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Table of Contents
ORIGINAL ARTICLE
Year : 2019  |  Volume : 9  |  Issue : 1  |  Page : 55-59

Optimal nerve transfer for elbow flexion restoration in brachial plexus injuries: An analysis of postoperative recovery


1 Center for Brachial Plexus and Traumatic Nerve Injury, Hospital for Special Surgery, New York, NY; Department of Orthopaedic Surgery, Duke University Medical Center, Durham, NC, USA
2 Center for Brachial Plexus and Traumatic Nerve Injury, Hospital for Special Surgery, New York, NY, USA
3 Healthcare Research Institute, Hospital for Special Surgery, New York, NY, USA

Date of Submission12-Sep-2019
Date of Acceptance23-Sep-2019
Date of Web Publication28-Feb-2020

Correspondence Address:
Dr. Eliana B Saltzman
Department of Orthopaedic Surgery, Duke University Medical Center, Box 3000, Durham, NC, 27710
USA
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/DORJ.DORJ_8_19

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  Abstract 


Aim: Following upper brachial plexus injury, one of the primary goals of reconstruction is reinnervation of elbow flexion (EF). Various reconstruction methods have been described including ulnar nerve fascicle and/or median nerve fascicle transfer to the musculocutaneous biceps brachii motor branch and/or the brachialis motor branch. However, there is no study that analyzes the efficacy of one set of transfers to another. We aim to determine if there are improved outcomes with the ulnar nerve transfer to biceps branch and median nerve transfer to brachialis branch (UBB/MBr, Group 1) compared to ulnar nerve transfer to brachialis and median nerve transfer to biceps branch (UBr/MBB, Group 2).
Methods: We performed a retrospective analysis of 12 patients who sustained C5–C6 ± C7 brachial plexus injuries and underwent nerve transfers for EF reconstruction. All clinical and electromyographic (EMG) data were captured for an average follow-up time of 35 months. Data were analyzed using a generalized estimating equation model (P < 0.05).
Results: Seven and five patients were included in Groups 1 and 2, respectively. At 6 months, Group 2 achieved a greater Medical Research Council score of global elbow function 4 versus 1.5 (P < 0.05), biceps strength 3.67 versus 2.13 (P < 0.05), and brachialis strength 3.5 versus 2.5 (P < 0.05). The brachialis EMG recruitment pattern also demonstrated improved results in Group 2 as compared to Group 1 at 12, 24, and 36 months (P < 0.05).
Conclusion: These findings indicate that UBr/MBB nerve transfer confers significantly faster recovery of global EF, biceps, and brachialis strength at 6 months. Although differences in strength equalized by 24 months, EMG data demonstrated increased muscle nerve potential in Group 2 at 12 months and beyond.
Clinical Significance: The median nerve fascicle transfer to the biceps branch and ulnar nerve fascicle transfer to brachialis branch appear to have advantages in EF function.

Keywords: Anatomy, axons, brachial plexus, elbow flexion, nerve reconstructive, nerve transfer, retrospective study


How to cite this article:
Saltzman EB, Fullerton N, Nguyen JT, Feinberg JH, Lee SK, Wolfe SW. Optimal nerve transfer for elbow flexion restoration in brachial plexus injuries: An analysis of postoperative recovery. Duke Orthop J 2019;9:55-9

How to cite this URL:
Saltzman EB, Fullerton N, Nguyen JT, Feinberg JH, Lee SK, Wolfe SW. Optimal nerve transfer for elbow flexion restoration in brachial plexus injuries: An analysis of postoperative recovery. Duke Orthop J [serial online] 2019 [cited 2020 Apr 7];9:55-9. Available from: http://www.dukeorthojournal.com/text.asp?2019/9/1/55/279435




  Introduction Top


High-energy upper brachial plexus traction traumas are devastating injuries that often leave the affected individuals with severe arm and shoulder deficits. Once the injury is established, microsurgical reconstruction of the brachial plexus has been shown to improve the patients' functional outcomes.[1],[2] The priorities of reconstruction begin with elbow flexion (EF), followed by shoulder stabilization, abduction, and external rotation. The importance of the return of EF for activities of daily living becomes imperative for the function of bringing the environment toward or away from the body.

Oberlin first described the partial ulnar nerve transfer to the musculocutaneous branch of the biceps brachii for reconstruction of EF in 1994. The argument for the superiority of this nerve transfer included: the proximity of the ulnar nerve to the musculocutaneous branch to the biceps brachii, allowing for direct repair without an intervening nerve graft, resulting in rapid reinnervation; the small size of the nerve to the biceps only requires a thin fascicle of the ulnar nerve for reinnervation; and the ease of ulnar nerve fascicle selection with the use of electrical stimulation.[3],[4]

Nine years later, sungpet described the use of the median nerve transfer to the motor branch of the biceps brachii muscle. In their review, four out of five patients achieved a Medical Research Council (MRC) score of M4 and one patient with a score of M3 with a follow-up of 32 months.[5] Subsequently, double-nerve transfers have been performed with the ulnar and median nerve transferred to the motor branch of the biceps brachii and brachialis muscle, resulting in superior results compared to either single-nerve transfers.[6],[7] One explanation was offered by Mackinnon et al., who recognized the brachialis muscle as the main elbow flexor and the biceps brachii as the main supinator of the arm; therefore, a nerve transfer to both muscles confers a significant advantage for improving EF strength.[6]

However, there is no consensus as to which nerve transfer combination, ulnar nerve to biceps brachii and median nerve to brachialis or median nerve to biceps brachii and ulnar nerve to brachialis, results in superior EF strength. The aim of this study was to investigate if one combination of nerve transfers for EF, ulnar fascicular nerve transfer to brachialis and median fascicular nerve transfer to biceps brachii motor branch or the ulnar fascicular nerve transfer to biceps brachii and median fascicular nerve transfer to brachialis motor branch, was superior to the other in order to guide future decisions on EF nerve transfer reconstruction in upper brachial plexus nerve injuries.


  Methods Top


This study was approved by the authors' institutional review board. All patients who require surgical intervention for brachial plexus injuries (BPI) are enrolled in the institutional registry. Records of MRC grade, range of motion, electromyographic (EMG) studies, surgical interventions, and demographics were reviewed.

We performed a retrospective analysis on all patients in the registry who sustained a C5–C6 or C5–C7 BPI who then underwent a double-nerve transfer with either an ulnar fascicular nerve transfer to brachialis and median fascicular nerve transfer to biceps brachii motor branch (UBB/MBr, Group 1) or an ulnar fascicular nerve transfer to biceps brachii and median fascicular nerve transfer to brachialis motor branch (UBr/MBB, Group 2), without the use of interposition grafts, between 2005 and 2013. Exclusion criteria included patients under the age of 18, atraumatic brachial plexus injury, complete and/or lower BPI, presentation >1 year following injury, and patients with other injuries in the affected arm.

Data on patient demographics, time to surgery, mechanism of injury, preoperative physical examination with MRC grade and EMG, and follow-up physical examination with MRC grade and EMG data were recorded at 3, 6, 9, 12, 24, and >36 months when available. EF strength was measured with the patient's forearm in supination and elbow at 90°. Patients were assigned a MRC score of M0–M5 according to validated grading standards.

EMG data was acquired prior to surgical intervention and at various postoperative intervals of each of the tested muscles. All EMGs were performed and interpreted by a single electrodiagnostic expert. The data were used to evaluate motor recruitment and was categorized according to a previously published scale. Briefly, functionally normal recruitment patterns were categorized as full. Large number of motor unit firing that does not fill the EMG screen is categorized as decreased. Small number of motor units firing with identifiable motor units being identified is categorized as discrete. Finally, when no motor units fire, the pattern is categorized as none. The variables were numbered on a continuous scale from 1 to 4.

Operative procedure

In both groups, the surgical procedure was performed with standard technique for nerve transfer. Identification of the ulnar and median nerve fascicles to be transferred was performed with electrical stimulation. Nerves were microsurgically coapted with 10-0 nylon. Fibrin glue was used to reinforce the repair. In Group 1, the ulnar fascicular nerve was transferred to biceps brachii musculocutaneous motor branch and the median fascicular nerve was transferred to brachialis musculocutaneous motor branch. In Group 2, the ulnar fascicular nerve was transferred to brachialis musculocutaneous motor branch and a median fascicular nerve was transferred to the biceps brachii musculocutaneous motor branch.

Statistical analysis

Means and standard deviations were used to report descriptive statistics of continuous data. Frequencies and percentages were used to report on discrete patient and clinical characteristics. Nonparametric Mann–Whitney U-tests were used to compare differences in continuous variables, while Fisher's exact tests were used to analyze categorical factors. Generalized estimating equation (GEE) modeling was used to assess the longitudinal assessment of patient outcomes between the two study groups. This modeling technique was chosen due to its robust nature of handling data, regardless of whether or not they meet the assumption of normality. In addition, GEE allows for the clustered analysis of all observations that have been collected longitudinally and accounts for any missing data from patients who were lost to follow-up. All observations were analyzed using maximum likelihood estimations. Models included time as the sole predictor (treated as a fixed effect) as well as observed differences between the two transfer groups. Bonferroni correction was used to adjust for multiple pair-wise comparisons. Statistical significance was defined as P ≤ 0.05. All analyses were performed with SPSS, version 22.0 (IBM Corp., Armonk, NY, USA).


  Results Top


Seven patients underwent ulnar fascicular nerve transfer to biceps musculocutaneous motor branch and median fascicular nerve transfer to brachialis musculocutaneous motor branch (UBB/MBr), labeled as Group 1. Five patients underwent ulnar fascicular nerve transfer to brachialis musculocutaneous motor branch and median fascicular nerve transfer to biceps brachii musculocutaneous motor branch (MBB/UBr), comprising Group 2. The mean follow-up time was 35 months [range: 8–98 months, [Table 1].
Table 1: Patient characteristics

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The mean age at the time of surgery was 37 years (range: 18–75 years). There was no significant difference in age between the two cohorts (P = 0.26). Similarly, there was no difference between the two cohorts in patients who sustained a C5–C6 injury and patients who sustained a C5–C7 injury (P = 0.23 and P = 0.60, respectively). The mechanism of injury between the two cohorts also did not differ significantly, with motorized vehicles leading to the majority of the injuries in both, comprising six patients in Group 1, and five patients in the Group 2 (P = 0.42). Finally, the average time to surgery was 5.6 months in Group 1 and 4.6 months in Group 2, which was not statistically significant (P = 0.46).

Analyzing global EF strength, there was no difference in MRC score at 3 months. However, at 6 months, there was a significantly higher average of MRC scores among patients in Group 2 as compared with Group 1 (P < 0.005). At 9 months and onward, the MRC scores were not significantly different, although there was an overall trend of higher MRC scores in Group 2.

The interval EMG tests demonstrated that there was no significant difference in the biceps brachii function between the two cohorts at each time point, although there appeared to be a trend of improved EMG recruitment in Group 2. The brachialis EMG showed significantly improved recruitment of the brachialis muscle in Group 2, at 12, 24, and 36 months (P = 0.01, 0.03, and 0.03, respectively).


  Discussion Top


Partial ulnar nerve transfer to the motor branch of the biceps brachii to restore EF in C5–C6 and C5–C7 injuries transformed microsurgical reconstruction of the brachial plexus.[2],[4],[8],[9],[10] The double-nerve transfer of partial ulnar and partial median nerve to the motor branch of the biceps brachii and brachialis muscle further improved EF strength outcomes.[6],[7],[11],[12] However, there is no consensus as to which nerve transfer, partial ulnar or partial median nerve, is more appropriate to target the motor branch of the biceps brachii or the motor branch of the brachialis.

This investigation demonstrated that there was significantly faster recovery in overall global EF strength at 6 months in the cohort of patients who underwent transfer of the ulnar fascicular nerve to brachialis and median fascicular nerve transfer to the motor branch of biceps brachii, Group 2. Differences in MRC scores showed no difference by 12 months. Furthermore, EMG results demonstrated parallel recruitment patterns as to the strength scores in the brachialis muscle at those same time points. In Group 2, the brachialis reinnervation pattern improved from an initial decreased recruitment pattern after surgery to a full recruitment pattern at the final follow-up. In contrast, in Group 1, the brachialis had a discrete recruitment pattern immediately after surgery which improved to only a decreased recruitment pattern at the final follow-up.

Previous research has shown that there is an optimal size match between the donor and recipient nerves that predicts clinically improved EF strength, with a minimum donor-to-recipient ratio of 0.7:1 predicting a successful transfer and with improved results with greater donor-to-recipient ratios. In the study by Schreiber et al., cadaveric dissection demonstrated that the ulnar fascicular nerve to biceps nerve transfer had a ratio of 1.1:1 and the median nerve to brachialis transfer had a ratio of 1:1. From the axonal counts, the median nerve to biceps nerve transfer ratio can be calculated to be 1:1 and the ulnar fascicular nerve to brachialis transfer ratio to be 1.1:1.[13] While it would have been interesting to see if in our study, there was a correlation between improved EF strength and increased donor-to-recipient ratios between the two cohorts, this was not a defined variable our study. More specifically, Group 2 may represent a superior reconstruction option as the result of the higher nerve ratio of the ulnar fascicular nerve to brachialis transfer as compared to the median nerve, thus providing more axons to regenerate the large elbow flexor muscle.

When examining the elbow flexors, the brachialis muscle is considered the main flexor of the elbow. The superficial head of the brachialis, innervated by the musculocutaneous nerve, originates on the anterolateral aspect of the humerus and inserts on the ulnar tuberosity, providing the greatest moment arm for EF. The deep head of the brachialis, innervated by the radial and musculocutaneous nerve, originates distal to the superficial head of the brachialis on the humerus and inserts onto the coronoid process, providing a greater flexion moment during elbow extension.[14] Although, reinnervation of two elbow flexors has proven to be superior to the innervation of a single elbow flexor, it is understandable that providing superior reinnervation to the stronger elbow flexor would result in improved global EF strength.[6],[7],[11],[12],[15] Therefore, one can imagine that the reinnervation of two elbow flexors can certainly lead to better outcomes, then reinnervation of one elbow flexor; however, functional outcome in dual reinnervation is likely still biased to quality of the reinnervation of the stronger elbow flexor for overall clinical improvement.

This study is not without limitations. Like most brachial plexus injury studies, the main limitation of this study is its small population size. A larger sample size could reveal increased differences between the two cohorts, particularly as there is a trend of increasing elbow function in Group 2, at 12, 24, and 36+ months. Finally, previous work by the same author group has demonstrated that patients with BPI continue to demonstrate clinical improvement even at 11 years following nerve transfers, so additional follow-up of this cohort may be valuable to demonstrate if there are long-term strength and functional differences between the two groups.[16] Nonetheless, we believe that the objective clinical and EMG improvements documented in this small cohort are representative of recovery after brachial plexus reconstruction for upper plexus palsy and may provide additional information to both surgeons and patients when deciding between these two surgical options.

Clinical significance

The results from this study may indicate that median nerve transfer to biceps and ulnar nerve transfer to brachialis motor branch, Group 2, confers faster recovery of global EF, biceps, and brachialis strength at 6 months. Furthermore, the EMG data also suggested increased muscle nerve potential in the median nerve to biceps and ulnar nerve to brachialis motor branch at 12 months and beyond. Given these results, the median nerve transfer to biceps and ulnar nerve transfer to brachialis motor nerve appears to have advantages in transfer technique for EF function in traumatic upper plexus BPI.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Swanson AN, Wolfe SW, Khazzam M, Feinberg J, Ehteshami J, Doty S. Comparison of neurotization versus nerve repair in an animal model of chronically denervated muscle. J Hand Surg Am 2008;33:1093-9.  Back to cited text no. 1
    
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Socolovsky M, Martins RS, Di Masi G, Siqueira M. Upper brachial plexus injuries: Grafts vs. ulnar fascicle transfer to restore biceps muscle function. Neurosurgery 2012;71:ons227-32.  Back to cited text no. 2
    
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Leechavengvongs S, Witoonchart K, Uerpairojkit C, Thuvasethakul P, Ketmalasiri W. Nerve transfer to biceps muscle using a part of the ulnar nerve in brachial plexus injury (upper arm type): A report of 32 cases. J Hand Surg Am 1998;23:711-6.  Back to cited text no. 10
    
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Martins RS, Siqueira MG, Heise CO, Foroni L, Teixeira MJ. A prospective study comparing single and double fascicular transfer to restore elbow flexion after brachial plexus injury. Neurosurgery 2013;72:709-14.  Back to cited text no. 12
    
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Schreiber JJ, Byun DJ, Khair MM, Rosenblatt L, Lee SK, Wolfe SW. Optimal axon counts for brachial plexus nerve transfers to restore elbow flexion. Plast Reconstr Surg 2015;135:135e-41e.  Back to cited text no. 13
    
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Leonello DT, Galley IJ, Bain GI, Carter CD. Brachialis muscle anatomy. A study in cadavers. J Bone Joint Surg Am 2007;89:1293-7.  Back to cited text no. 14
    
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Bhandari PS, Deb P. Fascicular selection for nerve transfers: The role of the nerve stimulator when restoring elbow flexion in brachial plexus injuries. J Hand Surg Am 2011;36:2002-9.  Back to cited text no. 15
    
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