Nerve graft versus nerve transfer for neonatal brachial plexus: shoulder outcomes

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  • 1 Department of Neurosurgery, University of Michigan, Ann Arbor, Michigan
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OBJECTIVE

The decision-making in neonatal brachial plexus palsy (NBPP) treatment continues to have many areas in need of clarification. Graft repair was the gold standard until the introduction of nerve transfer strategies. Currently, there is conflicting evidence regarding outcomes in patients with nerve grafts versus nerve transfers in relation to shoulder function. The objective of this study was to further define the outcomes for reconstruction strategies in NBPP with a specific focus on the shoulder.

METHODS

A cohort of patients with NBPP and surgical repairs from a single center were reviewed. Demographic and standard clinical data, including imaging and electrodiagnostics, were gathered from a clinical database. Clinical data from physical therapy evaluations, including active and passive range of motion, were examined. Statistical analysis was performed on the available data.

RESULTS

Forty-five patients met the inclusion criteria for this study, 19 with graft repair and 26 with nerve transfers. There were no significant differences in demographics between the two groups. Understandably, there were no patients in the nerve grafting group with preganglionic lesions, resulting in a difference in lesion type between the cohorts. There were no differences in preoperative shoulder function between the cohorts. Both groups reached statistically significant improvements in shoulder flexion and shoulder abduction. The nerve transfer group experienced a significant improvement in shoulder external rotation, from −78° to −28° (p = 0.0001), whereas a significant difference was not reached in the graft group. When compared between groups, there appeared to be a trend favoring nerve transfer in shoulder external rotation, with the graft patients improving by 17° and the transfer patients improving by 49° (p = 0.07).

CONCLUSIONS

In NBPP, patients with shoulder weakness experience statistically significant improvements in shoulder flexion and abduction after graft repair or nerve transfer, and patients with nerve transfers additionally experience significant improvement in external rotation. With regard to shoulder external rotation, there appear to be some data supporting the use of nerve transfers.

ABBREVIATIONS

AROM = active ROM; NBPP = newborn brachial plexus palsy; ROM = range of motion; SAN = spinal accessory nerve; SSN = suprascapular nerve.

OBJECTIVE

The decision-making in neonatal brachial plexus palsy (NBPP) treatment continues to have many areas in need of clarification. Graft repair was the gold standard until the introduction of nerve transfer strategies. Currently, there is conflicting evidence regarding outcomes in patients with nerve grafts versus nerve transfers in relation to shoulder function. The objective of this study was to further define the outcomes for reconstruction strategies in NBPP with a specific focus on the shoulder.

METHODS

A cohort of patients with NBPP and surgical repairs from a single center were reviewed. Demographic and standard clinical data, including imaging and electrodiagnostics, were gathered from a clinical database. Clinical data from physical therapy evaluations, including active and passive range of motion, were examined. Statistical analysis was performed on the available data.

RESULTS

Forty-five patients met the inclusion criteria for this study, 19 with graft repair and 26 with nerve transfers. There were no significant differences in demographics between the two groups. Understandably, there were no patients in the nerve grafting group with preganglionic lesions, resulting in a difference in lesion type between the cohorts. There were no differences in preoperative shoulder function between the cohorts. Both groups reached statistically significant improvements in shoulder flexion and shoulder abduction. The nerve transfer group experienced a significant improvement in shoulder external rotation, from −78° to −28° (p = 0.0001), whereas a significant difference was not reached in the graft group. When compared between groups, there appeared to be a trend favoring nerve transfer in shoulder external rotation, with the graft patients improving by 17° and the transfer patients improving by 49° (p = 0.07).

CONCLUSIONS

In NBPP, patients with shoulder weakness experience statistically significant improvements in shoulder flexion and abduction after graft repair or nerve transfer, and patients with nerve transfers additionally experience significant improvement in external rotation. With regard to shoulder external rotation, there appear to be some data supporting the use of nerve transfers.

In Brief

Primary brachial plexus nerve reconstruction consists of nerve grafting and nerve transfer. There is continued debate among surgeons regarding which of these two options provides the most optimal outcomes. This study examined outcomes for shoulder function in patients with either nerve grafting or nerve transfer. In this study, there appears to be an advantage in external rotation of the shoulder in patients who underwent nerve transfer repair.

Neonatal brachial plexus palsy (NBPP) occurs in approximately 1.5 of 1000 live births.1 The primary mechanism of injury involves downward traction on the shoulder, leading to damage to the upper plexus during the perinatal period.2 The most commonly used classification scheme comprises four groups based on the extent (or number) of nerve roots involved and the presence of Horner’s syndrome, rather than the severity of injury at each of the nerve roots. The natural history of these injuries indicates that 20%–30% of infants will have persistent disabilities and would likely benefit from surgical intervention.3 Specifically, the published literature has reported that infants who have not started to recover biceps muscle strength at 3 months of age and/or have flail arm or Horner’s syndrome tend to have poor outcomes without nerve reconstruction and will likely benefit from surgical intervention, although the timing and choice of surgical intervention remain controversial.4,5

The traditional treatment for NBPP involves nerve graft reconstruction.5 However, recently, nerve transfer surgery has become increasingly more common in the pediatric population. This change in the surgical management has come from increasing frequency of nerve transfer in adult brachial plexus palsy.6 Specifically, a recent study has shown that the Oberlin transfer provides early recovery of forearm supination when compared with grafting with equivalent elbow flexion in infants with NBPP.7 Regardless, there continues to be significant debate regarding the efficacy and benefits of nerve transfer versus nerve grafting in NBPP.

Benefits of nerve transfer surgery include shorter distance of nerve regeneration, direct motor-to-motor nerve coaptation, and less extensive surgical dissection.8 One of the first studies comparing nerve grafting to triple nerve transfers was conducted by O’Grady et al.9 and showed better functional shoulder external rotation and forearm supination, faster recovery, and lower cost when compared with nerve grafting. Another study demonstrated superior outcomes with spinal accessory nerve (SAN) transfer rather than traditional cervical root grafting for supraclavicular nerve reconstruction in NBPP.10 On the other hand, a similar study looking at supraclavicular nerve reconstruction with C5 nerve root grafting versus SAN transfer showed no difference in outcomes.11 These studies serve to reinforce the absence of clear evidence regarding the ideal management strategy for NBPP.

Furthermore, shoulder function and stability is emerging as perhaps the more important outcome measure in NBPP as the development of the shoulder joint with respect to bone, tendon, and the enthesis involves the mechanical forces of the musculoskeletal system.12,13 Therefore, this retrospective cohort study seeks to provide 1-year postoperative outcomes in shoulder function in infants with NBPP who underwent nerve transfer or nerve grafting.

Methods

Study Design

This retrospective cohort study reviewed infants with NBPP who underwent nerve transfer (n = 26) or nerve grafting (n = 19) for restoration of shoulder function at a single institution from 2005 to 2015. Data were retrieved from an IRB-approved institutional data repository. We collected patient demographics and NBPP-related factors at the initial clinic visit. An interdisciplinary brachial plexus team, including neurosurgeons, physiatrists, and occupational therapists, evaluated and diagnosed infants with NBPP via physical examination, electrodiagnostic testing, and/or imaging evaluation. None of the patients had previous surgical intervention prior to the initial assessment.

Outcomes of Interest

One of two certified occupational therapists assessed active range of motion (AROM) preoperatively and 1 year postoperatively. The physical evaluation was standardized regardless of the surgical procedure. Primary outcomes of the current study included AROM of shoulder flexion, abduction, extension, external rotation (in adduction and abduction), and shoulder internal rotation (in adduction and abduction), as these movements were relevant to the targeted movement after nerve reconstruction.

Patient demographic data included age at operation, sex, race, NBPP-involved side (left vs right), Narakas grade (number of nerve roots injured), and injury type (preganglionic, postganglionic, or mixed). The Narakas grade was not applied uniformly at 2–3 weeks of age. Rather, the Narakas grade was determined by a single surgeon by either 1) physical examination and neurological assessment at approximately 1 week of age or at the initial clinical appointment, or 2) the mother’s or obstetrician’s report of the child’s arm and hand movements at birth. The Narakas grade was dichotomized into grades I or II and III or IV in the current study. Injury type was determined by intraoperative assessment of the nerve roots in all cases. Patient demographic data, AROM of shoulder flexion, abduction, extension, external rotation (in adduction and abduction), and shoulder internal rotation (in adduction and abduction) in the group undergoing nerve transfer and the group undergoing nerve grafting were obtained.

Surgical Decision-Making

Preoperative imaging and electrodiagnostics were used as extensions of clinical examination and as supportive indications for surgery. However, the surgical decision-making regarding the nerve reconstruction strategy was primarily based on findings during intraoperative exploration of the brachial plexus. Prior to the widespread application of nerve transfers, graft repair with a sural nerve harvest was utilized when possible. If the C5 and C6 nerve roots were available for grafting, then nerve grafting was performed for reconstruction; if only a single nerve root (C5 or C6) was available, it was directed to the anterior division of the upper trunk via grafting, and SAN-to–suprascapular nerve (SSN) transfer was performed. Data continue to demonstrate the advantages of nerve transfer which is now an option, even for patients with intact nerve roots proximal to the site of injury. The triple transfer (SAN to SSN, Oberlin, and radial nerve branch to axillary nerve) was performed for late presentations or preganglionic lesions.14,15 A single surgeon performed all nerve reconstructions using the standard techniques of microsuturing and tissue glue on nerve transfers, and glue only on sural nerve cable grafts.

Statistical Analysis

We applied descriptive statistics to patient demographic data and NBPP-related factors. AROM for each movement at the initial preoperative visit and the 1-year postoperative visit, and the mean preoperative to postoperative changes in AROM were summarized. The Student t-test for continuous variables, Mann-Whitney U-test for ordinal variables, and chi-square test or Fisher exact test for categorical variables were applied to investigate differences between nerve transfer and nerve grafting groups; p < 0.05 was considered statistically significant. Commercially available software was used for all analyses (SPSS version 22, IBM Corp.).

Results

Forty-five patients met inclusion criteria for this analysis, 19 in the graft repair group and 26 in the nerve transfer group. The two groups were similar with respect to demographics with the exception of lesion type (Table 1). Understandably, 0 (0%) patients in the graft repair group had preganglionic lesions, whereas 8 (31%) patients in the nerve transfer group did.

TABLE 1.

Patient demographics

Nerve Graft (n = 19)Nerve Transfer (n = 26)p Value
Mean age ± SD, mos
 At initial appointment3 ± 32 ± 20.22
 At operation7 ± 26 ± 20.46
Sex0.63
 Male6 (32)10 (38)
 Female13 (68)16 (62)
Race0.29
 Caucasian11 (58)19 (73)
 Other8 (42)7 (27)
NBPP-involved side0.26
 Lt12 (63)12 (46)
 Rt7 (37)14 (54)
Narakas grade0.39
 I or II5 (26)10 (38)
 III or IV14 (74)16 (62)
Lesion type0.002
 Preganglionic only0 (0)8 (31)
 Postganglionic only16 (84)9 (35)
 Mixed3 (16)9 (35)
Lesion site0.12
 C5–66 (32)2 (8)
 C5–75 (26)10 (38)
 C5–T18 (42)14 (54)

Values represent the number of patients (%) unless stated otherwise.

Preoperatively, there were no appreciable differences in shoulder flexion, extension, abduction, external rotation, or internal rotation between the two groups (Table 2). Postoperatively, both groups demonstrated significant improvements in shoulder flexion and shoulder abduction. The nerve graft group improved from 41° to 76° (p = 0.02) in shoulder flexion and from 26° to 61° (p = 0.008) in shoulder abduction. The nerve transfer group improved from 32° to 82° (p = 0.0001) in shoulder flexion and from 23° to 70° (p = 0.0001) in shoulder abduction. Additionally, the nerve transfer group experienced a significant improvement in shoulder external rotation, from −78° to −28° (p = 0.0001), whereas a significant difference was not found in the graft group (Table 3).

TABLE 2.

Comparison of preoperative and 1-year postoperative AROM outcomes of the shoulder between the groups

Preop AROM (°)Postop AROM (°)Pre- vs Postop AROM Improvement (°)
Nerve Graft (n = 19)Nerve Transfer (n = 26)p ValueNerve Graft (n = 17)Nerve Transfer (n = 26)p ValueNerve Graft (n = 17)Nerve Transfer (n = 26)p Value
Flexion41 ± 2732 ± 380.3776 ± 4082 ± 390.6134 ± 5451 ± 310.26
Abduction26 ± 3023 ± 290.7961 ± 4270 ± 400.5137 ± 5147 ± 420.52
Extension−4 ± 142 ± 100.122 ± 64 ± 90.646 ± 141 ± 140.33
External rotation
 Adduction−52 ± 55−78 ± 380.09−36 ± 51−28 ± 480.6117 ± 6449 ± 510.07
 Abduction−56 ± 53−64 ± 410.56−24 ± 60−10 ± 570.4634 ± 7554 ± 450.33
Internal rotation
 Adduction47 ± 4654 ± 460.6470 ± 065 ± 190.1621 ± 4711 ± 320.40
 Abduction41 ± 4854 ± 460.3954 ± 3965 ± 190.2916 ± 6211 ± 320.70

Values represent the mean ± SD unless stated otherwise.

TABLE 3.

Comparisons between preoperative and 1-year postoperative AROM outcomes of the shoulder in both groups

Nerve Graft AROM (°)Nerve Transfer AROM (°)
Preop (n = 19)Postop (n = 17)p ValuePreop (n = 26)Postop (n = 26)p Value
Flexion41 ± 2776 ± 400.0232 ± 3882 ± 39<0.0001
Abduction26 ± 3061 ± 420.00823 ± 2970 ± 40<0.0001
Extension−4 ± 142 ± 60.262 ± 104 ± 90.64
External rotation
 Adduction−52 ± 55−36 ± 510.30−78 ± 38−28 ± 480.0001
 Abduction−56 ± 53−24 ± 600.08−64 ± 41−10 ± 57<0.0001
Internal rotation
 Adduction47 ± 4670 ± 00.0854 ± 4665 ± 190.10
 Abduction41 ± 4854 ± 390.2954 ± 4665 ± 190.10

Values represent the mean ± SD unless stated otherwise.

The change in range of motion (ROM) when nerve grafting and nerve transfers were compared did not reach statistical significance. The postoperative improvement for shoulder flexion, abduction, and extension for the graft and transfer groups were 34° and 51° (p = 0.26), 37° and 47° (p = 0.52), and 6° and 1° (p = 0.33), respectively. For shoulder external rotation, there appeared to be a trend favoring nerve transfer, with the graft patients improving by 17° and the transfer patients improving by 49° (p = 0.07). Shoulder internal rotation improved by 21° in the graft patients and 11° in the transfer patients (p = 0.40).

The average age was 7 months at graft repair and 6 months at nerve transfer (p = 0.46). AROM outcomes were plotted against time of operation, and there did not appear to be a significant trend for improvement with regard to earlier or later intervention.

Discussion

The management strategies for reconstruction in NBPP continue to evolve with the addition of data to the literature. Despite this growing body of literature, many areas deserve clarification. The persistence of multiple treatment algorithms at the major brachial plexus centers across the world is evidence that further investigation is necessary.16–18 A continuing area of debate is that of nerve graft versus nerve transfer in the postganglionic brachial plexus lesion. Graft repair used to be the gold-standard repair technique for these injuries; however, the success and refinement of nerve transfer techniques over the past 20 years has pulled this paradigm into question.14,17,19–21 This project’s aim was to evaluate for early differences in shoulder outcomes between nerve graft and nerve repair in neonatal brachial plexus injury.

Dr. Alain Gilbert championed the importance of shoulder function in patients with brachial plexus palsies many years ago.19 Recognizing the shoulder as the base articulation for the upper limb, the importance is clear. Functioning shoulder musculature is paramount in the development of the normal ball and socket of the glenohumeral joint.12,22–24 Without repetitive motion and pressure from the head of the humerus, the cup of the glenoid never develops. This puts the patient at risk for subluxations, internal rotation, and eventual contractures.22,25–27 With upper trunk injuries, there is an imbalance of injury of the nerves to the external rotators of the shoulder, including the deltoid, teres minor, and infraspinatus muscles. The weakness in external rotators, along with the persistence of viability in the major internal rotators of the shoulder, including the pectoralis group, places the shoulder in a state of constant internal rotation, leading to disabling contractures. Aside from the anatomical development of the joint itself, the function of the shoulder in the repaired arm has been found to be important to the overall use of that limb. A recent study on patient-initiated arm use after plexus repair demonstrated that shoulder function, not elbow flexion, was the sole parameter related to both the frequency and magnitude of use in the affected limb.13 Without a functioning group of shoulder muscles, patients have difficulty positioning the arm and hand in the useful space in front of the body and face. Aside from direct testing and use, a recent survey of parents of children with brachial plexus injuries demonstrated that, in children with shoulder weakness, parents perceive their child’s disability as more severe and would put themselves at higher medical risk to avoid weakness in the shoulder (communication with K.W.C. Chang).

For the aforementioned reasons, it is important to continue to learn what is best for patients with shoulder weakness due to brachial plexus injuries. The algorithm used in our practice to pursue a plexus repair has been previously described.18 In summary, when shoulder function recovery is lagging and the expected outcomes from surgical repair outperform the natural history, surgical repair can be offered. Once the decision for surgical repair is made, the method of repair must then be decided. Preganglionic lesions are not amenable to graft repair due to the lack of viable motor axons in the nerve roots, so nerve transfers are the only choice for primary nerve surgery. With postganglionic injuries the question of graft repair versus nerve transfer is more complex. Currently, there are no clear guidelines addressing this question in patients for whom both options are available. The classic teaching was to do graft repair if possible. However, the outcomes for nerve transfers have continued to improve, making this decision more difficult. Although there are many arguments for each approach, the proponents of nerve grafting most often cite that it allows for the repair back to the patient’s native neuroanatomy, including sensory reinnervation. One of the drawbacks for nerve graft repair is that the axons must traverse a longer distance and two areas of coaptation prior to reaching the motor end plates and sensory targets. Nerve grafting also often requires the sacrifice of a donor nerve. The proponents of nerve transfer argue that the single area of coaptation is much closer to the target muscle, allowing for earlier reinnervation, and that specific muscles can be targeted with the available motor axons. The limitations of nerve transfer include the lack of sensory repair and the motor relearning necessary to maximize function.

Nerve graft repair outcomes have been widely reported; however, a lack of homogeneity among the outcome scales makes a consensus statement difficult. The neonatal group is notoriously difficult to evaluate. The main outcome of our study was AROM, as grading strength in this age group continues to be difficult. Lin et al.28 demonstrated that shoulder flexion, abduction, and external rotation all improved significantly after nerve grafting and consistently outperformed neurolysis in both function and frequency of musculoskeletal secondary surgeries. In a large study by Gilbert et al.,29 80% of patients demonstrated good to excellent shoulder outcomes for C5–6, and 61% of patients had good to excellent outcomes for C5–7; however, this series consisted both of patients with primary reconstruction and those who required secondary surgery. In adults, the nerve transfer data for SAN-to-SSN have shown that 77% of patients achieve a good result.30 The outcomes for shoulder function in adults appear to be improved with the combination of SAN-to-SSN transfer with a radial to axillary nerve transfer, and this is often the approach we utilize.31 The comparative literature on shoulder function following nerve graft compared with nerve transfer is sparse. O’Grady et al.9 demonstrated that at 2 years, nerve transfers outperformed nerve grafting with regard to external shoulder rotation. Seruya and colleagues10 also demonstrated that nerve transfer outperformed nerve grafting, with improved functional outcomes and decreased secondary surgery. Contrary to these two reports, Tse et al.11 demonstrated no appreciable difference between the two groups, with a notably large cohort of 177 patients. Our data demonstrate a trend toward better shoulder outcomes for nerve transfer compared with nerve grafting, especially in external shoulder rotation. Timing did not appear to affect outcomes in nerve transfers; however, nerve grafting appeared to be slightly improved when performed earlier. Given the length of growth required in a nerve graft and the race against time for useful reinnervation, this outcome is not surprising.32

The targeted innervation of the SSN by the SAN gives function to the supraspinatus and infraspinatus muscles, leading to abduction and external rotation. The radial nerve–to–axillary nerve transfer gives function to the teres major and deltoid muscles, which help to strengthen shoulder abduction. Two of the three papers cited above and the present data demonstrate a slight advantage of nerve transfers for shoulder deficits. One theory for this observation could be the decreased distance of regeneration needed in nerve transfers. Long-term outcomes will be necessary to see if this effect remains or if the grafting group catches up eventually. Another potential reason for the improved external rotation noted in nerve transfer is that, by selectively reinnervating the SSN and the axillary nerve, we focus the repair on the main external rotators of the arm. Spinal nerves C5 and C6 contribute to both the internal and external rotators of the shoulder; however, the injury pattern creates an imbalance in favor of internal rotation. Theoretically, nerve transfers could benefit from restoration of external rotation by avoiding reinnervation of the C5 and C6 internal rotators. The importance of external rotation includes clearing the hand from the body, decreasing contractures, aiding in self-hygiene, and moving the hand and limb into the functional space in front of the body.

The use of nerve transfers is increasing among peripheral nerve surgeons for many reasons, including promising outcomes, decreased operative time, increased reimbursement, and avoidance of the injured or scarred region.33–35 It is important to more rigorously examine the outcomes of these procedures and more clearly define the indications to help nerve surgeons continue to make better decisions for their patients. It is our practice to favor nerve transfers with later presentations to provide the patient’s degenerating motor endplate with the most rapid reinnervation.

The most obvious limitation of this study is the small number of patients included in this cohort. This is a common shortcoming in studies of rare procedures, and it limits the strength of the conclusions that can be drawn from the data. Another limitation is the retrospective analysis, leading to a decreased level of homogeneity in both patients and procedures. The epoch-based change could have introduced some bias, as the primary surgeon had more experience caring for NBPP injury prior to adopting the nerve transfer techniques. We report outcomes in terms of ROM, but no one has yet to identify what a clinically meaningful change in ROM would be. Finally, these data represent early outcomes for nerve transfers and grafts, which may bias toward nerve transfers, as this is a known advantage of the procedure. Further studies with longer follow-up and more patients are required to make stronger conclusions.

Conclusions

The data for shoulder outcomes in patients with NBPP following nerve grafting versus nerve transfer continue to be disputed. This paper demonstrates a slight advantage for shoulder outcomes, especially external rotation, with nerve transfers.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Yang, Smith, Chang. Acquisition of data: Yang, Chang. Analysis and interpretation of data: all authors. Drafting the article: Smith, Chang, Koduri. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Yang. Statistical analysis: Chang. Administrative/technical/material support: all authors. Study supervision: Yang.

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    Lee SK, Wolfe SW. Nerve transfers for the upper extremity: new horizons in nerve reconstruction. J Am Acad Orthop Surg. 2012;20(8):506517.

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    Kozin SH. Nerve transfers in brachial plexus birth palsies: indications, techniques, and outcomes. Hand Clin. 2008;24(4):363376, v.

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    Lee SK, Wolfe SW. Nerve transfers for the upper extremity: new horizons in nerve reconstruction. J Am Acad Orthop Surg. 2012;20(8):506517.

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    Ray WZ, Chang J, Hawasli A, et al. Motor nerve transfers: a comprehensive review. Neurosurgery. 2016;78(1):126.

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