539865 research-article2014
JHS0010.1177/1753193414539865The Journal of Hand SurgeryBirch
JHS(E)
Review Article
Timing of surgical reconstruction for closed traumatic injury to the supraclavicular brachial plexus
The Journal of Hand Surgery (European Volume) 2015, Vol. 40E(6) 562–567 © The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/1753193414539865 jhs.sagepub.com
R. Birch Abstract While it is widely accepted that cases of traumatic injury to the brachial plexus benefit from early surgical exploration and repair, with results deteriorating with long delays, policies vary regarding the exact timing of intervention. This is one of a pair of review articles considering the clinical issues, investigations, and surgical factors relating to management of injuries to the supraclavicular brachial plexus, as well evidence from experimental work and clinical outcomes. In this article Professor Birch argues for early exploration of the brachial plexus as the optimum both to delineate the pathology and undertake reconstructive surgery. Keywords Brachial plexus injury, nerve repair, timing of surgery Date received: 22nd June 2013; revised: 30th September 2013; accepted: 16th October 2013
Introduction Subcutaneous injuries of the plexus must be regarded as serious injury either with or without operative interference. The number of spontaneous recoveries is exceedingly small and it is extraordinary how many patients have been allowed to progress to a hopeless state without operation and how many are not operated on until months have elapsed. In view of the gravity of the lesion, of the resulting disability and of the occasional intractable neuralgias, surgeons should insist on resort to operation, if not immediately, at least as soon as it can be demonstrated with reasonable certainty that spontaneous recovery is improbable. An excellent working rule is that of Sherren (1906) that all subcutaneous injuries which give reactions of degeneration at the end of ten days should be submitted to operation. Frazier and Skillern, 1911
There is a long history of surgical endeavour in repair of the brachial plexus and there have been many false dawns. The alternation between optimism and pessimism that marked earlier writings is striking. The revival of interest about half a century ago may be ascribed to two factors. First was the increase in the number of closed injuries caused by accidents involving the increasingly popular motor cycle and the imposition of the wearing of crash helmets so saving
more lives. Next, was the careful evaluation of the natural history, the definition of the pre- versus the post-ganglionic lesion, and the development of methods enabling distinction between the two by George Bonney (1954, 1958, 1959), who re-introduced a policy of urgent operation in severe injuries of the brachial plexus at St Mary’s Hospital 50 years ago. It is opportune now to examine the validity of this approach. The reasons why delay is harmful may be grouped under three heads.
Biological For many years clinicians have suspected that a violent proximal injury to a spinal nerve causes profound effect upon the spinal cord. Atrophy of the cord on the side of injury has been seen at late hemilaminectomy
War Nerve Injury Clinic, Defence Medical Rehabilitation Centre, Epsom, UK Corresponding author: R. Birch, War Nerve Injury Clinic at Defence Medical Rehabilitation Centre, Headley Court, Epsom, Surrey KT18 6JW, UK. Email: [email protected]
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Birch Table 1. Outcome of repair in 137 patients – by delay before operation. Interval between injury and repair
Number of patients
Early: within 1 month Delayed: 1–3 months Late: up to 6 months Neglected: more than 6 months
60 28 27 22
Good
Fair
Poor
Number
(%)
Number
(%)
Number
(%)
34 11 7 3
57 40 26 14
15 11 13 11
25 40 48 50
11 6 7 8
18 21 26 36
Drawn from Kato et al. (2006) and Surgical Disorders of the Peripheral Nerves, 2nd edn.6 A ‘good’ result means that the patient regained at least one function.
(Bonney, 1998). Examination of the spinal cord at necropsy years after amputation has confirmed severe loss of motor and sensory neurones (Dyck et al., 1984; Suzuki et al., 1993). The recognition that the soma of the neuron depends upon a supply of neurotrophins for survival after axonotomy is more recent (Anand et al., 1997). Neurotrophins are synthesized by target tissues and Schwann cells, and are transported to the cell body by the fast centripetal component of axonal transport (Birch, 2011a; Windebank and McDonald, 2005). Proximal axonotomy causes death of neurons in the dorsal root ganglion (Terenghi et al., 2011) and in the ventral horn (Groves and Scaravilli, 2005). The motor neurons are especially vulnerable to rupture or avulsion of the ventral root. Carlstedt (2007) estimates that about half of the motor neurons in the affected spinal cord segments have disappeared by 2 weeks after avulsion of the ventral root and he urges ‘swift intervention to re-establish contact between the injured nerve cells and the periphery with its supply of neurotrophic substances’. Here is the biological imperative: the sooner that reconnection is made between the neurons in the ventral horn and the peripheral tissues via the Schwann cell cylinders, the better (Birch 2011b). Dunkerton (1984) reviewed 85 patients operated between 1975 and 1983, in whom 125 repairs, by conventional graft, were performed. He found no clear relation between outcome and delay before operation, although the prognosis for lesions in continuity was more accurate in explorations done within 2 weeks. The vascularized ulnar nerve graft was introduced in 1975 for patients with irreparable injury to (C6, C7) C8 and T1, with post-ganglionic ruptures in C5 (C6, C7). The object was reinnervation of the median nerve or its lateral cord components. The first 42 cases were described in 1988 (Birch, Bonney) and results in 65 patients were outlined in 1998 (Birch and Bonney). The failure rate for the desired objective of hand function was high. Really useful hand function was seen in only three
patients, two adults operated within 7 days and one child at 8 weeks. Elements of hand function, a crude grip with elementary sensation, returned in ten more adults, most of whom were operated within 8 weeks. By the criterion of elbow flexion, the success rate was better than intercostal transfer but about the same as conventional grafting. Although there was a trend to greater regeneration in the early repairs, this should be set against the requirement for triceps to biceps transfer in at least four patients. This disorderly regeneration was one of the reasons why the operation had fallen from favour by the end of the 1980s. It was then reserved for the delayed case with a long gap and a scarred bed. Kato et al. (2006) examined 137 patients (284 repairs) with at least one avulsion; the average was 3.2 spinal nerves for each patient. The study was prospective, over two periods, 1986–1991 and 1999–2001. Although the main object of this work was to measure the response of pain, a clear relation between delay and outcome was found (Table 1). Rather similar conclusions were reached by Htut et al. (2006) who studied pain relief in 76 patients with particularly serious injuries. About 430 adult patients with closed traction lesion of the supraclavicular brachial plexus were operated in the 7 years between 1990 and 1996 (Birch, 2011c). A total of 43 patients were lost to follow-up. Cases of replantation were excluded, as were those where delayed operation was undertaken to relieve pain. The number of elements repaired was 898 in the 360 patients studied. The repairs were by conventional graft and transfer (Table 2). The seven patients who regained elements of hand function were operated within 14 days. It should be noted that relief of pain and useful recovery were seen in six from eight patients aged more than 60 years who were operated within 2 weeks. A later prospective study set out to define more closely the effects of delay and also to assess efficacy of different techniques including reinnervation of the ventral root. A total of 260 patients
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The Journal of Hand Surgery (Eur) 40(6)
Table 2. Results of repairs, in 360 patients, performed between 1990 -1996 by interval and by severity of lesion. Timing of repair. Overall totals (%) Functions attributed to the repair 0 1 2 3 or more Number of patients
Within 14 days
3 months
6 months
More than 6 months
Total
No. Pts.
%
No. Pts.
%
No. Pts.
%
No. Pts.
%
No. Pts.
%
23 25 33 76 157
15 16 24 47
28 32 32 15 107
26 30 30 14
16 12 16 6 50
32 24 32 12
28 10 8 0 46
61 22 18 0
95 79 89 97 360
25 20 22 25
Drawn from Surgical Disorders of the Peripheral Nerves, 2nd edn.6
Table 3. Results of repairs in 585 elements in 228 patients operated between 2000–2004 – by interval between injury and operation. Interval in days
0–7 8–14 15–28 29–56 57–84 85–112 113–182 More than 182
Number of patients
52 25 31 32 31 16 22 19 228
Results of repairs
Results (excluding ventral root repairs)
Good/ total
%
Good/ total
%
114/175 41/72 48/87 25/74 31/67 13/35 8/34 12/41 288/585
65 57 50 34 46 37 24 29 49
86/40 21/45 34/73 21/68 30/65 12/33 7/33 11/39 222/496
61 47 47 30 46 36 21 28 45
Average number of elements repaired in each patient
Average number of functions regained in each patient
3.4 2.9 2.8 2.3 2.2 2.2 1.5 2.2
5.4 3.8 3.3 1.6 1.8 1.9 1.1 1
The average numbers of repairs for each patient was 2.6. The average number of functions regained in each patient was 2.9; the total of functions regained was 658. Drawn from Surgical Disorders of the Peripheral Nerves, 2nd edn.6
were operated between 2000–2004. Eleven patients were lost to follow-up, urgent amputation proved necessary in three more with irreparable arterial injury, and planned repair was abandoned in seven more because of post-ischaemic fibrosis. Eleven patients were considered for re-implantation of avulsed spinal nerves. The results in the remaining 228 patients are set out in Table 3 (Birch, 2011c). The repairs included 377 grafts, 177 conventional nerve transfers, and 89 avulsed ventral roots repaired by transfer from the spinal accessory nerve or from one bundle of an adjacent ruptured or intact spinal nerve. The average number of pre-ganglionic injuries was 2.5. A ‘good’ result was defined as the recovery of at least one function, specified as the return of movement against resistance through two-thirds of the
range in one axis of a joint (Birch, 2011c). Some conclusions may be drawn. 1. The outcome was better when repair was performed within 7 days of injury, especially so in the presence of arterial injury. 2. The decline in outcome with increasing delay was more marked in the grafts. Of those performed within 7 days, 53% achieved a good result; the success rate for all grafts was 36%. No regeneration could be detected in just over one-quarter of them. 3. The average number of functions regained through a successful graft was 3.2, compared with 1.9 for the good ventral root repair, and 1.6 for the good conventional transfers. The admittedly few
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Birch cases of recovery of useful cutaneous sensation and motor function in the hand followed urgent grafts of ruptured spinal nerves. The report from Dickson and Biant (2010) shows what can be achieved. The whole plexus was repaired in two patients with complete lesions, combining graft with transfer on Day 6 after injury. Function was useful throughout the limb. There was recovery into the small muscles of the hand, with return of accurate localization to the digit, and warm and cool sensation. There was also recovery of sympathetic innervation into the skin of the hand.
Technical •• Operating in late cases is difficult because of fibrosis, which is worse after arterial injury or sepsis. Normal tissue planes become replaced by a massive scar in which it is often impossible to define a rupture or even an avulsed spinal nerve. It is far easier to recognize a rupture of a spinal nerve within a few days of injury than it is weeks or months later when scar mimics a lesion in continuity. •• Ruptured nerves recoil deep to the clavicle or even further and it is usually possible, in urgent operations, to reduce the gap between prepared stumps to 4 cm or less. •• Exploration within 48 hours of injury permits mapping of distal faces using the nerve stimulator. Distal, second, lesions can be detected, including those provoked by anoxia in cases of arterial injury. •• Repair, by nerve transfer, of an avulsed ventral root or by intradural re-implantation is generally possible only in the early days after injury.
Pain and rehabilitation Operation is no more than the first step in the long and arduous process of rehabilitation, a process that cannot start until a diagnosis has been made and all reasonable efforts to improve prognosis by nerve repair have been made. Pain is the main impediment to rehabilitation. Nearly all patients experience significant or severe pain; about two-thirds of those with constant pain experience it on the day of injury; so it is with about half of those developing shooting, convulsive pain. Pain is worst at about 3 months from injury, and less than half of patients record material relief from drugs (Birch, 2011c; Taggart, 2011). Distraction by work, study, retraining, or active rehabilitation is far more effective. Pain is relieved by reinnervation of muscle in over 70% of patients, often
quite suddenly some days before clinical signs of recovery. That relief is not related to recovery of skin sensation, nor to the return of sympathetic function (Berman et al., 1998; Htut et al., 2006). Kato et al. (2006) found that the earlier the operation is done, the more likely it is that the patient will experience relief of his or her pain, and observed that some patients showed dramatic improvement immediately after operation, whereas others experienced this shortly after their return to work. The mean, final visual analogue score was lower in those who returned to work than it was in those who did not. The fact that re-innervation usually eases pain even when it fails to restore worthwhile function (Htut et al., 2006), provides the strongest indication for operation and repair by one means or another even in the most severe cases. Common humanity dictates that the sooner the operation is done the better. The fact that return to work, retraining, or study is so much more effective for pain relief than any drug regime imposes upon the clinician the responsibility for overseeing the treatment of pain, and the prolonged and arduous course of rehabilitation. Return to work is rarely easy. Taggart (1998) recorded an encouragingly high rate of return to work, but the finding that four out of five patients returned to a different job indicates the importance of retraining. Our subsequent studies found that fewer patients needed to change jobs, but confirmed that time away from work or study was often prolonged. The problems of rehabilitation are much more difficult in the late or neglected case of a patient demoralized by uncertainty about recovery, about his or her future, by pain, and by prolonged process for compensation. Clinicians must get to these patients before the lawyers do.
Contraindications; some pitfalls The evidence in favour of the urgent approach is strong, but there are important contraindications. First is the condition of the patient. The associated injuries, notably to the head, chest, and spine, lead to delay beyond the favoured time of operation in about one-quarter of cases. Of the 228 patients operated in the years 2000 to 2004, most were referred by orthopaedic surgeons. A total of 98 were referred within the preferred interval of 7 days; urgent treatment of associated injury necessitated delay of up to 3 weeks in 68 more. The severity of injury was not initially appreciated in ten cases and an unduly optimistic prognosis was proposed in 33 more. We were responsible for some of these errors. The clinical diagnosis of a serious injury to the brachial plexus is usually straightforward. Evidence from the patient or witnesses about the violence of the injury
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and the axis of application of force upon the forequarter is of the highest importance. Severe pain within a paralysed or insensate limb indicates severe injury to the spinal nerves. Lightning-like, shooting, or convulsive pain radiating into the territory of a spinal nerve that is not working signifies pre-ganglionic injury to that nerve. Such pain is experienced by most who will suffer from it within 7 days of injury. Linear abrasions of the face, neck, and shoulder, and bruising of the tip of the shoulder, indicates violent distraction. Deep bruising in the posterior triangle shows that deep structures have been torn, perhaps also the subclavian artery. Tinel’s sign is a valuable indication of rupture of a spinal nerve. It is present on the day of injury in the conscious patient; it shows that axons have been ruptured at that level. The sign was detected in 142 nerves in 100 patients examined in 2004/2005. At operation, one nerve was found intact, ten proved to be avulsed, and 131 were indeed ruptured (Birch, 2011a). A second important contraindication to urgent operation is that of the lesion that seems to be naturally favourable. Observation is the proper course in patients after low energy transfer injury who do not have pain, in whom the lesion is incomplete and patchy, and where there is no Tinel sign. The nature of the lesion to the spinal nerve in the closed supraclavicular lesion is usually obvious in the urgent operation. The spinal nerves being intact or ruptured, or the presence of the dorsal root ganglion in the posteriortriangle confirms a pre-ganglionic, avulsion injury. The ‘stretch’ lesion, apparently in continuity, is unusual, and certainly much less common than in the infraclavicular traction lesion. There are two potential pitfalls that continue to perplex during operation at any time. The first is the rupture that extends centrally to involve the roots themselves (Type 4 – rupture with intradural component (Birch and Bonney, 1998)). The second is the rupture of ventral and dorsal roots without displacement of the dorsal root ganglion (Types 5 and 6). Measuring conduction in the central pathway, from the spinal nerve to the spinal cord, by somato sensory evoked potential monitoring goes some way to detecting these uncommon and difficult lesions during urgent operation, but the investigation will not detect the admittedly rare lesion of rupture confined to the ventral root. Conduction block has been shown in the proximal segment in a few cases where there was profuse bleeding into the posterior triangle.
Conclusion Expectations have moved beyond the idea that restoration of some movement at the shoulder and flexion at the elbow is a triumph. Nowadays, the aims of
treatment should include: regaining the highest level of function by repair of the nerve lesion; control of, indeed abolition of, pain; and securing return of the patient to a normal daily life. Three factors contribute to this raising of the bar. 1. The severity of the injury has been diminished over the years: in Rosson’s series (1988) nearly one in five patients suffered complete avulsion of C5-T1. Pre-ganglionic injury was found in 59% of all spinal nerves. The figures for the patients operated 2000–2004 in the same Unit reveal 7.2% of complete avulsion and an incidence of preganglionic lesion of 41%. 2. There have been great improvements in diagnosis, by clinical and imaging methods. 3. Intraoperative conduction studies have proved to be generally reliable. It is a fact that, at least in the severe cases, recovery through grafts falls away with the passage of every day; it is likely that the patient’s morale falls away with every week of delay before an accurate diagnosis and prognosis is made, and before control of pain is achieved. The longer a patient is out of work or study or retraining, the harder it is to start again. There is one caveat, and it is an important one. Early experience led to the impression that operations performed at between 4 and 8 weeks from injury, were often difficult because of the state of the tissues. There is good evidence for this in Table 3, where results were particularly closely matched to the timing of operation. Addas and Midha (2009) provide a good critique of nerve transfer, and they deprecate the trend towards relying on these instead of exposing and defining the lesion. Nerve transfers are undoubtedly useful in cases of C5, C6 lesion; about 20% of all our patients, but these should be combined with grafts wherever possible. At least one post-ganglionic rupture usually at C5, was displayed in more than half of our patients with C5, C6 lesion. The usefulness of this method is of itself, no good argument for avoidable delay. Conflict of interests None declared.
Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
References Addas BMJ, Midha R. Nerve transfers for severe injury. In: Spinner RJ, Winfree CJ (eds) Peripheral nerves: Injuries.
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Birch Neurosurgical Clinics of North America, 2009, 20: 27–38. Anand P, Birch R, Terenghi G et al. Endogenous nerve growth factor and ciliary neurotrophic factor levels in human peripheral nerve injury. Neuroreport. 1997, 8: 1935–1938. Berman JS, Birch R, Anand P. Pain following human brachial plexus injury with spinal cord root avulsion and the effect of surgery. Pain. 1998, 75: 199–207. Birch R. The neurotrophins. In: Birch R. Surgical disorders of the peripheral nerves, 2nd Edn. London, Springer UK, 2011a: 44–6. Birch R. The cell body and proximal stump. In: Birch R. Surgical disorders of the peripheral nerves, 2nd Edn. London, Springer UK, 2011b: 82–7. Birch R. The closed supraclavicular lesion. In: Birch R. Surgical disorders of the peripheral nerves, 2nd Edn. London, Springer UK, 2011c: 375–428. Birch R, Bonney G. Traumatic lesions of the brachial plexus. In: Birch R, Bonney G, Wynn Parry CG (Authors) Surgical disorders of the peripheral nerves. London, Edinburgh, Churchill Livingstone, 1998: 157–208. Birch R, Dunkerton M, Bonney G, Jamieson AM. Experience with the free vascularised ulnar nerve graft in repair of supraclavicular lesion of the brachial plexus. Clin Orthop Rel Res. 1988, 237: 96–104. Bonney G. The value of axon responses in determining the site of lesion in traction lesions of the brachial plexus. Brain. 1954, 77: 588–609. Bonney G. Prognosis in traction lesions of the brachial plexus. J Bone Joint Surg Br. 1959, 41: 4–35. Bonney G. Atrophy of the spinal cord. In: Birch R, Bonney G, Wynn Parry CG (Authors) Surgical disorders of the peripheral nerves. London, Edinburgh, Churchill Livingstone, 1998: 55. Bonney G, Gilliatt RW. Sensory nerve conduction after traction lesion of the brachial plexus. Proceedings of the college of medicine. 1958, 51: 365–7. Carlstedt T. Central nerve plexus injury. London, Imperial College Press, 2007: 83–100. Dickson J, Biant L. Recovery of hand function after repair of complete lesions of the brachial plexus: a report of two cases. J Bone Joint Surg Br. 2010, 92: 540–4. Dunkerton M. (1984) Measurement of function and results of repair. Unpublished work cited in: Birch R. Surgical disorders of the peripheral nerves, 2nd Edn. London, Springer UK, 2011: 411.
Dyck PJ, Nukada H, Lais CA, Karnes J. 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. Philadelphia, WB Saunders, 1984: 660–90. Frazier CH, Skillern PG. Supraclavicular subcutaneous lesions of the brachial plexus not associated with skeletal injuries. J Am Med Association. 1911, 57: 1957–63. Groves MJ, Scaravilli F. Pathology of peripheral neurone cell bodies In: PJ Dyke, PK Thomas (Eds.) Peripheral neuropathy, 4th Edn. Philadelphia, Elsevier Saunders, 2005: 683–732. Htut M, Misra P, Anand P, Birch R, Carlstedt T. Pain phenomena and sensory recovery following brachial plexus avulsion injury and surgical repair. J Hand Surg Br. 2006, 31: 596–605. Kato N, Htut M, Taggart M, Carlstedt T, Birch R. The effects of operative delay on the relief of neuropathic pain after injury to the brachial plexus. J Bone Joint Surg Br. 2006, 88: 756–9. Rosson JW. Closed traction lesions of the brachial plexus – an epidemic among young motor cyclists. Injury. 1988, 19: 4–6. Sherren NJ. Some points in the surgery of the peripheral nerves. Edin Med J. 1906, 20: 217–31. Suzuki H, Oyanagi K, Takahishi H, Kono H, Yokoyana M, Ikjta F. A quantitative pathological investigation of the cervical cord, roots and ganglia after long term amputation of the unilateral upper arm. Acta Neuropathol (Berl). 1993, 85: 666–73. Taggart M. Delay before return to work or study. In: Birch R, Bonney G, Wynn Parry CB (Authors) Surgical disorders of the peripheral nerves. London, Edinburgh, Churchill Livingstone, 1998: 461–3. Taggart M. Relief of pain with operation. In: Birch R. Surgical disorders of the peripheral nerves, 2nd Edn. London, Springer UK, 2011: 416–20. Terenghi G, Hart A, Wiberg M. The nerve injury and dying neurons: diagnosis and prevention. J Hand Surg Eur. 2011, 36: 730–4. Windebank AJ, McDonald ES. Neurotrophic factors in the peripheral nervous system. In: PJ Dyke, PK Thomas (Eds.) Peripheral neuropathy, 4th Edn. Philadelphia, Elsevier Saunders, 2005: 377–86.
Downloaded from jhs.sagepub.com at Kungl Tekniska Hogskolan / Royal Institute of Technology on November 14, 2015
JHS0010.1177/1753193414539865The Journal of Hand SurgeryBirch
JHS(E)
Review Article
Timing of surgical reconstruction for closed traumatic injury to the supraclavicular brachial plexus
The Journal of Hand Surgery (European Volume) 2015, Vol. 40E(6) 562–567 © The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/1753193414539865 jhs.sagepub.com
R. Birch Abstract While it is widely accepted that cases of traumatic injury to the brachial plexus benefit from early surgical exploration and repair, with results deteriorating with long delays, policies vary regarding the exact timing of intervention. This is one of a pair of review articles considering the clinical issues, investigations, and surgical factors relating to management of injuries to the supraclavicular brachial plexus, as well evidence from experimental work and clinical outcomes. In this article Professor Birch argues for early exploration of the brachial plexus as the optimum both to delineate the pathology and undertake reconstructive surgery. Keywords Brachial plexus injury, nerve repair, timing of surgery Date received: 22nd June 2013; revised: 30th September 2013; accepted: 16th October 2013
Introduction Subcutaneous injuries of the plexus must be regarded as serious injury either with or without operative interference. The number of spontaneous recoveries is exceedingly small and it is extraordinary how many patients have been allowed to progress to a hopeless state without operation and how many are not operated on until months have elapsed. In view of the gravity of the lesion, of the resulting disability and of the occasional intractable neuralgias, surgeons should insist on resort to operation, if not immediately, at least as soon as it can be demonstrated with reasonable certainty that spontaneous recovery is improbable. An excellent working rule is that of Sherren (1906) that all subcutaneous injuries which give reactions of degeneration at the end of ten days should be submitted to operation. Frazier and Skillern, 1911
There is a long history of surgical endeavour in repair of the brachial plexus and there have been many false dawns. The alternation between optimism and pessimism that marked earlier writings is striking. The revival of interest about half a century ago may be ascribed to two factors. First was the increase in the number of closed injuries caused by accidents involving the increasingly popular motor cycle and the imposition of the wearing of crash helmets so saving
more lives. Next, was the careful evaluation of the natural history, the definition of the pre- versus the post-ganglionic lesion, and the development of methods enabling distinction between the two by George Bonney (1954, 1958, 1959), who re-introduced a policy of urgent operation in severe injuries of the brachial plexus at St Mary’s Hospital 50 years ago. It is opportune now to examine the validity of this approach. The reasons why delay is harmful may be grouped under three heads.
Biological For many years clinicians have suspected that a violent proximal injury to a spinal nerve causes profound effect upon the spinal cord. Atrophy of the cord on the side of injury has been seen at late hemilaminectomy
War Nerve Injury Clinic, Defence Medical Rehabilitation Centre, Epsom, UK Corresponding author: R. Birch, War Nerve Injury Clinic at Defence Medical Rehabilitation Centre, Headley Court, Epsom, Surrey KT18 6JW, UK. Email: [email protected]
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Birch Table 1. Outcome of repair in 137 patients – by delay before operation. Interval between injury and repair
Number of patients
Early: within 1 month Delayed: 1–3 months Late: up to 6 months Neglected: more than 6 months
60 28 27 22
Good
Fair
Poor
Number
(%)
Number
(%)
Number
(%)
34 11 7 3
57 40 26 14
15 11 13 11
25 40 48 50
11 6 7 8
18 21 26 36
Drawn from Kato et al. (2006) and Surgical Disorders of the Peripheral Nerves, 2nd edn.6 A ‘good’ result means that the patient regained at least one function.
(Bonney, 1998). Examination of the spinal cord at necropsy years after amputation has confirmed severe loss of motor and sensory neurones (Dyck et al., 1984; Suzuki et al., 1993). The recognition that the soma of the neuron depends upon a supply of neurotrophins for survival after axonotomy is more recent (Anand et al., 1997). Neurotrophins are synthesized by target tissues and Schwann cells, and are transported to the cell body by the fast centripetal component of axonal transport (Birch, 2011a; Windebank and McDonald, 2005). Proximal axonotomy causes death of neurons in the dorsal root ganglion (Terenghi et al., 2011) and in the ventral horn (Groves and Scaravilli, 2005). The motor neurons are especially vulnerable to rupture or avulsion of the ventral root. Carlstedt (2007) estimates that about half of the motor neurons in the affected spinal cord segments have disappeared by 2 weeks after avulsion of the ventral root and he urges ‘swift intervention to re-establish contact between the injured nerve cells and the periphery with its supply of neurotrophic substances’. Here is the biological imperative: the sooner that reconnection is made between the neurons in the ventral horn and the peripheral tissues via the Schwann cell cylinders, the better (Birch 2011b). Dunkerton (1984) reviewed 85 patients operated between 1975 and 1983, in whom 125 repairs, by conventional graft, were performed. He found no clear relation between outcome and delay before operation, although the prognosis for lesions in continuity was more accurate in explorations done within 2 weeks. The vascularized ulnar nerve graft was introduced in 1975 for patients with irreparable injury to (C6, C7) C8 and T1, with post-ganglionic ruptures in C5 (C6, C7). The object was reinnervation of the median nerve or its lateral cord components. The first 42 cases were described in 1988 (Birch, Bonney) and results in 65 patients were outlined in 1998 (Birch and Bonney). The failure rate for the desired objective of hand function was high. Really useful hand function was seen in only three
patients, two adults operated within 7 days and one child at 8 weeks. Elements of hand function, a crude grip with elementary sensation, returned in ten more adults, most of whom were operated within 8 weeks. By the criterion of elbow flexion, the success rate was better than intercostal transfer but about the same as conventional grafting. Although there was a trend to greater regeneration in the early repairs, this should be set against the requirement for triceps to biceps transfer in at least four patients. This disorderly regeneration was one of the reasons why the operation had fallen from favour by the end of the 1980s. It was then reserved for the delayed case with a long gap and a scarred bed. Kato et al. (2006) examined 137 patients (284 repairs) with at least one avulsion; the average was 3.2 spinal nerves for each patient. The study was prospective, over two periods, 1986–1991 and 1999–2001. Although the main object of this work was to measure the response of pain, a clear relation between delay and outcome was found (Table 1). Rather similar conclusions were reached by Htut et al. (2006) who studied pain relief in 76 patients with particularly serious injuries. About 430 adult patients with closed traction lesion of the supraclavicular brachial plexus were operated in the 7 years between 1990 and 1996 (Birch, 2011c). A total of 43 patients were lost to follow-up. Cases of replantation were excluded, as were those where delayed operation was undertaken to relieve pain. The number of elements repaired was 898 in the 360 patients studied. The repairs were by conventional graft and transfer (Table 2). The seven patients who regained elements of hand function were operated within 14 days. It should be noted that relief of pain and useful recovery were seen in six from eight patients aged more than 60 years who were operated within 2 weeks. A later prospective study set out to define more closely the effects of delay and also to assess efficacy of different techniques including reinnervation of the ventral root. A total of 260 patients
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The Journal of Hand Surgery (Eur) 40(6)
Table 2. Results of repairs, in 360 patients, performed between 1990 -1996 by interval and by severity of lesion. Timing of repair. Overall totals (%) Functions attributed to the repair 0 1 2 3 or more Number of patients
Within 14 days
3 months
6 months
More than 6 months
Total
No. Pts.
%
No. Pts.
%
No. Pts.
%
No. Pts.
%
No. Pts.
%
23 25 33 76 157
15 16 24 47
28 32 32 15 107
26 30 30 14
16 12 16 6 50
32 24 32 12
28 10 8 0 46
61 22 18 0
95 79 89 97 360
25 20 22 25
Drawn from Surgical Disorders of the Peripheral Nerves, 2nd edn.6
Table 3. Results of repairs in 585 elements in 228 patients operated between 2000–2004 – by interval between injury and operation. Interval in days
0–7 8–14 15–28 29–56 57–84 85–112 113–182 More than 182
Number of patients
52 25 31 32 31 16 22 19 228
Results of repairs
Results (excluding ventral root repairs)
Good/ total
%
Good/ total
%
114/175 41/72 48/87 25/74 31/67 13/35 8/34 12/41 288/585
65 57 50 34 46 37 24 29 49
86/40 21/45 34/73 21/68 30/65 12/33 7/33 11/39 222/496
61 47 47 30 46 36 21 28 45
Average number of elements repaired in each patient
Average number of functions regained in each patient
3.4 2.9 2.8 2.3 2.2 2.2 1.5 2.2
5.4 3.8 3.3 1.6 1.8 1.9 1.1 1
The average numbers of repairs for each patient was 2.6. The average number of functions regained in each patient was 2.9; the total of functions regained was 658. Drawn from Surgical Disorders of the Peripheral Nerves, 2nd edn.6
were operated between 2000–2004. Eleven patients were lost to follow-up, urgent amputation proved necessary in three more with irreparable arterial injury, and planned repair was abandoned in seven more because of post-ischaemic fibrosis. Eleven patients were considered for re-implantation of avulsed spinal nerves. The results in the remaining 228 patients are set out in Table 3 (Birch, 2011c). The repairs included 377 grafts, 177 conventional nerve transfers, and 89 avulsed ventral roots repaired by transfer from the spinal accessory nerve or from one bundle of an adjacent ruptured or intact spinal nerve. The average number of pre-ganglionic injuries was 2.5. A ‘good’ result was defined as the recovery of at least one function, specified as the return of movement against resistance through two-thirds of the
range in one axis of a joint (Birch, 2011c). Some conclusions may be drawn. 1. The outcome was better when repair was performed within 7 days of injury, especially so in the presence of arterial injury. 2. The decline in outcome with increasing delay was more marked in the grafts. Of those performed within 7 days, 53% achieved a good result; the success rate for all grafts was 36%. No regeneration could be detected in just over one-quarter of them. 3. The average number of functions regained through a successful graft was 3.2, compared with 1.9 for the good ventral root repair, and 1.6 for the good conventional transfers. The admittedly few
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Birch cases of recovery of useful cutaneous sensation and motor function in the hand followed urgent grafts of ruptured spinal nerves. The report from Dickson and Biant (2010) shows what can be achieved. The whole plexus was repaired in two patients with complete lesions, combining graft with transfer on Day 6 after injury. Function was useful throughout the limb. There was recovery into the small muscles of the hand, with return of accurate localization to the digit, and warm and cool sensation. There was also recovery of sympathetic innervation into the skin of the hand.
Technical •• Operating in late cases is difficult because of fibrosis, which is worse after arterial injury or sepsis. Normal tissue planes become replaced by a massive scar in which it is often impossible to define a rupture or even an avulsed spinal nerve. It is far easier to recognize a rupture of a spinal nerve within a few days of injury than it is weeks or months later when scar mimics a lesion in continuity. •• Ruptured nerves recoil deep to the clavicle or even further and it is usually possible, in urgent operations, to reduce the gap between prepared stumps to 4 cm or less. •• Exploration within 48 hours of injury permits mapping of distal faces using the nerve stimulator. Distal, second, lesions can be detected, including those provoked by anoxia in cases of arterial injury. •• Repair, by nerve transfer, of an avulsed ventral root or by intradural re-implantation is generally possible only in the early days after injury.
Pain and rehabilitation Operation is no more than the first step in the long and arduous process of rehabilitation, a process that cannot start until a diagnosis has been made and all reasonable efforts to improve prognosis by nerve repair have been made. Pain is the main impediment to rehabilitation. Nearly all patients experience significant or severe pain; about two-thirds of those with constant pain experience it on the day of injury; so it is with about half of those developing shooting, convulsive pain. Pain is worst at about 3 months from injury, and less than half of patients record material relief from drugs (Birch, 2011c; Taggart, 2011). Distraction by work, study, retraining, or active rehabilitation is far more effective. Pain is relieved by reinnervation of muscle in over 70% of patients, often
quite suddenly some days before clinical signs of recovery. That relief is not related to recovery of skin sensation, nor to the return of sympathetic function (Berman et al., 1998; Htut et al., 2006). Kato et al. (2006) found that the earlier the operation is done, the more likely it is that the patient will experience relief of his or her pain, and observed that some patients showed dramatic improvement immediately after operation, whereas others experienced this shortly after their return to work. The mean, final visual analogue score was lower in those who returned to work than it was in those who did not. The fact that re-innervation usually eases pain even when it fails to restore worthwhile function (Htut et al., 2006), provides the strongest indication for operation and repair by one means or another even in the most severe cases. Common humanity dictates that the sooner the operation is done the better. The fact that return to work, retraining, or study is so much more effective for pain relief than any drug regime imposes upon the clinician the responsibility for overseeing the treatment of pain, and the prolonged and arduous course of rehabilitation. Return to work is rarely easy. Taggart (1998) recorded an encouragingly high rate of return to work, but the finding that four out of five patients returned to a different job indicates the importance of retraining. Our subsequent studies found that fewer patients needed to change jobs, but confirmed that time away from work or study was often prolonged. The problems of rehabilitation are much more difficult in the late or neglected case of a patient demoralized by uncertainty about recovery, about his or her future, by pain, and by prolonged process for compensation. Clinicians must get to these patients before the lawyers do.
Contraindications; some pitfalls The evidence in favour of the urgent approach is strong, but there are important contraindications. First is the condition of the patient. The associated injuries, notably to the head, chest, and spine, lead to delay beyond the favoured time of operation in about one-quarter of cases. Of the 228 patients operated in the years 2000 to 2004, most were referred by orthopaedic surgeons. A total of 98 were referred within the preferred interval of 7 days; urgent treatment of associated injury necessitated delay of up to 3 weeks in 68 more. The severity of injury was not initially appreciated in ten cases and an unduly optimistic prognosis was proposed in 33 more. We were responsible for some of these errors. The clinical diagnosis of a serious injury to the brachial plexus is usually straightforward. Evidence from the patient or witnesses about the violence of the injury
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The Journal of Hand Surgery (Eur) 40(6)
and the axis of application of force upon the forequarter is of the highest importance. Severe pain within a paralysed or insensate limb indicates severe injury to the spinal nerves. Lightning-like, shooting, or convulsive pain radiating into the territory of a spinal nerve that is not working signifies pre-ganglionic injury to that nerve. Such pain is experienced by most who will suffer from it within 7 days of injury. Linear abrasions of the face, neck, and shoulder, and bruising of the tip of the shoulder, indicates violent distraction. Deep bruising in the posterior triangle shows that deep structures have been torn, perhaps also the subclavian artery. Tinel’s sign is a valuable indication of rupture of a spinal nerve. It is present on the day of injury in the conscious patient; it shows that axons have been ruptured at that level. The sign was detected in 142 nerves in 100 patients examined in 2004/2005. At operation, one nerve was found intact, ten proved to be avulsed, and 131 were indeed ruptured (Birch, 2011a). A second important contraindication to urgent operation is that of the lesion that seems to be naturally favourable. Observation is the proper course in patients after low energy transfer injury who do not have pain, in whom the lesion is incomplete and patchy, and where there is no Tinel sign. The nature of the lesion to the spinal nerve in the closed supraclavicular lesion is usually obvious in the urgent operation. The spinal nerves being intact or ruptured, or the presence of the dorsal root ganglion in the posteriortriangle confirms a pre-ganglionic, avulsion injury. The ‘stretch’ lesion, apparently in continuity, is unusual, and certainly much less common than in the infraclavicular traction lesion. There are two potential pitfalls that continue to perplex during operation at any time. The first is the rupture that extends centrally to involve the roots themselves (Type 4 – rupture with intradural component (Birch and Bonney, 1998)). The second is the rupture of ventral and dorsal roots without displacement of the dorsal root ganglion (Types 5 and 6). Measuring conduction in the central pathway, from the spinal nerve to the spinal cord, by somato sensory evoked potential monitoring goes some way to detecting these uncommon and difficult lesions during urgent operation, but the investigation will not detect the admittedly rare lesion of rupture confined to the ventral root. Conduction block has been shown in the proximal segment in a few cases where there was profuse bleeding into the posterior triangle.
Conclusion Expectations have moved beyond the idea that restoration of some movement at the shoulder and flexion at the elbow is a triumph. Nowadays, the aims of
treatment should include: regaining the highest level of function by repair of the nerve lesion; control of, indeed abolition of, pain; and securing return of the patient to a normal daily life. Three factors contribute to this raising of the bar. 1. The severity of the injury has been diminished over the years: in Rosson’s series (1988) nearly one in five patients suffered complete avulsion of C5-T1. Pre-ganglionic injury was found in 59% of all spinal nerves. The figures for the patients operated 2000–2004 in the same Unit reveal 7.2% of complete avulsion and an incidence of preganglionic lesion of 41%. 2. There have been great improvements in diagnosis, by clinical and imaging methods. 3. Intraoperative conduction studies have proved to be generally reliable. It is a fact that, at least in the severe cases, recovery through grafts falls away with the passage of every day; it is likely that the patient’s morale falls away with every week of delay before an accurate diagnosis and prognosis is made, and before control of pain is achieved. The longer a patient is out of work or study or retraining, the harder it is to start again. There is one caveat, and it is an important one. Early experience led to the impression that operations performed at between 4 and 8 weeks from injury, were often difficult because of the state of the tissues. There is good evidence for this in Table 3, where results were particularly closely matched to the timing of operation. Addas and Midha (2009) provide a good critique of nerve transfer, and they deprecate the trend towards relying on these instead of exposing and defining the lesion. Nerve transfers are undoubtedly useful in cases of C5, C6 lesion; about 20% of all our patients, but these should be combined with grafts wherever possible. At least one post-ganglionic rupture usually at C5, was displayed in more than half of our patients with C5, C6 lesion. The usefulness of this method is of itself, no good argument for avoidable delay. Conflict of interests None declared.
Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
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