Evaluation of lower trapezius function after transfer of axillary nerve to suprascapular nerve in patients with ERB’s palsy

Abstract

BACKGROUND

It is expected that transfer of spinal accessory nerve to suprascapular nerve, which is widely used in the restoration of the shoulder function in brachial plexus birth injury (BPBI), impairs the trapezius function.

AIM

To hypothesize that the lower trapezius muscle remains functional after this neve transfer.

METHODS

In a retrospective cross-sectional study, patients with BPBI who underwent nerve transfer from accessory nerve to supraclavicular were followed for at least six months following the operation and demographic data were extracted from the database. To assess the lower trapezius function, shoulder abduction and external rotation were examined, and electromyography and nerve conduction velocity (EMG-NCV) was performed.

RESULTS

A total of 19 patients with a mean age of 2.69 ± 1.40 years and a mean follow-up of 10.5 months were included in the study. Shoulder abduction was disabled completely only in one patient (5.26%); 10 (52.63%) had good, 3 (15.78%) moderate, and 5 (26.31%) had poor shoulder abduction. Regarding external rotation, one (5.26%) was unable to externally rotate the shoulder; among 18 (94.73%) patients who had satisfactory results, 8 (42.10%) were evaluated to be good, 5 (26.31%) moderate, and 5 (26.31%) poor. EMG-NCV showed functional lower trapezius in all patients; its function was evaluated to be good in 11 (57.89%), moderate in 6 (31.57%), and poor in 2 (10.52%) cases.

CONCLUSION

This study supports the hypothesis that the lower trapezius muscle has a dual motor innervation which provides the possibility of further trapezius tendon transfer to restore a better shoulder function.

Key Words: Neonatal brachial plexus palsy; Upper extremity; Brachial plexus; ERB’s palsy; Spinal accessory nerve; Nerve transfer; Shoulder; Suprascapular nerve

Core Tip: The primary goal of neonatal brachial plexus palsy is restoration of hand function followed by elbow flexion and shoulder function. The motor branch of the spinal accessory nerve which is used for suprascapular nerve neurotization innervates the trapezius muscle and the sternocleidomastoid muscle, thus it is expected the aforementioned nerve transfer impairs the trapezius muscle function. Our paper supports the hypothesis that the lower trapezius muscle has a dual motor innervation. This is an important issue as a functional lower trapezius muscle can be used for further musculotendinous transfer to restore shoulder function.

INTRODUCTION

Management of the suprascapular nerve (SSN) injury as the most vulnerable nerve of the brachial plexus birth injury (BPBI). Is an important and challenging step to restoring the shoulder function which is the treatment goal in BPBI. The management and treatment goals for brachial plexus birth injuries typically involve a combination of medical, surgical, and rehabilitative approaches, with the primary goal of maximizing the child's arm function and minimizing disability. To restore active shoulder external rotation, transfer of spinal accessory nerve (SAN) to SSN is an option that was first introduced by Kotani in 1972 and increasingly has become the most common surgical method for this manner[1]. The possibility of SAN transfer to SSN is due to the accessory nerve anatomical position which is adjacent to the brachial plexus and makes the aforementioned transfer possible[2].

The motor branch of the SAN nerve which is used for SSN neurotization (the technique of relocating a healthy nerve or its proximal stump to reestablish an impaired sensory or motor pathway that has sustained irreparable damage) innervates the trapezius muscle and the sternocleidomastoid muscle, thus it is expected the aforementioned nerve transfer impairs the trapezius muscle function[3]. Several studies have focused on outcomes of SAN transfer and a wide range of results has been reported[1,4]. However, to the best of our knowledge, there has been no study on the function of the lower trapezius muscle after SAN transfer.

We hypothesize the lower trapezius muscle may be double innervated. Therefore, we aimed not only to assess the short outcome of SAN transfer but also to evaluate the lower trapezius muscle function after the SAN transfer.

MATERIALS AND METHODS

Study design and patient selection

In a retrospective cross-sectional study, all patients with BPBI who underwent nerve transfer of accessory nerve to supraclavicular between 2017 and 2019 in a single center were reviewed. Patients, who were under 3 years old at the time of operation, had BPBI due to birth, and six months had been passed from their operations were included in our study. Also, patients with traumatic injuries, history of previous surgery in neck or shoulder, and history of tendon transfer were excluded. Cases lost in follow-up and unwilling to participate in the study were also eliminated. For outcome assessment, patients were followed up for at least six months following the operation.

Inclusion criteria: Patients aged < 3 years at operation with isolated BPBI who underwent SAN-SSN transfer and completed at least 6 months follow-up were included. Partial BPBI cases were included if shoulder function was primarily affected.

Exclusion criteria: Patients with traumatic brachial plexus injuries, concurrent significant nerve injuries, previous neck/shoulder surgery, incomplete rehabilitation adherence, or lost to follow-up were excluded.

Data measurement and endpoints

Demographic data, including age (at the time of evaluation and surgery) and sex, as well as the side of the brachial palsy, date of operation, and radiological examinations, were extracted from the database. Shoulder abduction and external rotation were examined, and the results were classified into four groups of none, poor, moderate, and good. Also, electromyography and nerve conduction velocity (EMG-NCV) was done for all patients to evaluate the function of the lower trapezius muscle. Scoring was done from M1 to M5; M1 meant 1%-20% of muscle function, M2 20%-40%, M3 40%-60%, M4 60%-80%, and M5 meant 80%-100% of lower trapezius muscle function. Then, M1 and M2 were considered as poor, M3 and M4 as partially, and M5 as good. Also, a non-functional group was defined when a muscle had no function at all. The date on which EMG-NCV was performed was also recorded.

The EMG-NCV scoring system (M1-M5) was defined based on electromyographic criteria. Muscle function percentages were quantified primarily by evaluating motor unit recruitment patterns and compound muscle action potential amplitudes. Specifically, M1 represented minimal recruitment with amplitudes of 1%-20% of the contralateral side; M2, partial recruitment (20%-40%); M3, moderate recruitment (40%-60%); M4, good recruitment (60%-80%); and M5, nearly complete recruitment (80%-100%).

Surgical technique

All surgeries utilized a posterior approach. After identifying and isolating the SAN through a transverse incision, meticulous nerve coaptation to the SSN was performed using microsurgical techniques and 9-0 nylon epineural sutures under magnification. Postoperative rehabilitation consisted of immobilization for 3 weeks followed by structured physiotherapy emphasizing passive and active-assisted shoulder exercises, progressing to active strengthening exercises after 6 weeks.

Statistical analysis

Based on the study by Songcharoen[5], the success rate of nerve transfer from accessory nerve to supraclavicular was considered 75%. With an error of 5% and a power of 80%, 18 cases were needed for the study. Considering 10% of dropouts due to losing to follow-up or lack of data of patients, we estimated that 20 patients would be required.

RESULTS

Demographic data

In total, 19 patients with BPBI who underwent nerve transfer of accessory nerve to suprascapular were included. The mean age of patients was 2.69 ± 1.40 years (range: 1.1-7.1), and 8 of them (42.10%) were female. 14 cases (73.68%) had BPBI on the right side, while 5 (26.31%) had on the left; none of the patients had a bilateral injury. Also, the mean follow-up of patients was 10.5 months. Preoperative shoulder abduction and external rotation were severely impaired in all patients, averaging less than 15° of abduction and 5° of external rotation. Postoperative improvements are thus contextualized clearly against these initial limitations.

The mean age at the time of surgery was 10.36 ± 5.75 months (range: 5-24), and the mean time of performing EMG-NCV following operation was 1.47 ± 1.07 years (range: 1-5).

Operative outcomes

No postoperative complications were observed in any of the patients. Regarding shoulder abduction, it was disabled completely only in one patient (5.26%). Among other 18 patients (94.73%), 10 (52.63%) had good, 3 (15.78%) moderate, and 5 (26.31%) had poor shoulder abduction. The mean range of motion of abduction was 56.5°. Besides, 18 (94.73%) out of 19 patients had satisfactory results for external rotation; the only one (5.26%) who was unable to externally rotate the shoulder was the same patient with disabled shoulder abduction. External rotation was evaluated to be good, moderate, and poor in 8 (42.10%), 5 (26.31%), and 5 (26.31%) patients, respectively. The mean range of motion of external rotation was 54°.

Lower trapezius muscle function was evaluated by EMG-NCV, which classified the patients into good, partially, and poor if the muscle was functional. This test showed that all patients had functional lower trapezius muscle; its function was evaluated to be good in 11 (57.89%), moderate in 6 (31.57%), and poor in 2 (10.52%) patients (Table 1).

Table 1 Shoulder abduction and external rotation and electromyography and nerve conduction velocity results in patients with ERB’s palsy who underwent nerve transfer of accessory nerve to supraclavicular, n (%).

Variable	Classification
Shoulder abduction	None	Poor	Moderate	Good
	0 (0)	5 (26.31)	3 (15.78)	10 (52.63)
Shoulder external rotation	None	Poor	Moderate	Good
	1 (5.26)	5 (26.31)	5 (26.31)	8 (42.10)
EMG-NCV	Non-functional	Poor	Partially	Good
	0 (0)	2 (10.52)	6 (31.57)	11 (57.89)

Good: Shoulder abduction ≥ 90°; external rotation ≥ 60°, Moderate: Shoulder abduction 45-89°; external rotation 30-59°, Poor: Shoulder abduction < 45°; external rotation < 30°. EMG-NCV: Electromyography and nerve conduction velocity.

DISCUSSION

Based on the current study, EMG-NCV findings showed that all of the patients had a functional lower trapezius muscle after SAN-SSN transfer. This is an unexpected outcome as the SAN which is assumed to be the main motor nerve to trapezius muscle was totally dissected. This finding may demonstrates the SAN is not the only motor nerve of trapezius.

Many authors have mentioned that contributions from cervical plexus are present to innervate trapezius muscle[6-11]. Furthermore, Saunders et al[12] reported that the number of patients who experienced shoulder dysfunction after surgery was unexpected while the accessory nerve was preserved and cervical branches were cut[13].

In another study on 12 adult human cadavers, Gavid et al[14] showed that at least one communicating nerve branch between cervical plexus and SAN is present in each dissection. Motor nerves formed only 32% of the nerve fibers based on the intraoperative electromyography and it was concluded that trapezius receives motor supply from cervical plexus, but the motor innervation from cervical plexus is limited. Whilst Karuman et al[15] reported that 61% of communicating nerves were motor fibers regarding their histochemical evidence. Likewise, Soo et al[16], reported that not only SAN, C3 and C4 nerves, but also the T1 and T2 innervate the lower trapezius muscle.

On the other hand, some authors are completely against trapezius dual innervation hypothesis. In the study conducted by Kierner et al[17] on 11 human cadavers the innervation to all 22 lower trapezius muscles were by a single fine branch of the spinal accessory nerve and no other branch to descending portion was found; which is contrasted by results in our study. Nonetheless Stacey et al[18] claimed that the cervical plexus innervations is not clear accurately. Likewise, based on the literature much controversy are obvious regarding the exact proportion of trapezius which is innervated by either SAN, cervical plexus or a further undescribed motor supply[16].

The hypothesis of dual innervation is anatomically plausible due to documented cervical plexus contributions. Gavid et al[14] demonstrated consistent nerve communication between cervical plexus (C2-C4) and SAN, with variable motor fiber contributions. Conversely, Kierner et al[17] found exclusive SAN innervation of the trapezius. These anatomical discrepancies highlight the need for further cadaveric and clinical studies to clarify trapezius innervation comprehensively.

To sum up everything that has been stated so far, dual innervation of the trapezius muscle is not far from the mind. This may provide the possibility of further trapezius tendon transfer also known as tendon grafting or tendon transplantation, is a surgical procedure in which a healthy tendon is relocated from one part of the body to another to restore or improve the function of a damaged or weakened muscle or joint. To restore a better shoulder function. The use of physiotherapy and exercise would definitively strengthen the aforementioned muscle and so make it more suitable for tendon transfer. Moreover, further studies are recommended to determine the nerves responsible for motor innervation of trapezius as well as the factor which may affect the function of trapezius muscle after SAN transfer.

In addition, current study showed that the use of posterior approach for SAN-SSN transfer has a successful functional outcome; among our patients, 94.74% regained their shoulder abduction and external rotation with an average of 56.5° and 54° respectively during the mean follow up of 10 months. Only one patient didn’t gain any shoulder function. To describe more precisely 68.4% of patients had moderate or good shoulder abduction and poor recovery was seen only in 26.3% of them.

Songcharoen et al[5] reported the success rate of 80% with the mean shoulder abduction of 60% among 557 SAN transfer which was almost compatible with our study. On the contrary, Suzuki et al[19] demonstrated the 95% of regained shoulder function with the average abduction range of 70° during the mean follow up of 28.5 months. The higher success rate of the aforementioned study can be contributed to longer follow up time. On the other hand, Bertelli et al[20] reveled that among 22 patients, the 21 ones regained the shoulder abduction with the mean range of 56.5° while only two of them regained the external rotation. The authors claimed that the poor results are because of the multi-level injuries as well as the longer distance of the target muscle.

Numerous factors such as surgeon's experience, mechanism and simultaneous trauma, and rehabilitation programs can change the results of this operation. Determining the effectiveness of these factors is not possible due to the limited number of samples in many studies. Therefore, conducting multicenter studies to expand the study participants as well as conducting systematic review studies to summarize the findings in this field can help determine the final result and provide a guideline.

A major limitation of this study is its retrospective design and relatively small sample size (n = 19), which restricts the generalizability of the results. Future multicenter studies with larger cohorts are needed to validate these findings. Another limitation of our study is the relatively short follow-up period (mean 10.5 months). Longer-term studies are necessary to confirm the sustainability and progression of nerve recovery following SAN-SSN transfers. Given the retrospective nature, this study is susceptible to selection bias. Variations in rehabilitation adherence and patient compliance could also introduce confounding factors, potentially influencing outcomes.

CONCLUSION

This article supports the hypothesis that the lower trapezius muscle has a dual motor innervation. EMG-NCV showed functional lower trapezius in all patients after transferring the spinal accessory nerve to suprascapular nerve neve. This is an important issue as a functional lower trapezius muscle can be used for further musculotendinous transfer to restore shoulder function.