Early nerve repair in traumatic brachial plexus injuries ...dult traumatic brachial plexus injuries (ATBPI) are relatively rare lesions, but severe lesions have a profound impact on

CLINICAL ARTICLEJ Neurosurg 130:172–178, 2019

Adult traumatic brachial plexus injuries (ATBPI) are relatively rare lesions, but severe lesions have a profound impact on daily activities as a result of

the loss of upper limb function. The lesion usually consists of a closed nerve traction injury anatomically located in the supraclavicular part of the brachial plexus. The mag-nitude and direction of the forces acting during impact on the brachial plexus elements determine lesion severity. Spontaneous recovery can occur in mild lesions with ax-onotmesis in which the basal lamina tubes remain intact and axons elongate to their respective original end organs. Neurological recovery will then take place over the course of several months, depending on the distance between the lesion and the end organ.31

Spontaneous recovery will not occur, however, in cases of neurotmesis (nerve rupture) or avulsion of the nerve root from the spinal cord. In these cases, surgical recon-nection of the distal nerve is warranted through nerve

grafting or nerve transfer. Grafting entails bridging the gap by interposing a nerve graft between the proximal and distal nerve stumps of the severed nerve. Nerve transfers are performed when viable proximal stumps are not avail-able because of root avulsion. In such cases, the distal part of the target recipient nerve is connected to the proximal part of an undamaged donor nerve. Options for donors are extraplexal nerves (for example, the intercostal nerves21 or the spinal accessory nerve19), intact intraplexal nerves (for example, the pectoral nerves30), or individual fascicles of an intact intraplexal nerve (for example, fascicular transfer of the ulnar nerve to the terminal branches of the biceps and brachialis muscles25). Occasionally, nerve transfer can be the procedure of choice in large gaps since graft length is negatively correlated with outcome.27 Nerve transfer can also be preferred in older patients and in cases in which the interval between injury and repair is long.

In general, the outcome of ATBPI surgery is unsatisfac-

ABBREVIATIONS ATBPI = adult traumatic brachial plexus injury; CTM = CT myelography; MRC = Medical Research Council.SUBMITTED February 10, 2017. ACCEPTED July 6, 2017.INCLUDE WHEN CITING Published online January 26, 2018; DOI: 10.3171/2017.7.JNS17365.

Early nerve repair in traumatic brachial plexus injuries in adults: treatment algorithm and first experiencesWillem Pondaag, MD, PhD, Finn Y. van Driest, MD, Justus L. Groen, MD, PhD, and Martijn J. A. Malessy, MD, PhD

Department of Neurosurgery, Leiden Nerve Center, Leiden University Medical Center, Leiden, The Netherlands

OBJECTIVE The object of this study was to assess the advantages and disadvantages of early nerve repair within 2 weeks following adult traumatic brachial plexus injury (ATBPI).METHODS From 2009 onwards, the authors have strived to repair as early as possible extended C-5 to C-8 or T-1 le-sions or complete loss of C-5 to C-6 or C-7 function in patients in whom there was clinical and radiological suspicion of root avulsion. Among a group of 36 patients surgically treated in the period between 2009 and 2011, surgical findings in those who had undergone treatment within 2 weeks after trauma were retrospectively compared with results in those who had undergone delayed treatment. The result of biceps muscle reanimation was the primary outcome measure.RESULTS Five of the 36 patients were referred within 2 weeks after trauma and were eligible for early surgery. Nerve ruptures and/or avulsions were found in all early cases of surgery. The advantages of early surgery are as follows: no scar formation, easy anatomical identification, and gap length reduction. Disadvantages include less-clear demarcation of vital nerve tissue and unfamiliarity with the interpretation of frozen-section examination findings. All 5 early-treatment patients recovered a biceps force rated Medical Research Council grade 4.CONCLUSIONS Preliminary results of nerve repair within 2 weeks of ATBPI are encouraging, and the benefits outweigh the drawbacks. The authors propose a decision algorithm to select patients eligible for early surgery. Referral standards for patients with ATBPI must be adapted to enable early surgery.https://thejns.org/doi/abs/10.3171/2017.7.JNS17365KEY WORDS brachial plexus injury; nerve surgery; nerve grafting; nerve transfer; peripheral nerve

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tory. Especially in cases of total lesions, useful recovery of hand function is rare.24 Reanimation of elbow flexion is relatively successful, and results for shoulder function are intermediate. Currently, surgical intervention for ATBPI is only performed months after the trauma if spontaneous recovery does not occur.15,16,33

The main argument for waiting is that potential par-tial or substantial spontaneous recovery can eliminate the need for surgery or require an adaptation of the re-construction plan. In addition, it is argued that neuroma formation delineates healthy from damaged nerve, facili-tating intraoperative assessment of the level of resection. However, the results of nerve reconstruction are known to decline substantially as the interval between trauma and nerve reconstruction increases.6,7,27 Therefore, timing of the surgical intervention in cases of severe lesions is a cru-cial element in optimizing treatment. The clinical imple-mentation of early nerve reconstruction to take advantage of the beneficial circumstances for regeneration has not occurred on a wide scale. Until now, reports favoring early surgical nerve repair have mainly come from the United Kingdom.1–3,10,13,14,18

Since 2009, we have strived to operate on severe ATBPI as soon as possible. We reached out to referring specialists in the Netherlands with the slogan, “We want a call from the shock room,” in the hope that they would contact us preferably immediately after diagnosing an ATBPI. We operated on these patients as early as possible if a high suspicion of severe injury (neurotmesis or root avulsion) was present. Here we present our experience with this new strategy, our selection algorithm, and our preliminary re-sults.

MethodsWe performed a retrospective chart review to identify

patients who had been surgically treated for ATBPI in the period from 2009 up until 2011, which included sufficient follow-up. Patients with open lesions or with traumatic le-sions of the individual end nerves of the brachial plexus (that is, musculocutaneous nerve or axillary nerve) were excluded. We identified 42 patients with ATBPI who had undergone surgery in this time frame. Six patients were lost to follow-up, and 5 of them resided abroad. A total of 36 patients were further analyzed: 29 patients had had a motorcycle or moped accident, 5 patients had been in-volved in a car accident, and 2 patients had been hit by a motor vehicle while walking or biking. Thirty-three pa-tients had a supraclavicular traction lesion, 2 had an infra-clavicular traction lesion, and 1 patient had a lesion from a costoclavicular crush injury. Patient characteristics are listed in Table 1.

The biceps muscle was the primary target of the nerve reconstruction via nerve grafting or nerve transfer. Early nerve repair was defined as surgical reconstruction that could be performed within 2 weeks after the trauma.1,13 Following current definitions in the literature, we consid-ered late nerve surgery as reconstruction after 2 months; surgery occurring between 2 weeks and 2 months after the trauma was intermediate.13

After surgery, patients were scheduled for regular fol-

low-ups at our multidisciplinary outpatient clinic. The first follow-up was scheduled for 2 months after surgery; there-after, patients were followed up at 6- to 9-month intervals. The result of biceps volitional force was assessed using the Medical Research Council (MRC) motor grading scale between 0 and 5.23 The MRC grade at the last visit was used as the final result. Maximum score was limited to MRC grade 4, as MRC grade 5, or “normal,” cannot be achieved after nerve reconstruction.

IBM SPSS Statistics software (version 20, IBM Corp.) was employed for statistical analysis. We employed Fish-er’s exact test for comparisons between groups. A p < 0.05 was considered statistically significant.

Patient SelectionPatients referred to us within 2 weeks of trauma under-

went early surgery only if they had root avulsions based on clinical and radiological grounds (Fig. 1). Patients were eligible for early surgical intervention if the following cri-teria were met: 1) trauma resulted from high-velocity im-pact injury; 2) neurological deficit was concomitant with external signs such as supraclavicular bruising pointing to supraclavicular trauma; 3) neurological extent of the lesion

TABLE 1. Summary of characteristics in 36 patients with ATBPI

VariableNo.

Entire Cohort Early Treatment

Trauma Motorcycle 19 2 Moped 10 2 Car 5 1 Other 2Age in yrs Mean ± SD 30.8 ± 12.3 24.6 ± 8.9 Min–max 16–53 17–37Age group in yrs 16–19 11 3 20–29 8 30–39 7 2 40–49 7 50–53 3Sex Male 33 3 Female 3 2Lesion extent C5–6 8 1 C5–7 5 1 C5–8 7 1 Flail 13 2 Infraclavicular/crush 3Follow-up Mean in mos 26 Min–max in mos 11–59 Patients w/ <18 mos 5


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befitted complete lesion of at least spinal nerves C-5 and C-6; and 4) deafferentation pain or Horner sign befitting root avulsion. In the case of such lesions, prompt radio-logical workup was indicated to detect root avulsion. This workup consisted of MRI or CT myelography (CTM).4,5 Magnetic resonance imaging is used as the imaging mo-dality of choice. Our primary aim is to visualize continu-ity of the ventral and dorsal rootlets, and the secondary aim is to detect CSF inside or outside the foramen as a sign of dural root sleeve rupture. In some cases, the quality of the MR images was insufficient to judge with certainty the continuity of the ventral and dorsal rootlets; poor im-age quality was caused, for instance, by movement arti-facts or CSF pulsation artifacts. In these cases, additional CTM was performed.

Operative ProcedureAll procedures were performed by one of the senior

authors (W.P. or M.J.A.M.). The brachial plexus was ex-posed using a supraclavicular approach, which when necessary was extended to the infraclavicular level. The injured nerves were dissected, and the severity of the le-sion was assessed macroscopically. Clear nerve rupture, avulsion of the spinal nerve outside the foramen, or, in cases of delayed surgery, neuroma formation was noted. The nerves were stimulated (using a conventional bipolar forceps connected to an electrical 2.5-Hz pulse genera-tor with a maximum of 6 V), and axonal continuity was assessed by identifying contractions elicited by palpating the target muscle during stimulation. Additionally, the branches of the C-5, C-6, and C-7 spinal nerves to the long thoracic nerve at the juxtaforaminal level were stimulated. A negative response to stimulation indicates axonal dis-continuity from the central nervous system to the concern-ing C-5, C-6, and/or C-7 stump, befitting intraforaminal spinal nerve rupture or root avulsion.

The primary goal of surgery was to reanimate elbow flexion, and we intended to reach this goal preferably by nerve grafting and otherwise by nerve transfer. The de-cision to choose grafting or transfer was made during surgery. Nerve grafting requires the presence of a viable nerve stump proximal to the rupture. A stump was con-sidered viable if, on inspection and after appropriate trim-ming, the surface showed a fascicular structure without hemorrhage or fibrosis. We supported our visual inspec-tion (magnified by surgical loupes and microscope) with frozen-section examination, which also provided myelin content.22 A positive response to direct stimulation of the proximal branches to the long thoracic nerve and the pres-ence of root filaments on imaging further supported the use of a stump for grafting.

A nerve transfer to regain elbow flexion was employed when 1) there was no viable proximal stump due to root avulsion or intraforaminal neurotmesis, 2) long nerve grafts were necessary to bridge the gap between the stumps regardless of the viability of the proximal stump, or 3) there was a long time interval between trauma and reconstruction.

Nerve reconstruction was performed using autologous sural nerve grafts or nerve transfers, as described previ-ously.19,21 The avulsed C-6 root or the anterior division of

the superior trunk served as the distal targets for the graft-ing procedure. If transfer was thought to be the feasible option, fascicular transfers were performed using a func-tional fascicle from the donor nerve, which was coaptated end-to-end to the target. We usually employed an “Oberlin 2” transfer, which consists of 2 donor fascicles: one from the ulnar nerve that was coaptated to the nerve to the bi-ceps muscle and one from the median nerve that was coap-tated to the nerve to the brachialis muscle.17 In 2 patients, median nerve function was not normal and the “Oberlin 1” transfer was employed, which entailed one fascicle trans-fer from the ulnar nerve to reinnervate the biceps muscle.25 The intercostal nerve transfer was only used if an Oberlin transfer could not be performed because of insufficient function of both the ulnar and median nerves.

Secondary aims of reconstruction depended on the nature and extent of the nerve lesion in each individual patient. Recovery of shoulder function was pursued with

FIG. 1. Treatment algorithm to decide eligibility for early surgery follow-ing brachial plexus traction injury resulting from high kinetic trauma. *Severe nerve lesion is defined as complete lesion (C5–T1) or almost complete lesion (C5–8) with clinical suspicion of root avulsion; inter-mediate severity is defined as complete loss of C5–6 or C5–7 function. ABC = airway, breathing, circulation stable according to advanced trau-ma life support methodology, and preferably fractures have been treated adequately; EMG = electromyography; MR/CTM = MR/CT myelography.



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nerve grafting targeting the distal spinal C-5 nerve stump or the posterior division of the superior trunk and/or su-prascapular nerve, depending on the number of viable proximal stumps. The stump with the best appearance on inspection, frozen-section examination, stimulation, and imaging was used for biceps recovery; the second best, if available, for shoulder recovery.

After surgery, the patients were outfitted with a shoul-der immobilizer and soft neck collar for 2 weeks.

ResultsTiming of Surgery

Five of 36 ATBPI patients were referred early and were eligible for surgery within 2 weeks after trauma, 5 under-went surgery between 2 weeks and 2 months after injury, and the remaining 26 patients underwent surgery more than 2 months after injury. The mean interval between trauma and surgery in the late-treatment group was 147 days (SD 77 days). Recovery outcomes of nerve repair for the 5 early-treatment patients are detailed in Table 2.

Surgical FindingsIn all cases of early surgery, clear ruptures and/or root

avulsions were identified. The benefits of early surgery were as follows: 1) There was no scar formation, facilitat-ing simple identification of proximal and distal stumps; 2) distally displaced ruptured or avulsed plexus elements usually located behind or just above the level of the clav-icle could be easily repositioned in a proximal direction, thus shortening the gap several centimeters; 3) direct co-

aptation following intraplexal transfer was occasionally possible; and 4) dorsal root ganglions and anterior root filaments of avulsed nerves could be easily identified and dissected. After removing the dorsal ganglion, targeted grafting to the ventral motor part or sensory transfer to the postganglionic part was feasible.20,26 The drawbacks of early surgery were a less-clear demarcation of vital nerve tissue and an unfamiliarity with the interpretation of frozen-section examination findings. Scar and adhesion formation had noticeably started if surgery was performed more than 2 weeks after trauma. The beneficial effects of early surgery were then lost. In both early and later sur-gery, no complications were noted.

Biceps RecoveryMean follow-up among all patients was 26 months

(range 11–59 months). In 5 patients, the follow-up was less than 18 months. In these 5 patients, all of whom had un-dergone early treatment, biceps recovery to MRC grade 4 was achieved by that time, and this was scored as the final result despite the relatively short follow-up. All five “early” patients recovered a biceps force of MRC grade 4, as compared with 14 (54%) of 26 patients who were oper-ated on late (p = 0.068, Fisher’s exact test). Regardless of the surgical delay, MRC grade 4 strength was attained in 11 (85%) of 13 patients following Oberlin transfer (types 1 and 2 combined), compared with 7 (39%) of 18 patients after nerve grafting. The difference between these 2 surgi-cal techniques proved statistically significant (p = 0.013, Fisher’s exact test). Results of biceps recovery are present-ed in Table 3.

TABLE 2. Details on the early-treatment patients and outcomes of surgically targeted muscles

SexAge (yrs)

Lesion Extent Description of Imaging, Surgical, & Follow-Up Findings

M 19 C5–8I: MRI: CSF outside foramen, continuity of intraspinal nerves uncertain; CTM: certain avulsion C6–7, C-5 questionableS: 7 days/avulsion C5–8/ICN-MCN, transfer cervical plexus–C7F: 25 mos/biceps MRC grade 4

M 38 C5–7

I: MRI: (other institution) insufficient technical quality to judge intradural filaments; CTM: intact C-5; avulsion C-6 w/ CSF leakage outside foramen

S: 10 days/neurotmesis C-5, avulsion C6–7/OB2, NG C5-PDST 3 × 9*F: 16 mos/biceps MRC grade 4/flail shoulder

F 30 C5–6I: MRI: avulsion C-6S: 8 days/neurotmesis C-5, avulsion C-6, C-5 branch to long thoracic nerve no response on stimulation/OB2, NG C5–5 5 × 4*F: 14 mos/biceps MRC grade 4/flail shoulder

F 17 C5–T1

I: MRI: (elsewhere) insufficient quality to judge intradural filaments; CTM: intact C-5, avulsion C6–T1 w/ CSF & contrast outside foramen

S: 8 days/neurotmesis C-5/avulsion C6–T1/NG C5-ADST 4 × 7*F: 30 mos/biceps MRC grade 4/pec major MRC grade 2–3

M 19 C5–T1

I: CTM: avulsion C-7, C-8, T-1S: 8 days/neurotmesis C5–6, avulsion C7–T1/NG C6-ADST 4 × 5,* C5-PDST & PDMT 4 × 5,* C5-SSN 1 × 5,* C6–ant filaments

of spinal nerve root C-8 1 × 2*F: 25 mos/biceps MRC grade 4/flail shoulder, flail wrist, flail hand

ADST = anterior division of superior trunk; ant = anterior; F = follow-up: interval since surgery (mos)/surgical results: biceps/other muscles; I = imaging; ICN-MCN = intercostal nerve to musculocutaneous nerve transfer; NG = nerve grafting; OB2 = Oberlin 2 transfer; PDMT = posterior division of middle trunk; PDST = posterior divi-sion of superior trunk; pec major = pectoralis major muscle; S = surgery: interval since trauma/surgical findings/reconstruction of biceps and additional targets; SSN = suprascapular nerve.* A × B = A grafts of B cm.


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DiscussionSince 2009, we have strived to operate on patients with

ATBPI as soon as feasible if they presented with extended C-5 to C-8 or T-1 lesions or with complete loss of C-5 to C-6 or C-7 function as well as clinical and radiological suspi-cion of root avulsion. In our cohort of 36 patients, we found that the benefits of early surgery outweigh the drawbacks. Surgical dissection and identification was much easier and less tedious, due to the absence of scar tissue. Moreover, in all patients operated on early, the biceps muscle recovered to MRC grade 4. These results are at least equal to the re-sults obtained in delayed surgeries; therefore, we do not see any argument to change our direction.

Our results are in line with those of Bonney3 and Birch,2 who have been advocating early surgery for a long time. Given our experience, we support the plea for early surgery in cases of ATBPI, the first reinforcement from outside the United Kingdom.

The main argument to renounce early intervention is the potential for spontaneous recovery to occur. We be-lieve that this argument should not be generally applied to all ATBPIs. After all, waiting for rupture or avulsions to spontaneously recover is wasting costly time. The amount of regeneration declines as the interval between trauma and repair increases, and the patient is denied the ability to quickly start the recovery process.

In adopting early nerve reconstruction, we applied and modified the selection principles used by Bonney and Birch to identify ATBPIs with ruptures and avulsions. We propose an algorithm for patient selection, shown in Fig. 1 and described more extensively in the Methods. The preoperative workup consists of MRI or CTM.4,5 We use MRI as the imaging modality of choice and CTM for backup. The primary goal in our preoperative workup is to assess the presence of root avulsions. We reason that in the presence of a root avulsion, the severity of the lesion of neighboring clinically affected roots is likely to be ex-tensive enough that the chance for spontaneous recovery is

low. Therefore, the presence of avulsion justifies surgical exploration. Unfortunately, postganglionic neurotmetic le-sions cannot be reliably detected on clinical grounds or with current imaging techniques. The value of emerging imaging techniques such as diffusion tensor imaging or high-frequency ultrasound are promising but need evalua-tion in the early phase after trauma.8,35

During early surgery, dissection appeared to be straightforward given the absence of scar formation. Distal stumps could be easily repositioned proximally, thereby reducing the gap and consequently the length of the nerve grafts. In some cases, direct coaptation was possible, as in our experiences with specific types of neonatal BPIs.20,26 The disadvantages related to scar formation were decid-edly present if surgery was performed more than 2 weeks after the trauma. Two phenomena could be distinguished: stiffness of the nerves due to loss of flexibility and elastic-ity, and the presence of perineurial fibrosis inducing adhe-sions between the nerves and surrounding tissue.

Early surgery introduces specific challenges that need to be addressed. Identifying the site of resection between irreversibly damaged and viable nerve tissue in the early phase differs from that in the late phase. A clear demarca-tion between vital tissue and neuroma formation is not yet present. In fresh injuries, epineurial and intraneural hem-orrhages are present and potentially indicate the longitu-dinal extent of the lesion. In line with visual assessment of the nerve, the interpretation of intraoperative frozen sec-tions to assess the quality of the stumps must be appraised in early surgery as well. Myelin breakdown by phagocyto-sis is not yet present, and thus osmium stains may not be as useful as in the late surgical setting.22 Intraoperatively, we found clear nerve root avulsions and completely ruptured nerves in all patients. Therefore, assessing the severity of the nerve lesion did not pose a problem. However, should nerve lesions in continuity be encountered, interpretation of the nerve action potential recording would most likely need to be rethought.16

The key issue in early brachial plexus surgery is the ap-praisal of the proximal stump. In this respect, we judged the proximal stump to be viable enough for biceps reani-mation in only 2 patients who underwent early surgery. Given the results of biceps recovery after the related graft-ing procedures, we judged these cases correctly. However, our results in reanimating shoulder function were not very good. In these patients, we pursued shoulder movements despite an unreliable stump, for example, in the patient in case 3 in whom the proximal contributions to the long thoracic nerve were unresponsive. In 2 other cases, long grafts (7 and 9 cm, respectively) were necessary to bridge the nerve defect. These suboptimal grafting procedures were performed, although we realized beforehand that the chance for useful shoulder recovery was limited.

In the early phase of injury, cerebrospinal fluid leak-age during surgery occurred through the spinal foramen due to a fresh dural tear related to avulsion. The formation of a pseudomeningocele with a fibrotic delimitation, as seen in the late phase, usually prevents CSF leakage. The management of CSF leakage by meticulously plugging the intervertebral foramen requires special surgical attention in the early phase.

TABLE 3. Outcome of biceps strength according to MRC grade

Treatment No.Reconstruction

Procedure No.MRC Grade

0–2 3 4

Early (<14 days) 5NG 2 2OB2 2 2ICN 1 1

Intermediate 5NG 3 3ICN 2 1 1

Late (>2 mos) 26

NG 13 4 4 5OB1 2 1 1OB2 9 1 8ICN 2 2

Total 36NG 18 4 7 7OB1/OB2 13 2 0 11ICN 5 1 3 1

ICN = intercostal nerve transfer.Values indicate the number of patients.



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Early ATBPI exploration in total lesions provides the opportunity to reanimate C-8 and T-1 function. In the early phase, roots are still mobile and can be repositioned close to proximal stumps. Moreover, sensory and motor root filaments can be anatomically distinguished, and in our more recent experience, we established that direct stimu-lation of distal nerves could elicit a motor response up to 96 hours after trauma, facilitating functional targeting in reconstruction. In late surgery, these avulsed roots are usu-ally massively scarred and retracted distally. Reconstruc-tion is of no use because gaps are long. Besides, Schwann cell support for outgrowing axons is severely reduced and distal muscles atrophy during the time that axons elongate. We have attempted hand reanimation similar to our re-construction in neonatal BPIs,26 aiming for reanimation of some basic hand function in adults. This may be an impor-tant step forward in brachial plexus reconstruction since alternative techniques such as root reimplantation12,32 and application of contralateral C-7 transfer11,28,29,34 have not yet resulted in substantial improvement in regaining clinical usable hand function. Altogether, the challenges encoun-tered so far in early ATBPI surgery do not prevent us from continuing in this direction, but new experiences should be built to manage all specific aspects.

We recognize the limitations of our study. First, the number of patients who were referred early and who could be surgically treated early in this 3-year period was small. As ATBPIs are usually the result of a high-velocity motor vehicle incident, the first conditions that must be treated are potentially life-threatening lesions, usually lung con-tusions, blunt abdominal trauma, and associated fractures. Additionally, referring specialists are accustomed to an approach of waiting for spontaneous recovery. Since we changed our management approach, awareness of the need for early referral among neurologists and trauma special-ists has increased, and thus the number of patients that could be assessed early has increased as well. Despite the fact that the number of patients with sufficient follow-up was small, the differences between early and late ATBPI surgery as we have described are obvious. In addition, we have treated 15 more patients in the period from 2012 until now, during which our surgical findings have been similar to those described here.

Second, because the number of patients with sufficient follow-up was small, we cannot make very bold conclu-sions regarding the advantages of early repair in terms of final neurological recovery. We believe that the results for elbow flexion with early surgery were at least equal to those with delayed surgery. In 2 of the 5 early-treatment patients, a fascicular transfer had to be performed because viable proximal stumps for grafting were not available. This may have furbished our results as fascicular transfers have good results in late repair as well.9 The other early pa-tients were treated with nerve grafting or intercostal nerve transfer, for which recovery to MRC grade 4 is encourag-ing but not exceptional.

Third, the current analysis was limited primarily to the recovery of biceps strength. This outcome was chosen since it is the primary goal of ATBPI surgery, and recov-ery of elbow flexion was perceived in all patients. It would be highly interesting if early nerve reconstruction were to

yield better shoulder and hand function than late repair.Fourth, we did not prospectively quantify the ease of

surgery, for instance, operating time or blood loss during dissection of the damaged brachial plexus elements. In view of the heterogeneity of ATBPIs, multiple factors play a role, which are not always quantifiable. In addition, we do not have sufficient data to test our hypothesis that the ease in repositioning the distal stumps and the absence of neuroma formation lead to a shorter graft length.

The current series supports the experiences of others.1,2 We believe that early surgery for ATBPI should be further developed. Awareness should be created among referring specialists that early surgery is a potentially superior treat-ment option in ATBPI, requiring early referral. An addi-tional significant benefit of early referral is that coordina-tion of the essential diagnostic workup and the decision of when to operate is in the hands of a nerve surgical special-ist, without unnecessary delay.

ConclusionsEarly surgery for ATBPI is feasible and safe and results

in a good motor outcome, supporting further development of this treatment option. Referral patterns and customs should be adapted so that a specialized nerve surgeon can evaluate patients with such injuries as early as possible.

References 1. Birch R: Brachial plexus injury: the London experience with

supraclavicular traction lesions. Neurosurg Clin N Am 20:15–23, 2009

2. Birch R: Timing of surgical reconstruction for closed trau-matic injury to the supraclavicular brachial plexus. J Hand Surg Eur Vol 40:562–567, 2015

3. Bonney G: Watson-Jones Lecture, 1976. Some lesions of the brachial plexus. Ann R Coll Surg Engl 59:298–306, 1977

4. Carvalho GA, Nikkhah G, Matthies C, Penkert G, Samii M: Diagnosis of root avulsions in traumatic brachial plexus in-juries: value of computerized tomography myelography and magnetic resonance imaging. J Neurosurg 86:69–76, 1997

5. Doi K, Otsuka K, Okamoto Y, Fujii H, Hattori Y, Baliarsing AS: Cervical nerve root avulsion in brachial plexus injuries: magnetic resonance imaging classification and comparison with myelography and computerized tomography myelogra-phy. J Neurosurg 96 (3 Suppl):277–284, 2002

6. Fu SY, Gordon T: Contributing factors to poor functional recovery after delayed nerve repair: prolonged axotomy. J Neurosci 15:3876–3885, 1995

7. Fu SY, Gordon T: Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation. J Neurosci 15:3886–3895, 1995

8. Gallagher TA, Simon NG, Kliot M: Diffusion tensor imaging to visualize axons in the setting of nerve injury and recovery. Neurosurg Focus 39(3):E10, 2015

9. Garg R, Merrell GA, Hillstrom HJ, Wolfe SW: Comparison of nerve transfers and nerve grafting for traumatic upper plexus palsy: a systematic review and analysis. J Bone Joint Surg Am 93:819–829, 2011

10. Hems TE: Timing of surgical reconstruction for closed trau-matic injury to the supraclavicular brachial plexus. J Hand Surg Eur Vol 40:568–572, 2015

11. Hierner R, Berger AK: Did the partial contralateral C7-trans-fer fulfil our expectations? Results after 5 year experience. Acta Neurochir Suppl 100:33–35, 2007

12. Htut M, Misra VP, Anand P, Birch R, Carlstedt T: Motor re-


W. Pondaag et al.


covery and the breathing arm after brachial plexus surgical repairs, including re-implantation of avulsed spinal roots into the spinal cord. J Hand Surg Eur Vol 32:170–178, 2007

13. Jivan S, Kumar N, Wiberg M, Kay S: The influence of pre-surgical delay on functional outcome after reconstruction of brachial plexus injuries. J Plast Reconstr Aesthet Surg 62:472–479, 2009

14. Kay SP, Wiberg M, Thornton DJ: Nerves are living structures whose injury requires urgent repair. J Plast Reconstr Aes-thet Surg 63:1939–1940, 2010

15. Khu K, Midha R, Rochkind S: Management of adult brachial plexus injuries, in Quiñones-Hinojosa A (ed): Schmidek and Sweet: Operative Neurosurgical Techniques, ed 6. Phila-delphia: Saunders Elsevier, 2012, pp 2247–2260

16. Kline DG: Timing for brachial plexus injury: a personal ex-perience. Neurosurg Clin N Am 20:24–26, v, 2009

17. Liverneaux PA, Diaz LC, Beaulieu JY, Durand S, Oberlin C: Preliminary results of double nerve transfer to restore elbow flexion in upper type brachial plexus palsies. Plast Reconstr Surg 117:915–919, 2006

18. Magalon G, Bordeaux J, Legre R, Aubert JP: Emergency versus delayed repair of severe brachial plexus injuries. Clin Orthop Relat Res (237):32–35, 1988

19. Malessy MJ, de Ruiter GC, de Boer KS, Thomeer RT: Evalu-ation of suprascapular nerve neurotization after nerve graft or transfer in the treatment of brachial plexus traction lesions. J Neurosurg 101:377–389, 2004

20. Malessy MJ, Pondaag W: Neonatal brachial plexus palsy with neurotmesis of C5 and avulsion of C6: supraclavicular reconstruction strategies and outcome. J Bone Joint Surg Am 96:e174, 2014

21. Malessy MJ, Thomeer RT: Evaluation of intercostal to musculocutaneous nerve transfer in reconstructive brachial plexus surgery. J Neurosurg 88:266–271, 1998

22. Malessy MJ, van Duinen SG, Feirabend HK, Thomeer RT: Correlation between histopathological findings in C-5 and C-6 nerve stumps and motor recovery following nerve graft-ing for repair of brachial plexus injury. J Neurosurg 91:636–644, 1999

23. Medical Research Council: Aids to the Investigation of Pe-ripheral Nerve Injuries. Medical Research Council War Memorandom no. 7. London: His Majesty’s Stationery Of-fice, 1943

24. Narakas AO, Allieu Y, Alnot JY, Brunelli G, Merle M, Santos-Palazzi A, et al: [Complete supraclavicular paralysis. Surgical possibilities and results,] in Alnot JY, Narakas AO (eds): [Paralysis of the Brachial Plexus.] Paris: Expansion Scientifique Francaise, 1989, pp 130–162 (Fr)

25. Oberlin C, Béal D, Leechavengvongs S, Salon A, Dauge MC, Sarcy JJ: Nerve transfer to biceps muscle using a 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, 1994

26. Pondaag W, Malessy MJ: Recovery of hand function follow-ing nerve grafting and transfer in obstetric brachial plexus lesions. J Neurosurg 105 (1 Suppl):33–40, 2006

27. Samii M, Carvalho GA, Nikkhah G, Penkert G: Surgical reconstruction of the musculocutaneous nerve in traumatic brachial plexus injuries. J Neurosurg 87:881–886, 1997

28. Sammer DM, Kircher MF, Bishop AT, Spinner RJ, Shin AY: Hemi-contralateral C7 transfer in traumatic brachial plexus injuries: outcomes and complications. J Bone Joint Surg Am 94:131–137, 2012

29. Songcharoen P, Wongtrakul S, Mahaisavariya B, Spinner RJ: Hemi-contralateral C7 transfer to median nerve in the treat-ment of root avulsion brachial plexus injury. J Hand Surg Am 26:1058–1064, 2001

30. Stockinger T, Aszmann OC, Frey M: Clinical application of pectoral nerve transfers in the treatment of traumatic brachial plexus injuries. J Hand Surg Am 33:1100–1107, 2008

31. Sunderland S: Nerve Injuries and Their Repair: A Critical Appraisal. New York: Churchill Livingstone, 1991

32. Thomeer RT, Malessy MJ, Marani E: Nerve root repair. J Neurosurg 96 (1 Suppl):138–139, 2002

33. Tung THH, Moore AM: Brachial plexus injuries, in Mackin-non SE (ed): Nerve Surgery. New York: Thieme, 2015, pp 391–467

34. Yang G, Chang KW, Chung KC: A systematic review of con-tralateral C7 transfer for the treatment of traumatic brachial plexus injury: part 1. Overall outcomes. Plast Reconstr Surg 136:794–809, 2015

35. Zeidenberg J, Burks SS, Jose J, Subhawong TK, Levi AD: The utility of ultrasound in the assessment of traumatic pe-ripheral nerve lesions: report of 4 cases. Neurosurg Focus 39(3):E3, 2015

DisclosuresThe authors do not have financial or other disclosures in relation to this manuscript.

Author ContributionsConception and design: Pondaag, Malessy. Acquisition of data: Pondaag, van Driest. Analysis and interpretation of data: all authors. Drafting the article: all authors. Critically revising the article: Pondaag, Groen, Malessy. Reviewed submitted version of manuscript: van Driest, Groen, Malessy. Approved the final ver-sion of the manuscript on behalf of all authors: Pondaag. Statisti-cal analysis: Pondaag, van Driest. Study supervision: Malessy.

CorrespondenceWillem Pondaag: Leiden University Medical Center, Leiden, The Netherlands. [email protected].


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