Evaluation of nerve transfer options for treating total brachial plexus avulsion injury: a retrospective study of 73 participants

Kai-ming Gao, Jing-jing Hu, Jie Lao, Xin Zhao

1 Department of Hand Surgery, Huashan Hospital, Fudan University, Shanghai, China

2 Nursing Department, Huashan Hospital, Fudan University, Shanghai, China

3 Key Laboratory of Hand Reconstruction, Ministry of Health, Shanghai, China

4 Shanghai Key Laboratory of Peripheral Nerve and Microsurgery, Shanghai, China

Figure 1 Trial flow chart.

Introduction

Total brachial plexus-avulsion injury (BPAI) is extremely difficult to treat in the clinic (Allieu et al., 1984; Midha, 2004;Shin et al., 2005). Nerve transfer is recognized as the most successful method for treating BPAI (Chuang, 1995; Narakas et al., 1988). The phrenic nerve (Gu et al., 1996; Hou et al.,2002), spinal accessory nerve (SAN) (Songcharoen et al.,1996; Terzis et al., 2006; Rui et al., 2013), intercostal nerve(ICN) (Malessy et al., 1998; Goubier et al., 2011; Gao et al.,2013a, b, c) and contralateral C7(cC7) (Gu et al., 1992, 1998;Chuang et al., 1998, 2012; Gao et al., 2006; Chen et al., 2007)are all commonly used donors, and the surgical technique as well as the effect of treatment are well-established. As previously reported, shoulder function, elbow flexion, elbow extension, and wrist and finger functions have been restored successfully via spinal accessory nerve, phrenic nerve, intercostal nerve, and cC7transfers. Terzis et al. (2006) reported good or excellent results in 79% of patients for the supraspinatus muscle and in 55% for the infraspinatus muscle when the SAN was transferred to the suprascapular nerve (SSN).Monreal et al. (2007) reported 70% functional recovery of the biceps after phrenic nerve transfer. In another study, Gao et al. (2013a, b, c) reported 56% recovery of the triceps after ICN transfer. They also reported that functional recovery of the median nerve reached 49% for motor function and 63% for sensory function after cC7transferred to the median nerve.However, these studies only focused on a few elements of limb function, rather than the restoration of the entire range of limb functions. In different medical groups even within our own department, several different surgical strategies have been used for treating total BPAI, and the results have varied tremendously. Here, we investigated the effectiveness of different commonly used nerve-transfer choices to determine the best surgical strategy for treatment of total BPAI.

Participants and Methods

Participants

This was a retrospective study. The study protocol was approved by the Ethics Committee of Fudan University of China (approval number: 2015-064). From 1999 to 2006,approximately 200 patients with posttraumatic total BPAI underwent surgical exploration and nerve transfer of the brachial plexus. Phrenic nerve transfer was conducted in 115 cases, SAN transfer in 182 cases, ICN transfer in 137 cases and cC7transfer in 167 cases. Among these patients, 109 agreed to participate in our study and 73 were ultimately enrolled (Figure 1).

Inclusion criteria

Patients presenting with all of the following criteria were considered for study inclusion:

? Global root-avulsion brachial plexus injury

? Postoperative interval ≥ 3 years

? All operations were performed by the same medical team

? Nerve transfer was the only reconstruction method used

Exclusion criteria

Patients with one or more of the following conditions were excluded from this study:

? Diabetes (2 cases)

? Volkmann contracture (3 cases)

? Fracture on the affected limb (humeral fracture in 7 cases,radial fracture in 5 cases, ulnar fracture in 3 cases)

? Rib fracture (11 cases)

? Brain trauma (5 cases)

Evaluation

The recovery of postoperative motor and sensory functions was evaluated by the British Medical Research Councilgrading system (John, 1984) in all 73 patients after a minimal interval of 3 postoperative years. In the British Medical Research Council grading system, the motor and sensory function scores are divided into 6 grades from grade 0 to 5.A grade of three or above was regarded as an effective recovery of motor and sensory function. The efficacy rate of a procedure was calculated by dividing the number of effective recoveries for that procedure by the number of times that procedure was used.

Table 1 Methods of reconstructing the nerves of the affected limb

Table 2 Different outcomes for elbow flexion recovery using different reconstruction methods

Intraoperative findings of the injured brachial plexus

The injured brachial plexus was supraclavicularly explored in all patients under 2.5× magnification (Heine Surgical loupe, Dover, NH, USA). All 73 patients were con firmed to exhibit total BPAI. Using similar approaches, transfer of the phrenic nerve to the musculocutaneous nerve and transfer of the SAN to the SSN could be performed.

Posterior approach for transferring the SAN to the SSN

This surgery was performed with the patient in a lateral position and the affected side upward. An approximately 10 cm long transverse incision was made over the scapular spine.The trapezius insertion on the scapular spine was divided.The trapezius was then retracted upwards and the SAN was exposed. The SSN located in the suprascapular notch underthe transverse ligament of the scapula was then identified and isolated. The SSN was divided as far proximally as possible for transfer (Figure 2).

Table 3 Different outcomes for shoulder abduction recovery using different reconstruction methods

cC7 transfer

The cC7nerve transfer procedure was separated into two stages. The first stage was conducted by two teams simultaneously. One team explored the normal brachial plexus. The cC7nerve was exposed to its division level and a longitudinal epineurotomy was performed in the division to expose the constituent bundles. The other team transected the ulnar nerve at the level of the wrist on the affected limb and the full-length ulnar nerve was harvested. The ulnar nerve was vascularized by the superior ulnar collateral artery from the level of the elbow. The vascularized ulnar nerve was then passed across the chest through a subcutaneous tunnel to the normal neck. The partial or entire cC7nerve was coapted to the ulnar nerves at 4× magni fication (Heine Surgical loupe) with 8-0 microsutures.

In the second stage, the ulnar nerve on the affected side was neurotized into different recipient nerves. A longitudinal epineurotomy was performed on the ulna if it was going to be transferred to two recipient nerves simultaneously (Figure 3).

Figure 2 A patient under general anesthesia in the lateral position (A)and the skin incision superior to the scapular spine (B).

Figure 3 Preparation of the pedicled ulnar nerve graft.

Figure 4 Intercostal nerve harvesting.

Intercostal nerve harvesting

A continuous thoraco-brachial incision was performed in axilla, the lateral chest, and the arm. The thoracic part of the incision began from the inferior axilla and followed the curve of the anterior border of the latisimus dorsi muscle.The arm part of the incision was performed on the medial side of the arm.

The ICNs were exposed in the chest incision. The latisimus dorsi muscle and the serratus anterior muscle, as well as the periosteum of the ribs, were reflected and the intercostal nerves were exposed. The periosteum was detached and pulled downward to expose its posterior aspect, and the thin motor branch of each ICN was identi fied and harvested,while the split sensory branch was left inside (Figure 4). The numbers of ICNs harvested depended on the recipient nerves.

Reconstruction methods

The phrenic nerve was transferred to upper trunk in 25 patients and grafted to the musculocutaneous nerve in 19 patients. The SAN was transferred to the SSN via an anterior approach in 49 patients and via a posterior approach in 19 patients. The cC7was transferred to the median nerve in 51 patients, to the median + musculocutaneous nerves in 12 patients, and to the median nerve + the triceps branch in 10 patients. Two ICNs were transferred to the musculocutaneous nerve in 19 patients, to the axillary nerve in 36 patients, and to the radial nerve in 31 patients. Two or three ICNs were transferred to the triceps branch in 25 patients (Table 1).

Postoperative rehabilitation

Immediately after the operation, the affected limb was immobilized for 4 weeks. Physiotherapy began at 5 weeks to prevent joint contractures. Patients were also asked to breathe deeply, raise their shoulders, and to adduct their shoulders against resistance since contraction of the latissimus dorsi muscle of the healthy side.

Statistical analysis

All data were analyzed with Stata 13.0 software (Stata Corp,Baltimore, MD, USA). Data are expressed as percentages.Comparisons among postoperative groups were performed using chi-square tests. P values less than 0.05 were considered statistically signi ficant.

Results

Changes in the rates of functional recovery after surgery

Among the 73 patients, 79.45% (58/73) exhibited effective recovery for elbow flexion, 76.71% (56/73) for shoulder abduction, 45.71% (16/35) for elbow extension, 38.71% (12/31) for wrist and finger extension, 54.79% (40/73) for wrist and finger flexion, and 57.53% (42/73) for the sensation around the median nerve. No complications were found in any patient.

Postoperative functional recovery

Patients were divided into groups according to the reconstruction method and rates of functional recovery for each category were determined for each group.

For elbow-flexion function, the efficacy rate was 84%(21/25) in phrenic nerve-transfer group, 84.21% (16/19)in phrenic nerve-grafted group, 76.47% (13/17) in the ICN transfer group, and 66.67% (8/12) in the cC7transfer group.There was no statistically significant difference in efficacy between the groups (P ＞ 0.05;Table 2).

For shoulder-abduction function, the efficacy rate was 77.78% (21/27) in the anterior SAN-transfer group, 70%(7/10) in the posterior SAN-transfer group, 40% (2/5) in the group of ICNs transferred to the axillary nerve, and 83.87%(26/31) in the SAN + ICNs transfer group. Analysis showed that the efficacy rate for the group of ICNs transferred to the axillary nerve was signi ficantly worse than that for the other groups (P ＜ 0.05;Table 3).

Table 4 Different outcomes for median nerve functional recovery using different donor nerves

For the transfer of the cC7to the median nerve, the entire cC7root was used in 33 patients (22 underwent the transfer of the cC7to two recipient nerves simultaneously) and a partial cC7root was used in 40 patients. The motor function recovery for the entire-C7group was signi ficantly better than that for the partial C7group (P ＜ 0.05;Table 4). However, we found no statistically signi ficant difference in the recovery of sensory function between the groups (P ＞ 0.05;Table 4).

For elbow-extension function, the efficacy rate was 56%(14/25) in the ICNs-transfer group and 20% (2/10) in the cC7-transfer group (cC7transfer to the median nerve + triceps branch). Analysis showed that these efficacy rates were signi ficantly different (P ＜ 0.05;Table 5).

For wrist- and finger-extension function, ICN transfer was conducted in 31 patients and the efficacy rate was 51.61%(16/31).

Discussion

At present, the most successful method of restoring affected limb function in patients with total BPAI is nerve transfer(Seddon, 1963; Panupan, 1995). In our department, the surgical order for function restoration in patients with BPAI is elbow flexion, shoulder abduction and external rotation, elbow extension, wrist and finger flexion, and wrist and finger extension (Gu et al., 1984).

The commonly used reconstruction methods for restoring elbow flexion are phrenic nerve transfer (with or without grafting the nerve) (El-Gammal et al., 2002), ICN transfer (Ploncard, 1982; Nagano, 2001) and cC7nerve transfer(Gu et al., 2002; Wang et al., 2012; Gao et al., 2013a,b,c;Hu et al., 2014; Yang et al., 2015). In the current study, all four reconstruction methods were used and no statistically signi ficant difference was found in the rates of effective recovery. However, the cC7group was special in that the cC7was transferred simultaneously to the median nerve and the musculocutaneous nerve. In this group (12 patients), the effective recovery rates for the two recipient nerves were both acceptable (66.67% for elbow flexion and 75% for wrist and finger flexion). This suggests that simultaneous transfer of the entire root of the cC7nerve to the musculocutaneousand median nerves could be a good option for treating total BPAI because the median nerve and biceps branch are collaborative in motor functions (Terzis et al., 2009; Zou et al.,2010; Gao et al., 2013a, b, c).

Table 5 Different outcomes for elbow extension recovery using different reconstruction methods

For shoulder function, the most commonly used donor nerves are the SAN (Terzis et al., 2006) and ICNs (Terzis et al., 2006). In the current study, four different methods were used to reconstruct the shoulder and restore function,including anterior transfer of the SAN to the SSN, posterior transfer of the SAN to the SSN, transfer of ICNs to the axillary nerve, and transfer of the SAN to the SSN combined with transfer of ICNs to axillary nerve. According to the British Medical Research Council scale, the efficacy of ICN transfer to the axillary nerve was only 40%, which was signi ficantly worse than the other groups. This unsatisfactory result might have occurred because restoration of deltoid function alone could not provide enough stability for the glenohumeral joint, which is important for shoulder abduction. No statistically significant difference in efficacy was found between anterior and posterior transfers of the SAN to the SSN. Rui et al. (2013) conducted an electrophysiological study to compare the effectiveness of anterior and posterior approaches of SAN transfer to the SSN. Similar to the current study, they found no significant difference between approaches in the time it took for the infraspinatus to show low-incidence motor unit action potentials and an incomplete interference pattern. Additionally, the final percentage of patients that showed potential regeneration of the infraspinatus did not signi ficantly differ between the approaches. Our experience is that the anterior approach is more commonly used because it can be performed at the same time as brachial plexus exploration. Nevertheless, if a scapular fracture occurs, the posterior approach is recommended because the SSN might be injured by the fracture and need a surgical exploration. In this study, we found no difference between the recovery in SAN-transfer (anterior and posterior) group and the SAN + ICNs group. However,the efficacy of shoulder abduction regarding the power of the target muscle does not accurately reflect the recovery of shoulder function. Using the degrees of abduction and external rotation might be better criteria. In the anterior and posterior SAN-transfer groups, patients achieved an average shoulder abduction of 45° and an average external rotation of 10°. Recovery in the SAN + ICNs transfer group was markedly better, with the average shoulder abduction reaching 70° and the average external rotation reaching 30°.Cardenas-Mejia et al. (2008) reported that the average degree of shoulder abduction was 160° following triple-nerve transfers, 85° following double-nerve transfers, and 65° following single-nerve transfers. Average shoulder abduction following either double-nerve or triple-nerve transfer was signi ficantly greater than that achieved by single-nerve transfer. Thus,increasing the number of donor nerves appears to improve shoulder function and using the method that combines SSN and ICNs transfer is recommended for reconstructing the shoulder and restoring function.

For elbow extension, the usual treatment plan is to use the ICNs for direct transfer to the nerve of the long head of the triceps (Gao et al., 2013a, b, c), while in some special cases,the cC7nerve is transferred simultaneously to the median nerve and triceps branch (Gao et al., 2013a, b, c). In the current study, the efficacy was 56% (14/25) in the ICNs-transfer group, but only 20% (2/10) in the cC7-transfer group(cC7transfer to the median nerve + triceps branch), which was a statistically signi ficant difference. The median nerve and triceps branch were not collaborative for motor function, which might lead to poor recovery of triceps. In the ICNs group, two ICNs were used in 18 patients, and three ICNs in 7 patients.The recovery rate for the long head of the triceps was 55.56%in the two-ICNs group and 57.14% in the three-ICNs group,which was not a statistically signi ficant difference. According to previous studies, the number of nerve fibers in the ICN is relatively small at approximately 500—700; however, the use of all motor fibers guaranteed the quality of the donor.

Wrist- and finger-extension function was restored by ICNs with an efficacy reaching 51.61%. Most surgeons chose the ICN as the donor because wrist- and finger-extension functions are collaborative with elbow extension and because they are both innervated by the radial nerve. The ICN seems to be the relatively optimal donor for the triceps and using the same donor nerve to reconstruct these two functions is reasonable.

cC7nerve transfer is the most commonly used method for restoring function to the median nerve (Wang et al., 2011,2013; Gao et al., 2013a, b, c) because it contains many axons(Gu, 1994). However, some surgeons have recommended using only a portion of the cC7nerve (not the entire root) as the donor nerve to conserve more of the healthy limb’s sensory function (Sungpet et al., 1999; Gao et al., 2010). In the present study, three different ways were used to harvest cC7, including the entire root, 3/4 root, and half root. As shown inTable4, functional recovery for the whole-root cC7-transfer group was much better than that for the partial cC7-transfer group.Previous studies also reported similar results, indicating that transferring the entire cC7nerve results in dramatically better recovery of median nerve function than transferring a partially harvested cC7nerve (Waikakul et al., 1999; Panupan et al.,2001; Sammer et al., 2012; Tu et al., 2014). Using the entire cC7nerve provides a large number of donor nerve fibers and thus promotes recovery. Anatomic variation in the C7nerve root might erroneously lead a surgeon to use more sensory fascicles as donors than motor fascicles (Hierner et al., 2007). The functional reorganization of the cerebral cortex should be another important factor for consideration, especially the postoperative transhemispheric functional reorganization of the motor cortex (Sanes et al., 1997; Lou et al., 2006; Pan et al., 2012; Yang et al., 2017). However, this topic is still being actively researched.Despite the unknown mechanism, we strongly emphasize using the entire root as the donor rather than the partial fascicles. Our results showed that the cC7was also used to repair an additional recipient nerve together with the median nerve,without adversely affecting the recovery of the median nerve.

Although this study has a few limitations, such as being a retrospective study and having relatively low sample sizes, we can still preliminarily conclude that for total BPAI, optimal surgical treatment is phrenic nerve transfer for elbow flexion,SAN combined with ICNs transfer for shoulder function,ICNs transfer for elbow extension, entire cC7transfer for median nerve function and ICNs transfer for finger extension.For older people or those whose phrenic nerve is un fit to be the donor, we recommend SAN combined with ICNs transfer for shoulder function, entire cC7transfer for elbow flexion and median nerve function, and ICNs transfer for elbow extension and wrist and finger extension.

Author contributions:KMG designed the study. JJH and KMG performed experiment. JJH, JL and XZ analyzed the data as well as wrote the paper. All authors approved the final version of the paper.

Con flicts of interest:None declared.

Financial support:This study was supported by the National Natural Science Foundation of China, No. H0605/81501871. The funder played no role in the study conception and design, collection, analysis and interpretation of data,in the writing of the paper, and in the decision to submit the papaer for publication.

Research ethics:The study protocol was approved by the Ethics Committee of Fudan University of China (approval number: 2015-064). The trial was registered at ClinicalTrials.gov (identi fier: NCT03166033).

Declaration of participant consent:The authors certify that they have obtained all appropriate patient consent forms. In the form, participants have given their consent for their images and other clinical information to be reported in the journal. Participants understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Data sharing statement:Datasets analyzed during the current study are available from the corresponding author on reasonable request.

Plagiarism check:Checked twice by iThenticate.

Peer review:Externally peer reviewed.

Open access statement:This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under identical terms.

Open peer reviewers:

Luciana P. Cartarozzi, University of Campinas, Campinas, Brazil; Fabricio Ferreira de Oliveira, Department of Neurology and Neurosurgery,Universidade Federal de Sao Paulo, Brazil.

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