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Functional outcome of nerve transfers for upper-type brachial plexus injuries
Journal of Plastic, Reconstructive & Aesthetic Surgery (2011) 64, 1007e1013
Functional outcome of nerve transfers for upper-type brachial plexus injuries Emmanuel P. Estrella a,b,* a
Microsurgery Unit, Department of Orthopedics, University of the Philippines-College of Medicine, Philippine General Hospital, UP Manila, Philippines b ASTRO (Advanced Study and Research in Orthopedics) Study Group, National Institutes of Health, University of the Philippines, Manila, Philippines Received 7 June 2010; accepted 2 February 2011
KEYWORDS Brachial plexus injury; Upper-type brachial plexus; Nerve transfer; Nerve surgery
Summary Purpose: The purpose of this study was to present the results of treatment using nerve transfers for elbow and shoulder function in patients with upper-type (C5eC7) brachial plexus injuries. Methods: A retrospective review of a single surgeon’s experience was done on the results of treatment using nerve transfers for shoulder abduction and external rotation and elbow flexion in nine patients with upper-type brachial plexus injuries from 2005 to 2008. The average age at the time of surgery was 32 years. The average time from injury to surgery was 6.6 months (range, 3e11 months). Two patients had single-nerve transfers from the ulnar nerve to the biceps branch of the musculocutaneous nerve, and seven patients had double-nerve transfers from the ulnar nerve to the biceps branch and from the median nerve to the brachialis branch of the musculocutaneous nerve. All patients had additional nerve transfers of the spinal accessory nerve to the suprascapular nerve for shoulder abduction and external rotation. The average follow-up for all patients was 27.7 months (range, 12e48 months). Results: On latest follow-up, elbow flexion strength of M4 was achieved in eight out of nine patients. The average time to achieve an elbow flexion grade M3 was 7.6 months (range, 5e12 months). The average elbow range of motion was 128 19 with average elbow flexor strength of 2.7 1.5 kg. Shoulder abduction and external rotation were achieved in eight out of nine patients (average of 70 41 and 61 46 , respectively). Complications include transient sensory abnormalities in four patients and transient motor weakness in one. Conclusion: Nerve transfer procedures can result in functional recovery of the shoulder and elbow function in patients with upper-type brachial plexus injuries. ª 2011 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved.
* Microsurgery Unit, Department of Orthopedics, University of the Philippines-Philippine General Hospital, Manila 1000, Philippines. Tel.: þ63 (632) 5548466; fax: þ63 (632) 5218538. E-mail address: [email protected]. 1748-6815/$ - see front matter ª 2011 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.bjps.2011.02.002
1008 High-speed motor vehicular accidents account for a majority of all traumatic brachial plexus injuries.1 In developing countries, the number of motorcycle accidents has been steadily increasing, as this is the one of the main means of transportation.2 Incomplete injuries of the brachial plexus, especially those with upper-type injuries (C5eC6/7), have been reported to have a good functional outcome.3 Most brachial plexus surgeons would agree that restoration of elbow flexion followed by shoulder function are the top priorities in the reconstruction of brachial plexus lesion. The options for the restoration of elbow and shoulder function in brachial plexus lesions are many. The type of reconstruction is usually dependent on the type of injury, the availability of donor nerves or muscle to be used for the reconstruction and the time elapsed from injury to surgical treatment.4 One of the most versatile procedures for the restoration of upper-extremity function for brachial plexus lesions is nerve transfer. Nerve transfers allow the surgery to be performed on unscarred tissues and minimise muscle reinnervation time by making the nerve repair site closer to the target muscles.5 In 1994, Oberlin et al.6 reported a fascicular transfer from the ulnar nerve to the biceps branch of the musculocutaneous nerve to restore elbow flexion in upper-type brachial plexus injuries. Subsequent reports on the technique showed that elbow flexion strength of M4 can be achieved in 62e93% of patients with upper-type brachial plexus injuries using Oberlin’s method of nerve transfer.7e12 Poor results were attributed to C5eC7 avulsions, long preoperative delays, increasing age9 and possible lesions to the C8eT1.10 Recently, double fascicular or nerve transfer to two elbow flexors showed a majority of patients achieving M4 elbow flexion with little morbidity to the donor nerve.13,14 After elbow flexion, the second priority in upper-type brachial plexus injuries is the restoration of shoulder abduction and external rotation. The use of nerve transfers to restore shoulder function has been reported to restore M3 shoulder abduction in 80e100% of patients using single-, double- or multiple-nerve transfers.8,12,15e17 The objective of this study was to evaluate the clinical outcome of nerve transfers for the restoration of shoulder and elbow function in patients with upper-type brachial plexus injuries.
Patients and methods Patients The demographic data of the patients are shown on Table 1. Nine patients with incomplete brachial plexus injuries from 2005 to 2008, who had single- or double- nerve transfers from the ulnar nerve or the ulnar and median nerves for the restoration of elbow flexion and nerve transfers of the spinal accessory nerve to the suprascapular nerve for shoulder function, were identified and reviewed to determine results of treatment. There were seven males and two females. The average age of the patients at the time of surgery was 32 years (range, 17e47 years). The average time from injury to surgery was 6.6 3.0 months (range, 3e11 months), and the average
E.P. Estrella follow-up period was 27.7 13.3 months (range, 12e48 months). The protocol was approved by the ethics review board of the institution. Inclusion criteria for the study were patients with uppertype (C5eC7) brachial plexus injuries, who had nerve transfers for elbow flexion and shoulder abduction. The minimum follow-up period was 12 months. None of the patients had cervical myelography or computed tomography (CT) myelogram. All patients had no elbow flexion, shoulder abduction or shoulder external rotation preoperatively. Elbow extension was absent in five patients, and M3 in four. The indications for nerve transfers for shoulder abduction and external rotation and elbow flexion have been described in the literature.6,11 Associated injuries Six patients had associated injuries (Table 1). All associated injuries were fractures and/or dislocations, and were managed by the referring physician prior to referral to the Microsurgery Unit.
Surgical technique Technique of brachial plexus exploration All patients had standard brachial plexus exploration under general anaesthesia without the use of muscle relaxants. The nerve was stimulated at 10e20 mA using a portable hand-held peripheral nerve stimulator (Fisher & Paykel, Auckland, New Zealand) proximal to the neuroma, and distal contraction was observed. An internal neurolysis was carried out in the C5eC7 nerve roots to visualise the fascicles.1 Neuroma resection and nerve grafting was carried out if, after neurolysis, no normal-looking fascicles were visualised. If the roots were judged to be avulsed or non-graftable, a nerve transfer was done. We did not use any intra-operative monitoring, such as somatosensory evoked potentials (SSPEs) or spinal evoked potentials (SEPs), as well as choline acetyltransferase determination, as this was not available in our institution. We judged a nerve root to be avulsed or nongraft able if: (1) there was an obvious discontinuity of the root as it leaves the neural foramenein these cases, the foramen was empty and there was no available nerve material proximal to the neuroma and (2) under the operating microscope, there was no normal-appearing fascicle after external and internal neurolysis up to the neural foramen. These intra-operative findings were compared with our preoperative clinical and ancillary examination and a decision was made, if the involved root was suitable for grafting. If there was any doubt that the root was avulsed or non-graft able, we proceeded with the nerve transfers. In all cases, we deemed the C5 and C6 nerve root to be avulsed or non-graftable. Epineural adhesions were released first and, then, an epineuriectomy was done to expose the fascicles in all cases. Fascicle appearance was judged clinically under the operating microscope. Neurolysis of root elements was extended proximally up to the neural foramen and as distal as possible, if necessary.
Patient Demographic Data.
Patient
Age (years)
Sex
Mechanism of injury
Dominant hand involvement
Root involvement
Pre-operative delay (months)
Post-operative follow-up (months)
Associated injuries
Additional procedures done aside from neurolysis of C7
1
40
M
MA
No
C5eC7
7
40
2
17
M
MA
No
C5eC7
8
48
Open reduction and plating of symphysis pubis ORIF of all three fractures, Tendon transfer to restore finger and wrist extension
3 4 5
26 47 21
M F F
MA VA MA
Yes No No
C5eC7 C5eC7 C5eC7
3 6 11
42 18 16
Symphisis Pubis Diastasis; Cerebral Contusion Closed Fractures of Femoral Shaft R; Closed Tibial Shaft Fracture, L; ACL tear, L knee; Peroneal Nerve Palsy; Closed olecranon fracture, L; Cerebral Contusion None None Mandibular Fracture
6 7
28 39
M M
MA MA
No No
C5eC7 C5eC7
11 6
33 12
8 9
35 34
M M
MA MA
No Yes
C5eC7 C5eC7
3 4
AVE.
32 9 years
7M:2F
2Y:7N
C5eC7: 9
6.6 3.0 mos
16 24
Clavicle fracture Closed Radius and ulna fracture, L; Closed Radial head Fracture, L C7 transverse process None
None None Interdental wiring: mandible None ORIF of Radius and Ulna Fracture, L; Resection of radial Head, L Debridement, neck None
27.7 13.3 mos
None: 3 Yes:6
None: 4; Yes :5
Head: Brachial plexus injury, neurolysis, nerve transfer
Table 1
VA-Vehicular accident (pedestrian); MA- Motorcycle Accident; ACL-Anterior Cruciate Ligament; ORIF-Open Reduction Internal Fixation.
1009
1010
Nerve transfers to restore shoulder and elbow function The technique of nerve transfers for restoration of shoulder and elbow function has been well described in the literature.13,14 In this study, for restoration of elbow function, our first two patients (#1 and #2) had single-nerve transfers using a fascicle or fascicles of the ulnar nerve, while the rest had double-nerve transfers using both fascicles of the ulnar and median nerve to reinnervate the biceps and brachialis, respectively (Figure 1). For restoration of shoulder function, all patients had spinal accessory nerve to suprascapular nerve transfer.
Early postoperative management A soft neck collar and arm sling was worn for 4 weeks postoperatively. Gradual passive range of motion exercises were started at the end of the 4th week, until the first signs of muscle contraction were observed. Once contraction of biceps was observed, flexion exercises of the long flexors of the hand using a ‘stress ball’ and resistive wrist flexion exercises were advised 20 every 6 h, until anti-gravity elbow flexion was achieved.
E.P. Estrella was gradually increased. The heaviest weight that the patient can carry while flexing the elbow from 0 to 90 was recorded. Shoulder abduction was measured with the patient standing and shoulder laterally abducted. The angle between the long axis of the arm and the spine was measured from behind. Shoulder external rotation was measured with the elbow in 90 and in full internal rotation anterior to the abdomen. The angle between the long axis of the forearm and the abdomen was measured. All angle measurements were done three times, and the average taken using a standard goniometer. Pain was evaluated using the visual analogue scale (VAS) for pain before and after the reconstructive procedure. Grip strength was measured three times as well and the average taken. This was done preoperatively and post-operatively using the Jamar dynamometer (Sammons-Weston, Bolingbrook, IL, USA).
Data analysis All continuous data were expressed as mean SD. A t-test was used to compare pre- and postoperative pain scores and average grip strength (in kgf) using the Statistical Package for Social Sciences (SPSS) package 11.0. A p < 0.05 was considered significant.
Outcomes’ assessment
Results
All patients were followed-up at the Microsurgery Clinic. Our primary outcomes were restoration of elbow flexion, shoulder abduction and shoulder external rotation. Our secondary outcomes were pain relief, grip strength and improvement of previously weak or non-functioning muscles. Muscle strength for all muscles was evaluated using the modified British Medical Research Council (BMRC) grade to quantify muscle strength. On follow-up, the strength of the elbow flexion was assessed by asking the patient to hold a designated weight (in kilograms) and flex the elbow once to 90 . The weight was started at 100 g, and
The outcomes for elbow and shoulder functions are shown in Table 2. Elbow flexion strength of M4 was achieved in eight out of nine patients with an average of 128 19 (range, 100e155 ). In terms of muscle innervation, the average time for the first biceps contraction (M1) was at 4.4 1.7 months (range, 3e7 months) and the average time to achieve an MRC grade of M3 for elbow flexion was 7.6 2.9 months (range, 5e12 months). The average weight that the elbow could lift was 2.7 1.5 kg (range, 1e5 kg) (Figure 2). However, we noticed that, in some of our patients, a heavier weight for elbow flexion was
Figure 1 (Patient 7). A 39 year old male who had a double-nerve transfer of the left upper extremity for elbow flexion. Left arrow was the partial ulnar nerve transfer to the biceps branch and the right arrow was the partial median nerve transfer to the brachialis branch of the musculocutaneous nerve. On recent fullow-up at one year, M4 flexion grade was evident with a flexion force of 3 kg.
Head: Brachial plexus injury, neurolysis, nerve transfer Table 2 Patient
Summary of Functional Outcome for Shoulder and Elbow Reconstruction. Shoulder function Abduction ( )/MRC
a
1011
External rotation ( )/MRC
Elbow flexion
Range ( )
MRC
PAIN Initial elbow flexion strength in months M1
M3
Pre-Op
Post-Op
Weight in kilograms
1 2a 3 4 5
50/M3 120/M5 120/M4 50/M4 0
20/M3 130/M4 135/M4 60/M3 0
0e110 30e155 0e140 0e100 0
M4 M4 M4 M4 M1
7 3 3 4 6
12 7 6 8 0
10 7 7 3.5 0
4 5 5 0 0
6 7 8 9
20/M3 40/M3 45/M3 115/M4
45/M4 30/M3 20/M3 45/M3
0e135 0e135 15e110 10e140
M4 M4 M4 M4
7 4 3 3
12 5 5 6
10 6 7 7
6 2 2 5
1 4 4 1 0 (0.5 kg after Steindler Procedure) 2 3 1.5 5
AVE.
70 41b
61 46b
128 19b
4.4 1.7
7.6 2.9
6.4 3.1
3.2 2.3
2.7 1.6 kgb
a b
Single nerve (partial ulnar nerve) transfer. Average excluded patients with no recovery (M0).
possible if the weight was given to the patient with elbow already flexed at 90 . When the same weight was given with the elbow extended, the patient could not flex the elbow from 0 to 90 . The patient with no anti-gravity recovery of elbow flexion underwent a Steindler procedure 17 months after the initial double-nerve transfer. At 9 months postSteindler procedure, she has 0.5-kg elbow flexion strength. Shoulder abduction and external rotation was achieved in eight out of nine patients. For our secondary outcomes, the average VAS for pain significantly decreased from 6.4 3.1 to 3.2 2.2 (p < 0.05). There was no significant change in the average grip strength before (10.5 3.8 kgf/45% of contralateral) and on latest follow-up (11.9 3.8 kgf/42% of contralateral) (p > 0.05). Previously weak or absent elbow extension improved to M3 in six out of nine and to M4 in five out of nine patients.
Complications Two patients reported sensory abnormalities of both the ulnar and median nerve territories after the surgery, while another two had only sensory disturbance of the ulnar nerve territory using the two-point discrimination test. These, however, resolved within 3 months post reconstruction. In one patient, there was a downgrade of the flexor carpi radialis muscle from M5 to M4 after partial median nerve transfer with improvement to M5 8 months post-operatively (patient #9). Two patients continue to have tingling sensation over the index finger (patients #3 and #6).
Discussion Although restoration of elbow flexion was the main objective in the treatment of patients with brachial plexus injuries affecting the upper roots, shoulder function was also addressed during surgical reconstruction.6,12,13 In this case series, we evaluated patients with upper-type brachial plexus injuries treated with nerve transfers for restoration of elbow and shoulder function. Nerve surgery in brachial plexus reconstruction has been regarded as superior to any palliative muscle transfers and is usually indicated in incomplete, early injuries affecting the shoulder and elbow.3,13 In cases of avulsion injuries where nerve grafting or repair was not possible, nerve transfers offer a very good surgical alternative as a nerve reconstructive procedure.6e13
Restoration of elbow flexion and shoulder function
Figure 2 (Patient 2). Elbow flexion strength was 4 kg after single-nerve transfer using part of the ulnar nerve to the biceps branch of the musculocutaneous nerve at 48 months postoperatively.
The return of elbow flexion was a direct result of nerve transfers to the biceps and/or brachialis branch of the musculocutaneous nerve. Eight of nine patients recovered M4 elbow flexion strength, with an average flexion force of 2.7 1.6 kg, which was inferior compared with the doublenerve transfer series of Liverneaux et al.,14 (3.7 kg) and the
1012 single-nerve transfers of Teboul et al.10 (4.15 kg). However, it was comparable to the single-nerve transfer series of Sungpet et al.9 at 1.8 kg and of Leechavengvongs et al.7 in 1998 (2.6 kg) and in 2006 (2.6 kg).8 Tung et al.18 in 2003 reported dual elbow flexor innervations by transferring a part of the ulnar nerve to the biceps branch of the musculocutaneous nerve and various nerve donors to the brachialis in eight patients. Their results showed 100% M4 recovery of elbow flexion. Recently, single- and double-nerve transfers were compared,19 which showed similar elbow flexion and supination strength. The results of double-nerve transfers for elbow flexion showed an average of 84% of patients regaining M4 elbow flexion strength.3,14,19 We had one failure of elbow flexion, where the procedure was done 11 months post injury. Although the time frame is still within the recommendation of some authors,14 this might be a factor why elbow flexion strength did not progress beyond M1, even after 17 months after surgery. We also noticed that elbow extension improved to M3 in six out of nine patients. These results, however, cannot be attributed to the procedure alone, as improvement of the previously weak or non-functioning triceps may have occurred over time. Further investigations may be needed to verify this. The results of our shoulder reconstruction were inferior compared with that of Leechavengvongs et al.,8 Bertelli et al.10 and Uerpairojkit et al.15 One of the differences may be due to the number of donor nerves or muscles reinnervated to reconstruct shoulder function. In the report by Leechavengvongs et al.8 and Bertelli et al.,11 both the axillary nerve and suprascapular nerve were innervated. In the study by Uerpairojkit et al.,15 the serratus anterior muscle was innervated with a branch from the thoracodorsal nerve in addition to nerve transfers to the suprascapular nerve and axillary nerve. Essentially, three nerves were recipients of nerve transfers. In our case series, only one nerve transfer was used in the reconstruction of shoulder abduction and external rotation. Suzuki et al.16 noted that better shoulder function was observed among patients without scapular winging compared with those with winging. They advised that the long thoracic nerve palsy must be addressed to achieve better results for the shoulder reconstruction. Cardenas-Mejia et al.20 reported that range of motion of shoulder abduction increases with increasing number of donor nerves in early stage nerve transfers for shoulder abduction. However, in their study, different donor nerves were used in different combinations in assessing the outcomes and the triple-nerve transfers consisted only of four patients compared with the 43 patients each of singleand double-nerve transfers. However, it is clear that by providing more axons to the recipient nerve, the chances of reinnervation become higher. In cases of single-nerve transfer for shoulder reconstruction in upper-type brachial plexus injuries using the spinal accessory nerve transfer to the suprascapular nerve, results from two authors showed an abduction of 66 and 77 and external rotation of 44 and 16.7 , respectively.12,16 The results of single-nerve transfer for shoulder function of these two studies were comparable with ours at an average of 70 of shoulder abduction and 61 of external rotation. However, in the literature, single-nerve transfers12,16,17 for the restoration of shoulder function remain to be inferior compared with multiple-nerve transfers.8,11,20 Although the concept of double-nerve transfer
E.P. Estrella being better than single-nerve transfer in elbow flexion restoration has been recently questioned by Carlsen et al.,19 the same may not be true for shoulder functional restoration. More muscles may be needed to restore shoulder function, as shoulder motion is more complex than elbow motion, and a greater weight proportion of the upper extremity will be borne by the shoulder muscles as opposed to the elbow flexors. In terms of complications of the nerve transfers, none of these reports showed any on the donor nerve innervations. In this study, four patients experienced abnormality to the ulnar and median distribution after surgery. This resolved after 3 months. A downgrade of the flexor carpi radialis from M5 to M4 was observed in one case. The muscle recovered to M5 after 8 months. We always use an intra-operative nerve stimulator to identify fascicles for transfer, making sure that they are redundant so that when sacrificed, minimal morbidity will be expected. The probable cause for this may be secondary to the fascicular dissection of the median nerve or that the fascicle that served as donor may have contributed heavily to the sensory or motor innervation. On final follow-up, there was a significant reduction of pain in a majority of patients. Root avulsion and deafferentation pain have been reported as the cause of most brachial plexus pain.21,22 Bertelli and Ghizoni23 reported that brachial plexus pain is probably a result of non-avulsed roots, and that grafting on these non-avulsed roots results in a substantial relief of pain. The authors also argued that nerve transfers per se does not relieve pain, as these are primarily motor nerves and are not associated with any cutaneous area of pain, such as the hand or forearm. It may be possible that during surgical exploration of the brachial plexus, some form of decompression of the plexus elements occurred, which might explain pain relief. However, this speculation cannot be supported by this article, and further studies might be needed to prove this. In summary, nerve transfers for upper-type brachial plexus injuries were effective in regaining function of the shoulder and elbow.
Funding None.
Conflicts of interest None declared.
Ethical approval Approved.
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1013 13. Mackinnon S, Novak C, Myckatyn T, Tung T. Results of reinnervation of the biceps and brachialis muscles with a double fascicular transfer for elbow flexion. J Hand Surg 2005;30A: 978e85. 14. Liverneaux P, Diaz L, Beaulieu JV, Durand S, Oberlin C. Preliminary results of double nerve transfer to restore elbow flexion in upper type brachial plexus palsies. Plast Recon Surg 2006;117(3):915e9. 15. Uerpairojkit C, Leechavengnongs S, Witoonchart K, Malungpaishorpe K, Raksakulkiat R. Nerve transfer to serratus anterior mualce using the thoracodorsal nerve for winged scapula in C5 and C6 brachial plexus root avulsions. J Hand Surg 2009;34A:74e8. 16. Suzuki K, Doi K, Hattori Y, Pagsaligan JM. Long-term results of spinal accessory nerve transfer to the suprascapular nerve in upper type paralysis of brachial plexus injury. J Reconstr Microsurg 2007;23(6):295e9. 17. Terzis JK, Kostas I. Suprascapular nerve reconstruction in 118 cases of adult posttraumatic brachial plexus. Plast Reconstr Surg 2006;117:613e29. 18. Tung TH, Novak CB, Mackinnon SE. Nerve transfers to the biceps and brachialis branches to improve elbow flexion strength after brachial plexus injuries. J Neurosurg 2003;98:313e8. 19. Carlsen BT, Bishop AT, Spinner RJ, Shin AY. Comparison of single and double nerve transfer for elbow flexion after brachial plexus injury. Plast Reconstr Surg; 2010; doi: 10.1097/PRS.0b013e3181f95be7. PMID: 20871484. 20. Cardenas-Mejia A, O’Boyle CP, Chen KT, Chuang DCC. Evaluation of single-, double-, and triple-nerve transfers for shoulder abduction in 90 patients with supraclavicular brachial plexus injury. Plast Reconstr Surg 2008;122:1470e8. 21. Sindou MP, Blondet E, Emery E, Mertens P. Microsurgical lesioning in the dorsal root entry zone for pain due to brachial plexus avulsion: a prospective series of 55 patients. J Neurosurg 2005;102:1018e28. 22. Parry CB. Pain in avulsion lesions of the brachial plexus. Pain 1980;9:41e53. 23. Bertelli JA, Ghizoni MF. Pain after avulsion injuries and complete palsy of the brachial plexus: the possible role of nonavulsed roots in pain generation. Neurosurgery 2008; 62:1104e14.
Functional outcome of nerve transfers for upper-type brachial plexus injuries Emmanuel P. Estrella a,b,* a
Microsurgery Unit, Department of Orthopedics, University of the Philippines-College of Medicine, Philippine General Hospital, UP Manila, Philippines b ASTRO (Advanced Study and Research in Orthopedics) Study Group, National Institutes of Health, University of the Philippines, Manila, Philippines Received 7 June 2010; accepted 2 February 2011
KEYWORDS Brachial plexus injury; Upper-type brachial plexus; Nerve transfer; Nerve surgery
Summary Purpose: The purpose of this study was to present the results of treatment using nerve transfers for elbow and shoulder function in patients with upper-type (C5eC7) brachial plexus injuries. Methods: A retrospective review of a single surgeon’s experience was done on the results of treatment using nerve transfers for shoulder abduction and external rotation and elbow flexion in nine patients with upper-type brachial plexus injuries from 2005 to 2008. The average age at the time of surgery was 32 years. The average time from injury to surgery was 6.6 months (range, 3e11 months). Two patients had single-nerve transfers from the ulnar nerve to the biceps branch of the musculocutaneous nerve, and seven patients had double-nerve transfers from the ulnar nerve to the biceps branch and from the median nerve to the brachialis branch of the musculocutaneous nerve. All patients had additional nerve transfers of the spinal accessory nerve to the suprascapular nerve for shoulder abduction and external rotation. The average follow-up for all patients was 27.7 months (range, 12e48 months). Results: On latest follow-up, elbow flexion strength of M4 was achieved in eight out of nine patients. The average time to achieve an elbow flexion grade M3 was 7.6 months (range, 5e12 months). The average elbow range of motion was 128 19 with average elbow flexor strength of 2.7 1.5 kg. Shoulder abduction and external rotation were achieved in eight out of nine patients (average of 70 41 and 61 46 , respectively). Complications include transient sensory abnormalities in four patients and transient motor weakness in one. Conclusion: Nerve transfer procedures can result in functional recovery of the shoulder and elbow function in patients with upper-type brachial plexus injuries. ª 2011 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved.
* Microsurgery Unit, Department of Orthopedics, University of the Philippines-Philippine General Hospital, Manila 1000, Philippines. Tel.: þ63 (632) 5548466; fax: þ63 (632) 5218538. E-mail address: [email protected]. 1748-6815/$ - see front matter ª 2011 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.bjps.2011.02.002
1008 High-speed motor vehicular accidents account for a majority of all traumatic brachial plexus injuries.1 In developing countries, the number of motorcycle accidents has been steadily increasing, as this is the one of the main means of transportation.2 Incomplete injuries of the brachial plexus, especially those with upper-type injuries (C5eC6/7), have been reported to have a good functional outcome.3 Most brachial plexus surgeons would agree that restoration of elbow flexion followed by shoulder function are the top priorities in the reconstruction of brachial plexus lesion. The options for the restoration of elbow and shoulder function in brachial plexus lesions are many. The type of reconstruction is usually dependent on the type of injury, the availability of donor nerves or muscle to be used for the reconstruction and the time elapsed from injury to surgical treatment.4 One of the most versatile procedures for the restoration of upper-extremity function for brachial plexus lesions is nerve transfer. Nerve transfers allow the surgery to be performed on unscarred tissues and minimise muscle reinnervation time by making the nerve repair site closer to the target muscles.5 In 1994, Oberlin et al.6 reported a fascicular transfer from the ulnar nerve to the biceps branch of the musculocutaneous nerve to restore elbow flexion in upper-type brachial plexus injuries. Subsequent reports on the technique showed that elbow flexion strength of M4 can be achieved in 62e93% of patients with upper-type brachial plexus injuries using Oberlin’s method of nerve transfer.7e12 Poor results were attributed to C5eC7 avulsions, long preoperative delays, increasing age9 and possible lesions to the C8eT1.10 Recently, double fascicular or nerve transfer to two elbow flexors showed a majority of patients achieving M4 elbow flexion with little morbidity to the donor nerve.13,14 After elbow flexion, the second priority in upper-type brachial plexus injuries is the restoration of shoulder abduction and external rotation. The use of nerve transfers to restore shoulder function has been reported to restore M3 shoulder abduction in 80e100% of patients using single-, double- or multiple-nerve transfers.8,12,15e17 The objective of this study was to evaluate the clinical outcome of nerve transfers for the restoration of shoulder and elbow function in patients with upper-type brachial plexus injuries.
Patients and methods Patients The demographic data of the patients are shown on Table 1. Nine patients with incomplete brachial plexus injuries from 2005 to 2008, who had single- or double- nerve transfers from the ulnar nerve or the ulnar and median nerves for the restoration of elbow flexion and nerve transfers of the spinal accessory nerve to the suprascapular nerve for shoulder function, were identified and reviewed to determine results of treatment. There were seven males and two females. The average age of the patients at the time of surgery was 32 years (range, 17e47 years). The average time from injury to surgery was 6.6 3.0 months (range, 3e11 months), and the average
E.P. Estrella follow-up period was 27.7 13.3 months (range, 12e48 months). The protocol was approved by the ethics review board of the institution. Inclusion criteria for the study were patients with uppertype (C5eC7) brachial plexus injuries, who had nerve transfers for elbow flexion and shoulder abduction. The minimum follow-up period was 12 months. None of the patients had cervical myelography or computed tomography (CT) myelogram. All patients had no elbow flexion, shoulder abduction or shoulder external rotation preoperatively. Elbow extension was absent in five patients, and M3 in four. The indications for nerve transfers for shoulder abduction and external rotation and elbow flexion have been described in the literature.6,11 Associated injuries Six patients had associated injuries (Table 1). All associated injuries were fractures and/or dislocations, and were managed by the referring physician prior to referral to the Microsurgery Unit.
Surgical technique Technique of brachial plexus exploration All patients had standard brachial plexus exploration under general anaesthesia without the use of muscle relaxants. The nerve was stimulated at 10e20 mA using a portable hand-held peripheral nerve stimulator (Fisher & Paykel, Auckland, New Zealand) proximal to the neuroma, and distal contraction was observed. An internal neurolysis was carried out in the C5eC7 nerve roots to visualise the fascicles.1 Neuroma resection and nerve grafting was carried out if, after neurolysis, no normal-looking fascicles were visualised. If the roots were judged to be avulsed or non-graftable, a nerve transfer was done. We did not use any intra-operative monitoring, such as somatosensory evoked potentials (SSPEs) or spinal evoked potentials (SEPs), as well as choline acetyltransferase determination, as this was not available in our institution. We judged a nerve root to be avulsed or nongraft able if: (1) there was an obvious discontinuity of the root as it leaves the neural foramenein these cases, the foramen was empty and there was no available nerve material proximal to the neuroma and (2) under the operating microscope, there was no normal-appearing fascicle after external and internal neurolysis up to the neural foramen. These intra-operative findings were compared with our preoperative clinical and ancillary examination and a decision was made, if the involved root was suitable for grafting. If there was any doubt that the root was avulsed or non-graft able, we proceeded with the nerve transfers. In all cases, we deemed the C5 and C6 nerve root to be avulsed or non-graftable. Epineural adhesions were released first and, then, an epineuriectomy was done to expose the fascicles in all cases. Fascicle appearance was judged clinically under the operating microscope. Neurolysis of root elements was extended proximally up to the neural foramen and as distal as possible, if necessary.
Patient Demographic Data.
Patient
Age (years)
Sex
Mechanism of injury
Dominant hand involvement
Root involvement
Pre-operative delay (months)
Post-operative follow-up (months)
Associated injuries
Additional procedures done aside from neurolysis of C7
1
40
M
MA
No
C5eC7
7
40
2
17
M
MA
No
C5eC7
8
48
Open reduction and plating of symphysis pubis ORIF of all three fractures, Tendon transfer to restore finger and wrist extension
3 4 5
26 47 21
M F F
MA VA MA
Yes No No
C5eC7 C5eC7 C5eC7
3 6 11
42 18 16
Symphisis Pubis Diastasis; Cerebral Contusion Closed Fractures of Femoral Shaft R; Closed Tibial Shaft Fracture, L; ACL tear, L knee; Peroneal Nerve Palsy; Closed olecranon fracture, L; Cerebral Contusion None None Mandibular Fracture
6 7
28 39
M M
MA MA
No No
C5eC7 C5eC7
11 6
33 12
8 9
35 34
M M
MA MA
No Yes
C5eC7 C5eC7
3 4
AVE.
32 9 years
7M:2F
2Y:7N
C5eC7: 9
6.6 3.0 mos
16 24
Clavicle fracture Closed Radius and ulna fracture, L; Closed Radial head Fracture, L C7 transverse process None
None None Interdental wiring: mandible None ORIF of Radius and Ulna Fracture, L; Resection of radial Head, L Debridement, neck None
27.7 13.3 mos
None: 3 Yes:6
None: 4; Yes :5
Head: Brachial plexus injury, neurolysis, nerve transfer
Table 1
VA-Vehicular accident (pedestrian); MA- Motorcycle Accident; ACL-Anterior Cruciate Ligament; ORIF-Open Reduction Internal Fixation.
1009
1010
Nerve transfers to restore shoulder and elbow function The technique of nerve transfers for restoration of shoulder and elbow function has been well described in the literature.13,14 In this study, for restoration of elbow function, our first two patients (#1 and #2) had single-nerve transfers using a fascicle or fascicles of the ulnar nerve, while the rest had double-nerve transfers using both fascicles of the ulnar and median nerve to reinnervate the biceps and brachialis, respectively (Figure 1). For restoration of shoulder function, all patients had spinal accessory nerve to suprascapular nerve transfer.
Early postoperative management A soft neck collar and arm sling was worn for 4 weeks postoperatively. Gradual passive range of motion exercises were started at the end of the 4th week, until the first signs of muscle contraction were observed. Once contraction of biceps was observed, flexion exercises of the long flexors of the hand using a ‘stress ball’ and resistive wrist flexion exercises were advised 20 every 6 h, until anti-gravity elbow flexion was achieved.
E.P. Estrella was gradually increased. The heaviest weight that the patient can carry while flexing the elbow from 0 to 90 was recorded. Shoulder abduction was measured with the patient standing and shoulder laterally abducted. The angle between the long axis of the arm and the spine was measured from behind. Shoulder external rotation was measured with the elbow in 90 and in full internal rotation anterior to the abdomen. The angle between the long axis of the forearm and the abdomen was measured. All angle measurements were done three times, and the average taken using a standard goniometer. Pain was evaluated using the visual analogue scale (VAS) for pain before and after the reconstructive procedure. Grip strength was measured three times as well and the average taken. This was done preoperatively and post-operatively using the Jamar dynamometer (Sammons-Weston, Bolingbrook, IL, USA).
Data analysis All continuous data were expressed as mean SD. A t-test was used to compare pre- and postoperative pain scores and average grip strength (in kgf) using the Statistical Package for Social Sciences (SPSS) package 11.0. A p < 0.05 was considered significant.
Outcomes’ assessment
Results
All patients were followed-up at the Microsurgery Clinic. Our primary outcomes were restoration of elbow flexion, shoulder abduction and shoulder external rotation. Our secondary outcomes were pain relief, grip strength and improvement of previously weak or non-functioning muscles. Muscle strength for all muscles was evaluated using the modified British Medical Research Council (BMRC) grade to quantify muscle strength. On follow-up, the strength of the elbow flexion was assessed by asking the patient to hold a designated weight (in kilograms) and flex the elbow once to 90 . The weight was started at 100 g, and
The outcomes for elbow and shoulder functions are shown in Table 2. Elbow flexion strength of M4 was achieved in eight out of nine patients with an average of 128 19 (range, 100e155 ). In terms of muscle innervation, the average time for the first biceps contraction (M1) was at 4.4 1.7 months (range, 3e7 months) and the average time to achieve an MRC grade of M3 for elbow flexion was 7.6 2.9 months (range, 5e12 months). The average weight that the elbow could lift was 2.7 1.5 kg (range, 1e5 kg) (Figure 2). However, we noticed that, in some of our patients, a heavier weight for elbow flexion was
Figure 1 (Patient 7). A 39 year old male who had a double-nerve transfer of the left upper extremity for elbow flexion. Left arrow was the partial ulnar nerve transfer to the biceps branch and the right arrow was the partial median nerve transfer to the brachialis branch of the musculocutaneous nerve. On recent fullow-up at one year, M4 flexion grade was evident with a flexion force of 3 kg.
Head: Brachial plexus injury, neurolysis, nerve transfer Table 2 Patient
Summary of Functional Outcome for Shoulder and Elbow Reconstruction. Shoulder function Abduction ( )/MRC
a
1011
External rotation ( )/MRC
Elbow flexion
Range ( )
MRC
PAIN Initial elbow flexion strength in months M1
M3
Pre-Op
Post-Op
Weight in kilograms
1 2a 3 4 5
50/M3 120/M5 120/M4 50/M4 0
20/M3 130/M4 135/M4 60/M3 0
0e110 30e155 0e140 0e100 0
M4 M4 M4 M4 M1
7 3 3 4 6
12 7 6 8 0
10 7 7 3.5 0
4 5 5 0 0
6 7 8 9
20/M3 40/M3 45/M3 115/M4
45/M4 30/M3 20/M3 45/M3
0e135 0e135 15e110 10e140
M4 M4 M4 M4
7 4 3 3
12 5 5 6
10 6 7 7
6 2 2 5
1 4 4 1 0 (0.5 kg after Steindler Procedure) 2 3 1.5 5
AVE.
70 41b
61 46b
128 19b
4.4 1.7
7.6 2.9
6.4 3.1
3.2 2.3
2.7 1.6 kgb
a b
Single nerve (partial ulnar nerve) transfer. Average excluded patients with no recovery (M0).
possible if the weight was given to the patient with elbow already flexed at 90 . When the same weight was given with the elbow extended, the patient could not flex the elbow from 0 to 90 . The patient with no anti-gravity recovery of elbow flexion underwent a Steindler procedure 17 months after the initial double-nerve transfer. At 9 months postSteindler procedure, she has 0.5-kg elbow flexion strength. Shoulder abduction and external rotation was achieved in eight out of nine patients. For our secondary outcomes, the average VAS for pain significantly decreased from 6.4 3.1 to 3.2 2.2 (p < 0.05). There was no significant change in the average grip strength before (10.5 3.8 kgf/45% of contralateral) and on latest follow-up (11.9 3.8 kgf/42% of contralateral) (p > 0.05). Previously weak or absent elbow extension improved to M3 in six out of nine and to M4 in five out of nine patients.
Complications Two patients reported sensory abnormalities of both the ulnar and median nerve territories after the surgery, while another two had only sensory disturbance of the ulnar nerve territory using the two-point discrimination test. These, however, resolved within 3 months post reconstruction. In one patient, there was a downgrade of the flexor carpi radialis muscle from M5 to M4 after partial median nerve transfer with improvement to M5 8 months post-operatively (patient #9). Two patients continue to have tingling sensation over the index finger (patients #3 and #6).
Discussion Although restoration of elbow flexion was the main objective in the treatment of patients with brachial plexus injuries affecting the upper roots, shoulder function was also addressed during surgical reconstruction.6,12,13 In this case series, we evaluated patients with upper-type brachial plexus injuries treated with nerve transfers for restoration of elbow and shoulder function. Nerve surgery in brachial plexus reconstruction has been regarded as superior to any palliative muscle transfers and is usually indicated in incomplete, early injuries affecting the shoulder and elbow.3,13 In cases of avulsion injuries where nerve grafting or repair was not possible, nerve transfers offer a very good surgical alternative as a nerve reconstructive procedure.6e13
Restoration of elbow flexion and shoulder function
Figure 2 (Patient 2). Elbow flexion strength was 4 kg after single-nerve transfer using part of the ulnar nerve to the biceps branch of the musculocutaneous nerve at 48 months postoperatively.
The return of elbow flexion was a direct result of nerve transfers to the biceps and/or brachialis branch of the musculocutaneous nerve. Eight of nine patients recovered M4 elbow flexion strength, with an average flexion force of 2.7 1.6 kg, which was inferior compared with the doublenerve transfer series of Liverneaux et al.,14 (3.7 kg) and the
1012 single-nerve transfers of Teboul et al.10 (4.15 kg). However, it was comparable to the single-nerve transfer series of Sungpet et al.9 at 1.8 kg and of Leechavengvongs et al.7 in 1998 (2.6 kg) and in 2006 (2.6 kg).8 Tung et al.18 in 2003 reported dual elbow flexor innervations by transferring a part of the ulnar nerve to the biceps branch of the musculocutaneous nerve and various nerve donors to the brachialis in eight patients. Their results showed 100% M4 recovery of elbow flexion. Recently, single- and double-nerve transfers were compared,19 which showed similar elbow flexion and supination strength. The results of double-nerve transfers for elbow flexion showed an average of 84% of patients regaining M4 elbow flexion strength.3,14,19 We had one failure of elbow flexion, where the procedure was done 11 months post injury. Although the time frame is still within the recommendation of some authors,14 this might be a factor why elbow flexion strength did not progress beyond M1, even after 17 months after surgery. We also noticed that elbow extension improved to M3 in six out of nine patients. These results, however, cannot be attributed to the procedure alone, as improvement of the previously weak or non-functioning triceps may have occurred over time. Further investigations may be needed to verify this. The results of our shoulder reconstruction were inferior compared with that of Leechavengvongs et al.,8 Bertelli et al.10 and Uerpairojkit et al.15 One of the differences may be due to the number of donor nerves or muscles reinnervated to reconstruct shoulder function. In the report by Leechavengvongs et al.8 and Bertelli et al.,11 both the axillary nerve and suprascapular nerve were innervated. In the study by Uerpairojkit et al.,15 the serratus anterior muscle was innervated with a branch from the thoracodorsal nerve in addition to nerve transfers to the suprascapular nerve and axillary nerve. Essentially, three nerves were recipients of nerve transfers. In our case series, only one nerve transfer was used in the reconstruction of shoulder abduction and external rotation. Suzuki et al.16 noted that better shoulder function was observed among patients without scapular winging compared with those with winging. They advised that the long thoracic nerve palsy must be addressed to achieve better results for the shoulder reconstruction. Cardenas-Mejia et al.20 reported that range of motion of shoulder abduction increases with increasing number of donor nerves in early stage nerve transfers for shoulder abduction. However, in their study, different donor nerves were used in different combinations in assessing the outcomes and the triple-nerve transfers consisted only of four patients compared with the 43 patients each of singleand double-nerve transfers. However, it is clear that by providing more axons to the recipient nerve, the chances of reinnervation become higher. In cases of single-nerve transfer for shoulder reconstruction in upper-type brachial plexus injuries using the spinal accessory nerve transfer to the suprascapular nerve, results from two authors showed an abduction of 66 and 77 and external rotation of 44 and 16.7 , respectively.12,16 The results of single-nerve transfer for shoulder function of these two studies were comparable with ours at an average of 70 of shoulder abduction and 61 of external rotation. However, in the literature, single-nerve transfers12,16,17 for the restoration of shoulder function remain to be inferior compared with multiple-nerve transfers.8,11,20 Although the concept of double-nerve transfer
E.P. Estrella being better than single-nerve transfer in elbow flexion restoration has been recently questioned by Carlsen et al.,19 the same may not be true for shoulder functional restoration. More muscles may be needed to restore shoulder function, as shoulder motion is more complex than elbow motion, and a greater weight proportion of the upper extremity will be borne by the shoulder muscles as opposed to the elbow flexors. In terms of complications of the nerve transfers, none of these reports showed any on the donor nerve innervations. In this study, four patients experienced abnormality to the ulnar and median distribution after surgery. This resolved after 3 months. A downgrade of the flexor carpi radialis from M5 to M4 was observed in one case. The muscle recovered to M5 after 8 months. We always use an intra-operative nerve stimulator to identify fascicles for transfer, making sure that they are redundant so that when sacrificed, minimal morbidity will be expected. The probable cause for this may be secondary to the fascicular dissection of the median nerve or that the fascicle that served as donor may have contributed heavily to the sensory or motor innervation. On final follow-up, there was a significant reduction of pain in a majority of patients. Root avulsion and deafferentation pain have been reported as the cause of most brachial plexus pain.21,22 Bertelli and Ghizoni23 reported that brachial plexus pain is probably a result of non-avulsed roots, and that grafting on these non-avulsed roots results in a substantial relief of pain. The authors also argued that nerve transfers per se does not relieve pain, as these are primarily motor nerves and are not associated with any cutaneous area of pain, such as the hand or forearm. It may be possible that during surgical exploration of the brachial plexus, some form of decompression of the plexus elements occurred, which might explain pain relief. However, this speculation cannot be supported by this article, and further studies might be needed to prove this. In summary, nerve transfers for upper-type brachial plexus injuries were effective in regaining function of the shoulder and elbow.
Funding None.
Conflicts of interest None declared.
Ethical approval Approved.
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