth Bowden found that clinically detectable recovery was evident by 64 days in 14 cases of axonotmesis of the radial nerve (Bowden and Scholl 1954). An advancing Tinel sign may be found when only a few nerve fibres are regenerating as in cases where trunk nerves are entrapped within a fracture or joint. Useful function will not return if the target organs are damaged by fracture or sepsis or, above all, by ischaemia. An advancing Tinel sign should be treated with caution in lesions of the common peroneal nerve, where some degree of post ischaemic fibrosis of the anterior compartment is found in about one-fifth of cases. Centrifugal progress of the sign is often unreliable in predicting recovery of lesions of the sciatic nerve incurred during arthroplasty of the hip. Most of these are mixed lesions, some nerve fibres are intact, others sustain conduction block whilst many more have sustained degenerative lesions which may or may not

be naturally favorable. Tinel’s sign can be detected over such “motor” nerves, as the posterior interosseous, but it is more difficult to elicit the sign over deep seated nerves such as the circumflex, the eighth cervical or first thoracic nerves. The sign advances more rapidly in degenerative lesions of naturally favorable prognosis (axonotmesis) than it does after repair of a nerve. A rate of progression of about 2 mm a day is usual. Tinel’s sign progresses more rapidly after repair of proximal lesions, particularly so when the repair is done urgently. Progression at the rate of 3 mm a day is by no means unusual after urgent repair of the supraclavicular brachial plexus in the segment from the neck to the upper arm. Thereafter, progress slows. Similar rates of advance are seen after urgent repairs of the sciatic nerve wounded in the buttock. These rates are close to those recorded by Bowden and Scholl (1954). Bowden and Scholl offered a caveat: “the choice of time for exploration of an injured nerve cannot be based on estimates of rates of recovery alone; in each individual case, all clinical factors must be taken into consideration. Where there is any reasonable doubt about the state of the nerve or the integrity of a suture line, operation should not be delayed since in experienced hands exploration is without harmful effect.” The distance between the sign and a suitable fixed bony point is recorded in the case notes at every examination. The rate of progress of the sign in a healing nerve matches that of the slow anterograde axonal transport system.

5.7 Examination of Sensibility Highet proposed a system for the examination of sensibility and muscle power in a memorandum submitted to the Nerve Injuries Committee of the Medical Research Council in 1941 and this, with some modifications, was adopted by that Committee. The Medical Research Council (MRC) method of recording sensibility offers a reasonable method for recording and measuring progress. As is the case with all such schemes it has obvious disadvantages, but no comprehensive method has yet been devised that does not have the overwhelming disadvantage of extreme complication (Table 5.5). So far as possible, sensation to light touch and pin prick, vibration sense and position sense should be tested, and the area of skin affected should be recorded. The timing of the response to pin prick and the ability to localise to the area of stimulation should if possible be noted. Anhidrosis is easily perceptible; vasomotor paralysis is shown by warming of the skin and, in the finger tips, by capillary pulsation. The examiner should use the pulp skin of his or her fingers, not back of the hand, which is, of course, less densely innervated. Our methods: The modalities routinely tested are light touch, temperature, position sense, pain, two point discrimination,

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Table 5.5  Sensory recovery. The original grading by Highet (1941) Stage 0

Absence of sensibility in the autonomous zone of the nerve

Stage 1

Recovery of deep cutaneous pain sensibility within the autonomous zone

Stage 2

Return of some degree of superficial pain and tactile sensibility within the autonomous zone

Stage 3

Return of superficial pain and tactile sensibility throughout the autonomous zone with the disappearance of over-response

Stage 4

Return of sensibility as in Stage 3 with the addition that there is recovery of two-point discrimination within the autonomous zone

The Medical Research Council System by Seddon (1954) S0

Absence of sensibility in the autonomous area

S1

Recovery of deep cutaneous pain sensibility within the Autonomous area of the nerve

S2

Return of some degree of superficial cutaneous pain and tactile sensibility within the Autonomous area of the nerve

S3

Return of some degree of superficial cutaneous pain and tactile sensibility within the Autonomous area with disappearance of any previous over-reaction

S3+

Return of sensibility as in Stage 3 with the addition that there is some recovery of two-point discrimination within the Autonomous area

S4

Complete recovery

localisation and pressure. The stereognosis test has been used since 1975 (Wynn Parry and Salter 1976). Light touch: A wisp of cotton wool is moved lightly across the area under test. Temperature: Metal tubes are used: one contains cold water, the other, warm at about 35°C. These are applied alternately to the area under test. Position sense: All nearby joints, other than the one being tested, must be stabilised. The patient is first shown the direction in which the joint is being moved. Then, with eyes closed, he or she is asked to indicate the direction in which the joint is being moved. Pin prick: A bluntened pin is lightly applied to the skin and the patient is asked to say whether it feels sharp or blunt. Two point discrimination: This is done with the blunted points of a compass or the ends of a paper clip or with a special device. The patient is first instructed: “I shall touch your finger now with one point; now with two. If you feel one, say “one”; if you feel two, say “two”; if you are in doubt, say “one.”” Then, with closed eyes, the patient attempts distinction between one and two points. Two point discrimination is valuable because it indicates the degree of reinnervation of slowly adapting receptors. Of course, Highet (1941) used the test in his system of sensory grading. It is subject to limitations. The patient easily gets confused; it is difficult or impossible to ensure that the same

pressure is used throughout the test. Brand (1985) showed that even skilled clinicians used, during the test, pressures varying from 4 to 40 g/unit area. Such variability leads, of course, to error when results of different observers are compared. Bell and Burford (1982) using transducers and oscilloscopes, found that the difference between the pressure applied to one point and that applied to two easily exceeded the resolution threshold for normal sensitivity. They concluded that two point discrimination had poor validity. Refinements of the method were introduced by von Greulich (1976) and by MacKinnon and Dellon (1985). These were based on the use of as ring with circumferential prongs set at varying intervals. Useful instruments had, of course, been developed previously by Mannerfeldt. Dellon (1978) introduced the concept of moving two-point discrimination. The patient is asked to move his or her finger across a number of ridges separated by varying intervals. He or she then identifies the shortest interval appreciated, which is invariably less than that recorded by the static test. We think that this ingenious method is, to a certain extent, artificial since normal sensibility requires handling of an object between thumb and finger – a process that excites a far greater range of sensory receptors. However, Novak and MacKinnon (1999) found that a high degree of inter observer reliability between moving two point discrimination, static two point discrimination, and Semmes Weinstein filament tests. Localisation: We use the chart devised by Wynn Parry and Salter (1976) in which the hand is divided into different numbered areas. The blindfolded patient is asked to point to the area being touched, and this is recorded on the card. Thus, if a touch on the tip of the index finger is felt as a touch on the base, the number of the former area is recorded on the latter area on the chart. The localisation and texture and shape recognition charts were brought to the Peripheral Nerve Injury Unit by Christopher Wynn Parry when he joined the staff at the Royal National Orthopaedic Hospital as Director of Rehabilitation in 1975 (Figs. 5.35 and 5.36). Pressure: The padded blunt end of a pencil is used to indent the skin only lightly. We also use Von Frey hairs and the weighted pins (5 and 10 g) developed by Ruth Bowden. Recognition of textures and shapes: Riddoch (1940) asked patients to recognise different coins by touch. Porter (1966) asked patients to recognise steel type letters, in dimension 1.0 by 0.8  cm. The letters must be identical in reverse and H, O, U, V, Y are used. The “pick up” test (Moberg 1958) is, of course, a measurement of function as well as of sensibility. So is the assessment of ability to recognise objects, the importance of which we believe was first recognised by Wynn Parry and Salter (1976) and used at RAF Chessington and then subsequently in the PNI Unit at the Royal National Orthopaedic Hospital(Wynn Parry 1981). The blindfolded patient is presented with a series of objects of differing shape, texture and surface character, and asked to distinguish them. The number correctly identified and the

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Fig. 5.35  Chart recording improvement of the measurement of ability to recognise and to localise at intervals after repair of median nerve at wrist.

Fig. 5.36  Another example of recovery of recognition and localisation after repair of median nerve.

time taken are recorded. Later, common textures and small and large objects in daily use are presented for recognition. Rosen and Jerosch-Herold (2000), Jerosch-Herold (2000, 2005) thought that the shape and texture identification test may provide a better record of regeneration than those for two point discrimination.

5.8 Quantitative Sensory Testing Dyck et  al. (2005) classified methods of measurement of different modalities of sensation into three groups. Semi quantitative sensory tests include the usual techniques which are useful in traumatic neuropathy where there is a

164

normal limb available for control. Quantitative sensory testing (QST) is the use of stimuli which are more precisely quantitative and more rigorously tested but the environment is not controlled. In laboratory QST all aspects of the examination are predetermined, standardised and controlled. Our experience is drawn from the work of Praveen Anand who has examined many hundreds of patients at our joint clinics over the last 20 years, first at the London Hospital and later at Imperial College, London (Anand et  al. 1994, 1996) These investigations confirm the presence and the extent of axonopathy which cannot be detected by standard neurophysiological investigation. Focal, or generalised, neuropathy has been demonstrated in patients wrongly labelled as “complex regional pain syndrome Type 1” (CRPS Type 1) or even as malingerers. Our findings in some patients diagnosed with “CRPS Type 1” provide support for the critique from Oaklander et al. (2006). The differential susceptibility to the lesion between different groups of nerve fibres have been confirmed. The rates of recovery of different populations of nerve fibres have been analyzed in many cases of favorable, degenerative lesion (axonotmesis) and after repair. Profound differences between the infant and the adult have been revealed after repair of lesions of the brachial plexus (Anand and Birch 2002, Htut et  al. 2006). The general assumption that the smallest fibres regenerate more rapidly has been called into question and we have shown that reinnervation of the skin lags far behind reinnervation of skeletal muscle after repair of the brachial plexus in the adult. The methods used are now outlined. Thermal threshold: A thermal threshold testing system (Somedic, Stockholm, Sweden) with a rate of rise in temperature of 1°C/s, is used. The small thermode (15 × 25 mm) is placed at the appropriate site, and the base line temperature is set at a neutral point between 30°C and 32°C. Thermal threshold is determined for cool and warm sensation by four separate consecutive tests for reach modality. The mean difference from base line temperature is recorded as threshold. The patient indicates their recognition of the stimulus by pressing a button. No significant difference has been seen by using either verbal or manual indication of change. “Abnormal” (more than two SD above the mean) values in children are: warm sensation greater than 3.8, cool sensation greater than 2.3; for adults aged between 20 and 30 years, abnormal values are: warm sensation greater than 3.9 and cool sensation greater than 2.6 (Fig. 5.37). Light touch: Thresholds are determined using Semmes Weinstein hairs which are made by A. Ainsworth, University College, London, UK. The number of the hair reliably detected (three or more out of five trials) with the lowest force is recorded and values are then transferred into respective gram values. A threshold to light touch greater than that elicited by the number three filament (0.0479g) is abnormal (Fig. 5.38).

Surgical Disorders of the Peripheral Nerves

Fig. 5.37  Testing of warm and cool thermal thresholds (Courtesy of Dr. Peter Misra).

Fig. 5.38  Monofilament perception to assess punctate touch (Courtesy of Dr. Peter Misra).

Vibration sense: The threshold is measured with a biothesiometer (Biomedical Instrument Company, Newbury, Ohio, USA) placed at the distal interphalangeal joint of a

Clinical Aspects of Nerve Injury

Fig. 5.39  Measurement of vibration perception thresholds (Courtesy of Dr. Peter Misra).

digit or over bony prominence in more proximal joints. Three ascending and three descending trials are carried out and values averaged. In children, an abnormal value is more than 8 V; in adults, it is more than 10 V (Fig. 5.39). These are subjective tests, they depend on the patient’s own perception of stimulus. Other methods are used to measure function in the post ganglionic sympathetic efferent fibres and the histamine induced flare response mediated by the axon reflex. Sweating: This is measured in the palm of the hand using an evaporimeter (Servomed, Stockholm, Sweden) in grams per square meter per hour. The instrument has two sensors which measure the relative humidity in an open cylinder at different distances from the skin surface and signals derived from these transducers are computed to provide first, the partial pressure of the water saturation gradient and then the evaporation rate. A value less than 50% of the contralateral hand is considered abnormal (Fig. 5.40). The Histamine induced flare response: The flare induced by the intradermal injection of 0.03 ml of histamine 1 mg/ml is measured by laser Doppler fluxmetry (Fig. 5.41). We have investigated conduction in smaller nerve fibres and in the motor pathways by techniques which supplement classical neurophysiological investigative methods. Contact heat evoked potential stimulator (CHEPS) enables studies of conduction within small sensory fibres (Ad and C fibres). The CHEPS machine (Medoc Ltd., Ramat Yishai, Israel) rapidly stimulates cutaneous small nerve fibres, and resulting evoked potentials can be recorded from the scalp. The machine can be put into a MR scanner so that functional MR images are available. Patients with symptoms of sensory neuropathy have been studied using CHEPS, and the findings compared to other objective measures of small nerve fibres such as the histamine-induced skin flare response and intra-epidermal fibres counts (IEF). CHEPS has been compared with the results of quantitative sensory testing (QST)

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Fig. 5.40  Quantitative sweat testing (Courtesy of Dr. Peter Misra).

Fig.  5.41  Histamine induced flair assessment using laser Doppler scanning (Courtesy of Dr. Peter Misra).

(Atherton et al. 2007). Amplitudes of Ad evoked potentials (mV) following face, arm or leg stimulation were reduced in such patients. The reduced leg skin flare responses correlated

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the level of brachial plexus or spinal cord injury, and in the analysis of the variable susceptibility of different populations of nerve fibres (Figs. 5.42 and 5.43). Conduction in somatic efferent pathways: Transcranial magnetic stimulation (TMS) or transcranial electromagnetic evoked potentials (TCEMEP) is a technique in which the motor cortex is stimulated by a brief electromagnetic stimulus delivered through a hand held magnetic stimulating circular coil. We use single pulse TMS with the Magstim®200 Monophasic stimulator (Novametrix Medical Systems Ltd., Whitland, UK) to assess motor pathways (see Htut et al. 2007). A high power 90 mm coil is placed over the head at the area over the motor cortex or over the dorsal skin of the neck. The evoked motor response can be detected by electrodes placed over the relevant upper limb muscles and the motor action potentials recorded on an EMG machine. Facilitation is used whenever possible; the patient is asked to attempt to contract the muscle from which the recording is made, as this can improve the amplitude of the recorded motor response. Responses from the injured and the contra-lateral (intact) limb can be compared (Fig. 5.44).

with leg Ad amplitudes. In leg skin biopsies, IEF counts were reduced and these also correlated with Ad amplitudes. CHEPS appears to be a sensitive measure, with abnormalities observed in some symptomatic patients who did not have significant IEF loss and/or QST abnormalities. CHEPS thus provides a clinically practical, non-invasive and objective measure and it has proved to be a useful tool for the diagnosis of sensory small fibre neuropathy, in the assessment of

5.9 Examination of Muscles 5.9.1 Some Pitfalls

Fig. 5.42  Contact heat evoked potential studies. The skin is stimulated by a thermode (in this case placed over the forearm) and the evoked potentials are recorded and averaged using an electroencephalographic (EEG) system with appropriate electro-placements and filtering (Courtesy of Professor Praveen Anand and Dr. Peter Misra).

Trick movements. Accuracy of assessment may be impaired by failure to recognise substitution of the action of paralyzed

Cz [uV]

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Fig. 5.43  Findings from contact heat evoked potential stimulation. The evoked potentials recorded from electrodes placed on the scalp.

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Clinical Aspects of Nerve Injury

Fig. 5.44  Magnetic stimulation of, in this case, the brain demonstrates central and peripheral motor integrity and conduction times. Stimulation can also be applied to the neck so that the motor cortex and the motor roots are magnetically stimulated and recordings are made from limb muscles (Courtesy of Dr. Peter Misra).

muscle by the “trick” movement. Such movements are, of course, useful for the patient in providing function when the primary movers are permanently paralyzed. They may be produced by direct substitution, by an accessory insertion, by the “tenodesis effect” or by rebound. It is important for the examiner to palpate the belly of the muscle under examination and at the same time, to palpate the tendon of that muscle. Direct substitution: Most patients with paralysis of the deltoid muscle can, when the spinati and the rotator cuff are preserved, abduct the limb at the gleno-humeral joint. Even the clavicular part of pectoralis major and the long head of triceps can affect abduction when the humerus is rotated laterally by the action of the infraspinatus. When the biceps brachii and the brachialis muscles are paralyzed, the action of the brachioradialis alone often suffices to flex the elbow to, at least, power MRC Grade 4. Of course, the power of gravity suffices to extend the elbow in the absence of triceps. We have seen how a kind of opposition of the thumb can be produced by action of the flexor brevis and abductor longus when the thenar muscles supplied by the median nerve are paralyzed. Strong extension of the fingers can give an impression of an abducting action in the interossei, whilst strong flexion can give the appearance of an adducting action. The interosseous muscles extend the proximal interphalangeal joints whilst the metacarpophalangeal joints are flexed. Unfortunately, there is no substitute for the abductors of the hip. Lesions of the gluteal nerve leave the patient with serious defects in stability of the pelvis and in their gait. Accessory insertion: The abductor and flexor brevis pollicis have insertions to the extensor expansion, so that abduction of the thumb extends the interphalangeal joint, even when the extensor muscles are paralyzed.

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“Tenodesis” action: When the long flexors of the fingers are paralyzed, extension of the wrist produces in them sufficient tension to cause flexion of the interphalangeal joints. It is this action that is exploited in the tenodesis of paralyzed finger flexors to give a grip when the wrist is extended. Rebound: When the antagonist to a paralyzed muscle contracts strongly and relaxes quickly it may appear as a contraction of paralyzed muscles. In paralysis of the common peroneal nerve, the patient can mimic active extension of the toes or active extension at the ankle by strong contraction and sudden relaxation of the flexors. Anatomical variations: Some of these have been described in Chap. 1. T1 provides functional extension of the digits in at least 10% of patients. Powerful extension of the digits is seen in more than one-third of patients in whom C5, C6 and C7 have been ruptured or avulsed. The ulnar nerve frequently sends a branch to the distal medial head of triceps, the radial nerve consistently innervates part of the brachialis and there are commonly variations in the innervation of the small muscles of the hand. Measurement of muscle power: No system for recording of motor power has really superseded that proposed in 1941 by Highet (1954) to the Nerve Injuries Committee of the Medical Research Council (Table 5.6). The scale is non linear. Sharrard (1953) estimated that a lower limb muscle graded as MRC 4, possessed about 40% of normal strength and that a grade 3 muscle was about 15% as strong as normal. Trumble et al. (1995) made objective measurements of muscle power by the use of force transducers; they used the results to “quantitate” the MRC Grades. Thus, they reckon Table 5.6  Motor recovery. The original grading proposed by Highet (1941) Stage 0

No contraction

Stage 1

Return of perceptible contraction in proximal muscles

Stage 2

Return of perceptible contraction in both proximal and distal muscles

Stage 3

Return of function in both proximal and distal muscles to such an extent that all important muscles are of sufficient power to act against resistance

Stage 4

Return of function as in Stage 3 with the addition that all synergic and isolated movements are possible

Stage 5

Complete recovery

The Medical Research Council System by Seddon (1954) M0

No contraction

M1

Return of perceptible contraction in the proximal muscles

M2

Return of perceptible contraction in both proximal and distal muscles

M3

Return of perceptible contraction in both proximal and distal muscles of such degree that all important muscles are sufficiently powerful to act against resistance

M4

Return of function as in Stage 3 with the addition that all synergic and independent movements are possible

M5

Complete recovery

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that Grade M3 represented 17–42% of the function of the healthy muscle, and that Grade M4 represented 66–79%. The use of this technique is, unfortunately, too time consuming for use in most clinical work. Mills (1997) studied the first dorsal interosseous muscle in cases of amyotrophic lateral sclerosis. He found a linear relationship between the degree of wasting and the amplitude of the compound motor action potential (CMAP). That relation was exponential between the MRC Grade and the CMAP: “in effect, a reduction of one point on the scale is associated with, on average, halving of the CMAP amplitude.” Kaufmann (2005) comments:“the proportion of maximum strength required to overcome gravity is markedly different between muscle groups. Therefore manual muscle testing has limited value, particularly in the lower extremity.” Muscles work at about 25% of normal strength during walking, which is more or less equivalent to an MRC Grade of 3+ (Perry et al. 1986). The considerable reserve permits more strenuous activity and provides endurance. The assessment of motor function is extended by methods used to determine the stamina of muscles. The simplest method is to record with a stamina gauge or spring balance the length of time during which the subject can maintain contraction as a standard percentage of his or her maximal strength. Or, repeated contractions are made at maximal strength and the number that can be made before amplitude falls to 50% of the original, is recorded. A standard dynamometer or a sphygmomanometer with an aneroid or mercury gauge may be used. It is preferable to use a size of bulb to fit the size of the hand.

5.9.2 Our Methods We use the instruments devised by Mannerfeldt and made by HC Ulrich (Ulm) (Birch 1989; Birch and Raji 1991, Dunnet et al. 1995). The power of pinch grip is reduced by about one-third in low median palsy, and by nearly three quarters in low ulnar palsy. Power grip is reduced by about one-half in high ulnar palsy and it is as low as 20% in radial palsy, such is the importance of extension of the wrist (Fig. 5.45). A myometer (model D60107MK1. Penny and Giles Transducers, Christchurch, Hampshire) is used for the examination of more proximal muscles. For the shoulder and arm, the patient is seated comfortably with their back erect against the upright of a chair, both upper limbs are held in the same position. The examiner applies force against the arm using the appropriate cup. The amount of force required to overcome the patient’s resistance is noted and recorded as a percentage of the opposite limb. For hip flexion, the patient lies supine, on their side for abduction and for extension prone. Power of extension of the knee is best

Surgical Disorders of the Peripheral Nerves

measured with the patient sitting with the legs over the side of the couch (Fig. 5.46). Although many patients with isolated paralysis of deltoid show a complete range of active movement at the shoulder, the power of forward flexion and abduction is reduced to about 40% of the uninjured side. The power of extension of the shoulder, measured at 90° of abduction, is reduced to as little as 5%. The power of abduction after a “good” result of repair of the circumflex nerve reaches about 60% of the uninjured side. The power of elbow flexion after musculocutaneous palsy is reduced to between 20 and 40% of the uninjured side. It approaches 60–80% of normal after successful repair of the nerve. The power of dorsiflexion of the ankle after “good” results of repair of the common peroneal nerve is around 50% of normal, that of extension of the knee after successful repair of the femoral nerve, about 60% of normal. Although these figures fall short of normal, they are, of course, far superior to the power restored by muscle transfers.

5.9.3 Clinical Examination It is with the large proximal muscles, about the shoulder girdle and about the hip, that serious mistakes are most common. Delay before diagnosis of nerve injury is, in many cases, quite alarming despite the reliability of precise but elementary clinical examination. Thoraco scapular, thoraco humeral, and scapulo humeral muscles. Narakas (1993) described a simple clinical measure, the inferior scapulo-humeral angle (ISHA), which is very helpful in the analysis of injuries to the nerves to these muscles. The inferior scapulo-humeral angle is subtended by the long axis of the humerus and the lateral border of the scapula. The tip of that angle is centred over the glenohumeral joint. It is measured at rest and then with the arm in full active elevation. It measures the range of elevation at the glenohumeral joint (Fig. 5.47). Narakas acknowledged that Inman et  al. (1944) had earlier arrived at this concept. Narakas(1993) measured the inferior SHA in 170 patients with nerve injuries affecting the shoulder girdle, and also in patients with rupture of the rotator cuff. The active inferior SHA was reduced to 30° or less in patients with isolated rupture of the rotator cuff, in cases of suprascapular nerve palsy, or in combined lesions of these nerves with or without concomitant rupture of the cuff. The angle was substantially reduced in lesions of the spinal accessory nerve; it was least reduced in cases of serratus anterior palsy. We have used the method of Narakas since 1993. Its role in the analysis of shoulder deformities in more than 1,500 cases of birth lesion of the brachial plexus is described in Chap. 10. It has been applied in over 800 adult cases of nerve lesions affecting the thoraco-scapular girdle. This simple investigation measures the respective contributions to elevation provided by the

Clinical Aspects of Nerve Injury

169

Fig. 5.45  Measurement of grip and pinch. Top left measuring of pinch grip between thumb and index finger, top right showing the “median power grip” with use of thumb; bottom left showing “ulnar power grip” with thumb excluded; bottom right another method for measuring grip strength.

thoraco-scapular and the gleno-humeral joints. Stiffness of the joints is detected by measuring the passive range which, in the normal limb, lies between 170 and 180°. This simple investigation should be more widely used. Combined lesions of the accessory nerve and the nerve to serratus anterior are, fortunately, rare, for these are crippling and painful (Fig. 5.48). The trapezius muscle is tested by asking the patient to elevate the limb or to press forward against resistance. The lower fibres can be tested by asking the patient to put a hand

behind the back and press it against the trunk. The rhomboids are tested by pressing in the opposite direction (Fig. 5.49). The action of the levator scapulae muscle is best felt at the beginning of abduction of the shoulder from a resting position of 30° of abduction. In her study of iatrogenous lesions of the spinal accessory nerves, Camp (2010) found that the diagnosis was made by the responsible surgeon in only three cases and the average delay before diagnosis was no less than 18 months (Fig. 5.50). This delay is inexplicable. Most patients experienced

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Fig. 5.46  Measuring power of muscles at the shoulder. The patient is seated.

Fig. 5.47  The active inferior scapula-humeral angle (ISHA) in a normal shoulder lies between 150° and 170°.

immediate severe pain and demonstrated remarkable loss of function. The posture of the scapula is characteristic. It drops downwards, and away from the spine. The average ISHA, in Camp’s cases, was about 50°. The “winging” is often wrongly attributed to paralysis of serratus anterior muscle (Fig. 5.51). The nerve to serratus anterior is a frequent victim of the attentions of surgeons and transection is associated with pain

and loss of function only slightly less than that seen after accessory palsy. The usual way to test the serratus anterior muscle is to ask the patient to press against the wall with both hands. Weakness is shown by winging of the scapula on the affected side. The method is, unfortunately, inapplicable just when it is most needed: in paralysis of the upper limb from a complete lesion of the brachial plexus. The examiner

Clinical Aspects of Nerve Injury

171

Fig. 5.48  Two examples of combined palsy of the spinal accessory and the nerve to serratus anterior.

Fig. 5.49  The lower border of trapezius, 1, is demonstrated by forcing the left hand against the spine and the rhomboids, 2, are shown by pressing the right hand away from the spine against resistance. “T” towards, trapezius; “R” rearwards, rhomboids.

supports the paralyzed upper limb with one arm; the index finger and thumb of the examiner’s other hand grip below a pole of the scapula; the patient is asked to push forwards. Protraction of the scapula shows that serratus anterior is not paralyzed (Fig. 5.52). The nerve is particularly susceptible to involvement in neuralgic amyotrophy. The ISHA was, on average, 130° in 45 patients with lesions of the nerve. The scapula is elevated and approaches the spine (Fig. 5.53). The circumflex and suprascapular nerves – the rotator cuff. Inman et  al. (1944) studied the joints of the shoulder girdle by inserting pins into the skin of volunteers and recording movement, by radiographs and by measurement of

current action potentials, from the muscles. They observed: “it should be clearly recognized that the standard text book teaching on these motions is entirely incorrect. These state that gleno humeral motion occurs up to a right angle and that thereafter further elevation is brought about by rotation of the scapula. Roentgenography and examination of the living proved beyond any doubt that scapula and humeral motion are simultaneously continuous” (Fig. 5.54). Recognition of rupture of the circumflex nerve can be very difficult. One reason for this is the widely held (and erroneous) view that the deltoid muscle is the abductor of the gleno humeral joint (Figs. 5.55–5.57). Wynn Parry (1981) examined 145 patients with paralysis confined to the deltoid muscle. He found that the range of abduction was full, or nearly so, and described a system of training compensatory movements which enabled most of his patients to return to full military duties: “it must be stressed that these movements providing full abduction and elevation are not trick actions in the sense usually associated with this word; all the muscles involved normally help to abduct the shoulder. The scapulo-humeral rhythm is quite normal and in the later stages of re-education the patient does not even need to rotate the humerus externally to initiate the movement.” Seddon (1975) was a little more cautious: “this perfect abductor action of the supraspinatus is rare; it is more usual to find abduction to about 155°, with the arm a little in front of the coronal plane of the body.” Curiously, the loss of abduction caused by lesions of the suprascapular nerve and/or of rupture of the rotator cuff is frequently and wrongly attributed to a lesion of the circumflex nerve (Figs. 5.58–5.60). In 63 cases we found that the active ISHA was diminished by about 20° in uncomplicated ruptures of the circumflex when there was no stiffness of the shoulder. The

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Fig. 5.50  Right spinal accessory palsy. The scapula drops down and away from the spine. The active ISHA is 30°.

Fig. 5.51  Left spinal accessory palsy. Scapular winging, without prominence of the lower fibres of the trapezius, in a case where there is some early recovery into the upper fibres after repair of the spinal accessory nerve. At rest, the scapula is displaced downwards and away from the spine.

Clinical Aspects of Nerve Injury

Fig.  5.52  A method of examining serratus anterior. The examiner grasps the lower pole of the scapular between finger and thumb and the patient is asked to thrust the upper limb forwards. The examiner will be unable to block protraction of the scapula if serratus anterior is normal.

angle is reduced to less than 30° in most cases of suprascapular palsy or in complete ruptures of the rotator cuff (78 cases). Perhaps the most reliable sign of circumflex palsy is weakness of extension. The power of extension at the shoulder abducted to 90° is as little as 5–10% of normal when the deltoid is

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paralyzed. The diagnosis of rupture of the circumflex nerve is only easy when it is too late to do anything about it, that is, when the atrophy of the muscle is all too plain. It is a very hard matter for the clinician treating a patient with fracture/dislocation of the shoulder to examine function in the muscles. The area of loss of sensation is inconsistent and some patients will describe sensation of the skin over the muscle as abnormal rather than absent. It is probably helpful for the treating clinician to bear the possibility of nerve injury in mind and to plan for examination of the muscles about the shoulder at 1 week after urgent treatment by which time sensory loss and paralysis can be readily detected. Examination of the adductors and medial rotators of the shoulder is usually straight forward. The subscapularis, the most powerful of the muscles comprising the rotator cuff, is more difficult to test. Placing the hand behind the back is a complex movement and requires integrity of the thoracoscapular muscles. It is usually impaired in patients with lesions of the spinal accessory, the nerve to serratus anterior or dorsal scapular nerves. Isolated paralysis of the subscapularis is rare. If the tendon is ruptured many patients are still able to maintain a full range of medial rotation although power is reduced in the last 20° or 30° (Figs. 5.61–5.63).

Fig. 5.53  Scapular winging in nerve to serratus anterior lesion. This is easily distinguishable from the winging provoked by accessory palsy by the position of the scapula which is drawn upwards and towards the spine by the unopposed action of trapezius, levator scapulae, and rhomboids.

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Fig. 5.54  The deltoid. The anterior, middle, 1, and posterior, 2, components of the muscle should be observed and palpated during resisted abduction and extension.

All three heads of triceps should be examined for this provides information about which spinal nerves have been injured and offers an indication of the level of injury of the radial nerve (Fig. 5.64). Ruptures of the musculocutaneous nerve are frequently missed at first examination because brachioradialis is such a powerful flexor and also because the radial nerve often innervates the lateral portion of brachialis (Figs. 5.65 and 5.66). The power of supination and pronation of the forearm should be tested from the neutral position: it is important to remember that both biceps and supinator contribute to supination, and that the long flexor muscles of the forearm can often give useful pronation when the pronator teres muscle is paralyzed or weak. Paralysis of the extensor and flexor muscles of the wrist may be masked by the extensor and flexor muscles to the digits. Extensor pollicis longus is capable of extending the wrist, abductor pollicis longus can mimic this action if the wrist is partially pronated. It is important to palpate both the muscle and the tendon under examination (Fig. 5.67). The long flexors of the fingers: The flexor superficialis, usually innervated by the median nerve, acts on the proximal interphalangeal joints of the medial four digits. Its action on individual fingers is best tested by holding three of the digits almost straight and asking the patient to flex the free finger. Because the tendons of the superficialis are largely independent of each other and those of profundus are not, the former muscle will act to flex the proximal interphalangeal joint (Fig. 5.68).

Surgical Disorders of the Peripheral Nerves

The medial half of the flexor digitorum profundus (FDP) is usually innervated by the ulnar nerve; the lateral part, by the median nerve. With the exception of that to the index finger, the tendons are closely associated with each other, and independent movement is, in most cases, hardly possible. The test for the integrity of the profundus requires the subject to flex the distal interphalangeal joint of one finger with the proximal joints of that finger and all joints of the other fingers stabilised. One quick way to test the FDP simultaneously is to ask the patient to curl the fingers into the palm with the metacarpophalangeal joints extended. The examiner’s finger cannot extend the distal interphalangeal joint if the muscle is normal. The division of the supply of the intrinsic muscles of the hand between the median and ulnar nerves varies from subject to subject (Rowntree 1949). The most common arrangement is for the ulnar nerve to supply all muscles with the exception of the first lumbrical, the abductor brevis and opponens pollicis, and part of the flexor brevis pollicis. Most of the intrinsic muscles act on the metacarpo-phalangeal joints to flex, adduct and abduct. The particular action of the thenar muscles is to oppose the thumb to the little finger, and the muscle particularly responsible for rotating the metacarpal bone during that movement is the opponens. When the median nerve has been cut the opposing action of the thenar muscles can be mimicked by the combined action of an ulnar-innervated flexor brevis and the abductor longus muscle. Comparison with the intact side will usually show that this combined action does not reproduce the rotational action of the opponens. Similarly, the abducting action of the abductor brevis can in the absence of median nerve function be imitated by the action of the abductor longus muscle. These points are important in the early stages when there is no wasting to guide the examiner (Figs. 5.69 and 5.70). The action of the thumb in pinching against the forefinger is modified and weakened by the loss of the stabilising action of the flexor brevis pollicis on the first metacarpophalangeal joint. Without that action, pinch has to be mediated by the action of the flexor longus pollicis on the interphalangeal joint. The power of the ulnarinnervated muscles of the hand is best tested by examining the power of abduction and adduction of the fingers. The ease with which a sheet of paper may be pulled from between two adducted fingers gives some indication of this power.

5.9.4 The Lower Limb There is no great difficulty in testing the muscles connecting the pelvis to the femur in the healthy subject, but things are

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Fig. 5.55  Elevation of the upper limb in full medial rotation by the supraspinatus in the absence of deltoid in four cases of proven rupture of the circumflex nerve. Bottom left and right: note the activity in the clavicular head of pectoralis major.

different when this has to be done soon after replacement arthroplasty. Our observations suggest that in this situation there is also quite often a certain reluctance to look. In one case, a “drop foot” was observed soon after arthroplasty, but it was not until a year later that another examiner found paralysis of most of the muscles of the buttock. Superior gluteal palsy is crippling, yet delay in diagnosis is common. Much can be learnt from watching the patient walk. The integrity of the smaller glutei is tested with the patient standing; that of

the rotators of the hip with the patient seated, and that of the gluteus maximus with the patient prone (Fig.  5.71). It was common experience at times when poliomyelitis was common to see children and young adults walking quite well even though their quadriceps muscles were paralyzed (Fig. 5.72). Of course, they did this by a form of adaptation, a trick movement, in which the tensor fascia lata was responsible for stabilisation of the knee. In many cases there was the added factor of a hyperextension deformity of the knee. It is, however,

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Fig. 5.56  The movement of the scapula in another case of rupture of the right circumflex nerve. The active ISHA on the side of the injury(bottom right) is reduced by 20° showing that 20° of the range of elevation is provided by extra movement at the thoraco-scapular joint.

Fig. 5.57  Combined injuries to the suprascapular and circumflex nerves. Left: showing the range of elevation in a patient with irreparable injury to the right suprascapular nerve but with a good result after repair of the circumflex nerve. Right: showing the elevation in another patient in whom repair of the left suprascapular nerve was successful but whose circumflex nerve injury was irreparable.

Clinical Aspects of Nerve Injury

Fig. 5.58  The infraspinatus, 1, is examined by resisting lateral rotation with the warm against the side.

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the diagnosis was recognised only after the patients fell and damaged themselves. A lesion of the femoral nerve high enough to paralyze both hip flexors and extensor muscles of the knee is crippling. Examination of the power of flexion of the hip is best done with the patient lying supine. The power of extension of the knee is best measured with the patient sitting and the examiner should attempt to assess bulk and power in the three superficial components of the muscle, the vastus medialis, the rectus femoris, and the vastus lateralis. The flexors of the knee are best examined with the patient prone: it is usually possible to distinguish the action of the biceps femoris from that of the medial hamstrings. It is necessary, in testing the power of the flexors of the ankle, to make sure that the action is in fact effected by the soleus and gastrocnemius: the tibialis posterior and the flexors of the toes can produce ankle flexion, though they cannot sustain the patient’s weight. Both tibialis muscles effect inversion of the foot; the anterior muscle is the principal extensor of the ankle. It is not always easy to measure the strength in the evertor muscles of the ankle, (peroneus longus and brevis). It may be easier to detect early recovery with the patient lying on their side and the foot held plantigrade. The muscle belly and the tendon are observed and palpated (Fig. 5.73). We know of no really satisfactory way of testing the integrity of the intrinsic muscles of the foot. Some individuals can use these muscles independently of each other, most cannot (Fig. 5.74).

5.9.5 Late Signs of Nerve Injury

Fig. 5.59  Initiation of abduction, with opening of the active ISHA was the first sign of recovery into supraspinatus after repair of the suprascapular nerve. The lesion of the circumflex nerve was irreparable.

quite wrong to assume that an adult with a deep femoral nerve lesion could walk comfortably and without risk. In six of our cases of femoral palsies incurred during total hip arthroplasty,

Two weeks after a complete degenerative lesion, the area of loss of sensibility is well defined; the beginning of wasting indicates the extent of the motor affection. Anhidrosis is still present, but with the degeneration of peripheral fibres the warm isothermia of the skin gives way to poikilothermia and later to cold isothermia (Figs. 5.75 and 5.76). As time goes by, the changes of disuse appear: thinning of the skin; even ulceration from accidental injury; loss of substance in the tips of the digits; loss of skin markings; constant coldness and cyanosis; stiffness of joints; contractures; unmistakable wasting. Nails become brittle and discoloured and are prone to infection. Hair growth is disturbed, hairs are often coarse (Figs. 5.77–5.79). These changes occur rapidly in the ischaemic limb. At a late stage in partial denervation or with incomplete recovery after a deep lesion there may be muscle spasms and spontaneous fasciculation. Prolonged denervation of a growing limb leads to defective growth: this is of course well seen after birth injury of the brachial plexus. Lewis and Pickering (1936) thought that the changes in denervated limbs were simply the result of disuse rather than that of the loss of a “trophic” function of the nerves. However, it is a fact that in cases of greatly prolonged conduction block, the changes are always far less than they are in

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Fig. 5.60  Rupture of rotator cuff with lesions of the suprascapular and circumflex nerves from fracture/dislocation of the shoulder. Above showing the range of elevation at the right shoulder in 74 year old ex-paratrooper in whom there was clear evidence of recovery for both of the nerves. Below: this shipwright held onto a cable to rescue a man from the Thames. The weight of the man and the force of the current was such that he felt the muscles tearing in his right shoulder, then he felt the head of the humerus pulling out from the socket and then his arm went dead. Mr. Sait (Dartford) confirmed rupture of the rotator cuff by MR scan. Electromyography (Dr. Cordivari, Queen Square) showed that the suprascapular nerve was intact and that there was, at 8 weeks, reinnervation of the posterior deltoid. A Tinel sign was detectable at the posterior aspect of the shoulder. A subsequent repair of the rotator cuff, performed by Mr. Sait, was successful.

Fig. 5.61  The clavicular head, 1, of pectoralis major is best examined by resisting adduction and medial rotation with the arm elevated.

Fig. 5.62  The sternal head, 1, of pectoralis major is tested with the arm in adduction.

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Fig. 5.65  Brachio radialis is a powerful flexor of the elbow. The biceps muscle and its tendon should be observed and palpated. 1. Biceps brachii, 2. Biciptal aponeurosis, 3. Medial head of triceps, 4. Brachioradialis, 5. Biceps tendon.

Fig. 5.63  Teres major, 2, and latissimus dorsi, 3, are tested by resisting adduction. The muscles are seen and palpated. The posterior deltoid, 1, is seen.

Fig. 5.64  The lateral, 1, long, 2, and medial, 3, heads of triceps are examined by observing and palpating the muscle.

degenerative lesions. We have seen that in degenerative lesions profound changes take place in both motor and sensory end-organs. The distal axon normally maintains a dense population of end-organs in skin and sweat glands and in the muscular component of arterioles. It is hard to resist the conclusion that the changes of “disuse” are at least in part due to the loss of distal axons and of their end-organs, and to the effects of that loss on superficial tissues. An extreme form of severe trophic changes in long standing “conversion paralysis” is described in Chap. 14.

Fig. 5.66  Elbow flexion. 1. Brachioradialis, 2. Brachialis, 3. Biceps, 4. Bicipital aponeurosis.

By the time the changes of degeneration are present, the patient is a better candidate for the examination halls than for restorative treatment. The object of the clinician must be to make the diagnosis before the signs of peripheral degeneration have appeared; before the best time for intervention has passed. Unfortunately, the peripheral neurologist is still likely to be presented with cases in which delay in diagnosis has permitted the development of these signs. The last are at this stage well marked; their absence in association with

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Fig. 5.67  Activity in extensor carpi radialis brevis, 1, and longus, 2, is noted by observing and palpating the muscle bellies and their tendons.

Fig. 5.69  Below: the first dorsal interosseous, 1, and adductor pollicis, 2, muscles (ulnar nerve) are examined by thumb to index pinch grip. Above: abductor pollicis brevis, 3, (median nerve) is tested by resisting abduction of the thumb at right angles to the palm of the hand.

Fig. 5.68  Flexor digitorum superficialis is examined by immobilising the other digits.

persistent partial motor and sensory paralysis almost certainly means that the lesion was partly or wholly a conduction block.

5.9.6 Signs of Reinnervation The detection of initial and continuing reinnervation is often very important in aiding a decision about intervention. After

such a procedure, it is important as an indicator of success or failure, and consequently as a guide to a second intervention. In cases in which long spatial and temporal distances separate a lesion from the nerve’s target, the Tinel sign is useful but can mislead, especially when the target tissues have been damaged by ischaemia or sepsis. After a degenerative lesion, recovery proceeds centrifugally, so that the first sign of reinnervation is voluntary contracture in the muscle most proximally innervated. Sensibility too recovers centrifugally. As Head et  al. (1905) observed, its quality improves over successive months, doubtless with re-­myelination of the larger axons Recovery of sensibility may be preceded by recovery of sweating; indeed, sweating may be restored without any later recovery of sensibility; light touch sensibility may return in the absence of nociception and sweating In non degenerative lesions, recovery is not necessarily nor even generally centrifugal: distal muscles may well recover before proximal ones; loss or alteration of sensibility may anyway be patchy; vasomotor and sudomotor paralysis is rare. Because the lesion depends so much on demyelination, and in particular on demyelination of large fibres, a dissociated loss of position sense and vibration sense may be a good indicator of its type.

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Fig. 5.71  Above: the power of the abductors of the hip is tested with the patient in a lateral position, resisting abduction on the lower limb. Below: gluteus maximus is tested with the patient prone resisting extension at the hip.

Fig. 5.70  The small muscles of the hand in lesions of the ulnar nerve. Above: “Froment’s sign” is positive in the patient’s left hand. Below: clawing is corrected by passive flexion at the metacarpophalangeal joints.

Very often, in recovery after both degenerative and nondegenerative injuries, the patient experiences radiated pain and paraesthesiae and asks the clinician whether these feelings indicate progressive recovery. We have seen that Merrington and Nathan (1949) explored the nature and origin of paraesthesiae after conduction block: certainly, such feelings indicate recovery in that condition. They do not necessarily, nor even often, have that significance in the case of degenerative lesions. Features of imperfect recovery: Imperfect recovery, common in the adult after repair of a degenerative lesion, is apparent to the patient through: (1) Weakness and sometimes wasting; (2) alteration of sensibility;(3) dysfunction; (4) (sometimes) pain; (5) (sometimes) sensitivity over the site of the lesion; (6) exaggerated reaction of the affected part to external cold; (7) stiffness and even deformity of the joints of the affected part. The exaggerated reaction to cold requires some further comment; all other aspects are treated elsewhere. Cold affects healthy nerves: it affects even more severely those in which the number of functioning axons is

reduced, So, conditions of cold which would not seriously affect healthy nerves are liable badly to affect damaged nerves in which regeneration has been imperfect. Both motor and sensory function are affected. The cold affects not only nerve function; it affects too the skin and deep tissues of the affected limb, which is quick to cool and slow to warm. Sensitivity to cold may prevent return to work in the cold room of a butcher or fishmonger, or to outdoor work with machinery, even when recovery after repair of a median nerve at the wrist has been otherwise good. The response to cold stimulus was analyzed, in normal hands, by Davis and Pope (2002). Aching pain was experienced at temperatures of 15°C or less and prickling sensations were induced by even colder stimuli. Cold related symptoms after injury to peripheral nerves seem to be an exaggeration of this response. Irwin et  al. (1997) noted immediate onset of symptoms in one-third of their patients. Symptoms had developed within 3 months in the remaining two-thirds. The problem was worse after untidy injuries and after injury to the axial artery. Kay (1985) “found no relationship between arterial inflow and cold intolerance” but there was a tendency for the symptoms to be worse with poorer nerve function. Vasospasm may contribute to the problem (Backman et al. 1993). An unpleasant sensation of intense coldness was associated with blanching or discolouration of

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injured fingers in more than 70% of the patients described by Lithell et al. (1997). Malenfant et al. (1998) studied cold intolerance in patients with burns and demonstrated changes in sensation in normal skin in the contra lateral uninjured limb.

Surgical Disorders of the Peripheral Nerves

5.10 Records Recovery after severe injuries to nerves is prolonged, and persisting pain and loss of function interfere with rehabilitation. We have developed a number of systems which record the

Fig.  5.74  The small muscles of the foot, 1. The patient is asked to “make a fist” with their toes.

Fig. 5.72  Extension of the knee. The muscle bellies of vastus medialis, rectus femoris, and vastus lateralis can be seen and felt. Note the action of the tensor fascia lata which can, in some patients, extend the knee against gravity. Note the fascia lata, 1, the vastus lateralis, 2, the rectus femoris, 3, and vastus medialis, 4.

Fig. 5.73  Eversion at the ankle. The muscle bellies of peroneus brevis, 1, and longus, 2, and their respective tendons are observed and palpated.

Fig. 5.75  Late changes after nerve injury. Severe wasting of the hand with contractures, 1 year after stab wound to the lower part of the brachial plexus.

Clinical Aspects of Nerve Injury Fig. 5.76  Late changes after nerve injury. Left: there is sympathetic paralysis and unnoted burns after high lesion of the median nerve. Right: wasting and ulceration of the skin of middle finger and accidental injury to index finger after median nerve injury. The patient was working as a stone mason.

Fig. 5.77  Post ischaemic contracture in the hand. A 63 year old man lay in a coma for 18 h. There was compression of the axillary neurovascular bundle. The range of extension (left) and of flexion (right) is shown 1 year later.

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Fig. 5.78  Post ischaemic fibrosis. The lateral geniculate artery was lacerated during arthroscopic meniscectomy. The false aneurysm which ensued remained undetected for 4 days in spite of his intense causalgia. The position of the leg, ankle and foot 3 years after injury.

progress after nerve injury, associated injuries and their consequences, and after “reconstruction” operations. Information is collected about the effects on daily life, on work or training or study. The evolution of pain, its response to treatment or to recovery is recorded. The progress for the nerve is recorded

Fig. 5.79  Late skin changes after nerve injury. Left: a skin rash in the distribution of C5, 6 months after rupture. Right: skin rash in the distribution of the common peroneal nerve 1 year after rupture at the knee.

Surgical Disorders of the Peripheral Nerves

sequentially for motor, sensory, and sympathetic function and a final grade is offered for the whole nerve. Suitably modified forms are used for injuries to the shoulder girdle and gleno-humeral joint, for injuries in the lower limb and for penetrating missile wounds (Fig. 5.80). Other forms are used for traumatic lesions of the brachial plexus (Fig. 5.81a and b). The documents used for birth lesions of the brachial plexus are illustrated in Chap. 10. These records are placed in the case notes at the patient’s first attendance, and remain there until treatment is completed. Information is transferred from the form onto appropriate data bases throughout treatment. These computerised systems certainly ease analysis but never replace the hand written entry made at every visit. All systems fail to a greater or lesser extent in (1) failing adequately to record the stamina of muscles; (2) failing adequately to record function of the sensory end-organs in muscles, tendons and particular capsules and ligaments and (3) failing adequately to record co-contraction. Co-contraction is particularly common after injuries to the brachial plexus in adults and in infants. Special apparatus is indeed available for testing stamina of muscles, in particular those of the hand. The amount of time involved is, however, too great to permit the routine use of these methods. Evidently, tests such as Moberg’s “pick-up” test to some extent examine deep as well as superficial sensibility, but there is no good measure of the extent of re-innervation of muscle spindles. The examination of tendon reflexes is, evidently, a coarse method of testing the function of the Golgi organs and muscle spindles, but more precise methods are lacking. We do not know how much the function of a muscle recovered after nerve repair is impaired by defect of input from it. It is probable that impairment of the

Clinical Aspects of Nerve Injury

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Fig. 5.80  The document used for recording data in patients with compound nerve injury.

deep afferent pathway is one factor underlying co-contraction; such impairment is certainly a major cause of the regular failure of muscle transfers using reinnervated muscles.

5.11 Aids to Diagnosis Electrophysiological examination: We owe much to our colleagues, Dr. Nicholas Murray, Dr. Shelagh Smith, and Dr. Peter Misra, Dr. Carla Cordivari and their colleagues at the National Hospital for Nervous Diseases with whom joint electrodiagnostic clinics have been held for more than

20 years. More than 1,000 patients have been seen at these clinics, which provide prompt and valuable information about diagnosis and prognosis. This collaborative approach is also useful in teaching and in training. The cases are presented by the surgeon who offers a diagnosis of the level and of the depth of lesion and of the likely prognosis. That diagnosis is then confirmed, expanded or refuted by studies of sensory and motor conduction and by electromyography of selected muscles. More than 2,000 other patients have been seen by our colleagues at the National Hospital whose work represents a contribution in the analysis of injuries of profound importance.

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Electrophysiological examination (Wynn Parry 1953, Smith 1996, 1998, 1999) is certainly the foremost aid to diagnosis, though in the acute stage the process is often hampered by pain and by local conditions. It must be done properly and results must expertly be interpreted. It is no substitute for clinical observation; it must not be used as device for deferring decision and delaying action. It can help in diagnosis of

Fig. 5.81  The document used for collecting data about patients with injuries to the brachial plexus.

Surgical Disorders of the Peripheral Nerves

the site and depth of a lesion and in the recognition and measurement of recovery. The extension of the process to the detection and measurement of potentials evoked from the cortex provides valuable evidence in the case of suspected avulsion of the roots of the brachial plexus. Perhaps the simplest, yet often neglected, technique of electrophysiological examination is that of stimulating the nerve below the level of

Clinical Aspects of Nerve Injury

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Fig. 5.81  (continued)

the lesion and observing the motor response. If, 3 days after injury, stimulation below the level of the lesion produces a normal response in the muscles supplied by the nerve, the odds are that the lesion is a conduction block. If there is no motor response or if the response is much subdued, then the lesion is degenerative. The introduction of electrophysiological process during operation has brought massive advantages, in particular in (1) determining neural continuity across a lesion in continuity;

(2) determining the site of a conduction block; (3) determining which part of a nerve has suffered axonal interruption; (4) determining whether an apparently intact component of the brachial plexus has intact central connections. We are profoundly glad that the whole matter is considered at length in the next Chapter by an expert in the field. Magnetic resonance imaging: Whilst magnetic resonance neurography is uniquely informative in the diagnosis and accurate measurement of the extent of tumors in or near

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nerves, in the more difficult entrapment syndromes, and in closed traction injuries of the brachial and lumbo-sacral plexus, the full potential of the method in the diagnosis of closed injuries to peripheral nerves has yet to be fully exploited. Ultrasonography seems more promising High resolution ultrasonography: Dr. Susan Krone (2005) (Maidstone) read an exceptional paper at the Royal National Orthopaedic Hospital in 2005 in which she outlined the application of this method for the display of major nerves and of their constituent bundles during regional anaesthesia. She pointed out that this investigation could prove valuable in the first days after closed injury before fracture haematoma is transformed into scar. Krone further suggested that the method might have a place in the examination of the neonatal brachial plexus in cases of birth lesion at a time when ossification of the cervical spine is limited. Martinoli et al. (1996) provided an important review: When examined with high-frequency probes, peripheral nerves show a peculiar arrangement of their internal structures. Using 15 MHz transducers the nerve appears to be composed of multiple hypo-echoic parallel discontinuous linear areas separated by hyper-echoic bands. The hypo-echoic areas are arranged in series and appear well defined and elongated according to the longitudinal axis of the nerve. On transverse sections, the hypoechoic areas become rounded and are embedded in a homogenous hyper-echoic background. Side by side comparison between ultrasound scans and respective histologic slides demonstrated that the hypo-echoic areas coincide with fascicles of neuronal fibres, whereas the hyper-echoic background correlates with the epineurium and passes into the spaces between the individual fascicles of nerve substance.

These workers go on to point out that the arrangement of fascicles is related to the ultrasound frequency employed. 15 MHz transducers are optimal but tissue penetration of these is poor so that their use is limited to the examination of nerves running within 2 cm from the skin surface. Deeper nerves can be examined using lower frequency probes but the fascicular pattern is less well defined with such transducers. The arrangement of bundles can be detected using a frequency as low as 7.5 MHz. Chan (2003), and Perlas and his colleagues (Perlas et al. 2003) show that the brachial plexus, in the posterior triangle of the neck, can be closely examined using high resolution ultrasonography. The potential for diagnosing nerve transection by ultrasound was examined by Cartwright et al. (2007), from the Wake Forest school of Medicine in 2007. The median, ulnar and radial nerves were transected in the arms of fresh cadavers and sham skin incisions were performed throughout the arm. The nerves were then scanned by an ultrasonographer who was unaware of the sites of transection. High resolution ultrasound was able to identify transected nerves with 89% sensitivity and 95% specificity. These workers conclude that: “this proof of concept study shows that ultrasound can accurately identify a nerve transection, which should lead to further ultrasound studies in patients with traumatic peripheral nerve injuries.” Two such studies are

Surgical Disorders of the Peripheral Nerves

provided by Cokluk and Aydin (2007 a, b) of the Department of Neurosurgery in Samsun, Turkey, who published two important papers in 2007. In all, 58 patients were examined The nerves investigated in the upper limb included the brachial plexus (4 cases) the ulnar nerve (9 cases) the radial nerve (6 cases) the median nerve (17 cases). In the lower limb, the femoral nerve(5 cases) and the sciatic nerve (17 cases) were examined. The examination was performed using a Tosbee ultrasound (Toshiba Inc., Tokyo) with a 5–7.5  MHz linear probe. The patients with injuries in the upper limb were placed supine. Ultrasound gel was plastered on the probe surface and the skin to enhance visualisation of peripheral nerves and the musculo-skeletal structures. The examination commenced about 10  cm proximal to the suspected region and continued 10  cm distally. Bone, muscles, tendons, vascular structures, and peripheral nerves were identified and distinguished. “Continuity, architecture, shape, calibration and integrity of the involved nerve and peripheral tissues were examined in the perpendicular and transverse planes.” The femoral nerve was examined with the patient supine, the sciatic nerve was examined with the patient placed prone. Sixteen of these patients were examined within 3 days of injury. In most cases the diagnosis made by ultrasound was matched with the findings at subsequent operation. The investigation proved reliable in identifying the nerve, in localising the level of injury and in the recognition of the nature of that injury. Toros et al. (2009) provide further valuable information about the technique. It seems likely that ultrasonography, in skilled hands, has enormous potential in the early detection of ruptures or other serious injuries to nerves. A number of orthopaedic and fracture surgeons are already well versed in the technique and we hope that the very real difficulty of recognition of rupture of the nerve trunk in a closed fracture will be overcome by the widespread use of this method by interested clinicians.

References Anand P, Birch R (2002) Restoration of sensory function and lack of long-term chronic pain syndromes after brachial plexus injury in human neonates. Brain 125:113–122 Anand P, Warner G, Parrett A, Terenghi G, Kopelman P, Ghatei MA, Bloom SR, Sinicropi D, Williams-Chestnut RE (1994) Nerve growth factor related small fibre dysfunction in human diabetic neuropathy. Ann Neurol 36:284A Anand P, Terenghi G, Warner G, Kopelman P, Sinicropi DV, WilliamsChestnut RE (1996) The role of nerve growth factor in human diabetic neuropathy. Nat Med 2:703–707 Atherton DD, Facer P, Roberts KM, Misra VP, Chizh BA, Bountra C, Anand P (2007) Use of the novel contact heat evoked potential stimulator (CHEPS) for the assessment of small fibre neuropathy: correlations with skin flare responses and intra-epidermal nerve fibre counts. BMC Neurol 7:21

Clinical Aspects of Nerve Injury Backman C, Nystr m A, Balkman A, Bjerle P (1993) Arterial spasticity and cold intolerance after digital replantation. J Hand Surg Br 18:551–555 Bell J, Burford W (1982) The force time relationship of clinically used sensory testing instruments. Presented at the American Society for Surgery of the Hand, 37th Annual Meeting, New Orleans Birch R (1986) Lesions of peripheral nerves: the present situation. J Bone Joint Surg Br 68:2–8 Birch R (1989) The repair of peripheral nerves: experimental and clinical observations. Thesis for the degree of Master of Surgery, University of Cambridge Birch R, Raji ARM (1991) Repair of median and ulnar nerves. J Bone Joint Surg Br 73:154–157 Bonney G (1983) Peripheral nerve lesions. In: Harris NH (ed) Clinical orthopaedics, Wright, Bristol, pp 726 Bowden REM, Scholl DA (1954) Rates of regeneration. In: Seddon HJ (ed) Peripheral nerve injuries, vol 282, Medical Research Council Special Report Series. HMSO, London, pp 16–24 Brand PW (1985) Clinical mechanics of the hand. Mosby, St. Louis, pp 61–191 Buck-Gramcko D, Lubahn JD (1993) The Hoffman-Tinel sign. J Hand Surg Br 18:800–805 Camp SJ (2010) Lesions of the spinal accessory nerve. J Bone Joint Surg (in print) Canale ST, Beaty JH, Warner WC, Sharp RS (2000) Passive flexion sign: a simple tool for diagnosis of anterior interosseous nerve injury in children. J Bone Joint Surg 82:1354–1355 Cartwright MS, Chloros GD, Walker FO, Wiesler ER, Campbell WW (2007) Diagnostic ultrasound for nerve transection. Muscle Nerve 35(6):796–799 Chan V (2003) Applying ultrasound imaging to Interscalene brachial plexus block. Reg Anesth Pain Med 28:340–343 Cokluk C, Aydin K (2007a) Ultrasound examination in the surgical treatment for upper extremity peripheral nerve injuries: part I. Turk Neurosurg 17(4):277–282 Cokluk C, Aydin K (2007b) Ultrasound examination in the surgical treatment for upper extremity peripheral nerve injuries: part II. Turk Neurosurg 17(3):197–201 Coupland RM (1993) War wounds of limbs. Butterworth Heinemann, Oxford, London Davis KD, Pope GE (2002) Noxious cold evokes multiple sensations with distinct time cause. Pain 98:179–185 Dellon AL (1978) The moving two-point discrimination test: clinical evaluation of the quickly-adapting fibre receptor system. J Hand Surg 3:474–481 Dunnet W, Housden P, Birch R (1995) Results of flexor to extensor tendon transfer. J Hand Surg Br 20(1):26–28 Dyck PJ, O’Brien PC, Johnson DM, Klein CJ, Dyck PJB (2005) Quantitative sensory testing. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier, Philadelphia Gilliatt RW, Taylor JC (1959) Electrical changes following section of the facial nerve. Proc R Soc Med 52:1080–1083 Head H, Rivers WHR, Sherren J (1905) The afferent nervous system from a new aspect. Brain 28:99–116 Henderson WR (1948) Clinical assessment of peripheral nerve injuries. Tinel’s test. Lancet 2:801–806 Highet WB (1941) Memorandum to the nerve injuries committee of the Medical Research Council and published in the Special Report Series No. 282 1954. HMSO, London Highet WB (1954) Quoted by Zachary RB. In: Seddon HJ (ed) Peripheral nerve injuries Medical Research Council Special Report Series No 282. HMSO, London, p 355 Hoffman P (1915a) Über eine Methode, den Erfolg einer Nervennant zu beurteilen. Med Klin 11:359–360 Hoffman P (1915b) Weiterres über das Verhalten frisch regenerierter Nerven über die Methode, den Erfolg einer Nervennaht Frühzeitig zu beurteilen. Med Klin 11:856–858

189 Htut M, Misra P, Anand P, Birch R, Carlstedt T (2006) Pain phenomena and sensory recovery following brachial plexus avulsion injury and surgical repair. J Hand Surg Br 31:596–605 Htut M, Misra VP, Anand P, Brich R, Carlstedt T (2007) Motor recovery and the breathing arm after brachial plexus surgical repair including re-implantation of avulsed spinal nerves into the spinal cord. J Hand Surg 32E:170–178 Inman VT, Saunders JB, Abbott LC (1944) Observation on the function of the shoulder joint. J Bone Joint Surg 26:1–31 Irwin MS, Gilbert SEA, Terenghi G, Smith RW, Green CJ (1997) Cold intolerance following peripheral nerve injury. Br J Hand Surg 22:308–316 Jerosch-Herold C (2000) Should sensory function after median nerve injury and repair be quantified using two point discrimination as a critical measure? J Plast Reconstr Surg 34:339–343 Jerosch-Herold C (2005) Assessment of sensibility after nerve injury and repair: a systematic review of evidence for validity, reliability and responsiveness of tests. J Hand Surg Br 30:252–264 Kato N, Birch R (2006) Peripheral nerve palsies associated with closed fractures and dislocations. Injury 37:507–512 Kaufmann KR (2005) Quantitative muscle strength assessment. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier, Philadelphia, pp 1095–1102 Kay S (1985) Venous occlusion plethysmography in patients with cold related symptoms after digital salvage procedures. J Hand Surg Br 10:151–154 Keogh Sir Alred (1917) Introduction to: notes on military orthopaedics (Author. Robert Jones), Cassell, London Krone S (2005) Ultrasound guided regional anaesthesia. Invited paper to advanced orthopaedic anaesthesia and critical care. Royal National Orthopaedic Hospital, Stanmore, Middlesex, 16 September 2005 Landau WM (1953) The duration of neuromuscular function after nerve section. Neurosurgery 10:64–68 Landi A, Copeland S (1979) Value of the tinel sign in brachial plexus lesions. Ann R Coll Surg Engl 61:470–471 Lewis T, Pickering GW (1936) Circulatory changes in the fingers in some diseases of the nervous system, with special reference to the digital atrophy of peripheral nerve lesions. Clin Sci 2:149–183 Lithell M, Backman C, Nystr m Å (1997) Pattern recognition in posttraumatic cold intolerance. J Hand Surg 22:783–787 MacKinnon SE, Dellon AL (1985) Two point discrimination tester. J Hand Surg Am 10:906–907 MacKinnon SE, Dellon AL (1988) Ischaemia of nerve: loss of vibration sensibility. In: Surgery of the peripheral nerve. Thieme Medical Publishers/Georg Thieme Verlag, Stuttgart, New York, p 57 Malenfant A, Forget R, Amsel R, Papillon J, Frigon J-Y, Choinière M (1998) Tactile thermal and pain sensibility in burned patients with and without chronic pain and paraesthesia problems. Pain 77: 241–251 Martinoli C, Serafini G, Bianchi S, Bertoletto M, Gandolfo N, Derchi LE (1996) Ultrasonography of peripheral nerves. J Peripher Nerv Syst 1:169–178 Merrington WR, Nathan PW (1949) A study of post-ischaemic paraesthesiae. J Neurol Neurosurg Psychiatry 12:1–18 Mills K (1997) Wasting, weakness and the MRC scale in the first dorsal interosseous muscle. J Neurol Neurosurg Psychiatry 62:541–542 Moberg E (1958) Objective methods for determining the functional value of sensibility in the hand. J Bone Joint Surg Br 40:454–476 Narakas AO (1993) Paralytic disorders of the shoulder girdle. In: Tubiana R (ed) The hand, vol. 4. Saunders, Philadelphia, pp 112–125, Chapter 9 Novak VP, Baratz ME (2006) Antero-medial ecchymosis about the elbow in an adult with a distal humerus fracture. J Hand Surg Am 31:860–862 Novak CB, MacKinnon SE (1999) Letter to editor. J Hand Surg Am 24: 869–870

190 O’Brian M (ed) (2000) Aids to the examination of the peripheral nervous system, 4th edn. Elsevier, London Oaklander AL, Rismiller JG, Gelman LB, Zheng L, Chang Y, Gott R (2006) Evidence of focal small-fibre axonal degeneration in complex regional pain syndrome-1 (reflex sympathetic dystrophy). Pain 120:235–243 Perlas A, Chan V, Simons M (2003) Brachial plexus examination and localization using ultrasound and electrical stimulation. Anaes­ thesiology 99:429–435 Perry J, Ireland ML, Gronley J, Hoffer MM (1986) Predictive value of manual muscle testing and gait analysis in normal ankles by dynamic electromyography. Foot Ankle Int 6:254 Porter RW (1966) New test for finger sensation. BMJ 2:927 Rank BK, Wakefield AR, Hueston JT (1973) Surgery of repair as applied to hand injuries, 4th edn. Churchill Livingstone, Edinburgh Riddoch G (1940) The coin test. In: Surgical disorders of the peripheral nerves (Attributed: Seddon HJ 1975), Churchill Livingstone, Edinburgh, p 53 Rosén B, Jerosch-Herold C (2000) Comparing the responsiveness over time of two tactile gnosis test: two-point discrimination and the STI test. J Hand Surg 5:114–119 Rowntree T (1949) Anomalous innervation of the hand muscles. J Bone Joint Surg Br 31:505–510 Seddon HJ (1975) Surgical disorders of the peripheral nerves, 2nd edn. Churchill Livingstone, Edinburgh, London, New York, p 177 Seddon HJ (ed) (1954) Peripheral nerve injuries. Medical Research Council Special Report Series No 282. HMSO, London Sharrard WJW (1953) Correlations between the changes in the spinal cord and muscular paralysis in poliomyelitis. Proc R Soc Lon 40:346 Smith SJM (1996) The role of neurophysiological investigation in traumatic brachial plexus injuries in adults and children. J Hand Surg Br 21:145–148

Surgical Disorders of the Peripheral Nerves Smith SJM (1998) Electrodiagnosis. In: Birch R, Bonney G, Wynn Parry C (eds) Surgical disorders of the peripheral nerves, 1st edn. Churchill Livingstone, Edinburgh, London, pp 467–490, Chapter 19 Smith SJM (1999) Neurophysiological interpretation after nerve injury in the upper limb. Curr Orthopaed 13:27–32 Smith PJ, Mott G (1986) Sensory threshold and conductance testing in nerve injuries. J Hand Surg Br 11:157–162 Stewart M, Birch R (2001) Penetrating missile injuries. J Bone Joint Surg Br 83:517–524 Szabo RM, Gelberman RH, Williamson RV, Dellon AL, Yavu NC, Dimick NP (1984) Vibratory sensory testing in acute peripheral nerve compression. J Hand Surg Am 9:104–109 Tinel J (1915) Le signe du “fourmillement” dans les lésions des nerfs periphériques. Presse Méd 47:388–399 Tinel J (1917) Nerve wounds. Ballière Tindall & Cox, London. Authorised translation by Rothwell F, revised and edited by Joll CA Toros J, Karabay N, Őzaksar K, Sugun TS, Kayalar M, Bal E (2009) Evaluation of peripheral nerves of the upper limb of the upper limb with ultrasonography. J Bone Joint Surg Br 91:762–766 Trumble TE, Kahn U, Vanderhooft E, Bach AW (1995) A technique to quantitate motor recovery following nerve grafting. J Hand Surg Am 20:367–372 von Greulich M (1976) Der zweipunkte-Stern. Handchirurgie 8:97–99 Wynn Parry CB (1953) Electrical methods in diagnosis and prognosis of peripheral nerve injuries. Brain 76:229–265 Wynn Parry CB, Salter RM (1976) Sensory re-education after median nerve lesions. Br J Hand Surg 8:250–257 Wynn Parry CB (1981) Rehabilitation of the hand, 4th edn. Butterworth, London

6

Clinical Neurophysiology in Peripheral Nerve Injuries Shelagh Smith and Ravi Knight

Development of clinical neurophysiology as a diagnostic aid, applications and purpose of clinical neurophysiology, electrodiagnostic techniques and new methodologies, limitations and caveats, safety issues.

6.1 Introduction The Clinical Neurophysiologist participates in clinical evaluation of patients with known or suspected injury to a peripheral nerve, plexus or spinal root, and the information gained from neurophysiological evaluation often contributes directly to therapeutic decision making in such patients. Conduction along sensory and motor nerve axons is essentially an electrical process, and electrophysiological methods are a premier investigation for acquired disorders of peripheral nerves. Clinical neurophysiology alone does not always provide complete diagnostic information; nerve conduction studies and electromyography should be viewed as diagnostic aids, which extend the clinical examination and support other investigative tools, as outlined in Chap. 5. Electrodiagnostic techniques verify or exclude the clinical suspicion of a neuropathological process, and can offer a precise definition of the site, type and degree of a neural lesion, or reveal abnormalities that were clinically uncertain, silent or unsuspected. Electrodiagnostic study in neural injury is principally aimed at: • • • •

Localisation of the lesion Determination of pathophysiology Establishing severity Identification of reinnervation

The action potential in the peripheral nervous system was first described in the nineteenth century by Du Bois-Reymond and Bernstein (Seyffarth 2006; Pearce 2001) and is the fundamental unit of neural activity at the cellular level. The earliest application of electrophysiology in the study of human peripheral nerve disease was the demonstration that conduction velocity is slowed in injured regenerating nerve (Hodes et al. 1948). Considerable advances occurred during the 1940s and 1950s. Simpson reported delayed conduction in the median nerve in carpal tunnel syndrome (Simpson 1956), and Dawson in London developed an averaging technique for sensory nerve

recording using superimposed photographic traces of potentials (Dawson and Scott 1949). Further work with Dawson’s averaging method was carried out by Gilliatt and Sears at the Institute of Neurology in London, who applied it to the clinical study of nerve lesions (Gilliatt and Sears 1958), and P.K. Thomas, who described abnormalities of nerve conduction in ulnar neuropathies at the elbow and in the hand. An important contribution to the understanding of the basis of nerve conduction abnormalities was the experimental work on diphtheritic neuropathy by Lambert’s group at the Mayo Clinic, which identified segmental demyelination as the cause of slow nerve conduction velocity (Kaeser and Lambert 1962). Investigation of electrical properties of muscle fibres, notably by Lord Adrian and colleagues in Cambridge during the 1920s (Adrian 1925), and later by Buchthal in Sweden, led to the introduction of electromyography into clinical practice. Buchthal’s group went on to describe the characteristics of normal motor unit potentials, and the abnormalities seen on EMG in a wide range of myopathic and neurogenic disorders in man (Buchthal et al. 1957). Following these pioneering developments, a range of techniques for clinical study of peripheral and proximal nerves has been introduced and the pathophysiological basis of nerve conduction abnormalities clarified through correlation with morphological changes seen on nerve biopsy. The diagnostic role of electrophysiological investigation is further extended through introduction of methods for evaluation of previously inaccessible parts of the nervous system, including central motor and sensory pathways, and small myelinated and unmyelinated nerve fibres.

6.2 Electrodiagnostic Techniques In the clinical setting, summated responses from supramaximal stimulation of a sensory nerve (sensory nerve action potential) and motor nerve (compound muscle action potential) are

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respectively recorded over the cutaneous course of the sensory nerve, and from the belly of the muscle, using surface electrodes applied to the skin. Needle electromyography (EMG) records electrical activity from within muscle, and describes the integrity of the motor unit – which comprises a single alpha-motor neurone and all of the muscle fibres it innervates. Action potentials of single motor and sensory nerve fibres are summated to produce compound responses or potentials. These have a triphasic character, and parameters such as amplitude, duration, latencies and conduction velocities are determined efficiently by computer software integral to modern neurophysiological equipment. Normative data are available for a range of nerves and muscles, and enable quantification of any deviation from the norm. Conventional or standard nerve conduction studies assess function and conduction in large fast conducting nerve fibres – principally the A beta nerve fibres that mediate fine touch, with velocities in the range of 40–60  m/s. Slower conducting small myelinated A-delta and unmyelinated B fibres, mediating pain and temperature sensation, with typical conduction velocities of 3–10  m/s, cannot be assessed with standard nerve conduction tests. Evaluation of small fibre function requires specialised techniques previously accessible in a few neuroscience centres, but now more widely available (detailed application of these techniques in clinical practice is further discussed in Chap. 5). Somatosensory evoked potentials are of especial value in establishing presence of a pre-ganglionic lesion, proximal to the sensory or dorsal root ganglion, through measurement of the passage of near-field potentials resulting from stimulation of a mixed nerve or dermatome, at the level of the lumbar or cervical spine, and further cranially at the somatosensory cortex. They may indicate the presence of clinically unsuspected disease, or a second level injury in the central nervous system. Case Report: A 37 year old man had sustained multiple shrapnel injuries including one penetrating the neck anteriorly, with a fragment still lodged in the spinal canal. He developed proximal weakness in the right upper limb and paraesthesia in a C5 and C6 distribution; he also complained of numbness in the left leg. The right brachial plexus was explored approximately 1 week after injury. The plexus was considered intact by direct visual inspection; the subclavian vein was repaired. The patient was referred for neurophysiological investigation because of persisting sensory symptoms and arm weakness. The nerves studied were bilateral median, ulnar and radial sensory; right median motor, right ulnar motor, bilateral musculocutaneous and axillary motor. Extensive EMG sampling was undertaken in the deltoid, infraspinatus, biceps, triceps, brachoradialis and first DIO muscles of the right arm, and in mid and lower cervical paraspinal muscles bilaterally. Lower limb SSEPs were performed with tibial nerve stimulation to evaluate sensory symptoms in the left leg. The abnormal findings were a relatively small median sensory potential from the right thumb (12  uV compared

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with 35  uV in the left arm), and evidence of denervation (large or polyphasic MUPs, reduced recruitment) in right deltoid, infraspinatus and biceps. Fibrillations were present in infraspinatus > biceps. Cervical paraspinal muscles were normal. Cortical SSEPs from the left tibial nerve were poorly formed compared with the right leg; latency was normal but amplitude was reduced. Responses from the cervical cord were normal. Neurophysiological interpretation: evidence of a partial proximal lesion of the right brachial plexus affecting the upper trunk. The SSEP findings are suggestive of an axonal lesion in somatosensory pathways between the upper cervical spine and primary sensory cortex.

6.2.1 Glossary of Electrodiagnostic Procedures Compound sensory action potential (SNAP): is recorded following synchronous stimulation of a sensory nerve, or the sensory fibres within a mixed nerve. Stimulation and recording along the course of the sensory nerve are undertaken using electrodes placed on the skin surface. Needle electrodes may be used if the nerve is relatively inaccessible or deep to the skin surface (e.g., lateral femoral cutaneous nerve). SNAP amplitudes are small, in the order of microvolts; averaging of 10–20 responses is required to optimise signal to noise ratio (Fig. 6.1). SNAP onset and peak latencies are measured as the time interval to the initial deflection, and the next positive or negative deflection. Conduction velocity is calculated by dividing latency by the distance from the stimulating cathode (Fig. 6.2). Mixed nerve action potential (NAP): is obtained by percutaneous stimulation over nerve trunk, which contains sensory as well as motor fibres, such as the median nerve from

Fig.  6.1  Median sensory action potential recording (orthodromic): stimulation of digit 2, skin recording electrodes placed over median nerve at wrist.

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Fig. 6.2  Median sensory action potential: A2 response from digit 2, A3 response from palmar stimulation (recorded on Nicolet Viking™ EMG system). Markers are set to onset and peak latency; amplitude measures are shown in far right column of numerical data.

the palm, or ulnar nerve action potential recorded from ulnar groove; evoked responses recorded over the skin surface. Amplitude of the NAP is similar to that of SNAPs. Compound muscle action potential (CMAP): is the summated response from the synchronous stimulation of motor nerve fibres evoked by per-cutaneous stimulation over the trunk of a motor nerve. The CMAP response is recorded through skin or needle electrodes placed near to the motor point of a muscle or muscle belly, with a reference electrode placed over an inactive site such as the bony point of muscle insertion (Figs. 6.3 and 6.4). CMAP responses typically have amplitude of several millivolts: they are much larger than SNAP or NAP potentials, and averaging of summated responses is generally not required. CMAP amplitude is influenced by the size, duration, and temporal dispersion of single muscle fibre action potentials, and number of functional motor units within the muscle. Amplitude measurements are made to negative peak, or peak to peak; distal latency is the time interval between stimulation of the nerve and the onset of the response. Motor conduction velocity or speed or propagation of action potential along the nerve is calculated as conduction time/conduction distance (Fig. 6.5).

Fig. 6.3  Median nerve motor study: CMAP recorded with electrodes placed over the APB muscle, with stimulation of the median nerve at the wrist above the carpal tunnel.

H reflex (after Hoffman) : a late CMAP response of consistent latency obtained by anterograde stimulation of alphamotor neurones, which activates Ia fibres innervating muscle

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Fig.  6.4  Tibial nerve motor study: CMAP recorded with electrodes placed over the adductor hallucis muscle, with stimulation of the tibial nerve trunk at the medial malleolus.

spindles forming the afferent arc of this monosynaptic reflex. H reflexes are most readily obtained from the gastrocnemiussoleus muscles; the responses are analogous to the ankle jerk, and may be useful in suspected S1 radiculopathy. F response (from foot, where first obtained): is a late CMAP response of varying latency, produced by non-synaptic, retrograde activation of the anterior horn cell by electrical stimulation of the motor nerve. Activation of different motor units, and collision of action potentials accounts for

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the variability of latency. F responses are a useful measure of conduction in proximal parts of motor nerves, which may be inaccessible to direct stimulation. Central motor conduction time (CMCT): measures the latency of the cortical motor evoked potential (MEP) to a muscle, from which is subtracted the peripheral conduction time from the anterior horn cell to the muscle. The former is usually determined by transcranial magnetic stimulation over the scalp, the latter estimated from F response latency (Figs. 6.6 and 6.7). CMCT is a particularly useful test of the gross integrity of the corticospinal or pyramidal pathway to a muscle. Tests of neuromuscular transmission: include repetitive stimulation at low (3 Hz) and high (20–50 Hz) frequencies, to assess muscle fibre fatiguability, and single fibre EMG (SFEMG). In repetitive nerve stimulation, a decrement of CMAP amplitude and area of >10% is found in disordered post-synaptic transmission, as in acquired and congenital myasthenia gravis. Disorders of neuromuscular transmission cause increased temporal variability in the firing patterns of individual muscle fibres within the same motor unit (“jitter”). This is measured using specialised single fibre EMG needles to record pairs of potentials; SFEMG is a more sensitive (95–98%) test of disordered neuromuscular transmission than repetitive stimulation (Fig. 6.8). Electrotonus: is a generic term for nerve excitability studies, which provide information about the membrane properties of the axon at the site of stimulation. In contrast to

Fig. 6.5  Normal compound muscle action potential recorded from APB. Arrow marks distal motor latency; amplitudes of the distal (wrist) and proximal (elbow) responses are measured from baseline to negative peak.

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axon reflex loop, evoking a sweat response that can be quantified (QSART). This thermoregulatory sweat test is reliable and reproducible. 3. Thermal thresholds – a psychophysical test measuring threshold for perception of temperature sensation, useful in the interrogation of small myelinated A delta (cold threshold) and unmyelinated C (heat threshold) fibre function, with the method of limits used as the most common algorithm (Fig. 6.9).

Fig. 6.6  One of the authors (RK) demonstrating transcutaneous magnetic brain stimulation to measure central motor conduction time in a normal volunteer.

conventional nerve conduction techniques, electronus determines change in membrane potential caused by activation and deactivation of electrogenic ion pumps and channels (Kiernan et al. 2000, 2001a; Nodera and Kaji 2006). Nerve excitability studies are being used to delineate patterns and mechanisms of axonal injury, although there is to date very limited application in traumatic nerve injury. Quantitative sensory testing: small nerve fibre function can be assessed using 1. Sympathetic skin response – a galvanic response of the eccrine sweat glands to electrical (sometimes other sudden noxious) stimulation, and a useful screen of integrity of the sudomotor cholinergic system. The SSR is evoked by passing a current between two points on the skin, measuring electrical skin resistance between these points. 2. Sudomotor axon reflex – post-ganglionic sudomotor cholinergic axon terminals are antidromically stimulated with iontophoresed acetylcholine. This produces orthodromic release of acetyl choline at the nerve endings through an

Sensory evoked potentials (SSEPs) – external (electrical) stimulation of a peripheral nerve trunk in upper or lower limbs evokes responses in peripheral nerve pathways and the central nervous system. Short latency somatosensory evoked potentials (SSEPs) refer to that part of the waveform that occurs within 25 ms (N20) of median nerve stimulation, and within 40–50 ms of tibial nerve stimulation (P40). The best waveform is identified with multiple scalp recordings. Bilateral stimulation, and recording over multiple sites (peripheral nerve, plexus, spinal cord, somatosensory cortex) provides internal control and helps localise the anatomical level of the lesion (Fig. 6.10). Cutaneous stimulation in various dermatomal areas produces dermatomal SEPs (DSEPs). Sensory evoked potentials are used in evaluation of spinal cord disorders and radiculopathies, and in assessment of central sensory pathways. They are not disease specific, but reduction in amplitude generally indicates axonal loss, and prolonged latencies suggest demyelinating pathology, which may be subclinical. Electromyography (EMG): the recording and analysis of spontaneous, insertional and volitional electrical activity of muscle, usually by insertion of a concentric needle electrode. (The term “EMG” is often used colloquially to refer to electrodiagnostic studies that incorporate nerve conduction, with or without electromyography and other investigative techniques. This is misleading and should be avoided. Nerve conduction studies and electromyography, whilst inter-related, are distinct procedures).

• Insertional activity: describes electrical activity generated during needle electrode insertion. • Spontaneous activity following nerve injury leading to denervation typically includes fibrillation potentials and positive sharp waves (spontaneously generated action potentials of individual muscle fibres), fasciculations (spontaneous discharges of individual motor units), and complex repetitive discharges (polyphasic action potentials of uniform morphology and frequency [5–100 Hz], with abrupt onset and offset). EMG records motor unit action potentials (MUPs), generated from single discrete motor units, these being the anatomic and functional unit of an anterior horn cell and its connections (axons, neuromuscular junction) to the level of the muscle fibres. In EMG, MUPs represent the compound

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Fig. 6.7  Motor evoked potentials in abductor digiti minimi in the right hand, transcranial magnetic stimulation applied to scalp overlying the left motor cortex. Sequential cortical evoked responses are displayed; central motor conduction time is calculated using shortest latency responses (A5 & A6).

Fig. 6.8  Compound muscle action potential (CMAPs) evoked by repetitive stimulation at 3 Hz. In this normal subject, there is no significant drop in amplitude or change in area of the evoked potentials in the eight sequential responses.

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Fig. 6.9  thermal thresholds measured in foot of subject with Fabry’s disease (Morgan et al. 1990) in which there is preferential involvement of A-delta fibres, causing elevation of threshold to cooling.

firing characteristics or recruitment and interference pattern. Recruitment refers to the successive activation of motor units following volitional muscle contraction, and interference pattern, the electrical activity recorded during maximal contraction of the muscle (Fig. 6.11). Quantitative EMG (QEMG): uses descriptive as well as automated quantitative methods such as turns/amplitude analysis, frequency analysis to describe morphology and firing characteristics of MUPs. Surface EMG: this records grouped MUPs from muscles using surface electrodes applied to the skin surface, and is useful for multi-level muscle recording in neurogenic disorders to detect fasciculations, and in the study of neurological disorders such as tremor and dystonia (movement disorders in which there is sustained focal, segmental or generalised muscle contraction or tone).

6.2.2 Intra-operative Neurophysiological Procedures

Fig. 6.10  SSEP recording, median nerve stimulation at wrist, evoked response in plexus (N9), spinal cord (N13) and sensory cortex (N20).

action potentials of muscle fibres within the recording territory of the needle electrode, and are described in terms of their duration, amplitude, number of phases, and by the

Electrophysiological monitoring is used in a wide range of surgical procedures to assist the surgeon and maximise functional return for the patient. Techniques have been developed to guide dissection, identify the region of injury, monitor function in sensory and motor nerves and pathways, and protect against iatrogenic injury. A medico-legal role is secondary to these clinical purposes. Monitoring techniques must have the fundamental ability to provide rapid and reliable information about function, at an early and reversible stage

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Fig. 6.11  Normal MUPs recorded from concentric EMG needle placed in deltoid. Upper trace shows full recruitment pattern of motor units of varying size and firing rates.

of potential neural injury. Choice of technique is determined by surgical procedure and neural structures at risk; careful planning between clinical neurophysiologist, surgeon and anaesthetist is required ahead of surgery to select the most appropriate monitoring procedure, enable correct positioning of electrodes used for recording and stimulation, and optimise anaesthesia. Inhalation anaesthetics abolish or markedly attenuate SSEPs, and full neuromuscular blockade will prevent acquisition of EMG; for monitoring of motor nerve or root function using free running or stimulated EMG, partial neuromuscular blockade (up to 75%) (Holland 1998) or short acting neuromuscular blocking agents are required. Free running and stimulated EMG: is used to monitor function in muscles innervated by specific motor nerves or motor roots considered to be at risk during surgery; needle EMG electrodes are placed into the belly of muscles to record motor unit activity evoked by neural stimulation, or to record abnormal high frequency EMG activity (neurotonic discharges) which appear when blunt trauma is applied to motor nerves (Beatty et  al. 1995). For stimulated EMG, bipolar neural stimulation is preferable, as this minimises current

spread to closely lying or adjacent nerves – particularly problematic in plexus surgery. Current spread may also occur through liquid pools in the surgical field; in this situation, hook electrodes can be used to lift the nerve clear for stimulation. EMG signals cannot be recorded during diathermy, because of high frequency artefact. Nerve action potentials: are recorded direct from a nerve to assess continuity across the site of a nerve injury or lesion. In the setting of a post-ganglionic nerve injury, the presence of a nerve action potential indicates at least several thousand intact or regenerating axons, and correlates with functional recovery (Kline and Happel 1993), potentially obviating the need for nerve graft or repair. Somatosensory, dermatomal and root evoked potentials: are used to assess afferent pathways from peripheral nerve or dermatome through plexus and dorsal columns of the spinal cord to somatosensory cortex. Intra-operative SSEPs are the most commonly used modality in spinal surgery to reduce iatrogenic neurological injury, but give limited or no information about individual roots and motor pathways. Recording electrodes may be placed epidurally, on the surface of the

Clinical Neurophysiology in Peripheral Nerve Injuries

cervical cord, or over the cortex. Predictors of post-operative deficit are a 50% reduction in SSEP amplitude; the operation should stop if this occurs, and resume only when there is recovery of the potential. Evidence that SSEP monitoring may protect against spinal cord injury is drawn principally from retrospective reviews of outcome, with and without monitoring; there are no randomised controlled trials of efficacy – such trials now viewed as being unethical. Motor evoked potentials (MEPs): are increasingly used to assess efferent motor pathways and function in corticospinal tracts during spinal surgery and neurosurgery (Sutter et  al. 2007). Current methodology includes ‘D’ wave monitoring and direct recording of EMG in individual muscles. The ‘D’ wave recorded epidurally, represents descending asynaptic volleys in the fast conducting neurones in the corticospinal tract, evoked by single pulse transcranial stimulation. Direct EMG/MUP recording requires multi-pulse stimulation, with multiple motor tracts being involved in generation of responses. Long term motor deficit has been reported to occur post-operatively when there is >50% reduction in the cord D wave in combination with bilateral loss of muscle EMG (Deletis and Sala 2007), whereas motor function was only transiently impaired following surgery in those cases showing unilateral or bilateral loss of muscle EMG, but an unchanged or lesser reduction (<50%) in D wave response (Sala et al. 2001). Additional intra-operative techniques: include cranial nerve monitoring in skull base surgery: recording of facial muscle EMG and facial nerve stimulation to evoke CMAPs; brain stem acoustic evoked responses to monitor function in the VIII cranial nerve; and free running EMG to assess function of the trigeminal nerve, spinal accessory nerve, and the cranial nerves innervating extra-ocular muscles.

6.2.3 Electrodiagnostic Techniques and Localisation Clinical neurophysiology offers a powerful menu of techniques to assess neural integrity along the entire length of peripheral and central nervous systems. Sensory nerve recording is used to determine whether a lesion lies in postganglionic or pre-ganglionic fibres; focal nerve lesions can be precisely identified by demonstration of focal conduction block and inching techniques, with stimulation of a nerve at different levels along its course, and needle EMG sampling of the muscles and myotomes it supplies. Delineation of the site of damage in the brachial plexus or lumbo-sacral plexus is established by measuring evoked responses in sensory and motor nerve branches arising from plexus elements, in combination with EMG sampling of multiple muscles. The electrodiagnostic triad of root avulsion is (1) normal SNAP (first recognised in seminal work by Bonney and Gilliat 1958) and

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a preserved histamine response (2) denervation in paraspinal muscles and (3) loss of the somatosensory evoked potential. Together with evidence of fibrillations and absence of voluntary motor unit activity in peripheral muscles supplied by the root, this localising triad is of great value in distinguishing a proximal root lesion from more distal pathology, when there is clinical suspicion of root avulsion in traumatic injuries affecting the brachial plexus. Anatomical localisation using a combination of nerve conduction studies and EMG is illustrated by the patient who presents with unilateral foot drop. Loss of the superficial peroneal SNAP and denervation in tibialis anterior, peroneus longus and peroneus tertius muscles indicates a lesion of the common peroneal nerve at the knee, and slowing of motor conduction and reduction in evoked muscle action potential (conduction block) on stimulation of the nerve as it traverses the lateral knee localises a compressive lesion to the fibula head. If there are denervation changes on EMG in short head of biceps femoris, this would signify a more proximal lesion involving the peroneal component of the sciatic nerve. A normal superficial peroneal sensory response and denervation in tibialis posterior as well as muscles in the anterior and lateral compartments of the lower leg are indicative of L5 radiculopathy.

6.3 Limitations and Pitfalls of Electrodiagnostic Investigation There are pitfalls that may trap the unwary in both the performance and interpretation of nerve conduction studies. Biological variables can affect nerve conduction, and these must be taken into account and controlled for carefully. Age is an important factor (Hyllienmark et  al. 1995): in children below the age of 5 years, conduction velocities are approximately one-third to one-half those in older children and adults, due to age related progressive myelination of peripheral nerves. Amplitudes of sensory nerve action potentials decline in the elderly; transcutaneous sural nerve responses and certain other sensory potentials may not be recordable above the age of 65 years. Normative data used in the neurophysiology laboratory must be appropriate for the age range of the patient population. Height can also affect peripheral nerve conduction velocity, more so in lower limb nerves: conduction velocity in sural, tibial and peroneal nerves is inversely correlated with height, whereas median nerve conduction velocity shows no relationship to height in normal subjects (Rivner et al. 1990). One possible explanation for the height effect is axonal size – distal segments of longer length axons have smaller diameter, less myelin and shorter inter-nodal distance. However, the most important biological variable in clinical practice is limb temperature. Skin temperature below 30°C will reduce nerve conduction velocity and enhance neuromuscular transmission

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(Denys 1991). Amplitudes of nerve action potentials are increased in cool limbs, possibly as a result of temperaturerelated lengthening of the opening time of sodium channels in the nerve membrane. It should be standard practice to measure skin temperature, and to maintain skin surface temperature above 30°C for the duration of the test. If measured, skin temperature should then be documented in the neurophysiological report. Technical factors influence nerve conduction measurement and validity of data. Waveform morphology and amplitude is dependant on the position of the indifferent or reference electrode. Stimulus artefact may affect signal quality, and limit the ability to accurately measure latency and amplitude of potentials. Normative data are referenced to maximal stimulation of nerves; insufficient or sub-maximal stimulation may result in spuriously low amplitudes or slow velocities. A nerve response that is apparently absent may be so because of erroneous placement of recording electrodes – this is particularly challenging when assessing unfamiliar nerves, notwithstanding the wealth of excellent reference texts of surface anatomy. Inaccurate measurement of nerve length, either technical or the result of incorrect assumption as to the course of a nerve, is a common source of error when calculating nerve conduction velocity – and is especially problematic in short nerve segments, such as the ulnar nerve as it circumvents the elbow through the ulnar groove. Least error will made in an ulnar nerve conduction study if the elbow is flexed to >90° for stimulation. Knowledge of normal anatomical variants or anomalous innervation is essential (Sonck et al. 1991), and some anomalies are relatively common. The Martin–Gruber anastomosis between the median and ulnar nerves in the forearm is estimated to occur in about 20% of the population. In this anastomosis, median nerve fibres leave the main nerve trunk or the anterior interosseus branch in the forearm, cross over to the ulnar nerve and terminate in intrinsic hand muscles normally supplied by the ulnar nerve. This manifests electrophysiologically as a median evoked CMAP at the wrist being larger than that evoked by stimulation at the wrist – a reversal of the usual pattern of CMAP amplitude – and/or anomalous morphology of the CMAP. A Martin-Gruber anastomosis can present diagnostic difficulties in carpal tunnel syndrome, because some median fibres will be spared from compression at the wrist, and the anatomical variant may also affect electrodiagnosis of ulnar neuropathies at the elbow, where a severe lesion may appear less so because of anomalous innervation of intrinsic hand muscles by the crossed median nerve fibres. Other anomalous innervations include the “all median” and “all ulnar” hands, variations in sensory innervation on the dorsal side of the hand, and the accessory deep peroneal nerve, a branch of the deep peroneal nerve which runs around the lateral malleolus to innervate part of the extensor digitorum muscles in the foot.

Surgical Disorders of the Peripheral Nerves

Errors can be led by the examiner, who may fail to test enough nerves for identification of a more diffuse problem such as a generalised neuropathy underlying an apparently focal entrapment, or who may omit stimulation of nerves in proximal sites for detection of high level conduction block, or who applies the wrong procedure for the clinical problem, such as standard nerve conduction studies in a patient whose clinical symptoms suggest a small fibre neuropathic process. In EMG examination of muscles, several sites must be sampled, since the recording area of a concentric needle is quite small, with the potential to miss a focal area of denervation, reinnervation or myopathic change. Reinnervation proceeds along time as well as space, and assessment of its rate and degree will require serial EMG recordings. Whilst needle EMG may confirm reinnervation, clinical return of movement across the joint may not occur as the number of reinnervated muscle fibres may not be sufficient. Unlike certain other laboratory tests which have absolute meaning if abnormal, clinical neurophysiological data must always be placed in clinical context, and numerical results should not be over-interpreted. For example, sub-clinical slowing of median nerve conduction across the wrist does not equate in itself to carpal tunnel syndrome. Over simplification of findings must be avoided: some patients will have multiple diagnoses, such as a co-existing neuropathy in a patient with obvious primary muscle disease. Crucially, the test strategy should be based on the patient’s symptoms and signs, rather than adhering to fixed protocols of investigation. An important consideration when using serial nerve conduction studies to evaluate progression of a neuropathy, or recovery of a focal nerve lesion, is inter- and intra-examiner variability. Intra-examiner consistency of results is high, whereas amplitudes of SNAPs and CMAPs can vary quite considerably when tests are performed by different examiners (Bleasel and Tuck 1991). Hence, longitudinal nerve conduction studies are best undertaken by the same examiner. Most will be gained from clinical neurophysiological testing if the questions posed by the referring clinician are specific, explicit and answerable. Referrals should be considered in terms of (1) what knowledge will be gained about the patient from the investigation (2) how and whether the result may alter management (3) the degree of urgency of the request. The latter has some practical importance in the UK where clinical neurophysiology is a relatively scarce resource. Regular collaboration and communication between clinicians and clinical neurophysiologists is highly advantageous; the joint peripheral nerve trauma clinics run between the Royal National Orthopaedic Hospitals and the Clinical Neurophysiology department at the National Hospital, Queen Square, since the mid 1980s are a testament to the clinical value of such interaction. The report of the investigation should contain numerical data for all nerves and muscles included in the test, a

Clinical Neurophysiology in Peripheral Nerve Injuries

summary of the findings, and a clinical interpretation. Styles vary according to local laboratory practice, and to some extent, automated report generating systems embedded in modern neurophysiology recording equipment.

6.4 Safety Aspects Nerve conduction studies and needle EMG are generally well tolerated, although patients will experience some discomfort from transcutaneous nerve stimulation and EMG needle insertion. Test procedures are relatively safe, being largely non-invasive (American Association of Electro­ diagnostic Medicine Professional Practice Committee 1999), but there are some risks associated with procedures (Al Shekhlee et  al. 2003). EMG can be hazardous in patients with coagulation disorders or who are taking anti-coagulants, such as warfarin, that prolong prothrombin or partial thromboplastin time. Patients on intensive care often have a higher risk of clotting disorders, or may be on high dose heparin; a clotting screen is prudent before EMG investigation is performed. Needle EMG is safe in patients on low dose aspirin. Peritonitis is a potential complication of needle examination of intercostal and abdominal muscles, and pneumothorax is a risk of needle insertion into intercostal, serratus anterior, suprapinatus and paraspinal muscles. Nerve injury may occur on needle EMG examination of gluteal muscles (sciatic), flexor pollicis longus (superficial radial), pronator quadratus (ulnar) and pronator teres (median). These hazards can be avoided by appropriate positioning of the patient and careful EMG technique. There is a small risk that the electrical field generated by nerve stimulation may alter function of implanted cardiac pacemakers and cardioverter/defibrillator devices, and cardiological advice should be obtained before proceeding. Electrodes must be placed at least 15  cm from the device; stimulus duration should be less than 0.2 ms, and repetition rate no more than 1 Hz. Repetitive nerve stimulation techniques, including those for evaluation of recovery cycles and nerve excitability should not be performed in patient with pacemakers in situ. Appropriate infection control measures are used to minimise risk of transmission of diseases such as Hepatitis B and C, HIV and transmissible spongiform encephalopathies. Infection risk is increased when performing EMG in intrinsic foot muscles in patients with peripheral vascular disease, or in limbs of patients who have undergone extensive lymph node dissection, such as in breast cancer surgery (Al Shekhlee et al. 2003), and should only be performed in such cases if the clinical value of diagnostic information obtained from EMG outweighs infection hazard.

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6.5 Pathophysiological Correlates Neurophysiological correlates of morphological and functional changes following different types of neural injury, distinction between neurapraxia, axonotmesis, neurotmesis, time course of neurophysiological changes after injury, neurophysiological markers of regeneration and reinnervation

The pathophysiological response of large fibre peripheral nerves to a wide range of injurious processes and pathologies is limited either to loss of axons or demyelination, or a combination of these two processes. The repertoire of response in small diameter unmyelinated nerve fibres is even more restricted – these will either survive or show axon loss (Table 6.1). The principal electrophysiological markers of demyelination are reduction in conduction velocity and occurrence of conduction block. Axonal loss manifests electrophysiologically as attenuation of amplitude of evoked sensory or motor response, with relatively little change in conduction velocity, unless axonal degeneration is of severe degree. Up to 30% reduction in conduction velocity may be seen in less extensive axonal atrophy, due probably to axonal shrinkage or secondary demyelination (Baba et al. 1982). Needle EMG has particular value in assessing the degree and duration of motor nerve axonal loss. Fibrillation potentials and other markers of acute denervation appear first in proximal muscles; the timing of their appearance is dependant on the distance between the site of the nerve lesion and muscle, and is also influenced to some extent by age (see later section on birth lesions of the brachial plexus). There may be an interval of up to 10–40 days before fibrillations appear, limiting the value of early EMG in assessment of axonal damage after nerve trauma, and quantification of fibrillations does not give Table 6.1  electrophysiological consequences of demyelination. Electrophysiological change Pathophysiological basis Slowing of conduction

Caused by delays in regeneration of action potentials at the nodes of Ranvier, or by a transformation of saltatory to linear conduction in a demyelinated segment (Bostock and Sears 1976)

Conduction block

Failure of transmission of action potentials

Decrement in CMAP

Impaired transmission of trains of action potentials manifest as decrement of the CMAP to repetitive stimulation at high frequencies, as a result of greater internal longitudinal resistance and unavailability of current for impulse propagation in the demyelinated segment (Davis 1972). CMAP compound muscle action potential.

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a direct measure of the degree of axonal loss. As the motor unit undergoes remodelling during denervation and reinnervation, motor unit potentials undergo morphological change from highly polyphasic, complex unstable units seen in the earlier stages to more stable, large units of longer duration that signal axonal reinnervation and re-growth.

6.5.1 Types of Nerve Lesion: the Electrophysiological Consequences In severe focal nerve injury which results in axonal damage or death, conduction failure or block occurs at the site of injury. Distal to this, axons undergo a process of Wallerian degeneration but continue to conduct impulses until axonal degeneration is sufficiently advanced to cause conduction failure. With lesser degrees of neural injury, myelinated nerve fibres may undergo focal demyelination, resulting in either conduction slowing or conduction block. Conduction slowing per se does not produce clinical symptoms, whereas the clinical effects of conduction block are similar to those of axon loss, resulting in weakness or sensory deficit. Demyelinating conduction block may co-exist with axonal degeneration, and the CMAP can aid distinction of focal demyelination causing conduction block from axonal degeneration – a near normal CMAP at 7 days after injury in a clinically weak muscle indicates that significant axonal loss or denervation has not occurred. Both conduction block and conduction failure affect amplitudes of evoked responses from motor and sensory nerves. However, in conduction block, amplitudes are affected when stimulating above or at the site of block, but not below the lesion, whereas conduction failure affects amplitudes when stimulating at any point along the nerve length, distal or proximal to the lesion. The optimal timing for neurophysiological assessment of degree and type of lesion after the initial injury is usually between days 8 and 10, but the length of the distal stump is important in determining the time course of pathophysiological change, with short distal stumps showing the earliest onset of SNAP or CMAP abnormality. In general terms, the CMAP response declines by day 3–5 after nerve injury, and is absent by day 7–9 (Chaudhry and Cornblath 1992). Changes in the sensory response tend to lag behind CMAP diminution by 2–3 days. Immediately after nerve transection, no changes are evident at the level of the neuromuscular junction and the sarcolemmal membrane. Depending upon the length of the distal stump, there is failure of neuromuscular transmission 8–20  h after nerve section (Miledi and Slater 1970). Other length dependent changes of note are a reduction in resting membrane potential and increased sensitivity to acetyl choline (denervation hypersensitivity). The latter occurs as a result of a proliferation of acetyl choline receptors at sites

Surgical Disorders of the Peripheral Nerves

other than the endplate. In motor nerves, abnormal spontaneous activity (fibrillations, sharp waves) occurs 1–4 weeks after the injury, according to distance between the site of neural injury and the motor units in the target muscle. Fibrillation potentials appear when there is spontaneous and asynchronous depolarisation of the muscle membrane. At the ultrastructual level, fibrillations are initiated at the endplates as result of increased sodium conductance, and propagate along the muscle fibre (Smith and Thesleff 1976). The intensity of fibrillation activity approximates to the severity of axonal damage, and the size of the potentials and frequency of firing diminish over time (Fig. 6.12). Nerve lesions due to compression, which are characterised by neurapraxia or axonotmesis, result in focal slowing of conduction as a consequence of localised narrowing, with nodal and paranodal demyelination. Distal to the point of compression, axonal narrowing may produce slowing along the length of the nerve. The earliest electrophysiological abnormality in compressive neuropathies producing conduction block is a significant reduction of the amplitude of the CMAP proximal to the site of the compression. If Wallerian degeneration occurs, there is disruption of axonal conduction to the muscle fibre, which then fires spontaneously, manifesting electrophysiologically as fibrillations and positive sharp waves. Compressive neuropathies can be primarily Schwann cell mediated, rather than a mild form of Wallerian degeneration. Animal studies have shown early Schwann cell apoptosis and proliferation following nerve compression, with down-regulation of myelin

25

20

15

10

5

0

1

2

3

4

5

6

7

8

9

10

Number of days after nerve injury CMAP amplitude (mV) SNAP amplitude (microvolts) Fibrillations (frequency)

Fig. 6.12  Temporal sequence of electrophysiological changes after nerve injury.

Clinical Neurophysiology in Peripheral Nerve Injuries

203

proteins, myelin associated glycoprotein in particular. Axonal integrity is generally unimpaired, allowing for local de-and remyelination, as well as axonal sprouting. Seddon in his classic review (Seddon 1943), recounts the historical classification of nerve injuries into (1) complete anatomical division, (2) a lesion in continuity, and (3) transient block. He credits Prof Henry Cohen with creation of the now standard terms of neurotmesis, where there is loss of anatomical and functional continuity, although the epineurium may be intact, axonotmesis, in which complete peripheral (Wallerian) degeneration occurs but recovery takes place because of the preservation of axon sheaths and the internal architecture, and neurapraxia, where invariably complete recovery of function occurs without peripheral degeneration. Sunderland extended classification of neural injury by emphasising histological changes that occur in a nerve trunk in his categorisation of five different types or degrees of nerve injury (Sunderland 1990). The relationship between these classification systems, and the electrophysiological changes that may be seen in different types of nerve injury, are summarised in (Table 6.2). Neurapraxia: blunt trauma or stretch produces neurapraxia, which is characterised pathologically by focal demyelination. Loss of the myelin sheath impairs the transmission of impulses by changing the biophysical properties of the paranodal and internodal membranes (Bostock and Sears 1976). There is an increase in membrane capacitance and a reduction in the transverse resistance in paranodal and internodal regions, with a resultant deficiency in the current available to depolarise the next node of Ranvier. Demyelination of the paranodal segment in particular markedly influences membrane capacitance, with exposure of the potassium channels leading to persistent hyperpolarisation. In addition, the Na+/K+ ATPase electrogenic pump further drives the membrane towards the

K+ equilibrium potential, which in turn reduces the safety factor for transmission of the action potential (Sears and Bostock 1981). Conduction block thus ensues, characterised clinically by acute weakness in the affected limb, and motor nerve conduction studies typically demonstrate a significant drop in amplitude across the demyelinated nerve segment. Early experimental work confirmed the earliest involvement of large myelinated fibres (Aguayo et al. 1971), with the most superficial fibres being most severely affected. In an animal model of traumatic conduction block in the baboon (Papio papio), in which neurapraxia was induced by pneumatic pressure, the spatial extent or length of the compressive lesion correlated directly with the severity and duration of conduction block (Ochoa et al. 1971). Since axons remain intact in a neurapraxic lesion, function is restored by focal remyelination within days to weeks. Nerve dysfunction may be even more shortlived in transient conduction block following deforming mechanical injury such as compression and traction. The contribution of vascular or ischaemic injury to conduction block was raised by Denny-Brown and others (Denny Brown and Brenner 1944), with subsequent researchers concluding that both biomechanical and vascular factors were responsible. However histological evidence from the work of Gilliatt and associates (Gilliatt 1981), in particular the finding of nodal intussusception, reinforces the role of mechanical deformation as the principal mechanism in the pathogenesis of conduction block in compressive nerve lesions. Neurophysiologically, the neurapraxic lesion manifests with a small/absent CMAP stimulating at and above the site of the lesion, whereas nerve stimulation below the lesion evokes a normal response. Focal slowing of conduction may be demonstrable across the lesion. There are similar changes in the evoked responses of sensory nerves, but demonstration of conduction block in sensory nerves is more difficult, since

Table 6.2  Nerve injury classification and their electrophysiological correlates. Classsification Seddon Sunderland Pathology

Electrophysiological Correlate

Neurapraxia

Grade 1

Myelin injury or ischaemia

Conduction block, with or without conduction slowing

Axonotmesis

Grade 2

Axon loss

Fibrillations

Stromal derangement

Mild diminution to complete absence of SNAP and CMAP responses, in proportion to degree of axonal loss

Endoneurium, perineurium and epineurium intact

± varing degrees of conduction block and slowing associated with myelin injury

Grade 3

Endoneurium disrupted

Fibrillations

Grade 4

Perineurium disrupted

Grade 5

Epineurium disrupted

Nerve distal to lesion shows normal conduction

Absent SNAP and CMAP responses Fibrillations Absent SNAP and CMAP responses Neurotmesis

Fibrillations

Absent SNAPs and CMAPs CV conduction velocity, SNAP sensory nerve action potential, CMAP compound muscle action potential.

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there is a normal drop in SNAP amplitude when the distance between recording and stimulation sites is 25  cm or more. Fibrillations and other evidence of denervation do not occur in neurapraxic injury. However, since these changes may not appear for up to 2 weeks, neurapraxic lesions cannot be conclusively distinguished from axonal degenerative lesions in the first few days after injury. The term neurapraxia, which typically guarantees rapid and complete recovery, is best reserved for those situations where electrodiagnosis has conclusively shown that demyelinating conduction block is solely responsible for the neural lesion. Axonotmesis: In axonal injuries that do not involve the supporting perineurium, the perineurial sheath provides a channel for axonal regeneration from the cell body, facilitating recovery. Although axonal function is disrupted immediately after the injury, the disconnected distal segment survives for the next 4–7 days. As Wallerian degeneration proceeds centrifugally, the distal segment becomes progressively inexcitable. Axonotmesis and neurotmesis show similar electrophysiological features in the first few days after nerve injury. Initially, the CMAP is small or absent proximal to the lesion, and normal below the site of injury, prior to Wallerian degeneration. In the second week after injury, axonotmetic lesions show progressive reduction in CMAP and SNAP amplitude distal to the site of injury, and fibrillations may appear, depending on distance between site of injury and muscle. Regeneration occurs from the intact nerve cell body, at an average rate of 1 mm/day. The extent to which recovery is possible depends on the degree of internal disorganisation within the nerve, and the distance between the lesion site and the end organs. Neurotmesis In neurotmesis, the nerve is severed or axonal disorganisation is so severe that axonal regrowth is impossible. Axons in the nerve segment below the site of injury remain viable, and therefore excitable, for a few days. If in the second week of injury, stimulation of the distal segment evokes no response, the term neurotmesis can be applied. However, even up to 2 weeks after injury, axonotmesis or lesser degrees of axonal damage cannot be reliably distinguished from neurotmesis using electrophysiologic testing. Neurotmesis is established with certainty only by direct observation of the nerve, but will be suspected in open wounds where significant axonal loss is likely to have occurred through penetrating injury. Since electrodiagnostic testing cannot reliably distinguish neurotmesis and lesser degrees of axonal injury in the first few days after nerve injury, early surgical exploration is recommended if there is suspicion that the nerve is transected or fully sectioned. However early (day 2–3) EMG examination is advocated in the context of iatrogenous nerve injury, since demonstration of even a few volitional motor unit action potentials is evidence for neural continuity although this may not be clinically apparent (Aminoff 2004). Demonstration of conduction across the site of the nerve injury using direct nerve stimulation is also valuable in this situation.

Surgical Disorders of the Peripheral Nerves

6.5.1.1 Special Types of Neural Injury Cold thermal nerve injury: significant nerve injury is found at temperatures below 10°C. Action potentials are preserved between 5°C and 15°C (Paintal 1965). Depending upon the degree of cooling and the duration of exposure, the continuum of pathology includes mild reversible conduction block at the milder end, and axonal swelling and Wallerian degeneration at the severe extremity. The epineurium and perineurium are relatively resistant to injury and are therefore preserved (Denny-Brown et al. 1945). Electrophysiologically, there is an increase in the nerve action potential amplitude and duration (area under the curve) initially, with significant reduction of amplitude and area beginning at 16°C. The temperature is independent of nerve diameter, but lower in unmyelinated nerve fibres (Franz and Iggo 1968). There is also a reduction in conduction velocity, likely related to altered function at the sodium channels (Kiernan et al. 2001b), although experimental studies on rat sciatic nerve suggest that passive properties of the axon may contribute to the reduction in conduction velocity seen at low temperatures (Stecker and Baylor 2009). In the clinical situation, trench foot caused by non-freezing cold, is a typical example of cold induced nerve injury. Although the literature is scarce, case reports suggest damage to myelinated and unmyelinated nerve fibres, with ischaemia and reperfusion contributing to the injury (Irwin et al. 1997). Electrical neural injury: these represent 3–6% of admissions to burns units (Sances et al. 1979). The mechanism of injury is somewhat contentious, although generated heat is generally regarded as being the principal causative agent (Lee and Astumian 1996). Electroporation, a transient opening of ion channels in the cell membrane and ion fluxes leading to cell death, is sometimes invoked as a mechanism in tissue injury (Jellinek 1960). A direct correlation between the strength of current and duration of exposure, with a critical level of irreversible injury (30 mA/3 mm nerve diameter/5 s shock) was noted in experimental studies (Alexander 1941), but scarring and concomitant vascular injury significantly influence the severity and ultimate outcome of neural injury. Nerve injuries may be caused by direct heat (contact burn), and range in severity from reversible conduction block to severe axonal loss. Typically, isolated or multiple mononeuropathies in the vicinity of the electrical discharge occur acutely in about a third of electrical injuries (Duncan 2001) although delayed motor neuronopathies, suggesting involvement of the anterior spinal cord have been described (Ratnayake et  al. 1996; Fu et al. 2008), and may relate to ischaemia of the anterior spinal artery (Ko et al. 2004). Radiation injury to nerves: ionising radiation as a cause of extrinsic nerve damage has been recognised for several decades. The pattern of the response is independent of the type of ionising radiation, and shows an initial period of enhanced activity, reflected in increased conduction velocity

Clinical Neurophysiology in Peripheral Nerve Injuries

and spike amplitude, and reduction in threshold, likely caused by a physico-chemical change in the nerve membrane itself. There is then progressive decline of activity, with the greatest vulnerability seen in small diameter sensory fibres. The total dose of irradiation, rather than the frequency, determines the severity of damage, which may range from myelin fragmentation to Wallerian degeneration (Love 1983). Secondary neural damage is caused by fibrotic and ischaemic change. The most common clinical situation is iatropathic, with brachial and lumbosacral plexus lesions following radiotherapy for adenocarcinomas of the breast, ovary, and lymphomas accounting for most cases. Rare mononeuropathies of the sciatic and femoral nerve have been described (Gikas et al. 2008). Radiation induced brachial plexopathy is more common in younger patients and in those receiving concomitant chemotherapy, and is directly correlated with fraction size, with >2 Gy doses producing more extensive and severe lesions (Olsen et al. 1993). Sensory disturbance is universal. Electromyography is useful in differentiating neoplastic from radiation plexopathy, as myokymias and fasciculations are characteristic of the latter (Lederman and Wilbourn 1984).

6.5.2 Regeneration and Reinnervation Rates of axon regeneration appear to be similar in all somatic nerve fibres (Sunderland 1991). The rate of maturation correlates inversely with nerve thickness, and is influenced by local factors such as level, duration and severity of the lesion, as well as systemic factors such as age and temperature. Nerve repair occurs by two processes – axonal sprouting, with new growth of axons making functional contact with end organs or muscle fibres, and axonal regeneration along the nerve fibres. Histologically, nodal sprouting from the nodes of Ranvier, as well as terminal sprouting from intact nerve terminals, can be identified (Edds 1949). Nodal sprouting is principally determined by the distance between the node and the endplate zone, through the vacant perineurial sheath (Hoffman 1950; Slack and Williams 1981). Factors influencing nodal sprouting include age, type of injury (crush versus complete section), and type of muscle fibre (fast versus slow twitch). When nerve injury is complete, recovery can only take place through axonal regeneration, and reliable electrophysiological monitoring of motor nerve axonal growth is difficult until neuromuscular junctions begin to be reestablished. Reinnervation is heralded by reduction in the amount of fibrillations and other spontaneous activity in a muscle, but this is not easily quantified. The earliest definite electrophysiological evidence of reinnervation is recruitment of a few small unstable MUPs on volitional effort, or evoked by stimulation of the motor nerve distal to the site of injury (nascent units) (Table 6.3).

205 Table  6.3  Electromyography (EMG) findings in denervation and reinnervation. Denervation

Reinnervation

Spontaneous activity – fibrillations, positive sharp waves in acute denervation; fasciculations and complex repetitive discharges in chronic denervation Early

Normal MUPs with increased duration because of late potentials or satellite fibres incorporated through collateral sprouting

On-going

Moderate amplitude polyphasic MUPs of long duration, unstable firing due to variable conduction along unmyelinated sprouts and low safety margin of neuromuscular transmission

Late

Large amplitude increased duration MUPs with stable transmission

MUP motor unit potential.

Immature nerves are typically relatively inexcitable and require higher levels of stimulus intensity to evoke a response. Regenerating nerves also show slower conduction speeds, before remyelination is complete, which manifests as slow velocity and increased distal motor latencies. As maturation and regeneration proceeds, the number of MUPs and size of evoked CMAP increases. On needle EMG, MUPs show increased duration reflecting the enlarged motor unit, and increased polyphasia reflecting reinnervation and increased temporal dispersion of the individual muscle fibre potentials. Recruitment is reduced, and MUP firing rates increase disproportionately in relation to the number of motor units activated. Evidence of recovery of sensory nerves is usually found around the same time as the small unstable MUPs begin to be detected. Regenerating sensory potentials are initially low amplitude and often show dispersion. Recordable nerve action potential responses indicate the presence of at least several thousand moderate-diameter regenerating fibres, and this number of fibres correlates with clinical recovery of injured nerves in experimental animal models (Kline and DeJonge 1968). Whilst clinical tests such as an advancing Hoffman-Tinel sign provide useful indication of recovery in sensory nerves, quantitative sensory tests can help to establish the degree and type of small fibre involvement, although agreement between the two methods may not be evident (Leffler and Hansson 2008). In partial nerve injury, recovery incorporates regeneration of severely affected axons, and reinnervation through collateral sprouting from nerve fibres spared by the injury. Collateral reinnervation usually precedes axonal regeneration, and results in motor units that have increased amplitude, fibre density, territory and duration. The degree of motor axon regeneration may be quantifiable through measures such as automated analysis of MUP shape and firing

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rates (Dorfman et al. 1989), estimation of motor unit number (McMomas et al. 1971) and estimation of axon number by approximation of conduction velocity (Dorfman 1984). Electrophysiological evaluation can play only a very limited role in the early stages of neural regeneration, before sensory or muscle end organs are reinnervated – although this is arguably the stage at which assessment of potential for recovery would be most valuable for the clinician. Even the detection of a few motor units in previously paralyzed muscles does not necessarily imply that recovery will be complete enough to result in return of useful clinical function.

6.6 Clinical Applications Neurophysiological findings in focal nerve lesions of the upper and lower limbs, plexopathies, radiculopathies, diffuse or multilevel disorders; clinical applications and uses of specific electrodiagnostic techniques

6.6.1 Upper Limb Neuropathies 6.6.1.1 Median Nerve Median neuropathy at the wrist Carpal tunnel syndrome, with a corrected average annual incidence of 60–120/100,000 is probably the commonest surgical referral to the neurophysiology department. Dysfunction of the median nerve is caused by increased pressure between the flexor retinaculum and the floor of the carpal tunnel. Clinical symptomatology includes weakness in the hand, and sensory disturbance that may involve the forearm and upper arm, as well as the hand, with nocturnal and positional provocation of sensory symptoms as well recognised features. There is a bimodal distribution of frequency with a peak at 50–59 years, and another at 75–84 years. Aetiology is multifactorial, with factors such as age, sex, body mass index (BMI) and pregnancy, as well as diseases such as diabetes and rheumatoid arthritis contributing to the disorder (Bland 2005; Becker et al. 2002). Some controversy surrounds the aetio-pathogenesis of the nerve damage, with both deranged myelination and ischaemic axonal injury invoked as primary mechanisms (Kiernan et al. 1999). Correlation of clinical severity with degree of neurophysiological abnormality has been validated in several studies. Bland, using one of the largest databases of 8,501 patients with carpal tunnel syndrome, has demonstrated a strong linear correlation of clinical with neurophysiological severity using a 7 point scoring system of electro physiological abnormality (Bland 2000) (Table 6.4).

Surgical Disorders of the Peripheral Nerves Table 6.4  Neurophysiological grading of median nerve compression in carpal tunnel syndrome, Canterbury system (Adapted from Bland 2000). Grade Degree of Neurophysiological abnormality severity 0

Nil

Nil

1

Very mild CTS

Abnormality detected only in two sensitive tests (e.g., inching, palm-wrist median/ulnar comparison, ring finger “double peak”)

2

Mild CTS

Orthodromic sensory conduction velocity from index finger to wrist < 40 m/s with motor terminal latency from wrist to abductor pollicis brevis [APB] < 4.5 ms

3

Moderately severe CTS

Motor terminal latency > 4.5 ms and < 6.5 ms; preserved index finger SNAP

4

Severe CTS

Motor terminal latency > 4.5 ms and < 6.5 ms, with absent SNAP

5

Very severe CTS

Motor terminal latency > 6.5 ms

6

Extremely severe CTS

Surface motor potential from APB < 0.2 mV, peak-to-peak

Median and sensory nerve conduction studies (NCS) provide accurate and reproducible measures that allow diagnosis or confirmation of carpal tunnel syndrome with a high degree of sensitivity (66–82%) and specificity (82–97%) (Jablecki et al. 2002). Using a clinical questionnaire as a criterion standard, standard electrophysiological tests have moderate sensitivity and specificity, with ulnar-median sensory latency comparison having the highest diagnostic accuracy. Electrodiagnostic yield is increased by combining standard NCS with additional sensory and motor nerve tests (Chang et  al. 2002), including short nerve segment testing such as palm-wrist sensory conduction (Mills 1985), comparison of conduction measures in the median nerve with those in other unaffected nerves, such as the ulnar or radial nerve, second lumbrical/first dorsal interosseus motor latency comparison (Walters and Murray 2001) and median terminal latency comparison (Lee et al. 2009). The clinical value of new electrodiagnostic methods, which bring very small incremental improvement in diagnostic yield, may be debatable: additional new tests must be robust and efficient in application, with no undue prolongation of overall procedure time for quality of information gained. The British Society for Clinical Neurophysiology has developed good practice guidelines for electrodiagnostic verification of suspected carpal tunnel syndrome, that are suitable for multi-disciplinary use (www.BSCN.org.uk) (Table 6.5). Needle EMG of abductor pollicus brevis is indicated in suspected carpal tunnel syndrome when there is clinically

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Table  6.5  Standards, guidelines and options for electrodiagnostic procedures in suspected carpal tunnel syndrome (Adapted from practice guidelines published by the British Society for Clinical Neurophysiology, www.BSCN.org.uk). Neurophysiological test Additional procedure Standards

Hand temperature is measured and maintained above 30°C

Report includes numerical data and statement of abnormality detected

SNC in median digital sensory nerve in most affected hand using surface electrodes, and measuring response amp. & latency/velocity

Professional status of practitioner performing the investigation and report is identified

Comparative test of conduction in a digital nerve not innervated by the median nerve is performed in the same hand

The report is signed by the person taking medico-legal responsibility for it

Median MNC across wrist is measured in affected hand, using surface electrode and measuring response amp. & latency/velocity Guidelines

Digital SNC is performed in the contra-lateral hand

Referrals are screened to assess appropriateness

A second test of median SNC performed. This may include: median palmar sensory study; median/ulnar palmar ratio; median/radial sensory latency comparison to thumb; median/ulnar sensory latency comparison to ring finger

Clinical history and examination performed to identify co-existing disease

MNC in the ulnar nerve is performed in the affected limb using surface electrodes and measuring response ampl. & latency/conduction velocity Median MNC is performed in the contra-lateral limb Options

A second test of median MNC is performed, such as median/ulnar motor latency comparison to second lumbrical and second interosseous

The report contains illustrations of recorded waveforms

Needle EMG recording of median innervated arm muscles is performed by a medically qualified practitioner. This may include recording of the abductor pollicis brevis CMAP during median nerve stimulation, but not as a substitute for MNC measured as per standard above F wave latencies are recorded SNC sensory nerve conduction, ampl amplitude, MNC motor nerve conduction, EMG electromyography, CMAP compound muscle action potential.

evident muscle wasting, or carpal tunnel syndrome graded as severe or above, and in acute presentation of traumatic/atraumatic median nerve compression to detect axonal damage. More extensive nerve and muscle testing will be required if there is suspicion of co-existing disease, or disorders encompassing mononeuritis multiplex and generalised polyneuropathy to motor radiculopathy and anterior horn cell disease. Whilst symptoms usually begin and are more severe in the dominant hand, population based studies have demonstrated bilateral electrophysiological abnormalities in over half of the sample surveyed (Bland and Rudolfer 2003). The incidence of bilateral carpal tunnel syndrome rises to 87% in a hospital based prospective series (Padua et  al. 1998) and underlines the importance of examining both hands. The degree of conduction abnormality seen pre-operatively is some guide to the rate and amount of recovery of neural function following surgery. When pre-operative nerve conduction studies demonstrate conduction block as the predominant abnormality, full and rapid response to carpal tunnel decompression is expected. Recovery will be slower if axonal damage has intervened, and probably incomplete. Goodman and Gilliat’s studies of the effect of treatment in what was

then characterised as severe carpal tunnel syndrome (distal motor latency to abductor pollicis brevis >10 ms) showed that median motor latency took up to 18 months to recover, and residual abnormalities were common. In their cases deemed moderate, with latency of 7–10  ms, motor conduction took 8–12 months to recover; mild cases (latency <5 ms) recovered within 6 months (Goodman and Gilliatt 1961). Sensitive techniques such as analysis of stimulus response curves show transient reduction in amplitude of the CMAP as well as the input-output curve at approximately 1 month after surgical decompression (Ginanneschi et al. 2008) . These parameters were significantly improved at 6 months, drawing attention to the early apparent electrophysiological deterioration, likely caused by impaired efficiency of axonal recruitment immediately following surgery. High median neuropathies: These unusual lesions occur at the level of the shoulder, elbow or within the forearm, with direct trauma accounting for the majority of cases. Extrinsic compression, such as caused by axillary crutches, may also produce a high median neuropathy, in isolation or combination with radial and ulnar neuropathies. A lesion of the median nerve in the shoulder region is associated with

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weakness of forearm pronation and wrist flexion, and flexion of the lateral two digits. Flexor digitorum superficialis involvement also produces weakness of flexion involving the proximal interphalangeal joint of the ring and little fingers. Sensory loss involves the thenar eminence and the thumb, index and the lateral side of ring finger. At the elbow, the nerve may be compressed at three discrete sites: proximally by an aberrant ligament of Struther’s above the medial epicondyle, at or just below the elbow by the pronator teres muscle, or more distally when the trunk continues in the forearm as the anterior interosseous nerve. A distinct pronator syndrome was described by Seyffarth in 1951, where compression is attributable to the lacertus fibrosus, a hypertrophied pronator teres, or a fibrous band of the flexor digitorum superficialis (Seyffarth 1951). Proximal median entrapment neuropathies may mimic symptoms of carpal tunnel syndrome (Lee and Lastayo 2004), or produce nonspecific pain and sensory disturbance in the forearm, provoked by repetitive forearm movement. Needle EMG sampling is the single most useful electrophysiogical examination in high median neuropathies, as sensory and motor studies in the hand do not discriminate between distal and proximal nerve lesions. Electromyography also helps exclude differential diagnoses that include cervical radiculopathy and anterior horn cell disease. Case Report: This 25-year old serving soldier suffered open fractures of his left radius and ulna upon exposure to 105  mm artillery round (shrapnel): multiple entry wounds were seen over the dorsal and volar surfaces of the forearm. He underwent fasciotomies and a left sural cable graft to the median nerve in the forearm within the first week of his injuries. Post-operatively, extensive soft tissue scarring made clinical assessment of muscle function difficult. There was no discernible movement in thenar muscles. The patient was thus referred for neurophysiological assessment, to evaluate post-operative neural continuity, and reinnervation of more distal muscles. Electrophysiology, by short segment inching stimulation studies along the median nerve below the elbow to the level of flexor pollicis evoked low amplitude CMAPs from APB. EMG examination of APB and FPL revealed nascent type unstable motor unit potentials, indicative of axonal regeneration and functional continuity of the nerve 4 months after surgical repair. It was possible to offer a favorable prognosis for recovery (Fig. 6.13). Anterior interosseous nerve syndrome: This purely motor branch arises about 5 cm distal to the lateral epicondyle, and innervates the flexor pollicis longus, flexor digitorum superficialis to the index and middle finger and pronator quadratus. Isolated lesions are associated with trauma, and occur as a feature of brachial neuritis. Whilst needle EMG sampling remains the electrodiagnostic investigation of choice, distal latency to the pronator quadratus muscle may show prolongation, and is a useful adjunct (Nakano 1977).

Surgical Disorders of the Peripheral Nerves

Fig.  6.13  Post-operative appearance of forearm in case 2, following fasciotomy and sural cable graft to median nerve.

6.6.1.2 Ulnar Nerve Ulnar neuropathy at the elbow: Simpson in 1956 was the first to demonstrate the utility of nerve conduction studies in the localisation of ulnar neuropathy at the elbow (Simpson 1956). The importance of electrophysiology in localisation of the nerve lesion is underscored by a recent study reporting poor sensitivity (28–60%) and specificity (53–80%) of the clinical utility of provocative tests such as Tinel’s sign in the diagnosis of ulnar entrapment neuropathies at the elbow (Beekman et al. 2004). A standard ulnar nerve electrodiagnostic study should include recording of an ulnar digital SNAP, ulnar NAP at elbow, CMAP from an ulnar-innervated hand muscle, ulnar nerve conduction velocity measured elbow to wrist, above elbow to wrist, and above elbow to below elbow, and needle EMG examination of the first dorsal interosseous (the most frequently abnormal muscle, Stewart 1987) and ulnar innervated forearm flexor muscles. Ulnar nerve conduction studies have been beset by controversy regarding the optimal elbow position in which to test the nerve, given the discrepancy between true length of the nerve and measured skin distance in different elbow positions, potentially resulting in spuriously slow conduction around the elbow. The recommended elbow position is flexion between 70° and 90° from horizontal, as this minimises errors in measurement of nerve length (Campbell et al. 1999). Nerve conduction studies can localise a lesion to the elbow either by demonstration of slowing of the conduction velocity in the across-elbow segment compared to normal, or slowing of conduction in the elbow segment in relation to the below elbow to wrist segment. Published practice parameters (Campbell et al. 1999) recommend an across elbow conduction velocity of less than 50  m/s, or slowing of more than 10  m/s in the above elbow to below elbow segment compared to the below elbow to wrist segment as being indicative of abnormal conduction. A reduction in CMAP amplitude of more than 20% or a clear change in compound muscle

Clinical Neurophysiology in Peripheral Nerve Injuries

action potential morphology between the below elbow and above elbow sites are also suggestive of ulnar neuropathy at the elbow. Electrodiagnosis in mild lesions of the ulnar nerve, manifesting with sensory symptoms alone, can be difficult as nerve conduction studies are often normal or equivocal in these cases. Abnormalities of the ulnar sensory potential are sensitive for detection of ulnar nerve pathology, but do not usually help to localise the lesion. Motor studies have been shown to be more sensitive than the ulnar mixed sensory study across the elbow in localising ulnar neuropathy of the elbow (Kothari et al. 1998a). Considerable methodological variability contributes to the wide confidence intervals of electrodiagnostic accuracy in different published studies, but overall, the literature reports sensitivities of 25–100% for slowing of motor conduction, and up to 68% for conduction block. If routine motor studies recording from adductor digiti minimi are inconclusive, conduction studies should then be made using the first dorsal interosseus muscle, or vice versa, as nerve fibre bundles to individual muscles may be differentially affected in compressive lesions of the ulnar nerve at the elbow. Peripheral nerves have a

209

complex internal arrangement, comprising fascicles in which nerve fibres bound for a particular target are organised together. In a partial nerve lesion, fascicular involvement will be determined by proximity of a specific fascicle to the injurious lesion. Short segment conduction studies (“inching”) significantly increase detection of ulnar nerve lesions at the elbow (Gooch et al. 2003), and may also provide precise localisation, such as to the cubital tunnel region where the nerve is vulnerable to compression by the fascia connecting the two heads of the flexor carpi ulnaris muscle. The technique of inching involves movement of the stimulating electrode over small distances, looking for abrupt change in CMAP amplitude, morphology or latency (Campbell and Geiringer 1998); it can be utilised for the localisation of many focal neuropathies in upper and lower limbs. Whilst the typical electrophysiological findings in ulnar neuropathy at the elbow are attenuation or loss of the ulnar digital sensory response, and conduction slowing around the elbow, other features of demyelination, such as temporal dispersion and conduction block may also be present (Figs. 6.14–6.16).

Fig. 6.14  Slowing of the evoked motor response from adductor digiti minimi, maximal across the elbow.

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Surgical Disorders of the Peripheral Nerves

Fig. 6.15  Temporal dispersion of the compound muscle action potential (CMAP) from first dorsal interosseous at the elbow.

Intra-operative electroneurography at the time of ulnar nerve exploration can assist precise localisation of the site of ulnar nerve compression – Campbell and colleagues have employed peri-operative stimulation for this purpose, and to identify residual compression in patients undergoing reexploration (Campbell et al. 1988). In addition to defining the level of the lesion, electrodiagnosis can help determine prognosis. Electrodiagnostic signs of demyelination – presence of motor conduction block and motor velocity slowing across the elbow – were found to be associated with better outcome, independent of other factors in 74 ulnar neuropathies at the elbow (Beekman et al. 2004). In a recent review of a large series (n = 244 arms) of ulnar neuropathy at the elbow, severe motor conduction block signified by conduction block of greater than 50% was associated with a more favorable long term prognosis as assessed by clinical examination and patient assessment at a median follow up period of 25 months (Dunselman and Visser 2008). In those with severe motor conduction block, outcome as assessed by clinical examination was good in 81%, and 84% when judged by patient assessment. These outcomes were significantly better than those in the patient group showing motor conduction block of 20% or less (44% and 41% respectively).

As with other apparent mononeuropathies, an underlying or predisposing neuropathy may be present in patients with ulnar nerve lesions at the elbow, and electrodiagnostic assessment should include examination of at least one other upper limb nerve. If denervation in hand muscles is found in suspected ulnar neuropathy at the elbow, needle EMG should be performed in non-ulnar muscles innervated by the C8 root, medial cord and lower trunk, to exclude brachial plexopathy or a radicular lesion. Lesions of the ulnar nerve in the upper arm above the elbow such as due to compression by the arcade of Struthers or external compression in the axilla by arm crutches are difficult to distinguish reliably from more distal lesions using EMG. In these cases, percutaneous serial short segment stimulation or inching studies may help in localisation through demonstration of highly focal conduction block or other CMAP abnormality. Distal ulnar nerve lesions: Ulnar nerve lesions at or below the wrist are relatively uncommon; the clinical neurophysiologist is most likely to encounter a distal lesion in Guyon’s canal, or a lesion of the deep palmar branch to first dorsal interosseus. Distal ulnar neuropathies can manifest with a pure motor, pure sensory or mixed clinical picture, according

Clinical Neurophysiology in Peripheral Nerve Injuries

211

Fig. 6.16  Conduction block below the elbow, with significant (>50%) drop in amplitude in the proximal segment.

to whether the lesion is sited in the main nerve trunk, sensory branch or deep motor branches. Wu and colleagues have developed a precise classification of distal ulnar lesion, by categorising 55 published cases of ulnar neuropathy at the wrist into five groups according to clinical and anatomic presentation (Wu et al 1985). The type I lesion (commonest) is proximal to or within Guyon’s canal, involves both the superficial and deep branches, and causes mixed motor and sensory deficit. The neurophysiological findings will be reduction or loss of the ulnar digital SNAP, denervation of all ulnar innervated hand muscles, and abnormalities of conduction dependant on degree of demyelination and axonal damage in the nerve. The dorsal ulnar cutaneous branch, which exits the main trunk of the ulnar above the wrist, is spared, and this SNAP is a useful discriminator between distal ulnar neuropathy and ulnar nerve lesions at the elbow. The type II lesion, usually located in Guyon’s canal or in the palmaris brevis, involves the superficial branch and will manifest neurophyiologically with a small or absent ulnar digital SNAP. Types III through V are pure motor syndromes. Type III is caused by a lesion proximal to the branch to the hypothenar muscles, and causes global ulnar hand weakness. Type IV is caused by a lesion distal to the hypothenar branches, resulting in

weakness of all muscles except the hypothenars. Type V (least common) is caused by a lesion just proximal to the termination of the palmar branch, and produces weakness limited to the first dorsal interosseous and adductor pollicis, sparing other interossei and the ulnar innervated lumbricals. Neurophysiological findings in the pure motor types are typically denervation in relevant ulnar hand muscles. Needle EMG examination of palmaris brevis, innervated by the superficial branch of the ulnar nerve arising near Guyon’s canal, is helpful, as this muscle is spared in deep motor branch lesions (Iyer 1998). When the lesion is primarily compressive, such as in damage to the deep branch of ulnar in keen cyclists, there may be prolongation of distal motor latency to first dorsal interosseus (Ebeling et al. 1960).

6.6.1.3 Radial Nerve The radial nerve can be compressed or damaged in the upper arm, or around the elbow; occasionally a lesion may affect the superficial sensory branch in the forearm or at the wrist. Radial or posterior interosseus nerve involvement occurs in multifocal motor neuropathy with conduction

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block, and the radial nerve is also selectively affected in leprosy and lead poisoning. A frequently encountered radial neuropathy is “Saturday night palsy,” when the nerve is compressed against the humeral shaft within the spiral groove of the humerus bone. Although the lesion is primarily neurapraxic in type (Watson and Brown 1993), additional mild denervation is often seen on EMG in extensor digitorum communis, extensor pollicis longus, supinator and extensor carpi radialis. The lateral head of triceps may also be involved, depending on the exact point of nerve compression. It is sometimes possible to locate the site of conduction block in the upper arm by measuring CMAPs from extensor pollicis longus or extensor indicis proprius, stimulating the radial nerve above and below the spiral groove. Recovery may be protracted and eventually incomplete if amplitudes of the radial SAP and CMAPs from radially innervated muscles are reduced by more than 50% distal to the site of compression (Watson and Brown 1993). Lesions of the C7 root, or a brachial plexopathy involving middle trunk or posterior cord, are the main differential diagnoses in suspected lesions of the radial nerve above the elbow, and electrodiagnostic assessment should include needle EMG of other muscles innervated by the C7 root (serratus anterior, latissimus dorsi, lower cervical paraspinal muscles). Posterior cutaneous sensory conduction studies may confirm a postganglionic C7 lesion localisation or exclude a posterior interosseous neuropathy; when abnormal, they may predict a poor outcome (Lo et al. 2004). Pure lesions of the superficial radial nerve are rare, and then usually due to direct compression such as from handcuffs, tight casts or a watch band, or a superficial radial neuritis (Wartenberg syndrome). Symptoms can be misleading, and some cases are misdiagnosed as tenosynovitis in the wrist. Diagnosis is established by showing an abnormal superficial radial sensory potential, typically a reduction in amplitude and perhaps slowing of sensory conduction, in comparison with the unaffected arm or the lateral antebrachial cutaneous nerve on the same side (Spindler and Dellon 1990). Posterior interosseus neuropathy. This motor branch of the radial nerve exits the main trunk just below the elbow, to enter the supinator muscle under the arcade of Frohse. Compression at the arcade or within the supinator muscle will result in wrist and finger drop, but weakness of wrist extension is partial due to sparing of extensor carpi radialis. Nerve conduction studies in posterior interosseous neuropathy are of limited use (Fisher 1993). Denervation on EMG may be seen in muscles innervated by the posterior interosseus nerve; normal EMG findings in supinator, extensor carpi radialis and other proximal muscles distinguishes a posterior interosseus neuropathy from a high radial nerve lesion. The superficial radial sensory response is unaffected, or shows minimal reduction in amplitude. Conduction block or focal

Surgical Disorders of the Peripheral Nerves

slowing in the region of the arcade of Frohse may be demonstrable in neurapraxic posterior interosseus lesions, but is technically difficult. A radial or posterior interosseus neuropathy is sometimes considered in patients with treatment resistant “tennis elbow” or pain on repeated supination/ pronation of the elbow – and often classified as “radial tunnel syndrome.” Variable neurophysiological abnormalities have been reported in such cases. A series of 28 patients found that routine radial motor conduction studies were of no value, but an increase in motor latency of more than 0.5  ms was seen when conduction studies were repeated during forced supination of the arm. Inconclusive abnormalities were found on EMG of muscles innervated by the posterior interosseus nerve (Rosen and Werner 1980). Whether these cases represent a true compression neuropathy is uncertain.

6.6.1.4 Suprascapular Nerve Suprascapular nerve entrapment should be considered in patients with unexplained shoulder pain or weakness. The nerve is most commonly compressed within the suprascapular notch, resulting in denervation of both infraspinatus and supraspinatus muscles. Less often, entrapment is located distally at the spinoglenoid notch, and infraspinatus alone is affected (Kiss and Komar 1990, Bouzaidi et al. 2005). The suprascapular nerve appears to be vulnerable to injury at any point along its length due to relative fixation of the nerve at its origin in the brachial plexus and termination in the infraspinatus muscle, with potential for angulation at the suprascapular notch (Rengachary et  al. 1979). Studies by Sever before current research ethical standards showed that if the head and shoulder of an infant at post-mortem were pulled in opposite directions with great force, the suprascapular nerve was the first to snap (Sever 1916). Electro­ diagnosis is principally by needle EMG, to reveal denervation in supraspinatus and/or infraspinatus, and distinguish suprascapular nerve lesions from more widespread processes, brachial plexopathy or C5 root pathology. Neurogenic changes on EMG are not uncommonly chronic in type as diagnosis of suprascapular entrapment is often a late clinical consideration. Additionally, suprascapular nerve conduction can be measured (Kraft 1972), stimulating at Erb’s point and measuring CMAPs in the supraspinatus and infraspinatus muscles using either surface or needle electrodes; normative data for amplitudes and latencies have been published (Casazza et al. 1998). Latency and CMAP values may have predictive value for outcome of treatment: in a retrospective survey of patient rated motor outcome, 12 of 16 patients with good or excellent outcome who did not undergo surgery had normal motor latency but significant reduction (greater than 50%) in CMAP amplitude, implying reversible conduction block not requiring surgical decompression (Smith 2004).

Clinical Neurophysiology in Peripheral Nerve Injuries

6.6.1.5 Spinal Accessory Nerve Whilst a rare neuropathy overall, this nerve is not infrequently damaged during lymph node dissection in the neck. Lesions typically produce weakness of the trapezius, with scapular winging – which in our experience is not uncommonly mis-diagnosed clinically as a long thoracic nerve palsy (Fig. 6.17a and b). Very proximal lesions, such as due to infiltration by neoplastic processes, may also produce weakness of lateral neck rotation, with involvement of the sternomastoid. Electromyography helps to exclude other causes of scapular winging such as lesions of the long thoracic or dorsal scapular nerves. Intra-operative studies have been described as helpful in revealing lesions in continuity, with nerve action potentials recorded beyond the lesion or demonstration of trapezius contraction on direct stimulation of the spinal accessory nerve (Donner and Kline 1993). Case Report: This 55 year old woman presented with shoulder weakness and stiffness following surgical removal of a cervical lymph node. Scapular winging was evident. She was seen in the joint Royal National Orthopaedic

a

b

213

Hospital/National Hospital for Neurology and Neurosurgery peripheral nerve trauma clinic, where clinical and electromyographic examination confirmed an isolated right spinal accessory nerve lesion with fibrillations and a reduced interference pattern of wide duration motor units in the trapezius muscle, with sparing of the sternomastoid, allowing for uncomplicated surgical reconstruction of the nerve, and near complete recovery.

6.6.1.6 Axillary (Circumflex) Nerve The axillary nerve is the smaller division of the posterior cord of the brachial plexus, and derives from the C5–6 roots. From its origin in the axilla, the nerve passes deep and posterior to the subscapularis, and enters the quadrilateral space, where the branch to teres minor separates. It then passes deep to the posterior part of the deltoid muscle, gives off the superior lateral brachial cutaneous branch, and winds around the neck of the humerus, innervating the lateral and anterior fibres of the deltoid. The nerve is most frequently damaged by traction injury to the shoulder, and is clinically characterised by weakness of shoulder abduction and sensory loss in the chevron distribution. Anterior shoulder dislocation and fractures of the proximal humerus account for a significant proportion of the traumatic lesions (de Laat et  al. 1994). Unreduced dislocations and older age are significantly associated with nerve damage (Pasila et  al. 1978). Neuralgic amyotrophy not infrequently affects the axillary nerve – 6% as a mononeuropathy in Parsonage and Turner’s classic series, and 42% in combination with the suprascapular nerve (Parsonage and Turner 1948). Nerve conduction studies are of limited value in axillary nerve injuries, as the single proximal (or supraclavicular) site of stimulation at Erb’s point precludes distinction between axonal and demyelinating lesions. The key electrodiagnostic procedure is needle EMG to examine deltoid and teres minor, with sampling of other muscles as appropriate to exclude a brachial plexopathy or accompanying trauma of other nerves such as the suprascapular. Needle EMG is also helpful in assessing extent and timing of recovery as teres minor and the posterior fibres of the deltoid recover earliest after the initial insult.

6.6.1.7 Long Thoracic Nerve

Fig. 6.17  (a) and (b) showing trapezius muscle wasting in a case of spinal accessory neuropathy (case 3 above).

The long thoracic nerve arises from the anterior rami of the C5, C6 and (usually) C7 roots, passes lateral to the brachial plexus behind the clavicle, and down the anterolateral chest wall to supply the serratus anterior muscle. Blunt, as in backpack use, or penetrating trauma are often implicated in isolated lesions of this nerve (Makela et  al. 2006). The long thoracic nerve is involved in as much as 70% of cases of

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idiopathic brachial neuritis (van Alfen and van Engelen 2006). Presentation of a long thoracic nerve lesion is with muscular pain, and weakness of shoulder abduction caused by a failure of anterior rotation, and scapular winging exacerbated by shoulder abduction is noted on clinical examination. Needle EMG will demonstrate neurogenic changes in serratus anterior, and helps to exclude more extensive neural involvement such as in brachial neuritis, or a muscle disorder such as facio-scapular muscular dystrophy, which may present to the orthopaedic surgeon with isolated unilateral scapular winging.

6.6.1.8 Brachial Plexus Lesions Diverse pathologies affect the brachial plexus – trauma, neoplastic infiltration, radiation induced damage, inflammatory processes including brachial neuritis, hereditary pressure palsies, and compression due to cervical ribs or bands. In a large series (n = 203) of brachial plexus lesions from the Johns Hopkins hospital (Moghekar et al. 2007), of median age 37 years ranging from birth to 79 years, the three commonest pathologies were brachial neuritis, birth injury and trauma. The lesion was supraclavicular in 90%, and infraclavicular in 10%, with the upper trunk being most often affected (27%), followed by the lower trunk (11%), upper and middle trunks 11%, lower and middle trunk 7%, and upper, middle and lower trunk in 25%. In general, electrophysiological testing is primarily focused on establishing the level of pathology through the combination of sensory nerve studies (amplitudes of SNAPs for median digits 1–3, ulnar, radial, lateral antebrachial cutaneous, medial antebrachial cutaneous) and needle EMG, to delineate lesions affecting roots, trunks, cords and peripheral nerves and distinguish a pre-ganglionic lesion from a process affecting neural elements distal to the dorsal root ganglion. Electrodiagnostic evaluation must be comprehensive, even exhaustive, to identify clinically unsuspected involvement within the plexus (Table 6.6).

Table 6.6  Electrodiagnostic findings in pre and post-ganglionic lesions. Post-Ganglionic Pre-Ganglionic SNAPs

Absent/small

Normal/intact

CMAPs

Absent/small

Absent

F responses

Absent or delayed

Absent

Distal muscles

Denervation

Denervation

Paraspinal muscles

Normal

Denervation

Plexus SSEP

Absent

Intact

Cortical SSEP Absent Absent SNAP sensory nerve action potential, SSEP somatosensory evoked potential.

Ferrante and Wilbourn (Ferrante and Wilbourn 1995) assessed utility of sensory nerve conduction responses in 53 cases of brachial plexopathy with a single truncal element involved. In upper trunk lesions, almost all had abnormal median digit 1 and lateral antebrachial cutaneous SNAPs; 58% showed small or absent radial sensory responses. In patients with lower trunk lesions, the ulnar (digit 5) SNAP was abnormal in almost all, and the medial antebrachial cutaneous SNAP in 65%. The single case with a middle trunk lesion showed abnormality of the median digit 3 SNAP. Evidence of denervation on needle EMG in spinatii, biceps, deltoid, triceps, pronator teres and ECR indicates an upper trunk lesion; in ECR, ECU, EDC and EIP, a middle trunk lesion, and in FCU and intrinsic hand muscles, a lower trunk lesion. Reduction in CMAP responses from median and ulnar innervated muscles provides additional evidence of a lesion affecting the lower trunk or medial cord. Cervical root and brachial plexus lesions can be distinguished by measuring SNAPs, median and ulnar SSEPs, and needle EMG of axial, limb and paraspinal muscles. Needle sampling of rhomboids, innervated by the dorsal scapular nerve which exits directly from the C5 root, differentiates an upper trunk plexopathy from C5 radiculopathy. EMG of serratus anterior is useful for identification of a C7 lesion, as the long thoracic nerve leaves the plexus above the upper and medial trunks (Table 6.7). Determining the type of neural injury is more difficult, particularly in acute plexus lesions, as evidence of axonal damage may not manifest for several days after injury, and conduction block is less readily demonstrated in plexus elements compared with more accessible peripheral nerve trunks. Proximal conduction is amenable to measurement by use of F responses and percutaneous high intensity electrical stimulation of cervical roots in the neck and the plexus at Erb’s point; median and ulnar SSEPs may be used to evaluate conduction in sensory pathways traversing the brachial plexus and cervical cord. Adult traumatic brachial plexopathy: The need for, and timing, of surgical exploration in adults with acute traumatic injury of the brachial plexus will often be determined by associated injury to bony and vascular elements. Moreover, operative repair should be undertaken as promptly as permitted by the clinical condition of the patient, since outcome of surgery to the brachial plexus is adversely influenced by delay in operation. Thus, the contribution of neurophysiological evaluation in acute plexus trauma is limited before surgery, as the evidence of denervation in distal muscles and features which allows confident electrodiagnostic distinction of partial from complete neural injury is not apparent in the first few days after nerve trauma. Indeed, the optimal time for neurophysiological evaluation is somewhere between 3 and 12 weeks after plexus injury – electrodiagnostic testing is likely to be falsely negative for denervation, if EMG is undertaken within 3 weeks of trauma.

Clinical Neurophysiology in Peripheral Nerve Injuries

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Table 6.7  Brachial plexus elements – innervation of muscles and origin of upper limb sensory nerves. Level Nerves Muscles Snap Roots Trunk

C5

Dorsal scapular

Rhomboids

C5,6,7

Long thoracic

Serratus anterior

Upper

Suprascapular

Supraspinatus Infraspinatus

Middle

Lower

Cords

Lateral Posterior

Medial

Lateral pectoral

upper part of pect. major

Musculocutaneous

Biceps, brachialis

Median (lateral)

Pronator teres, FCR

Part of radial

Brachoradialis

Axillary

Deltoid, teres minor

Thoracodorsal

Latissimus dorsi

Subscapular

Teres major

Radial

all except brachoradialis

Median (lateral)

Pronator teres, FCR

Medial pectoral

lower part of pect. major

Ulnar

all ulnar muscles

Median (medial)

FDS, FDP (2,3), FPL, median hand muscles

Radial (C8 fibres)

EIP, EPB, (EDC,ECU)

Musculocutaneous

Biceps, brachialis

Median (lateral)

Pron. Teres, FCR

thoracodorsal

Latissimus dorsi

Subscapular

Teres major

Axillary

Deltoid, teres minor

Radial

All radial innervated

Ulnar

All ulnar innervated

Median (medial)

FDS, FDP, FPL, median

Median digit 1, lateral antebrachial cutaneous, some radial

Median digit 2 & 3, some radial

Ulnar digit 5, dorsal ulnar cutaneous, med. antebrachial cutaneous

Hand muscles

At the time of surgery, nerve continuity can be assessed by direct intraoperative nerve stimulation to record evoked nerve responses or EMG, and by perioperative SEP recording (Hetreed et al. 1994). Following surgical repair, serial neurophysiological measurement of temporal rate and magnitude of regeneration in central and peripheral neural pathways provides supportive evidence of clinical motor and sensory functional recovery. Misra and colleagues at Imperial College and the Royal National Orthopaedic Hospitals, London, have used EMG studies, transcranial magnetic cortical stimulation and quantitative sensory tests (axon reflex vasodilatation, thresholds for thermal and light touch sensation) to evaluate regeneration and functional plasticity in patients who have undergone spinal root repair and/or reimplantation of avulsed ventral roots into the spinal cord after brachial plexus injury. Reinnervation on EMG, first evident at 9–15 months after

surgery, normal latency and conduction properties of transcranial evoked motor potentials, together with clinical signs of recovery of sensation and muscle strength, demonstrates the potential for axonal regrowth and reinstatement of local segmental spinal cord circuits in human spinal cord after repair of avulsed spinal roots (Carlsted et al. 2000). The “stinger injury”: Stingers are well known amongst players of American football and ice hockey. The injury, which follows a neck or shoulder blow, is characterised by an electric shock sensation that travels down the arm, sometimes accompanied by paralysis of the arm. Stingers are typically transient, lasting minutes to days, but some cases may develop a prolonged syndrome with muscle wasting and sensory loss. Possible mechanisms include traction of the brachial plexus with lateral flexion of the neck, a percussive injury to the plexus at Erb’s point, and neck hyperextension and ipsilateral rotation (Kuhlman and McKeag 1999). Whilst damage is

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generally considered to occur at brachial plexus level, the potential mechanisms have led to proposals that traumatic injury to cervical roots is more likely. Stingers amongst UK rugby players have not yet been reported in the medical literature, but sporting bodies and players are familiar with the injury, and incidence may be rising as a result of changing body habitus and tackling style. Gareth Payne and two colleagues from Cardiff and Bristol have undertaken electrodiagnostic studies in 14 cases of stinger injury in professional and amateur rugby football players (Payne 2008, personal communication). In seven players, the pattern of denervation in infraspinatus, supraspinatus, deltoid, biceps implicated the upper trunk of the brachial plexus. Five had findings suggesting an isolated axillary nerve lesion, or an upper trunk lesion restricted to the axillary nerve fascicles. One player, with a history of repeated stingers, had more widespread weakness and wasting of the arm suggesting multiple brachial plexus injuries. True neurogenic thoracic outlet syndrome: Electrophys­ iological findings in thoracic outlet syndrome (TOS) were first described by Roger Gilliatt and others in their seminal paper published in the Journal of Neurology, Neurosurgery and Psychiatry in 1970 (Gilliatt et  al. 1970), and in a later publication from the same group, nerve conduction studies were shown to localise the lesion to the lower trunk of the brachial plexus affecting predominantly the C8-T1 roots (Gilliatt et al. 1978). Compression of the lower trunk of the brachial plexus produced by a fibrous band from an elongated C7 transverse process, or a rudimentary cervical rib was demonstrated in all patients in Gilliatt’s series. Neural and vascular elements traversing the thoracic outlet are variably affected by these vestigial structures, and the condition is best considered as being either one which is purely vascular, purely neurogenic (“true neurogenic thoracic outlet syndrome”), or involving both neural and vascular elements to a greater or lesser extent. True neurogenic TOS is very rare. The salient presentation is in a female patient who describes upper limb pain, often poorly localised, sensory deficit in the inner forearm and hand, and unilateral atrophy of thenar muscles (“the Gilliatt hand”). Widely accepted diagnostic neurophysiological criteria for true neurogenic TOS, indicative of chronic axonal loss in the lower trunk of the brachial plexus, are a small or absent ulnar sensory response, small or absent medial antebrachial cutaneous sensory response, normal median sensory response, attenuated motor CMAP amplitude from the abductor pollicis brevis, and low amplitude ulnar motor response (Le Forestier et al. 1998; Kothari et al. 1998b; CruzMartinez and Arpa 2001). Side to side comparison of nerve conduction studies significantly increases the sensitivity of electrodiagnostic testing (Tsao et al. 2008). Diagnosis of true neurogenic syndrome is challenging, not least because clinical symptoms are frequently non-specific, and overlap with carpal tunnel syndrome and ulnar nerve

Surgical Disorders of the Peripheral Nerves

entrapment neuropathy. Many techniques have been proposed over the years to enhance diagnosis and detect cases at an early stage before the development of usually irreversible hand muscle atrophy. Wulff and Gilliatt measured F waves recorded from hypothenar muscles evoked by stimulation of the ulnar nerve at the wrist and found prolongation of latency in the affected hand compared with the opposite limb (Wulff and Gilliatt 1979). In a majority of cases, the latency remained abnormally long after surgery, suggesting permanent degeneration of faster conducting fibres. SSEPs have been used to show abnormalities of proximal sensory conduction through the brachial plexus (Chodoroff et  al. 1985); the N9 plexus response evoked by stimulation of the ulnar nerve may be of reduced size and latency, whereas median nerve N9 responses are normal. Cervical root stimulation using magnetic or high intensity electrical stimulation has been used to assess proximal conduction; Felice and colleagues describe a patient with unilateral proximal conduction block on root stimulation, who showed modest improvement in hand function post-operatively (Felice et  al. 1999). For cases of mild lower brachial plexus lesions, Seror has suggested a new electrodiagnostic pattern of comparatively low or low amplitude medial antebrachial cutaneous sensory response, normal median and ulnar sensory and motor action potential amplitudes and normal or slightly reduced interference pattern in some C8-T1 innervated muscles (Seror 2004). Neurophysiological evaluation of the patient presenting with suspected neurogenic TOS should include exclusion of median nerve compression at the wrist and an ulnar neuropathy at the elbow. When SNAP abnormalities are equivocal, the differential diagnosis of apparent unilateral hand muscle wasting includes anterior horn cell diseases, radicular pathologies and multifocal motor neuropathy. Neuralgic amyotrophy: Neuralgic amyotrophy is a disorder characterised by an acute attack of neuropathic type pain followed by patchy weakness in a limb. The usual clinical course is with acute onset of pain in the neck or shoulder region, initially continuous and severe (and typically impairing sleep), lasting up to 4 weeks, with subsequent paresis. Sensory involvement occurs in three quarters of cases, but is mild relative to the neuropathic pain and muscle atrophy. Neuralgic amyotrophy usually occurs sporadically; rare hereditary forms exist, with predisposition to recurrent painful peripheral nerve lesions. A characteristic presentation is the young adult who experiences an acute and very painful brachial neuropathy with subsequent winging of the scapula. However, since the earliest description of cases by Parsonage and Turner, it has become apparent that neuralgic amyotrophy is a complex disorder which typically, but not always, affects the upper limbs, with a highly variable phenotype. The complexity is possibly due to the pathophysiological process being that of a mononeuritis multiplex, comprising multifascicular inflammatory

Clinical Neurophysiology in Peripheral Nerve Injuries

and constrictive lesions, as argued by Austin Sumner (Sumner 2007). The variability in location and extent of symptoms suggests that the alternative diagnostic label of brachial neuritis is a misnomer, as the disorder can affect the lumbo-sacral plexus as well as many peripheral nerves, albeit with a predilection for involvement of the cervical roots, brachial plexus and neural branches thereof. The most commonly affected nerves in a series of 40 cases (Cruz-Martinez et  al. 2002) were in rank order, the suprascapular, axillary, musculocutaneous, long thoracic and radial nerves; a small number of patients had lesions of the anterior interosseus, lateral antebrachial cutaneous or phrenic nerves. In a large series of neuralgic amyotrophy (n = 246, 199 sporadic cases, and 47 with hereditary form) reported from the Netherlands (van Alfen and van Engelen 2006), damage occurred most frequently (71.1%) in the upper and middle trunk distribution with involvement of the long thoracic and/or suprascapular nerve. The characteristic prodrome of severe neuropathic pain and patchiness of neural involvement will usually prompt diagnosis, and a further clue is the relatively common occurrence of an antecedent event, such as infection, strenuous exercise, surgery, pregnancy/puerperium or vaccination. Recognition is more challenging in those cases where pain is mild or absent: 3.7% in the Dutch series, but considerably higher at 47% in the cohort reported from the Johns Hopkins Hospital (Moghekar et al. 2007). Electrodiagnosis in neuralgic amyotrophy serves to supplement clinical examination by confirming or excluding involvement of specific nerves or plexus elements, and it may contribute to an estimation of recovery, before this is apparent to the patient. It also aids differentiation of neuralgic amyotrophy from hereditary neuropathy with liability to develop pressure palsies (HNPP), in which neurophysiological pointers to a more diffuse neuropathic disorder will be evident through abnormalities of motor and sensory conduction in the clinically unaffected arm and lower limbs. Birth lesion of the brachial plexus: Traumatic injury to the neonatal brachial plexus is uncommon, but it carries the potential to cause severe long term functional disability. There is a spectrum of neural damage ranging through transient conduction block, a lesion in continuity, severe neural rupture to root avulsion and the extent of injury can vary from a single nerve element to all components of the brachial plexus. We have found that traumatic plexus injury in neonates is most likely to produce partial intradural damage and to result in some residual conducting tissue across lesions because of the anatomical arrangement of spinal cord and roots within the spinal canal of the newborn, and the less abrupt nature of traction compared with adult traumatic plexopathy (Birch et al. 1998; Bisinella et al. 2003). Neurophysiological assessment of traumatic birth lesions of the brachial plexus (BLBP) has as its main purpose the

217

identification of children with poor prognosis for recovery – those with severe degenerative axonal injuries or root avulsion – in whom surgical repair offers the best opportunity for a good functional outcome. Electrodiagnostic and radiological investigation of traumatic BLBP should supplement clinical examination by clearly indicating the severity of neural injury at each level of the plexus. Ideally, ancillary investigations should also offer clues as to aetiology, allowing separation of rare palsies that occur during the intrauterine period from those resulting from events at the time of birth. Despite the opportunities for electrodiagnostic testing to answer questions regarding prognosis and causation, few centres use EMG in traumatic BLBP. This appears to be due to perception that EMG studies are insufficiently reliable and accurate, with high false/positive rates or findings that are unduly optimistic or pessimistic when measured against functional outcome (Slooff 1993; Yulmaz et al. 1999). Royden Jones has reviewed the limitations of neurophysiological assessement of brachial plexus injuries in children (Jones 1996). Demonstration of preserved SNAPs and fibrillations in cervical paraspinal muscles – the hallmarks of root avulsion – may be difficult or impossible to achieve in small neonates for technical and safety reasons. The spectrum of sensory nerve responses available for measurement is more limited than in older children or adults, particularly for digital nerves, and those nerves with relatively short distance between stimulating and recording electrodes (radial, cutaneous antebrachial nerves) since stimulator artifact may affect SNAP quality. Normative values for SNAPs amplitudes show wide variation in infants and judging normality or otherwise may be difficult especially in the instance of bilateral brachial plexus injury. Amplitude of the CMAP is age dependant, with a threefold increase in size in the arm through maturity. Infants also have smaller muscle fibres (17  mm at 3 months of age compared with approximately 60 mm in adults, Brooke and Engel 1969), and their motor unit potentials are both smaller and shorter in duration. Neurophysiological distinction between intra-uterine plexopathy and birth related traumatic damage to the brachial plexus is reliant on accurate knowledge of the time course of change in CMAPs, SNAPs and motor unit potentials in the neonate, but there is very little information on this time course, as so few EMG studies are undertaken in the immediate few days after birth. Theoretically, fibrillations should occur much earlier in neonates than in adults, since babies have nerves which are shorter in length and smaller in diameter. The time that fibrillations appear is inversely correlated to the volume of the denervated segment of the nerve below the level of section; calculations based on neonatal nerve length and size suggest that fibrillations would be expected to appear within a few days of injury (Van Dijk et al. 2001). Experimental work in piglets with brachial plexus section supports presence of fibrillations in denervated muscles within 24 h of injury (Gonick

218

Surgical Disorders of the Peripheral Nerves

et al. 1998), and implies maximal reduction in CMAPs within 24–48 h, and SNAPs being reduced 1–2 days later. Fibrillations and other evidence of denervation have indeed been demonstrated within 4–5 days of birth in infants with traumatic BLBP days of birth (Colon and Vredeveld 2001; Mancias et al. 1994). There are strong arguments for advocating very early and sequential EMG studies to detect first appearance of fibrillations, and thereby enable accurate timing of injury, especially in cases where there is circumstantial evidence of birth related trauma (Jones et  al. 2003; Pitt and Vredefeld 2005). Intrauterine injury may be suspected if EMG reveals chronic denervation within the first 1–2 weeks of birth: Paradiso and colleagues described an infant born by difficult breech delivery, in whom C5 and C6 muscles showed wasting and chronic denervation on EMG at 18 days after birth, findings which clearly placed the lesion as occurring some weeks before birth (Paradiso et al. 1997). The intra-uterine environment does not protect against pressure palsy of nerves– focal mononeuropathies of radial (Ross et  al. 1983) and peroneal (Jones et  al. 1996) have been identified in neonates, and were shown neurophysiologically to pre-date birth. In addition to needle EMG, techniques applied in neurophysiological evaluation of traumatic BLBP include axillary and musculocutaneous motor latency, upper limb motor and sensory conduction, ulnar H reflex (Eng et al. 1996,), SSEP for detection of root avulsion (Hashimoto et al. 1991), and intra-operative CMAP, NAP and SSEP recording to determine neural continuity (Papazian et al. 2000). Heise and colleagues used CMAP measures to estimate degree of axonal damage or loss; they found axillary and radial nerve CMAP amplitudes below 10% of the unaffected arm were accurate in predicting outcome for C5 and C6, and ulnar nerve CMAPs were useful for C8 and T1 prognosis (Heise et al. 2004). Our preferred method for neurophysiological evaluation in BLBP is to combine median and ulnar mixed nerve action potentials in the forearm (NAP) with EMG. In 73 infants aged 3 months or older with slowly recovering brachial plexus injury who were managed conservatively (Bisinella

et  al. 2003), neurophysiological prediction of a favourable long term outcome (NAP amplitude 50% or above of unaffected arm, presence of significant amounts of reinnervation or normal motor units on EMG) was confirmed at long-term follow up with mean of 4.3 years in 93% of C6 lesions and 97% of C7 lesions. Predictions for C5 were confirmed in a smaller proportion (78%), possibly because of inability to record an NAP for C5 and the high frequency of secondary shoulder pathology contributing to functional disability. An unexpected finding in this series of slowly recovering traumatic BLBP was the neurophysiological evidence suggesting neurapraxic injury in a significant number of roots – normal NAP responses, reduced recruitment of normal MUPs and absence of denervation/reinnervation change on EMG. The mean age at which neurophysiological studies were performed was 5 months, and one of these infants with apparent prolonged conduction block was age 10 months at the time of evaluation. None of the infants whose neurophysiological assessment implied neurapraxic injury had clinical function in biceps by age 3 months, and they were clinically indistinguishable from cases with more severe lesions, prompting referral to the tertiary centre. All had a very good outcome with conservative management. The explanation for long lasting conduction block is unclear, but identification is important as there is a very good chance of spontaneous recovery. Eng and colleagues identified similar cases of prolonged conduction block (n = 8) in their large series of 135 children with obstetric palsy (Eng et al. 1978). Our group has also found strong correlation between neurophysiological prediction of lesion type, based on NAP and EMG measures, and nerve injury type identified at operation (Birch et  al. 2005), suggesting that more severe degrees of axonal injury can be discriminated from those with potential for recovery using pre-operative electrodiagnosis (Table 6.8). Whilst needle EMG is the most important measure of which roots are involved, and whether there is discontinuity in nerve supply, reliance on EMG alone may produce inaccurate information – the so-called “overly optimistic EMG” (Vredeveld

Table 6.8  Birth lesions of the brachial plexus – proposed correlation between neurophysiological diagnosis and type of nerve lesion, adapted from Birch et al. 2005. NAP/SAP EMG Neurophysiological Pathophysiology or IOP SEP at Foramen/Stimulation diagnosis Lesion type distal to lesion Normal or near normal

NSA

50% or above of normal

Fibrillations +/−

Absent or less than 50% normal

Fibrillations +

Present in some, more often absent

Fibrillations ++

Conduction block

Neurapraxia

Not applicable

Favourable rupture

Axonotmesis

Normal/>50%

Unfavourable rupture

Neurotmesis

Reduced/<50%

Avulsion and/or severe rupture

Pre-ganglionic or total neurotmesis

Both reduced/absent

Normal units Copious MUP activity Limited MUP activity

Very limited MUP activity NSA no spontaneous activity; MUP motor unit potential.

Clinical Neurophysiology in Peripheral Nerve Injuries

et al. 1996). Van Dijk and colleagues have suggested possible explanations for an unduly optimistic or pessimistic EMG picture in their thoughtful review of obstetric lesions of the brachial plexus (Van Dijk et al. 2001). These include an incorrect clinical examination, as is more likely in the severe or complete lesion, or overestimation of MUP activity by the neurophysiologist, because of the small size of neonatal muscle fibres relative to recording needle. There may be luxury or polyneuronal innervation at birth, possibly derived from multiple segments or roots; distribution of individual spinal nerve roots is more diverse than traditionally indicated in anatomical textbooks (Colon et al. 2003). Central nervous system involvement could play a role in modifying recruitment patterns following deafferentation injury in neonatal brachial plexus injury. Aberrant regeneration or misdirected axons can result in MUPs appearing in the wrong muscle, as in “the breathing hand,” and synkinesis may be difficult to assess in the less cooperative infant or child. Finally, whilst neurophysiology can identify continuity of neural conduction, this is not the only important factor in regaining useful arm function following brachial plexus injury in the neonate.

6.6.2 Lower Limb Neuropathies 6.6.2.1 Sciatic Nerve The sciatic nerve arises from the lumbosacral plexus and is formed by the L4/5 and S1 roots. The long anatomical course from the ischial notch through the thigh renders this nerve prone to traumatic injury. The peroneal division, by virtue of the fascicular arrangement of fibres that are encased in loose areolar tissue, and tethered at the sciatic notch and the fibular neck, is particularly vulnerable and is usually disproportionately affected. The most common pathological mechanisms for sciatic nerve injury are compression, traction or direct injury by mechanical disruption as is seen in intragluteal muscle injection, still a significant factor in developing countries. In an extensive review of the published literature, hip surgery was identified as the most common cause by far (Plewnia et  al. 1999). Iatrogenic lesions have also been reported in cardiac surgery (Kempster et al. 1991; McManis 1994), gynaecological procedures (Burkhart and Daly 1966), femoral nailing (Britton and Dunkerley 1990) and craniotomy in the sitting postion (Gozal and Pomeranz 1994; Keykhah and Rosenberg 1979). Other traumatic causes include direct injury to the nerve from gun-shot or knife wounds, and compartment syndromes caused by prolonged immobility (Hynes and Jackson 1994). Traction related sciatic neuropathies have been reported following assumption of unusual limb positions as in Yoga (Vogel et  al.1991) and after martial arts (M Pitt, 2009, Great Ormond Street Hospital, London, personal communication). Rarely, recurrent sciatic neuropathy

219

raises the possibility of an underlying liability to pressure palsies (Ichikawa and Nezu 2005). The typical electrophysiological features of a sciatic nerve lesion are attenuation of sensory and motor nerve responses in both peroneal and tibial divisions. In an electrophysiological review of 100 consecutive patients with sciatic neuropathy (Yuen et  al. 1995), the peroneal division was more severely involved in most cases (66%), with 12% demonstrating sole involvement of this division. Evidence of axonal change was the predominant electrophysiological finding. However, electrodiagnostic testing revealed involvement of the tibial division in some patients, not apparent on careful clinical testing. It may be difficult to differentiate sciatic neuropathy with predominant involvement of the peroneal division from a common peroneal nerve lesion. In such cases, needle EMG of the short head of biceps femoris is useful, as this muscle is supplied by the lateral trunk of the sciatic nerve (Katirji and Wilbourn 1994; Katirji 2002). The differential diagnosis of sciatic neuropathy includes lumbosacral plexopathy, which may be excluded by needle EMG sampling the gluteal and anterior femoral muscles, and root lesions at lower lumbar and sacral levels. Piriformis syndrome: Sciatic nerve compression in the piriformis syndrome is purported to be caused by hypertrophy of the piriformis muscle, or an anatomical variation in the course of the sciatic nerve as it crosses the piriformis muscle. This anomaly, which usually involves the peroneal division, has been identified in 5% of cadavers (Peccina 1979), with the implication that the syndrome may be under-recognised. Most patients described with piriformis syndrome present with buttock or leg pain or other sciatic symptoms, typically developing on exercise or in certain postures such as sitting. There are no specific electrodiagnostic features other than those indicative of a sciatic nerve lesion. The FAIR (flexion, adduction, internal rotation) provocative H reflex test has been proposed as increasing sensitivity for diagnosis (Fishman and Zybert 1992; Fishman et  al. 2002). However, Holder at University College Hospital in London found a positive FAIR test in only two of 35 cases with suspected piriformis syndrome (Holder, 2009, Neurophysiological Diagnosis and Intervention in Piriformis Syndrome, personal communication) – and the pathophysiological basis of rapid increase in H reflex latency would be difficult to explain on the basis of a process presumed to be compressive with resultant conduction block. Needle EMG may be of most value in cases of so-called piriformis syndrome to guide therapeutic intra-muscular injection of local anaesthetic, steroid or botulinum toxin.

6.6.2.2 Common Peroneal Nerve The lateral division of the sciatic nerve continues as the common peroneal nerve below the knee, winding around the neck of the fibula. This renders it susceptible to compression: common

220

peroneal nerve lesions at the knee are the commonest type of lower limb mononeuropathy. An Italian multicentre study of peroneal neuropathy identified a traumatic causation in 32%, with a preponderance of direct and indirect iatrogenous injury (25%). Surgery at remote sites such as the thyroid and abdomen accounted for most of the iatrogenic cases. In 16%, no cause was identified (Aprile et al. 2005). Other rare sites of a common peroneal nerve lesion include the lower leg and under the extensor retinaculum of the ankle. Electrodiagnosis of a common peroneal neuropathy is based on the demonstration of an attenuated SNAP in the superficial peroneal nerve, and reduction in the CMAP amplitudes from the peroneal muscles such as extensor digitorum brevis and tibialis anterior. Slowing of motor conduction across the fibular head, and/or conduction block will suggest a demyelinating lesion. As in ulnar entrapments at the elbow, inching or short segment studies may aid diagnosis of a demyelinating lesion across the fibular head (Raudino 2004). In cases where the principal pathological process is demyelination, as indicated by focal conduction block, prognosis should be favorable: an absent or severely diminished motor response showed strong inverse correlation with recovery (Cruz-Martinez et al. 2000). In a large case series review of 116 lesions (Katirji and Wilbourn 1988), axonal loss was the most common electrophysiological finding (55%), conduction block was identified in 17% of patients, and mixed axonal/demyelinating features were seen in 25%. Motor conduction studies to the tibialis anterior muscle identified conduction block more consistently than extensor digitorum brevis. In the series reported by Kang and colleagues, a diminished superficial peroneal nerve response was seen in slightly less than half (48%) of cases, suggesting fascicular selectivity Kang et al. 2005. A generalised underlying polyneuropathy must always be excluded in cases presenting with a common peroneal nerve lesion. L5 radiculopathy is an important consideration in the differential diagnosis, particularly as lateral disc herniation may produce compression distal to the dorsal root ganglion affecting the superficial peroneal sensory response (Levin 1998). In the patient presenting with foot drop, EMG evidence of denervation in tibialis posterior muscle will usually reliably distinguish a common peroneal neuropathy from an L5 root lesion.

6.6.2.3 Tibial Nerve and its Branches Isolated lesions of the proximal part of the tibial nerve are relatively uncommon, as the nerve is well protected in the knee. Nerve damage may however occur following direct knee injury, in cases of Baker’s cyst (DiRisio et al. 1994), and iatrogenically such as during placement of fixation screws or endoscopic vein surgery (Geselschap et al. 2001).

Surgical Disorders of the Peripheral Nerves

Neurophysiological studies will usually reveal evidence of axonal loss – reduced amplitude of the abductor hallucis CMAP and neurogenic change in calf muscles and intrinsic foot muscles innervated by the tibial nerve. The H reflex recorded from soleus may be small or absent. Lesions above the popliteal fossa result in reduction or loss of the sural sensory response. In the lower leg, the tibial nerve passes behind and below the medial malleolus through the tarsal tunnel, underneath the flexor retinaculum. The calcaneal sensory branch may be given off proximal to the tunnel, but the medial and lateral plantar nerves arise within the tarsal tunnel. Any of these nerves may be affected in the (posterior) tarsal tunnel syndrome, which is the pedal counterpart of the carpal tunnel syndrome. This rare entrapment neuropathy is frequently misdiagnosed as plantar fasciitis. Trauma such as ankle fracture or dislocation is most commonly implicated in the pathogenesis, but medical conditions such as rheumatoid arthritis may also be causative, as is joint hypermobility (Francis et al. 1987). Pain in the sole of the foot, particularly prominent at night, is the most common clinical symptom in reported cases. Weakness of the intrinsic foot muscles may be present, but is difficult to define clinically. Prolongation of the distal motor latency to abductor hallucis and/or abductor digiti quinti is a very suggestive electrodiagnostic finding in suspected tarsal tunnel syndrome. However absent or diminished sensory responses from the sole, and the great toe, may be a more sensitive feature (Guiloff and Sherratt 1977), except in patients over 65 years in whom lower limb SNAPs may be difficult to record even in the absence of pathology. Motor recording from the first dorsal interosseous muscle supplied by the lateral plantar nerve, may also be useful (Galloway and Greathouse 2006). Needle EMG assists exclusion of first sacral radiculopathy, which may produce similar symptoms, and the examination should include at least one muscle innervated by the common peroneal nerve to rule out a sciatic neuropathy. Most clinical neurophysiologists will share our experience that many of the cases of possible tarsal tunnel syndrome referred for electrodiagnosis show normal nerve conduction studies and EMG findings. The anterior tarsal tunnel syndrome, whilst very uncommon overall, appears to be more frequent in persons frequently adopting the kneeling (or Namaz) position at prayer (Akyuz et  al. 2000). Pain in the dorsal forefoot, worse at night and relieved by a change in position, are the principal clinical features. Electrophysiological confirmation is by demonstration of disproportionately prolonged distal motor latency to extensor digitorum brevis, with denervation in the muscle on needle EMG sampling. Morton’s metatarsalgia was probably the earliest focal neuropathy to be clearly described in the literature, but the actual pathology, a traumatic neuroma of the lateral digital nerve, was only recognised in the 1940s (King 1946). The

Clinical Neurophysiology in Peripheral Nerve Injuries

clinical feature of burning pain over the head of the fourth metatarsal which radiates forward to the toe, is sufficiently characteristic, but near nerve recording from the interdigital nerves from toes four and five may help in confirmation of the diagnosis. Demyelination is not a prominent feature. Other rare pedal entrapment neuropathies include Joplin’s neuroma, caused by traumatic fibrosis of the perineurium of the medial plantar digitial nerve of the great toe. Pain and variable sensory loss over the medial aspect of the great toe are noted clinically. Electrophysiological confirmation is by near needle recording from the tibial nerve at the ankle, stimulating the medial plantar digital nerve in the great toe (Cichy et al. 1995; Oh 2007). Sural neuropathy: The sural nerve emerges from the fascial layer of the postero-lateral leg about 20  cm above the lateral malleolus, passing behind the lateral malleolus and supplying the skin of the lateral ankle and foot up to the little toe. The most common cause of an isolated sural neuropathy currently is iatrogenic viz. nerve grafting or biopsy. However, the sural nerve can also be injured by a Baker cyst in the popliteal fossa, and during surgical vein stripping or compression. Orthopaedic procedures at the ankle, tumors and direct traumatic injury also contribute. The lesion is usually axonal, and a side to side reduction in amplitude of less than 45% in comparison with the normal leg confirms the diagnosis (Seror 2002).

6.6.2.4 Femoral Nerve Femoral nerve lesions are usually due to nerve compression – during pelvic surgery, from a retroperitoneal haematoma, and as a result of prolonged lithotomy positioning. The nerve is also vulnerable during hip surgery, particularly hip revision or replacement. Clinical manifestations are weakness of hip flexion if the lesion is above the inguinal ligament proximal to the motor branch to psoas, weakness of knee flexion, and sensory loss in the antero-medial thigh. Electrodiagnostic findings in femoral neuropathy are determined by whether the lesion is primarily axonal, when there will be loss of the saphenous SAP and denervation on EMG, or of demyelinating type, consequent to external compression or stretch injury. Demyelinating lesions may show a reduced CMAP of rectus femoris or vastus medialis, stimulating the femoral nerve at the groin, an EMG pattern suggesting conduction block (reduced recruitment of normal MUPs) and preservation of the saphenous SAP. The CMAP size has prognostic value in axonal femoral neuropathy – if the response is less than 50% of the unaffected side, fewer than half of patients had recovered by 1 year, whereas all patients with a CMAP exceeding 50% showed full recovery (Kuntzer et  al. 1997). EMG is the most useful procedure in a suspected femoral neuropathy, to aid localisation and to exclude extra-femoral involvement. Neurogenic EMG abnormalities will be seen in

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the psoas muscle when the lesion is sited within the pelvis above the inguinal ligament. In lumbar plexopathy, extra-­ femoral denervation is found, involving all or some of tibialis anterior, peroneal muscles and thigh adductor muscles, and the saphenous and superfical peroneal SAPs may be reduced or absent. Denervation will also be more extensive in lumbar radiculopathy, including paraspinal muscles. The entity of “diabetic amyotrophy” was previously and erroneously considered to be a femoral neuropathy based on presentation with acute severe pain in the upper leg, lower back or buttock with weakness and wasting of proximal leg muscles. However, electrodiagnosis reveals denervation in several lower limb muscles in different myotomes, and often evidence of a generalised sensori-motor axonal neuropathy. Although the precise level of pathology is uncertain (Chokroverty 1987), it should be considered as a diffuse disorder affecting lumbosacral plexus, lumbo-sacral roots and peripheral nerves (BrunsGarland syndrome).

6.6.2.5 Other Lower Limb Nerve Disorders Meralgia paraesthetica (Bernhardt-Roth syndrome): This entrapment neuropathy of the lateral femoral cutaneous nerve, which arises from the upper lumbar plexus, is not uncommon, and deserves especial consideration. Unpleasant paraesthesias affect the upper outer thigh, with a small area of well circumscribed sensory loss. The focus of entrapment is at the level of the inguinal ligament, through or under which traverses the lateral femoral cutaneous nerve. Pregnancy, obesity or rapid weight gain and diabetes are significantly associated with this condition. Although the diagnosis is primarily clinical, electrodiagnosis is useful to establish the lesion, and to rule out a femoral neuropathy, L4 radiculopathy or lumbo-sacral plexopathy, principally by needle EMG in lower limb muscles. Other diagnostic techniques include lateral femoral cutaneous SNAP amplitude and sensory conduction velocity measurement, but the nerve can be difficult to study with surface or skin electrodes and near nerve needle recording may be required. Side to side comparison, rather than the absolute amplitude of the sensory response, is more sensitive in identifying abnormality (Lagueny et al. 1991; Seror and Seror 2006). Obstetric nerve injuries: The medical literature reports a frequency of postpartum lumbosacral spinal and lower extremity nerve injury between 0.8 and 50/100 000. A large survey (6,057 women) of post-partum lower extremity injuries in the United States estimates the incidence of post-partum nerve injury at 0.92% (Wong et  al. 2003). The mechanisms of nerve injury in labour are diverse, and include transection, stretch, compression as well as ischaemic/vascular injury. The most common nerve lesion (60%) is that of unilateral or bilateral injury of the lateral cutaneous nerve

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(meralgia paraesthetica), with the hyperlordosis of pregnancy associated with compression of the nerve by the posterior fascicle of the inguinal ligament. Stretching by retractors during Caesarian section, as well as actual severing during a wide Pfannenstiel incision are other aetiopathogenic mechanisms. Femoral neuropathy is the second most common injury, with most women demonstrating hip flexion as well as knee extension weakness. Interestingly, none of the women reported in the study by Wong had caesarian delivery. Excessive hip abduction and external rotation is considered to stretch the intra-pelvic portion of the femoral nerve, and stretch–induced ischaemia may be aggravated by poor blood supply. Other peripartum neural complications described in the literature include sciatic (Roy et al. 2002), common peroneal, obturator (Lindner et al. 1997) and lumbosacral plexus lesions. Saphenous nerve lesions: Saphenous neuropathy is most frequently caused by saphenous vein harvesting for coronary artery bypass grafts (Chauhan et al. 1981). Occasional causes include compression by the femoral artery, schwannomas, damage to the nerve at knee level during arthroscopy and other orthopaedic procedures (Mochida and Kikuchi 1995), and during varicose vein surgery (Cox et  al. 1974). Focal lesions can be confirmed by sensory nerve recording, with needle EMG if there is suspicion of lumbar radiculopathy (L4) or a partial femoral nerve lesion.

6.6.2.6 Lumbosacral plexopathy The lumbosacral plexus has two structurally and functionally discrete divisions- the lumbar plexus, formed by the anterior rami of the L1 to (most of ) L4 roots, and the sacral plexus which is formed by the lumbosacral trunk (part of L4, L5) and the anterior rami of the S1-S4 roots. The lumbar plexus lies within the posterior part of the psoas muscle. Sensory innervation includes the skin of the pubis and (partly) the external genitalia. It also supplies the front, inner and posteromedial thigh via the genito-femoral and obturator nerves, and the inner and anteromedial leg to the ankle (saphenous-femoral nerves). Muscular contribution includes the iliacus and psoas muscles, as well as the anterior and medial femoral muscles through the femoral and obturator nerves. The sacral plexus is located over the anterior surface of the piriformis muscle, in the posterior pelvis, and is therefore in close proximity to the pelvic organs such as colon, bladder, uterus and rectum. Of the divisions of the sacral plexus, the sciatic nerve is the largest, formed by the fusion of anterior (tibial) and the upper four posterior (peroneal) divisions. Other divisions are the gluteal and posterior femoral cutaneous nerves. Lumbosacral plexopathies are much less frequent than brachial plexus lesions, with non-traumatic causes accounting

Surgical Disorders of the Peripheral Nerves

for a majority of cases reported in the literature. Neoplastic infiltration was found to be eight times more frequent than trauma, with infiltration by malignancies of the pelvic organs (uterus, bladder, rectum) being more common than primary tumours of the lumbosacral plexus such as neurofibromas (Jaeckle 2004). Pelvic fractures resulting from motor vehicle accidents, falls, and industrial accidents are the usual injuries associated with traumatic lumbosacral plexopathies; transverse sacral fractures are particularly liable to damage nerve roots (Wilbourn 2007). Motor vehicle accidents more frequently involve the upper plexus, whereas gunshot wounds tend to produce discrete, multifocal lesions of the lumbosacral plexus, predominantly affecting the upper part of the plexus (Chiou-Tan et al. 2001). The co-existence of skeleto-muscular trauma makes precise localisation difficult clinically, and electrodiagnostic evaluation is complex and challenging in such cases. Our own experience from the joint Peripheral Nerve Injury and National Orthopaedic and National Hospital clinic is that a much higher proportion of the lumbosacral plexopathy cases we see are due to pelvic fracture and penetrating missile injuries. Accurate localisation to the lumbar or sacral plexus is more difficult than in brachial plexus lesions for a number of reasons. There is a limited repertoire of sensory nerve responses (sural, saphenous, superficial peroneal) that can be reliably studied in the lower limbs, especially in elderly subjects; moreover, motor involvement is often the predominant feature of a lumbo-sacral plexopathy. In a large series, only a third of 171 cases could be localised to the sacral plexus, using the criteria of reduced/absent SNAPs, denervation of plexus innervated muscles, and absence of paraspinal denervation (Tavee et al. 2007). Age related loss of sural SNAPs, prior lumbar surgery and duration of the lesion contribute to the imprecise localisation (Wilbourn 2007). Differential diagnosis includes traumatic sciatic and common peroneal nerve neuropathies. A peroneal pattern of sensory loss and weakness was seen most frequently in a retrospective series of neurological injuries associated with pelvic trauma (Chiodo 2007). This is explained by the anatomical proximity of the peroneal division to the sacroiliac joint. Prognosis for gait outcome was significantly associated with abnormalities of peroneal nerve conduction, and denervation in the tibialis muscle; gluteal involvement tended to be mild and did not contribute to gait abnormality. Neuropathic pain was seen in 37%, and was not correlated to the type or level of injury. As in brachial plexopathy, evidence of myokymia on EMG can be specifically helpful in differential diagnosis of tumor and radiation induced lumbosacral plexopathy. Myokymic discharges were seen in 57% of patients with radiation damage, but in none of the cases with neoplastic infiltration (Thomas et al. 1985).

Clinical Neurophysiology in Peripheral Nerve Injuries

6.6.2.7 Electrodiagnosis in Root Lesions Radiculopathies are one of the most common reasons for referral to the Clinical Neurophysiologist, and electrodiagnostic testing has been used in the evaluation of nerve root compression for many years as a complement to neuroimaging. In occasional cases, EMG studies may confirm diagnosis even when radiological examination is negative (Wilbourn and Aminoff 1988). The approach of combining nerve conduction studies and needle EMG sampling has recently shown comparative diagnostic efficiency with neuroradiological examination in lumbosacral radiculopathies (Fisher et al. 2008). In general, with the exception of an L5 root compression (Levin 1998; Ho et al. 2004), sensory nerve conduction studies are normal in radiculopathy since the lesion lies in the preganglionic segment of sensory fibres, proximal to the dorsal root ganglion. Motor nerve conduction studies may reveal abnormalities of CMAP amplitude, as well as aberrations of F waves and the H response. However, nerve conduction studies play the conjunctive role of exclusion of a co-incidental focal peripheral nerve lesion in suspected radicular disease. In those patients with radiculopathy who have normal EMG findings, one explanation for a false negative study is the greater variability in cervical and lumbosacral myotomes than is usually indicated in standard texts. Levin and colleagues compared surgical and electromyographic localisation of single cervical root lesions, and found a fairly stereotyped pattern of muscle involvement in C5, C7 and C8 lesions, whereas it varied in C6 radiculopathies. In half of these cases, muscles affected were similar to those in C5 root lesions with additional involvement of pronator teres; in the remainder, the pattern resembled that of a C7 radiculopathy (Levin et al. 1996). Further challenges are uncertainties as to precise segmental level in paraspinal muscles at both cervical and lumbosacral regions, and the persistence of EMG abnormalities following previous spinal surgery. The value of SSEPs in radicular disease is limited. Relatively short segments of demyelination in sensory roots may not manifest with significant prolongation of latency, and amplitude of SSEP components is overall too variable to allow reliable identification of focal conduction block. Several peripheral nerves derive from multiple nerve roots – the median nerve for example contains fibres from C6, C7, C8 and T1. Sensitivity of dermatomal SEPs varies from 25% of cases showing abnormality (Aminoff et  al. 1985) to 95% (Katifi and Sedgwick 1987); the difference in study findings may be explained by use of wider criteria for abnormality. Use of magnetic stimulation of roots to measure motor evoked responses (Chokroverty et al. 1989) is limited by uncertainty as to exact site of stimulation, and to a lesser extent by discomfort of the procedure. The “double crush” syndrome This syndrome was first proposed by Upton and McComas based on their observation of patients with a combination of cervical root lesions and upper

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limb entrapment neuropathies, such as carpal tunnel syndrome or ulnar neuropathy at the elbow (Upton and McComas 1973). The double crush concept is based on the occurrence of focal compression at more than one site along the length of a nerve fibre. Upton and McComas proposed that a sub-clinical distal focal neuropathy could be converted into a clinical lesion, probably through serial constraint of axonal flow, and thus a distal compressive lesion had a greater effect when in the presence of a proximal lesion. The double crush syndrome became a widely accepted concept, and was further expanded to include the reverse double crush, whereby a distal lesion such as affecting the ulnar nerve at the wrist could trigger an ulnar neuropathy at the elbow by comprising retrograde axonal transport (Dahlin and Lundborg 1990), and even multiple-crush syndromes. However Wilbourn and Gilliatt have provided a compelling critique of the double crush concept, arguing that it is far more widely cited than is justifiable on anatomical or physiological grounds (Wilbourn and Gilliatt 1997). The principle most often breached in clinical examples of the double crush syndrome is the most basic – the requirement for anatomical continuity of nerve fibres between the two (or more) lesion sites. This is especially so when the distal lesion affects a peripheral nerve that has extensive proximal origin such as the median nerve at the wrist, which derives from four cervical roots, and then traverses multiple components of the brachial plexus. Hence, a patient who presents with median nerve compression at the wrist and clinico-radiological evidence of a C6 cervical radiculopathy is likely to have two neurological lesions which are not directly related. The other context in which the double crush concept poses difficulty is when the proximal lesion involves sensory radicular fibres within the intra-spinal canal, and thus proximal to the dorsal root ganglion. Pre- and post-ganglionic fibres are not in anatomical continuity, and injury to one set of fibres will not affect the other unless the dorsal root ganglion is also damaged. Morgan and Wilbourn analyzed a large series (n = 12,736 limbs) of carpal tunnel syndrome or ulnar neuropathy at the elbow (Morgan and Wilbourn 1998). In 435 limbs (3.4%), there was a coexisting cervical radiculopathy, but only 98 limbs (0.8%) had an association that was anatomically appropriate. Cumulatively, only 69 of the 12,736 cases of carpal tunnel syndrome or ulnar neuropathy at the elbow satisfied pathophysiologic and one of the anatomic requirements of the double crush hypothesis, suggesting that a cervical radiculopathy could only rarely serve as the proximal lesion with these entrapment neuropathies in the double crush syndrome.

6.6.3 Diffuse Problems It is important to remember that an isolated, apparently compressive or traumatic lesion of a peripheral nerve or nerve

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root can be the presentation of a more diffuse process. This may be an hereditary polyneuropathy such as hereditary neuropathy with liability to pressure palsies (HNPP), a myopathy such as facio-scapulo-humeral dystrophy, or even a disorder of the anterior horn cell such as the amyotrophic lateral sclerosis form of motor neurone disease. The role of the electromyographer therefore extends beyond localisation and prognostication of nerve or nerve root injury to recognition and diagnosis of diffuse neuromuscular disorders, or a condition unsuspected by the referrer. Electrodiagnostic evaluation of a generalised polyneuropathy is directed towards assessing the degree of involvement of sensory and/or motor fibres, and identifying whether the neuropathy has pathophysiological features of an axonopathy or a demyelinating neuropathy. The distinction between these two types of neuropathy is determined principally by conduction velocity – if there is slowing of nerve conduction velocity, the neuropathy is demyelinating in type. In axonal neuropathies, there is reduction in size or loss of sensory and/or motor nerves responses; conduction velocities are relatively preserved, depending on the degree of axonal loss. The distribution of abnormality reveals whether the neuropathy is symmetrical or multifocal, as in mononeuritis multiplex syn. multifocal neuropathy, or a chronic demyelinating polyneuropathy. Distal dying back axonopathies of metabolic aetiology such as diabetes, or due to toxins such as alcohol or chemotherapeutic agents, initially involve the longest i.e., lower limb nerve fibres. Neurophysiological characterisation of the type and pattern of a polyneuropathy is of substantial help when considering possible underlying causes. Case Report: A 62 year old man presenting with symptoms suggesting median nerve compression in the right wrist underwent carpal tunnel decompression. There was no clinical improvement following surgery. The finding of a positive Tinel’s sign over the median nerve at the elbow led to operation at this site, again without any improvement in sensory symptoms. The patient was then referred for nerve conduction studies. These revealed absent median and ulnar sensory responses in both hands, a small superficial radial sensory response of 6 mV, and absent lower limb sensory responses. Conduction velocities and F responses were abnormally slow in several motor nerves of the arms and legs, with patchy involvement of different nerve segments. Conduction block was seen in both ulnar nerves at the elbow and in the left common peroneal nerve. Mild degrees of chronic partial denervation were seen in distal limb muscles. The nerve conduction studies thus revealed a diffuse polyneuropathy, of demyelinating type in view of slow conduction velocities. The patchy nerve involvement suggested an inflammatory cause i.e., chronic inflammatory demyelinating polyneuropathy, later confirmed on nerve biopsy, and successfully treated with immunosuppressive therapy.

Surgical Disorders of the Peripheral Nerves

Muscle weakness and atrophy are cardinal features of anterior horn cell disorders – which comprise motor neurone diseases, spinal muscular atrophies, poliomyelitis and other neurotrophic viral infections. Bulbar as well as spinal muscles may be affected. Fasciculations are often a prominent physical sign; reflexes may be brisk or lost, depending on the degree of involvement of upper and lower motor neurones. Anterior horn cell disorders are diagnosed by demonstrating EMG features of acute and chronic partial denervation; central motor conduction studies can be used to reveal pathological involvement of upper motor neurones in the cortico-spinal tracts. Electromyography has a critical role in showing the extent of segmental involvement of denervation, and in identifying subclinical neurogenic abnormality. The peripheral nerve disorder, motor neuropathy with multifocal conduction block (Chaudhry et al. 1994) can mimic motor neurone disease clinically. This immunologically mediated and treatable condition is distinguished by electrophysiological demonstration of conduction block in peripheral motor nerves. Detailed and careful electrodiagnostic assessment is critical, since the conduction block may be in atypical sites such as the mid forearm, or in the very proximal parts of motor nerves. Muscle or myopathic disorders include genetically determined conditions such as limb girdle dystrophy and Duchenne muscular dystrophy, and acquired disorders such as polymyositis and inclusion body myositis. Muscle diseases present with weakness, fatiguability and variable muscle atrophy. Myopathic motor units have a characteristic low amplitude short duration appearance on EMG, although the pattern is not specific to primary muscle disease, being seen in disorders affecting the neuromuscular junction and occasionally in neurogenic processes. The pattern of muscle involvement is an important clue to diagnosis – facial muscles, sternomastoid, spinatii and upper arm muscles are affected in the genetic disorder facio-scapulohumeral muscular dystrophy, whereas quadriceps, tibialis anterior and forearm deep flexor are preferentially involved in inclusion body myositis (IBM). IBM usually presents in older men and may be associated with dysphagia. Its cause is uncertain. Additional EMG findings can help in differential diagnosis of primary muscle disease, although are not specific for aetiology. Thus, fibrillations occur in inflammatory myopathies such as polymyositis; and myotonic discharges are a feature of myotonic dystrophies. There are no electromyographic findings which reliably distinguish between relapse of myositis and drug induced myopathy in patients with inflammatory muscles disease treated with steroids. Case Report: This 21 year old man presented with acute shoulder weakness and scapular winging following an accident while waterskiing. The clinical suspicion was of an acute long thoracic nerve lesion, and this was the referral question when the patient was sent for neurophysiological studies. Needle electromyographic examination of serratus anterior and trapezius was normal, confirming the integrity

Clinical Neurophysiology in Peripheral Nerve Injuries

of the long thoracic and spinal accessory nerves. Instead, EMG revealed myopathic changes (short duration low amplitude and highly polyphasic motor units) in deltoid, brachioradialis, tibialis anterior, peroneus longus, and infraspinatus, leading to a diagnosis of facio-scapulo-humeral dystrophy. This is a primary muscular dystrophy of genetic origin, with autosomal dominant inheritance. The patient was adopted, and had no knowledge of his family history.

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7

Operating on Peripheral Nerves

Operating on nerves: indications for operation; conditions and requirements; general principles of operation; intra-operative diagnosis; methods of repair; neurolysis; approaches to individual nerves; possibilities of intradural repair; ­hazards in entrapment neuropathy; pitfalls in operating on nerve tumours.

7.1 Indications and Objects of Intervention Petrie (2006) defines an experimental study as one: “in which the investigator intervenes in some way to affect the outcome. Such studies are longitudinal and prospective; the investigator applies the intervention and observes the outcome some time later”. The objects of intervention are (1) to confirm or establish diagnosis; (2) to restore continuity to a severed or ruptured nerve; (3) to remove a noxious agent compressing or distorting or occupying a nerve. It is difficult to overstate the significance of worsening of pain and deepening of nerve lesion caused by expanding haematoma or ischaemia. Clinicians must never forget that nerves compressed in a swollen ischaemic limb or in a tense compartment progress from conduction block to much deeper and much less favourable degenerative lesions. Pain persisting after a focal injury to a nerve is an indication for operation at almost any interval after injury. No one should forget the lesson of case 3 in Birch and Strange’s (1990) series. There, exploration and decompression of the sciatic nerve in the notch 3 years after injury was rapidly followed by relief of pain and recovery of a paralysis affecting the common peroneal component. That lesion was of course a conduction block prolonged by external causes. Montgomery et al. (2005) reported a similarly gratifying outcome after neurolysis of the sciatic nerve in a patient who had endured severe pain for a number of years. The lesion was predominantly a conduction block, prolonged and maintained by fibrosis tethering the nerve following total hip arthroplasty. Even more remarkable is the case described by Camp, Milano and Sinisi (2008). The patient suffered intractable and increasing pain for 18 years. Pain was abolished by neurolysis of the ulnar nerve which had become adherent to the pulsatile vein graft used to repair the brachial artery. That lesion was a conduction block, prolonged by external causes: the pain was neurostenalgia.

“It has all been done before” (Holmes 1881). The British Medical Journal of 15 May 1915 carried a report of an address by Inspector-General Delorme (1915) to the Académie de Médecine on the treatment of gunshot wounds of the nerves. In this address most of the procedures to be recommended here are canvassed, including the use of electrical stimulation during operation. Alas! The medical world then was evidently unprepared for Delorme’s proposals, many of which were sharply criticised by the great and good. Bland-Sutton (1930) relates that in the 1870s J. W. Hulke, then surgeon to the Middlesex Hospital in Mortimer Street London, repaired the cut median and ulnar nerves of a woman. Bland-Sutton continues: “The operation was successful and this was the first instance of a successful secondary suture of a divided nerve in London. Surgeons had been afraid to suture cut nerves in this way for fear of tetanus” The harmfulness of delay before repair and the limitations of the different methods of repair have been described in Chapters 3 and 4. Some important practical advantages of urgent exploration include the ease of recognising a rupture and the ease with which the stumps can be approximated. The best time to explore such injuries is before distal conduction is lost (Figs. 7.1–7.3). There is no need to explore the nerve if the clinician expects spontaneous recovery. Seddon (1975a) had this to say about nerve lesions complicating closed fractures of the shaft and the lower end of the humerus: “however, on balance, it would seem proper to await spontaneous recovery of the nerve, provided the two conditions are satisfied. The first is reasonable apposition of the bony fragments, and the other complete certainty that there is no threat of ischaemia of the forearm muscles”. If however, the clinician elects to convert a closed fracture to an open one by internal fixation, then it is wisest to expose nerves which are not working. The fracture surgeon who does not do this is asking for trouble (Fig. 7.4). We define primary repair as one performed within 5 days of injury and delayed primary repair

R. Birch, Surgical Disorders of the Peripheral Nerves, DOI: 10.1007/978-1-84882-108-8_7, © Springer-Verlag London Limited 2011

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for one completed at intervals from 5 days to 3 weeks after injury. Secondary repair is performed at between 3 weeks and 3 months after injury. Late, or neglected, repair is reserved for those cases where delay exceeds 3 months.

7.1.1 Special Units: Their Role

Fig.  7.1  Ease of diagnosis at operation done soon after injury. Incomplete transection of the femoral nerve occurred during a difficult pelvic operation. The surgeon recognised the event and enabled display and repair 24 h after wounding.

From 1956 onwards primary suture of severed nerves was practised at St Mary’s Hospital whenever it was possible. This policy was extended to revascularisation of damaged limbs, to replantation of amputated hands and severe injuries of the brachial plexus. With growing experience it became obvious that Special Units would evolve to provide opinion and treatment without delay. These require the constant availability of adequately supported senior advice. It is essential that all members of staff understand the overriding purpose of such a Unit which is to provide urgent advice and

Fig.  7.2  Ischaemia and conduction. Traction lesion of the brachial plexus was accompanied by rupture of the subclavian artery. There was a weak pulse. At operation, 54 h after injury, stimulation of the avulsed ventral roots of C7, C8 and T1 evoked strong contraction in the relevant muscles distally. This showed that there was neither critical ischaemia

within the limb nor that there was a second, more distal, lesion. Strong SSEP’s were recorded from the stumps of C5 and C6 (1). The dorsal root ganglia of C7, C8 and T1 (2) and their ventral roots (3) are shown. An extensive repair was done (Case investigated and referred by Mr Tanaka and Mr Shandall, Royal Gwent Hospital).

Operating on Peripheral Nerves

Fig. 7.3  It is often very hard to determine from inspection alone the nature of the injury in delayed or neglected cases. Ten weeks after a severe lesion of C5, C6 and C7 it was not possible to distinguish between rupture and avulsion. The phrenic nerve (1) suprascapular nerve (2) and the neuroma (3) are seen.

Fig. 7.4  The explanation for persisting painful median palsy in a 7 year old child after fracture of distal humerus, which had been treated by “closed” wiring, was revealed when the nerve was found embedded within the bone 11 months later (Courtesy of Mr Roderick Dunn, Salisbury).

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organism before admission and MRSA carriers are treated in isolation beds. Emergency admissions are admitted into single rooms until their MRSA status is known. Elective admissions are stopped if the number of positive MRSA cases exceeds the number of single rooms available. This admirable policy of segregation is not a new one. Rodger (2004) describes how the building of the Royal Naval Hospitals at Haslar (Portsmouth) and at Stonehouse (Plymouth) came about because of the perceived need to control epidemics of typhus: “At a cost of over £100,000…. Haslar provided for the highest standards of medical care, careful segregation of infectious diseases, and (not least) careful guard against the risk of desertion. Haslar, and even more the second naval Hospital, Stonehouse near Plymouth (finished in 1762), the first to be built on the “pavilion” system with separate blocks isolated from one another, became a model studied and copied all over Europe”. Those responsible for the control of hospital infection might learn something from recent Naval experience: “throughout the eighteenth century British naval officer’s fanatical attention to cleanliness of their ships and men aroused the astonishment of visiting foreigners, but it had unquestionably good results in limiting disease” (Rodger 2004). The difficulties and the obstacles faced by Special Units are increasingly severe but they must have an important role particularly in the treatment of severe injuries to the brachial and lumbosacral plexi and also in the treatment of iatrogenous injuries. Special Units must work closely with the referring hospital to ensure continuity of care through the process of rehabilitation and they should provide good records drawn from adequate follow up with thorough audit. One object of a Special Unit is to plan its own demise by training surgeons to take on the work in their own hospitals.

7.2 General Principles of Operation 7.2.1 Control of Bleeding

urgent treatment. Systems were developed to facilitate hospital to hospital transfer (Giddins et  al. 1998). The work of such Units require commitment and support from hospital managers as it must from those senior to whom they must answer. Such support unfortunately appears to be less and less forthcoming as Bircher et al. (2006) point out when they relate the difficulties imposed upon their work with patients with fracture dislocations of the pelvis. Bircher et al. (2006) cite interference with referrals, the imposition of waiting time targets, and the failure to provide isolation beds to cope with the problem of hospital acquired infection. The last of these is a serious and growing problem. Nixon and his colleagues (2006) describe their policy for the control of methicillin resistant staphylococcus aureus (MRSA) infection in orthopaedic wards. All elective patients are screened for the

The development of methods to control bleeding is described, with graceful scholarship, by Kirkup (2007) in “A History of Limb Amputation”. Petit’s screw, invented in 1718 “dominated practise for more than two centuries, being still available during World War I”. Crumplin and Harrison (2005) relate how Nelson lost his right arm at Santa Cruz in 1795. He was struck on the right elbow by either a canister round or a musket ball: “he was bleeding, and Nisbet, after concealing this with his hat, removed his silk stock and bound the Admiral’s arm above the elbow to control the haemorrhage, so saving the Admiral’s life”. Blutleere (bloodless) surgery, introduced by Esmarch (1873), was advocated by Stromeyer (Smith 2006) who commented “in Edinburgh, some opposition was shown, as usually happens with everything that is admired in London”.

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Crumplin (2007) describes how Guthrie, from 1808, controlled the subclavian artery by digital compression against the first rib. Hennen (1820) recorded that in one case of shoulder disarticulation at the Battle of Vitoria (1813) “the amount of blood loss from the principal artery was no more than the quantity contained between the point of pressure and the point of incision through the vessel”. Digital compression of the femoral artery at the groin was used to control bleeding in the first successful case of disarticulation at the hip. Hennen (1820) described a successful case operated 19 days after injury, at Waterloo and he observed that “the haemorrhage was very little more than in the common amputation with the tourniquet”. The emergency control of bleeding by pressure is an art to practice for we have seen cases where patients were close to exsanguination following stab wounds to the axillary or brachial, or to the superficial femoral arteries. Such extreme blood loss might have been reduced by firm pressure above and below the wound. The tourniquet is potentially dangerous. One of us, as an aspirant surgeon, was asked what was the correct course of action should a surgeon realise that a tourniquet had been left, inflated, overnight after an operation: the correct answer was that the tourniquet should be left inflated, and that the surgeon should speak with the Presidents of the Colleges of Surgeons before proceeding to amputation of the limb. Such a catastrophe is inconceivable nowadays but we are indebted to Professor Averil Mansfield for the observation that the use of a tourniquet in a limb in which an arterial prosthesis has been inserted, is absolutely contra-indicated. It seems that the implant is insufficiently elastic to dilate after release of the cuff; also, collateral circulation is likely to be defective. Tourniquet times must be reduced in patients with rheumatoid arthritis, diabetes mellitus, alcohol addiction or other possible causes of neuropathy. In many such patients it is best to avoid altogether the use of a tourniquet. Klenerman (2003) provides an important manual about tourniquet use. The superficially attractive idea of temporary release of the tourniquet is undermined by Concannon et al. (1992) who studied patterns of free radical production after tourniquet ischaemia. Post operative pain is worsened by the tourniquet by longer periods of ischaemia and in older patients (Ömeroglu et al. 1998). The duration of application, inflation pressure and site of application should be always recorded in an ordered operating note and the times of application and release should be written on board in the operating theatre and in the case notes. The duration of tourniquet ischaemia is reduced by inflating the cuff after preparation and towelling of the limb. We prefer Lister’s (1879) method of elevation of the limb before inflation of the cuff to the exsanguinating bandage. Because these operations are usually time-consuming, it is especially important adequately to protect the pressure points at the knee, the elbow and elsewhere with suitable padding. In operations on the nerves of the neck in particular, special care

Surgical Disorders of the Peripheral Nerves

must be taken to avoid air embolism, to recognise it if it does occur and to be prepared to deal effectively with any such occurrence. In the case of severe injuries to the brachial plexus, when there may be a sudden release of spinal fluid, it is necessary to be prepared quickly to alter the position of the patient to avoid “coning” of the medulla. If it seems likely that nerve or vein grafts are going to be needed, the donor sites should be prepared and monitoring equipment, arterial and venous lines and the the drapes should be placed accordingly.

7.3 Apparatus and Instruments Most operations on injured peripheral nerves are best done with general anaesthesia. If the anaesthetist uses a muscle relaxant must be prepared to reverse its effect when the nerve stimulator/recorder is being used. Special apparatus required includes bi-polar diathermy, stimulating and recording apparatus and instruments for magnification. Neurophysiological examination: “It is astonishing that in this age of technological idolatory, exploration of nerves is still being performed without the aid of this instrument” (Seddon 1975b). Seddon refers here to a simple nerve stimulator. Nerve stimulation and the recording of nerve conduction is used to (1) identify the nerve, (2) to identify individual bundles within a nerve or in a prepared stump, (3) to demonstrate conduction across a lesion and (4) to record continuity between the central and peripheral nervous systems. Intraoperative neurophysiological studies have been performed in more than 4,000 operations since 1953. For simple stimulation and observation of motor response only the simplest uni- or bi-polar stimulator is necessary. For stimulation and recording from muscle and nerve, more elaborate apparatus is required. We now use the Medelec synergy monitoring system (Vaisys Health care, Madison, Wisconsin, USA) (Fig.  7.5). The electrodes are provided by Ambu, Ballerup, Denmark. In measuring conduction across a lesion, hand held bi-polar stimulators are placed on either side of the lesion. The ground electrode can be placed in a convenient adjacent area. The interval between the electrodes and between each electrode and the lesion is measured. Kline et al. (2008a) relate further experience with this method in an extensive and authoritative manner, describing findings in nearly 2,300 patients operated between 1967 and 2001 (Fig. 7.6). For recording somatosensory evoked potentials (SSEP’s) the reference electrode is placed on the forehead, the ground electrode at the temple, and the recording electrode on the skin overlying the second or third cervical intervertebral space. The skin is prepared with abrasive paste and alcohol wipes to lower resistance with the object of balancing impedance between reference and recording electrodes, at a level

Operating on Peripheral Nerves

Fig. 7.5  The apparatus for recording sensory evoked potentials.

less than 2.0 kOhms. Once the surface electrodes are positioned they are secured with tape. A hand held stimulator is used to record signals from the median and ulnar nerves before preparing and towelling the upper limb, using the uninjured side as a control. A sterile hand held bi-polar stimulator is used to stimulate the nerve directly. Somato-sensory evoked potentials (SSEP) are recorded using a stimulus rate of 3–5 pulses per second, of duration 2.0 mS, and intensity 150–300 V. Signals are averaged from between 50 and 200 sweeps. The stimulus rate for the hand held bi-polar stimulator is 3–5 pulses per second. The quality of the traces may be adversely affected by a number of factors. Ambient noise interference from electrical equipment in the operating theatre was a particular problem in the operating theatres at St Mary’s Hospital. Difficulties are encountered when nerves are embedded in dense fibrosis

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or the operating site is permitted to become too wet or too dry. Compression of nerves by haematoma causes anoxic conduction block. SSEP’s are relatively unaffected by most anaesthetic agents, but muscle relaxants block neuromuscular conduction (Fig. 7.7). We have no experience with transcranial electromagnetic evoked potentials (TCEMEP) during operation. Schwartz and colleagues (2007) observed that changes in TCEMEP appeared some minutes before alterations in somato-sensory evoked potentials (SSEP) during operations on the deformed spine. By this method, Lee and colleagues (2006) detected anterior haematoma in two cases of anterior fusion of the cervical spine. The first case was diagnosed by a sudden fall in amplitude of TCEMEP. Improvement in TCEMEP correlated with recovery of the cord in the second case. Lee et al. conclude that: “TCEMEP is… proving to be considerably more sensitive than conventional SSEP monitoring which carries an unacceptably high rate of false negative results in cervical spinal surgery”. Magnification: the operating microscope was used by ophthalmic and ENT surgeons for decades before its regular use in orthopaedic and plastic surgery (Nylen 1972). The discipline of microsurgery seems to have acquired a mystique which is not altogether justified. The elements of microsurgical technique are no more than the application of basic surgical skills. They are acquired by practice. (Birch 1987). For magnification we use loupes or the operating microscope. The microscopes are OPMI 6SD FC and OPMI 6 (both Carl Zeiss, Oberkochen): the stand is the universal S3B (Carl Zeiss, Oberkochen) Instruments: Stromeyer (Smith 2006) commented: “I used my stay in London to buy surgical instruments for the Freiburg clinic at Weiss and Fergusson. They were excellent. Professor Hecker, when he amputated for the first time with an English knife, was quite alarmed at its sharpness.” Our earliest micro-instruments were bought from John Weiss of Wigmore Street, and Dumont’s watch makers forceps were bought, ten at a time for £12, from the jewellers of Hatton Garden. Probably the best of the early microsutures was that developed by Owen (1975) who swaged a 4 mm needle onto a 10/0 perlon filament. The Joll’s thyroid retractor is excellent for reflection of skin flaps in the neck. The small Deaver’s retractor is useful in the neck. A set of malleable retractors are essential. Conventional toothed self retaining retractors are avoided, because of the risk to nerves and vessels. Three sizes of vascular clamps are used. The Satinsky clamp is especially useful in end to side anastamosis. DeBakey’s scissors and forceps are used for both arterial and nerve work. The range of sutures includes: 6/0, 8/0 nylon on a 6 or 8 mm vascular needle and 8/0, 9/0, 10/0 and 11/0 on a 4 mm or a 6 mm needle used with the appropriate needle holders. Howarth’s dental elevator and Lemperts raspatory are very good for fine bone work. A range of spinal punches,

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Fig. 7.6  Severe pain and deep paralysis complicated closed dislocation of the gleno-humeral joint in a 78 year old woman. The nerves were exposed 3 months later; there were no ruptures. CNAP and SSEP were recorded traversing the lesions of median, ulnar and musculocutaneous nerves. They were absent across the radial nerve. Recovery through the radial nerve extended only to the triceps and flexor to extensor transfer was performed later. The other nerves recovered, there was early relief of pain.

angled bone nibblers and bone cutters are needed. Plasma “glue” (Young and Medawar 1940, Tarlov 1944) was regularly used in our hospitals until the early 1980s when the raw material became unavailable. A commercial product was reintroduced which is now used, (Tisseel (TM) Immuno Ltd, Arctic House, Rye Lane, Dunton Green, Sevenoaks, TN14 5HB). The aprotinin must be diluted with sterile water: otherwise there is a risk of inducing fibrosis. The undiluted preparation is reserved for haemostasis. The needle tip should be directed away from the repair to avoid disruption. A steady

gentle pressure is exerted so that a film of the fluid bathes the repair and seals it . Fibrin clot glue acts as an envelope around the nerve but offers no resistance to tension. Narakas (1988) found that the proportion of good results of his nerve repairs was increased by 15% after turning to fibrin clot glue. Prevention of Pain: Surgeons can and should do more to prevent post operative pain. The complications of blind nerve or regional blocks can be severe (Chapter 3). Henry (1975) describes his technique of thigh amputation without tourniquet or general anaesthetic by a method first described before

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Fig. 7.7  Examples of normal and abnormal SSEP traces.

the Second World War: “so, after infiltrating areas of flap or cuff, and all the operative field – most thoroughly- with procaine (0.5%), we can in comfort see and block the great sciatic trunk”. Then follows ligation of main vessels and then: “during these activities, however, the great sciatic trunk will rest in peace – until the time comes to remove the limb. With procaine infiltration, not less than 20 min must elapse before injecting and dividing this capacious conduit of shock impulse. And that, indeed, is little time enough”. Surgeons can and should do a great deal more to diminish postoperative pain by the simple and safe expedient of infiltration of the line of incision and the skin on either side, with local anaesthetic. We use a preparation of Levobupivicaine 0.25%, with adrenalin 1:200,000. The maximum dose is 2 mg per Kgm body weight. It is a simple matter to infiltrate the tissues around the

supraclavicular nerves and to inject local anaesthetic into the joint itself for operations at the shoulder. If amputation of the lower limb is indicated because of a deformed and painful foot, a circumferential block of the skin of the mid thigh is made before exposing the sciatic nerve. This is bathed in local anaesthetic infused through an epidural catheter, with its tip adjacent to the nerve, before proceeding to amputation. The infusion is maintained for 48 h after operation. Other nerves are infiltrated with local anaesthetic before cutting them. The use of prolonged nerve block in the treatment of the painful nerve lesion is outlined in Chapter 12. Incisions need to be adequate and, where possible, extensile. There is no place for short incisions. Main nerves and major vessels are exposed first proximal to the lesion and then distal to it. The lesions are displayed by dissection from

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Mandibular br. of facial n.

Surgical Disorders of the Peripheral Nerves

Lesser occipital n. Splenius capitis Great auricular n. Spinal accessory n.

Transverse cervical n.

Sternocleidomastoid m.

Supraclavicular n.n.

Trapezius m.

Fig. 7.8  Some of the more important superficial nerves in the neck. Note that the mandibular branch of the facial nerve comes at one point below the lower margin of the mandible. The cervical branch has been omitted.

above and below. All tissues must be treated gently. They are, after all, alive, and on their continued viability depend the healing of the wound without infection and the recovery of the nerve lesion. Indeed, avoidance of infection probably has more to do with tender handling of the tissues and accurate haemostasis than has the administration of antibiotics. The line of the proposed incision should be marked and cross-hatched and be planned with cutaneous innervation in mind. Lasting trouble can follow wounding of an apparently trivial cutaneous nerve; it is an ill matter for a surgeon purporting to assist healing of lesions of peripheral nerves to damage one set of nerves on the way to repairing another (Figs. 7.8 and 7.9). In the neck, the skin flaps should include

the platysma; elsewhere, they should be cut to full thickness. Skin flaps should be held with fine skin hooks; if the procedure is going to take a long time, the flaps should be sutured back to the surrounding skin. So far as possible, dissection should be done with the knife or with sharp blunt-ended scissors. Although in the limbs the pneumatic tourniquet can be used during dissection and exposure, it must be released for stimulation, repair and closure. The best possible haemostasis must be secured after the cuff has been deflated, by diathermy, ligation and haemostatic sponge. Cut bone surfaces should be sealed with wax or similar preparation. Once the flaps are raised, the field should be kept as free of blood as possible, but it must be kept moist by regular irrigation. Even well shielded operation lamps generate enough heat to accelerate desiccation of the tissues. When muscles have to be divided, their ends should be marked with sutures and if necessary labelled, so that when the procedure is completed they can accurately be re-united. Nerves should be handled with extreme care; retracted with very fine skin hooks in the epineurium or with plastic slings. Colour coding of the slings adds pleasing variety to the proceedings and, more importantly, permits the surgeon to identify to the assistant the nerve to be retracted. They should not be mobilised over such a length as to impair their blood supply. The wound should not be closed before bleeding points have been checked; even with good haemostasis it is wise to use a suction drain in most wounds. However, the business end of the drain should not be placed near the site of repair, for fear of damage to the anastomosis by the suction or by later withdrawal of the drain. Divided muscle layers should be repaired accurately and securely. In the neck the platysma should carefully be closed with interrupted sutures. Although with careful handling of tissues wound infection is rare, the exposure is often so much prolonged that prophylactic use of antibiotics is advisable. Such cover should always be used if there is any liability to ischaemia or if there is an associated fracture. We use antibiotic cover (cefuroxime 750 mg intravenously three times in 24 h starting just before operation) in all cases of major intervention

Extensor pollicis longus

Fig. 7.9  Radial side of the hand, with further warning about the terminal branches of the radial nerve and lateral cutaneous nerve of forearm (see also Fig. 1.29).

Extensor pollicis brevis

Dorsal carpal branch of radial a.

Abductor pollicis longus

Extensor carpi radialis longus

Extensor retinaculum

Lateral cutaneous n. of forearm

Superficial radial n.

Operating on Peripheral Nerves

on the brachial plexus, in all compound nerve injuries, in interventions on the proximal part of the sciatic nerve and in most second operations on main nerves. The record should carefully be maintained: it is best to follow a standard form and to supplement this with a diagram and photographs. Under no circumstances must descriptions of the lesion, of the state of the stumps after resection or of the gap after resection be omitted. The operation record should be written or dictated by the operating surgeon as soon as possible after completion of the procedure. The first copy is retained with the medical case notes, a copy is sent to the family practitioner, another to the referring clinician, and the final copy is stored with files of coded operating records (Figs. 7.10 and 7.11).

7.4 Methods of Repair There are remarkable similarities between the technique of repair of nerves and vessels. In arterial injury the first principle is rapid control of the vessels proximal and distal to the wound. Whilst the situation is less urgent in nerve repair, the nerve should be exposed first in healthy tissue above and below the level of lesion. Damaged vessel and nerve must be resected, the repair will fail unless healthy tissues are coapted. Undue tension guarantees failure. Adventitial tissue must be resected to expose the media and the epineurium (Fig. 7.12).

7.4.1 The Vascular Repair Of combined venous and arterial injury Barros d’Sa (1982) says: “ligation (of the vein) should be avoided at all costs. A vein tolerates lateral suturing much better than an artery. At least one major channel of satisfactory calibre must be restored so as to avoid a serious rise in peripheral venous resistance and pressure which reduces arterial flow to the limb and can lead to thrombosis at the site of the arterial repair with disastrous consequences. In combined venous and arterial injury, the vein should be repaired first”. Having secured proximal and distal control of the injured vessel any associated fracture or dislocation must be neutralised as rapidly as possible. A Rush nail, passed from proximal to distal provides rapid and adequate stability of the humerus before repair of the axillary or brachial artery. Direct suture is sometimes possible in the fresh stab wound; a vein patch is better than lateral suture at the mouth of a false aneurysm. Interrupted sutures are preferred to continuous suture to reduce the risk of stenosis at the suture line, ease co-aptation of vessels of different diameter, and facilitate end to side suture.

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Division of the axillary and brachial sheath and of the deep fascia of the forearm is essential in all cases save those where a simple wound is successfully sutured within 3 h of injury. Subcutaneous fasciotomy of the forearm is adequate if there is no distal injury of elbow and forearm. The deep fascia of the forearm is exposed through a short incision on the medial side of, and parallel to, the biceps tendon. The skin is retracted and the plane between it and the deep fascia is gently developed by blunt dissection. The fascia is now incised and the plane deep to it opened out in a similar manner so that the fascia can be split safely using blunt tipped scissors. In more severe cases a fasciotomy should include the skin: this is usually susceptible to delayed primary closure at about 48 h. The indications for fasciotomy are more stringent in the lower limb. Barros d’Sa (1992) emphasised that decompression of all four compartments of the leg is essential in repair of shot gun wounds to the popliteal vessels. This principle should be followed in closed lesion complicated by fractures of the tibia or deep contusion of the muscles. We use two incisions. That over the fibula exposes the deep fascia enclosing the anterior and lateral compartments. The medial incision starts just above the midpoint between the medial malleolus and the Achilles tendon and extends to the upper leg. It is very important to identify and to open the fascia over the deep flexor compartment. Repair of Artery or Vein: Both proximal and distal vessels can be infused with heparinised saline but systemic anti-coagulation is not used. The proximal and distal stumps of the vessels are securely controlled by plastic slings and appropriate clamps. A skilful and patient assistant is charged with controlling the clamps and adjusting their position. Adventitia is removed after confirming back flow from the distal stump of the vessel. Repair is by interrupted sutures, 5/0 or 6/0 nylon for the subclavian, axillary, femoral or popliteal arteries, 7/0 or 8/0 for brachial, radial, ulnar and tibial arteries. The first two sutures are placed at the equator. It is often easier to repair the posterior wall first before turning the clamps to expose the anterior wall. The sutures pass through the media and the intima at intervals of about three quarters of a millimetre. The reversed vein graft. This is taken from an uninjured limb where possible. The long saphenous vein in the leg is best for larger arteries. The prepared stumps of the artery are gently drawn together and the gap between them measured, then the vein graft is prepared to match that gap. A very light touch must be used in handling the vein. Diathermy should not be used on the small branches. The proximal vessel is tied off leaving a long strand of suture to indicate that this must be placed distally during the repair. A flexible cannula, mounted on a syringe, is introduced into the distal stump of the vein and secured with another tie. The segment of the vein is distended with heparinised saline. This reduces spasm. End-to-side anastomosis is used when there is disproportion between the stumps of the

240 Fig. 7.10  An example of an operating record.

Surgical Disorders of the Peripheral Nerves

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Fig. 7.11  A further example of operating record.

vessels (Fig.  7.13). Bleeding from the suture lines is best controlled by pressure for several minutes before inserting further sutures. The repaired vessel should be kept exposed for as short a time as possible and kept moist at all times. Nerve grafts must be elevated as swiftly as possible and much of this can be done whilst the arterial repair is underway. “Plasma” glue is invaluable in these cases, for its saves a great deal of time.

7.4.2 The Nerve Operations 7.4.2.1 Neurolysis A good deal of the argument about the value of “neurolysis” arises from imperfect definition of the term. We owe a great deal to Frykman and colleagues (1981) for their

clarification of this matter. They plainly showed the amount of fibrosis that follows so simple a procedure as interfascicular injection of saline; that which follows interfascicular neurolysis is certain to be more severe. That is not the only danger: their investigation was prompted by paralysis after a very careful interfascicular neurolysis of a radial nerve. External neurolysis is the freeing of the nerve from a constricting or distorting agent by dissection outside the epineurium. The first description of external neurolysis remains one of the best. Horsley (1899 ) operated on a cavalry officer who had dislocated his knee 8 months previously whilst putting his horse at a fence. The patient had returned to active service in spite of a persisting complete common peroneal palsy. There was extensive scarring in the popliteal fossa and the lateral aspect of the thigh. Horsley wrote: “I suggested that as a preliminary measure he could try massage, but that proved no good, and therefore I

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Fig. 7.12  Rupture of axillary artery from fracture/dislocation in a 68 year old man. The atheromatous intima was fractured. A reversed vein graft was necessary after resection back to healthy intima.

Surgical Disorders of the Peripheral Nerves

determined to cut down upon it. I raised a flap of skin, and found the nerve was not only involved in a scar for about 7 in., but for about 3 in. of its course was greatly reduced in size. After dissecting it quite free from the scar I removed all the scar tissue I could and laid the flap of skin back again over the nerve, which by this time looked a great deal the worse for wear. To make a long story short, he has now recovered motion and sensation in the parts supplied by the external popliteal, after about an interval of a year or 13 months after the operation”. External neurolysis is especially valuable when the nerve is intact but tethered, strangled or immobilised by scar. Pain (neurostenalgia) is usual in such cases and relief of pain with improvement in function is regularly seen after external neurolysis and decompression. External Neurolysis after Repair or Amputation. Neurolysis is usually fruitless in a nerve which has been repaired. The decision to revise that repair is governed by failure to progress, persisting pain and a static Tinel sign (Fig.  7.14). However, it is not uncommon to find that the function regained after successful suture of the median or ulnar nerves at the wrist is marred by pain because the nerve has become adherent to the adjacent flexor tendons. Pain is worsened by movements of the digits and the neuroma can be seen moving up and down during flexion and extension. Liberating the nerve by incision of adhesions is often successful but a bed of healthy synovium must be restored. A

Fig. 7.13  Reversed vein grafting in the axilla: end-to-side (above) and end-to-end (below).

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7.4.2.2 Biopsy

Fig. 7.14  Futile neurolysis. Poor recovery after primary suture of an ulnar nerve. The nerve was re-explored at 8 months. A CNAP was detectable and neurolysis was done. There was little recovery.

neuroma which has become adherent to the scar over an amputation stump is often extremely painful. Again, liberation of the nerve from scar, which may require cutting the nerve again so that the stump lies in healthy tissue usually relieves the pain. Epineurotomy: means the simple division of the epineurium in the line of the nerve and it probably has a limited place in cases of damage from injection of a noxious substance near a nerve or by localised pressure on a nerve, which has produced localised thickening and fibrosis of the epineurium. Unhappily, the fibrosis is unlikely to be limited to the perifascicular epineurium: there is likely to be fibrosis of the interfascicular epineurium too. The place of epineurotomy in radiation neuropathy is uncertain. The most that can at present be said for it is that when done carefully it is unlikely to do any harm.Internal neurolysis or inter fascicular neurolysis is the exposure of the bundles by epineurotomy and their separation by dissection between them or by the removal of interfascicular scar tissue. It is an essential part of three important procedures: (1) separation of intact from damaged fascicles in nerves which have suffered partial damage; (2) separation of a motor fascicle of a nerve for transfer; (3) separation of intact fascicles during removal of a benign but infiltrative tumour. Nagano and colleagues 1996 show that it may be required in at least one entrapment syndrome.The traction lesion in continuity is a common finding at exploration and it is very difficult. The nerve, which is usually in the axilla or at the knee, is exposed after a severe closed traction injury, and is found elongated by one third or more. The epineurial blood vessels are torn, but the perineurium and individual bundles appear intact. The damaged segment may exceed 25 cm. in length and resection and repair of such extensive lesions is scarcely feasible. Useful recovery occurs naturally in one third to one half of these injuries (Chapter 8). It seems that the damaged segment acts as an imperfect graft because the perineurium is in continuity and some, at least, of the Schwann cells survive.

Biopsy of a nerve requires removal of portions of conducting tissue and it necessitates at least epineurotomy and excision of one or more bundles so that the perineurium and its contents are made available for examination. Biopsy may extend to the entire nerve. The examination of teased single nerve fibres was reintroduced by JZ Young and PK Thomas and this method has greatly enhanced understanding of peripheral neuropathies (Dyck and Thomas 2005). Nerve biopsy is neither trivial nor without risk and it should never be a matter of unthinking routine. Dyck et  al. (2005) provide a detailed account of biopsy of one fascicle from the sural nerve and the experience of one of them, who underwent the procedure, provides a salutary example of persisting pain and sensory disturbance after a meticulously performed biopsy. One of our patients, a 52 year old woman with chronic inflammatory peripheral neuropathy experienced increasing pain and a deepening sciatic neuropathy raising the possibility of plasmacytoma. One fascicle of the nerve was biopsied. On the following day she noted a virtually complete but painless, sciatic palsy. Haematoma was excluded by ultrasonography and by reexploration. The biopsy excluded plasmacytoma and it seems that an apparently relatively innocuous intervention in which a segment of one fascicle of the sciatic nerve was removed induced a dense ischaemic lesion of the whole trunk. It is in the investigation of nerve tumours that the greatest errors are seen. Case Report: A 43 year old woman presented with a 3 year history of intermittent abdominal symptoms; a mass was palpable. MRI showed a large tumour in the retroperitoneum, extending from L1 to the sacrum. A diagnosis of soft tissue sarcoma was made on the basis of a needle biopsy and the mass was excised, including a segment of the lumbo sacral plexus L4, L5 and S1. Chemo-and radiotherapy followed, complicated by a massive pulmonary embolism. We reviewed the histological material: the diagnosis was revised to a benign schwannoma. The patient now has profound weakness of the abductors and extensors of the hip, paralysis of the dorsi flexors of ankle and foot, weakness of quadriceps and other muscles of the lower limb. She is able to walk 50 yards with two sticks. Knight and her colleagues (2007) described the complications attending biopsy, usually by fine needle, in 53 patients with benign solitary schwannoma. 1. Eight biopsies failed to yield diagnostic material. 2. Ten biopsies removed portions of normal nerve. 3. An erroneous diagnosis of a soft tissue sarcoma was made in two core needle biopsies. 4. Most patients experienced significant or severe pain as a result of the biopsy and there was significant loss of function in 22 of them. 5. Fibrosis induced by the biopsy distorted the tissue planes of the nerve and added greatly to the difficulties of later enucleation of this benign tumour.

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leaving the nerve well alone, closing the wound and referring the patient to an interested colleague. We emphasise the importance of frozen section biopsies during resection of MPNST which are essential in proving an adequate margin of resection. Santos-Pallazzi (1991) of Barcelona, has, for many years, examined specimens from the stumps of ruptured spinal nerves by frozen section which has enabled him to classify the potential for regeneration by the amount of fibrosis. Gschmeissner et al. (1991) offered a 2 min assessment of the quality of the stumps by examination at frozen sections.

7.5 The Nerve Repair Fig. 7.15  Biopsy of a benign lesion of the femoral nerve caused severe pain and complete paralysis of the extensor muscles of the knee. No action was taken for 10 months. The first surgeon did not examine the specimen. Histological findings: fascicles of a main nerve.

It is important for the surgeon who comes to treat such lesions to ask to see the sections taken from the material removed at the primary operation. Often enough, a cross ­section of a trunk nerve is included in the specimen (Fig. 7.15). Geisinger and Abdul-Karim (2001) emphasise the limitations of fine needle aspiration biopsy of soft tissue tumours. The sample may not be representative of the tumour and it may prove insufficient to make a diagnosis. There is no justification for biopsy in tumours of nerves which are clearly benign. The clinical features supported by the findings from MR and US scanning enable the accurate diagnosis of nearly all cases of schwannoma and intraneural ganglion. An incorrect diagnosis of a benign lesion in malignant peripheral nerve sheath tumour (MPNST) may cost the patient his or her life because of dissemination of tumour from the nerve into adjacent soft tissues or because of the continuing extension of the tumour during the months before the correct diagnosis becomes all too clear. We have seen ten such cases and in five of these the initial error, compounded by delay, lost the chance of adequate surgical excision. Whilst biopsy is essential in cases in which there is any doubt about diagnosis and in particular in those where there is a possibility of primitive neurectodermal tumour, neuro-epithelioma or extra osseous Ewing’s tumour, we think that such biopsy is best performed within the Institution where definitive treatment will take place. The possibility that the tumour is catecholamine secreting should be considered in adrenal and extra-adrenal retroperitoneal lesions (Sood et al. 2007). It is for the responsible surgeon to decide whether biopsy is needed and which method is used. It is the responsibility of that surgeon to examine the biopsy tissue with an experienced pathologist. Surgeons do not always get things right, neither do radiologists or pathologists. We believe that a surgeon encountering an unexpected tumour within a nerve, one which is not evidently a benign schwannoma will do no harm in

The object of nerve repair is the accurate coaptation of healthy conducting elements without tension. In practical terms this means accurate coaptation of the bundles (Birch and Raji 1991). This is done after skeletal injuries have been stabilised and vessels repaired, and after muscles, tendons, joint capsule and synovium have been drawn together so restoring gliding planes. Cover by healthy full thickness skin is essential. In delayed repair the incision is planned so that a skin flap is raised over the nerve (Fig. 7.16). Once the decision is made for or by the surgeon, the nerve ends are cut back progressively until healthy pouting bundles show in the cut surfaces (Fig. 7.17). Resection is less in urgent repairs. No more than 1–2 mm of nerve is removed in tidy wounds. Finding the right level of section in the closed traction rupture or in the untidy wound is much easier in urgent repairs where there is still conduction in the distal trunk. In ruptures of the spinal nerves, the stimulator is moved slowly from the rupture towards healthy tissue until an SSEP becomes detectable (proximal stump), or, until muscular activity returns (distal stump). This usually coincides with a healthy looking nerve face. In traction ruptures, the amount of tissue resected usually lies between 5 and 10 mm. More nerve must be resected in late

Fig.  7.16  A tidy wound. Primary repair of all divided structures is indicated.

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2. It is impracticable to bridge with grafts gaps in lesions of the whole sciatic nerve. Sufficient graft material is not available. The gap has to be closed by flexion of the knee and extension of the hip and later maintenance of that position for the appropriate time. 3. Anterior transposition of ulnar or radial nerves gives at most 3 cm. 4. No gaps in the median nerve in the forearm can be closed by end to end suture. Ideally, it is best to match bundle to bundle, sensory fibres to sensory fibres and motor fibres to motor fibres. It is often easy to match bundle to bundle simply by looking at the nerve end under the microscope or with the loupe, though the changing architecture of the nerve along its length makes this difficult when a long gap has to be bridged. When operation is done soon after injury, it is easy, as Vandeput and colleagues (1969) suggested, to determine the sites of motor fascicles in the distal stump and to effect an “electrophysiological orientation”: Certainly Kato and his colleagues (1998) improved anatomical matching in repair of low median and ulnar nerve lesions by displaying individual bundles and orientating them by electrical stimulation. However, the late distinction between motor and sensory fibres requires more advanced methods. The possibilities of histochemical identification of nerve fibres are reviewed by Brushart (1999). Fig. 7.17  Good stumps after resection in traction injury of the radial nerve. Below: The rupture displayed: Above: resection is done back until clearly separated “pouting” bundles are visible.

cases. When the case has been complicated by infection as much as 4 cm of proximal and distal stumps are irretrievably fibrosed. Palpation of the nerve detects the difference between soft, healthy tissue from the firm or hard, scarred segment. Then the ends must be united, preferably by end to end suture. So long as the gap after resection is small, little mobilisation of the nerve is needed to close it, and the repaired nerve lies without tension, without excessive flexion of adjacent joints. One simple test as to the advisability of direct suture of a nerve trunk at the wrist or in the forearm involves passing an epineurial suture of 7.0 nylon, with the wrist flexed to no more than 30°. If this suture will draw the stumps together without tearing the epineurium and without causing blanching of the epineurial vessels, then suture is reasonable. Failing that, grafting is necessary. It will be seen that in many circumstances it is better to bridge a gap with a graft than to force direct suture; it is better to resect to healthy bundles and create a wide gap than to resect too little in order to facilitate direct suture. We take as guides the following principles: 1. End to end suture of the nerves of the brachial plexus above the clavicle or of the accessory nerve is rarely practicable.

7.5.1 Methods of Suture Orgell (1987) described a modified fascicular suture: “group fascicular suture” and he concluded that since there was little difference between the results of epineurial and perineurial suture, epineural suture was “the technique of choice for most acute nerve lacerations.” He pointed out that it was easier and faster and entailed less manipulation of the internal structure of the nerve than did fascicular suture. Spinner (2008) thinks that “fascicular” suture is useful in distal median and ulnar repairs and he emphasises that the most important cause for failure of suture is “inadequate resection of injured nerve back to healthy tissue”. During urgent or emergency operation the surgeon should indeed proceed to a neat epineurial suture using 6/0 or 7/0 sutures or to immediate grafting if circumstances permit. We have seen many excellent results following this approach in severe cases of injury or when the nerve has been inadvertently divided during an operation. Accurate matching is assisted by the orientation of epineurial vessels, and by making a sketch of the prepared faces indicating the size and the disposition of different bundles. We prefer bundle (fascicular) suture, combined with epineurial suture for most main nerves, with the exception of the sciatic. In the early days after division of a nerve bundles

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are mobile within the epineurium, and epineurial suture increases the risk of malalignment. Dissection within the nerve is avoided as this surely leads to fibrosis. The needle is passed through the condensed inner epineurium and the perineurium to secure accurate coaptation of larger bundles. The repair is completed by epineurial suture. In delayed repair, fibrosis within the epineurium stabilises the bundles so that they cannot rotate within the epineurium. In these, epineurial suture may be adequate. The atrophy of the distal stump and the

extent of fibrosis in both proximal and distal stumps increases the difficulties in neglected cases (Figs. 7.18 and 7.19). In both primary and secondary suture, the areolar adventitial tissue is pushed back from each stump to expose the true epineurium. In fascicular suture, matched bundles, identified by size and by position in the nerve, are united by perineurial sutures of 9/0 or 10/0 nylon. Once these “key” bundles have been united, the union is completed by passing sutures of 8/0 or 9/0 nylon through perineurium and epineurium The nerve

Fig. 7.18  Primary suture of median nerve at the wrist. Top right: the pattern of the bundles is examined. Top left: The first sutures pass through the perineurium of the larger bundles then follows epi-­

perineurial suture. Middle: the nerve is rolled on a swab for access to the posterior aspect. The completed repair is seen below.

Operating on Peripheral Nerves

Fig. 7.19  The opportunity for primary suture was lost in this transection of median nerve displayed 3 months after wounding.

can be rotated on a saline-soaked dental swab, first from one side and then from the other, so that the whole circumference is accessible. Between 18 and 25 sutures are used to repair the adult median nerve at wrist level. In epineurial repair, orientation of bundles is achieved as well as is possible, and the epineurium is united with two lateral sutures of 8/0 nylon, the ends of which are left long. The repair of the anterior face is completed with sutures of 8/0 or 9/0 nylon, and the nerve is then rotated by manipulation of the lateral sutures so that the posterior epineurium can be united. If plasma glue is available this reduces the number of sutures required. The glue is applied after suture. Heavier epineurial sutures (4/0, 5/0 or 6/0) are used for suture of the sciatic nerve.

7.5.2 Grafting Wherever possible we use cutaneous nerves from the damaged limb and prefer the medial cutaneous nerve of forearm (MCNF) if it is available. The superficial radial nerve (SRN) and the lateral cutaneous nerve of forearm (LCNF) provide valuable innervation to the skin of the hand and neither should be used unless the parent nerve is irretrievably damaged. The ipsi lateral sural nerve should never be used for the repair of a low lesion of the tibial nerve for this adds to the denervation of the skin of the heel. These patients are better off losing one of the medial cutaneous nerves of forearm. No graft should be elevated until the injured nerves have been exposed and the extent of lesion defined and the gap between the prepared faces measured. This is a good time for the surgeon to pause for a few minutes of reflection, so that the repair can be properly planned. This is particularly important when repairs of several main nerves are necessary. A map of the proximal and distal faces is prepared outlining the pattern of the bundles in each stump and measuring the length of the gap between the prepared stumps. Then, a

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calculation is made of the number of grafts required for each nerve, and the disposition and length of the grafts which are cut to about 15% more than the measured gap. Elevation and preparation of the graft. The MCNF is taken from the arm through a straight incision. One anterior branch will be seen in the middle of the arm, lower down the nerve divides into two branches which straddle the main brachial vein. The SRN is delivered through separate incisions. The nerve is identified where it emerges from deep to the brachioradialis. The terminal branches are divided at the wrist. The radial nerve is displayed between brachio-radialis and brachialis, and the superficial branch identified by gentle traction. It is delivered into the elbow wound, a manoeuvre which has the advantage of stripping it of much of its adventitia. Up to 30 cm of nerve are available in the adult. The LCNF is found just lateral to the biceps tendon and it can be displayed, in the lower part of the arm, between the biceps and brachialis muscles. About 15 cm of graft is available. Reissis and his colleagues (1992) showed that the terminal 4 cm of the posterior interosseous nerve provides useful material for grafting palmar digital nerves (Fig. 7.20). The sural nerve(s) is almost always required in repair of lesions of the brachial plexus in the adult and in cases where more than one main nerve must be repaired. The patient is prone for repair of the sciatic nerve and its divisions, otherwise they are placed supine. The lower limb(s) is elevated by a stoical assistant or the knee is flexed to about 70° with the foot resting on the table. The nerve is exposed through a long midline incision which moves laterally in the distal one third of the leg to a point midway between the posterior aspect of the lateral malleolus and the lateral margin of the Achilles tendon. The incision may be extended into the popliteal fossa as a Z. Up to 50 cm of graft is available. The grafts, tenderly handled, are laid between saline soaked swabs and cut to appropriate length with a new blade or with vascular scissors. The nerve ends are prepared so that the fascicles protrude, and are laid in the prepared bed which must be healthy and unscarred. Fixation is usually by fibrin clot glue but the grafts can be sewn into place, two lateral sutures of 9/0 nylon being used for each. The sutures unite the fascicles of the stumps with the grafts. Because the individual strands of the grafts are likely to be around the same size as the individual bundles, the suture unites epineurium of graft to perineurium of bundle (Fig. 7.21). Millesi (1981) commences his dissection of the “fascicle groups” in the healthy nerve above and below the lesion, and makes the section at the point at which each group loses its healthy appearance. In the distal stump, for instance in a lesion of the median nerve at the wrist, the fascicle groups are traced back from the point of identification of their destination to the level just distal to the lesion. Fascicular patterns of distal and proximal stumps are matched, and individual grafts are used to unite the fascicular groups. Millesi resects fascicular groups at different levels, then uses 10/0 nylon through interfascicular

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Fig. 7.20  Nerve grafts. Above left: The superficial radial nerve (1) and lateral cutaneous nerves of forearm (2) are displayed at the elbow. Above right: the radial nerve is drawn into this wound after section of the distal branches at the wrist. Below: the communicating branches of the sural nerve are variable. This nerve is best elevated through a long

incision. Below left: the sural nerve divides into its terminal branches close to the short saphenous vein (3) above the ankle. Below right: note the communicating branch from the common peroneal nerve in the upper leg (4).

epineurium or perineurium for coaptation. The result is to produce grafts interdigitating with the fascicle of the stumps. We prefer to graft the proximal stump of the nerve first, leaving the distal ends of the grafts laid out across the bed before proceeding to the distal stump, matching as far as is possible, fascicle to fascicle. It is very important, once both ends have been anastomosed, carefully to inspect the grafts and the suture lines to make certain that during the union of one end the union of the other end has not been disturbed. It is better to bridge the gap with grafts if intact fascicles have been separated from the lesion. All nerve repairs must be secluded from naked bone, tendon, or lacerated muscle by healthy tissue. Grafts are stabilised by closing healthy synovium or fat, or muscle, over them. The fat pad is a valuable shield in the posterior triangle of the neck and it should be carefully apposed over the repair. It is necessary to restate that repairs of nerves and vessels must be covered by healthy, full thickness skin. Split skin grafts induce severe fibrosis which strangles. Vascularised grafts: The evolution application results and limitations of the free vascularised ulnar nerve graft in repair of the brachial plexus is described in Chapter 9 (Fig. 7.22).

The method was a development of the ingenious operations described by Strange (1947) and MacCarty (1951). In Strange’s operation the ulnar nerve is used to repair the median nerve in cases where both are otherwise irreparable and in MacCarty’s technique the common peroneal nerve is used to bridge long gaps in the tibial nerve in otherwise hopeless injuries of the sciatic nerve. These techniques provide a full calibre graft which is not only vascularised but also predegenerate and remain valuable in the most severe injuries. The steps required are described using the sciatic nerve injured in the mid or lower part of the thigh as an example. 1. At the first operation the proximal and distal stumps are identified and the gap between them measured. 2. The proximal stumps of the tibial and common peroneal nerves are prepared and then sutured together. 3. The proximal segment of the common peroneal nerve is traced and then the bundles within the trunk are cut across at a distance from the suture line equivalent to the gap already measured. The blood vessels in the mesoneurium and in the epineurium are preserved. In effect a vascularised graft has been prepared.

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Fig.  7.22  Free vascularised ulnar nerve graft. Above: the nerve is shown based on superior ulnar recurrent vessels (1). Below: shows the condition of a VUNG displayed close to the clavicle during an operation for non union 28 months after grafting.

Fig. 7.21  In grafting the suture unites epineurium of graft to perineurium of the bundle.

4. At the second operation, which is performed no sooner than 3 weeks after the first, the proximal segment of the common peroneal nerve is sectioned and brought down to the distal stump of the tibial nerve to which it is sutured. Bleeding, which is at times quite copious, is seen at the face of the common peroneal graft when it is apposed to the distal tibial nerve. Case Report: An 18 year old woman sustained open fracture of mid shaft of femur in a road traffic accident. Most of the skin of the lower part of the thigh was avulsed and there was much destruction of muscles. Extensive skin grafting proved necessary. The tibial nerve was repaired by the pedicle technique: a

24 cm long segment of the proximal common peroneal nerve was prepared and it proved a simple matter to separate this from the tibial division as far as the level of the neck of the femur. The proximal stumps of the tibial and of the common peroneal nerves were prepared and sutured. The bundles within the common peroneal nerve were sectioned 25 cm proximal to this suture line. Four weeks later the common peroneal graft was mobilised and sutured to the distal stump of the tibial nerve in the upper part of the leg. She regained flexion of the heel and of the toes to power MRC grade 4, warm and cool sensation in the sole of the foot and could accurately localise to the plantar skin without over reaction. There was recovery of sweating.

7.5.3 Indications For and Methods of Nerve Transfer Nerve transfers work best when a healthy nerve, or a portion of a healthy nerve, is transferred to a nerve to muscle of roughly equivalent size without any interposed nerve graft (Narakas 1987). They cannot be asked to do too much; a rivulet cannot feed the Nile. Addas and Midha (2009) provide a valuable review of this field. They say “nerve transfers tend

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to take the surgeon away from exploring the injury site, the brachial plexus, which carries the potential for surgeons to not even offer an anatomic nerve reconstruction, even in situations when these are perfectly appropriate…. With the increasing use of transfers, newly trained peripheral nerve surgeons are less likely to have exposure to the brachial plexus and they will be increasingly unfamiliar with the detailed anatomy and intraoperative electrophysiology assessment of the lesion”. These are important warnings. We offer two more. The first is that no nerve of vital function should be used for the sake of a non vital function. A birth lesion of the phrenic nerve is a life threatening complication. Some adults with severe injuries to the brachial plexus experienced breathing difficulties because of the associated lesion of the phrenic nerve. The second is that reinnervation of muscle, to be successful, must involve reinnervation of the deep afferent pathway from the muscle spindles and the Golgi tendon organs. This fact may account for the disappointing results following transfer of the hypoglossal nerve because afferent pathway from the tongue passes through the lingual nerve. Some of the more common methods are now described.

7.5.3.1 The Intercostal Nerves The patient is placed in a semi-sedentary position with preparation including the forequarter and the chest wall from the mid line to the iliac crest. An incision is made below the fold of pectoralis major extending to the axilla as a “Z”. The serratus anterior is exposed, and the neurovascular pedicle to that muscle identified and protected. The lateral perforating branches of the intercostal nerves are identified. The upper four digitations of the serratus anterior are released from the ribs, leaving a sufficient cuff of muscle for later repair. The muscle is reflected so opening the plane between the muscle and the rib cage.. The cutaneous branch of the intercostal nerve is traced back to a narrow foramen in the external intercostal muscle. The muscle is released from the rib above as far as the posterior angle. The deep division of the intercostal nerve is found by dividing the attachment of the middle intercostal muscle from the rib above. Gentle traction with a phrenic hook, underneath the upper rib, reveals the deep branch which is divided anteriorly. A Gelpi knee retractor can now be inserted to spread the rib cage. The deep division is traced back to its junction with the perforating branch. Elevation of the nerve becomes progressively easier. Bi-polar diathermy must be used throughout (Fig. 7.23). The intercostal nerves from T3 to T6 are available by this method. These are brought to the anterior surface of serratus anterior through a tunnel in the upper part of the muscle. The serratus anterior is repaired.

Surgical Disorders of the Peripheral Nerves

Fig. 7.23  Nerve transfer. Upper left intercostal nerves T2, T3, T4 (1) raised and united to the lateral cord of the plexus (2).

If only one or two deep divisions of the intercostal nerves are being used for the nerve to serratus anterior, then a suitably placed transverse incision in that muscle is adequate. It is wise always to see a radiograph of the chest before the patient leaves the operating theatre. The Spinal Accessory Nerve: This is a powerful motor and it should be used with discrimination. THE INNERVATION OF THE UPPER ONE THIRD OF TRAPEZIUS MUST NOT BE COMPROMISED. Even when the nerve is divided deep to the clavicle, the loss of function is less but it is not insignificant. The nerve is found at the lateral end of the transverse supraclavicular incision in the plane between the fat pad and the deep face of trapezius. The nerve passes down it in a rather sinuous fashion and is accompanied by a longitudinal artery and vein. These can cause troublesome bleeding. The nerve is joined by a branch from the cervical plexus just above the level of the clavicle and intra-operative stimulation here only occasionally evokes a muscle twitch. The nerve is sectioned distal to that junction (Fig. 7.24). Ulnar to Biceps Transfer (Oberlin et al. 1994) is regularly effective in cases of avulsion of C5 and of C6. With care, it can be extended to cases where C5, C6, C7 or even C5, C6, C7 and C8 have been avulsed. Fastidious dissection of the bundles within the ulnar nerve is necessary. The nerves are exposed through an incision along the length of the brachial bundle. The musculocutaneous nerve is identified. It is not uncommon to find that the nerves to biceps and brachialis arise directly from the median nerve. The nerve to biceps is accompanied by a sizeable artery and vein. It is traced proximally and separated from the main nerve. It is sectioned here so that it drops down onto the ulnar nerve. The epineurium of the ulnar nerve is incised and the bundles exposed. Nerve stimulation used at very low intensity leads the surgeon to a bundle in the antero-lateral quadrant of the nerve passing to the flexor muscles of the forearm but not to the muscles of the hand. This is divided and an end-to-end suture is done.

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This valuable principle has been extended widely, using bundles from the median or the ulnar nerve to nerves to triceps, to the nerve to extensor carpi radialis brevis or to reinnervate free functioning muscle grafts and it has proved particularly

valuable in the repair of injuries to the brachial plexus in which some spinal nerves are intact whilst others are avulsed. In these a bundle from an intact nerve may be used to reinnervate the suprascapular nerve or an avulsed ventral root (Figs. 7.25–7.28).

Fig. 7.24  Accessory (1) to suprascapular (2) transfer. Above, seen from the head: the spinal accessory nerve is displayed on the inner face of the trapezius at the base of the posterior triangle, Middle and below, the view from the shoulder: the suprascapular nerve is passed deep to the fat pad and united to the spinal accessory nerve.

Fig. 7.25  Avulsion of C5 and of C6 with dorsal scapular palsy. The suprascapular nerve was reinnervated by one bundle from C7. The suprascapular nerve (1) posterior division of upper trunk (2) anterior division of upper trunk (3) C7 (4) and the selected bundle from C7 (5) are displayed.

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Fig. 7.26  Reinnervation of the avulsed ventral roots of C6 and C7 from the proximal stump of C5. The ventral root of C6 is apposed to the stump of C5. Grafts were passed to the ventral root of C7 and to suprascapular nerve. C5 (1), C6 (2), C7 (3), the ventral root of C6 (4) and the grafts (5) are seen.

7.5.3.2 Direct Muscular Neurotisation This technique is useful in lesions of the circumflex or musculocutaneous nerves in which the nerve has been avulsed directly from the muscle or, in the case of circumflex, the distal stump of the nerve is wrecked by fibrosis. The proximal stump is prepared in the usual way and two lengths of graft, usually the MCNF are united to the proximal stump and then implanted into the muscle through short incisions through its sheath. The grafts are passed subcutaneously, and the portal of entry is exposed by a short incision of the skin at those points. About ten portals of entry are fashioned using the terminal branches of the graft or by subdivision of the distal stump. The entry points of the implanted nerve are sealed with fibrin clot glue (Fig. 7.29). Freeze thawed muscle graft (FTMG). This is useful in the repair of cutaneous nerves or their branches which have formed a painful neuroma. The stumps of the nerve are prepared and the gap measured. A segment of adjacent muscle, of the equivalent calibre, is excised. This should

Fig. 7.27  Reinnervation of part of the circumflex nerve (1) by a nerve to long head of triceps (2) (Operation performed by Dr Andrew Yam RNOH).

be at least two and a half times the length of the measured defect in the nerve. The muscle is then enveloped by a piece of aluminium foil and immersed in liquid nitrogen for about 60 s. The packet is then placed in distilled water for a couple of minutes. The prepared muscle graft can then be trimmed to appropriate length and breadth and it may be secured to the nerve stumps by suture and then sealed by plasma clot glue. Fragmentation is usual with muscle grafts more than 3 cm long.

7.5.4 Immobilisation He or she labours in vain who repairs a nerve and leaves the junction or junctions open to the hazards of movement of fragment of a bone or of movement of a related joint. Although the antique methods of immobilisation and gradual

Operating on Peripheral Nerves

Fig. 7.28  Transfer of a bundle from the ulnar nerve (2) to the nerve to biceps (1) (Oberlin’s operation).

extension by “turnbuckle” or hinged plaster after its cessation are now rarely necessary, repaired nerves still need protection during at least the first 3 weeks after repair. In most cases, a simple plaster slab gives sufficient protection. Only in the case of extensive proximal lesions of the whole sciatic nerve is elaborate protection required. Narrowing of the gap to permit end to end suture or adequate repair by graft requires flexion of the knee and avoidance of flexion of the hip. The necessary position of immobilisation in a hip spica is awkward and uncomfortable; further, gradual extension of the knee after 3 weeks may be necessary in order to protect the line of the repair. Usually, it is sufficient when the splint is removed to warn the patient about the danger of excessive movement of related joints, and to rely on the patient steadily to restore movement of those joints. There is particular difficulty in protecting repairs of the brachial plexus, an even greater problem when it becomes necessary to protect roots re-united to the spinal cord. In these cases, Fournier (2005) applies a Minerva plaster of Paris jacket. At present we rely on a sling for the upper limb of the adult: the best in our

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Fig.  7.29  Muscular “neurotisation”. Above: The nerve graft is prepared. Below: It is passed from the proximal stump of the circumflex nerve and implanted into the muscle.

experience is that designed by Evelyn Hunter RGN. Alternatively, slings with straps which secure the arm across the body, can be used (Fig. 7.30). We supplement the sling with a soft cervical collar after repairs of the supraclavicular brachial plexus. A plaster of Paris “cocoon” is applied after repair of the plexus in infants. The method used in the post operative care of severe wounds at the wrist is as follows (Fig. 7.31). The splint holds the elbow at 90 degrees of flexion, the wrist at between 30 and 40 degrees of flexion, the metacarpophalangeal (MCP) joints at about 70 degrees of flexion, and the proximal interphalangeal (PIP) joints at no more than 30 degrees of flexion. The dorsal splint extends to the tips of the fingers and the palmar splint to the PIP joints only. The splints are bandaged so that there is restriction but not rigid immobilisation. Gentle, active flexion of the fingers and the thumb is encouraged from the outset. The arm is supported in a sling, but there should be encouragement of gentle active lateral rotation and of elevation of the shoulder to 90° from the first

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movements of the joints can be done by the patient or by his or her parents, but weekly supervision by a physiotherapist is useful in keeping the mind concentrated on the work during the long march towards recovery. In the case of the metacarpophalangeal joints of the fingers and the carpo-metacarpal joint of the thumb, “lively” splints are useful, but the problem of the stiff metacarpo-phalangeal joint in the paralysed hand persists. Accurate diagnosis is the foundation of rehabilitation and operations for repair of the nerves should be seen as but the first stage in that process. It should be superfluous to add that the sooner the diagnosis is established the better, and that urgent efforts must be made to improve the prognosis.

7.6 Approaches to Individual Nerves The Neck: cervical and brachial plexus; the subclavian and axillary vessels; the spinal nerves; spinal accessory nerve; suprascapular nerve.

7.6.1 The Transverse Supraclavicular Approach: (Anterior, or Anterolateral) Fig.  7.30  Evelyn Hunter’s sling for control of the fore quarter after repair of the brachial plexus. Note the check on lateral rotation at the gleno-humeral joint.

postoperative day. At 3 weeks the splints and the sutures are removed. The next splint does not restrict the elbow. The wrist is splinted to prevent extension beyond 20°. The dorsal hood, which again extends to the tips of the fingers, blocks the MCP joints to 30 degrees of flexion and the PIP joints to 30 degrees of flexion. Increasingly, vigorous active flexion of the fingers and the thumb is now permitted and gentle active flexion at the wrist is also encouraged within the confines of the splint, bandaged as it is to the forearm and hand. In direct sutures of nerves in the elbow region a hinged splint is applied at 3 weeks from operation. This permits active flexion but blocks extension. The range of permitted movement is increased at weekly intervals by adjusting the hinge. By 6 weeks, splints are discarded and vigorous active flexion work against resistance is introduced. Now, gentle passive stretching work can be introduced for the fingers and the thumb. Early gentle active movements within the confines of the splint and the bandages are encouraged. It is of course very important during the period of recovery to maintain the mobility of the joints some or all of whose governing muscles are paralysed and to warn the patients of the danger, especially in cold weather, of accidental damage to the anaesthetic skin. Most of the work on passive

This is used for exposure of the supraclavicular part of the brachial plexus. Its disadvantage is that the vertebral artery stands between the operator and the most proximal parts of the nerves. The risk of skin necrosis is negligible. The scar is reasonable. The length and the level of the incision are modified according to the lesion. In the urgent case the incision extends from beyond the mid line to beyond the anterior fold of the trapezius and is placed just above the clavicle. For lesions of the upper trunk of the brachial plexus the incision is shorter and is placed about two fingers breadth above the clavicle. The exposure of Fiolle and Delmas (1921) is achieved by adding a vertical limb to the transverse supraclavicular wound. Bonney’s transclavicular approach (Birch et al. 1990) is, in effect, a medial extension of the transverse supraclavicular approach and it gives excellent access to the first part of the subclavian artery, the first part of the vertebral artery and the whole of the brachial plexus. The Operation. The patient lies supine in a semi-sedentary position, with the head elevated to about 30° and the neck in extension. After placing recording electrodes to the scalp and the skin of the neck, the head is bandaged to a neurosurgical rest. The neck is extended but not rotated. The area of skin preparation includes the whole of the forequarter, extending to the jaw line and the ear, beyond the mid line to the inferior rib margin. The skin flap is developed deep to the platysma (Fig. 7.32). This is easier to identify at the posterior margin of the

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Fig. 7.31  Protection after repair. Above: Plaster after repair of both nerves and flexor tendons at the wrist. Below: Hinged plaster with adjustable check.

sternocleidomastoid muscle. Below, the flap is developed to reveal the inferior margin of the clavicle; above as far as the greater auricular and transverse cervical nerves crossing the anterior face of sternocleidomastoid (SCM). The incision is deepened in the plane between external jugular vein and the SCM, displacing the supraclavicular nerves posteriorly. The lateral part of the insertion of the muscle can be elevated from the clavicle. The fat pad and the omohyoid muscle are

now seen. The omohyoid is divided between stay sutures and reflected. The fat pad may present as two leaves, split by branches of the transverse cervical vessels. These must be preserved in cases of rupture of the subclavian artery because of their contribution to the collateral circulation (Fig. 7.33). The scalenus anterior is exposed and the phrenic nerve is seen coursing obliquely across it. It is mobilised and held in nerve sling. Access to bony structures behind the plexus

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Fig.  7.32  The transverse supraclavicular approach to the brachial plexus. Note the position of the patient and the line of incision.

should be achieved by separating the component nerves rather than by forward retraction of the plexus. Following the phrenic nerve cranially brings the surgeon to the fifth cervical nerve and it is sometimes helpful to work on the medial side of the phrenic nerve to expose a ruptured stump at C5 or C6. The upper trunk and the suprascapular nerve are traced. After traction injury it may be easier to identify the suprascapular nerve first and follow it back to the upper trunk. The seventh cervical nerve can now be seen behind the upper trunk. Division of scalenus anterior reveals the subclavian artery; the plane between the muscle and the subclavian artery requires careful definition. We have seen the subclavian artery crossing anterior to scalenus anterior in three cases and through it in seven more. The eighth cervical and first thoracic nerves are traced by following the plane between the artery and the lower trunk. The nerve to serratus anterior lies lateral and deep to the upper trunk, behind the suprascapular nerve and posterior to scalenus medius. The rami forming this nerve are displayed by dividing scalenus medius. There are usually three, usually that from C6 is the largest. The spinal accessory nerve, is identified running in a vertical

Surgical Disorders of the Peripheral Nerves

and sinuous manner on the deep face of trapezius. The dorsal scapular nerve can be found passing posteriorly away from C5. Kline (2008b) provides a good demonstration of the course and relations of this nerve (Fig. 7.34). Extension by the operation of Fiolle and Delmas. This affords full display of the supra, retro and infra clavicular plexus, of the second part of the subclavian to the terminal axillary artery and of the subclavian and axillary veins deep to the clavicle. The originators said “the exposure of the vessels can be achieved in three minutes” and this is possible in an emergency. There is no doubt that the operation secures rapid access to and control of major vessels from the scalenus anterior to the lowest part of the axilla. The plexus itself is exposed from the spinal nerves above to the terminal branches below. It is especially valuable in fresh cases of laceration or rupture of the great vessels deep to or below the clavicle and in later cases of false aneurysm, and is often necessary for the delayed exposure of ruptured nerves after primary vascular repair. It is the exposure of choice in the closed infraclavicular rupture of vessels and nerves. The incision is T-shaped, the vertical limb running in the deltopectoral groove, retracting the cephalic vein medially, then curving into the apex of the axilla underneath the fold of pectoralis major. In urgent cases a Gigli saw is used to divide the clavicle at the lateral edge of SCM: otherwise, a hole is drilled and prepared for a compression screw, inclined at 45° to the long axis of the clavicle. Subsequent fixation is made easier by contouring a plate to the bone and drilling and preparing one hole in the lateral fragment. The clavicle is cut at 90° to the axis of the hole for the compression screw. It is possible, in some cases, to avoid cutting the clavicle. The bone can be drawn upwards or downwards by a nylon tape (Figs. 7.35 and 7.36). The fascia at the root of the axilla is divided and the finger develops a plane between pectoralis major and minor in front, and the axillary bundle behind. Pectoralis major is detached from the humerus. Pectoralis minor is reflected taking care for the musculocutaneous nerve. The limb is rolled into lateral rotation so that the trunks, divisions and cords of the brachial plexus are displayed with their accompanying vessels. The exposure has been used in more than 250 cases. We know of nine cases of non union of the clavicle; infection complicated three of these.

7.6.2 The Transclavicular Exposure Bonney developed this operation in 1976 as an approach to the anterior aspect of the cervico-dorsal spine for excision of malignant cartilaginous tumour which had eroded the bodies of C7 and D1 and compressed the spinal cord. The approach was designed to give adequate exposure and control of the

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Fig. 7.33  Above left: The posterior margin of sternocleidomastoid is defined, anterior to the external jugular vein and supraclavicular nerves (1). Above right: This is retracted to display the fat pad and transverse cervical vessels (2). Below left: The omohyoid is divided between stay

sutures. Below right: the nerve to serratus anterior (3) is displayed by section of scalenus medius deep to the upper trunk (5). The largest ramus comes from C6. There is often a communicating branch from the dorsal scapular nerve (4).

venous trifurcation, the first part of subclavian artery, the vertebral artery and the recurrent laryngeal nerve. Duval (1921) faced with the problems of deep wounds in the neck outlined an approach in which the sternoclavicular joint was turned downwards. He described it as: “this major and hazardous intervention which should be undertaken only by the most consummate surgeon”. Antibiotics, blood transfusion and advances in anaesthetics have greatly diminished some of these hazards but the intervention remains an extensive and difficult one calling for a high degree of anatomical knowledge and practical versatility. The exposure rests on the elevation of the osseo-muscular flap comprising the medial portion of clavicle with the sterno clavicular joint based on the sternocleidomastoid muscle (SCM). The whole of the brachial plexus can be displayed after some lateral work; the cervico dorsal spine can be seen from C3 to T3 by developing the plane between the carotid sheath and the visceral axis (Fig. 7.37).

The transverse limb of the incision runs from the fold of the trapezius on the side of operation to the mid point of the opposite posterior triangle. This limb can be extended to increase the exposure. The vertical limb runs to the sternal angle. The flaps are widely elevated to include platysma. The SCM is defined anteriorly and posteriorly from its insertion below to the uppermost limit of the wound above. The accessory nerve is identified. The clavicle is displayed subperiosteally at its middle point. The subclavius muscle and suprascapular vessels are divided. The omohyoid muscle is divided and reflected. Pectoralis major is detached from the inferior portion of the medial clavicle revealing the subclavian vein. The strap muscles are released from the notch of the manubrium and the plane deep to this developed carefully using a dental Howarth elevator and a curved Adson’s dissector. The plane is enlarged with the finger and a malleable retractor passed. The first costochondral junction is defined after detaching pectoralis major from the adjacent manubrium

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Fig.  7.35  The Fiolle Delmas exposure. The incision at the shoulder was made for the purpose of inserting an intramedullary nail. The wound, caused by the fracture, has been left open.

Fig. 7.34  Rupture of C5 and C6 with avulsion of C7, C and T1 displayed at 6 days after injury. Above: the fat pad is split to display the transverse cervical vessels (1). Middle: the phrenic nerve (2) is seen deep to the pre vertebral fascia. Below: division of the fascia reveals the ruptured stumps of C5 and C6 (3) and the avulsions of C7, C8 and T1 (4).

and the interval between the first and second sternocostal junction is developed deep to the sternum by the means outlined above. A malleable retractor is passed to meet its fellow from above. The first costal cartilage is cut with a scalpel, a

fine osteotome is used to divide the manubrium with an L-shaped cut. The clavicle is now divided and the medial clavicle, sternoclavicular joint and upper corner of the manubrium are elevated on the SCM. The residual strap muscles are released. The internal jugular vein is now seen and traced to its junction with the subclavian vein. The brachiocephalic vein is traced and lightly held in a vascular sling. The phrenic nerve is elevated from scalenus anterior and the muscle divided. The first part of subclavian artery, the vertebral artery and the recurrent laryngeal and vagus nerves are seen. To display the whole of the plexus pectoralis major and pectoralis minor are detached from the humerus. When it comes to closure, the manubrio-clavicular fragment is reattached to the manubrium with wires, and to the clavicle with a plate and screws. The soft tissue layers are carefully closed. This exposure has been used on 80 occasions, chiefly for tumours of the brachial plexus. One patient, a 62 year old man, with a malignant neurofibroma complicating neurofibromatosis type 1(NF1), died of consumptive coagulopathy. Osteomyelitis of

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Fig. 7.36  Two large neurofobromata exposed through the approach of Fiolle and Delmas. Top left: the skin incision. Bottom left: The tumour exposed and, Top right: removed. There was no loss of function

(Courtesy of Marco Sinisi). Bottom right: Another neurofibroma arising in the posterior triangle of the neck. It was not necessary to divide the clavicle in either of these cases.

the clavicle occurred in two cases, and non union in four more. The recurrent laryngeal nerve is more vulnerable on the right side. Damage to the thoracic duct can usually be avoided, except in a scarred field and is usually recognised because of the leak of milky fluid. It is best to identify and repair the lesion, because if the pleura has been opened, there is a real danger of formation of a chylothorax. If the hole cannot be repaired, it can be plugged with a muscle graft.

that the upper ribs are exposed. The first rib is defined and removed extra-periosteally, if necessary after the second rib has been removed sub-periosteally to facilitate exposure. The scalenus medius muscle is partly liberated during the removal of the first rib, and further mobilisation permits its upward retraction to display the brachial plexus. Kline and colleagues (1978) warn that it is necessary to avoid damage to the nerve to serratus anterior during this process. By medial retraction of the posterior paravertebral muscles the foramina can be opened by hemi-laminectomy. Closure after completion of the procedure is by re-uniting the muscles carefully over a drain or drains Dubuisson and colleagues (1993) describe the three potential complications: winging of the scapula, instability of the cervical spine if more than two facet joints are removed, and damage to various related structures. We certainly accept as firm indications: (1) In the thoracic outlet syndrome: prior operation by the transaxillary or supraclavicular routes for removal of the first thoracic or seventh cervical rib, when the posterior third of the rib remains; (2) In tumours of the plexus: tumours with intraforaminal and extra foraminal

7.6.3 The Postero-Lateral Route This, the posterior subscapular route, provides very good access to the most proximal parts of the nerves and in particular to the nerves in the intervertebral foramina (Kline and colleagues 1978). The patient is almost supine, with the limb on the affected side resting on a separate table. The incision is convex medially, truly parascapular. The scapula is freed by the division of the trapezius and rhomboid muscles and, if necessary, the levator scapulae and it is retracted laterally so

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Fig.  7.37  The transclavicular exposure. Top left: the position of the patient and line of incision. Top right: elevation of the skin flaps with platysma and definition of sternocleidomastoid muscle (1). Middle left: The clavicle exposed and the phrenic nerve (2) and subclavian artery (3) traced. Middle right: the bone flap is elevated, taking care for the

subclavian vein (4). The trunks of the brachial plexus (5) are seen. Malleable retractors (6) are inserted deep to the manubrium before section of the first costochondral junction and division of the manubrium. Bottom: the tumour (7) is seen deep to the subclavian artery, where it enveloped the vertebral artery.

lateral components; (3) In radiation neuropathy when there is extensive change in the skin and deep tissues of the neck and chest wall: (4) In traumatic lesions when the evidence is that a reparable lesion is in or near the foramen. Our posterolateral approach owes more to Adson and Brown (1929) than to Kline and his colleagues (Fig. 7.38a–c). It affords a less extensive view to the more distal (lateral) part

of the supraclavicular plexus than does Kline’s. The patient is put in the lateral position, the affected side uppermost, and the limb is included in the field. The incision, convex laterally, is centred over the seventh cervical vertebral spine. The flaps are raised. The trapezius is divided close to the midline and the muscle is retracted laterally. The next layer then comes into view: the upper part of the rhomboids, and the lower part of

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a

b Splenius capitis Rhomboids Levator scapulae Supraspinatus Acromion C7

Trapezius

C7 T1 T2

c

T3 T4 T5

Scalenus medius

T6

Fig. 7.38  Posterior approach to the left brachial plexus. (a) The incision. (b) The division of the trapezius. (c) Removal of posterior elements and detachment of scalenus medius to expose the proximal part

of the plexus. Note that the nerve to serratus anterior is shown. In many cases of proximal injury to the plexus, it will have been damaged with the main nerves.

the splenius capitis. The levator scapulae, running from the scapula to the upper cervical transverse processes, and the splenius cervicis, running from the third to the sixth thoracic vertebral spines to the upper cervical transverse processes, are rather lateral. The upper part of the rhomboids and the lower part of the splenius capitis are divided near the mid line and the erector spinae group is exposed. Lateral to this, the

transverse processes of the first thoracic and lowest four cervical vertebrae can be felt. The transverse processes and lateral masses are exposed by blunt dissection, with medial retraction of the erector spinae group. The back of the first rib is exposed at the lower end of the field, and the scalenus medius is cleared from its upper surface. That muscle is detached from its origin on the posterior tubercles of the lowest three of four cervical

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transverse processes. The nerves are then shown distal to the transverse processes, the proximal branches of the fifth, sixth and seventh vertebrae going into the scalenus medius to form the nerve to the serratus anterior. Now the posterior tubercles of the fifth and sixth vertebrae and part of the transverse process of the seventh are nibbled away to show the most proximal parts of the nerves. If necessary, the first thoracic transverse process and the first rib can be removed to increase the exposure of the lowest part of the plexus. Later, if necessary, one or two interfacetal joints can be removed to show the nerves in their dural sheaths in the foramina. It is necessary to proceed carefully and methodically in this exposure, securing good haemostasis at each stage. It is not an easy exposure, but it is the preferred route when there is a very proximal lesion and access by the anterior route is barred by the sclerosis of a previous intervention. Two muscle layers and one subcutaneous layer are closed over a suction drain. This route opens possibilities for exposure of the central segment of the spinal nerve and the opportunities for repair of the roots of the spinal nerves will now be considered.

7.7 Repair of the Roots of the Spinal Nerves in an Avulsion Lesion In these cases the cord has already been damaged by the avulsion of one to five spinal nerves. The risks of interfering, however marginally, on this damaged cord are clear. The anterior spinal artery is maintained by radicular vessels which enter the spinal canal in company with the spinal nerves. These vessels must be ruptured in an avulsion lesion. It is likely that the incomplete Brown Séquard syndrome, seen in so many cases of avulsion lesions, is ischaemic in origin. This fact must be at the forefront of thinking about reconnection between the spinal cord and the avulsed spinal nerve. Some contraindications to direct repair or reimplantation of avulsed spinal nerves include severe associated injuries to the head, the chest or the viscera; rupture or occlusion of the subclavian artery or the vertebral artery; fracture of a cervical, or upper thoracic vertebra and any hint of cord lesion. These are hazardous operations and it is most unwise to add to those hazards by delay when fibrosis and the sealing off of the rent in the dura will add to difficulties. The posterior subscapular exposure has been described above, three other approaches are available. The endoscopic transforaminal approach to the anterior aspect of the spinal cord was opened by the experience of one of us working with Thomas Carlstedt in 1995. A 10 year old boy with a complete lesion of the brachial plexus was operated on 2 weeks from injury. C7, C8 and T1 were avulsed. A small arthroscope introduced through the foramen of C8, gave a surprisingly good view of the cord and of

Surgical Disorders of the Peripheral Nerves

the stump of the ventral root of C8. The presence of useful stumps of C5 and C6, and the state of the avulsed nerves persuaded us against reimplantation. Transforaminal endoscopy has been used on a number of occasions. A 2 mm diameter small joint arthroscope is used. The lower foramina are best suited for this manoeuvre because of their size and because of their relation to the vertebral vessels. Carlstedt (2007a) says that: “more information regarding remaining intradural root stumps or full root avulsions can be gained with this technique than through ancillary investigations”. Direct repair was possible in one case; in the others, short interposed grafts, using dorsal rootlets from the avulsed spinal nerves, were used. This method is usually possible only within a few days of injury. It is safe, it is relatively straight forward and it merits further attention. The possibility of repairing the ventral root by endoscopic methods through an enlarged foramen, with proper care for the vertebral artery, is attractive. The anterolateral transvertebral approach. Fournier and his colleagues have developed an antero-lateral approach to the ventral root entry zone (Fournier et al. 2001, 2005). The exposure is described as a “lateral interscalenic multi-level oblique corpectomy”. Pre operative vertebral angiography is essential. The patient lies supine, with the head slightly extended, and lightly rotated to the opposite side. The incision follows the posterior margin of the sternocleidomastoid muscle. The great vessels and the viscera are not formally displayed, as dissection passes deep to them. The cervical column is exposed between the scalenus anterior and the scalenus medius, by following the cervical spinal nerves. The phrenic nerve is isolated and scalenus anterior resected. The longus colli and the sympathetic chain are retracted medially. The vertebral artery is exposed and mobilised with great care using high magnification and it may be taken forwards or back. Now, part of the vertebral body and part of the adjacent intervertebral disc are removed to expose the dura mater. This is opened and nerve grafts which are passed behind the vertebral artery and the phrenic nerve are inserted through a small incision in the pia at the level of the ventral root entry zone, to a depth of about 2 mm. Plasma glue is used to support the position of the grafts. The dura mater is repaired. Stabilisation of the cervical spine is not necessary because the articulations have not been disturbed. Fournier and his colleagues recognise some limitations to this approach: it is not feasible to expose all five of the ventral roots; reimplantation of the dorsal roots is not possible. The lateral approach was used by Bonney and Jamieson in the first case of reimplantation in 1977 (see Chapter 9) and is described by Carlstedt and Birch (2000) and by Carlstedt (2007b) and it is possible to extend the exposure from the anterior spinal artery to the dorsal root entry zone as well as the supra and infraclavicular brachial plexus. The patient is placed laterally, (Kratimenos and Crockard 1993)

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263

Spinal accessory n. Levator scapulae

Scalenus posterior Sternocleidomastoid

C5

a

Trapezius

b Levator scapulae

Brachial plexus

Scalenus posterior

Scalenus posterior

Erector spinae

N. XI

Longissimus (divided) Trapezius (divided)

Transverse proc. (post tub.)

c

Longissimus

d

Trapezius

Splenius

Levator scapulae

Fig. 7.39  The lateral approach to the brachial plexus. (a) The skin incision. (b) The trapezius muscle is split protecting the accessory nerve. (c, d) The longissimus is approached between the levator scapulae and

the scalenus muscles and it is split longitudinally to expose the posterior tubercles of the transverse processes (Drawn from Carlstedt and Birch 2000).

with the head supported in a Mayfield Clamp. The neck is slightly flexed away from the side of operation whilst the head of the table is elevated to about 30°. It is possible to tilt the table to assist anterior and posterior exposure. The skin incision is transverse supraclavicular extended to the spinous process of C5 (Fig. 7.39). It is possible for two surgeons to work simultaneously, the first exposing the brachial plexus in the posterior triangle of the neck, the second working towards the posterior aspect of the cervical spine. The posterior tubercles of the transverse processes of C4 to

C7 are exposed between the levator scapulae and posterior and medial scalene muscles, splitting the longissimus muscle longitudinally. The paravertebral muscles are detached from the hemilaminae and retracted dorso-medially. The dura is exposed through a hemilaminectomy. The medial part of the processes of the facet joints may be removed. The dura mater is incised longitudinally and held with stay sutures; the denticulate ligaments are detached laterally and held with stay sutures which permits very gentle rotation of the cord. Grafts are fed through the intervertebral canals

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using fine vascular slings or a silicon catheter. These are implanted through slits in the pia mater and secured with plasma glue (Fig.  7.40). Carlstedt (2007b) provides a detailed account of the method of implantation and a compact disc (CD) showing the operation is supplied with his publication. The nerve graft can be split into separate bundles and these are introduced to a depth of between 1 and 2 mm: Carlstedt says “a small Roton instrument in the shape of a hockey stick, is useful in this manoeuvre; its “blade” being 1–2 mm in length, can be used as a depth gauge when implanting the root or the nerve graft. Implanted grafts are maintained in position by glue (Tisseel) or they can be stitched to the pia. The pia is slightly elastic and closes around the introduced tips of the nerve graft. In cases of root ruptures, the nerve graft is directly apposed to the trimmed end of the ventral root stump… if the foramen is blocked, the grafts are passed through the incision in the dura and outside the vertebral canal”. The dura is closed by a vein patch or a patch of artificial dura. An early case was complicated by a CSF leak. Since then a lumbar drain has been retained for up to 7 days.

Fig. 7.40  Grafts are drawn through the canals of C6 and C7 and implanted through short slits in the pia mater (Courtesy of Thomas Carlstedt).

Surgical Disorders of the Peripheral Nerves

7.7.1 The Spinal Accessory Nerve The incision is often dictated by the site through which the nerve was originally damaged. Often enough, the original incision can be extended either as a “Z” or in the direction of the lines of skin tension. The usual site of injury is in the posterior triangle between the sternocleidomastoid muscle and trapezius muscles, though occasionally the nerve is wounded in its course through the former muscle or proximal to it. The greater auricular nerve is the key to the exposure of the proximal stump which emerges from behind the sternocleido muscle about 5 mm cephalad. The nerve emerges from deep to the muscle as one trunk, and at this point a fine branch is seen which innervates the uppermost part of the upper one third of the trapezius. This must be respected. The course and relations of the nerve are remarkably constant (Fig. 7.41). The incision extends to the anterior face of the SCM, displaying the greater auricular and transverse cervical nerves. Exposure of the accessory nerve should begin in unscarred tissue, and the lesion should preferably be exposed after proximal and distal trunks have been defined. The proximal stump may have retracted deep to the sternomastoid. It can be identified anterior to the muscle or branches to the sternocleido mastoid are identified with a nerve stimulator. The distal part is found beneath the anterior part of the upper fibres of the trapezius where it must not be confused with branches of the supraclavicular plexus which pass obliquely or horizontally in front. Atrophy of the distal trunk is a common finding because of the long delay before diagnosis. There is no point in attempting end-to-end suture after

Fig. 7.41  The spinal accessory nerve emerges, as one trunk (1), from deep to sternocleidomastoid about 5 mm cephalad to the greater auricular (2) and transverse cervical (3) nerves. In this case the nerve had been transected 15 months earlier and there is atrophy of the distal stump (4).

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resection: the gap is usually too great, and in any case, the mobility of the forequarter on the axial skeleton forbids the use of such a method because of the hazards of disruption. On a few occasions we have been forced to reinnervate the distal trunk by transfer of part of the lateral pectoral nerve.

7.7.2 The Suprascapular Nerve We prefer the lateral position and a transverse incision. The flaps are raised, and the supraspinous part of the trapezius muscle is detached from its origin and raised to show the supraspinatus muscle, or the fibres of trapezius can be split to show the underlying supraspinatus, which is lifted from its scapular origin to reveal the suprascapular nerve traversing the notch. The accompanying artery is usually superficial to the transverse ligament or bony bridge. Ochiai and his colleagues (1997) showed that the suprascapular nerve might be seriously damaged in several places and describe an exposure which exposes the nerve along its entire course as far as the infraspinatus and which can be extended to display the circumflex nerve anteriorly.

7.7.3 The Infraclavicular Part of the Brachial Plexus With the full opening of the delto-pectoral interval the pectoralis minor muscle is exposed crossing the field to its attachment on the coracoid process. Below and above it is the neurovascular bundle, covered by a layer of fascia and, in the lower part of the field, by the flat reflected tendon of the sternal part of the pectoralis major. The easiest way to define the interval between the pectoralis minor and the coraco brachialis is to pass the index finger behind the upper margin of pectoralis minor and feel for the interval. The tendon of pectoralis minor is divided. The muscle is drawn medially, care being taken of the medial pectoral nerve piercing it and going on to the pectoralis major. Now the fascia over the plexus is divided above and below the former site of the pectoralis minor. If it is absolutely necessary, the flat reflected tendon of the pectoralis major too can be divided. Thus the whole neurovascular bundle is displayed. The lateral cord is the most prominent component, the axillary artery is behind it and the axillary vein medial to it. In the lower part of the field the median nerve is formed from the contributions from the medial and lateral cords. Just at the formation of the lateral cord the lateral pectoral nerve arises to pierce the clavipectoral fascia and enter the pectoralis major. The posterior cord lies deep to the lateral cord and axillary artery; the medial

Fig. 7.42  The infraclavicular brachial plexus splayed over a massive lipoma. The axillary artery(1) is marked by the blue sling, the median nerve (2) by a red sling and the ulnar nerve (3) by a white sling. The medial cutaneous nerve of forearm (4) is seen and the radial nerve (5) lay deep to the tumour. The appearances before (above) and after (below) removal of the tumour (Courtesy of Marco Sinisi).

cord is deep to the axillary vein. Some mobilisation of both great vessels is necessary for the full display of the cords (Fig. 7.42). The musculocutaneous nerve arises from the lateral cord above the level of the coracoid process and runs laterally into the coraco-brachialis muscle. It may be a single branch but can consist of several branches arising at different levels from the cord. The posterior cord and its lateral and terminal branches are exposed between the lateral cord and the axillary artery. The three subscapular nerves are seen, and in the lower part of the field the separation of the trunk into radial and circumflex nerves is visible. Reflection of coracobrachialis from the tip of the coracoid process improves exposure of the anterior “door” of the quadrilateral space and permits exposure of the distal stump of a ruptured circumflex nerve. This display may be extremely difficult in the late case, especially after arterial injury.

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7.7.4 The Circumflex Nerve In cases of rupture the anterior (proximal) stump is almost always found just below the coracoid process and repair sometimes requires exposure of the posterior (distal) stump through a separate posterior incision. Repair has to be effected by graft, and it is certainly easier to secure good placement and attachment through two incisions than through one giving limited access. The posterior circumflex artery is often ruptured by the head of humerus, in anterior dislocation. This can lead to serious bleeding, or to a false aneurysm. The distal stump of the nerve may be strangled in fibrosis and in these cases direct muscular neurotisation is useful as it is when the nerve has been avulsed from the muscle (Fig. 7.43).

7.7.5 Median and Ulnar Nerves in the Arm and the Axilla The incision crosses the anterior axillary fold and the axilla, and descends the medial side of the arm. The flaps are raised and the axillary fat displaced downwards. The neurovascular bundle is found in its sheath in the lower part of the axilla: most medial is the axillary/brachial vein; the nerves are grouped around the lower part of the axillary and the brachial arteries. In the upper arm, the medial cutaneous nerve of forearm (MCNF) lies anterior to the brachial vein and is the most superficial of the nerves within the neurovascular bundle. The nerve perforates the deep fascia in the middle part of the arm. The slender medial cutaneous nerve of the arm (MCA) runs outside and posterior to the neurovascular sheath. Communicating branches between the MCNF and MCA are common. The axillary artery is embraced by the

Fig. 7.43  Rupture of the circumflex nerve at the entrance to the quadrilateral tunnel. The proximal stump (1) and, somewhat unusually the distal stump (2) are visible.

Surgical Disorders of the Peripheral Nerves

two roots of the median nerve, which starts on its lateral side and crosses it in the arm. The musculocutaneous nerve most commonly arises as a single branch from the lateral cord at or below the level of the coracoid process, but it may consist of several branches arising at intervals along the line of the lateral root of the median nerve. It passes laterally into the coracobrachialis muscle and the flexors of the elbow. The ulnar nerve and the medial cutaneous nerve of the forearm are on the medial side of the artery. The former passes posteriorly about half way down the arm to pierce the medial intermuscular septum and to lie between it and the medial part of the triceps muscle, to which it usually gives a branch. Deepest of all is the radial nerve, which crosses anterior to the tendon of latissimus dorsi and then passes posteriorly between the long and medial heads of triceps. The nerve runs behind the humerus deep to the lateral head of the triceps and gains the lateral aspect of the lower part of the arm by piercing the lateral intermuscular septum. The neurovascular bundle can be traced up into the axilla to expose the cords and the origin of the circumflex and radial nerves.

7.7.6 The Radial Nerve The proximal part of the radial nerve is quite easily displayed in the upper part of the axillo-brachial incision; the distal part is easily found through an anterolateral incision in the lower part of the arm and by entering the interval between the biceps and brachialis medially and the brachioradialis and extensor carpi radialis longus laterally (Fig.  7.44). Finding the middle part - the part most likely to be in trouble - is rather more difficult. It is to be found through a posterior incision, and by separation of the superficial part of the triceps (the long and lateral heads) from its deep part (the medial head). The flaps are raised and the lower part of the deltoid muscle and the superficial part of the triceps muscle are exposed. The V-shaped interval between the upper parts of the long and lateral heads is now defined, by locating the upper part of the long head and following its lateral border distally. The “seam of the half sleeve” (Henry 1975) – that is, the junction of the long and lateral heads of the triceps – is now opened from the top towards the olecranon (Fig. 7.45a, b). Further exposure of the radial nerve is anterior to the lateral head of the triceps muscle, by entering the interval between the biceps/ brachialis and the brachioradialis/extensor carpi radialis longus. If there is difficulty in bridging a gap after resection, some length can be obtained by re-routing the distal stump towards the upper medial aspect of the arm deep to the biceps and brachialis muscles. For exposure of the more distal parts of the nerve the incision may be extended round the side of the arm to the medial side of the brachioradialis. Thence it runs across the anterolateral

Operating on Peripheral Nerves Fig. 7.44  Transverse section through the arm above the level of the insertion of the deltoid muscle, just below the level of the posterior movement of the radial nerve.

267

Biceps (short head) and coracobrachialis Musculocutaneous n.

Median n.

Biceps (long head) Deltoid Humerus Triceps (medial head)

Ulnar n. Radial n. Tendinous lamina

Triceps (lateral head) Triceps (long head)

aspect of the elbow into the forearm. With this anterior approach the radial nerve and its terminal branches are found in the interval between the biceps/brachialis and the brachioradialis/ extensor carpi radialis longus. There are important branches from this segment of the nerve. The nerve to brachialis, passing antero-medially is often seen about five finger breadths above the lateral epicondyle. The nerve to brachioradialis passes postero-laterally about 2 cm more distal. More distally still, is the branch to extensor carpi radialis longus and then, after that, branches, usually two, to extensor carpi radialis brevis (Fig. 7.46).

7.7.7 The Posterior Interosseous Nerve In the Henry (1975) approach, the incision is made on the posterolateral aspect of the upper forearm between the mobile mass of the brachioradialis and the radial extensors of the wrist, and the extensor communis digitorum. The interval between the extensor carpi radialis brevis and the extensor communis digitorum is then opened and the supinator muscle exposed. The posterior interosseous nerve passes between the superficial and deep parts of this muscle, to emerge at the lower margin of the superficial part and to run for about 4–5 cm before breaking up into its terminal (motor) branches. The point of emergence can quite easily be found, and the nerve then followed proximally by division of the superficial part of the muscle along its line (Fig. 7.47a, b).

7.7.8 The Lower Part of the Median Nerve The median nerve is easily displayed at and just below the elbow and in the lower part of the forearm through a sinuous incision winding down from the elbow. At elbow level it is found medial to the brachial artery. It then descends between the superficial and deep heads of the pronator teres The median nerve can be traced down into this tunnel, and can to some extent be mobilised by division of the deep (ulnar) head of the pronator teres. Having negotiated the pronator teres, the nerve runs down the forearm between the deep and superficial flexor muscles, loosely attached by areolar tissue to the deep surface of the flexor digitorum superficialis. It can be exposed in this part of its course by separating the flexor superficialis from its radial origin and retracting the muscle. The anterior interosseous nerve is now displayed. The nerve enters the hand just deep to and between the tendons of the palmaris longus and flexor carpi radialis. The “bottle neck” (Lanz 1993) of the carpal tunnel is formed posteriorly and laterally by the concavity of the carpus; in particular, the scaphoid, lunate, hamate, and pisiform bones. It is roofed by the flexor retinaculum and anchored medially to the pisiform and hamate bones and laterally, to the scaphoid and the trapezium. The width of the retinaculum is about 2.5 cm; its length is about the same. Proximally it blends with the ante-brachial fascia, and distally with the palmar aponeurosis. The tendon of the palmaris longus is attached to it anteriorly. A deep lamina on the radial side is attached to the medial lip of a groove on the trapezium. Between this layer

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Surgical Disorders of the Peripheral Nerves

b

a

Deltoid

Teres major

Ulnar n.

Profunda a.

Deltoid

Triceps (lateral head)

Brachial a. Median n.

Triceps (long head)

Radial n. and branches to lateral and medial heads

Lateral head of triceps Tendinous laminae of long head (with cut fibres of lat. head)

Olecranon

Fig. 7.45  The exposure of the radial nerve in the arm. (a) The “seam of triceps” (AK Henry). The finger is introduced between the long and lateral heads and separated. (b) The opening of the “seam” reveals the

and the more superficial part lies the tendon of the flexor carpi radialis muscle in its synovial sheath. On the ulnar side a localised thickening of the ante-brachial fascia extends laterally from the pisiform bone as a superficial part of the retinaculum, passing superficial to the ulnar nerve and vessels to blend with the retinaculum lateral to them. The positions of the motor and the palmar cutaneous branches of the median nerve are very important for the surgeon. Lanz (1993) illustrates 12 variants of the main nerve and its motor branch. In most cases the motor branch arises from the radial side of the nerve in the carpal tunnel and runs laterally, soon branching to supply the short abductor of the thumb, and often part of the opponens and flexor brevis. A particular hazard for the surgeon is produced by an origin from the ulnar side of the nerve and a course across it, either deep or superficial, to the retinaculum. Wadsworth (1984) shows an excellent illustration of the variations in origin and course of the motor branch The palmar cutaneous branch arises from the median nerve about 7 cm above the wrist crease and runs distally, medial to the tendon of the flexor carpi radialis to innervate

radial nerve from the start of its course on the back of the humerus to the piercing of the lateral intermuscular septum.

Fig. 7.46  The radial nerve at the elbow exposed during repair of posterior interosseous nerve cut during operation for fracture of radial head. The nerve is seen in the valley between brachio-radialis and biceps lying on fibres of brachialis. The nerves to brachioradialis (1) to extensor carpi radialis longus and brevis (2) the proximal part of the posterior interosseous nerve (3) a further branch to extensor carpi radialis brevis (4) and the superficial radial nerve (5) are shown. A segment of the lateral cutaneous nerve of forearm (6) has been prepared as a graft.

Operating on Peripheral Nerves

a

269 Extensor carpi radialis brevis

b

Head of radius

Supinator

Extensor digitorum communis

Fig. 7.47  Exposure of the posterior interosseous nerve (After Henry 1975). (a) The incision (left) and the separation of the extensor carpi radialis brevis from the extensor communis (right). (b) The posterior interosseous nerve and supinator exposed.

the skin over the thenar eminence and the radial side of the proximal part of the palm. Damage to this can cause a profound, persistent painful state, with very troublesome hyperaesthesia and hyperalgesia, and even hyperpathia and allodynia (Semple and Cargill 1969; Carrol and Green 1972; Taleisnik 1973) (Fig. 1.28).

7.7.9 The Lower Part of the Ulnar Nerve As the ulnar nerve approaches the elbow, it runs behind the medial intermuscular septum and then passes subcutaneously behind the medial epicondyle of the humerus in the retro-condylar groove. Schroeder and Scheker (2003) define the “arcade of Struthers” thus: “the arcade was better described as a fibrous canal with an average length of 5.7 cm, its openings, at either end, were 3.9 and 9.6 cm proximal to the medial epicondyle”. The components of the arcade include not only the tough medial intermuscular septum of the arm but also the sheath of the medial head of triceps, which can be seen enveloping the nerve, as well as the internal brachial ligament. The ulnar nerve then passes superficial to the medial capsule of the elbow joint and deep to the arcade, joining the two origins of the flexor carpi ulnaris muscle (the arcuate ligament). This is the “cubital tunnel”. The nerve then runs between the flexor carpi ulnaris and

flexor digitorum profundus muscles, joining the ulnar artery in its course down the forearm. The muscular branches arise just below the elbow. The nerve is vulnerable to external pressure. It may be compressed between the arcuate ligament and the medial capsule and with relaxation of this ligament it may become hypermobile, dislocating forward when the elbow is flexed. Because of the excursion required of it during movement of the elbow, it may be stretched during flexion if its movement is restricted by changes due to damage by external pressure. Wadsworth (1977) dealt with the “external compression” syndrome of the ulnar nerve, drawing on Osborne’s (1970) exposition of the role of the arcuate ligament in different positions in the elbow. The ulnar nerve and artery pass down the forearm within a well defined sheath which is found deep to the anterior margin of flexor carpi ulnaris. The nerve and artery may become tightly compressed by swollen anoxic muscle and, later, by post ischaemic fibrosis. Arterial bleeding from a wound on the ulnar aspect of the forearm indicates damage to the ulnar nerve. The ulnar nerve divides into its superficial (sensory) and deep (motor) components at about wrist level. Both components run into Guyon’s space (the piso-retinacular space of Denman (1978)) (Fig.  7.48). The superficial branch passes superficially to supply the palmaris brevis and the skin of the medial two digits; the deep branch runs between the abductor and the flexor of the little finger to pierce the opponens and

270 Palmaris longus

Surgical Disorders of the Peripheral Nerves Hook of hamate bone

Pisohamate ligament

Ligamentous band Ulnar n. (deep branch)

Ulnar n. (superficial branch) Pisiform bone Flexor retinaculum Volar carpal ligament

Flexor carpi ulnaris Ulnar a. Ulnar n.

Fig. 7.48  Guyon’s space. Note the possibilities for entrapment at, and distal to, the volar carpal ligament.

then runs across the deep palmar space with the deep palmar arch, ending by supplying the adductor and flexor brevis of the thumb and the first palmar interosseous muscle. Deep as it is, the deep branch is vulnerable to wounds from glass or knife. Horsley (1899) describes a typical case: “It is the case of a young lady who succeeded in performing, by accident, an exceedingly difficult operation upon her own hand. She was engaged in wood carving, and was working with a very long and narrow chisel. The chisel slipped and stuck into the palm of the hand. She succeeded in just missing the cutaneous branch of the nerve and cut the deep branch”. Horsley sutured the nerve and the patient had complete recovery. The nerve is best followed by an incision beginning above the wrist, entering the ulnar side of the palm and curving across the distal palm in a crease. It is isolated in the upper part of the incision lateral to the tendon of flexor carpi ulnaris and medial to the ulnar artery and followed to its bifurcation. Then the deep branch is followed between the hypothenar muscles. Its deep course has to be revealed by mobilisation of the deep and superficial flexor tendons. The multitude of the motor branches of this nerve, to most of the intrinsic muscles of the hand, has to be borne in mind during this exposure, though it is impossible to avoid some of these in a scarred field.

7.7.10 Nerves in the Abdomen and Pelvis The lumbar plexus is accessible through the lower quadrant of the abdomen, by the same transverse muscle cutting incision

and extra-peritoneal approach that is used for lumbar sympathectomy (Kline et al. 2001a). The exposure may be helped by placing the patient in the lateral or semi-lateral position. The incision is made between the rib cage and the iliac crest. The external oblique is split and the deeper muscle is cut, with opening of the lateral part of the rectus sheath. The underlying fascia is delicately opened and the peritoneum is swept away from the abdominal wall and vertebral column. The lateral cutaneous nerve of thigh, the ilio-inguinal nerve and the iliohypogastric nerve are encountered approaching the lateral and posterior margin of the psoas muscle. The femoral nerve lies in a gutter between the iliacus and the psoas major. The obturator nerve runs medial to the psoas muscle. The lumbo-sacral trunk is closer to the mid line and deep to the great vessels. The spinal nerves passing to the femoral nerve run deep to the psoas muscle in much the same way as the cervical spinal nerves run deep to scalenus anterior and the muscle must be cut or reflected to display them. This approach gives good access to the lumbar plexus in the psoas muscle and to the femoral and obturator nerves on each side of the lower part of the psoas. Access to the lumbosacral plexus is rather restricted through this extra-peritoneal approach. A trans-peritoneal approach makes access easier, but the viscera have to be mobilised with the consequent risks of ileus after operation and of late complications from adhesions. Injuries to the lumbosacral plexus are often associated with forbidding scarring. The femoral nerve can be traced down to the level of the inguinal ligament from above through an abdominal incision and exposed again in the thigh through a separate anterior crural incision. Kline et  al. (2001b) suggest that the crural incision can be extended laterally above the inguinal ligament and the lower abdominal muscles split to give an extraperitoneal approach. The sacral plexus We have no experience of the exposure described by Sedel (1975). Sedel attributes this “voie transiliaque” to Judet and comments that it is relatively destructive to the skeleton but that the exposure of the lumbo-sacral plexus and of the hypogastric venous plexus is excellent. The patient lies in a semi prone position. The incision is vertical, and runs from the inferior margin of the rib cage to the level of the greater trochanter. The iliac crest is exposed and then the gluteus maximus is detached from its insertion and reflected laterally and inferiorly so that the blade of the bone is exposed as high as the sciatic notch. The sciatic nerve and its accompanying vessels are carefully exposed and retracted out of harms way. The internal face of the ilium is exposed by subperiosteal dissection. The bone is now divided between the iliac crest and the sciatic notch. Sedel uses a Gigli saw with malleable retractors protecting deeper structures. It is now necessary to open the sacro-iliac joint by detaching the sacro-iliac ligaments and incising the capsule in the deep face the joint so that the bone flap can be reflected posteriorly with muscles still attached to the crest. The lateral flank of the fifth lumbar vertebra, and “la fossette de Cuneo et Marcille” which

Operating on Peripheral Nerves

a

271

b

Femoral n.

S1

Lumbosacral trunk

S2

Fig. 7.49  The trans iliac exposure of the sacral plexus (After Sedel 1975). (a) The position of the patient and line of incision left and the line of division of the ilium right. (b) Reflection of the fragments of the ilium provides access to the sacral plexus.

contains the lumbo sacral trunk, the obturator nerve, and the ilio-lumbar artery and vein is now accessible. The upper sacral roots appear below, running on the piriformis muscle (Fig. 7.49a, b). Closure of the wound commences with internal fixation of the Ilium followed by careful reattachment of gluteus maximus. The dorsal trans-sacral approach This was described by Linarte and Gilbert (1986). It offers exposure of the cauda equina, the sacral spinal nerves, and also the sciatic nerve which is seen at the sciatic notch after reflection of the origin of gluteus maximus. The patient lies prone. An incision is made from the spinous process of L3 curving somewhat as far as the ischial tuberosity. The para-spinal muscles are elevated from L4 and L5 and from the sacrum. The spinous processes are removed to expose the laminae and the dorsal sacrum as far lateral as the dorsal lateral foramina. The spinal canal can now be opened by hemilaminectomy (Fig. 7.50). This approach enables diagnosis of the level of lesion of the lumbar and sacral spinal nerves and offers the opportunity to place grafts onto the superior gluteal and the sciatic nerves, bypassing severe scar. Carlstedt (2007c) observed that the spinal nerves were either compressed or transected in fractures involving the sacral foramina, rarely avulsed.

Fig.  7.50  Display of cauda-equina after dislocation of hemi pelvis. Severe pain and extensive paralysis were relieved after liberating L4 and L5 from adhesions, 3 months after injury in a 28 year old woman (Courtesy of Marco Sinisi).

7.7.11 The Sciatic Nerve Two exposures are regularly used. In the first, the gluteus maximus muscle is split as in the posterior approach to the hip. This provides an adequate exposure of the sciatic nerve where it traverses the neck of the femur. Up to 15 cm of the trunk can be seen. A second, more extensive, approach is described by Henry (1975.) The prone position is used for both.

272

Surgical Disorders of the Peripheral Nerves

Fig. 7.52  The extended exposure of the sciatic nerve damaged by fracture/dislocation of the hip (After Henry 1975).

Fig. 7.51  Exposure of sciatic nerve by transgluteal approach. Above: The patient lies prone and the incision is made between the tip of the greater trochanter and the ischial tuberosity. Below: the nerve is exposed as it crosses the neck of the femur.

Splitting the gluteus maximus The incision runs obliquely about two finger breadths above the line drawn from the ischeal tuberosity to the tip of the greater tuberosity. The gluteus maximus is exposed and gently split along the line of its fibres noting and preserving branches of the inferior gluteal nerve and securing careful haemostasis. The muscle flaps are held apart with the large Deavers retractor. The nerve is seen crossing the posterior aspect of the neck of the femur, and it can be traced up to the sciatic notch if necessary by division of the piriformis (Fig. 7.51). The wound is closed by repair of the sheath of gluteus maximus, the fat and the skin. This approach is very useful in exploration of lesions of the sciatic nerve incurred during arthroplasty of the hip and the patient is encouraged to mobilise. Full exposure of the sciatic nerve and of the superior and inferior gluteal nerves and vessels is achieved through the more extensive operation described by Henry (1975). Henry compares the “gluteal lid” with a parallelogram whose shorter sides are almost longitudinal and whose longer (upper and lower) sides are oblique. The caudal edge is virtually unattached.

The incision can follow the “question-mark” shape advised by Henry, or can run from the iliac crest at the junction of the gluteus maximus and the iliotibial tract, obliquely down the back and lateral side of the buttock to reach the great trochanter and then turn medially to descend in the mid line of the thigh. It is necessary to look out for the posterior cutaneous nerve of the thigh, piercing the deep fascia in the upper part of the thigh and descending in the midline. It should be identified under the fascia below the lower border of gluteus maximus. Now, the gluteus maximus is detached from its insertion to the femur; the cephalic side of the muscle is separated from the ilio-tibial tract, and both tendinous and muscular insertions to the femur are divided. Then, with continued care for the posterior cutaneous nerve of the thigh, the gluteal lid is hinged back on its pelvic origin. Excessive traction upon the superior gluteal vessels must be avoided. The structures displayed are the gluteus medius and the short lateral rotators of the hip, the superior and inferior gluteal vessels and nerves, the pudendal nerve and vessels and the sciatic nerve. The sciatic nerve can be followed into and through the great sciatic notch by division of the tendon of the piriformis and retraction of the muscle. Downward extension of the vertical limb of this incision permits display of the whole of the sciatic nerve (Fig. 7.52). Careful closure of the wound is essential. In particular, the gluteus maximus must be reattached laterally and cephalad. One or two suction drains should be used. The subcutaneous tissues should be closed.

7.7.12 The Tibial and Common Peroneal Nerves in the Popliteal Fossa and Below The incision starts above the back of the knee and skirts the crease to return to the midline below the knee, to descend in

Operating on Peripheral Nerves

the midline for about 10 cm. The flaps are raised. Care must be taken of the sural nerve arising from the tibial nerve and descending in the midline, at first just under the deep fascia and piercing that in the proximal part of the leg. The tibial nerve and popliteal artery and vein are found above in the mid-line; the common peroneal nerve has at this level deviated laterally to lie close to the tendon of the biceps femoris. The gastrocnemius is split in the midline to expose the underlying soleus muscle, which also is split to show the nerve and vessels below the knee. The tibial nerve in the leg and behind the ankle is exposed through a straight or sinuous incision over the medial head of the gastrocnemius and medial to the tendo calcaneus. The medial head of the gastrocnemius is exposed, freed and retracted laterally to expose the medial part of the soleus. Then, the medial part of the soleus is mobilised by division of the medial “pier” of its tendinous arch and of its medial origin. The soleus is then retracted laterally, to expose the deep compartment of the leg with the tibial nerve and vessels (Fig. 7.53a, b). Exposure of the common peroneal nerve necessarily takes the popliteal incision laterally, to descend on the lateral side of the leg and permit exposure of the deep peroneal and superficial peroneal divisions in which the nerve terminates just below the neck of the fibula. The operator must remember that the common peroneal nerve is very close to the surface behind the head of the fibula and lateral to its neck. We have seen it partly divided by the initial skin incision. The nerve is embraced by fascia enveloping the biceps femoris and is displaced with that muscle in dislocation of the knee.

7.7.13 The Lower Tibial Nerve and the Plantar Nerves The lower part of the tibial nerve is easily found on the medial side of the ankle, under the flexor retinaculum, between the flexor tendons of the hallucis and the flexor digitorum. The terminal plantar branches are traced into the foot by division of the retinaculum and then by bringing back the abductor hallucis muscle after defining its superior edge and detaching it from its origin on the distal part of the retinaculum. The plantar nerves are found between the deep and superficial layers of the plantar muscles in the plane between, on the one hand, the two abductors and the flexor brevis digitorum and on the other, the flexor accessorius and the tendons of the long flexors (Fig. 7.54a, b).

7.8 Entrapment Neuropathy The concept of the entrapment syndrome is attractive; the belief that symptoms from such syndromes are easily relieved

273

by simple operation is especially espoused by operative masons. In practice, the matter is not so simple, because when things go wrong symptoms are likely to be severe, persistent, and resistant to treatment. No letter fills us with more gloom and apprehension as one requesting an opinion on symptoms persistent after operation for entrapment neuropathy. The proffered case is indeed likely to prove a poisoned chalice. The term “entrapment neuropathy” should probably be reserved for instances in which a small addition to the crowding produced by existing anatomical arrangements is liable to cause compression, constriction or distortion of a peripheral nerve or, by interfering with the ability of the nerve to glide, to cause traction injury. The situation of the median nerve deep to the flexor retinaculum provides an obvious example of such an anatomical arrangement, and the causes of lesions there provide a microcosm of the wider field. Comtet (2005) points out that “pure nerve compression is rare” and that it is usually compounded by traction, shear, or vibration as well as by the effects of generalised disease. In many cases, it appears , at first sight, impossible to distinguish a precipitating cause other than the anatomical situation of the affected nerve. However, the more rigorously investigation is pressed, the fewer true entrapments will be found. Investigation should be thorough because the recurrence of an “entrapment syndrome” may be the first sign of serious underlying disease, and both surgeon and patient may have cause, later, to regret a temporarily successful operation (Spinner and Spencer 1974; Gelberman et  al. 1993.) Rosenbaum and Ochoa (1993) show, that in a combined series of 2,705 patients with “carpal tunnel syndrome” there were 321 with rheumatoid arthritis, 166 diabetics, and 94 with hypothyroidism, a total of 581 patients. In another 30, the condition was related to pregnancy or to an oral contraceptive. Most of our experience is drawn from failures of primary operations. Since 1979, more than 500 patients have been treated because of failure of, or complications of, first operation for entrapment neuropathy. Four causes head the list. 1. Error in diagnosis. The symptoms of entrapment neuropathy may, in fact, point to a proximal lesion of the nerve or to a generalised disease of nerve or muscle or to a systemic endocrine, neoplastic or circulatory disorder. Many errors can be prevented by the appropriate electrodiagnostic investigation (Chapter 6). 2. Inadequate decompression. 3. Damage to the nerve, to branches of the nerve, to adjacent nerves or vessels. 4. Provocation of the fibrosis which entraps the nerve with even more vigour than before operation. The gliding mechanism is destroyed and it is this often unavoidable complication of operation that underlines the failure of so many interventions. The rate of recurrence of symptoms increases with the duration of follow up. Scar is inevitable after operation. It is worse after clumsy surgery and worse still following a haematoma.

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Surgical Disorders of the Peripheral Nerves

Fig. 7.53  Exposure of the tibial nerve in the leg (After Henry 1975). (a) The soleus exposed and the line for its detachment shown. (b) The tibial nerve and vessels revealed by the retraction of the soleus.

a

Popliteal a.

Gastrocnemius (medial head)

Popliteus Line of incision dividing medial pier of soleus arch Divided edge of soleus

Plantaris

Tibia

Tibialis posterior 2nd layer of deep fascia Flexor digitorum longus

Tibial n. Posterior tibial a. 1st layer of deep fascia

b Popliteus

Gastrocnemius (medial head)

Tibial n. Tibioperoneal trunk

Nerve to flexor digitorum longus

Posterior tibial a. and v. Tibia

Medial pier of soleus arch divided and turned back

Tibial attachment soleus turned back Peroneal a. and v.

Plantaris tendon

Tibialis posterior

1st layer of deep fascia

Flexor digitorum longus

Posterior tibial a. and tibial n.

Operating on Peripheral Nerves Fig. 7.54  Exposure of the plantar nerves through a medial incision (After Henry 1975). (a) Retraction of abductor hallucis reveals the medial plantar nerve. (b) Release of the tendon of the flexor longus hallucis gives access to the whole of the deep compartment of the sole.

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a

Navicular tubercle

Master Knot of Henry

Long saphenous v. Flexor hallucis longus Flexor hallucis brevis Flexor digitorum longus

Medial plantar bundle

Flexor digitorum brevis

Abductor hallucis Lateral plantar bundle

Navicular tubercle

b

Divided Master Knot of Henry

Tibialis posterior

Short plantar ligament Tibialis anterior tendon Flexor hallucis brevis Flexor hallucis longus

Lumbricals Abductor hallucis

Peroneus longus tendon

7.8.1 The Thoracic Outlet Syndromes Wilbourn (1993) described thoracic outlet syndrome as one of the most confusing and certainly the most controversial of all peripheral disorders: “The confusion exists mainly because many physicians are unaware that several different entities are grouped under this one heading, entities that have little in common beyond their known or presumed lesions site”. Narakas (1993) described more than 18 different types of compression syndromes arising between the cervical spine and the inferior margin of pectoralis major and he proposed the general term “syndrome de la traversée cervico-­thoraco-brachiale”. This

Lateral plantar bundle

Flexor Flexor Long Quadratus Medial digitorum plantae plantar digitorum plantar ligament brevis bundle longus

concept has been developed by Poitevin (2005a, b) who introduced the term “upper limb inlet” to include complete and incomplete tunnel like spaces spanning from the axial skeleton of the thorax and cervical spine to the lower border of the pectoralis major muscles. Poitevin (2005a) writes: “The scalene complex is a common mass running from the cervical vertebrae and reaching the first and second ribs. During development, this mass is fragmented in a variable fashion. As a result of this fragmentation, muscular bridges remain joining anterior and middle scalene muscles, passing in between the neurovascular bundles. These muscular bridges sub divide and reduce the interscalene space which is altered or diminished by

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variations in the shape, the number and the extension of the insertions of scalene muscles and also by the presence of a cervical rib”. The lower part of the brachial plexus and the lower trunk in particular, joined at the first rib by the subclavian vessels, run a regular obstacle course on their way to the lower borders of the pectoralis minor muscle. Some of the more important obstacles are now described

Surgical Disorders of the Peripheral Nerves

Rhomboid lig.

Scalenus medius

Scalenus anterior

V

7.8.2 The Suprapleural Membrane (Sibson’s Fascia)

A Subclavius

In its pure form, the suprapleural membrane is a thin, fanshaped structure attached apically to the tip of the seventh cervical transverse process and peripherally to the medial edge of the rib. The extent of its peripheral attachment varies. The deep part of the membrane may be quite tough and aponeurotic. The scalenus minimus is the muscle that sometimes replaces the deep or posterior part of the membrane. The muscle may be up to 10 mm in diameter in its widest part, but is usually much smaller than that. The posterior border of the membrane forms, with the edge of the first rib, the foramen through which the first thoracic nerve escapes. The membrane covers the apical pleura and intervenes between it and the subclavian artery.

7.8.3 The First Rib The broad first rib, whose surface is more horizontal than vertical, extends from the head at the vertebral body, the neck and the costotransverse articulation, over the apical pleura to curve round to the costo-chondral junction and then to the manubrium (Fig. 7.55). The apical pleura is, in the healthy state, easily separable from the head and neck and most of the underside of the first rib. Anteriorly, it becomes rather adherent to the underside of the rib, in relation to the costochondral junction. The scalenus medius is attached to the upper surface of the rib posteriorly. The upper part of nerve to the serratus anterior is usually formed in the muscle by branches from the fourth, fifth and sixth cervical anterior rami; it emerges from the lateral surface of the scalenus where it is usually joined by the contribution from the seventh cervical nerve. In front of the scalenus medius the surface of the rib is, in the adult, grooved by the passage of the first thoracic nerve and lower trunk. There is a distinct tubercle at the attachment of the scalenus anterior, behind which is the slight depression for the subclavian artery. In front of the scalenus tubercle the subclavian vein runs over the upper surface of the rib. The intercostal muscles are attached to the

Serratus anterior

Scalenus posterior

Fig. 7.55  The upper surface of the left first rib, showing the sites of the arterial and venous crossings and the muscular attachment (After Frazer 1920).

edge of the rib. The lower part of the cervicothoracic (stellate) ganglion lies on the head of the first rib, deep to the proximal part of the vertebral artery arising from the subclavian. The major part of the first thoracic nerve is at first below the rib, then medial to its edge. The white pre-ganglionic ramus of the first thoracic nerve connects it to the stellate ganglion; the grey ramus (post-ganglionic) is less noticeable. The size and disposition of the scalenus anterior varies. It may bifurcate to include the artery, the muscle itself may be bulky and the tendon may curve posteriorly round the artery to form a kind of snare. Deep to the scalenus, a very thin fascia covers the artery. The phrenic nerve, chiefly derived from the fourth cervical anterior ramus, curves round the muscle to run down in front of it into the thorax, lying at first behind the internal jugular vein and crossing behind the subclavian vein. On the left the thoracic duct and on the right the right lymphatic duct enter the brachiocephalic (innominate) vein at the subclavian-jugular (tri-radiate) junction.

7.8.4 The Seventh Cervical Rib Parry and Eastcott (1992) and Narakas (1993) credit the second-century physician and anatomist Galen with the first description of the seventh cervical rib. A little later, Gruber (1869) published his classification of such ribs according to their size and connections. Narakas (1993) indicates an incidence of seventh cervical ribs of 0.004 to 1% and he says that cervical rib “is asymptomatic in 90% to 95% of persons”. The extent of the rib, which is rarely bilaterally symmetrical, ranges from a prolongation and pointing of the seventh cervical transverse process to a complete rib in all respects like a

Operating on Peripheral Nerves

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TYPE I

C7

T1

Omohyoid TYPE II

TYPE III

C7

C7

T1

T1

TYPE IV

TYPE V

C7

C7

T1

T1

Fig. 7.56  Variations of the seventh cervical rib, ranging from elongation of the seventh cervical transverse process to a virtually complete additional rib (After Sargent 1921).

first thoracic rib. The classification proposed by Sargent (1921) is illustrated in Fig. 7.56. Arterial Thoracic Outlet Syndrome This was the first of the syndromes to be recognised and the first to be treated surgically. Cooper wrote (Cooper and Travers 1817): “I have

seen an exostosis arise from the 6th or 7th cervical vertebrae or perhaps from both”. He went on to describe the case of a woman who came into Guy’s Hospital with no pulse at the wrist or elbow and with “venous redness” of the upper limb, which was cold, “enumbed” and painful. There was a projection of the lower cervical vertebrae towards the clavicle, with consequent pressure on the subclavian artery. Coote (1861) reported the removal of a left seventh cervical rib causing aneurysm of the subclavian artery. Two physicians, Lewis and Pickering (1934) pointed to the mechanism of production of the arterial lesion – namely, intimal breakage with local thrombosis and distal embolisation. Arterial affection occurs as the subclavian artery crosses a “normal” first rib or a seventh cervical rib, commonly one with bony union to, or synchondrosis or synostosis with, a boss on the first rib at about its middle part. The vessel is distorted by the bone and constricted by a leash formed by the tendon of insertion of the scalenus anterior. There is commonly dilation of the artery distal to the point of constriction: that dilation may proceed to the formation of a true aneurysm (Wickham and Martin 1962) Complete obstruction of the main vessel with distal embolisation may lead to critical ischaemia. The most dangerous complication is that demonstrated by Symonds in 1927, that of contralateral hemiplegia, doubtless from embolisation from thrombus extending proximally to the carotid vessel. The arterial form of this outlet syndrome is a condition predominantly affecting young women; the occurrence of such symptoms in older persons must suggest a primary diagnosis of atherosclerosis or other systemic disorder . The symptoms are initially those of a Raynaud phenomenon with episodic blanching and temperature change; episodic pain with muscular activity; distal ulceration and necrosis. The extremity may be cooler than the unaffected limb; there is likely to be a pulse difference, even the absence of a pulse. Even if the hands are the same colour at rest, slightly dependant, there is likely to be blanching of the affected hand on elevation. The artery is prominent, displaced upward and anteriorly by the underlying rib. There is a loud bruit, there may be a thrill. Doppler ultrasound examination is likely to show abnormality: Parry and Eastcott (1992) named principally the finding of a clamped, monophasic velocity signal anywhere over the arterial tree of the upper limb. Radiographs will, of course, show the seventh cervical rib if one is present. Magnetic resonance angiography and duplex ultrasonography, have generally superseded arteriography in this and in other fields. These confirm the site and extent of the obstruction, the extent of stenosis and aneurysm formation, and the degree of distal occlusion (Fig. 7.57). Operation is required urgently in cases of critical ischaemia, and soon in cases in which ischaemia is threatened. It may be indicated when a cervical rib is present, causing no symptoms, but producing deformity of the subclavian artery

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Surgical Disorders of the Peripheral Nerves

Fig.  7.58  Appearance at operation in two cases. Above: showing thrombosis, stenosis and post stenotic dilatation of the subclavian artery, with peri-arteritis (and distal embolisation) in a girl with a cervical rib. Below: another case of thrombosis in a young woman. The right subclavian artery has been opened to show the detached intima.

ing four stages of arterial affection in the presence of a seventh cervical rib. Their recommendations are as follows

Fig. 7.57  Angiographic appearances. Above: complete occlusion over cervical rib. Middle: complete occlusion at the outlet in a 40 year old woman, a heavy smoker. Below: obstruction of the artery at the outlet with elevation of the limb.

sufficient to cause a steady bruit over the vessel. Such a bruit must surely indicate distortion of the vessel which is likely, in time, to cause intimal breakage and thrombosis (Fig. 7.58). In cases with clear signs of arterial affection it is rarely sufficient simply to remove the seventh cervical or first rib and to rely on the decompression so afforded. Haug and Sanders (1991) follow Scher and colleagues (1984) in defin-

Stage 0. Rib(s) with no symptoms and no aneurysm should be left alone, though the presence of a bruit is an indication for angiography. Stage 1. Rib(s) with minimal stenosis and mild post stenotic dilation are treated with arterial decompression by resection of the abnormal rib. Stage 2. Rib(s) with aneurysm, intimal damage and mural thrombosis should be treated by resection of the rib and excision and repair or ligation and bypass of the aneurysm. Stage 3. Rib(s) with distal embolisation require distal embolectomy and cervico-thoracic sympathectomy in addition to rib resection and arterial recon­ struction. Parry and Eastcott (1992) recommend endarterectomy or resection and anastomosis for short stenoses, strip resection

Operating on Peripheral Nerves

for a large aneurysm, and saphenous vein grafting for more extensive lesions. A long by-pass graft may be necessary. We have no personal experience of such cases, but have seen critical ischaemia relieved by this intervention. The arterial thoracic outlet syndrome is uncommon rather than rare and it is potentially dangerous. The bruit from a prominent subclavian artery associated with underlying seventh cervical rib, cannot be ignored. Investigations need to be pursued to define the extent of distortion of the artery. The Neurogenic Thoracic Outlet Syndrome This is rare. As Gilliat (1984) pointed out a number of cases were seen at the National Hospital for Nervous Diseases, Queen Square, in the early years of the last century, with wasting of the thenar muscles which were attributed to a cervical rib. In fact, these patients probably had a carpal tunnel syndrome. The confusion was not resolved for more than 40 years until the application of nerve conduction studies defined the much more common disorder. Gilliatt put the annual incidence, in the general population, of the cervical rib syndrome with muscle wasting, as low as one in one million. The patients are usually young to middle aged women. The abnormalities are confined to one upper limb in the great majority. The symptoms are insidious, and often mild, so that presentation is delayed for some years, usually by the sudden realisation that the hand is wasted. There is pain in the medial aspect of the forearm. There may be some blunting of sensibility in that area and in the little finger which is frequently shorter than it is in the normal hand, suggesting that the affliction of the fibres in the lower trunk commenced before skeletal maturity. There is wasting of the superficial thenar muscles which sometimes extends to all of the small muscles of the hands (Fig. 7.59). There may be weakness of the flexor muscles of the forearm, most evident in those innervated by the ulnar nerve. We detected a bruit over the subclavian artery in 14 of our 38 cases of true neurogenic thoracic outlet syndrome. Radiographs of the neck show rudimentary cervical ribs or elongated transverse processes of the seventh cervical vertebrae. The diagnosis is confirmed by the neurophysiological evidence described in Chapter 6. Operation is indicated in these patients in the expectation of alleviation of pain, improvement in sensation and some improvement in strength but recovery of the wasted small muscles of the hand is rare. Neural Outlet Syndrome without plain motor signs. This is much more difficult. A large variety of symptoms has been attributed to compression at the outlet in addition to pain, paraesthesiae and numbness affecting the ulnar side of the forearm and hand, and circulatory disorder of the hand. We think that the clinician, having excluded causes outside the thoracic outlet, should first attempt to identify conditions which are or could be precursors of the “true” neural syndrome. Here is a typical example. A woman in her twenties or thirties presents with paraesthesiae affecting the ulnar side

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Fig.  7.59  The classical neurological outlet syndrome: shortening of the little finger is often evident. Above: Severe wasting of the intrinsic muscles of the right hand in a 35 year old woman. Below: the right lower trunk is seen angulated over a “scalenus sickle”. There is extreme attenuation of the trunk, which, in the photograph, appears to be rather lateral to the sickle. When the nerve was first exposed at operation, the zone of attenuation was, in fact, at the site of angulation. There was slow improvement after decompression.

of her forearm and hand and mild circulatory changes in the hand. There is tenderness over the lower part of the plexus above the clavicle on the affected side but none on the unaffected side. There is an impression of fullness in this site of tenderness; tapping produces radiated paraesthesiae. There is a bruit over the subclavian artery at rest on the affected side but not on the unaffected side. The radial pulse on the affected side is labile, disappearing with bracing of the shoulder or elevation of the limb. Radiographs show elongation of the seventh cervical transverse process or some degree of seventh cervical rib. Magnetic resonance imaging shows distortion of the lower part of the brachial plexus (Panegyres et al. 1993). Electrophysiological examination shows F-wave abnormalities in the ulnar nerve. Lucky is the clinician who is presented with so full a picture! But it does happen and when it does, a period of “conservative” treatment is given,

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Surgical Disorders of the Peripheral Nerves

recommend a first operation on the thoracic outlet; even the boldest may recoil from the prospect of a second operation in a scarred field. It may however be inevitable when (1) the primary operation limited to scalenectomy has plainly for a time relieved symptoms; (2) there are true signs of recurrent interference with structures at the outlet; (3) damage to nerves has been inflicted during the primary operation.

7.8.5 Considerations About Operation

Fig. 7.60  Entrapment of the lower trunk through abnormality of the suprapleural membrane and scalenus medius. Above: the right lower trunk is trapped between the aponeurotic edge of the scalenus medius posteriorly and the suprapleural membrane anteriorly. Below: a “scalenus sickle” and an anomalous scalenus anterior. The left lower trunk passes over the edge of the sickle and behind the part of the scalenus anterior that passes behind the subclavian artery.

but is no more than a formality, and operation is recommended when that treatment fails (Fig. 7.60). Far more difficult is the case in which the symptoms are more diffuse and the signs less clear. The finding of a bruit over the subclavian vessel on the symptomless side as well as on the affected side is at least discouraging, as is lability of the radial pulse on the unaffected side. Failure to gain support from electrophysiological evidence, from arteriography or from magnetic resonance imaging should encourage clinicians to give “conservative” methods a trial. Most difficult of all is the case in which operation, usually simple section of the scalenus anterior muscle, has been undertaken on a largely speculative basis and has at first succeeded, but then symptoms have recurred. All who operate regularly at the thoracic outlet know well the extraordinary amount of scarring which can follow even so simple an operation as anterior scalenotomy. No one should lightly

Three routes are available for access to the thoracic outlet and neurovascular bundle: (1) Anterior supraclavicular; (2) Transaxillary; (3) Posterior. The anterior route offers the best exposure of the plexus, the artery and the sympathetic chain, and of the proximal structures likely to distort or compress them. Its disadvantages are the difficulty of access for removal of the first rib and the restricted access to the subclavian vein. The incision is placed just above the clavicle. It is important that division of the scalenus anterior should be complete and should include the fascia at the back of the muscle, so as to permit display and later mobilisation of the subclavian artery. The suprapleural membrane is now visible. It is defined and divided so that the apical parietal pleura can be pushed away from the sides of the vertebrae and the inside of the chest wall. Once the vessel is mobilised, it is possible to display the plexus from the fifth nerve just lateral to the scalenus anterior to the first thoracic nerve winding round the medial side of the posterior part of the first rib to join the eight cervical nerve and form the lower trunk. At this stage it should be possible to see or feel any distortion or compressing agent such as a scalenus minimus, a scalenus medius band or a seventh cervical rib. A scalenus minimus or an aponeurotic thickening of the posterior edge of the suprapleural membrane should be divided. A scalenus medius band should be removed as follows. First, it is carefully cut at its attachment to the first rib below the first thoracic nerve then it is traced up behind the lower trunk, and between the eighth and seventh cervical nerves, to its attachment to the seventh cervical transverse process. Its deep surface is separated from the muscular part of the scalenus medius, its attachment to the transverse process is divided and it is removed. If the underlying muscle appears to be distorting the lower part of the plexus, its prominent part should also be removed. The question will now arise as to whether the decompression effected is adequate. Before the wound is closed the surgeon should certainly put a finger between the first rib and the clavicle and then manipulate the upper limb to make sure the finger is not trapped in any position of the shoulder girdle. If there is clear evidence of costo-clavicular compression, the first rib should be removed since the

Operating on Peripheral Nerves

opportunity to do this with relative ease will not occur again. If there is no such compression the rib should be left alone. Removal of the seventh cervical and first thoracic ribs. It is safer to remove the rib(s) piecemeal, dividing them into sections. Useful instruments include a 5 mm spinal punch, and bone nibblers angled to 60°. The seventh cervical ribs should be removed from the level of the tip of the transverse process to the attachment to the first rib wherever the latter may be and in whatever manner it may be formed. The posterior end is best reached between the seventh and eighth nerves; its middle between the eighth and first thoracic nerves, and the lower end below the first thoracic nerve, either behind or in front of the artery. Any articulating bony boss on the first rib should be removed with the attached tendon of scalenus anterior. Particular care has to be taken with the removal of the anterior part of the first thoracic rib since the subclavian vein can be nipped, and the pleura is often adherent here to the under surface of the rib. The rib is divided near the costo-chondral junction or separated from the costal cartilage. The importance of the extra-periosteal removal of ribs is stressed. The wound is closed over a suction drain. A few stitches reunite the fatty areolar tissue, the omohyoid muscle is repaired, and the platysma and skin are closed. A subcuticular suture is neat, but a well-placed and well-sutured wound heals well whatever type of suture is used. Dangers of operation: The spinal nerves and the trunks of the plexus are displaced forward and laterally by the abnormal rib(s) and are at risk during the exposure. Sometimes the first thoracic nerve is so attenuated over a scalenus medius band or seventh cervical rib that the surgeon may fail to see it and may accidentally divide it. It is difficult to avoid damaging the phrenic nerve by traction, so producing a temporary paralysis of the hemi-diaphragm. The subclavian artery is sometimes fragile, even when symptoms are predominantly neural. The most serious immediate danger is that of wounding the subclavian vein behind the clavicle. It may be difficult to effect repair in this restricted space because of the difficulty of achieving control. In these circumstances it may be necessary, while bleeding is controlled by pressure, to extend the exposure by elevation of the manubrio-clavicular flap. It is in the region of the vein and tri-radiate junction on the left side that the thoracic duct may be injured especially in a scarred field. This damage is usually recognised because of the leak of milky fluid. It is best to identify and repair the leak, because if the pleura has been opened there is a real danger of formation of a chylothorax. If the hole cannot be repaired, it can be plugged with a muscle graft. Damage to the pleura is a tiresome but sometimes unavoidable complication usually necessitating the introduction of an intercostal catheter connected to a water seal. Sometimes the hole can effectively be repaired, the air aspirated and the lung expanded, and the necessity for pleural drainage avoided.

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The principal delayed complication of operation is the development of a painful neuropathy, with extensive scarring around the nerves In a proportion of cases, even when the utmost care is taken to avoid rough handling of the plexus, a painful and persistent neuropathy develops, resistant to treatment with analgesics and in particular to further non specific exploration for decompression. It is this complication which should be present in the mind of every surgeon about to propose operation for thoracic outlet syndrome, and in particular for an outlet syndrome not associated with a clearly defined lesion. The transaxillary approach is admirable for access to the subclavian/axillary vein and the middle and anterior parts of the first rib. Its use is of course mandatory on the rare occasions when there is distal obstruction in the axilla. We have never found it easy; we have always found access to the posterior part of the first rib is limited and we are not alone in discerning the risk to the plexus imposed by the position of the limb. Roos’ (1981) detailed description of the procedure is required reading. It is an admirable approach for a second operation following recurrence after a supraclavicular procedure. It is the obvious approach for relief of costo-clavicular compression causing predominantly “venous” symptoms. The positioning of the patient is very important. Best is a lateral position, with the table slightly rolled towards the surgeon. The assistant holds the affected limb at an angle of 90° to the axial line avoiding lateral rotation, and should be prepared to relax the position for a few minutes every 15 min. The incision is in the skin crease at the level of the third rib, just below the hair line. The flaps are raised and the chest wall and neurovascular bundle are displayed. As with all transaxillary procedures, it is as well to define early with the stimulator the position of the nerve to serratus anterior in the posterior part of the wound. The intercosto-brachial nerve running down the axilla is seen and preserved. Later, the superior thoracic artery and vein are tied and divided to allow access to the upper part of the axillary tunnel. With swab dissection the operator follows the chest wall, under the neurovascular bundle, into the apex of the axilla until the lateral edge of the first rib is felt. It is as well at this stage to verify identification of the rib on the screen: the second rib has been mistaken for the first. Roos has said that with abduction of the shoulder the axilla opens up like a oyster. He may perhaps, in writing this, have forgotten that for the unpractised hand opening an oyster is very difficult. Access does indeed depend critically on abduction of the shoulder, but the surgeon must at all times bear in mind the limits of tolerance of that position by the nerves of the plexus. We have found Deaver retractors useful, but Roos (1981) prefers the Heaney vaginal retractor as being less liable to damage the vein and muscles. The first rib, whose lateral margin is at first the only part easily visible, is cleared by swab dissection to reveal the

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upper surface crossed by the first thoracic nerve and subclavian artery and receiving the attachment of the scalenus anterior. In front of this is the crossing of the subclavian vein. Anterior to the vein is the tendon of the subclavius muscle. Laterally, the edge of the first rib receives attachment of the intercostal muscles. Once these have been cleared from the rib, the apical pleura can be separated from its lower surface. The tendons of the subclavius and the scalenus anterior muscles are divided and the nerve, artery and vein are very carefully mobilised from the upper surface of the rib. The scalenus medius muscle is cleared from the upper surface of the posterior part of the rib, then the suprapleural membrane can be freed from the medial surface of the rib. In these proceedings the Howarth dissector and the small Doyen raspatory are useful. The aim is to remove the rib extra-periosteally from, anteriorly just in front of the subclavian vein to, posteriorly, behind the crossing of the first thoracic nerve. The anterior division is the easier: with the vein held up and the pleura depressed, the rib can be divided with fine bone cutters or simply separated from the costal cartilage. The posterior division is more difficult, because of the presence of the first thoracic nerve. This can be held and pushed out of the way during the division of the bone - usually, just distal to the costo-transverse joint. The rib is strong here: it can rarely be divided with a single bite of the bone cutters. Bleeding is checked before closure. The wound comes together very well with the lowering of the limb. The subcutaneous fascia and skin are closed over a suction drain; if the pleura has been opened, an intercostal catheter should be added. Dangers and complications: The chief immediate danger is that of damage to the subclavian vein. Bleeding is very severe. It must be checked with local pressure until the vein is sufficiently accessible proximally and distally to permit isolation of the segment and repair of the tear. The lesion most often suffered by the plexus during the operation is that inflicted by prolonged abduction and lateral rotation, neither of which should be permissible. It must be remembered that the first thoracic nerve is very vulnerable during the exposure and division of the posterior part of the rib. The posterior approach gives the best access to the posterior ends of the first rib and a seventh cervical rib, and allows the operator to separate the first thoracic nerve from the neck of the first rib. On the other hand, access to the vessels, the anterior part of the first rib and the distal part of the plexus is restricted. We have found it too difficult and too traumatic and bloody to be suitable as a primary route for the removal of a seventh cervical or first thoracic rib. Pain is common after this operation, doubtless because of the amount of muscle cutting and retraction necessary. Neural, vascular and pleural complications are rare. We prefer to reserve this approach for the removal of a remnant of the first rib or a seventh cervical rib left after a previous operation by the anterior route.

Surgical Disorders of the Peripheral Nerves

7.8.6 Carpal Tunnel Syndrome It was the paper by Brain, Wright and Wilkinson (1947) that opened British eyes to the existence of the condition and to the benefits of treatment by operation. Brain and his colleagues did not deal only with clinical features and results of operations; they also made measurements of variations of pressure in the carpal tunnel. It is interesting to note that those measurements showed that extension of the wrist produced a rise of pressure in the carpal tunnel much greater than that produced by flexion. Since 1947 the carpal tunnel industry has expanded enormously: so too has the understanding of the underlying causes. However, practice has tended to run ahead of the systematic search for an underlying cause. Decompression is, after all, superficially a simple, and generally successful operation, but the clinician must bear in mind the possibility of a systematic cause for neuropathy. Kretschmer and his colleagues (2009) provide an important and salutary account of the risks of endoscopic carpal tunnel release. Our experience with the method is confined to the treatment of its complications in 38 patients.

7.8.7 Technique of Operation (Open Method) General anaesthesia is necessary after failure of a primary operation. If a bloodless field is used the cuff should always be released and bleeding checked before closure. We rely on the effect of elevating the hand on pillows and prefer local anaesthetic. The incision should be planned to avoid damage to the palmar cutaneous branch of the median nerve. It starts proximal to the wrist crease, just to the ulnar side of the mid line. The median nerve is identified before it passes deep to the flexor retinaculum. This enables detection of aberrant branches, and avoids damage to the nerve if it has become adherent to the under surface of the retinaculum. The retinaculum is divided from proximal to distal under vision and the nerve, tendons and synovial membranes are exposed. The state of the nerve, tendons and synovial membrane is recorded. If there is any doubt about the condition of the synovial membrane, a piece is removed for histological examination. If a cuff is used, it is released at this stage and particular note is taken of the reperfusion of the nerve. Bleeding is checked and the skin is closed. We have not thought it necessary to resort to ligamentoplasty. There is no case for internal neurolysis and external neurolysis is only done if the nerve is adherent to adjacent structures. After the closure a padded dressing is applied. This is supplemented with a plaster slab holding the wrist in 20 degrees of extension. This is removed at about 48 h after operation (Fig. 7.61). The ulnar nerve at the elbow The diagnosis of focal ulnar neuropathy at the elbow may be easy, as in the case of a

Operating on Peripheral Nerves

Fig. 7.61  Release of the carpal tunnel. Our preferred incision is shown above. The operation is done using infiltration with local anaesthetic usually without tourniquet. The incision is placed to protect the palmar cutaneous nerve and it extends proximal to the wrist crease where the median nerve is identified. Middle: A tourniquet was used in this case and the nerve “flushes up” after release of the cuff. Note the zone of

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constriction formerly deep to the retinaculum. Below: The wound is dressed with paraffin gauze and a plaster of Paris splint is applied holding the wrist in 20 degrees of extension. This reduces discomfort and also the risk of prolapse of the nerve. It is removed at 48 h after operation.

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patient in his thirties with serious deformity of the elbow following previous injury, with motor and sensory signs in the distribution of the ulnar nerve, with tenderness of an ulnar nerve thickened at the elbow, and with marked slowing of conduction along the nerve at the elbow. It may be difficult, as in the case of a man in his sixties with weakness and wasting of the small muscles of both hands and with marked degenerative changes at the cervical spine. An easily made, though rare error, is to confuse “snapping” of an enlarged or abnormal medial head of triceps over the medial epicondyle with abnormal mobility of the ulnar nerve (Spinner and Goldner 1998). The more important and much more common difficulty is to determine the level or even the levels at which the nerve cell is being compressed, distorted or otherwise damaged. Is it in the anterior horn cell, in the spinal canal, in the intervertebral foramen, at the thoracic outlet, at the elbow or in the wrist or hand?

7.8.8 Operations for Ulnar Neuropathy at the Elbow Simple Decompression. (Osborne 1970), is adequate in most cases. Nathan et  al. (1995) showed good or excellent relief after decompression of 164 nerves in 131 patients. At an average of 4.3 years good relief was maintained in 79%. Their predictors of good outcome were: absence of subluxation after operation, greater body weight and normal two point discrimination before operation. The ulnar nerve is displayed through a curved postero medial incision running distally from above the level of the medial epicondyle. A posterior branch of the medial cutaneous nerve of forearm (MCNF) seems always to be in the way and this must be seen and preserved. The arcuate ligament is divided and the fibres of the flexor carpi ulnaris are separated. The nerve is inspected before and after release of the cuff if this has been used, and the area is examined to exclude the possibility of a compressing agent, such as a ganglion. The cuff is released and haemostasis secured. Osborne (1970) sutured the arcuate ligament deep to the ulnar nerve to provide a bed for it, but we have not followed this practice. The skin is closed. There is no need for immobilisation; indeed, immobilisation can lead to tethering and to later trouble. Transposition. Transposition is necessary when there is severe deformity, extreme osteophytosis, recurrent subluxation over the medial epicondyle or recurrence of signs of nerve compression after simple decompression. Both the surgeon and the patient must recognise the limitations and hazards of this procedure. A bloodless field and general anaesthesia are necessary. The long postero-medial incisions starts 10 cm above the medial epicondyle and ends 10 cm below it. The anterior skin flap is raised in its full thickness. Special care must be taken to identify and preserve the posterior terminal branch of the medial cutaneous nerve of

Surgical Disorders of the Peripheral Nerves

forearm, which runs obliquely in an awkward position, distal to the medial epicondyle. Now the flexor origin and the undisplaced ulnar nerve are displayed. In the next step the ulnar nerve is mobilised, with its extrinsic axial vessels, from about 8 cm above to 6 cm below the epicondyle. Above the epicondyle by division of the overlying fascia; below it, the arcuate ligament has to be divided and the two parts of the flexor carpi ulnaris are separated. In the lower part the uppermost muscular branches are displayed and mobilised, either with the main nerve or away from it. Now, the medial intermuscular septum is excised. Subcutaneous transfer is recommended in most cases. The nerve is lifted from its bed and re-routed in front of the medial epicondyle and the flexor origin, care being taken to avoid kinking or obstruction at either end of the altered course. The cuff is deflated and bleeding is controlled. The two heads of the flexor carpi ulnaris can be brought together above the point of re-entry of the ulnar nerve, but there must be no constriction at that point. It is quite a good plan to put two or three sutures between the subcutaneous fat and the underlying aponeurosis of the flexor origin in order to retain the nerve in its new course. The skin is closed over a suction drain. In order to lessen adhesions around the transferred nerve, gentle movement of the elbow is encouraged on the day of operation. We identify three chief causes of failure of primary operation in 85 cases coming to reexploration as (1) inadequate resection of the medial intermuscular septum through an inadequate incision, (2) fibrosis induced by haematoma leading to tethering and constriction of the nerve and (3) damage to the medial cutaneous nerve of forearm (Fig. 7.62). We are sure that there is no place for intramuscular transposition and, increasingly, whether there is a case for deep muscular transposition. We have seen constriction, adhesion and distortion of the nerve in the sub muscular bed, just as we have seen them in the intramuscular bed. However, Lowe and MacKinnon (2004) provide a great deal of evidence to support their preference for submuscular transposition and clinicians considering this method should read their chapter before embarking on operations. The oblique course of the terminal part of the posterior branch of the MCNF is particularly well illustrated. Dellon and Coert (2004) provide a well illustrated account of the operation.

7.8.9 The Less Common Entrapment Syndromes – Upper Limb It is with some of the less common “entrapment neuropathies” that we see real difficulties in diagnosis. Nagano (1987) casts a shadow over the concept of entrapment of the anterior interosseous nerve by revealing, at electromyography, denervation in muscles beyond the territory of that nerve. The shadow is deepened by Seki and his colleagues

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Fig. 7.63  Pelvic chondrosarcoma in a 17 year old girl who was initially treated for “neuralgia paraesthetica”.

7.8.11 Meralgia Paraesthetica

Fig. 7.62  Complications of anterior transposition of the ulnar nerve at the elbow. Above: A 43 year old man experienced worsening of pain after sub muscular transposition of the ulnar nerve. The nerve was found rigidly immobilised and constricted by dense fibrous tissue (white sling). A branch of MCF had been cut (red sling). After external neurolysis the nerve was placed subcutaneously in an unscarred bed. Below: A 28 year old man experienced worsening of pain and of symptoms after partial excision of medial epicondyle. The nerve was transposed into an intra muscular position at a second operation. His pain worsened. At third operation, the nerve was found tethered, immobilised, and angulated in scar tissue. The epineurial vessels were obliterated.

(2006) who describe fifteen cases of neuralgic amyotrophy presenting with affection of the anterior interosseous nerve. Nagano and colleagues (1996) describe another cause for anterior interosseous nerve palsy by demonstrating “hour glass like” constriction of the median nerve. Similar lesions have been seen affecting the posterior interosseous nerve. We have operated in only a few cases of “entrapment neuropathy” of either of these nerves and doubt that the intervention altered the natural course in any case.

7.8.10 Some Entrapment Neuropathies in the Lower Limb The difficulties facing the clinician in establishing the diagnosis are even greater in the lower than they are in the upper limb.

Entrapment of the lateral cutaneous nerve of the thigh at the level of the inguinal ligament has a long and distinguished history. It is in its character as a symptom of underlying disease that this “entrapment” is particularly important. Krikler and Grimer (1993) record the case of a pelvic chondrosarcoma presenting with “meralgia paraesthetica”, and indeed that was the mode of presentation to us in 1960 of a young girl with that affliction (Fig. 7.63). Dawson and colleagues (1990) rightly remark that “differential diagnosis consists of an anatomic exercise to establish whether the lateral femoral cutaneous nerve is the only structure affected”. The possibilities that must be excluded are (1) a general neuropathy; (2) a local manifestation of some other generalised condition; (3) a more proximal lesion of the second and third lumbar nerves; (4) a local condition affecting the lumbar plexus or the lateral cutaneous nerve within the abdomen. Perhaps in no other entrapment syndrome are there so many possibilities of missing an important and potentially serious underlying condition. We see this syndrome in its true form increasingly seldom. Our preference is for simple decompression, having sought unavailingly to relieve intractable pain in eighteen patients sent to us after section of the nerve.

7.8.12 Entrapment of the Pudendal Nerve Amarenco and colleagues (1988) first described the syndrome of entrapment of the pudendal nerve in “Alcock’s canal” or “perineal paralysis of the cyclist”. They described five cases, the first, bilateral, in a man of 38 who had

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travelled “several hundred kilometres” on a cycle with a new saddle. Robert and colleagues (1989) made clinical, neurophysiological and anatomical studies and reported on the results of nine operations aided by the microscope. The pudendal nerve, arising from the second, third and fourth sacral nerves, leaves the pelvis through the great sciatic foramen and soon re-enters it through the lesser. In its course on the medial side of the ischium it may be trapped between the ischial spine or the sacro-spinous ligament and the sacro-tuberous ligament. Later the nerve or its branches may be trapped by the falciform edge of the ligament. Its vulnerability to external pressure during cycling is obvious; less so is a mechanism determining entrapment in the absence of such external pressure. Eight of Robert and colleagues’ (1989) patients were women; only one was a cyclist. Carlstedt (2008) has provided us with details of 20 cases of entrapment of the pudendal nerve successfully treated by operation. These patients were investigated by electromyography in conjunction with Dr Andrew Baranowksi (National Hospital for Nervous Diseases, Queen Square). Pudendal blocks were used which were followed by lasting relief in a few cases. Recurrence of symptoms after a successful block is a pre-requisite before advising operation. In most patients symptoms were caused by blunt injury, a fracture of the pelvis, or pelvic surgery. The patient is placed prone and the nerve is approached by splitting the gluteus maximus and identifying the inferior gluteal pedicle where it emerges below the piriformis muscle. The sacro-tuberous ligament is divided and the pudendal nerve is found by swab dissection through areolar tissue where it traverses the sacrospinous ligament. The ligament is now divided. Carlstedt has observed that the nerve seems to be stretched over the ligament and that it may be tethered by scar although no case of direct damage to the nerve has been encountered. The results have been gratifying. One patient who had endured severe pain for more than 12 years after operation for prolapse of the uterus, reported complete and lasting relief of her pain which had disappeared by 24 h after operation.

7.8.13 The Piriformis Syndrome The sciatic nerve, with the inferior gluteal and pudendal nerves and the inferior gluteal vessels, leaves the pelvis through the lower part of the greater sciatic foramen deep to the piriformis muscle running from the inner face of the bony pelvis to the great trochanter. The nerve passes over the tendon of the obturator internus muscle with the gemelli. There is an obvious liability to entrapment with hypertrophy or excess activity of the piriformis muscle. Stewart (2000) defines criteria for the diagnosis of this rather nebulous syndrome: the symptoms and signs arise from a focal lesion of

Surgical Disorders of the Peripheral Nerves

sciatic nerve; neurophysiological investigations confirm a focal lesion; a mass lesion is excluded by magnetic resonance imaging or ultrasound scanning; appropriate findings at operation, and relief of symptoms by that operation. Benson and Schutzer (1999) described 14 patients, in whom symptoms were provoked by direct blunt blow to the buttock. The piriformis muscle was found thickened or fibrosed in all cases. The symptoms were abolished in 11 patients who were all able to return to work. From Bendszus and colleagues (2003) comes a well illustrated report of three patients with refractory sciatica in whom high resolution MRI revealed compression of the sciatic nerve in the buttock by varicose gluteal veins. Severe pain in the leg and buttock was provoked by sitting or lying on the affected leg and rapidly relieved by standing and walking. The pain was abolished by decompression in two patients, in the third, pain subsided with carbamazepime. In our single case, a young man came with pain, paraesthesiae and motor weakness. There was supporting electrophysiological evidence of a focal lesion of the sciatic nerve. At operation, there was entrapment at the level of the crossing of the sciatic nerve by the piriformis muscle, division of which was followed by complete and lasting relief. We have seen eleven patients in whom pain was not relieved, or was even worsened by operation.

7.8.14 The Tarsal Tunnel Syndrome It was probably Lam (1967) who introduced the concept of entrapment of the tibial nerve beneath the medial retinaculum at the ankle. We should state that we have no real experience of dealing primarily with the syndrome; only that of dealing with the ill effects of operation upon the basis of that diagnosis. Katirji and Wilbourn (2005) say: “nonetheless, this is probably the most over diagnosed of the various nerve lesions of the lower limb. Thus, most patients referred to our EDX laboratories with this diagnosis are shown to have problems other than distal tibial neuropathies……. On a yearly basis, we evaluate more patients for failed TTS surgery than we do for failed carpal tunnel syndrome surgery, although the latter operation is far more common”. On the other hand, Dellon (2004) provides extensive evidence showing that the operation, when carefully performed, for the correct indications, is valuable in the treatment of diabetic neuropathy by relieving pain, restoring sensation and preventing ulceration and amputation. MacKinnon and Dellon (1988) described the indications for operation and offer a detailed illustrated account of the procedure. We reserve our position in this matter. Plantar pain, paraesthesiae and numbness may indeed be caused by compression of the tibial nerve under the retinaculum, but the possibility of

Operating on Peripheral Nerves

a more proximal cause must be excluded, and the diagnosis should be supported by the results of electrophysiological examination. When operation is done, the possibility that there may be a tumour or ganglion near the nerve or a tumour in it must be borne in mind. In one of our cases the cause of “tarsal tunnel syndrome” was a synovioma occupying the medial plantar nerve at the level of the malleolus. In that case the pain and the numbness of the great toe had led to a primary diagnosis of multiple sclerosis. A schwannoma, neurofibroma, ganglion, aneurysm of tibial artery has been revealed at exploration. Our experience of dealing with the failures of operation for tarsal tunnel syndrome is very discouraging. Five of the most severe pain states we have ever seen followed such procedures. Errors at the first operation included four lacerations of tibial nerve, five wounds of the calcaneal nerves and three arterial injuries.

7.8.15 “Morton’s Metatarsalgia” Perhaps some clinicians do not always remember that to section a nerve must be followed unavoidably and inevitably by formation of a neuroma. We have seen 14 patients who were much worse off after excision of Morton’s “neuroma” in the sole of the foot. Claustre and Simon (1978) indicate a course less drastic than neurectomy: they follow Gauthier and Dutertre (1975) in practising simple division of the metatarsal ligament through a dorsal incision

7.9 Pitfalls in Operating on Tumours of Peripheral Nerves “The trouble about these tumours is that they are just common enough to come within the experience of almost all surgeons and rare enough to cause embarrassment in diagnosis and treatment.” (Seddon 1975c) Some common difficulties in the treatment of two benign tumours, the schwannoma and the neurofibroma, and one tumour like condition, the ganglion, and also the malignant tumour of nerve are now described.

7.9.1 The Solitary Benign Schwannoma (Neurolemmoma, Neurinoma) Schwannomas arise from Schwann cells anywhere in the peripheral nervous system including the third to the twelfth cranial nerves close to their origin from the brain stem. Bilateral vestibular (eighth nerve) schwannomas are pathognomonic of neurofibromatosis Type II, schwannomas are

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common in neurofibromatosis Type I. Most, be they sporadic or an expression of neurofibromatosis Type II, show deletion of the neurofibromatosis Type II gene on chromosome 22 (Giannini 2005; Meltzer 2001; Fletcher 2001). The schwannoma is enveloped by a true capsule which consists of the perineurium of the nerve bundle of origin, surrounded by a condensation of the deepest layers of the epineurium. This allows excision of the tumour without damage to the parent nerve although the rare plexiform variant of the schwannoma may infiltrate between nerve bundles. Knight and her colleagues (2007) studied 234 schwannomas and they found that distribution between the sexes was equal. Eighty per cent of patients were aged between 30 and 69 years whilst the mean age of the patients was 45.2 years. The site of origin is set out in Table 7.1. Four patients presented with tetraparesis due to an intraspinal extension. Deep seated tumours in the posterior mediastinum and the lumbo sacral spinal nerves and plexus can grow to an impressive size. The average delay before diagnosis was 5.2 years in the 13 large schwannomas reported by Abernathy and his colleagues (1986). Nawabi and Sinisi (2007) described 25 patients with schwannoma of the tibial nerve treated in the Peripheral Nerve Injury Unit. Only three were diagnosed within a year of presentation. The median interval to diagnosis was 48 months. The delay before diagnosis was, in one case, 30 years! Eleven patients had been referred to a Pain Table 7.1  Solitary benign schwannomas: 340 cases 1975–2007. Upper limb Cranial nerves and sympathetic chain

5

Supraclavicular brachial plexus

96

Infraclavicular brachial plexus

21

Circumflex nerve

1

Musculocutaneous nerve

2

Median nerve

32

Ulnar nerve

45

Radial nerve

20

Cutaneous nerve

13

Muscle or bone

3

Total

238

Pelvis and lower limb Lumbar spinal nerves

3

Lumbosacral plexus

7

Femoral nerve

8

Sciatic nerve

18

Tibial nerve

36

Common peroneal nerve

18

Cutaneous nerves

6

Muscle or bone

6

Total

102

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Clinic. Four had operations to decompress the tarsal tunnel, and two more went through lumbar discectomy. All patients complained of pain, which was usually felt in the sole of the foot and a Tinel like sign was detected in all patients. The clinical diagnosis was confirmed by magnetic resonance or ultrasound scanning. The most frequent presentation of schwannoma is a swelling, which is painful to pressure. Progressive neurological deficit occurs only when the tumour arises in a confined space, as in intradural, extramedullary extension, or when it is deep to the clavicle. Diagnosis in the limbs is straightforward. The lump is mobile from side to side but not in the vertical axis of the limb. Percussion induces painful paraesthesiae in the territory of the nerve of origin, similar to the Tinel sign. This finding is the single most useful sign in the diagnosis of schwannoma. At times the tumour causes severe pain, particularly when it arises in the sole of the foot or in the buttock and is exposed to pressure on walking or sitting (Table 7.2). The tumour, when exposed, forms an eccentric oval swelling, usually less than 5 cm in diameter with nerve bundles stretched over it. It may be multinodular or plexiform, infiltrating the nerve of origin, so that enucleation is impossible. Larger tumours within the body cavities, the buttock or the axilla, develop cysts and show degenerative changes of haemorrhage, calcification and hyalinisation. The appearance of the epineurial vessels coursing over the capsule of the tumour is quite characteristic; they are engorged and tortuous. The cut surface is yellowish, and in larger tumours, is cystic and may be blood stained. Rarely the tumour is semi fluid, of the consistency of toothpaste, and appears to infiltrate between nerve bundles. The diagnostic histological feature is the organisation of Schwann cells either into areas of compact bundles (Antoni-A tissue) or a less orderly arrangement of spindle or oval cells in a loose matrix (Antoni-B tissue). There may be an abrupt change from one to the other. Pallisading or compact parallel rows of cells forming Verocay bodies are features of Antoni-A tissue (Weiss and Goldblum 2001a). In larger tumours nuclei may appear hypochromatic, large, and multi lobed (Ancient schwannoma) and the diagnosis of malignancy may be made on the basis of these findings, as it may also be for those schwannomas formed exclusively from Antoni-A tissue (the Table  7.2  Benign solitary schwannoma: symptoms and signs in 198 primary referrals 1984–2004. Symptoms and signs Number of patients (%) Painful swelling

194 (98)

Tinel-like sign

155 (81)

Spontaneous pain

60 (31)

Alteration in cutaneous sensibility

53 (27.7)

Weakness

19 (10)

Rapid increase in size Drawn from Knight et al. 2007.

25 (13)

“cellular” variety). Schwannomas, particular cellular areas, strongly express the S-100 protein, and this is particularly useful in distinguishing the large retroperitoneal tumours from such soft tissue sarcomas as leiomyosarcoma (Folpe and Gowan 2001). Electronmicroscopy shows Schwann cells forming stacks and layers of long cytoplasmic extensions surrounded by basement membranes. Nerve fibres are sometimes seen in looser Antoni-B tissue (Fig. 7.64).

7.9.1.1 Treatment The incision must be adequate so that the nerves and vessels are properly displayed above and below the tumour. With the help of the loupe or microscope, the surgeon should make a longitudinal incision in the epineurium over the most prominent part of the tumour. In nearly all cases it will possible to develop a plane of cleavage between the tumour and the nerve bundles and remove the tumour whole, without disturbing conducting tissue. Sometimes a small bundle may have to be divided to permit removal. Bleeding is checked with bi-polar diathermy in all parts of the wound. Earlier biopsy increases difficulties by causing scar formation in the plane between the tumour and the nerve bundles (Fig. 7.65). Access is a particular problem for those tumours in the upper most part of the spinal canal, those lying ventral to the denticulate ligament and for those with large intra spinal extensions. In these, it may be safer to remove the intraspinal extension at the first operation before returning to excise the extraspinal component at a second operation (Fig.  7.66). Crockard and Bradford (1985) developed the transoral, transclival route to remove a schwannoma lying anterior to the cranio-vertebral junction. Their patient, who presented with a severe tetraparesis, made a full recovery. The transclavicular approach is particularly valuable in the treatment of tumours involving the lower roots of the brachial plexus with extension adjacent to it or within the canal (Fig.  7.67). Abernathy et al. (1986) approached giant sacral schwannomas either by an anterior abdominal exposure or by a posterior retrorectal transacral route. They attempted to preserve the first three sacral nerves and the pudendal nerves, and found that unilateral section of the third sacral nerve could be performed without incurring severe significant neurological deficit. The risk of inflicting damage on the nerve during a well executed operation, is low but it is wise to warn patients about these risks and about the steps that can be taken to diminish those risks and about what can be done in the event. A measurable defect in function was found in five of our cases after operation. In two of these, haematoma from epineurial vessels compressed the nerve. There was partial recovery after urgent decompression. In three more cases of tumours arising at the wrist or in the hand, removal of the bundle entering the tumour led to some loss of sensation or

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Fig. 7.64  Histopathological features in benign schwannoma. Above left: Antoni-A and B tissue, palisading and Verocay bodies. Haematoxylin and eosin × 250. Above right: ancient changes. There is hyalinisation of the walls of the small blood vessels, haemorrhage, haemosiderin pigment and cystic change. Haematoxylin and eosin × 250. Below left:

S-100 positive staining of Schwann cells within a plexiform schwannoma. The myelinated nerve fibres were demonstrated by solochrome cyanin × 160. Below right: elctronmicrograph showing long interleaving Schwann cell processes × 2250 (Courtesy of Dr Jean Pringle).

of power. Sawada and his colleagues (2006) found that the risk of increasing neurological deficit by operation was greater in cases where there was already sensorimotor disturbance. There is a measurable risk of recurrence: Knight et al. (2007) found four cases out of a total of 234. In two of these the tumour was poorly encapsulated and “infiltrative”; excision was incomplete at first operation in two cases of intraextraspinal tumour. Malignant transformation is rare. Woodruff and his colleagues (1994) describe two cases, and reviewed seven “acceptable” reported examples.

exploration, but the risks to conducting tissue attaching to removal must be exposed to the patient. Spinner and his colleagues (2003) have clarified this rather mysterious disorder in a very helpful manner. A study of peroneal intraneural ganglia demonstrated the importance of the articular branch of the nerve showing that this is the pathway for synovial fluid passing from the proximal tibio-fibular joint into the trunk of the nerve. The “pedicle” is, in fact, the articular nerve. A characteristic cystic transverse limb of the articular branch has been defined as a pathognomonic sign for peroneal intraneural ganglia (Spinner et al. 2006a). Spinner and his colleagues extend this concept to ganglia at other sites including the shoulder (Spinner et al. 2006b) and the tibial nerve at the ankle (Spinner et al. 2007) (Fig. 3.37). Exploration will soon reveal the extent of the attachment of the ganglion to the nerve. If it is early clear that (1) the swelling is a ganglion and (2) the ganglion is intimately associated with the nerve, it is important to identify the pedicle (Parkes 1961) which is so dilated that the sheath is translucent, and follow this to the proximal tibio-fibular joint. The

7.9.2 The Intraneural Ganglion This is often the source of needless maiming. The diagnosis of ganglion of the common peroneal nerve must be borne in mind when a patient comes with a pain in the leg, a swelling in the region of the nerve and possibly weakness of the anterior tibial muscles. There is no alternative to the recommendation of

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Fig. 7.65  Schwannoma of the upper trunk of the left brachial plexus. Top left: The swelling was mobile, tender, and percussion evoked painful “pins and needles” sensation into the forearm and thumb. Right: The

tumour exposed at operation. Note the central position, with uniform expansion of the nerve. Bottom left: The tumour during enucleation. There was no neurological deficit after operation.

pedicle is divided between transfixion sutures as close as possible to the joint which invariably leaves a defect in the joint capsule. The pedicle is excised and the main nerve decompressed by incision and expression of contents. Failure to identify and remove the pedicle will lead to recurrence. In such cases we have interposed flaps of fascia and fat between the joint and the main nerve.

and fibrous. The dilated and tortuous epineurial vessels so characteristic of the schwannoma are absent. Neurofibromas do not possess a true capsule and staining for S-100 protein is less intense and less uniform than in the Schwannoma. Light microscopy shows interlacing bundles of elongated cells with wavy dark staining nuclei interspersed with strands of collagen (Weiss and Goldblum 2001a) (Fig. 7.68). There are three chief reasons why neurofibromas are clinically significant. First, they may grow to a very large size causing pressure on adjacent structures; they may also extend along a spinal nerve into the spinal canal. The largest benign solitary neurofibroma that we have removed measured 22 × 8 × 7 cm. Next, the neurofibroma of a trunk nerve is not separable from nerve bundles, which become intimately involved within it. Enucleation is not possible. Finally there is a slight

7.9.3 The Solitary Neurofibroma The solitary neurofibroma arising in a major nerve trunk is easily recognisable. The tumours appear uniformly greywhite and translucent, and in consistency they are rubbery

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291

Fig. 7.66  Dumb-bell tumour (schwannoma) in the cervical region. Upper left: Plain radiograph shows an erosion of pedicles and enlargement of the foramina. Upper right: Digital subtraction angiography shows distortion of the vertebral artery. Below: Magnetic resonance imaging shows the extent of the tumour at levels C2/3 and C3/4. The tumour was approached first by laminectomy of C4 toC6, allowing the intradural extramedullary component to be excised (Mr R Bradford, Royal Free Hospital). Six weeks later the remainder was excised by antero-lateral approach, and the spine stabilised with bone graft and plate.

but definite risk of malignant transformation which has been estimated at around 1% (Weiss and Goldblum 2001a). We have found that the large peripheral neurofibromas arose from slender nerves adjacent to the brachial plexus or major nerve trunks and their removal was relatively straightforward causing little loss of function. In four of the dumbbell tumours conduction in the spinal nerve had been lost before operation, so that removal did not add to neural deficit. In other tumours

arising within the cervical spinal nerves, the greater part of the tumour was removed, preserving displaced nerve bundles. Painful recurrence indicates malignant transformation. Case report: A 34 year old man presented with a palpable lump in the posterior triangle which had been present for at least 12 months. It had increased in size and was causing pain. There was no clinical evidence of neurofibromatosis nor any suggestive family history. The tumour appeared to

292

Fig.  7.67  Massive schwannoma in the mediastinum compressed the brachio-cephalic veins. It was successfully removed by the transclavicular exposure.

Fig. 7.68  Solitary benign neurofibroma. Above left: the matrix is fibrillary and there are comma shaped nuclei. Haematoxylin and eosin × 250. Above right: S-100 positive staining. Below left: a “cellular” neurofi-

Surgical Disorders of the Peripheral Nerves

arise from the first rib with no extension into the spinal canal. At operation the tumour (10 × 8 × 8 cms in dimension) arose from the first rib, distorting and stretching the whole of the plexus and accessory nerve and the subclavian artery, indenting the pleura but not involving it, and merging into the scalene muscle. The tumour and rib were removed, with affected soft tissues. The pathological diagnosis was benign neurofibroma with foci of myxoid degeneration. There was no evidence of malignancy, no hypercellularity and very scanty mitoses, but there was however extension into the medullary cavity of the first rib. Eight years later, a routine radiograph of chest showed two nodules in the upper and lower lobe of the left lung. Upper lobectomy was done; histological appearances were identical with those of the first tumour. Four years later, the patient represented with a further mass in the left posterior triangle of the neck with increasing pain and weakness in the left upper limbs. MRI showed massive recurrence. The tumour was incompletely removed and in this specimen there was pleomorphism, small areas of multi-nucleated tumour cells but the mitotic rate remained low at less than 1 per 10 high powered fields. A course of radiotherapy was completed. A further partial excision of tumour from the left chest wall was performed 2 years later: histological

broma. There is some pleomorphism. Haematoxylin and eosin × 250. Below right: these cells stained positively for S-100 (Courtesy of Dr Jean Pringle).

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Fig. 7.69  Large solitary neurofibroma. Malignant change. The final recurrence 14 years later. Left: MR scan. Right: fibroblast like cells predominated. × 5600 (Electronmicrographs prepared by Mr Stephen Gshmeissner).

appearances now were frankly malignant, with loosely arranged spindle and round or oval cells, nucleur pleomorphism and a mitotic index of 1 per 10 hpf. Sixteen years after the original presentation, extensive metastases in abdomen and chest were evident. Chemotherapy was given (Fig. 7.69). The clinical behaviour of this tumour, invading the first rib and scalenus anterior, suggests that it was malignant from the outset. The slow but inexorable progression in this case is reminiscent of the behaviour of some other soft tissue sarcomas and reminds us that neurofibromas are always potentially malignant. We have operated on seven similar cases. These were massive tumours extending the length of between three and six vertebrae. The transclavicular approach, sometimes supplemented by removal of the first rib, provided adequate access in all. The neurological deficit after excision was trivial in five cases; it was significant in two. One patient suffered paralysis of gleno-humeral muscles and the second had paralysis of long flexor muscles and small muscles of the hand.

7.9.4 Malignant Peripheral Nerve Sheath Tumours (MPNST) MPNST are amongst the most terrible of soft tissue tumours. Increased understanding of their origin and improved methods of diagnosis have not altered their prognosis. These patients have but one chance and that chance is lost by delay in diagnosis, by inappropriate or inadequate biopsy or by inadequate excision. Attempts to preserve function by restricting the resection or by repairing the excised nerve are futile and dangerous. Most of these tumours arise from cells within the endoneurium, and in particular, from Schwann cells. The Schwann cells are formed from a neural crest, not from the mesoderm, and it may be unwise to follow,

uncritically, the principles of treatment developed for soft tissue sarcomas. The perineurium is the true compartment of most MPNST’s and when the tumour has burst out of the epineurium, extending into muscle or bone, or axial blood vessels, then attempts at “limb sparing” operations are usually futile. In one of our cases tumour was detected within the perineurium 20 cm proximal to the main mass in frozen section biopsies. There are three groups. The most dangerous are those arising in patients with neurofibromatosis, and these account for about one third of the total. The risk of a malignant or a central nervous system tumour developing in patients with NF1 has been measured in extensive population studies by Huson and her colleagues (1989a, b) and by Sorensen et al. (1986). It lies between 3% and 5%. Dall (2007) investigated 123 cases of MPNST treated, between the years 1979 and 2002, at the Royal Orthopaedic Hospital, Birmingham, and the Peripheral Nerve Injury Unit at the Royal National Orthopaedic Hospital. Thirty three patients (27%) had NF1. The median age of the patients with NF1 was 26 years compared with 53 years for the sporadic MPNST. The 5 year survival rate for the NF1 patients was 32% compared with 60% in the cases of sporadic MPNST. Tumours in NF1 tend to be more centrally located, and are usually larger. It is often very difficult to detect a malignant tumour arising within a plexiform neurofibroma at an early stage. Pain, sudden enlargement and interference with conduction are common in plexiform neurofibromas. These difficulties have been eased by the work of Rosalie Ferner and her colleagues working at Guy’s, King’s and St Thomas’ Hospitals. (Ferner et al. 2000) Fluorodeoxyglucose positron emission tomography (FDG PET) was used to detect malignant tumours arising within 23 plexiform neurofibromas in 18 patients. Seven malignant peripheral nerve sheath tumours were diagnosed in five patients. The next identifiable group are those tumours arising years after irradiation. (Sordillo and colleagues 1981,

294

Ducatman et al. 1986). We have indentified five such cases. In the case of a 63 year old man who presented with massive swelling deep to and below the clavicle full mantle radiotherapy had been used for Hodgkin’s disease 15 year previously. When we saw him the history and physical signs admitted only one possible diagnosis, that of MPNST. Two biopsies had already been performed, one by needle and one at open operation, both of these were incorrectly reported as benign. The tumour arose from the medial cord. Frozen sections revealed tumour in the eighth cervical nerve root, 15 cm proximal to the main mass. Forequarter amputation had been considered but had to be abandoned because the chance of cure had already passed because of dissemination of the tumour throughout the field. The third group, the solitary MPNST, are somewhat less dangerous. The peak incidence is in the fourth, fifth and sixth decades and the tumour tends to arise more peripherally. There is no significant differences between the sexes. The head, neck and upper limb are the most common sites, accounting for over 40% of tumours; the lower limb is the site of approximately one third, the remainder are found within the trunk, usually arising from spinal nerves and in close relation of the spinal column (Weiss and Goldblum 2001b).

Surgical Disorders of the Peripheral Nerves

ing the longitudinal spread of tumour within the perineurium and the nerve trunk.

7.9.4.2 Pathology Detailed and beautifully illustrated accounts of the histological characteristics can be found in Weiss and Goldblum (2001b, c). The most common histological appearance is reminiscent of fibrosarcoma with masses of spindle shaped cells organised into sweeping bundles or lamellae. Irregularity of the cells and a characteristic wavy or buckled appearance of the nuclei is often found. Metaplastic differentiation occurs in about 20% of tumours. Bone, cartilage and muscle are the most common tissues seen; epithelioid differentiation into glandular or squamous tissue is less common. Woodruff and colleagues (1973) described three new cases of rhabdomyosarcomatous change, the so called triton tumour, and reviewed the seven previously published cases. They agreed with Masson and Martin (1938) in proposing that muscle is formed from malignant Schwann cells. Nine of their patients were dead within a year of diagnosis (Fig. 7.70).

7.9.4.3 Principles of Operation 7.9.4.1 Clinical Features The cardinal clinical feature of MPNST is pain. This is usually attended by clear evidence of impairment of nerve conduction. A tender and enlarging mass is found in all but the most deeply located tumours. Errors in diagnosis are not uncommon; there are numerous references to unnecessary laminectomy or excision of a cervical rib before a correct diagnosis was made. Nerve conduction studies are not useful. CT and MRI scan are always valuable in showing the extent of tumour and in distinguishing between benign and malignant. Myelography has a place in defining intraspinal extension and is extremely good for this when combined with CT scan. Moser and Parrish (2001) issue an important caveat. In most cases radiological features cannot distinguish reliably between benign and malignant soft tissue tumours. It is imperative that a final interpretation of CT scan or MRI findings is not given until the cross sectional imaging has been correlated with plain radiographs. Failure to adhere to this principle results in serious errors in management, The clinical features and findings at operation are more important in diagnosis of MPNST than are histological characteristics, most of all in the so called low grade malignant neurofibromata. Detection of metastases, notably in the lungs, has obvious implications for the planned treatment. Conventional methods of staging these tumours must be used with discretion because of the risk of underestimat-

“Because the proper treatment for a neurosarcoma should not be less than a radical excision the biopsy should be of the whole specimen and of a considerable length of the nerve trunk on either side of it – provided it is possible to make the diagnosis of malignancy on the clinical evidence and on the appearances displayed at operation”. (Seddon 1975c) Biopsy must never be a matter of unthinking routine and it should be seen as a preliminary step before urgent and definitive excision of the tumour (Fig. 7.71). Wide excision of the trunk nerve is the correct treatment for a tumour which is still confined within the epineurium. Examination of frozen section biopsies, taken during the operation, is essential to establish adequate clearance. It proved necessary to section the spinal nerve at the foramina to secure clearance in seven of our cases and resection of the intraspinal segment of the nerve was required in three more. We think that it is futile to attempt repair of the resected nerves. The object of the operation must be wide resection of the parent nerve with adequate margins of clearance (Bolton et al. 1989). The prospect of restoring useful function in the foot or hand by grafting gaps in excess of 20 cm, in a field which will, in all likelihood, be irradiated, is negligible. We have seen three cases where inadequate resection followed by grafting of the affected nerve led to a fatal outcome. One of these was the case of a 32 year old man, in good general health, who was reviewed 12 months after an operation

Operating on Peripheral Nerves

Fig.  7.70  Histopathological findings in four malignant peripheral nerve sheath tumours. Above left: a proportion of the tumour cells are expressing myoglobin, in particular, larger cells. Triton tumour. × 400 (Courtesy of Dr Kim Suvarna). Above right: another triton tumour.

during which an 8 m segment of the medial cord was resected and grafted. This resection was wholly inadequate. The tumour soon recurred, and enveloped the neurovascular bundle. Forequarter amputation was performed. Tumour extended 14 cm proximal to the upper pole of the tumour and it had infiltrated the nerve graft. Amputation is probably indicated when the epineurium has been breached, and in rapidly growing recurrence. Lusk, Kline and Garcia (1987) recommended forequarter amputation for MPNST arising within the brachial plexus. We agree that this is necessary with recurrence after apparently adequate excision or when there is such involvement of the plexus that no function can be preserved. It may be necessary for palliation even if it cannot cure; the pain caused by malignant infiltration of the brachial plexus is terrible. Fungation of tumour must be prevented (Fig. 7.72). The outcome of treatment in our 56 cases of MPNST is bleak. Of the 15 tumours in known NF1, nine died within 2 years of treatment. One patient died from a second intrapelvic MPNST after successful forequarter amputation. Two more patients have active disease at less than 12 months from operation. Of the 41 patients with sporadic tumours eight

295

There is S-100 positive staining. Mitoses are evident. × 400. Below right: S-100 positive staining showing glandular differentiation × 400. Below left: only a few cells show S-100 positive staining in this tumour × 400 (Courtesy of Dr Jean Pringle).

Fig.  7.71  Open biopsy was performed on a lump in the thigh in an 87 year old woman. She experienced intense pain and rapid progression of neural deficit. The lesion was re-explored 1 month later, the tumour had burst out of the epineurium and infiltrated the muscles of the thigh and extended to the skin. (Courtesy of Marco Sinisi).

died within 2 years and 6 patients are known to have active disease. Twenty one appear free of disease at a minimum of 4 years from operation. Of those “cured” twelve were treated

296

Fig. 7.72  MPNST in a 53 year old man with NF1. Forequarter amputation was performed to relieve his pain. His death was caused by erosion into the carotid vessels. Below: the tumour is densely cellular with moderate pleomorphism and high mitotic index. Haematoxylin and eosin × 400 (Courtesy of Dr Jean Pringle).

by excision of the nerve, six by amputation of the limb and three by forequarter amputation. Surgical ablation was impossible in six cases because of intra-spinal extension. Death was caused by invasion of great vessels, of the spinal canal or viscera in seven cases, and in six more the threat of

Surgical Disorders of the Peripheral Nerves

this remains. Death was caused by pulmonary and visceral metastases in eight cases. Primitive Neurectodermal Tumours: Our experience with these is too small to be worthy of discussion. En bloc excision is impossible in most large primitive neurectodermal tumours (PNET) extra-osseous Ewing’s tumours and in neuroblastomas (Figs. 7.73 and 7.74). Removal of as much of the tumour as is possible may increase the chance of a positive response to chemo and radiotherapy. Edward Kiely has described his approach to the abdominal and pelvic neuroblastomas in an inspiring Hunterian lecture (Kiely 2007). Two hundred and thirty four children were operated, almost 60% of these presented with distant metastatic disease (stage 4). Kiely points out that these tumours do not extend deep to the adventitia of major blood vessels and his technique rests on developing the plane, by meticulous scalpel dissection, between the tumour and the media. Dissection starts below the lower limit of the tumour: “this usually means the common external iliac vein on the right side or the corresponding artery on the left side”. The dissection advances proximally precisely in the mid line of the vessel. The major visceral arteries are treated in a similar fashion, and the tumour and adventitia are incised along the midline of these vessels and along each of their branches as far as necessary. The lumbo sacral trunk and the obturator nerve are identified and are separated from the tumour without great difficulty. At least one hypogastric nerve is preserved wherever possible. Clearance of the coeliac and superior mesenteric arteries inevitably removes the sympathetic nerve supply to the gut and post operative diarrhoea is common. There is also sympathetic paralysis in the ipsi lateral lower limb. There were two post operative deaths. Removal of at least 95% of tumour was achieved in 90% of children. Twenty six of the 29 children presenting with tumours in the midline or crossing the midline or with contra lateral involvement of lymph nodes (Stage 3) were alive 5 years after operation. The 5 year survival for children presenting with Stage 4 disease was 30% (Fig. 7.75).

Operating on Peripheral Nerves

Fig.  7.73  Neuroepithelioma. Left: the tumour arose from the sciatic nerve in a 14 year old boy with NF1. The significance of his intense pain and the swelling in the upper thigh was not grasped for several months. Above right: another example of tumour arising from the sci-

297

atic nerve in a 19 year old man. Middle: there are areas of rosette formation. Haematoxylin and eosin × 400 (Courtesy of Dr Jean Pringle) Below right: intense mitotic activity. Electronmicrograph × 8075 (Prepared by Mr Stephen Gshmeissner).

298

Surgical Disorders of the Peripheral Nerves

Fig. 7.74  Extra osseous Ewing’s tumour arising from the sympathetic chain. Left: the extent of the tumour is demonstrated by MRI. Right: the tumour consists of undifferentiated cells, many of these containing glycogen × 7000 (Prepared by Mr Stephen Gshmeissner).

Fig. 7.75  A massive neuroblastoma extending from C5 to T4 enveloped the subclavian vessels and the brachial plexus in a 14 year old girl,. About 90% of the tumour was excised through an extended transclavicular approach. The operation was done with Mr R Spicer

(Children’s Hospital, Bristol). Above: the approach to the tumour after elevation of the flap. The subclavian artery was freed from one of the lobes of the tumour. Below: Although the first thoracic nerve was excised little defect was evident 20 months later.

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Operating on Peripheral Nerves for C5–C6 avulsion of the brachial plexus: anatomical study and report of four cases. J Hand Surg 19A:232–237 Ochiai N, Nagano A, Mikam V, Yamamoto S (1997) Full exposure of the axillary and suprascapular nerves. J Bone Jt Surg 79B: 532–533 Ömeroğlu H, Uçaner A, Tabak AY, Guneg O, Cimŏglua B, Gűnel U (1998) The effect of using a tourniquet on the intensity of postoperative pain in forearm fractures. Internat Orthop 22:369–373 Orgell MG (1987) Epineurial versus perineurial repair of peripheral nerves. In: Tertzis JK (ed) Microreconstruction of nerve injuries. WB Saunders, London, pp 97–100 Osborne GV (1970) Compression neuritis of the ulnar nerve at the elbow. Hand 2:10–13 Owen E. (1975) Microsutures. Presented and used during the Royal Coll. Surg (Eng) Microsurgical Workshop organised byEarl Owen, John Cobbett and Richard Ackland Panegyres PK, Moore N, Gibson R, Rushworth G, Donaghy M (1993) Thoracic outlet syndromes and magnetic resonance imaging. Brain 116:823–841 Parkes AR (1961) Intraneural ganglion of the lateral popliteal nerve. J Bone Jt Surg 43B:784–790 Parry EW, Eastcott HHG (1992) Cervical rib and thoracic outlet syndrome. In: Eastcott HHG (ed) Arterial surgery, 3rd edn. Churchill Livingstone, Edinburgh, pp 333–353 Petrie A (2006) Statistics in orthopaedic papers. J Bone Jt Surg 88B:1121–1136 Poitevin LA (2005a) Thoracic outlet syndrome, scalene complex and Interscalene passages. In: Tubiana R, Alain Gilbert, Taylor & Francis, Abingdon, United Kingdom, ISBN 1-85317-494-7, Chapter 21, pp 321–332 Poitevin LA (2005b) Anatomical bases for brachial plexus and subclavian artery compression. In: Tubiana R, Gilbert A, Taylor & Francis, Abingdon. United Kingdom, ISBN 1-85317-494-7, Chapter 20, pp 313–320 Reissis N, Stirrat A, Manek S, Dunkerton M (1992) The terminal branch of the posterior interosseous nerve: a useful donor for digital nerve J. Hand Surg 17B:638–640 Robert R, Labat JJ, Lehar PA, Le Borgne J, Le Barbin JY (1989) Réflexions cliniques, neurophysiologiques et thérapeutiqies à partir des donnés anatomiques sur le nerf pudendal (honteux interne) lors de certaines algies périnéales. Chirurgie 115:515–520 Rodger NAM (2004) The Command of the Ocean. A naval history of Britain. 1649–1815. First published by Allen Lane 2004. Published in Trade Paperback by Penguin Books 2005 and in this format by Penguin Books in 2006, pp 308–309 Roos DB (1981) Essentials and safeguards of surgery for thoracic outlet syndrome. Angiology 32:187–192 Rosenbaum RB, Ochoa JL (1993) Carpal tunnel syndrome and other disorders of the median nerve. Butterworth Heinemann, Oxford Santos-Pallazzi C (1991) The quality of the stumps in post ganglionic ruptures of the spinal nerves. International Symposium on Brachial Plexus Injuries, Lausanne Sargent P (1921) Lesions of the brachial plexus associated with rudimentary ribs. Brain 44:95–124 Sawada T, Sano M, Ogihara H, Omura T, Mivra K, Nagano A (2006) The relationship between pre-and post operative symptoms, operative findings and post operative complications. J Hand Surg 31B:629–634 Scher LA, Veith FJ, Haimovici H, Samson RH, Ascer E, Gupta SK, Sprayregen S (1984) Staging of arterial complications of cervical rib: guidelines for surgical management. Surgery 95:644–649 Schroeder HP, Scheker LR (2003) Redefining the “Arcade of Struthers”. J Hand Surg 28A:1018–1021 Schwartz DM, Auerbach JD, Dormans JP et al (2007) Neurophysiological detection of impending spinal cord injury during scoliosis surgery. J Bone Jt Surg 89A:2440–2449

301 Seddon HJ (1975a) Common causes of nerve injury. In: Surgical disorders of peripheral nerves, 2nd edn. Churchill Livingstone, Edinburgh, pp 67–88 Seddon HJ (1975b) Operative treatment. In: Surgical disorders of peripheral nerves, 2nd edn. Churchill Livingstone, Edinburgh, pp 250–286 Seddon HJ (1975c) Nerve tumours. In: Surgical disorders of peripheral nerves, 2nd edn. Churchill Livingstone, Edinburgh, pp 154–171 Sedel L (1975) Voies d’abord des nerfes du member inférieur. Med Chir Technol Chirurg Orthop (Paris) 445301:1–8 Seki M, Nakamura H, Kono H (2006) Neurolysis is not required for young patients with a spontaneous palsy of the anterior interosseous nerve. J Bone Jt Surg 88B:1606–1609 Semple JC, Cargill AO (1969) Carpal tunnel syndrome. Results of surgical decompression. Lancet i:918–919 Smith PF (2006) Louis Stromeyer (1804–76) German orthopaedic and military surgeon and his links with Britain. J Med Bibliography 14:65–74 Sood SK, Balasubramani AN, Harrison BJ (2007) Percutaneous biopsy of adrenal and extra-adrenal retroperitoneal lesions: beware of catecholamine secreting tumours. Surgeon 5:279–281 Sorensen SA, Mulvihill JJ, Neilson A (1986) Nation wide follow up of Recklinghausen neurofibromatosis survival and malignant neoplasms. New Eng J Med 314:1010–1015 Sordillo PP, Helson L, Hajdu SL et al (1981) Malignant schwannoma – clinical characteristics, survival and response to therapy. Cancer 47:2503–2509 Spinner M, Spencer PS (1974) Nerve compression lesions of the upper extremity. Clin Orthop Relat Res 104:46–67 Spinner RJ (2008) Operative care and technique. In: Kim DH, Midha R, Murovic JA, Spinner RJ (eds) Kline and Hudson’s nerve injuries, 2nd edn. Saunders, Elsevier, Philadelphia, PA, Chapter 6, pp 87–106 Spinner RJ, Amrami KK, Kliot M, Johnston SP, Casanas J (2006a) Suprascapular intraneural ganglia and glenohumeral joint attachments. J Neurosurg 104:551–557 Spinner RJ, Atkinson JLD, Teil RL, Birch R et al (2003) Peroneal intraneural ganglia: the importance of the articular branch. A unifying theory. J Neurosurg 99:330–343 Spinner RJ, Dellon AL, Rosson GD, Anderson SR, Amrami KK (2007) Tibial intraneural ganglia in the tarsal tunnel: is there a joint connection? J. Foot Ankle Surg 46:27–31 Spinner RJ, Desy NM, Amrami K (2006b) Cystic transverse limb of the articular branch: a pathognomonic sign for peroneal intraneural ganglia at the superior tibio fibular joint. Neurosurgery 59:157–166 Spinner RJ, Goldner RD (1998) Snapping of the medial head of triceps and recurrent dislocation of the ulnar nerve J. Bone Jt Surg 80A:239–247 Stewart JD (2000) Focal peripheral neuropathies, 3rd edn. Lippincott Williams & Wilkins, Philadelphia, PA. ISBN 0-7817-1717-5 Strange FG, St C (1947) An operation for pedicle nerve grafting. Brit J Surg 34:423–425 Symonds CP (1927) Cervical rib: thrombosis of subclavian artery, contralateral hemiplegia of sudden onset, probably embolic. Proc R Soc Med 20:1244–1245 Taleisnik J (1973) The palmar cutaneous branch of the median nerve and the approach to the carpal tunnel. J Bone Jt Surg 55A:1212–1217 Tarlov IM (1944) Autologous plasma clot suture of nerves. JAMA 126:741–748 Vandeput J, Tanner JC, Huypens L (1969) Electrophysiological orientation of the cut ends in primary peripheral nerve repair. Plast Reconstr Surg 44:378–383 Wadsworth TG (1977) The external compression syndrome of the ulnar nerve at the cubital tunnel. Clin Orth Rel Res 124:189–204 Wadsworth TG (1984) Variations of the motor recurrent branch of the median nerve. In: Birch R (ed) DM Brooks operative surgery. The hand. Butterworth, London, p 481

302 Weiss SW, Goldblum JR (2001a) Benign tumours of peripheral nerves. In: Weiss SW, Goldblum JR (ed) Enzinger and Weiss’s soft tissue tumours, 4th edn. Mosby. St Louis, Chapter 30, pp 1111–1208 Weiss SW, Goldblum JR (2001b) Malignant tumours of the peripheral nerves. In: Weiss SW, Goldblum JR (eds) Enzinger and Weiss’s soft tissue tumours, 4th edn. Mosby, St Louis, Chapter 3, pp 1209–1264 Weiss SW, Goldblum JR (2001) Primitive neurectodermal tumours and related lesions. In: Weiss SW, Goldblum JR (eds) Enzinger and Weiss’s soft tissue tumours, 4th edn. Mosby, St Louis, Chapter 32, pp 1265–1322 Wickham JEA, Martin P (1962) Aneurysm of the subclavian artery in association with cervical abnormality. Br J Surg 50:205–209

Surgical Disorders of the Peripheral Nerves Wilbourn A (1993) Thoracic outlet syndromes. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 3rd edn. Elsevier, Philadelphia, PA, pp 936–942 Woodruff JM, Chernik NL, Smith MC, Millett JB, Foote WF (1973) Peripheral nerve tumours with rhabdomyosarcomatous differentiation. (Malignant “triton” tumours). Cancer 32:426–439 Woodruff JM, Selig AM, Crowlely K, Allen PW (1994) Schwannoma with malignant transformation: a rare distinctive peripheral nerve tumour. Am J Surg Pathol 18:882–895 Young JZ, Medawar PB (1940) Fibrin suture of peripheral nerves. Lancet 2:126

8

Compound Nerve Injury

We define compound nerve injuries as those in which damage to a nerve or nerves is associated with major damage to other tissues or organs such as skin, muscle, the skeleton, viscera and major vessels at the same site. There are some obvious categories. 1. Penetrating missile injuries 2. Severe open wounds, partial or complete amputation 3. Nerves injured by fracture or dislocation, open or closed, notably at the shoulder, elbow pelvis, hip and the knee. 4. Burns The timing of nerve repair in compound injuries remains controversial. Horn (1959) practised primary suture of median and ulnar nerves at the Accident Hospital in Birmingham, reserving grafting for more severe proximal injuries. From 1956 onwards primary suture of severed nerves was practised at St Mary’s Hospital whenever it was possible. There, in 1965, Michael Laurence achieved an outstanding result from primary repair of all flexor tendons, radial and ulnar arteries and median and ulnar nerves sectioned at the wrist. O’Brien (1975), one of the founders of modern microsurgical work, proved that primary repair of nerves was better even in the most severe injuries, in reattached limbs amputated by crush or traction. We think that the general contra-indications to primary repair include:

stumps need to be removed before repair in the tidy wound. The difficulties in preparing the stumps in traction rupture have been exaggerated. It is a simple matter, on the day of injury, to remove the tips of the stumps until a recognisable architecture of nerve bundles is revealed. This usually coincides with the level at which conduction can be demonstrated unless ischaemic conduction block has occurred following wounding of the axial artery or a compartment syndrome in the distal part of the limb. In the distal segment of the nerve it is a simple matter to move a nerve stimulator centrifugally away from the stump until the appropriate muscular response is seen. The recognition of the level of physiological continuity in the central portion of the nerve involves moving the stimulator centripetally away from the tip of the rupture whilst recording responses through electrodes secured to the skin of the scalp or over the spine. Delay before repair of a divided nerve is damaging particularly when there is associated injury to the adjacent artery. The best result that we have seen following repair of sciatic nerve was achieved by Mr Plaha, orthopaedic surgeon, London, who sutured the transected sciatic nerve in the left thigh, and also the right common peroneal nerve at the knee during an emergency operation (Fig.  8.1) for severe bleeding from multiple stab wounds in both lower limbs.

1. The poor condition of the patient. 2. Inexperience of the surgeon and lack of suitable facilities. 3. Most but not all of penetrating missile injuries. Ouellette (2000) recommends primary repair of nerves ruptured by civilian gunshot wounds in children. Delayed primary repair is the current policy is followed by the surgeons of the Royal Army Medical Corps (RAMC) in war wounds. 4. Most burns some aspects of thermal and cold injury are related in Chapter 3. 5. Cases of severely contaminated wounds from machinery, road accidents or agricultural injuries in which the prevention of sepsis must be the priority. The risk of sepsis is far less in the tidy wound and less still in the closed traction rupture. Little, if any, of the divided nerve

Fig. 8.1  Function 18 months after emergency suture of sciatic nerve in the left thigh and of the common peroneal nerve at the right knee by Mr Plaha (London).

R. Birch, Surgical Disorders of the Peripheral Nerves, DOI: 10.1007/978-1-84882-108-8_8, © Springer-Verlag London Limited 2011

303

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One of the best results that we have seen following repair of a closed rupture of the common peroneal nerve was that achieved by Mr Roussow, orthopaedic surgeon (London) who, on the day of injury, grafted the rupture at the same time as he repaired the lateral ligament complex of the knee. Function was excellent by 22 months by which time the patient considered his function normal. This is a remarkable result, the defect in the nerve was over 15 cm. Our material is drawn from around 3,500 patients passing through the fracture service of St Mary’s Hospital, Paddington between 1965 and 1991 and the Peripheral Nerve Injury Unit at the Royal National Orthopaedic Hospital between 1965 and 2008. Most patients were referred from other hospitals. Our observations do not permit inferences about the incidence of nerves injured by fractures or dislocations nor about the course to spontaneous recovery in non operated cases. Some elements of the findings from the cases seen before 1998 are set out in Tables  8.1 and 8.2. Arterial injury or ‘compartment syndrome’ complicated about one fifth of these. Spontaneous recovery occurred in about one half of the cases of circumflex palsy, in 40% of the radial palsies and in only one third of the lesions to the common peroneal nerve. One hundred and eighty six patients sustained nerve injuries during operations for skeletal injury from a total of 2,330 cases (8.1%). A more detailed record (Chapter 5) was used to collect data from 1,271 patients seen after the year 2000. The most disturbing finding in the later group is the increase

Table  8.1  Operations in compound nerve injuries. St Mary’s Hospital – Royal National Orthopaedic Hospital 1965–1998. Number of patients Arterial injury or compartment syndrome 1,816

322

Open fracture/ dislocation

359

110

Penetrating missile wound

155

51

Closed fracture/ dislocation

Total 2,330 483 186 nerves were injured during operation for skeletal injury.

Table 8.2  Circumflex, radial and common peroneal nerves injured by fracture/dislocation. Operated and non-operated cases (1965–1998). Nerves showing Nerve Number Arterial injury/ good spontaneof nerves “compartment ous recovery syndrome” Circumflex

380

41

198

Radial

738

92

301

Common peroneal

318

98

104

1,436

231

603

Total

in the number of iatrogenous injuries. Three hundred and twenty three patients (25.4%) sustained such injuries. There are three general factors which determine the final outcome of nerve injury and repair and which strongly influence the timing of that repair. They are: the nature of wound and the risk of sepsis; vascular injury, and loss of skin.

8.1 The Wound One of the achievements of Robert Jones was to secure agreement amongst the surgeons on the Allied side on the Western Front in 1917 of a common policy of treatment of missile wounds. The elements of this included debridement, in its true sense of unbridling or decompression, wound excision and delayed closure. Hull and Rob (1997) write: ‘such were the infection rates following amputation and primary closure of the stump in the early months of the First World War that the chief surgeon of the British Expeditionary Force issued an order that forbad primary suture’. Wright (1915) and Fleming (1915) at St Mary’s Hospital, described the evolution of colonisation in war wounds which came from sporebearing clostridia, non spore-bearing gut organisms and pyogenic cocci. Clostridia was detected in 90% of wounds at the first dressing station; pyogenic cocci in 15%. Mellor et al. (1997) remind us that contamination and delay is a characteristic of battle wounds so that the natural history in the untreated cases was putrefaction followed by gas gangrene, or by cellulitis and septicaemia which was later recognised as ‘hospital’ streptococcal infection. Clarke (1959) emphasised that much of the primary contamination of wounds comes from the clothes and the skin of the patient: ‘this became important during World War Two when surgeons transferred their attentions from the Libyan Desert to the cultivated terrain of Italy. In the desert the techniques of wound exploration based on World War One experience appeared no longer necessary and this was unfortunately attributed to the use of sulphonamides. Experience in Italy showed this to be an illusion; full wound exploration and decompression became essential. The difference depended not only on the germ free desert but also on the fact that the wounded men were often wearing not more than a thin pair of shorts. A dangerous feature in Italy was often the germladen clothing in the depths of the wound.’ Clarke emphasised that debridement is to properly extend the wound and he argued against a needless excision: ‘the scalpel cannot and need not excise all micro-organisms’. These important lessons were soon forgotten and it seems that the principles of wound surgery must be relearned during conflict: at times it seems as if some civilian surgeons never grasped them. Cooper and Ryan (1990), in commenting on the trend in civilian practice to minimal surgical

Compound Nerve Injury

intervention and primary closure of wounds with increasing reliance on antibiotics, say ‘it is timely to remind our civilian colleagues that this approach, transferred to the battle field will result in catastrophe for many of the wounded’. No surgeon will overlook the excellent advice from Gustilo and Anderson (1976): ‘if there is the slightest doubt in the surgeon’s mind as to whether there has been adequate debridement of the wound after an open fracture, the wound should not be closed regardless of the type of open fracture. For the surgeon who manages only an occasional open fracture, the safe rule is not to close the wound.’ We have had to treat seven cases of gas gangrene in which fundamental principles had not been followed. For these patients only urgent amputation or radical excision of infected tissues availed. Case Report: An 18 year old man suffered a closed traction lesion of the brachial plexus with rupture of the axillary artery, and closed fractures of humerus and both forearm bones (Fig. 8.2). Circulation was restored through a prosthesis. At his arrival to St Mary’s Hospital, 18 h after this operation, the diagnosis was immediately obvious. He had a heliotrope complexion, a extraordinary sang froid and a racing pulse. Gas was palpable under the skin of the arm. Emergency amputation was performed through the upper humerus; the skin flaps were closed 72 h later. The errors which led to this outcome include: failure to stabilise the skeleton; failure to decompress the limb; and to a lesser extent use of a prosthesis rather than a vein graft. Case Report: A 28 year old man suffered fracture of femur, complicated by a sciatic nerve palsy in a road traffic accident. The fracture was open, and the skin wound which was 3 cm in diameter was sutured before the patient was transferred to us. He arrived with gas in the muscles of the thigh. Excision of all of the flexor muscles of the thigh was necessary. One of us is reminded of the demonstration by Peter London, at the Accident Hospital in Birmingham: on being presented with a thigh after the fracture had been reduced and the skin closed, London immediately manipulated the limb so that the ends of the fracture were forced through the wound. Road tar and a cigarette stub were impaled onto a spike of the femur.

Fig. 8.2  Gas gangrene.

305

8.1.1 War Wounds: Current Practice Eardley et al. (2009) restate the principles of the treatment of war wounds based on their experience in current conflicts. ‘the aims of war wound management are to prevent infection and enable safe and timely closure. All war wounds are considered to be contaminated. The culture medium is eliminated by wound excision, decompression and antibiotics.’ They set out four principles. I. The effects of ballistic injury extend beyond the area of the wound and thorough primary and secondary surveys with careful records are essential. II. The administration of antibiotics, of prophylaxis against tetanus and of agents to stabilise blood coagulation are essential steps during the initial phase of resuscitation. III. Wound surgery is staged. Whilst the objects of the first operation include the removal of contaminated and devitalised tissue this must be undertaken with a view to subsequent procedures particularly in relation to the provision of soft tissue cover. IV. The outlook for recovery within the injured limb is largely determined by the success of the first operation. Eardley and his colleagues identify eight stages which are essential for success. 1. Preparation: a pneumatic tourniquet may be applied before non sterile cleansing. Towels are placed so that there is no hindrance to the exposure of axial vessels or of potential vein graft. This is done rapidly. 2. Lavage is performed using 6–9 L of warmed normal saline at low pressure, not by pulsatile delivery. 3. Excision of skin is confined to that which is clearly dead at the edges of the wound. 4. Extension of the wound by longitudinal incisions, suitably modified across joints reveals the true extent of ballistic injury. 5. Inspection which permits removal of all non viable tissue, requires exposure of all structures in the wound cavity. Damaged muscle is excised back to healthy tissue, recognised by its contractility, consistency, colour and capillary bleeding. Unattached bone fragments of foreign material are removed and the search for small metallic fragments and intact bullets should not be prolonged. On the other hand mud, fragments of clothing and organic material must be removed. Main vessels are repaired. Frayed tendon ends are trimmed smooth. Disrupted nerves are carefully tagged by a fine suture to each other or to adjacent soft tissues. No nerves are repaired at the first operation. 6. Decompression is extensive. In the upper limb this should include opening the carpal tunnel and other compartments within the hand. The risks from swelling within the muscle compartments are increased by ventilation during evacuation.

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Surgical Disorders of the Peripheral Nerves

7. Stabilisation of fractures is performed early. All methods have their advantages and disadvantages; the poor application of any one of them usually leads to a poor result. 8. Dressing, ALL WOUNDS ARE LEFT OPEN. They are lightly packed with fluffed gauze dressing. The injured limbs are elevated. 9. The ‘second look’ operation is performed at 3–5 days later. Dressings are left undisturbed so long as the patient remains apyrexial and does not experience pain or undue swelling of the limb proximal to the wound. Now it may be possible to proceed to delayed primary closure (DPC) depending on the condition of the wound, the patient and the requirement for more elaborate methods of fracture stabilisation and skin cover (Figs. 8.3 and 8.4). Eardley and Stewart (2010) describe the application of these principles in a seminal paper describing the early management of ballistic hand trauma. They emphasise that excision must be precise and limited to dead tissue and also that any viable tissue, such as fragments of bone which have retained their blood supply or flaps of skin which are still innervated must be kept as potential ‘building blocks’ in later reconstruction. Early rehabilitation is central to the concepts developed by Eardley and Stewart and the hand is splinted in the position of function with the wrist extended, the metacarpophalangeal joints lightly flexed and the proximal interphalangeal joints extended before and after the first operation. An important observation is made about the organisation of the operating team: ‘when an estimated 2 h or more of damage control surgery of the abdominal cavity or a lower limb surgery is anticipated, we use a team of three surgeons, one of whom has expertise in the hand and operates solely on the injured hand’. The policy described by Eardley and Stewart is driven by the fact that so many of the wounded have suffered severe injuries or even amputation of the lower limbs so that it is important to restore the highest level of function possible in the upper limbs and hands.

8.2 The Vascular Lesion Advances in arterial and venous surgery, with the introduction of antibiotics, blood transfusions and improvements in anaesthesia are the basis of modern surgical practice particularly in the treatment of severe wounds. It is a source of dismay that trends in training make it less likely that orthopaedic surgeons of the future will be as capable of dealing with the injured artery, or for that matter coping with the problem of skin loss as were those who contributed to these advances. Bonney (1963) and Kirkup (1963) successfully dealt with femoral arterial injury caused by fractures of the femur. We think that the first successful replant of the hand was performed by Mr David Harris, an orthopaedic surgeon, and that

Fig.  8.3  Penetrating missile wounds of leg treated by debridement (above) external fixation (middle) and rotation of a full thickness skin flap to cover the bone (below) (Courtesy of Major K Brown RAMC).

one of us was perhaps the first to successfully replant an amputated thumb in the United Kingdom. We think that Bonney (1963) ‘Surgeons treating fractures of long bones must be prepared to treat associated vascular injury’, London (1967a) ‘there is nothing so difficult about sewing up an artery as to make it the strict preserve of the vascular specialist’, and Birnstingl (1982) ‘the ability to repair blood vessels should now be part of the repertory of every accident surgeon’, are right.

Compound Nerve Injury

307

Fig. 8.4  Blast wound of hand, treated by emergency repair of the ulnar artery, simple stabilisation of the skeleton and delayed closure of the skin. Fig. 8.6  This soldier suffered multiple fragment wounds. He held his face together with one hand and he used the other to compress the left femoral artery which had been transected.

Fig.  8.5  A glass wound to the axilla transected the axillary artery. Spasm of the stumps prevented catastrophic bleeding.

Hunter (1793) noted the effect of transection of major arteries in the limbs of the boar and the dog. The vessels constricted ‘before the animal weakened’ (Figs.  8.5 and 8.6). Hallowell (1761) wrote to John Hunter telling him of repair of a brachial artery by means of a Farriers stitch. Murphy

(1897) was probably the first successfully to repair a severed femoral artery. The foundations of modern surgical technique were laid by Carrel (1902), who was awarded the Nobel prize, and by Guthrie (1912), whose contributions were no less significant. Pringle (1913) used vein grafts to repair two cases of aneurysm. Sherrill (1913) described successful suture of a brachial artery ‘by the method of Carrell employed by Crile’ and there are occasional reports in these years from German surgeons such as Lexer (1913). The First World War saw important work. Makins (1919) advised suture of arteries in selected cases. The Serbian surgeon Subbotitch (1913), described repairs of 135 arterial injuries and of 32 arteriovenous fistulae during the Balkan Wars. The Russian surgeon Weglowski (1925) described 51 vein grafts for arterial repair in the wounded of the Eastern Front. The Second World War inevitably saw advances. The work of the Vascular Injuries Committee of the Medical Research Council, chaired by Sir Thomas Lewis, was summarised in the MRC War Memoranda No. 13 (1944). We

308

think it should be re-issued, slightly modified, to all accident and orthopaedic surgeons: ‘The memorandum is intended for guidance of those who have had only limited previous experience of the early treatment of arterial wounds.’ It described pathological changes and principles of diagnosis, and strongly recommended axial anastomosis for stab wounds of vessels and the use of artificial tubes where tension was too great for end to end suture: ‘In the war of 1914– 1918 Tuffiers cannula usually failed in its purpose, because thrombosis occurred within a few hours; the use of heparin, however should prevent this.’ This technique was designed to maintain blood flow for 3–4 days before removal of the tube and ligation of the artery, giving time for increased collateral circulation. The memorandum referred to early work with free vein grafts, commenting that heparin was necessary, and adding ‘they are considered unsafe for use in heavily contaminated wounds and are likely to be applicable only in special vascular injury centres’. However, ligation was widely practised and the results of this are shown by DeBakey and Simeone (1946, 1955) in a series of nearly 2,500 arterial injuries. Three hundred and forty six from 502 limbs were amputated after ligation of the popliteal artery. Overall, nearly 50% of limbs came to amputation after ligation of an axial vessel. The results following arterial repair in 120 cases were a good deal better even in those difficult times when the average interval between wounding and operation was 10 h. Arterial repair was regularly practised during the Korean War, a conflict in which the incidence of arterial injuries in those surviving wounding increased and the interval from injury to operation dropped to 6 h. An amputation rate of 13% was recorded by Hughes (1958) and by Jancke (1958). One significant publication describing experiences in civilian practice came from Porter (1967) who described 100 cases of arterial injury treated at the Accident Hospital in Birmingham between 1956 and 1965. Eighteen of 19 major vessels were successfully repaired. In 48 cases the condition of the limb was such that amputation was necessary. Morris et al. (1960) reported 220 cases. Arterial repair was successful in 86%. Fourteen major vessels were ligated early in this series, which led to five amputations, hemiplegia in two of three ligated carotid arterial lesions and two deaths. The conflicts in Vietnam and Ulster saw an evolution of emergency arterial repair so that failure should be the exception. In 1966 the Vietnam Vascular Registry was established at the Walter Reed Hospital, carrying on a tradition of centralisation of information so permitting analysis and improvement, a tradition established in this country and now, sadly, abandoned with the same alacrity as the bandwagon of audit, outcome studies and clinical governance rolls inexorably forwards. Rich et al. (1970) reviewed 1,000 arterial injuries: in 42% there were associated peripheral nerve injuries; there were fractures in 28.5%. Hewitt et al. (1973) and Rich et al. (1975) discussed 558 false aneurysms and arterio-venous fistulae. The popliteal artery remained a problem; an

Surgical Disorders of the Peripheral Nerves

amputation rate of 30% was recorded by Rich et al. (1974). The principles of urgent arterial repair are set out in Barros d’Sa’s (1992) outstanding chapter in Eastcott’s work describing intra-luminal shunts for the early restoration of blood flow to the leg after knee-capping injury in which a close range shot gun blasts the contents of the popliteal fossa and fragments the femur and tibia. He comments that shunts have revolutionised the treatment of vascular injuries complicating fractures of the lower limbs. Barros d’Sa set out the principles of treatment in 188 major vascular injuries in the lower limbs of 118 patients in his Hunterian Lecture of 1982 (Barros d’Sa 1982). These include: revascularisation within 4 h; fasciotomy of all four compartments; vein grafting for the artery, and repair of at least one major vein. This led to an amputation rate of 5% for cases of popliteal artery arterial injury, the lowest of any civilian or military series yet published. Most patients were admitted within 30 min, indeed one half were admitted within 15 min of injury. Shunts permit adequate fixation of a fracture before definitive repair of the vessels. We are in no doubt that Barros d’Sa’s Hunterian Lecture stands as one of the most important contributions to the surgery of injury ever published. We make no apology for repeating the comments of Hughes and Bower (1961) who write of the incidence of gangrene after ligation of a major artery: ‘It is realised that these percentages, derived from battlefield wounded may be slightly higher than may be encountered in many injuries in civilian life; these should serve as a grim reminder of the dangers of ligation of major arteries and may deter some individuals so inclined. We have been amazed at the lack of interest and knowledge of many surgeons who have no idea as to which vessels may be safely ligated.’ Harsh words! Sadly we have found them applicable today. Perhaps now is as good a time as any to comment on arterial spasm. We have never seen a case of spasm alone producing obstruction in an adult; we have seen it in children. As to sympathetic block, or sympathectomy, Seddon (1964) when writing of acute ischaemia said ‘let us hope that the completely futile sympathetic block will not have been done’. Birnstingl (1982), vascular surgeon to the Royal National Orthopaedic Hospital for some years, said ‘sympathetic block is useless’; ‘sympathectomy has no place in the treatment of acute ischaemia; spasm should never be diagnosed unless the artery has been exposed at operation and either distended with saline or opened to exclude an intimal tear’. There is, too, the view of Eastcott and colleagues in his monumental work Arterial Surgery (1992): ‘sympathetic block or denervation are practically useless in the treatment of acute limb ischaemia’. The concept that arterial spasm is induced by the sympathetic nerves was demolished by Kinmonth and his colleagues (1956) who were unable to induce spasm in large arteries by stimulation of the sympathetic system or dispel it by sympathectomy, and finally laid to rest by Holden (1979) and Eadie (1979) in two articles of exceptional importance.

Compound Nerve Injury

309

Table 8.3  Arterial injuries in association with nerve lesions: including the supraclavicular plexus and penetrating missile wounds (1975–2006). Closed Open Total Repaired Total Repaired – 203 – 122 – 374 – 291 4

0

4

1

Subclavian

82

40

13

9

Axillary

63

54

35

27

Brachial

17

11

35

31

Radial and ulnar

5

2

224

198

Common femoral

0

0

4

3

Superficial femoral

2

2

4

4

Profunda femoris

2

1

2

1

Vertebral

Inferior gluteal

2

0

1

0

14

9

32

10

Posterior tibial

3

1

7

4

Anterior tibial

9

2

13

3

Popliteal

Table 8.4  Traumatic false aneurysms and arterio-venous fistulae with associated nerve lesions 1875–2006. Aneurysms – 75 Arterio-venous fistulae – 13 Region – artery Posterior triangle of neck

5

2

Axillary

44

3

Brachial

11

3

Iliac

1

2

Femoral

3

1

Profundus femoris

2

0

Inferior gluteal

1

0

Popliteal

5

2

Posterior tibial

2

0

Anterior tibial

1

0

Our own experience in the treatment of arterial injuries complicated by nerve lesions of one sort or another is set out in Tables  8.3 and 8.4. Methods of exposure and repair are described in Chapter 7. Arterial lesions are sufficiently common a complication of injuries to three joints, the shoulder, the knee, and the elbow as to merit separate consideration.

8.2.1 The Shoulder ‘Arterial injury should be suspected when there is a large and sometimes pulsatile axillary swelling even though a radial pulse be still perceptible’ (London 1967b). As Barros d’Sa(1992) pointed out it is sometimes difficult to recognise critical ischaemia after injuries to the axillary artery because

of the extensive anastomotic network of collateral vessels around the shoulder: ‘the distal limb may look perfectly viable to the extent that even the pulse may be maintained … failure to recognise and surgically correct an axillary artery injury may result in an expanding false aneurysm and marked compression of the cords and nerves of the brachial plexus within a limited space’. The persistence of peripheral pulses with normal capillary refill may lead the unwary clinician to neglect the underlying arterial injury. The consequences of neglect of a late bleed from a false aneurysm were described in a report (Syed and Williams 2002) of an 80 year old woman who suffered a fracture of the humerus. Bleeding recommenced after 4 months leading to erosion of the humerus. The diagnosis was not made for 2 weeks, by which time the upper limb was ischaemic and disarticulation of the shoulder was necessary (Fig.  8.7). The dangers of late closed reduction were shown by Flaubert (1827) who described attempted late reduction of a dislocation by traction applied by six (!) medical students which led to rupture of the axillary artery, avulsion of the brachial plexus, injury to the spinal cord and death (perhaps this experience stimulated his son to describe the fate of the wretched Hippolyte in Madame Bovary); and by Calvet et al. (1942) who collected 90 cases of arterial injury from dislocation, in 68 of whom late reduction had been attempted. There was a 50% mortality. Watson-Jones (1936) reported a fatal outcome from rupture of the axillary artery in a man with recurrent anterior dislocation of the shoulder. Bigliani et al. (1991) said that ruptures of the axillary artery, secondary to shoulder fracture or dislocations, account for 7% of all arterial injuries. Puri et al. (1985) made a significant observation: ‘the intima had fractured cleanly and circumferentially’. Mullett et al. (1998) are not alone in urging swift action and avoiding delay for the sake of angiography. Amongst others, Gallen et  al. (1984), Nash et  al. (1984) Laverick et al. 1990 and Helm and Watson (2002) urge alertness and swift action (Fig. 8.8). Emadian and Lee (1996) say ‘Regardless of the mechanism, vascular injury must be suspected in all cases of anterior shoulder dislocation where there is evidence of plexopathy or isolated neuropathy … delayed diagnosis and treatment invariably leads to permanent neurological deficit and morbidity’. In one of our cases, of fracture/ dislocation of the shoulder in a 59 year old man, the patient’s complaints of pain and the signs of deepening of lesion were not appreciated for several days. Angiography was done which showed bleeding from the subscapular artery. Two unsuccessful attempts were made to occlude this by embolisation. We first saw him at 6 weeks. He was in right heart failure. His haemoglobin was 4.9 gm per 100 mL. He was in great pain and there was a total and deep plexopathy. An MR scan which accompanied him showed an enormous haematoma occupying the axilla and the arm and suggested continuing bleeding. Treatment was simple: the axillary artery was exposed and controlled above pectoralis minor and the brachial artery exposed and controlled in the arm. More than 4 L

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Fig. 8.7  Leaking aneurysm 20 weeks after fracture of the neck of the humerus in an 83 year old woman. She made a good recovery after repair of the defect. Above left. Radiograph on day of injury. Top right.

of altered blood were removed from the sac. The defect in the axial vessel was, at most, 2 mm in diameter and it was closed by direct suture. His pain was relieved. There was gradual recovery of the nerves but the small muscles of the hand never recovered. A much happier outcome was achieved in another case because of the alertness of Andrew Unwin (London), acting surgeon to the Ascot race course. A champion jockey fell at a hurdle and a horse following stamped on his left shoulder. There was immediate severe pain. We saw him within 12 h. Pain was intense: there was complete paralysis of deltoid and weakness and sensory loss involving the median and radial nerves. There was no bruit. The radial pulse was present. There was ecchymosis, bruising, and swelling in the lower part of the axilla. A clinical diagnosis of bleeding from one of the offsets of the axillary artery was made and this was

Surgical Disorders of the Peripheral Nerves

Radiograph at 18 weeks. Below left. MR scan at 18 weeks. Below right. Angiogram on the day of operation.

Fig. 8.8  Rupture of axillary artery from fracture of proximal humerus in a 68 year old woman. The robust collateral circulation contributed to delay in diagnosis. A large haematoma in the axilla caused pain and deepening of the nerve lesion.

Compound Nerve Injury

311

Fig. 8.9  A 78 year old woman sustained a double circumferential rupture of the intima of the axillary artery of the intervening thrombosis: in effect a floating segment of the vessel. Repair was successful.

confirmed by exposing and controlling the axillary artery using the inferior portion of the exposure of Fiolle and Delmas. The posterior circumflex humeral artery, which was 2.5 mm in diameter, had ruptured and 1.5 L of fresh blood were removed from the axilla and the quadrilateral tunnel. The artery was ligated. The ruptured circumflex nerve was repaired. The median and ulnar nerves recovered within days and there was early relief of pain. The first signs of reinnervation of the posterior deltoid were detected at 3 months after operation and by 9 months the general recovery was good, he was back riding and winning. By 15 months the range of movement at the shoulder was full, and the power of forward flexion, abduction and extension at the shoulder was measured at 90% of the uninjured shoulder (Patel et al. 2001). An

invited reviewer criticised the conduct of this case because angiography had not been performed. We thought this very odd: that bleeding was occurring in the axilla was beyond doubt and rapid exposure and control of the first part of the axillary artery was the obvious, unavoidable, and correct course. Embolisation would have done nothing to stem the bleeding from the distal artery which measured, in diameter, 2.5 mm, nor would it have decompressed the affected nerves. Repair of the circumflex nerve would have been delayed. The first injury in closed traction is fracture of the intima, which in more violent injury progresses to rupture of all coats of the vessel (Fig. 8.9). The intimal injury can be seen easily as a pale crescentic line, the damaged segment of the artery filled with thrombus. Attempts to restore flow using embolectomy catheters are invariably futile in such cases and cause such extensive longitudinal damage to the intima that later repair is impossible. Torrential bleeding after rupture of the whole vessel is unusual in the closed traction lesion. The tips of the artery generally contract down but in one case the proximal stump of the vessel was plugged by an adjacent ruptured nerve trunk. There was great haemorrhage when this plug was removed. The length of damage ranged from 3–28 cm. The brittle atheromatous vessels of older patients are vulnerable even in low energy injuries. Arteriography, whilst always valuable, should not unduly delay operation. A reasonable circulation to the skin is not the issue: what is important is whether muscle is perfused. Failure to restore flow through damaged axillary or common brachial artery within 6 h of injury is almost always followed by, at least, severe ischaemic fibrosis. In most of our cases of closed infraclavicular lesion we did not proceed to arteriography because the clinical evidence was clear. In these cases the posterior triangle was neither swollen nor deeply bruised; the subclavian pulse was palpable whereas in the infraclavicular fossa there was swelling with bruising of the skin and the brachial pulse was absent. The axillary artery was ruptured deep to pectoralis minor at the level of the coracoid process. It is important to remember that these severe complications may follow low energy injuries especially in an older patient. Stenning and his colleagues (2005) described 16 cases where arterial injury occurred after dislocation of the shoulder or fracture of the proximal humerus (Table 8.5). The diagnosis was made by the delayed onset of nerve palsy or the deepening of the nerve lesion whilst under observation.

Table 8.5  87 nerve lesions in 20 patients with arterial injury from low energy injuries to the shoulder. Median Ulnar Radial Musculocutaneous Circumflex

Total

Conduction block (Neurapraxia)

9

17

18

16

9

69

Favourable degenerative (Axonotmesis)

10

2

1

1

2

16 (recovery was incomplete in 4 cases)

Unfavourable degenerative (Neurotmesis)

1

0

0

0

1

2

20

19

19

17

12

87

Drawn from Stenning et al. (2005).

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All patients had severe pain. Nine ruptures of the axillary artery were repaired by reversed vein grafts; in one, this was undertaken at the primary treating hospital. Of the seven ruptures of branches of the axillary artery, the defect was oversewn in five and repaired by vein patch in two. Anticoagulants were never used. The onset of nerve palsy was evident within 6 h in six patients and within 24 h in five more. It ranged from 1 to 7 days in two limbs and from 8 days to 16 weeks in seven more. In nearly every case the nerve palsy was initially incomplete and there was steady worsening in the ensuing 12–24 h. This deepening in cases of late onset of palsy is diagnostic of secondary haemorrhage. Most of the affected nerves recovered rapidly (conduction block); the remainder recovered more slowly(axonotmesis).

8.2.2 The Elbow Morris et  al. (1960) described 53 wounds to the brachial artery. Forty nine of these were repaired; three came to amputation. Five arteries were ligated. From these there were two amputations and one death. We have seen 52 cases and have repaired 42 arteries. Seventeen arteries were ruptured in closed lesions. We agree with Barros d’Sa (1992) that the technique must be meticulous, using interrupted sutures under magnification. Some ischaemic fibrosis was detectable in the 22 patients in whom the brachial artery was not repaired or where delay before restoration of flow exceeded 6 h. The collateral circulation at the elbow is more robust than that at the knee. The alternative pathways include the profunda brachii artery which accompanies the radial nerve through the lateral intermuscular septum where it becomes the radial collateral artery. The superior ulnar collateral artery accompanies the ulnar nerve; in the adult it may be as wide as 1.5 mm at its origin hence its regular use for the free vascularised ulnar nerve graft. The inferior ulnar collateral artery is regularly seen during medial approaches to the elbow as a vessel which pierces the intermuscular septum to curl around the humerus between the triceps and the bone. On occasion, there is a substantial artery running with the median nerve. These vessels anastomose with recurrent branches from the ulnar and radial arteries. This network may maintain perfusion of the hand and the extensor muscles in cases where the brachial artery has been divided in the lower one third of the arm when there is no associated fracture or dislocation, but the situation is very much worse if the ulnar or radial nerve is entrapped within the fracture or compressed by haematoma, because collateral circulation will diminish or altogether cease. A similar situation obtains if a surgeon is so unwise as to apply a suprasystolic cuff in a pulseless limb. We are particularly grateful to Mr Philip Coleridge Smith (London) for his advice about flow through peripheral arteries and also for informing us about the work of Wajcberg and his colleagues (2006) who used high resolution

Surgical Disorders of the Peripheral Nerves

ultrasonography to measure the rate of flow through the brachial artery in adults and in children. Flow was calculated by multiplying the velocity-time interval of the Doppler flow signal by the heart rate and the cross-sectional area of the vessel according to Laplace equation: BF(blood flow) = [p × (D/2)]2 × FV(flow velocity). The mean diameter of the brachial artery in children aged between 4 and 5 years is 2.7 mm, which provides a resting flow of about 200 mL per min. The reader will at once note the significance of the diameter of the vessel from the equation of Laplace and this factor is emphasised by Poiseuille’s law which states that flow through a vessel is affected by three variables; the radius of the cylindrical vessel, the total tension in the wall and the pressure gradient. Poiseuille’s law is the physical law describing the volume of flow (F) of an incompressible uniform viscous liquid, where R is the internal radius of the tube, P the pressure difference between the two ends, h the dynamic fluid viscosity and L the total length of the tube: F=

π R 4 [DP ] 8η L

The diameter of the superior ulnar collateral artery at the elbow in children is no more than 1 mm. This calibre provides flow of about 20 mL per min assuming that the pressure gradient is the same as that in the brachial artery itself. These facts must be borne in mind by any clinician inclined to the view that cessation of flow through the brachial artery is a matter of little consequence. Case Report: A 20 year old woman fell downstairs suffering fractures of the distal humerus (Fig. 8.10). On arrival at hospital the limb was noted to be pulseless. The fracture was fixed through a posterior approach. The artery was not explored and the forearm was not de-compressed. Twelve hours later an operation was performed attempting to restore circulation, which failed. The patient was advised to undergo cervical sympathectomy, advice which she declined. She was then referred to St Mary’s Hospital where prompt decompression of the extensor muscles saved them. The flexor muscles of the forearm were necrotic; indeed, they were liquefied and were totally excised.

8.2.3 The Knee The arrangement of the popliteal artery, of its branches and the paucity of collateral vessels makes it particularly vulnerable to injury, adds greatly to the difficulties of repair and leads to the most severe consequences in the event of failure. We think these are amongst the most technically difficult of peripheral arterial injuries. Eastcott’s phrase ‘the lifeline of the leg’ is clearly shown by the amputation rate in such civilian series as Orcutt and colleagues (1983), who found survival of the leg after repair of the popliteal artery in 95% of the penetrating

Compound Nerve Injury

wounds, but in only 70% of those from blunt injury; and by a recorded amputation rate following popliteal artery injury from dislocation of the knee of from 30% to 80% (Lefrac 1976; Green and Allen 1977; Alberty et al. 1981) (Fig. 8.11).

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Four fractures are notably associated with arterial injury. Arterial rupture occurs in 3% of supracondylar fractures of the femur, in 30% of dislocations of the knee, in 10% of fractures of the proximal tibia, and fractures of the proximal part of the fibula are associated with damage to the anterior tibial artery. The technical difficulties of repair increase with injuries close to the trifurcation of the popliteal artery. In such cases there is more likely to be gross injury to the skin, muscle and nerve. Case Report: A 58 year old man was knocked down by a car and suffered open fractures of femur and tibia, with rupture of the popliteal artery (Fig. 8.12). The limb was critically ischaemic and had been so for 2h by the time the patient reached theatre. The skeleton was rapidly stabilised by a Küntscher nail passed from the hip to the ankle. Then with the patient prone the femoro-popliteal trunk was exposed. The vessels were atheromatous, and the gap between the prepared stumps was 15 cm. A reversed vein graft from the distal femoral artery to the posterior tibial and to the anterior tibial (by means of a branch) successfully restored circulation. The fractures healed; persisting discharge from the tibial fracture ceased at 9 months after removal of the nail. The patient had no pain, normal function of the ankle and foot and a range of flexion of the knee between 0° and 80° (Figs. 8.13 and 8.14).

8.2.4 The False Aneurysm and Arteriovenous Fistulae Fig. 8.10  Damage to the brachial artery associated with severe supracondylar fracture of the humerus in a 20 year old woman. There is extensive occlusion of the brachial artery caused by intimal damage, thrombosis and spasm. There was infarction of all the flexor muscles of the forearm.

Fig. 8.11  Dislocation of the knee in a 68 year old woman was treated by manipulation and plaster of Paris. The appearance of the foot on removal of the splint some days later is shown.

Complete section of the artery does not inevitably lead to exsanguination as the vessel may constrict in spasm: an observation first made by John Hunter. The partial wound is

314

more likely to cause catastrophic bleeding but may also lead to the formation of a false aneurysm from a breach of the arterial wall. The sac contains thrombus, its wall is formed from perivascular soft tissues which may include nerve

Fig. 8.12  Open fractures of the femur and tibia, with rupture of the popliteal artery. Internal fixation and reversed vein graft to the anterior and posterior tibial arteries.

Fig. 8.13  The popliteal artery was ruptured by a fracture/ dislocation of the knee in a 31 year old man. The main artery was successfully repaired. The anterior tibial artery was ligated. Most of the anterior compartment of the leg had to be excised.

Surgical Disorders of the Peripheral Nerves

trunks. Aneurysms may also occur in a closed traction lesion of the infraclavicular plexus because of avulsion of such an offset as the suprascapular, circumflex, humeral or suprascapular arteries. We have encountered 33 such cases. Aneurysms and fistulae lead to a general decline of nerve function which is all the more rapid with expansion of the vascular lesion. Nerves embedded within the sac of a false aneurysm or fistula are badly damaged; recovery is always imperfect, and may not occur at all. Those more remotely affected will recover after prompt treatment. Pain indicates that nerves are closely related to the false sac; in these, complete loss of autonomic function is the rule even when deep pressure sense and other modalities are still partially preserved (Dunkerton and Boome 1988). In some of our cases diagnosis was delayed and in nine cases of false aneurysm the preoperative diagnosis was neurotmesis of an adjacent main nerve. Case Report: A 37 year old man suffered a perforating injury in the delto-pectoral groove from fine steel wire. There was immediate loss of sensation in the hand. There was no local swelling. The patient was seen by us 3 months after the injury, with loss of elbow flexion, complete median palsy and a tender swelling in the axilla with a positive Tinel sign radiating into the territory of the nerve. There was a good radial pulse. At operation a false aneurysm of the axillary artery was found. The musculo cutaneous nerve had been severed, the median nerve was wrapped around the wall of the sac. The sac was excised, the artery repaired by reversed vein graft, the musculo-cutaneous nerve was grafted, a median neurolysis was done. Good circulation was maintained. At 9 months the biceps muscle regained power to MRC 5. There was a Tinel for the median nerve in the middle part of the forearm, with recovery in the superficial forearm flexors.

Compound Nerve Injury

315

Fig. 8.14  The popliteal artery and vein were ruptured by dislocation of the knee in a 28 year old man. The vessels were successfully repaired and a four compartment fasciotomy was completed within 6 h of the injury.

Larger arterio-venous fistulae produce the local and systemic responses described by Sumner et al. (1992): ‘the drop in total peripheral resistance is the essential patho-physiological aberration’. This fall leads to a drop in diastolic pressure, an increase in pulse rate, increase in cardiac output, and ultimately to heart failure. There is hyperventilation. The local effects are a reflection of deprivation of blood which may lead to venous insufficiency. The part is swollen, dry and discoloured. The diagnosis is made by listening to the murmur which is continuous but louder in systole. The level of arterial injury is not necessarily related to the entry wound. One false aneurysm was caused by a gunshot wound in the opposite arm, 4 years previously: a fragment in this arm migrated around the chest wall and embedded itself in the wall of the axillary artery of the opposite limb. In another case of high velocity missile injury the entry point was at the anterior axillary line whilst the exit wound lay at the spine of the scapula. Arterio-venous fistula between subclavian artery and vein developed where they traversed the first rib. Case Report: A 28 year old soldier was wounded in the posterior triangle of the neck by a fragment from an exploding tank. He presented with severe pain, and complete loss of function of C5 and C6. A rumbling bruit in the neck with palpable thrill diagnosed an arterio-venous fistula. The lesion was successfully embolised by Dr Al Kutoubi (St Mary’s Hosppital). There was rapid reduction of pain, with considerable spontaneous recovery of the deficit in C5 and C6 (Fig. 8.15). Case Report: The following description is typical of a true causalgia. One of our patients, a man of 27, was shot in the

arm by a bullet from a hand gun during a street robbery. He was an innocent bystander. He experienced immediate, intense, burning pain in the arm, forearm, and hand, which worsened over the following days. Nothing relieved it. We first saw him at four weeks after injury. He was quiet, withdrawn, answering questions in monosyllables. He had lost weight, and was exhausted from lack of sleep. He protected the affected arm against his body; he could not tolerate examination, nor pressure or contact from his sleeve. Light draught provoked intolerable pain. The hand was swollen, mottled

Fig. 8.15  A bullet caused a fistula between the internal iliac artery and vein which was successfully embolised by Dr Al Kutoubi.

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with alternating red and blue discolouration. There was profuse sweating. The nails were coarse, the hair on the back of the hand had overgrown. He had learned that some protection came by keeping the hand and forearm wrapped in a cool, moist cloth. There were deep but incomplete lesions of the median and ulnar nerves. There was a pulsatile swelling in the upper arm, and this, with a continuous rumbling bruit,  led to the diagnosis of a large arterio venous fistula (Fig. 8.16). He was in right heart failure and the veins of the neck were so distended that sympathetic blocks or sympathectomy could not be considered. The fistula was successfully corrected by excision of 12cm of the axillary artery and replacing it with a reversed vein graft and by suturing the defects in the axillary vein. The median nerve was embedded in the wall of the fistula, the epineurium was disrupted and individual bundles were splayed out over sac. The ulnar nerve was more remote from the fistula. Pain relief was early, dramatic and enduring.

Surgical Disorders of the Peripheral Nerves

At three years the patient noted only imperfect sensation in the thumb and index but little else abnormal. Case Report: Lateral meniscectomy through the arthroscope was performed in a 31 year old man. He experienced intense pain on awakening which was not controlled by morphine. The leg became swollen, blue and cold. He was given anticoagulants on the suspicion of deep vein thrombosis. The true diagnosis of false expanding aneurysm of the lateral genicular artery was not made until it was too late to prevent massive ischaemic fibrosis of all muscles in the leg. We saw him 5 years after the event. One of us was sharply condemned by the lawyers and doctors involved in this case for our temerity in suggesting that 5 years without any form of active treatment was a touch unreasonable! Case Report: A 55 year old woman developed intense pain after removal of a lipoma in the axilla (Fig. 8.17). We saw her at 2 weeks because of suspected damage to the median nerve. The hand was red and dry, but not insensible; there was weakness of the flexor muscles of the forearm and the intrinsic muscles of the hand. The radial pulse was diminished. The arteriogram showed a block in the distal part of the axillary artery. At operation, a false aneurysm was displayed; its wall was formed from the brachial sheath and the median nerve which was splayed out: the ulnar nerve was displaced and compressed. Sumner, Eastcott and Rich (1992) emphasise that arteriography can be misleading in the peripheral aneurysm and that ultrasonography may be the more valuable investigation: of course first one must think of the diagnosis.

8.2.5 Ischaemia and the Nerve

Fig. 8.16  Large arterio-venous fistula in the axilla.

It is difficult, in the clinical situation, to separate the effects on the nerve of pure ischaemia from those of ischaemia associated with compression, traction and distortion. Certainly we see: (1) ischaemia of the nerve trunk itself. Seddon (1975a) described several cases. In one case of severe Volkmann’s ischaemic contracture, amputation was performed: the branches of the median nerve within the palm of the hand, where they were not compressed, were completely infarcted. Lamerton’s (1983) case is interesting as an example of painful ischaemia of the sciatic nerve relieved by the reconstruction of the internal iliac artery. (2) Ischaemia associated with compression or stretching of the nerve by haematoma or aneurysm, which is worse when the nerve is embedded in the sac. (3) Ischaemia of nerves compressed distally by swollen muscle. Parkes (1945) recognised the effect of compression by swollen muscles and noted venous obstruction rather like strangulation of a hernia leading to irreversible changes in the nerve at between 12 and 24 h. An intact intrinsic system may nourish a considerable length of the nerve trunk. In one case in which the entire flexor

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Fig. 8.17  Iatrogenous false aneurysm in the brachial artery.

compartment of the forearm was excised for ischaemia the median nerve survived because of the longitudinal supply over a length of 24 cm. The nerve recovered. In another case, in which the posterior muscles of the thigh were excised for gas gangrene the sciatic nerve was maintained by its longitudinal supply over a length of 38 cm. There was useful recovery. In one of our early hand replants we noticed that the median artery was so large that its repair provided sufficient circulation to the hand while more elaborate reconstruction went on. One of the best descriptions of the effect of ischaemia upon nerves, and upon nerves alone, and of the rapid deepening of the defect is provided by Wilbourn (2005). He, with Tsao described a compartment syndrome following axillary arteriography in 2003. Wilbourn suggests that bleeding into the medial brachial fascial compartment, which extends from the axilla to the elbow and which is bounded by the tough medial intramuscular septum and the axillary sheath, is responsible for the majority of infraclavicular plexopathies following axillary regional block and possibly for most of the neuro-vascular injuries which result from closed or penetrating missile injuries into this region. Sensory symptoms precede the motor. Reversible ischaemic conduction block is responsible for the initial symptoms but the lesion soon deepens into a degenerative one and this is marked by paralysis. The diagnosis rests upon the history and upon detecting

haematoma or ecchymosis in the axilla or arm. Wilbourn says: ‘distal pulses are normal, as they are with most compartment syndromes because the elevated pressure, although sufficient to collapse the vaso nervora, is far below mean arterial pressure. Ultrasound, MR, and CT may reveal the vascular lesion, but, considering the very brief time available for surgical decompression before irreversible nerve damage occurs, obtaining these is rarely justified.’ Patients explored within 4 h from onset of symptoms were eight times more likely to recover completely than those who were observed or treated with delayed operations. In these, there was permanent residual defect often accompanied by severe pain (Fig. 8.18). The lumbosacral plexus is vulnerable to haematoma. Allieu and colleagues (1986) studied the effects of haematoma on the femoral and sciatic trunks. Their advice is salutary: ‘conservative treatment of a haematoma is to be condemned’. Ultrasound is useful in diagnosis: decompression is a matter of urgency. The reader is referred to the excellent review of lesions of the lumbo sacral plexus from Donaghy (2005) who recognises two distinct syndromes of compression of the lumbo sacral plexus by retro peritoneal haemorrhage. In the first bleeding within the psoas muscle damages the obturator and femoral nerves. In the second, haematoma within the iliacus muscle compresses the lumbo sacral plexus. Because the

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Fig. 8.18  The brachial artery was occluded by embolism in a 58 year old man. Embolectomy and fasciotomy were carried out 8 h later. There is fibrosis of the muscles of the forearm and continuing pain.

iliacus fascia is less capacious than that overlying the psoas muscle the effects are more severe. Donaghy describes how to distinguish between these two syndromes by clinical examination: ‘psoas muscle haematomas do not cause profound pain on forced hip extension, the hip is not held flexed, no haematoma is palpable or visible in the iliac fossa or groin, and there is weakness of the thigh abductors indicating involvement of the obturator nerve’. He emphasises that the important differential diagnosis in these syndromes is abscess secondary to appendicitis or following laparotomy. Urgent retrieval of a nerve from a joint or fracture, urgent correction of expanding haematoma, or urgent decompression in compartment syndrome is usually followed by rapid and complete recovery. Delayed action or inaction may lead to such damage of the nerve that repair is needed, or to irretrievable damage to the nerve, the muscle and other target organs. Effects on the tissue – compartment syndrome: When an artery is occluded there is death of tissue. It is wrong to apply the term compartment syndrome to the events which follow ligation of the popliteal or anterior tibial arteries, to the gangrene of peripheral vascular disease or the gangrene of arterial embolus. However, muscles confined within semi-rigid spaces bounded by bone and inelastic fascia are vulnerable to perfusion block, which may occur as a result of arterial

Surgical Disorders of the Peripheral Nerves

injury and in the event of delayed restoration of circulation, but it may also occur because of swelling within the compartment, as in bleeding from a fracture or haemophilia or infusion of fluids. The swelling following unaccustomed exercise or after the prolonged compression sustained in coma is more akin to the effect of delayed restoration of circulation. All these effects may be exacerbated by tight external bandages or splints. The term compartment syndrome was introduced by Matsen (1975) This is useful for it draws attention to the ‘final common pathway’ of ischaemia (Pellegrini and McCollister Evarts (1991). Of course, abnormal events precede ischaemia of muscle. There is collapse and block of flow through low pressure systems, first the lymphatic and then the venous. There is now tissue hypoxia and derangement of fluid and electrolyte exchange across cell membranes so that fluid passes from vessels to the extra vascular compartment. Barros d’Sa (1992) emphasises that the increased permeability of vessels from hypoxia leads to increase of pressure within compartments by exudation. The final event is the closure or obstruction of perfusing arterioles when tissue or extra vascular pressure exceeds the critical closing pressure of those vessels (Burton 1951). The vicious cycle is complete (Eaton and Green 1972). Fluid entering the compartment cannot get out; it continues to leak into the compartment until the pressure within that compartment is so high that inflow is blocked. The tissues will now die. Ellis (1958) found 4.3% of ischaemic contractures in his series of tibial shaft fractures and Owen and Tsimboukis (1967) found a clawing of toes from contracture of the deep flexor compartment in no less than 10% of such fractures. In the upper limb the compartments most at risk are the flexor compartment of the forearm, then the extensors of the forearm, the small muscles of the hand, especially the interosseous muscles and adductor pollicus, and the pronator quadratus. We have seen cases involving the deltoid and pectoralis major. In the lower limb the deep flexor compartment of the leg leads the way, followed closely by the anterior compartment. Then follows the other compartments of the leg, and the small muscles of the foot; the syndrome is not rare in the gluteal muscles and it also , on occasion, involves the muscles of the thigh. Holden’s review (1979) is particularly good. One cannot add to his criteria for clinical diagnosis and action which are, first and foremost, pain persisting after reduction of fracture and refractory to moderate analgesia: and tense swelling of the afflicted compartment. We agree with Holden that clinical suspicion is the most important indication for intervention and this must be acted upon before the onset of neural deficit. Ragland et al. (2005) described 24 cases of compartment syndrome in the new born. Urgent decompression is recommended – most of these infants required multiple operations but even so they were left with permanent defects in growth, nerve function and skeletal development.

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8.2.6 Iatrogenous Ischaemic Injury We have seen an alarming increase in the number of these cases over the last 10 years. Table 8.6 outlines 164 cases of post ischaemic contracture treated by palliative operations since 1980. More than one half of these were seen after 2000. A main artery was damaged during operation in 78 patients (Fig. 8.19). Most of the wounds to the popliteal and anterior tibial arteries occurred during elective arthroplasty, ligament reconstruction or arthroscopy of the knee. The posterior tibial and peroneal arteries were most often injured during operations for fracture. Correction of deformity or limb lengthening, using frames, accounted for some serious injuries throughout the leg. The 84 cases of compartment syndrome were related to operation; those directly caused by fracture, crush, coma or sepsis are excluded. Delayed intramedullary nailing of closed fractures of the tibia was responsible for 18 cases. It seems that some clinicians persist in the belief that oxygenation of muscle and nerve enclosed within rigid osseofascial compartments can be assessed by noting return of circulation to the nail bed. Others persist in the false notion that compartment syndrome is a distinct entity from the effects of anoxia caused by interruption of flow through an axial artery. The difference is one of degree. The final common pathway is the same: anoxia causes breakdown of homeostasis across the membrane of the cells of the capillaries, muscles, Schwann cells and axons. The annotation on compartment syndrome by Klenerman (2007) is compulsive reading: ‘In 1896, Starling had pointed out that under normal conditions, a state of near equilibrium exists at the capillary membrane, whereby the amount of fluid filtering outward through arterial capillaries equals the quantity of fluid which is returned

Table 8.6  164 cases of iatrogenous post ischaemic contracture of leg and foot treated by operation (1980–2007). A: Cause Lesion of popliteal artery

20

Lesion of anterior tibial artery

26

Lesion of posterior tibial artery

32

Lesion of peroneal artery “Compartment syndrome” Total

2 84 164

B: Compartments affected All four compartments

24

Anterior and lateral

46

Deep flexor

55

Deep and superficial flexor

32

Small muscles of foot

7 164

More than one half of these cases were seen after 2000.

Fig.  8.19  Massive false aneurysm from the lateral geniculate artery caused by the arthroscope during lateral meniscectomy. This was not diagnosed for three days.

to the circulation by re-absorption at the venous ends of the capillaries.’ To Klenerman’s abnegation of the ‘emergence of evidence based orthopaedics’ might be added that some recent meta analyses and ‘Cochrane reviews’ are flawed by ignoring earlier work, work published in other languages or the contributions made by other disciplines. Valuable monographs and reference texts are excluded. ‘Evidence-based’ medicine which relies on the partisan and selective review of recent literature is an ugly distortion of the work of Cochrane. The earliest symptom of peripheral ischaemia is pain, often so intense that it does not respond to morphine and alteration in sensibility in the extremity soon follows. The earliest fibres to suffer are the largest, those conveying proprioceptive and vibration sense. Deepening of sensory loss and the first signs of weakness of muscle are proof positive of critical ischaemia. One of the effects of anoxia is to increase the permeability so that to the true ischaemia caused by cessation of arterial supply is added that caused by rising pressure within the fascial compartment. The pathophysiology of ischaemia and the risks from re-perfusion are reviewed by Barros d’Sa and Harkin (2005) who outline the grading system for ischaemia developed by the Society for Vascular Surgery and the International Society of CardioVascular Surgery. Class 2A describes a limb which is

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threatened, in which symptoms are limited to a mild sensory loss. Limbs with pronounced sensory loss, mild to moderate motor loss, even with audible Doppler signals are immediately at risk: for these, delay is unacceptable. The recommended treatment for Class 3 limbs, where Doppler flow is absent and where there is paralysis with total sensory loss, is delayed amputation which is performed after resuscitation as attempts to restore blood flow would lead to hyperkalaemia and myoglobinuria. The classification sets out treatment of the lower limb in which circulation has been imperilled by thrombo-embolism. Perhaps it is time to replace the much abused term ‘critical ischaemia’ by this classification. McQueen and Court-Brown (1996) have clarified the role of intracompartmental monitoring. Many of the cases outlined in Table 8.6 could have been prevented by their method. Chant (2005), in commenting on the recent recommendations from the Vascular Surgical Society (2001) says: ‘it notes the introduction of so-called “clinical governance” and goes on to say “general surgeons who are not vascular specialists undertake no active emergency arterial surgery, and it is difficult for them to justify treating vascular emergencies under the scrutiny of clinical governance”. In other words, if a general surgeon in the UK now performed an operation for a vascular emergency, and were that patient to die or perhaps lose a leg unnecessarily, then that surgeon may well be open to litigation.’ Chant adds a comment which must bring a chill to the heart of doctors and patients alike: ‘if you choose to live or work in a remote area, then it is unlikely that you will get the very best of medical treatment. That is a reality of life.’ Our experience suggests patients do not need to live in the Outer Isles to receive sub standard care. One wonders what might have been said about the actions of an experienced surgeon who encountered profuse bleeding whilst operating on a fracture of the proximal tibia. A cuff had been placed about the thigh but it was not inflated. He immediately packed the wound, inflated the cuff and turned the patient prone. The incision was extended, the popliteal artery and its branches were exposed and then, having secured control of the vessels, the tourniquet was released and he sutured the wound of the vessel. The operation of internal fixation of the fracture was then completed. The patient made an uneventful recovery. We think that the surgeon’s conduct in this difficult and indeed dangerous case was wholly admirable. Case Report: A 26 year old man sustained a tidy wound in the mid arm of his dominant upper limb. The brachial artery and median and ulnar nerves were transected. Spasm from the divided artery prevented copious bleeding and an opinion was taken from a vascular surgeon who considered that no action was necessary because the circulation to the skin of the hand was adequate. We were asked to see this patient at 8 months after his injury for consideration of repair of the nerves. They were exposed: the state of the proximal and of the distal stumps was such that no repair was worthwhile. This is a

Surgical Disorders of the Peripheral Nerves

tragedy because primary repair by any competent surgeon would have virtually guaranteed a high level of function. Matters are not helped by the imposition of changes, in reduction or withdrawal of medical staffing. Continuity of care has been abolished. A 33 year old man, who had previously served in the Armed Forces, was operated for reconstruction of a ligamentous injury at the knee. The operation concluded at 7 pm, and this is relevant for no member of the operating team was on call that night. The patient became aware of severe pain and increasing numbness of the foot 2 h after returning to the ward. At 4 h pain was intolerable, and resistant to opiates. The duty doctor was not a member of the orthopaedic department and took no action. The operating surgeon saw him early the next morning, (Saturday) and immediately took the patient to theatre where the leg was decompressed by open fasciotomy of all four compartments. The anterior compartment was infarcted and it had to be excised. Absence of a pulse in the presence of a fracture is an indication for exploration: pain, tense and tender swelling is an indication for decompression of a compartment even in the presence of a distal pulse. Sensible monitoring of intracompartmental pressure in the leg is useful. The correction of fixed ischaemic deformity is outlined in Chapter 13.

8.3 Skin The safe and regular closure of major defects in the skin is the third and most recent technical advance in the surgery of wounds. It rests upon the recognition that large areas of skin can be elevated on a pedicle of one artery and its vena comitans (as in the groin flap); that blood supply may pass to skin through perforating vessels from underlying muscle (the major myocutaneous flaps); or through deep fascia and intermuscular septa, (the fascio-cutaneous flaps) (Hallock 1992). McGregor and Jackson described the groin flap in 1972. This represented a real revolution for those brought up with the difficulties of split skin grafts or the cumbersome random or tubed flaps. This, the first axial pattern flap, remains exceptionally valuable in the emergency treatment of the hand and the distal forearm. During these years microsurgical techniques advanced so that there are now a large number of flaps which are in regular use for free tissue transfer. In 1986 Godina described the outcome in no less than 572 patients following ‘microsurgical’ reconstruction of the injured extremities, who were divided into three groups. Free flap transfer was performed within 72 h of the injury in Group 1, between 72 h and 3 months after the injury in Group 2 and later than that in Group 3. The failure rate of the flaps was 0.75% in Group 1, 12% in Group 2, and 9.5% in Group 3. Post operative infection occurred in 1.5% of Group 1, 17.5% of Group 2, and 6% of Group 3 patients. The average time to

Compound Nerve Injury

bone union was 6.8 months in Group 1, 12.3 months in Group 2, and 29 months in Group 3. The average of the length of hospital stay and the number of operations was far lower in Group 1. The evidence is decisive: delay only makes things worse. Godina’s contribution is a very great one, and his work is gracefully acknowledged in the review by Lister (1988) of emergency flaps. Lister and Scheker (1988) describe 31 emergency free flaps which were used for severe injuries to the upper limb. Twenty nine flaps survived, 27 of the 31 patients returned to work, 18 of them to their original employment. Gopal (2000) and his colleagues treated 84 cases of severe open fractures of the leg by debridement and excision of the wound extending to healthy tissue, stabilisation of the fracture and early soft tissue cover by a vascularised flap of muscle. The results are impressive and these workers observe that immediate internal fixation with healthy soft tissue cover is safe and that that most of the problems encountered were caused by delaying soft tissue cover beyond 72 h (Fig. 8.20). It is a considerable mistake for fracture or orthopaedic surgeons to decline knowledge of these advances. With vascular repairs, they must remain part of the repertoire of any accident surgeon. Surgical details, indications and complications are reviewed by Gilbert et al. (1990) who described flaps for the upper limb, and by Oberlin et al. (1994) for both upper and lower limbs. These last authors used a charming grading of between one and four for technical difficulty, akin to mountaineering terminology (or for the more sedentary reader, the Michelin star system). Grades one and two encompass those

Fig. 8.20  A 28 year old woman suffered a gunshot wound to the elbow destroying the brachial artery and the median nerve. These were repaired and skin cover provided by a free latissimus dorsi myocutaneous flap. Operation done with Professor Roy Sanders.

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flaps which have served us well and which do not need elaborate equipment nor extensive experience in micro-vascular work, neither do the pedicle flaps, admirably described by Mathes and Nahai (1979). Grades 3 and 4, on the other hand, are for the expert! One most important lesson is that nerves which have been repaired or which are embedded in scar require healthy, full thickness and unscarred skin cover. Nothing less will do (Fig. 8.21 a, b). With these lessons in mind we turn to the first group of ‘compound nerve injuries’.

Fig. 8.21  Secondary revision of repair of median nerve and brachial artery with full thickness skin cover. A 23 year old man sustained a penetrating missile wound to the left antecubital fossa which destroyed the brachial artery and median nerve. The artery was repaired in the field hospital, the median nerve grafted five days later and the wound covered by split skin graft. The vein graft thrombosed at about 48 h after repair and the wound became infected. The nerve did not recover and the patient experienced severe pain. 10 months later the split skin graft was excised (above), a large neuroma had formed at the proximal stump of the median nerve (seen below) and occlusion of the vein graft was confirmed. A free full thickness skin flap was inserted and the vascular pedicle was used to repair the brachial artery so restoring through flow. The median nerve was, again, grafted. Pain was relieved and Tinel’s sign progressed distally at the rate of 2 mm a day. By 22 months he had recovered accurate and rapid localisation to the tips of the thumb, index and middle fingers, vaso- and sudomotor function and recovery of the thenar muscles. His power grip, 60%, was due in part to a high median tendon transfer (Courtesy of Mr Roderick Dunn, Salisbury).

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8.4 Penetrating Missile Injuries Delorme (1915) then Inspector General of the Medical Services of the Armies of France outlined a method of treatment for shell and bullet wounds of nerves based on three principles: resection of scar until a healthy bed is secured; excision of damaged nerve until healthy stumps are reached; and tension free suture by adequate mobilisation and flexion of adjacent joints or grafting. His paper was heavily criticised. The verdict of history goes to Delorme and against his detractors. Tinel (1917) supported the proposals of Delorme adding ‘when the distance between the segments of the nerve trunk is too great to permit direct suture the only legitimate operation is nerve grafting as recommended by J and A Déjerine and Mouzon’. He further added ‘there is nothing but nerve tissue can serve as a conductor for regenerating axis cylinders’ and roundly castigated ‘mischievous’ operations such as lateral implantation, transplantation of a motor nerve into a sensory one and isolation of nerve by foreign body. Only the interposition of a ‘muscular-or better still, a fatty-layer’ between a nerve and callus or bony projection is permitted. It seems difficult to add to this. Owen-Smith (1981) and Omer (1991, 1998) point out that the effects of these injuries were well known in the nineteenth century. In 1894 Horsley (Adams 1982) showed that the wound was caused by transmission of energy from bullet to tissues and that the cause of tissue destruction was related to the velocity and spin of the missile. Woodruff (1898) introduced the term ‘cavitation’ for the damage caused at a distance from the wound track because of the creation of a cavity in the target into which air was sucked. Omer (1991) showed that neither energy transfer nor wound severity could be judged by the velocity of the missile alone. Indeed, he (Omer 1974, 1982) found, from a prospective study of 595 gunshot wounds, that spontaneous recovery occurred in 69% of both low velocity and high velocity wounds and that there was little difference in the time for recovery between the two groups. The Red Cross Wound Classification (Chapter 5) focuses the mind on the wound, not the weapon; Lindsey (1980) pithily condemns ‘the idolatry of velocity, or lies, damn lies and ballistics’. A number of writers have described the dangerous nature of the close range shotgun wound. Raju (1979) reported 39 shotgun wounds and 72 gunshot vascular injuries over 13 years, finding the shotgun injuries much the most severe. Shepard (1980) emphasised the significance of the mass of shotgun pellets in his series of 42 cases; so did Luce and Griffen (1978) who reported 77 cases of penetrating missile injuries of the upper limb collected over 7 years. Forty five of these patients had nerve lesions; the shotgun wounds fared particularly badly. Of the nine patients with combined injury to the brachial plexus and major vessels only one had a useful result and three came to amputation. We should not forget the lesson given us by McCready et al. (1986) who found good

Surgical Disorders of the Peripheral Nerves

recovery of the nerves after prompt decompression of haematomas compromising the brachial plexus in their series of 34 cases of open wounds of the subclavian and axillary vessels. The devastating effect of close range shot gun wounds was shown by Stewart and Kinnimonth (1993) from the Royal Infirmary in Glasgow, who treated 23 patients with 28 shotgun wounds to limbs in the course of 4 years. Their valuable paper uses the Red Cross Wound Classification. No limbs were amputated for vascular injury alone but three amputations in the lower limb were considered necessary because of the associated injury to sciatic or to tibial nerve. The functional outcome was disappointing in three more cases of shotgun injury to the forearm in which median and ulnar nerves had been torn. These were treated by early grafting, skin cover was achieved by free full thickness flap transfer. The authors comment ‘nerve repair was unsuccessful and left the patients with significant pain and disability two years after injury’. Stewart (Stewart and Birch 2001) recommends the term ‘massive energy transfer’ (MET) to describe those wounds, which with injuries caused by blast, do not fit conveniently into any method of classifying wounds (Fig. 8.22). Seddon (1975b) described the varying injury to a nerve following ‘through and through’ missile injuries. ‘the shock wave has caused more or less disturbance of function and structure in the nerve, ranging from fleeting paralysis (many combatants remark that the injured limb “went completely dead” for a few minutes) to neurapraxia and axonotmesis, and to internal disruption sufficient to cause moderate or severe intraneural fibrosis; all this short of actual severance of the nerve. The longitudinal extent of the fibrosis is a reflection of the distortion that the nerve has suffered and in this there is probably an element akin to traction’ (Figs. 8.23 and 8.24). Seddon thought that secondary repair is obligatory because only after a few weeks could the extent of intraneural fibrosis be recognised. In his series of 379 median and ulnar nerves damaged by missiles no less than 70% of them had been divided or partially divided. In commenting on nerves injured by missiles he said ‘patients who present with

Fig. 8.22  Shot gun blast to the neck. Bleeding from the first part of the subclavian artery was controlled through the transclavicular exposure.

Compound Nerve Injury

Fig. 8.23  Military rifle bullet wound. The entry wound, on the medial side of the knee was quite small, the exit wound was much larger. The nerve had not been transected, there was no compound nerve action potential detectable across the lesion but the lesion was not resected because of distal progression of Tinel’s sign. The nerve recovered.

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group of scientists in Oxford who closely collaborated with Seddon, then in charge of the Wingfield Morris special hospital. They included Young, Medawar, Holmes, Sanders, Gutmann and Guttmann. Young summarised some of this work in 1993. The first evidence of axonal transport was revealed. The rate of nerve regeneration, the effects of disuse, the regeneration of proprioceptors, the maturation of regenerated fibres under retrograde influence and nerve grafting were amongst the fields of enquiry. Much of this clinical and the laboratory work was assembled and analysed by the Nerve Injuries Committee under the chairmanship of George Riddoch and it appeared in 1954 in Report No. 282 from the Medical Research Council, ‘Peripheral nerve injuries’. The quality and the scope of this document remain unsurpassed. ‘Aids to the examination of Peripheral Nerve Injuries’ appeared in 1943 based on the work of Riddoch, Ritchie Russell, Learmonth and McArdle at Gogarburn Peripheral Nerve Injury Centre near Edinburgh. This slim volume is now in its 4th edition under the direction of Michael O’Brian. All clinicians should possess it; even better, they should use it.

8.4.1 Suture and Grafting During World War Two: The MRCR Evidence

Fig. 8.24  Transection of the median and ulnar nerves by a bomb fragment were treated by delayed primary suture (Mrs Webb, Birmingham). Neurolysis was carried out 10 weeks later. Recovery for both nerves was good.

complete paralysis require exploration anyway, because there is no other means of knowing whether the nerve has been completely severed. Discovering it to be in continuity is fortuitous. The debate then centres on finding reason why resection and suture should not be performed.’ The lessons learned from the First World War were implemented soon after the beginning of the second. Hugh Cairns, Professor of Surgery in Oxford, was put in charge of injuries to the nervous system. Five nerve injuries centres were established as part of the emergency medical service. The three in England were directed by Rowley Bristow, Platt and by Seddon; the two in Scotland by Learmonth and by Illingworth. In spite of the hazards of war and dictates of geography concentration of cases, continuity of treatment and supervision was very good. Much fundamental work was undertaken by a

Zachary (1954) set out the results of 1,441 sutures performed in the five Special Hospitals. The follow up was remarkably good, with 1,108 patients presenting for review at a minimum of 3 years after the operation. Zachary points out: ‘the lapse rate for patients suffering from radial nerve lesions was nearly twice as great as that for any other group (82 out of 195, 42%). Radial paralysis is very disabling: no victim of it who had passed through a nerve injury centre would be ignorant of the possibility of tendon transplantation if the result of nerve suture was disappointing. Therefore, there is a strong probability that in this group at any rate, some patients defaulted because they were well satisfied rather than because they were disappointed.’ The results were graded by strict, even stringent, criteria and close reading of the Special Report reveals some results which would be pleasing to the most exacting modern clinician. In the case of the common peroneal nerve Zachary considers that a patient who regains active extension and eversion of the ankle against resistance as only M1(3) because of persisting paralysis of the extensor muscles of the toes. Most recent publications consider that a patient able to walk without an orthosis in a normal shoe has a pretty good result. Zachary described some findings which are of general interest. (1) Many patients continue to improve for up to 5 years after operation. All must be followed for at least 3 years before assessment of recovery can be made. (2) Delay before repair is most harmful. (3) High velocity injuries are

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worse because of greater destruction of nerve tissue and also because more of these wounds are complicated by sepsis. (4) The more proximal the lesion the poorer the prospect of recovery. (5) About 50% of all cases of suture made a useful recovery by the exacting criteria used throughout the study. Three hundred and eighty four sutures of the ulnar nerve were reviewed at 5 years. Strong interosseous function was seen in 24% and useful recovery in 46% more. Recovery of interosseous function was at least useful in 78.5% of 141 low sutures of the nerve. There were 350 repairs of the median nerve. Ninety per cent of the high sutures (above elbow) regained useful grasp and a strong abductor pollicus brevis was found in one third. Useful sensation (S2+) was restored in 53%. Thirty eight per cent of patients regained some two point discrimination and lost any overreaction. The results of the 114 radial nerve sutures followed for a minimum of 5 years are particularly interesting: nearly 90% regained extension of the wrist and 61% regained some extension of the digits. Independent action for the thumb and the index finger was restored in 36%. The sciatic nerve was considered in terms of its two components, the tibial (132 cases) and the common peroneal (264 cases). Zachary seems to have been agreeably surprised by the results for the tibial nerve, with 56% of patients regaining powerful heel flexion and 80% showing some response to pin prick in the sole of the foot. Thirty six per cent of the common peroneal nerves recovered so that patients were able to walk without a brace or modified shoe, but 59% achieved this result when the level of suture was low, the delay short and the nerve defect small. There were 12 amputations following suture of the sciatic nerve because of deformity of the foot and ulceration on the sole: ‘amputation was performed for poor function of the limb and not primarily for poor neurological recovery’. Zachary also graded the recovery for 107 sutures of the sciatic nerve by the level of function. A good result implied no ulceration, no more than light pain, the ability to walk more than 1 mile and the ability to carry out work necessitating a fair amount of walking or standing. An excellent result meant that the patient could walk for 5 miles and could run, could carry out work requiring walking or standing and took no time off for at least 6 months, because of trouble with the leg. There was some discrepancy between neurological recovery and function: ‘eight patients with no recovery whatever had “good” function of the limb’.

8.4.2 Grafts Seddon (1954) described the results of 67 cases operated between January 1941 and October 1947. Nearly all of these were done at the Wingfield Morris Hospital, in Oxford. The outcome is analysed with the same precision that is a feature of

Surgical Disorders of the Peripheral Nerves

the memorandum as a whole. Twenty four main nerves were grafted using cutaneous nerves, by the method which Seddon described as cable grafting, perhaps a rather unfortunate term which has led to persisting misinterpretation since. As we have seen (Chapter 7) Seddon did not bundle the grafts together. The lesion of the main nerve was partial in six cases. These were unfavourable cases with large defects in nerves and frequent arterial injuries. The operations were successful in five of the six partial lesions and in eight of the eighteen complete lesions. There were four complete failures. Good recovery was recorded in one of five cases of repair by graft of the upper trunk of the brachial plexus; there was some recovery in a second case. A portion of a main nerve, usually from a proximal stump of an otherwise irreparable lesion was used to repair 15 median nerves. Useful function was restored in nine of these cases; there was no recovery at all in only two. Some results were remarkably good. In one case a 7 cm gap within the median nerve was bridged by using one half of the proximal stump of the nerve. The long flexor muscles had been destroyed. By 39 months the abductor pollicus brevis was graded at M4, there was recovery of sensibility without overreaction, fair localisation and two point discrimination averaging 7 mm. In another case (M.66) the proximal stump of a hopelessly damaged ulnar nerve was used to bridge a 7 cm gap in the median nerve. By 30 months the thenar muscles were graded at M3, there was recovery of sensibility and localisation without overreaction and two point discrimination lay between 15 and 20 mm. On the other hand the results using this method for repair of the trunk nerves of the lower limb were generally unsuccessful. Three out of the four nerve pedicle grafts succeeded. The successful case of grafting of the brachial plexus (patient Q.4) is, we think one of the first reported. Seddon (1975c) acquired enormous experience in the repair of war injuries to nerves, for in addition to the 379 cases of median and ulnar nerve repair he also described outcome in over 240 cases of missile injury to the sciatic nerve or its major divisions. Clearly, Seddon felt exploration was indicated in those cases with no clear evidence of clinical recovery as soon as the patient’s condition permitted. But Seddon used grafts for nerve repair at a time when this was not fashionable. The extensive experience of the military surgeons of the USA is brought together in the monumental work of Woodhall and Beebe (1956). On the basis of 3,418 nerve sutures in war wounds they said that: ‘delay in suture involves a loss of, on average, about 1% of maximal performance for every six days of delay’. Those clinicians, for there are some around, who countenance delay before dealing with injury to a main nerve might care to refresh their memories from the voluminous earlier published work. Omer has written extensively about peripheral nerves injured by penetrating missile wounds (1974, 1991, 1998); his works are required reading. Much of his work relates to

Compound Nerve Injury

the war in Vietnam. In 1974 he reported that only four from 34 grafts, followed for a minimum of 12 months, demonstrated return of functional activity but perhaps the period of follow up was rather short. He, with Eversmann (Omer and Eversmann 1994) came to the view that pedicle nerve grafting gave results superior to free nerve grafting. Omer (1974) sutured 83 nerves finding useful recovery in 40%. The worst group was the above elbow high velocity injury. Brown (1970) sutured 135 nerves in the upper limb; 44% of these regained useful function. The ulnar nerve fared worse but the continued long term study of the patients operated by Brown (Omer and Eversmann 1994) showed continuing improvement in function. Several cases of high repair of the ulnar nerve regained function in the small muscles of the hand at intervals exceeding two years after the operation. Omer (1998) says that: ‘the longest time elapsed before functional return was eight years after nerve suture. These well-documented late returns of neurological function to the intrinsic muscles of the hand are contrary to all results previously reported in the medical literature.’ The harmfulness of delay was emphasised by both Brown and Omer. Armed conflict within or between States continues and these have led to a number of significant contributions. Secer and his colleagues (2008) analysed 2,106 patients treated over the course of 40 years. Nerve injuries were equally divided between those caused by fragments and those caused by missiles. The median nerve accounted for 605 lesions, more than one quarter of the whole. 641 (30.4%) occurred in the lower limb. There were ruptures with separation of stumps or ruptures in continuity in 747 cases (35.5%), and partial ruptures in 191 nerves (9.1%). Lesions were recovering in 413 (19.6%). The most common cause of lesion was compression or entrapment within scar. There were 859 of these, 40.8% of the whole. Three main causes of nerve injury are identified: a shock wave leading to cavitation; affection from arterial injury, and direct impact upon the nerve. The characteristics of the lesion in continuity are described, and colour, consistency, and the state of the epineurial vessels are all pointers to the likelihood of recovery. Fibrosis was particularly severe in cases complicated by sepsis. Recovery was best for the tibial nerve, followed by the musculocutaneous and radial nerves. It was worst for injuries to the brachial plexus and the common peroneal nerve. The conclusion of this extensive work is important: earlier repair is more effective and there is a ‘strong correlation between functional recovery and relief of pain’. Gousheh (1995) relates his experience in the treatment of 369 injuries from the war between Iran and Iraq. Major arterial injury, false aneurysm or arterio-venous fistula complicated 74 of these. Using his own assessment Gousheh considered that results were good in 45 of 54 repaired spinal nerve elements, and in 86.5% of 107 cord elements. He found that repair of the ulnar nerve was worthwhile and concluded that results from repair in these injuries are better than those

325

caused by closed traction lesion. Gousheh et al. (2008) report 684 cases of injuries to the divisions of the sciatic nerve, incurred during the same war. 116 tibial nerves were repaired by graft, and 80 by direct suture. On occasion a segment of the common peroneal nerve or the ulnar nerve from an amputated limb was used. 308 lesions in continuity were extricated from scar or other entrapment and the general results for the tibial division were good. Powerful heel flexion returned in 86.3% of them and only a few cases were complicated by overreaction. 74 common peroneal nerves were grafted, 144 were sutured, and external neurolysis proved necessary in 272. Recovery for these nerves was remarkably similar to that found by Zachary. Useful dorsiflexion of the ankle returned in 46% of the grafts and in 41.7% of the sutures. The level of lesion was an important factor in outcome for both divisions. Gousheh and his colleagues observe that one reason for the vulnerability of the common peroneal nerve is that its vessels lie peripherally whereas those to the tibial nerve ‘lie in the crevices between the bundles’. The particular vulnerability of the common peroneal nerve is explored further by Hamdan et al. (2008) who studied no less than 1,463 civilians injured in Iraq over the course of 3 years. Ninety three per cent of these injuries were caused by bullets and 97% of the lesions occurred within the thigh. The tibial nerve was involved far less frequently; 64 cases were complicated by fracture of femur and/or arterial injury. Hamdan et al. refer to the tethering of the nerve above by the piriformis and found the nerve passing through the muscle in as many as one third of cases. The nerve below is tethered by the biceps and peroneus longus muscles. The nerve is smaller, it is endowed with less connective tissue and the blood supply is less rich than it is for the tibial nerve which is cushioned by the fat pad in the popliteal fossa and in the lower segment of the thigh. Roganovic and his colleagues from the University hospital in Belgrade offer extensive and important evidence drawn from experience in the recent Balkan wars. A paper describing 586 lesions of the ulnar nerve seen over three years, appeared in 2004 (Roganovic 2004). Operations were not performed in 181 of these. Bullets were responsible for just under 40% of the cases, fragment wounds for 60.9%. About one quarter of the nerves were ruptured in a different plane from the passage of the missile. Ruptures in continuity were characterised more by unusual colour, consistency, and poor circulation than they were by the usual neuroma formation: ‘such nerves were thinned, soft, “boil like”, or conversely, diffusely fibrotic especially if long-term local infection existed within the vicinity of the nerve’. There were 43 sutures and 85 grafts. Fifty six of 128 repairs restored material improvement in function, indeed the result was graded excellent in 10 cases. Deleterious factors include: the defect between the stumps; delay; and associated injury to the median nerve. A defect in the nerve exceeding 4.5 cm and a delay exceeding 5.5 months proved particularly deleterious. Roganovic points out that the

326

detection of a compound nerve action potential (CNAP) across the lesion is not necessarily associated with a good outcome. He draws similar conclusions from his study of 81 repairs of the median nerve (Roganovic 2005a). A high level injury, a gap exceeding 5.5 cm and a delay in excess of 4.5 months were materially deleterious to recovery. His study of the common peroneal nerve appeared in 2005 (Roganovic 2005b). No less than 702 cases were seen in the three years 1991 and 1994. The policy of emergency treatment in most of these cases included stabilisation of the skeleton by external fixation, early provision of good skin cover and approximation of the nerve stumps. Operations upon the nerve were performed in 472 cases; there were 157 repairs. Roganovic repeats his earlier observation, and it is an important one, that the nerve stumps were often found in different planes from the track of the missile and that they were: ‘sometimes grabbed by adjacent callus or abundant scar tissue’. Only 7 nerves could be sutured; grafts were necessary in 120. There was a high incidence of associated injuries: fractures in 45.9%, a major artery in 24.4%, and severe soft tissue injury in 24.8%. Results were useful in 57.4% of repairs where the gap was less than 4 cm. There were no useful results where the gap exceeded 8 cm. Useful function was regained in 47.9% of repairs performed within 4 months of injury but in only 3 of the 61 later repairs. Roganovic emphasises the importance of proper primary treatment of the wound and he recommends identification and formal tethering of the nerve stumps. In all, about one third of these repairs restored function, a proportion similar to that recorded by Zachary and by Seddon. Roganovic et  al. (2007) discuss the association between false aneurysm and peripheral nerve lesions. 2,239 injuries to peripheral nerves were observed in the course of three years; 300 of these (13.4%) were complicated by arterial injury. There were 90 cases of false aneurysm which were directly associated with an adjacent nerve lesion in 22. Four of these were located in the axillary artery, seven in the brachial, three in the femoral and eight in the popliteal artery. The severe pain presenting in ten patients responded to correction of the arterial injury and the lesion of the nerve. Roganovic and his colleagues make this very significant observation: the lesion of the nerve progressively deepens with time and if a delay of more than 3–5 days is permitted a conduction block of the nerve is transformed into a much deeper injury. David Kline and his colleagues in New Orleans have acquired a great experience in the treatment of civilian gunshot injuries. Kline and Hudson (1995) describe over 150 cases of wounds to the lumbo sacral plexus, the femoral nerve, the sciatic nerve and its divisions. In 1989 David Kline (Kline 1989) reported 140 wounds of the brachial plexus (90 operated cases), and in nearly one third of these there was major vascular injury. 125 nerve elements were repaired and recovery was useful for C5, C6 and for C7 lesions, and for lesions to the upper and middle trunks and the posterior and

Surgical Disorders of the Peripheral Nerves

lateral cords but results of repairs of C8 and T1, of the lower trunk or the medial cord were generally rather poor except in children. Kline emphasises the role of detecting conduction across the lesion. Compound nerve action potentials (CNAP) were detected in 76 such lesions, and these were left alone. There was useful spontaneous recovery in nearly all of these. The later paper from New Orleans, (Kim et  al. 2004) provides more information about 118 cases of gunshot wounds to the brachial plexus. 156 elements were repaired. Recovery was good in 14 of the 21 sutures and in 73 of the 135 grafts. Kim and his colleagues offer clear indications for operation after such injuries: the presence of causalgia or other severe pain; suspected or proven arterial injury or false aneurysm or fistula, and the failure of progression towards recovery for lesions of C5, C6 and C7 or their derivatives. It is possible to offer some general observations from these publications which together provide information about thirteen thousand cases of penetrating missile wounds. The first operation to the wound itself is most important; arterial injuries must be treated and sepsis must be prevented. General factors mitigating against the likelihood of recovery include: delay before repair; extensive damage to the nerve, to the adjacent soft tissues and to the skeleton; the presence of arterial injury, and the level of the lesion. It is clear too that some nerves do particularly badly; amongst these the common peroneal nerve heads the field. We continue to use the admirable operations of nerve pedicle transfer developed by Strange (1947) for otherwise irreparable injuries of median and ulnar nerve and the analogous operation developed by MacCarty (1951) for otherwise irreparable injuries to both divisions of the sciatic nerve. These methods are described in Chapter 7.

8.4.3 Experience from St Mary’s and the Royal National Orthopaedic Hospitals Between 1975 and 2000 we operated on 117 patients and repaired 116 ‘elements’. The indications for operation were: 1. In emergency – for severe wound and /or bleeding 2. Aneurysm or arterio-venous fistula with nerve lesion 3. For severe pain 4. For deep defect in a nerve or nerves The injuries were complicated by wounds to major arteries in 41 patients.

8.4.4 The Brachial Plexus Stewart (Stewart and Birch 2001) has studied 58 injuries of the brachial plexus, 51 operated cases, and his analysis of the

Compound Nerve Injury

327

different types of missile injuries is particularly helpful. He recognised three groups: 1. Bullet wound, usually from the military rifle or machine gun (32) 2. Fragment, from explosion shell or grenade (11) 3. Blast from close range shot gun wound (15) There was a high incidence of associated injuries of adjacent structures which had been treated by operation before referral. Major vascular lesions (24%) and chest injuries (38%) predominate. Emergency neurovascular repair had been performed in three cases. Injury to the spinal cord occurred in three patients and two others, with complete plexus lesions, had intradural injury and a Brown Séquard syndrome. The Red Cross Wound Classification was used to score, retrospectively, the features of each wound. The wounds were graded according to the amount of tissue damage: grade 1, low energy transfer (LET); grade 2, high energy transfer (HET); and grade 3, massive energy transfer (MET). The wounds were then typed according to the structures involved, soft tissue, vital structures or fractures. The nominal category of the wound was derived from a combination of the grade and type to give an indication of the complexity and severity. Shot gun blasts caused complex HET or MET wounds with severe and diffuse neurological injury. Bullets generally cause HET wounds but there were fewer disruptions of the plexus, most were single nerve injuries. Fragments usually caused small LET wounds. The indications for further operation were, in order of priority, known or suspected vascular injury (16), severe and intractable pain (33), and persistent deep loss of function in a major nerve trunk or trunks (51). The seven patients showing recovery were not operated. One of these suffered from causalgia but he experienced spontaneous remission some months after injury, a phenomenon described by Barnes (1954). The neurovascular axis was usually approached by the exposure of Fiolle and Delmas, but the transclavicular approach (Chapter 7) was used in three patients with

arterial injury. False aneurysms or arterio-venous fistulae were repaired in 13 patients. The first arterial repair was revised in two more. Normal flow was restored in 13 cases. One hundred and three damaged nerve elements were encountered. Some nerves were wholly transected, others partially so. Others showed the effects of displacement and traction, lying in a tortuous path resembling a ‘barley sugar’ (or Jacobean table leg) appearance of a traction lesion. The diagnosis for transected nerves did not present a problem but the lesion in morphological continuity certainly did. The distinction between degenerative lesions of favourable from those of unfavourable prognosis rested on the demonstration of intact bundles traversing the lesion, the detection of distal muscular contraction from stimulating the nerve proximal to the lesion and the presence of compound nerve action potentials (CNAP) traversing it. Examples of prolonged conduction block were seen in cases in which nerve trunks were displaced or compressed by an expanding haematoma or false aneurysm. In these, the diagnosis was established by demonstrating persisting conduction in the distal trunk. The ruptured nerves were grafted; external ‘neurolysis’ was used for nerves which were constricted or distorted in scar tissue. A fine catheter was placed adjacent to the plexus in patients presenting with severe pain, allowing infiltration of local anaesthetic for up to five days after operation. One or more elements of the plexus were repaired in 36 patients. Repair of the spinal nerves or of the upper, middle and lower trunks produced good or useful results in 10 from 14 patients. Repair of the divisions, cords or terminal branches of the plexus produced good or useful results in 16 of 22 patients. Three of the six repairs of the medial cord or ulnar nerve were rated as useful or better. The result was poor in all cases where there was an injury to the spinal cord. ‘Neurolysis’ or, as it should be termed, decompression, was generally useful and significant improvement in neurological function was seen in the 13 patients after repair of a subclavian or axillary aneurysm or fistula (Table 8.7).

Table 8.7  Penetrating missile wounds of the brachial plexus. Outcome Results of repair of 56 nerve elements in 36 patients Spinal nerve trunks Cords, nerves No. of No. of No. of No. of nerves patients nerves patients

Results of decompression of 47 nerves in 23 patients Spinal nerve trunks Cords, nerves No. of No. of No. of No. of nerves patients nerves patients

Good

2

2

1

1

13

7

5

4

Useful

12

8

20

15

11

3

15

7

Poor

15

4

4

4

0

0

0

0

Unknown

0

0

2

2

0

0

3

2

29 14 27 22 24 10 23 13 Results of repair were poor in five of the cases of spinal cord lesion. Pellets or fragments in the spinal canal were evident in these poor results Drawn from Stewart and Birch (2001).

328

8.4.5 Pain Stewart recognised four syndromes in 35 patients presenting with severe pain (see Chapter 12). Ten patients presented with causalgia, which was caused by aneurysm or fistula in five. All of these patients experienced rapid improvement or abolition of their pain after operation which included repair of ruptured nerves in eight cases. Sympathectomy was performed twice, in earlier years. This method was abandoned after we realised that correction of the vascular lesion, extrication of the nerves and repair of divided nerves with prolonged infusion of local anaesthetic after the operation achieved the desired result. All 19 patients with neurostenalgia experienced very great improvement after operation. The rapid relief of neurostenalgia after liberating nerve trunks from entrapment in scar tissue or callus, or after removal of a missile fragment, is characteristic. In all of these cases the nerve trunk was intact and the lesion was neurapraxia, or at worst, axonotmesis. In neurostenalgia the nerve is, in some way, irritated, tethered, compressed or ischaemic and treatment of the cause relieves pain. On the other hand, post traumatic neuralgia caused by rupture or partial transection of a nerve in four patients proved more difficult. Two patients experienced improvement in their pain, two did not. Case Report: A 21 year old man sustained multiple LET gunshot wounds. Emergency surgery included a right hemicolectomy, right thoracotomy and enucleation of an eye. A right supraclavicular wound was not explored. He discharged himself from hospital, but presented 6 weeks later with severe pain and profound loss of function in his right arm and hand. There was no major neurological deficit. The bullet was lodged in the transverse process of the sixth cervical vertebra; the pain was improved for about 12 h by blockade of the stellate ganglion. Digital subtraction angiography showed no evidence of vascular injury (Fig. 8.25). At operation, a bullet was found to be embedded in the scalenus anterior muscle, adjacent to the seventh cervical nerve. There was no evidence of direct injury to the spinal nerve, or to the trunks of the plexus, but considerable fibrosis surrounded the middle and lower trunks of the subclavian artery. The bullet

Surgical Disorders of the Peripheral Nerves

adjacent to the seventh cervical nerve was removed and a cervical sympathectomy was carried out. There was dramatic relief of pain after operation and at follow up at two years there was good function. The bullet adjacent to C7 caused diffuse, severe pain in the arm and functional disability. At the time, the pain was considered to be causalgia, and a sympathectomy was undertaken because of the good response to the sympathetic block. In retrospect, we considered the pain was probably a neurostenalgia; its dramatic relief with recovery of function should probably be attributed to removal of the bullet adjacent to the spinal nerve. Case Report: A 24 year old woman sustained an MET supraclavicular wound from a shot gun blast to her left brachial plexus with rupture of all five spinal nerves and a Brown-Séquard syndrome (Fig. 8.26). Within weeks of her injury she gave a clear description of post traumatic neuralgia. At operation, 2 months after the wounding, all five spinal nerves were grafted. Her pain remained intense for 6 months but it settled after 14 months. Two years after injury there was some recovery of finger flexion, the sternal head of pectoralis major, of deltoid, latissimus dorsi and triceps. Tinel signs were observed for the median and ulnar nerves in the middle of the forearm, and for the radial nerve, at the elbow. The injury to the spinal cord had improved considerably, but there was still some clinical evidence of Brown Séquard syndrome at four years after injury. Further recovery was largely confined to C8 and T1, with useful function in the sternal head of pectoralis major, triceps and flexor digitorum superficialis. Transfer of the third and fourth intercostal nerves to innervate serratus anterior achieved power in that muscle of MRC grade 5, and there was no longer a requirement for flail arm splints. Protective sensation, comprising warm perception, delayed pressure sense and some pin prick sensation, was present below the elbow. This was an unexpected and encouraging result after a MET wound. Since there were no pellets within the spinal canal, the Brown Séquard syndrome was thought to reflect an injury to the brachial plexus. Interruption of vessels accompanying the lower roots of the plexus may have provoked a partial and perhaps transient episode, affecting the ipsi lateral part of the cord. We consider that repair of the plexus was at least partially responsible for the relief of her pain.

8.4.6 The Peripheral Nerves

Fig.  8.25  Causalgia caused by a bullet which was embedded in the transverse process of C7.

Our earlier experience is summarised in Table  8.8. Severe pain was the presenting symptom in more than one half of patients. Causalgia was recognised in three cases of upper limb injury and in four more cases within the lower limb. Neurostenalgia, from embedded pellets or retained foreign bodies within the nerve trunk or displacement by the sac of a

Compound Nerve Injury

329

Fig. 8.26  Close range shot gun blast caused massive destruction of the paravertebral muscles. There were no pellets within the spinal canal. Table 8.8  Penetrating missile wounds of the peripheral nerves in the upper and lower limbs 1975–2000. Wound type No. of Nerves Vessels Fractures patients repaired repaired

Skin loss (flaps)

Fragment

15

13

8

5

3

Bullet

26

24

10

17

4

Blast

25

23

10

16

10

Total

66

60

28

38

20

Nerves transected: level of lesion Upper limb Median

Lower limb 18

Arm

Forearm

Hand

11

2

5

Sciatic

17

Hip

Thigh

Knee

Leg

7

9

1

0

Ulnar

18

13

2

3

Femoral

3

2

1

0

0

Radial

9

6

2

1

Tibial

7

0

4

3

0

Musculocutaneous

3

3

0

0

Common peroneal

10

1

3

5

1

haematoma or aneurysm was seen in the remainder. Pain was relieved by correction of the cause (Fig. 8.27). Bullet wounds are more likely to be associated with a fracture, and the treatment of these is often difficult. In seven cases where external fixation had been adopted we were faced with the problems of non union and sepsis. There must be no short cuts in the emergency treatment of the wound; debridement must be thorough and adequate irrespective of the chosen method of fixation to reduce the risk of sepsis.

Case Report: A 17 year old boy was shot in the arm with a Kalashnikov bullet. External fixation was used to stabilise the humerus. We first saw him at seven days, with deep sepsis in the arm which extended to the pin track site. Salmonella Type 5 was cultured from the fracture site, which was excised and packed with antibiotic impregnated cement beads. Two weeks later repair of the brachial artery and of the median and radial nerves was possible. At 3 months the non union was treated by internal fixation and interposed bone graft. The facture united; there was, ultimately, useful function in the hand.

330

Surgical Disorders of the Peripheral Nerves

Fig. 8.27  Sacular aneurysm from a bullet wound to the subclavian artery which was repaired using a Dacron graft (George Bonney 1964).

8.4.7 Recent Experience Nearly all service men and women injured in Iraq or Afghanistan pass through the Defense Medical Rehabilitation Centre at Headley Court and those with nerve injuries are seen in a dedicated clinic and investigated using the methods described in Chapter 5. Information is entered on the compound nerve injury form (see Fig. 5.80) suitably modified to the study of war wounds. The methods of grading results have been described in Chapter 4 and later in this chapter. Incidence, cause and distribution: The incidence of nerve injuries is about 12% which is higher than that seen in earlier conflicts. One explanation for this is the lower mortality amongst the wounded in current conflicts. This stands at 88.2%, compared to 76.4% for those wounded in the Vietnam war and 69.7% for those injured in World War II (Eardley and Stewart 2010). The incidence of nerve injuries is higher

in the lower limb than it was in the MRC Report because of the preponderance of wounds caused by blast or explosion. Most of the lower limb injuries occurred in massive energy transfer wounds (Table 8.9). The lesion of the nerve: the lesions of the nerves have been grouped according to the predominant quality of that lesion. Apart from those cases where the nerve was torn apart there were few pure lesions. Two patterns of conduction block have been recognised. The first is caused by distortion, displacement and traction upon the nerve by the passage of a nearby bullet or fragment. The second is caused by blast and recovery is prolonged and more complete for larger nerve fibres (see Chapter 3) (Table 8.10). Pain: No case of causalgia required active treatment although several patients related a history consistent with the diagnosis and its spontaneous resolution. Post traumatic neuralgia persisted in four patients with lesions to the superficial

Compound Nerve Injury

331

Table 8.9  Ballistic peripheral nerve injuries by nerve (a) and level (b) 232 nerves in 91 patients. (a) Upper limb (133 nerves) Above clavicle

Below clavicle

Buttock/hip Thigh and below

Ulnar

29

  High: Above FCU

10

Cervical sympathetic chain

1

  Inter: Above wrist

17

Spinal accessory

3

  Low: Wrist and Hand

2

C5

7

Radial

22

C6

8

  High : above triceps

5

C7

7

  Inter: above PIN

14

C8

6

T1

4

Dorsal scapular

1

Suprascapular

6

Nerve to serratus anterior

1

Circumflex

6

Musculocutaneous

4

Radial

22

Median

25

Ulnar

29

Lower limb (99 nerves) Pelvis

Table 8.9  (continued)

S1

1

S2

1

S3

1

Inferior gluteal

5

Inferior gluteal

5

Femoral

3a

Tibial

38

Common peroneal

39

Sural

4b

Saphenous

2b

(b) Level by main nerves Common peroneal nerve

39

  Buttock

7

  Thigh

7

  Knee

16

  Leg

8

  Ankle and foot

1

Tibial

38

  Buttock

7

  Thigh

6

  Knee

14

  Leg

8

  Ankle and foot

3

Median

25

  High: above superficial flexor branch

13

  Inter: Between superficial flexor branch and wrist crease

10

  Low: Wrist and Hand

2

  Low: PIN 3 a The three femoral nerves were injured below the branches to ilio psoas muscle. b Sural and saphenous nerves were injured in the leg. Table 8.10  The cause, and significant associated injuries at the level of nerve lesion: 216 nerves (85 patients). Cause (216 nerves) Associated injury (85 patients) Explosion or blast

150 (69%

Main vessel

27 (31.5%)

Penetrating missile wound from bullet or fragment

66 (31%)

Fracture

48 (56.5%)

radial, the sural or saphenous nerves. Post traumatic neuralgia complicated two cases of below knee amputation in which the neuroma had become adherent to the scar. Pain was abolished by revision of the stump. Neurostenalgia, caused by the strangulation of a nerve by fibrosis deep to split skin grafts was more common (11 patients) and this was the single most important indication for second operation which involved the excision of split skin graft and replacement by a full thickness skin flap. Recovery: Post ischaemic fibrosis was identified in only one patient. In this case emergency repair of the brachial artery maintained flow for about 2 days before thrombosing. The moderate fibrosis of the flexor muscles of forearm was corrected by serial splinting and stretching. In two patients direct damage to the flexor muscles of the leg required subsequent step elongation of the affected tendons. The nerves: Recovery for the nerves was graded by the methods set out in Chapter 4 and later in this chapter (Table 8.11). Recovery was good in all cases of conduction block and in most of the examples of axonotmesis. Recovery in six of the nine primary sutures was good (three sciatic, one median, one ulnar, one tibial) and was poor in only one case of suture of a radial nerve. Recovery was good in 7 of the 26 grafts, it was poor in 10. Results in the three cases of direct muscle neurotisation and in the one case of frozen muscle graft were fair. The quality and speed of recovery in the successful primary sutures was remarkable and these included three repairs which were performed in the field hospital. Decompression and neurolysis proved necessary in 23 nerves and in 10 patients this involved replacement of scar by a full

332

Surgical Disorders of the Peripheral Nerves

Table 8.11  The nature of the lesion in 211 nerves and the outcome of that lesion in the 199 nerves adequately followed. The lesion Outcome Conduction block (neurapraxia)

75 (36%)

Good: including 13 repairs and 21 neurolyses

133 (67%)

Favourable degenerative (axonotmesis)

81 (38%)

Fair: including 15 repairs and 2 neurolyses

34 (17%)

Unfavourable degenerative (neurotmesis)

55 (26%)

Poor: including 11 repairs

32 (16%)

thickness skin flap. There were 21 good results. Early relief of pain and rapid recovery of function was evident in all patients following revision of the scar. Ramasamy and his colleagues (2009) conclude that: 1. Loss of sensation in the sole of the foot is not an indication for amputation because of the high incidence of prolonged conduction block or axonotmesis of the sciatic or tibial nerves. 2. Proper treatment of the wound at the first operation with restoration of circulation and perfusion, with stabilisation of the skeleton together with a rigorous approach to the control of pain enables early repair of divided nerves. 3. Neurophysiological evidence is valuable in confirming the level and the depth of lesion. Recovery is best monitored by clinical examination and, in particular, by the behaviour of the Tinel sign. Persisting neuropathic pain is a strong indication for exploration of the nerve. 4. Nerves and vessels must be protected by full thickness healthy skin. The condition of the patient and of the limb often precludes elaborate and lengthy operations for the purpose of skin cover. In these cases its seems better to defer the nerve repair until that has been done. (Seddon 1954) (Figs. 8.28 and 8.29).

Fig. 8.28  Bilateral lesions of the median nerve from penetrating missile wounds. The right median nerve and brachial artery were repaired by Mr Power (Birmingham). Recovery was good. The injury to the left median nerve was accompanied by destruction of the flexor muscles and fractures. Recovery was poor.

8.5 Neurovascular Injuries: Amputation Revascularisation In these injuries the prognosis of the nerve is determined above all else by successful restoration of arterial perfusion. The most extreme example is, of course, the amputated part. Malt (1964) and Chen, Ch’en and Pao (1963) successfully reattached an amputated hand. Komatsu and Tamai (1968) reported the first successful reattachment of amputated thumb and Cobbett (1969) the first successful free transfer of a great toe to replace a lost thumb. Buncke, Buncke and Valauri (1991) reviewed the technical developments which permitted these achievements and indeed were spurred on by them. Chief amongst these was

Fig.  8.29  Penetrating missile wound to right forearm destroyed the flexor muscles and damaged both median and ulnar nerves. The median nerve was grafted and a lateral thigh flap (Mrs Webb Birmingham) was performed at 5 days. Both nerves recovered. There was never, at any time, pain. There was a partial lesion of the median nerve in the left forearm.

the regularly successful repair of vessels of 2 mm in diameter or less, by interrupted sutures of 9×0, 10 × 0 or 11 × 0 filaments on needles of 2–4 mm in arc and 50–100 microns in

Compound Nerve Injury

calibre. Kleinert and colleagues were amongst the first to describe these techniques in limb salvage (1963). Chen, Meyer, Kleinert, Beasley (1981) reported the results of a co-operative study between Shanghai, Louisville and Zurich in 181 cases. The best results followed replantation of limbs amputated through the distal forearm and wrist with useful results in 79% to 83% of cases; the worst results were from replantation of the limb amputated or avulsed at shoulder level. Avulsion injuries fared very much worse than guillotine or crush injuries. The extent of vascular damage is, of itself, no barrier to successful replantation. In one of our cases a 28 year old woman threw herself under a train in an attempt at suicide. The dominant hand was amputated at the junction of the distal one third and proximal two thirds of the forearm. The gap between healthy vascular stumps ranged from 5 to 12 cm and five vein grafts were used for the radial and ulnar arteries and for three veins. Primary suture of nerves was possible because of bone loss of about 3 cm. Circulation was restored and by two years recovery for the median nerve was fair and for the ulnar nerve good (Fig. 8.30). The function of the hand was limited by the poor excursion of long tendons from extensive disruption of the muscle bellies but this result, together with those from two other successful replantations of the amputated hand performed between 1979 and 1982 proved to our satisfaction that primary suture even in these most severe cases gave results far superior to those following delayed repair

Fig. 8.30  Replantation of a hand amputated through the forearm by a railway wheel. Recovery of median and ulnar nerves was good. A subsequent free skin flap was put in by Mr David Evans. The function is shown before reconstruction of long flexor and extensor tendons.

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Failure to restore flow through a main axial vessel is almost always followed by muscle fibrosis to some degree; in the lower limb the effects are catastrophic. But there is a generally depressing effect on nerve recovery when the lesion is associated with rupture of the adjacent artery. Shergill (Shergill et  al. 2000) provided evidence about the deleterious effect of arterial injury in his study of 260 repairs of the radial nerve. Thirty five out of the 55 repairs in cases of associated vascular injury failed, that is very nearly two thirds. Osborne (Osborne et al. 2000) came to a similar conclusion in his study of 85 repairs of the musculocutaneous nerve. We shall return to these papers later in this chapter. Incised wounds of nerves and vessels in the limbs are best treated by primary repair. Failing that urgent repair of the artery with an early return to the nerves is nearly as good.

8.5.1 The Brachial Plexus The tidy wounds from knife, glass and scalpel are amongst the most rewarding of all nerve injuries to repair. When the opportunity for repair within hours or days of injury is grasped, the results for C5,C6 and C7 wounds are excellent; better by far than equivalent results even for early repair of more distal nerve trunks ruptured by traction injuries. They are worthwhile for C8 and T1 too. We emphasise that in virtually no other nerve laceration is the harmfulness of procrastination so clearly shown as in the supraclavicular stab wound. On the other hand the nature of the wound is such that other and more pressing problems frequently arise. Setting aside the cases of damage by scalpel there are three distinct patterns. When the blade or bottle is thrust from above down (as it was in Hector’s case) the lower trunk, subclavian vessels and lung are damaged. Such wounds may be as rapidly fatal as they were for the Prince of Ilium. When the blade is thrust towards the face or neck the fifth, sixth and seventh cervical with phrenic nerves are damaged: in addition to the jugular and carotid vessels, the trachea and the oesophagus are at risk. However in the cases coming to us the vertebral body shields the viscera, the knife point glides laterally, severing the spinal nerves close to their exit from the intervertebral foramina. Lastly, the lateral thrust divides the upper and middle trunks, the nerve to serratus anterior and the accessory nerve. The temptation to suture the severed nerves directly should be resisted. Grafts are better, even if only half a centimetre in length. Some examples follow: Case Report: A 26 year old man was stabbed in the neck. The internal jugular vein was ligated by the receiving surgeon who gave us the opportunity to repair the neural lesion within 36 h. The fifth, sixth and seventh cervical nerves had been severed close to their foramina: the phrenic nerve had also been severed. Twenty four grafts were used to repair the

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Surgical Disorders of the Peripheral Nerves

Fig. 8.31  The outcome 3 years after repair, 36 hours after injury, of stab wound of right C5, C6 and C7 and the phrenic nerve.

defect of 2 cm. By three years the only defect at the shoulder was lateral rotation which was restricted to 40° by capsular contraction. Sensation in thumb, index and middle was good without hypersensitivity. The power of deltoid, biceps, triceps and wrist extension was 80% of the uninjured side: the phrenic nerve recovered, there was accurate localisation of touch with two point discrimination less than 8 mm. in the thumb, index and middle fingers (Fig. 8.31). Case Report: A 21 year old nurse was assaulted and stabbed on her way home from duty in her Accident and Emergency Unit. Mr Maelor Thomas (Kings College Hospital) transferred her to us so that repair was performed within 24 h from injury. The knife had severed the upper and middle trunks and the nerve to serratus anterior. Nineteen grafts were used to bridge the defect of 1 cm. At four years this patient considered function in her upper limb to be normal. Measured power of serratus anterior, of the muscles of the shoulder, arm and forearm were MRC Grade 5: power grip in the afflicted (dominant) hand was 90% of the uninjured hand. Two point discrimination sense was 6–8 mm in the median territory of the hand. Early recovery of sympathetic function was a striking feature. Case Report: A 22 year old man was stabbed in the neck with a broken bottle and clearly remembered the downward thrust of the weapon which entered the neck just above the medial one third of clavicle. At emergency exploration

copious bleeding from the offsets of subclavian vessels was controlled. The seventh and eighth cervical nerves were severed with about 50% of the sixth cervical nerve. The glass had scored the first rib, lacerating the pleura. Sixteen grafts were used in the repair. At two years the one significant defect of function was thumb opposition which was mitigated by muscle transfer. Power grip for the whole hand was 85% of normal, pinch grip between thumb and index 75% of the uninjured (dominant) side. There was no pain and no serious sensory deficit (Fig. 8.32). A striking feature of these and of other cases or urgent repair of stab wounds is the speed of recovery, the absence of pain and a level of recovery superior to repair of more distal wounds of trunk nerves. Stab wounds involving the infraclavicular plexus often cause torrential bleeding. This can be reduced by firm pressure to the wound and by compression of the subclavian artery where it crosses the first rib (Guthrie’s manoeuvre) (Fig. 8.33).

8.5.2 The Closed Infraclavicular Lesion It is perhaps in the case of the traction lesion of the infraclavicular brachial plexus that the deleterious effect of

Compound Nerve Injury

Fig. 8.32  The outcome at 2 years after repair, on the day of injury, of a stab wound of left C6, C7 and C8.

Fig 8.33  The outcome 2 years after repair, on the day of injury, of a stab wound of the circumflex, musculocutaneous and radial nerves, and of the axillary artery. A flexor to extensor transfer was performed at 9 months.

arterial injury and the profoundly harmful effect of delay before nerve repair is most clearly expressed. This is among the worst of all true peripheral nerve injuries. It is

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characterised by the violence of the cause of the lesion, by the high incidence of rupture of the subclavian or axillary arteries (about 30% of our cases) and by the complexity of the nerve lesion. It is common to find nerve trunks ruptured at different levels up and down the limb, and it is not rare to find them avulsed from muscle bellies. The distinction according to level is to some extent artificial. There is overlap between the supraclavicular, the retroclavicular and the infraclavicular injury in closed traction lesion, with double lesions of supraclavicular lesions combined with more distal ruptures in about 10% of cases. Two patterns can be discerned. The first, which is more common, is caused by violent hyperextension at the shoulder. There is almost always a fracture of shaft of the humerus or injury to the gleno humeral joint; the incidence of vascular injury is high; the level of proximal rupture is deep to pectoralis minor which acts as a guillotine on the neurovascular bundle. The second pattern is even more severe and even more dangerous. In these injuries the forequarter is virtually avulsed from the trunk. There is disruption of the anterior arch of the shoulder girdle. The subclavian artery suffers and it is usually torn in its first or second part. There is usually avulsion of the eighth cervical and first thoracic nerves which is combined with ruptures of the cords of the plexus more distally. The forequarter drops down and away from the trunk because of the savage disruption of musculo-skeletal supporting elements. There is often a lesion of the spinal accessory nerve and of the nerve to serratus anterior. There is, almost always, a phrenic palsy. There must be no delay in the treatment of these limb and life threatening injuries. Restoration of ventilation and control of bleeding are critically important and robust stabilisation of the injury to the skeleton is necessary to enable repair of the main artery and , if circumstances permit, the main nerves. Guy Broome (Carlisle) demonstrated one such case at the first meeting of the British Plexus Club in Warrington in 2006. The patient, a pedestrian, was knocked down by a car and sustained a ‘floating shoulder’ with fracture/dislocation of the acromio-clavicular joint and complex fracture of the glenoid and the scapula body. These were rapidly stabilised before successful repair by vein graft of the rupture of the third part of the subclavian artery. A rupture of the lateral cord of the brachial plexus was then primarily grafted. Perfusion was restored, there was no ischaemic fibrosis of the forearm muscles, the repair of the lateral cord was successful and this, with good spontaneous recovery through the traction lesion of the medial cord, permitted later successful flexor to extensor transfer. The gleno-humeral joint was arthrodesed 15 months after the injury. The patient, now at work, is free of pain and has a useful arm (Fig. 8.34). Of course the overwhelming priority is to repair the vessel and it may not be feasible to deal with the nerve injury at the same operation (Fig. 8.35). The injuries to the nerves in these cases are extremely complex. It is common to find nerve trunks ruptured at

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Surgical Disorders of the Peripheral Nerves

Fig.  8.34  Incomplete avulsion injury of the right forequarter. The shoulder girdle was smashed, and the first part of the axillary artery ruptured (above left). The lateral cord was ruptured (above right). The

function at 2 years is shown below. The gleno humeral joint was arthrodesed (Courtesy of Guy Broome, Carlisle).

different levels up and down the limb; it is not rare to find them avulsed from muscle (Figs. 8.36 and 8.37). The advantages of urgent repair of the vessel and of the nerves are overwhelming. They include ease of identification of ruptured structures; the use of the nerve stimulator to detect more distal nerve injuries and the ability to diminish the gap between nerve stumps, which retract widely after rupture (Fig. 8.38). The exposure of Fiolle and Delmas is ideal (see Chapter 7). Cavanagh et  al. (1987) revie