Restoring elbow flexion is 1 of the primary goals in treating patients with brachial plexus injury.1 For such treatment, transfer of an ulnar nerve fascicle to the biceps motor branch has been widely accepted as an effective surgical technique to restore elbow flexion following an upper brachial plexus injury.2-5 Nevertheless, according to some authors, restoring elbow flexion through isolated reinnervation of the biceps muscle may be insufficient for 2 reasons.6-10 First, some patients may be able to raise their arm against gravity but may not be able to lift objects, and, in these cases, other procedures, such as the Steindler flexorplasty, are necessary to further improve the elbow flexion strength.11,12 Second, the muscle activity differs between biceps or brachialis muscle contraction: the primary function of the biceps muscle is forearm supination, acting as a secondary elbow flexor, whereas the brachialis muscle acts primarily as an elbow flexor.8 These observations have led some authors to recommend concomitant biceps and brachialis muscle reinnervation to improve elbow flexion strength.6-10
Tung et al8 first reported the concomitant reinnervation of the biceps and brachialis muscles in 2003. Since then, several reports on the use of this technique in brachial plexus surgery have been published and have demonstrated excellent results concerning elbow flexion strength.6,9,12-14 Although the degree of improvement obtained with this procedure seems unquestionable, a prospective comparison between single and double muscle reinnervation for restoring elbow flexion following an upper brachial plexus injury has not yet been performed. Therefore, we designed the present study to prospectively compare the morbidity and results of both techniques.
MATERIAL AND METHODS
Study Design and Setting
The study was a prospective surgical trial comparing 2 techniques performed to restore elbow flexion in patients with partial brachial plexus injury and was conducted from February 2007 to February 2012 at the Peripheral Nerve Surgery Unit of the Division of Neurosurgery at the University of São Paulo Medical School and the Division of Neurosurgery at the Santa Marcelina Hospital. A total of 43 patients were randomly alternately assigned to 2 groups of treatment. The protocols were approved by the ethics committee of each hospital (Protocols 0382/08 and 13/07, respectively), and an informed consent was obtained from all participants.
Patients with brachial plexus traction injuries associated with preserved function of the lower roots were eligible for this study. After admission, all patients underwent systematic assessment of light-touch sensation and muscle strength of the upper limb to characterize the extent and degree of brachial plexus injury. This degree was classified as predominantly compromising the C5 and C6 roots (C5C6) or C5, C6, and C7 roots (C5C6C7). A standard investigation including electromyography, nerve conduction studies, and cervical computed tomomyelography was also performed. Surgery was recommended for patients who had no signs of spontaneous recovery 3 months after injury or for patients admitted later with a fixed deficit.
Distal nerve transfers to restore elbow flexion were indicated based on the timing of clinical presentation, imaging findings, or intraoperatively defined root aspect. For patients who presented more than 6 months after injury (n = 31) or for those with evidence of root avulsion identified by tomomyelography (n = 6), distal nerve transfer was undertaken without root exploration, and the brachial plexus was exposed only partially to transfer the distal spinal accessory to the suprascapular nerve. Distal nerve transfers were also indicated if unavailable roots were identified during the brachial plexus exposure (n = 6).
In both groups, the surgical procedure was performed according to the previous description of Oberlin's technique of transferring an ulnar nerve fascicle to the biceps motor branch in the arm,2 which includes fascicle selection based on electrical stimulation and neurorrhaphy with the use of 10-0 nylon sutures (Figure 1). In group A, the single muscle reinnervation group, the surgical procedure was restricted to Oberlin's technique. In group B, the double muscle reinnervation group, patients received the surgical procedure performed as described in group A as well as a fascicle transfer from median nerve to the musculocutaneous motor branch to the brachialis muscle.8 To this end, distal dissection of the musculocutaneous nerve allowed identification of the motor branch to the brachialis muscle that was sectioned proximally and rerouted to the median nerve. Electrical stimulation was used to determine which section of the median nerve should be explored. The epineurium of the median nerve was opened longitudinally under the microscope, and further electrical stimulation was used to select the fascicle, preferentially those related to flexor carpi radialis or pronator teres muscles innervation. The selected fascicle was sectioned and coapted to the motor branch of the brachialis muscle by means of 10-0 nylon sutures (Figure 2). Transfer of the distal accessory spinal nerve to the suprascapular nerve was also performed in all patients. After this, the wounds were closed in layers, and the limb was immobilized for 3 weeks postoperatively before resuming a physical rehabilitation program.
Variables and Measurements
Postoperative assessment included measurement of the elbow flexion strength and evaluation of the morbidity related to donor nerve transfer. Elbow flexion strength was evaluated 12 months after surgery by using a push-and-pull dynamometer (Baseline, Fabrication Enterprises, Inc, Elmsford, New York) on both the healthy and compromised sides. In order to reduce the subjectivity of the Medical Research Council in testing muscle strength,15,16 an index, named the flexion index (FI), was calculated by dividing the elbow flexion strength obtained on the injured side by the same measurement evaluated on the healthy side, and compared between the 2 groups. Accordingly, the healthy side from each patient served as its own control.
Morbidity related to donor nerve was evaluated preoperatively and 3 months after surgery, with subsequent evaluations at 6 and 12 months. Thumb, index, and small fingertip sensibility was assessed by the Semmes-Weinstein monofilaments test (Sorri, Brazil) and static 2-point discrimination evaluation (2-point discriminator, Baseline), whereas the Medical Research Council scale was used for both pre- and postoperative evaluation of the wrist flexors and intrinsic hand muscles. Handgrip and lateral pinch grip strength were measured by using a Jamar dynamometer (North Coast Medical Inc, Gilroy, California) on the second handle position and a hydraulic pinch gauge (Baseline), respectively. The best value of 3 consecutive trials was used in each case for both measurements. All the measurements performed with dynamometers were measured in kilograms.
Bias and Study Size
In order to reduce a potential source of bias, all evaluations were made by the same examiner, and all surgeries were performed by the same surgeon (R.S.M.), but he was not blinded to the treatment group.
The sample size was calculated with part of the collected data at the end of the second year of this study. Considering the mean and standard deviation, we performed a statistical power analysis to estimate the number of subjects who would be required to reach significance with P less than .05 and power at .80. An almost prohibitive number of 84 patients were obtained in each group, which would require 17 years for the project to be completed impending its implementation in a single institution. So, the study was completed for 40 subjects after 5 years from the initial inclusion.
Results were expressed as means and standard deviations. Statistical analysis was performed by using Bioestat (version 2.0, Ayres M, Belém, Brazil) and SPSS (version 13.0; SPSS, Inc, Chicago, Illinois) software.
A comparison between the 2 groups was established with the use of parametric and nonparametric tests. Each variable was tested to evaluate the symmetry and kurtosis and subjected to the Shapiro-Wilk test to ensure normality.17,18 An independent t test was used to compare age and the interval between surgery and injury between the 2 groups. The FI was compared between groups by the Mann-Whitney U test. Contingency tables were constructed, and Fisher exact tests were performed to compare the distribution of patients concerning the clinical presentation between groups and to assess whether the distributions of patients who had reduced handgrip and lateral pinch strength differed according to the operative technique.
Spearman coefficient was used to determine the relationship between the 2 main factors related to prognosis after brachial plexus surgery, age and interval between injury and surgery, and the results of FI. All tests were 2-tailed, and a significance level of 5% was used for all comparisons.
Participants and Descriptive Data
A total of 43 patients were initially assigned to this study. Three patients were lost during the follow-up period and were not considered in the final analysis. Therefore, 40 patients completed the minimal follow-up period of 12 months, with 20 subjects in each group.
Table 1 summarizes the sample characteristics. The mean age was 28.7 ± 8.4 years, ranging from 18 to 49. No difference was identified in age between the 2 treatment groups (t test: t(38) = −0.373 and P = .712). Likewise, the time between the injury and surgery was not statistically different between the 2 groups (t test: t(38) = −0.618 and P = .536) (Figure 3). In the majority of cases (93%), the brachial plexus injury was due to a motorcycle (n = 35) or bicycle accident (n = 2); fall (n = 2) and car accident (n = 1) were the causative factors in the remaining patients.
Table 2 shows the distribution of patients according to the extent of injury to the brachial plexus roots. There was a predominance of the C5C6 root injuries, presenting in 75% of the patients, and no significant difference between the 2 groups regarding the extent of root involvement was identified (Fisher exact test, P = .274).
Outcome Data and Main Results
Elbow Flexion Strength
The mean elbow flexion strength measured by a push-and-pull dynamometer, evaluated on the normal (SN) and injured (SI) side after a 12-month period was 21.76 ± 5.29 and 4.87 ± 2.93 Kgf in all patients. The mean values of SN and SI in group A were 21 ± 5.71 Kgf and 4.14 ± 3.27 Kgf, respectively. For patients submitted to the double muscle reinnervation technique (group B), the values of SN and SI were 22.53 ± 4.87 Kgf and 5.6 ± 2.41 Kgf, respectively. The mean value of the FI was 0.20 ± 0.13 in group A and 0.25 ± 0.10 in group B; there was no statistically significant difference between the groups (Mann-Whitney U test, P = .078; 95% confidence interval, 0.18-0.26). Table 3 presents the mean values of the SN, SI, and FI in both treatment groups. Elbow contractures were not identified in any group.
No significant correlation was observed between age and FI (rs = 0.02, P = .89) or between the time from injury to surgery and FI (rs = −0.24, P = .143).
No major complications related to the surgical procedure were reported. In the single muscle reinnervation group, 1 patient had a short dehiscence of the proximal arm incision that resolved with local care within a few days of treatment.
Eight patients, 6 belonging to group A, showed worsening of the pressure thresholds assessed by the Semmes-Weinstein monofilaments test comparing the preoperative evaluation and the measurements performed 3 months after surgery. In all of these cases, impaired recovery of the pressure thresholds was detected on subsequent evaluations during the follow-up period. More commonly, in 75% of the cases, this recovery occurred between the second and third evaluations, and, in only 2 patients, one from each group, the improvement was observed between the preoperative and the final examination. No impairment was observed concerning the static 2-point discrimination evaluation.
The mean values of pre- and postoperative handgrip and lateral pinch grip strength are presented in Tables 4 and 5. Three months after surgery, compared with the preoperative evaluation, the assessment of morbidity in the hand showed worsening of the handgrip strength and lateral pinch strength in 8 (20%) and 9 (22.5%) patients, respectively. Worsening of the handgrip strength occurred in 3 patients who underwent single muscle reinnervation and in 5 patients submitted to the double muscle reinnervation. There was no significant difference between the 2 groups concerning worsening of the handgrip strength (Fisher exact test, P = .695). All patients with impaired handgrip strength after surgery showed improvement during the follow-up period. This improvement was observed 6 and 12 months after surgery in 5 and 3 patients, respectively. Impairment of lateral pinch strength was identified in 2 cases treated with the technique of single muscle reinnervation and 7 patients who underwent double muscle reinnervation. All patients who presented worsening in thumb pinch strength after surgery showed improvement during the follow-up period. Except for 1 patient whose restoration of thumb pinch strength was identified only in the final evaluation, all patients showed improvement 6 months after surgery. No significant difference was identified between the 2 groups regarding the impairment of thumb pinch strength (Fisher exact test, P = .127).
The comparison of the strength of the elbow flexion by the ratio between the strength measured in injured and normal side using a push-and-pull dynamometer showed that single and double muscle reinnervation following partial brachial plexus injury are both equivalent. There was no correlation between elbow flexion strength and factors classically associated with unsatisfactory results after brachial plexus surgery, such as age and the time between the injury and surgery.19-21
The results of the present study confirm that fascicle transfers for restoring elbow flexion have favorable outcomes, with an acceptable incidence of morbidity. Subjective symptoms, such as tingling in the hand, occurred in 0% to 50% of patients and usually resolved within a few weeks or months after surgery.22-24 On the basis of the present study, alteration in fingertip sensitivity, represented mainly by an impairment of the tactile perception threshold, can be observed in up to 20% of cases with recovery usually over a year after surgery.
Limitations of the Study
The present study has 3 major limitations. First, the examiner was not blind to the distribution of patients in each group. Second, there was no evaluation of forearm supination, a movement requiring heavy participation of the biceps muscle. Third, this study lacks high statistical power because of the small number of subjects. Despite these drawbacks, this study provides important information regarding distal nerve transfers for the recovery of elbow flexion, and it is the first prospective study that compares the 2 main techniques used for this purpose.
Interpretation of Findings in Relation to Previously Published Work
It would be reasonable to expect that concomitant reinnervation of the biceps and brachialis muscles should result in greater elbow flexion strength in comparison with isolated reinnervation of the biceps muscle. Despite this expectation, our results showed equivalent results for both techniques. A similar observation was reported recently in a retrospective study comparing the 2 techniques.25 In fact, the exact involvement of the brachialis muscle in the dynamics of the elbow flexion is still controversial, which could justify these results.
According to several authors, forearm supination is the main function of the biceps muscle, which acts as a secondary muscle in elbow flexion, whereas the brachialis muscle is the strongest flexor of the elbow.6,8,10 Although these observations are widely accepted, several studies have presented contradictory evidence. Tendon transfer of the brachialis muscle has been used to treat deformities and to improve hand function after brachial plexus injuries; in these cases, loss of elbow flexion has not been reported.26,27 Otherwise, transfer of the biceps muscle has been associated with a reduction in the strength of elbow flexion.28,29 Findings obtained from the treatment of brachial plexus injuries with nerve transfer also suggested that the function of the brachialis muscle in elbow flexion strength needs to be reevaluated.30,31 As reported by Palazzi et al30 and Zheng et al,31 impairment of the elbow flexion strength was not observed after using the motor branch to the brachialis as a donor nerve. Furthermore, according to Palazzi et al, the brachialis muscle contributes only 10% to 20% to the total strength of elbow flexion.24,30 Comparison between nerve transfer to the biceps muscle and isolated reinnervation of the brachialis muscle should be investigated in a future study to clarify this issue.
Our results concerning the relationship between elbow flexion strength and preoperative delay are consistent with studies published by Teboul et al and Sedain et al, who also evaluated results after the Oberlin procedure.12,32 Teboul et al found no significant difference in the recovery of biceps muscle strength when comparing patients operated on before or after 6 months from injury.12 In Sedain et al, although the surgery was performed with a mean time of 12.2 months after injury, the elbow flexion strength was classified as M3 or better in 77.8% of the subjects.32 Two possible factors contribute to the lack of a correlation between the time from injury to surgery: the proximity between muscle and neurorrhaphy and the direct coaptation between donor and recipient nerves. As a consequence, regenerating axons need to travel only a short distance, which reduces the axonal loss. Furthermore, nerve transfer with direct sutures represents only 1 obstacle at the site of coaptation to regenerating axons, instead of 2 in reconstruction with an interposed nerve graft.33-35 These observations are corroborated by the findings of a recent systematic review performed by Garg et al,36 who compared distal nerve transfers with reconstructions with grafts from 31 studies evaluating surgical results after a partial injury of the brachial plexus. The authors concluded that outcomes related to the recovery of shoulder abduction and elbow flexion after nerve transfers are better in comparison with those obtained by reconstruction with grafts.36 Similar results concerning elbow flexion strength were recently published by Socolovsky et al37 in a study comparing transfer of an ulnar nerve fascicle to the branch of the biceps muscle with reconstruction by using nerve grafts following partial injury of the brachial plexus.
The results regarding motor morbidity in the hand are consistent with those reported in previous studies on patients submitted to distal nerve transfer after partial injury of the brachial plexus. A worsening of the grip and pinch strength was observed in a small number of patients, with recovery of both functions during follow-up.3,8-10,13,22
Elbow flexion strength did not differ significantly between the groups treated with single or double reinnervation of the elbow flexor muscles. Deterioration of the handgrip, pinch strength, and sensibility measured by using Semmes-Weinstein monofilaments was temporary, resulting in low morbidity for both techniques.
This study was supported by the National Council for Scientific and Technological Development (CNPq). The authors have no personal financial or institutional interest in any of the drugs, materials, or devices described in this article.
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This article is a prospective study comparing single and double fascicular transfers to restore elbow flexion after brachial plexus injury. As more and more transfer procedures are described, it is important to delineate which of these procedures are actually contributing to the patient's recovery vs those that are being done because they are feasible. This article is important in that it is well designed, albeit with some flaws as indicated by the authors, to investigate very specifically a single transfer vs a double transfer to restore elbow flexion. The results point to the conclusion that a single transfer is sufficient. This knowledge saves the surgeon and the patient from the performance of an unnecessary procedure. As evidence-based medicine and surgery move to the forefront of our practices, this type of article becomes ever more valuable.
Allen H. Maniker
New York, New York
1. In treating an upper trunk brachial plexus injury, what is the advantage of double nerve transfer over single nerve transfer for restoring elbow flexion?
a. Improved elbow flexion strength
b. Increased hand strength
c. Decreased time to reanimation
d. No advantage
2. The transfer of an ulnar fascicle to the musculocutaneous nerve to restore elbow flexion can result in new hand weakness. What is the average time to recovery of hand grip strength after these surgeries?
a. 1 month
b. 3 months
c. 6 months
d. 12 months
e. 24 months
3. In addition to elbow flexion, what is another function of the biceps muscle?
c. Arm abduction
d. Arm extension