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Outcome of contralateral C7 transfers to different recipient nerves after global brachial plexus avulsion

Abstract Introduction Contralateral cervical seventh nerve root (CC7) transfer has been widely applied for treatment of traumatic brachial plexus injury. The purpose of the study was to evaluate outcomes of patients with global brachial plexus avulsion (GBPA) after CC7 transfer and compare the recoveries of median nerve as the only recipient nerve and one of the multiple recipient nerves. Methods A retrospective review of 51 patients treated with CC7 transfers after GBPA was carried out. The British Medical Research Council (MRC) grading system and range of joint motion (ROM) were used for motor and sensory assessment. Results The effective rates of FCR were 57.7%, 45.5%, and 36.4% in CC7 transfer to median nerve (CC7‐Md), CC7 transfer to median nerve and biceps branch (CC7‐Md+Bic) and CC7 transfer to median nerve and triceps branch (CC7‐Md+Tric) groups, respectively. There were no statistical differences no matter in FCR or FDS among groups. The effective rate in biceps had no significant difference with that in triceps. The effective sensory recovery rate was 65.4%, 54.5%, and 36.4% in CC7‐Md, CC7‐Md+Bic, and CC7‐Md+Tric groups. There were no statistical differences in the sensory effective recovery rate among groups. All the ROMs were improved significantly after surgery. The improvement of ROM of elbow flexion after surgery in CC7‐Md+Bic group was significantly larger than that of elbow extension after surgery in CC7‐Md+Tric group (p = 0.047). Conclusions The CC7 transfer contributed to the functional improvement of the hand and wrist for the patients with global brachial plexus avulsion. The whole CC7 could be used to repair more than one recipient nerve (including median nerve) without affecting the recovery of median nerve. When CC7 was used to repair two nerves, biceps branch might be preferred to choose as one recipient nerve rather than triceps branch.


| ME THODS
A retrospective review of 51 patients treated with CC7 nerve transfer after posttraumatic global brachial plexus injury was carried out. The clinical research was reviewed and approved by the institutional review board of Huashan Hospital Affiliated to Fudan University (Approval No: 2015-163), and all patients gave informed consent. The inclusion criteria included global root avulsion (C5 to T1 avulsion) and CC7 root as donor nerve in the treatment. The exclusion criteria included diabetes, Volkmann contracture, fracture on the affected limb, and brain trauma. According to medical records, inclusion and exclusion criterions, the enrolled patients were confirmed. Then the patients were called in our department for outcome measure. We removed the extreme age range patients (13 and 59 years old) from the statistics. The average delay to surgery was 2.7 months, but the highest is 17 months. We removed the long preoperative delay case (17 months) from study to get better comparison between different series (Table 1). Therefore, 48 patients were involved in the statistical analysis. All the operations were done by the same group of surgeons.

| Surgical technique
A transverse incision was made superior to the clavicle on the contralateral side for exploring C7 root. C7 nerve root was confirmed by anatomic identification of its location and electric stimulation, which resulted in shoulder adduction, elbow extension, and wrist extension (Gu, Xu, Chen, Wang, & Hu, 2002). CC7 root was blocked by 2% lidocaine epineurium injection.
When the recipient nerve was median nerve, triceps branch, or biceps branch, the vascularized ulnar nerve was adopted as nerve graft. The first stage: The vascularized ulnar nerve graft based on the superior ulnar collateral artery was harvested from the affected arm and passed across the chest through a subcutaneous tunnel to the normal neck from the opposite axilla . Then the ulnar nerve was sutured to the whole CC7 nerve root under 2.5 × magnification, using 8-0 microsutures. The second stage (4-6 months after the first stage): The ulnar nerve on the affected side was resected and sutured to the recipient nerve ( Figure 1). The patient was immobilized by a head and arm rack to keep the head from turning to the affected side for one month.

| Postoperative rehabilitation
Physical therapy and electrostimulation therapy were started 4 weeks postoperatively. Patients were instructed to adduct his contralateral shoulder against resistance, while doing the action of the affected limb according to the recipient nerve. For example, if the recipient nerve was median nerve, the patient was instructed to practice wrist and finger flexion in the affected limb while adducting his contralateral shoulder against resistance. We formulated a scheme for patients: Physical therapy was done three times per day and each time physical therapy lasted for 1 hr.
The electrostimulation therapy was carried out twice per day.
The postoperative rehabilitation, including physical therapy and electrostimulation therapy, lasted for at least 2 years.

| Evaluation
The

| Statistical analysis
All analyses were performed using Statistical Package for Social Sciences (SPSS version 19.0, Chicago, IL, USA). Comparison between preoperative and postoperative ROM was analyzed using t test for parametric data and Wilcoxon signed rank sum test for nonparametric data. P-values were two-tailed, and p values <0.05 were considered significant.

| RE SULTS
According to the difference of recipient nerves, the patients could be divided into three groups. 26 patients had CC7 transfer to median nerve (CC7-Md). 11 patients had CC7 transfer to median nerve and biceps branch (CC7-Md+Bic; Figure 2), while 11 patients had CC7 transfer to median nerve and triceps branch (CC7-Md+Tric).

| MRC grading (motor power)
All of the muscle strength was M0 in the affected limb with global brachial plexus avulsion preoperatively. The muscles tested were the main targets of the recipient nerves. Median nerve: flexor carpi radialis (FCR) and flexor digitorum superficial (FDS); Biceps branch: Biceps; Triceps branch: Triceps. As Figure 3a shown, the effective

| MRC grading (sensory assessment)
The radial side of palm and the palm-sides of thumb, index, and middle fingers were the regions which median nerve dominated. Figure 3b showed different sensory recoveries of median nerve according to different recipient nerves. In CC7-Md group, there were three patients with S4 recovery, 14 patients with S3, 2 patients with S2, and 7 patients with S0. The effective sensory recovery rate was 65.4%. The sensation of the radial side of palm and the 1-3 palmar digit recovered to S3 in 6 patients, S1 in two patients, and S0 in three patients in CC7-Md+Bic group, which indicated the effective sensory recovery was 54.5%. In CC7-Md+Tric group, there were one patient with S4 recovery, three patients with S3, one patient with S2, three patients with S1 and three patients with S0. The total effective rate of median nerve sensory recovery after different CC7 nerve transfer was 56.3%. Comparing sensory recoveries of median nerve after whole CC7 transfer to different recipient nerves, there were no statistical differences in the sensory effective recovery rate ( Figure 3b).
F I G U R E 2 CC7 stage II: The ulnar nerve was sutured to the median nerve and biceps branch (triangle-median nerve, thick arrow-ulnar nerve, star-biceps branch)

| ROM improvement
The wrist and digital flexion ranges were all improved significantly in CC7-Md, CC7-Md+Bic, and CC7-Md+Tric groups (p < 0.05). The total EF (elbow flexion range) and EE (elbow extension range) were also significantly improved in CC7-Md+Bic and CC7-Md+Tric groups, respectively, compared with those before surgery. Figure 3c showed ROM improvement after CC7 transfer to different recipient nerves. The

ROMs of WF and DF both decreased from CC7-Md group to CC7-
Md+Tric group via CC7-Md+Bic group, but there were no statistical differences among groups. The ROM of EF in CC7-Md+Bic group was significantly larger than that of EE in CC7-Md+Tric group (p = 0.047).

| Satisfaction with surgery
In the CC7 transfer to median nerve group, 16 patients answered "definitely yes" or "probably yes" in response to the question on their readiness to undergo surgery again. Ten patients answered "uncertain". The satisfaction rate was 61.5% in the CC7-Md group.
The satisfaction rates of the CC7-Md+Bic and CC7-Md+Tric transfer were both 54.5% (Figure 3d). There were no significant differences of the satisfaction with surgery between groups. The total satisfaction rate for all patients with CC7 nerve transfer was 58.3%.

| Complications
A total of 38 patients experienced paresthesia on the thumb, index, and middle pulp of the donor hand within three months after surgery and the sensory deficit completely recovered spontaneously in all patients now.  (Bonnel & Rabischong, 1980). The difference of the numbers of nerve fibers between whole CC7 and median nerve explained the study result "the effect recovery rates of FCR and FDS after whole CC7 only transfer to median nerve had no statistical differences with those after whole CC7 transfer to median nerve and other nerves." According to the result of ROM improvement, the wrist and digital flexion ranges were improved significantly by CC7 transfer to median nerve, which implied CC7 nerve transfer contributed to the functional improvement of the hand and wrist for the patients with global brachial plexus avulsion. The effective rate of biceps was higher than that of triceps and the ROM of EF in CC7-Md+Bic group was significant larger than that of EE in CC7-Md+Tric group, which indicated the recovery of biceps was better than that of triceps after CC7 transfers. The satisfaction result showed more than half of the patients were basically satisfied with CC7 nerve transfer. The patients' subjective evaluation reflected CC7 nerve transfer was an acceptable operation by most of the people.

| D ISCUSS I ON
In August 1986, the world's first case of contralateral C7 nerve transfer was finished by Gu et al. (1992) and he reported the overall motor recovery rate (≥M3) was 50%-80% depending on different recipient nerves and the sensory recovery rate (≥S3) was above 60% (Zhang & Gu, 2011). Waikakul (Waikakul, Orapin, & Vanadurongwan, 1999) reported that only 52% of patients had ≥M3 recovery after contralateral C7 transfer to musculocutaneous nerve, and 20% re- respectively. The success rate for recovery of elbow flexion in CC7-Md+Bic group was 83%. Terzis reported the summing rates of fair (M2+~M3), good (M3+~M4−), and excellent (M4+~M5−) in 56 cases were 74% for biceps; 57% for triceps; 62% for wrist and finger flexors; and 50% for wrist and finger extensors, respectively (Terzis & Kokkalis, 2009 This study had some limitations. Motor strength and ROM could also be improved by postoperative rehabilitation including physical therapy and electrostimulation therapy, which was an influence factor of muscle recovery. In this study, although we formulated a scheme of postoperative rehabilitation for patients, we did not collect the actual information of patients' postoperative rehabilitation, which might induce some potential bias. The evaluation methods were MRC and ROM without electromyogram (EMG) in our study.
The amplitude and latency of compound muscle action potential (CMAP) of the muscles were not used for evaluation, which were more accurate assessments of the recovery of muscle reinnervation. There was no functional outcome evaluation such as DASH questionnaire scoring to analyze the results in terms of the usefulness of the regained movements in the study. This study belonged to a single-center clinical study, so the results had certain regional limitations.
Our study was a retrospective study. The findings of the study applied to the patients with global brachial plexus avulsion.
Contralateral C7 transfer could be used to repair different recipient nerves according to the function which the patient needs to restore.

| CON CLUS IONS
The CC7 nerve transfer contributed to the functional improvement of the hand and wrist for the patients with global brachial plexus avulsion. The whole CC7 could be used to repair two recipient nerves (including median nerve) without influencing on the recovery of median nerve. When CC7 was used to repair two nerves, biceps branch might be preferred to choose as one recipient nerve rather than triceps branch.

ACK N OWLED G M ENTS
This study was supported by Shenzhen's Sanming Project