Upper brachial plexus injury in adults: comparative effectiveness of different repair techniques

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OBJECT

Adult upper trunk brachial plexus injuries result in significant disability. Several surgical treatment strategies exist, including nerve grafting, nerve transfers, and a combination of both approaches. However, no existing data clearly indicate the most successful strategy for restoring elbow flexion and shoulder abduction in these patients. The authors reviewed the literature to compare outcomes of the three surgical repair techniques listed above to determine the optimal approach to traumatic injury to the upper brachial plexus in adults.

METHODS

Both PubMed and EMBASE databases were searched for English-language articles containing the MeSH topic “brachial plexus” in conjunction with the word “injury” or “trauma” in the title and “surgery” or “repair” as a MeSH subheading or in the title, excluding pediatric articles and those articles limited to avulsions. The search was also limited to articles published after 1990 and containing at least 10 operated cases involving upper brachial plexus injuries. The search was supplemented with articles obtained through the “Related Articles” feature on PubMed and the bibliographies of selected publications. From the articles was collected information on the operation performed, number of operated cases, mean subject ages, sex distribution, interval between injury and surgery, source of nerve transfers, mean duration of follow-up, year of publication, and percentage of operative success in terms of elbow flexion and shoulder abduction of the injured limb. The recovery of elbow flexion and shoulder abduction was separately analyzed. A subanalysis was also performed to assess the recovery of elbow flexion following various neurotization techniques.

RESULTS

As regards the restoration of elbow flexion, nerve grafting led to significantly better outcomes than either nerve transfer or the combined techniques (F = 4.71, p = 0.0097). However, separating the Oberlin procedure from other neurotization techniques revealed that the former was significantly more successful (F = 82.82, p < 0.001). Moreover, in comparing the Oberlin procedure to nerve grafting or combined procedures, again the former was significantly more successful than either of the latter two approaches (F = 53.14; p < 0.001). In the restoration of shoulder abduction, nerve transfer was significantly more successful than the combined procedure (p = 0.046), which in turn was significantly better than nerve grafting procedures (F = 5.53, p = 0.0044).

CONCLUSIONS

According to data in this study, in upper trunk brachial plexus injuries in adults, the Oberlin procedure and nerve transfers are the more successful approaches to restore elbow flexion and shoulder abduction, respectively, compared with nerve grafting or combined techniques. A prospective, randomized controlled trial would be necessary to fully elucidate differences in outcome among the various surgical approaches.

ABBREVIATIONMRC = Medical Research Council.

OBJECT

Adult upper trunk brachial plexus injuries result in significant disability. Several surgical treatment strategies exist, including nerve grafting, nerve transfers, and a combination of both approaches. However, no existing data clearly indicate the most successful strategy for restoring elbow flexion and shoulder abduction in these patients. The authors reviewed the literature to compare outcomes of the three surgical repair techniques listed above to determine the optimal approach to traumatic injury to the upper brachial plexus in adults.

METHODS

Both PubMed and EMBASE databases were searched for English-language articles containing the MeSH topic “brachial plexus” in conjunction with the word “injury” or “trauma” in the title and “surgery” or “repair” as a MeSH subheading or in the title, excluding pediatric articles and those articles limited to avulsions. The search was also limited to articles published after 1990 and containing at least 10 operated cases involving upper brachial plexus injuries. The search was supplemented with articles obtained through the “Related Articles” feature on PubMed and the bibliographies of selected publications. From the articles was collected information on the operation performed, number of operated cases, mean subject ages, sex distribution, interval between injury and surgery, source of nerve transfers, mean duration of follow-up, year of publication, and percentage of operative success in terms of elbow flexion and shoulder abduction of the injured limb. The recovery of elbow flexion and shoulder abduction was separately analyzed. A subanalysis was also performed to assess the recovery of elbow flexion following various neurotization techniques.

RESULTS

As regards the restoration of elbow flexion, nerve grafting led to significantly better outcomes than either nerve transfer or the combined techniques (F = 4.71, p = 0.0097). However, separating the Oberlin procedure from other neurotization techniques revealed that the former was significantly more successful (F = 82.82, p < 0.001). Moreover, in comparing the Oberlin procedure to nerve grafting or combined procedures, again the former was significantly more successful than either of the latter two approaches (F = 53.14; p < 0.001). In the restoration of shoulder abduction, nerve transfer was significantly more successful than the combined procedure (p = 0.046), which in turn was significantly better than nerve grafting procedures (F = 5.53, p = 0.0044).

CONCLUSIONS

According to data in this study, in upper trunk brachial plexus injuries in adults, the Oberlin procedure and nerve transfers are the more successful approaches to restore elbow flexion and shoulder abduction, respectively, compared with nerve grafting or combined techniques. A prospective, randomized controlled trial would be necessary to fully elucidate differences in outcome among the various surgical approaches.

ABBREVIATIONMRC = Medical Research Council.

Upper trunk brachial plexus injuries involving the C5–6 roots result in significant disability due to a loss of shoulder abduction, external rotation, elbow flexion, and forearm supination. Involvement of the C-7 spinal root may lead to deficits involving additional movements, including finger, wrist, and elbow extension. The severity of these injuries varies from a neurapraxic injury, which typically resolves spontaneously, to a complete avulsion injury, which has no potential for spontaneous recovery. In adults, the restoration of elbow flexion is the highest priority, followed by shoulder abduction and external rotation.3,68

Historically, repair strategies have consisted of brachial plexus exploration and reconstruction with nerve grafting. More recently, distal nerve transfers, which have traditionally been reserved for nerve root avulsion injuries, have been popularized for the treatment of postganglionic nerve injuries. This approach sacrifices a functional donor nerve fascicle in an attempt to reinnervate a recipient denervated target muscle. In fact, many surgeons now choose to forgo brachial plexus exploration and rely solely on distal nerve transfers.1,11,38,62 However, no prospective, randomized controlled trials have compared these surgical repair strategies. We reviewed the literature to evaluate the outcomes of three surgical approaches for the repair of postganglionic upper trunk brachial plexus injuries in adults, including nerve grafting, nerve transfer, and a combination of both techniques.

Methods

Literature Review

In January 2013, we searched the PubMed and EMBASE databases for articles containing the MeSH topic “brachial plexus” in conjunction with the word “injury” or “trauma” in the title and “surgery” or “repair” as a MeSH subheading or in the title, excluding pediatric articles and those articles limited to avulsions. We limited our search to English-language articles published after 1990 and articles containing at least 10 operated cases involving upper (or upper plus middle) brachial plexus injuries. The search was supplemented with articles obtained through the “Related Articles” feature of PubMed and the bibliographies of selected publications. All abstracts were reviewed, and those that were clearly unrelated to the purpose of our study were discarded. At least two authors reviewed each remaining article for relevance and data. If an article reported more than one surgical approach, we attempted to separate outcomes in each group. If this was not possible, the article was eliminated from further review unless at least 60% of the cases utilized a single approach. From the articles, we abstracted information on the operation performed, number of operated cases, mean subject ages, sex distribution, interval between injury and surgery, source of nerve transfers, mean duration of follow-up, year of publication, and percentage of operative success in terms of elbow flexion and shoulder abduction of the injured limb. We also recorded the mean length of nerve grafts when available. We defined success as a British Medical Research Council (MRC) score of at least 3.42

Analysis

We compared three operations, including nerve repair (grafting), nerve transfer, and combinations of both techniques, to determine the optimal approach in an adult presenting with traumatic injury to the upper brachial plexus. The recoveries of both shoulder abduction and elbow flexion were assessed separately. We also performed a subanalysis in which we compared recovery of elbow flexion after each of the three nerve transfer techniques: partial ulnar nerve transfer (Oberlin procedure), intercostal transfer, and other procedures. Variables were abstracted from individual publications, tested to exclude heterogeneity,33 and pooled. We pooled data on success rates and demographics meta-analytically by using an inverse variance-weighted random-effects model.17 Rates of different approaches were compared using 1-way ANOVA, with Bonferroni correction for ad hoc comparisons. The effects of patient age, injury-to-surgery period, and other covariates (predictive factors) were evaluated using meta-regression. Meta-analytical pooling, meta-regressions, and statistical comparisons of outcomes involved the use of Stata version 12 (StataCorp LP). A p value < 0.05 was considered significant.

Results

Literature Review

Our search yielded 2330 publications, many of which lacked utilizable data (Fig. 1). We used 71 case series in our analysis, including 5 series reporting more than one surgical approach (Table 1).2,4–10,12–16,18–20,22–27,29–32,35–37,39–41,43,44,46,48–61,63–67,69–82 However, none was a controlled trial, and all must be considered Class IV evidence. Fifteen series (747 cases) reported the results of nerve grafting. In the nerve transfer group, there were 54 reports with a total of 2440 cases. For combined procedures, the totals were 8 and 587, respectively. A breakdown of the nerve transfer group yielded 300 cases with partial ulnar transfer, 1052 with intercostal transfer, and 1088 undergoing other transfer procedures.

FIG. 1.
FIG. 1.

Summary of the structured literature review performed, showing numbers of abstracts reviewed, articles read and/or used in our analysis, and reasons for rejections.

TABLE 1

Case series used in an analysis of surgical procedures for upper brachial plexus injuries in adults

Authors & YearNo. of Operated CasesOperation
Allieu et al., 199743Graft
17Transfer
Berger & Becker, 199458Transfer
Bertelli & Ghizoni, 2004710Transfer
Bertelli & Ghizoni, 2004512Combined
Bertelli & Ghizoni, 2010637Combined
Bertelli & Ghizoni, 2010822Combined
Bhandari et al., 200920Transfer
Bhandari & Deb, 201140Transfer
Chuang et al., 199266Transfer
Chuang et al., 199511Transfer
Coulet et al., 201040Transfer
Doi et al., 200322Transfer
Dubuisson & Kline, 200259Combined
El-Gammal & Fathi, 200229Transfer
Ferraresi et al., 200443Transfer
Friedman et al., 199014Transfer
Goubier & Teboul, 200710Transfer
Gu et al., 1990164Transfer
Haninec et al., 200795Graft
Haninec & Kaiser, 201214Transfer
Hou & Xu, 200223Transfer
Htut et al., 200726Transfer
Jivan et al., 200927Graft
Kakinoki et al., 201016Transfer
Kandenwein et al., 2005119Graft
Kim et al., 2003175Graft
Kline, 198938Transfer
Leechavengvongs et al., 199832Transfer
Leechavengvongs et al., 200615Transfer
Liverneaux et al., 200615Transfer
Malessy & Thomeer, 199825Transfer
Malessy et al., 199912Graft
Malessy et al., 200424Graft
29Transfer
Merrell et al., 200115Transfer
Moiyadi et al., 200751Transfer
Nagano et al., 1989149Transfer
Nagano et al., 199279Transfer
16Graft
Nagano et al., 1995112Transfer
Nath et al., 200640Transfer
Ochiai et al., 199321Transfer
Ogino & Naito, 199520Transfer
Okinaga & Nagano, 199911Transfer
Ray et al., 201129Transfer
Ricardo, 200513Graft
Richardson, 199710Transfer
Ruch et al., 199517Transfer
Samadian et al., 200917Graft
Samardzic et al., 199222Transfer
Samardzi et al., 200225Transfer
91Combined
Samii et al., 199754Graft
Samii et al., 200344Combined
Siqueira & Martin, 200910Transfer
Socolovsky et al., 201134Graft
Socolovsky et al., 201218Transfer
17Graft
Songcharoen, 1995222Transfer
23Graft
Songcharoen et al., 1996216Transfer
Sulaiman et al., 2009131Transfer
Sungpet et al., 20007010Transfer
Sungpet et al., 20007136Transfer
Suzuki et al., 200712Transfer
Teboul et al., 200434Transfer
Terzis et al., 1999204Combined
Terzis & Kostas, 2006118Combined
Tonkin et al., 199617Transfer
Vekris et al., 201078Graft
Venkatramani et al., 200815Transfer
Waikakul et al., 19997996Transfer
Waikakul et al., 199980205Transfer
Xu et al., 200215Transfer
Xu et al., 200515Transfer
Zyaei & Saied, 201010Transfer

Demographics, Surgical Timing, and Follow-Up

Findings on patient demographics, surgical timing, and follow-up are summarized according to treatment group in Table 2. There were no significant differences among the three groups with regard to patient age, sex ratio, or time between injury and surgical repair. Similarly, no significant pairwise differences existed. The duration of follow-up was significantly shorter in the nerve transfer group than in the graft or combined groups (p < 0.001 in each case).

TABLE 2

Summary of demographic and procedural factors for surgical groups treated for upper brachial plexus injuries

FactorGraft Mean ± SDTransfer Mean ± SDCombined Mean ± SDFp Value
Age (yrs)25.900 ± 3.25626.418 ± 3.35725.744 ± 0.6960.2050.815
Proportion of males0.917 ± 0.0310.913 ± 0.0630.855 ± 0.0472.6820.079
Injury-to-surgery period (mos)5.405 ± 2.7135.078 ± 1.3326.062 ± 1.1870.9540.391
Length of follow-up (mos)44.082 ± 10.80129.928 ± 10.97335.725 ± 23.4416.3770.003

Comparative Effectiveness

Restoration of Elbow Flexion

As shown in Table 3, nerve grafting resulted in significantly better outcomes than either nerve transfer or combined procedures (F = 4.71, p = 0.0097); pairwise comparisons demonstrated p values of 0.034 and 0.018, respectively. Our experience with favorable outcomes following the Oberlin procedure, as opposed to non-Oberlin nerve transfers, prompted a secondary analysis. Separating partial ulnar nerve transfer from the other neurotization procedures revealed that the former was significantly more successful (F = 82.82, p < 0.001; Table 3), although the two did not differ from each other (p = 0.289). Furthermore, when the Oberlin procedure was compared with nerve grafting or combined procedures, it was significantly more successful than either (F = 53.14; p < 0.001).

TABLE 3

Relative success of surgical procedures for upper brachial plexus injuries in adults

ProcedureMean ± SDFp Value
Restoringelbow4.710.0097
 Graft0.692 ± 0.241
 Transfer0.661 ± 0.153
 Combined0.630 ± 0.268
Restoringelbow82.82<0.001
 Oberlin0.825 ± 0.122
 Intercostal0.658 ± 0.167
 Other nerve transfer0.678 ± 0.095
Restoring shoulder abduction5.530.0044
 Graft0.560 ± 0.260
 Transfer0.654 ± 0.165
 Combined0.633 ± 0.265

Restoration of Shoulder Abduction

Nerve transfer was significantly more successful than the combined procedure (p = 0.046), which in turn was significantly better than nerve grafting procedures (F = 5.53, p = 0.0044; Table 3).

Predictive Factors

The mean patient age, sex distribution, delay to repair, length of follow-up, or year of publication had no significant correlation with outcome, as analyzed by meta-regression. This was true for analyses for both elbow flexion and shoulder abduction. In the nerve grafting group, graft length did not correlate with success rates of either elbow or shoulder surgery.

Discussion

Consensus on the most successful surgical treatment strategy for upper trunk brachial plexus injuries in adults is lacking, and in the absence of a randomized controlled trial to guide clinical decision making, we reviewed the literature to evaluate outcomes of three surgical approaches for the repair of postganglionic upper trunk brachial plexus injuries in adults, including nerve grafting, nerve transfer, and a combination of both techniques. Our results indicated that the Oberlin procedure and nerve transfers were more successful approaches to the restoration of elbow flexion and shoulder abduction, respectively, than nerve grafting or combined techniques.

Our approach to pooling data from multiple published reports is similar to that used by Garg et al.21 as well as Yang and associates,83 although the model itself is somewhat different. Unlike those authors, we extended our analysis to include different nerve transfers and were able to show that partial ulnar transfer seemed to result in greater success in elbow flexion recovery than did graft repair. Yang et al. did not identify a reconstruction strategy that was superior for the recovery of shoulder abduction, whereas our data, like those of Garg et al., suggested that nerve transfer is superior to nerve grafting in the case of shoulder abduction recovery as well.

In upper trunk brachial plexus injuries in adults, according to our data, the Oberlin procedure and nerve transfers are more successful approaches to the restoration of elbow flexion and shoulder abduction, respectively, compared with nerve grafting or combined techniques. While the debate over nerve grafting versus nerve transfer has been ongoing among peripheral nerve surgeons over the last few decades, it is still unclear how one approach produces better outcomes than another. We hypothesize that the superiority of nerve transfers in promoting nerve regeneration is probably the result of a combination of factors, including a shorter distance required for nerve regeneration, single suture junction, use of a vascularized albeit injured nerve transfer recipient, and reduced fibrosis at the operative site as compared with that at the injury site. In the absence of a prospective, randomized clinical trial, resolving the debate over nerve transfer versus nerve graft is unlikely. However, data in the present study arm the clinician with valuable information that can be used to counsel patients when considering various surgical approaches.

A comparative effectiveness study is not the equivalent of a well-run and well-powered randomized controlled trial. At best, it can approximate the results of such a trial. As in any mathematical model, the many simplifications and assumptions may have influenced our conclusions, and the differences among groups are relatively small. However, this suggests that the rather large sample size needed would make a clinical trial impractical, especially in light of the impact of injury type on the repair technique and the lack of clinical equipoise among peripheral nerve experts. Our use of a dichotomous outcome, such as MRC scores above and below 3, has been reported to reduce the statistical power of clinical trials,45 although this is not always the case.28

This study has several additional limitations. Very few published case series reported outcomes stratified by injury mechanisms, and the indications for surgery were not uniform, thereby limiting our analysis. Thus, it is possible that the reported groups are not strictly comparable. Specifically, for the group undergoing combined procedures, it was not clear, based on the available literature, if both nerve grafts and transfers were performed to restore a common function. In addition, the reviewed literature lacked sufficient detail to determine which combinations of nerve grafts and transfers were most successful in restoring motor function. Moreover, in assessing outcomes for shoulder abduction, no distinction was made between specific targets for nerve reinnervation (that is, axillary versus suprascapular nerve), nor were adequate data available to separate success in restoring axillary versus suprascapular nerve function. In at least some cases, the findings at the time of exploration dictated surgical approach. If so, our comparison introduced a degree of selection bias, which might be avoided in a randomized controlled trial. We could not limit our analysis to cases in which there was clinical equipoise in surgical treatment, as very few publications separated outcomes of nerve transfers in patients with nerve root avulsions from those in patients with other brachial plexus lesions. In addition, variations in the intensity and duration of physical therapy can confound pooled results. Many secondary procedures, including osteotomies and tendon transfers, are available for these patients. Although they are widely used and affect function, we excluded them from this analysis since the goal of this study was to isolate the success of primary surgical approaches to brachial plexus injury.

The adult brachial plexus injury population is heterogeneous, and the clinician is responsible for considering several factors on an individual basis in developing an appropriate management plan for each patient. While our study provides a decision framework for the clinician to consider surgical treatment strategies, it should not serve as a substitute for the individualized clinical decision making required to manage these patients effectively. Furthermore, when considering brachial plexus reconstruction strategies, nerve transfers, without operative exploration of the supraclavicular brachial plexus, may limit the surgeon's appreciation of the unique pathology in each case.

Conclusions

In upper trunk brachial plexus injuries in adults, the Oberlin procedure and nerve transfers are more successful approaches to the restoration of elbow flexion and shoulder abduction, respectively, as compared with nerve grafting or combined techniques. A prospective, randomized controlled trial would be necessary to fully elucidate differences in outcomes among the various surgical approaches.

Author ContributionsConception and design: Ali, Heuer, Stein, Zager. Acquisition of data: Faught, Kaneriya, Sheikh, Syed. Analysis and interpretation of data: Ali, Heuer, Stein, Zager. Drafting the article: Ali, Stein. 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: Ali. Statistical analysis: Stein. Study supervision: Stein, Zager.

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  • 44

    Moiyadi AVDevi BINair KP: Brachial plexus injuries: outcome following neurotization with intercostal nerve. J Neurosurg 107:3083132007

    • Search Google Scholar
    • Export Citation
  • 45

    Murray GDBarer DChoi SFernandes HGregson BLees KR: Design and analysis of phase III trials with ordered outcome scales: the concept of the sliding dichotomy. J Neurotrauma 22:5115172005

    • Search Google Scholar
    • Export Citation
  • 46

    Nagano AOchiai NOkinaga S: Restoration of elbow flexion in root lesions of brachial plexus injuries. J Hand Surg Am 17:8158211992

    • Search Google Scholar
    • Export Citation
  • 47

    Nagano ATsuyama NOchiai NHara TTakahashi M: Direct nerve crossing with the intercostal nerve to treat avulsion injuries of the brachial plexus. J Hand Surg Am 14:9809851989

    • Search Google Scholar
    • Export Citation
  • 48

    Nagano AYamamoto SMikami Y: Intercostal nerve transfer to restore upper extremity functions after brachial plexus injury. Ann Acad Med Singapore 24:4 Suppl42451995

    • Search Google Scholar
    • Export Citation
  • 49

    Nath RKLyons ABBietz G: Physiological and clinical advantages of median nerve fascicle transfer to the musculocutaneous nerve following brachial plexus root avulsion injury. J Neurosurg 105:8308342006

    • Search Google Scholar
    • Export Citation
  • 50

    Ochiai NMikami YYamamoto SNakagawa TNagano A: A new technique for mismatched nerve suture in direct intercostal nerve transfers. J Hand Surg Br 18:3183191993

    • Search Google Scholar
    • Export Citation
  • 51

    Ogino TNaito T: Intercostal nerve crossing to restore elbow flexion and sensibility of the hand for a root avulsion type of brachial plexus injury. Microsurgery 16:5715771995

    • Search Google Scholar
    • Export Citation
  • 52

    Okinaga SNagano A: Can vascularization improve the surgical outcome of the intercostal nerve transfer for traumatic brachial plexus palsy? A clinical comparison of vascularized and non-vascularized methods. Microsurgery 19:1761801999

    • Search Google Scholar
    • Export Citation
  • 53

    Ray WZPet MAYee AMackinnon SE: Double fascicular nerve transfer to the biceps and brachialis muscles after brachial plexus injury: clinical outcomes in a series of 29 cases. Clinical article. J Neurosurg 114:152015282011

    • Search Google Scholar
    • Export Citation
  • 54

    Ricardo M: Surgical treatment of brachial plexus injuries in adults. Int Orthop 29:3513542005

  • 55

    Richardson PM: Recovery of biceps function after delayed repair for brachial plexus injury. J Trauma 42:7917921997

  • 56

    Ruch DSFriedman ANunley JA: The restoration of elbow flexion with intercostal nerve transfers. Clin Orthop Relat Res 314951031995

    • Search Google Scholar
    • Export Citation
  • 57

    Samadian MRezaee OHaddadian KSharifi GAbtahi HHamidian M: Gunshot injuries to the brachial plexus during wartime. Br J Neurosurg 23:1651692009

    • Search Google Scholar
    • Export Citation
  • 58

    Samardzic MGrujicic DAntunovic V: Nerve transfer in brachial plexus traction injuries. J Neurosurg 76:1911971992

  • 59

    Samardzić MGrujicić DRasulić LMilicić B: Restoration of upper arm function in traction injuries to the brachial plexus. Acta Neurochir (Wien) 144:3273352002

    • Search Google Scholar
    • Export Citation
  • 60

    Samii ACarvalho GASamii M: Brachial plexus injury: factors affecting functional outcome in spinal accessory nerve transfer for the restoration of elbow flexion. J Neurosurg 98:3073122003

    • Search Google Scholar
    • Export Citation
  • 61

    Samii MCarvalho GANikkhah GPenkert G: Surgical reconstruction of the musculocutaneous nerve in traumatic brachial plexus injuries. J Neurosurg 87:8818861997

    • Search Google Scholar
    • Export Citation
  • 62

    Shin AYSpinner RJSteinmann SPBishop AT: Adult traumatic brachial plexus injuries. J Am Acad Orthop Surg 13:3823962005

  • 63

    Siqueira MGMartins RS: Phrenic nerve transfer in the restoration of elbow flexion in brachial plexus avulsion injuries: how effective and safe is it?. Neurosurgery 65:4 SupplA125A1312009

    • Search Google Scholar
    • Export Citation
  • 64

    Socolovsky MDi Masi GBattaglia D: Use of long autologous nerve grafts in brachial plexus reconstruction: factors that affect the outcome. Acta Neurochir (Wien) 153:223122402011

    • Search Google Scholar
    • Export Citation
  • 65

    Socolovsky MMartins RSDi Masi GSiqueira M: Upper brachial plexus injuries: grafts vs ulnar fascicle transfer to restore biceps muscle function. Neurosurgery 71:2 Suppl Operativeons227ons2322012

    • Search Google Scholar
    • Export Citation
  • 66

    Songcharoen P: Brachial plexus injury in Thailand: a report of 520 cases. Microsurgery 16:35391995

  • 67

    Songcharoen PMahaisavariya BChotigavanich C: Spinal accessory neurotization for restoration of elbow flexion in avulsion injuries of the brachial plexus. J Hand Surg Am 21:3873901996

    • Search Google Scholar
    • Export Citation
  • 68

    Songcharoen PWongtrakul SSpinner RJ: Brachial plexus injuries in the adult. Nerve transfers: the Siriraj Hospital experience. Hand Clin 21:83892005

    • Search Google Scholar
    • Export Citation
  • 69

    Sulaiman OAKim DDBurkett CKline DG: Nerve transfer surgery for adult brachial plexus injury: a 10-year experience at Louisiana State University. Neurosurgery 65:4 SupplA55A622009

    • Search Google Scholar
    • Export Citation
  • 70

    Sungpet ASuphachatwong CKawinwonggowith V: Restoration of shoulder abduction in brachial plexus injury with phrenic nerve transfer. Aust N Z J Surg 70:7837852000

    • Search Google Scholar
    • Export Citation
  • 71

    Sungpet ASuphachatwong CKawinwonggowit VPatradul A: Transfer of a single fascicle from the ulnar nerve to the biceps muscle after avulsions of upper roots of the brachial plexus. J Hand Surg Br 25:3253282000

    • Search Google Scholar
    • Export Citation
  • 72

    Suzuki KDoi KHattori YPagsaligan JM: Long-term results of spinal accessory nerve transfer to the suprascapular nerve in upper-type paralysis of brachial plexus injury. J Reconstr Microsurg 23:2952992007

    • Search Google Scholar
    • Export Citation
  • 73

    Teboul FKakkar RAmeur NBeaulieu JYOberlin C: Transfer of fascicles from the ulnar nerve to the nerve to the biceps in the treatment of upper brachial plexus palsy. J Bone Joint Surg Am 86-A:148514902004

    • Search Google Scholar
    • Export Citation
  • 74

    Terzis JKKostas I: Suprascapular nerve reconstruction in 118 cases of adult posttraumatic brachial plexus. Plast Reconstr Surg 117:6136292006

    • Search Google Scholar
    • Export Citation
  • 75

    Terzis JKVekris MDSoucacos PN: Outcomes of brachial plexus reconstruction in 204 patients with devastating paralysis. Plast Reconstr Surg 104:122112401999

    • Search Google Scholar
    • Export Citation
  • 76

    Tonkin MAEckersley JRGschwind CR: The surgical treatment of brachial plexus injuries. Aust N Z J Surg 66:29331996

  • 77

    Vekris MDBeris AEPafilas DLykissas MGXenakis TASoucacos PN: Shoulder reanimation in posttraumatic brachial plexus paralysis. Injury 41:3123182010

    • Search Google Scholar
    • Export Citation
  • 78

    Venkatramani HBhardwaj PFaruquee SRSabapathy SR: Functional outcome of nerve transfer for restoration of shoulder and elbow function in upper brachial plexus injury. J Brachial Plex Peripher Nerve Inj 3:152008

    • Search Google Scholar
    • Export Citation
  • 79

    Waikakul SOrapin SVanadurongwan V: Clinical results of contralateral C7 root neurotization to the median nerve in brachial plexus injuries with total root avulsions. J Hand Surg Br 24:5565601999

    • Search Google Scholar
    • Export Citation
  • 80

    Waikakul SWongtragul SVanadurongwan V: Restoration of elbow flexion in brachial plexus avulsion injury: comparing spinal accessory nerve transfer with intercostal nerve transfer. J Hand Surg Am 24:5715771999

    • Search Google Scholar
    • Export Citation
  • 81

    Xu WDGu YDXu JGTan LJ: Full-length phrenic nerve transfer by means of video-assisted thoracic surgery in treating brachial plexus avulsion injury. Plast Reconstr Surg 110:1041112002

    • Search Google Scholar
    • Export Citation
  • 82

    Xu WDXu JGGu YD: Comparative clinic study on vascularized and nonvascularized full-length phrenic nerve transfer. Microsurgery 25:16202005

    • Search Google Scholar
    • Export Citation
  • 83

    Yang LJChang KWChung KC: A systematic review of nerve transfer and nerve repair for the treatment of adult upper brachial plexus injury. Neurosurgery 71:4174292012

    • Search Google Scholar
    • Export Citation
  • 84

    Zyaei ASaied A: Functional outcome of ulnar nerve fascicle transfer for restoration of elbow flexion in upper brachial plexus injury. Eur J Orthop Surg Traumatol 20:2932972010

    • Search Google Scholar
    • Export Citation

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Article Information

Contributor Notes

Correspondence Zarina S. Ali, Department of Neurosurgery, University of Pennsylvania, 3400 Spruce St., 3rd Fl. Silverstein Pavilion, Philadelphia, PA 19104. email: zarinasali@gmail.com.INCLUDE WHEN CITING Published online October 31, 2014; DOI: 10.3171/2014.9.JNS132823.DISCLOSURE The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
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    Summary of the structured literature review performed, showing numbers of abstracts reviewed, articles read and/or used in our analysis, and reasons for rejections.

References
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  • 13

    Chuang DCYeh MCWei FC: Intercostal nerve transfer of the musculocutaneous nerve in avulsed brachial plexus injuries: evaluation of 66 patients. J Hand Surg Am 17:8228281992

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    Coulet BBoretto JGLazerges CChammas M: A comparison of intercostal and partial ulnar nerve transfers in restoring elbow flexion following upper brachial plexus injury (C5–C6±C7). J Hand Surg Am 35:129713032010

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    Dubuisson ASKline DG: Brachial plexus injury: a survey of 100 consecutive cases from a single service. Neurosurgery 51:6736832002

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    El-Gammal TAFathi NA: Outcomes of surgical treatment of brachial plexus injuries using nerve grafting and nerve transfers. J Reconstr Microsurg 18:7152002

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  • 19

    Ferraresi SGarozzo DBuffatti P: Reinnervation of the biceps in C5-7 brachial plexus avulsion injuries: results after distal bypass surgery. Neurosurg Focus 16:5E62004

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  • 20

    Friedman AHNunley JA IIGoldner RDOakes WJGoldner JLUrbaniak JR: Nerve transposition for the restoration of elbow flexion following brachial plexus avulsion injuries. J Neurosurg 72:59641990

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  • 21

    Garg RMerrell GAHillstrom HJWolfe SW: Comparison of nerve transfers and nerve grafting for traumatic upper plexus palsy: a systematic review and analysis. J Bone Joint Surg Am 93:8198292011

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  • 22

    Goubier JNTeboul F: Technique of the double nerve transfer to recover elbow flexion in C5, C6, or C5 to C7 brachial plexus palsy. Tech Hand Up Extrem Surg 11:15172007

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  • 23

    Gu YDWu MMZhen YLZhao JAZhang GMChen DS: Phrenic nerve transfer for treatment of root avulsion of the brachial plexus. Chin Med J (Engl) 103:2672701990

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  • 24

    Haninec PKaiser R: Axillary nerve repair by fascicle transfer from the ulnar or median nerve in upper brachial plexus palsy. Clinical article. J Neurosurg 117:6106142012

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  • 25

    Haninec PSámal FTomás RHoustava LDubovwý P: Direct repair (nerve grafting), neurotization, and end-to-side neurorrhaphy in the treatment of brachial plexus injury. J Neurosurg 106:3913992007

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  • 26

    Hou ZXu Z: Nerve transfer for treatment of brachial plexus injury: comparison study between the transfer of partial median and ulnar nerves and that of phrenic and spinal accessary nerves. Chin J Traumatol 5:2632662002

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  • 27

    Htut MMisra VPAnand PBirch RCarlstedt T: Motor recovery and the breathing arm after brachial plexus surgical repairs, including re-implantation of avulsed spinal roots into the spinal cord. J Hand Surg Eur 32:1701782007

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  • 28

    Ilodigwe DMurray GDKassell NFTorner JKerr RSMolyneux AJ: Sliding dichotomy compared with fixed dichotomization of ordinal outcome scales in subarachnoid hemorrhage trials. Clinical article. J Neurosurg 118:3122013

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  • 29

    Jivan SKumar NWiberg MKay S: The influence of presurgical delay on functional outcome after reconstruction of brachial plexus injuries. J Plast Reconstr Aesthet Surg 62:4724792009

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  • 30

    Kakinoki RIkeguchi RDunkan SFNakayama KMatsumoto TOhta S: Comparison between partial ulnar and intercostal nerve transfers for reconstructing elbow flexion in patients with upper brachial plexus injuries. J Brachial Plex Peripher Nerve Inj 5:42010

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  • 31

    Kandenwein JAKretschmer TEngelhardt MRichter HPAntoniadis G: Surgical interventions for traumatic lesions of the brachial plexus: a retrospective study of 134 cases. J Neurosurg 103:6146212005

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  • 32

    Kim DHCho YJTiel RLKline DG: Outcomes of surgery in 1019 brachial plexus lesions treated at Louisiana State University Health Sciences Center. J Neurosurg 98:100510162003

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  • 34

    Kline DG: Civilian gunshot wounds to the brachial plexus. J Neurosurg 70:1661741989

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    Leechavengvongs SWitoonchart KUerpairojkit CThuvasethakul PKetmalasiri 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 23:7117161998

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  • 36

    Leechavengvongs SWitoonchart KUerpairojkit CThuvasethakul PMalungpaishrope K: Combined nerve transfers for C5 and C6 brachial plexus avulsion injury. J Hand Surg Am 31:1831892006

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    • Export Citation
  • 37

    Liverneaux PADiaz LCBeaulieu JYDurand SOberlin C: Preliminary results of double nerve transfer to restore elbow flexion in upper type brachial plexus palsies. Plast Reconstr Surg 117:9159192006

    • Search Google Scholar
    • Export Citation
  • 38

    Mackinnon SEColbert SH: Nerve transfers in the hand and upper extremity surgery. Tech Hand Up Extrem Surg 12:20332008

  • 39

    Malessy MJde Ruiter GCde Boer KSThomeer RT: Evaluation of suprascapular nerve neurotization after nerve graft or transfer in the treatment of brachial plexus traction lesions. J Neurosurg 101:3773892004

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    • Export Citation
  • 40

    Malessy MJHoffmann CFThomeer RT: Initial report on the limited value of hypoglossal nerve transfer to treat brachial plexus root avulsions. J Neurosurg 91:6016041999

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  • 41

    Malessy MJThomeer RT: Evaluation of intercostal to musculocutaneous nerve transfer in reconstructive brachial plexus surgery. J Neurosurg 88:2662711998

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  • 42

    Medical Research Council: Aids to the Examination of the Peripheral Nervous System. Memorandum No. 45 LondonHer Majesty's Stationary Office1976

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  • 43

    Merrell GABarrie KAKatz DLWolfe SW: Results of nerve transfer techniques for restoration of shoulder and elbow function in the context of a meta-analysis of the English literature. J Hand Surg Am 26:3033142001

    • Search Google Scholar
    • Export Citation
  • 44

    Moiyadi AVDevi BINair KP: Brachial plexus injuries: outcome following neurotization with intercostal nerve. J Neurosurg 107:3083132007

    • Search Google Scholar
    • Export Citation
  • 45

    Murray GDBarer DChoi SFernandes HGregson BLees KR: Design and analysis of phase III trials with ordered outcome scales: the concept of the sliding dichotomy. J Neurotrauma 22:5115172005

    • Search Google Scholar
    • Export Citation
  • 46

    Nagano AOchiai NOkinaga S: Restoration of elbow flexion in root lesions of brachial plexus injuries. J Hand Surg Am 17:8158211992

    • Search Google Scholar
    • Export Citation
  • 47

    Nagano ATsuyama NOchiai NHara TTakahashi M: Direct nerve crossing with the intercostal nerve to treat avulsion injuries of the brachial plexus. J Hand Surg Am 14:9809851989

    • Search Google Scholar
    • Export Citation
  • 48

    Nagano AYamamoto SMikami Y: Intercostal nerve transfer to restore upper extremity functions after brachial plexus injury. Ann Acad Med Singapore 24:4 Suppl42451995

    • Search Google Scholar
    • Export Citation
  • 49

    Nath RKLyons ABBietz G: Physiological and clinical advantages of median nerve fascicle transfer to the musculocutaneous nerve following brachial plexus root avulsion injury. J Neurosurg 105:8308342006

    • Search Google Scholar
    • Export Citation
  • 50

    Ochiai NMikami YYamamoto SNakagawa TNagano A: A new technique for mismatched nerve suture in direct intercostal nerve transfers. J Hand Surg Br 18:3183191993

    • Search Google Scholar
    • Export Citation
  • 51

    Ogino TNaito T: Intercostal nerve crossing to restore elbow flexion and sensibility of the hand for a root avulsion type of brachial plexus injury. Microsurgery 16:5715771995

    • Search Google Scholar
    • Export Citation
  • 52

    Okinaga SNagano A: Can vascularization improve the surgical outcome of the intercostal nerve transfer for traumatic brachial plexus palsy? A clinical comparison of vascularized and non-vascularized methods. Microsurgery 19:1761801999

    • Search Google Scholar
    • Export Citation
  • 53

    Ray WZPet MAYee AMackinnon SE: Double fascicular nerve transfer to the biceps and brachialis muscles after brachial plexus injury: clinical outcomes in a series of 29 cases. Clinical article. J Neurosurg 114:152015282011

    • Search Google Scholar
    • Export Citation
  • 54

    Ricardo M: Surgical treatment of brachial plexus injuries in adults. Int Orthop 29:3513542005

  • 55

    Richardson PM: Recovery of biceps function after delayed repair for brachial plexus injury. J Trauma 42:7917921997

  • 56

    Ruch DSFriedman ANunley JA: The restoration of elbow flexion with intercostal nerve transfers. Clin Orthop Relat Res 314951031995

    • Search Google Scholar
    • Export Citation
  • 57

    Samadian MRezaee OHaddadian KSharifi GAbtahi HHamidian M: Gunshot injuries to the brachial plexus during wartime. Br J Neurosurg 23:1651692009

    • Search Google Scholar
    • Export Citation
  • 58

    Samardzic MGrujicic DAntunovic V: Nerve transfer in brachial plexus traction injuries. J Neurosurg 76:1911971992

  • 59

    Samardzić MGrujicić DRasulić LMilicić B: Restoration of upper arm function in traction injuries to the brachial plexus. Acta Neurochir (Wien) 144:3273352002

    • Search Google Scholar
    • Export Citation
  • 60

    Samii ACarvalho GASamii M: Brachial plexus injury: factors affecting functional outcome in spinal accessory nerve transfer for the restoration of elbow flexion. J Neurosurg 98:3073122003

    • Search Google Scholar
    • Export Citation
  • 61

    Samii MCarvalho GANikkhah GPenkert G: Surgical reconstruction of the musculocutaneous nerve in traumatic brachial plexus injuries. J Neurosurg 87:8818861997

    • Search Google Scholar
    • Export Citation
  • 62

    Shin AYSpinner RJSteinmann SPBishop AT: Adult traumatic brachial plexus injuries. J Am Acad Orthop Surg 13:3823962005

  • 63

    Siqueira MGMartins RS: Phrenic nerve transfer in the restoration of elbow flexion in brachial plexus avulsion injuries: how effective and safe is it?. Neurosurgery 65:4 SupplA125A1312009

    • Search Google Scholar
    • Export Citation
  • 64

    Socolovsky MDi Masi GBattaglia D: Use of long autologous nerve grafts in brachial plexus reconstruction: factors that affect the outcome. Acta Neurochir (Wien) 153:223122402011

    • Search Google Scholar
    • Export Citation
  • 65

    Socolovsky MMartins RSDi Masi GSiqueira M: Upper brachial plexus injuries: grafts vs ulnar fascicle transfer to restore biceps muscle function. Neurosurgery 71:2 Suppl Operativeons227ons2322012

    • Search Google Scholar
    • Export Citation
  • 66

    Songcharoen P: Brachial plexus injury in Thailand: a report of 520 cases. Microsurgery 16:35391995

  • 67

    Songcharoen PMahaisavariya BChotigavanich C: Spinal accessory neurotization for restoration of elbow flexion in avulsion injuries of the brachial plexus. J Hand Surg Am 21:3873901996

    • Search Google Scholar
    • Export Citation
  • 68

    Songcharoen PWongtrakul SSpinner RJ: Brachial plexus injuries in the adult. Nerve transfers: the Siriraj Hospital experience. Hand Clin 21:83892005

    • Search Google Scholar
    • Export Citation
  • 69

    Sulaiman OAKim DDBurkett CKline DG: Nerve transfer surgery for adult brachial plexus injury: a 10-year experience at Louisiana State University. Neurosurgery 65:4 SupplA55A622009

    • Search Google Scholar
    • Export Citation
  • 70

    Sungpet ASuphachatwong CKawinwonggowith V: Restoration of shoulder abduction in brachial plexus injury with phrenic nerve transfer. Aust N Z J Surg 70:7837852000

    • Search Google Scholar
    • Export Citation
  • 71

    Sungpet ASuphachatwong CKawinwonggowit VPatradul A: Transfer of a single fascicle from the ulnar nerve to the biceps muscle after avulsions of upper roots of the brachial plexus. J Hand Surg Br 25:3253282000

    • Search Google Scholar
    • Export Citation
  • 72

    Suzuki KDoi KHattori YPagsaligan JM: Long-term results of spinal accessory nerve transfer to the suprascapular nerve in upper-type paralysis of brachial plexus injury. J Reconstr Microsurg 23:2952992007

    • Search Google Scholar
    • Export Citation
  • 73

    Teboul FKakkar RAmeur NBeaulieu JYOberlin C: Transfer of fascicles from the ulnar nerve to the nerve to the biceps in the treatment of upper brachial plexus palsy. J Bone Joint Surg Am 86-A:148514902004

    • Search Google Scholar
    • Export Citation
  • 74

    Terzis JKKostas I: Suprascapular nerve reconstruction in 118 cases of adult posttraumatic brachial plexus. Plast Reconstr Surg 117:6136292006

    • Search Google Scholar
    • Export Citation
  • 75

    Terzis JKVekris MDSoucacos PN: Outcomes of brachial plexus reconstruction in 204 patients with devastating paralysis. Plast Reconstr Surg 104:122112401999

    • Search Google Scholar
    • Export Citation
  • 76

    Tonkin MAEckersley JRGschwind CR: The surgical treatment of brachial plexus injuries. Aust N Z J Surg 66:29331996

  • 77

    Vekris MDBeris AEPafilas DLykissas MGXenakis TASoucacos PN: Shoulder reanimation in posttraumatic brachial plexus paralysis. Injury 41:3123182010

    • Search Google Scholar
    • Export Citation
  • 78

    Venkatramani HBhardwaj PFaruquee SRSabapathy SR: Functional outcome of nerve transfer for restoration of shoulder and elbow function in upper brachial plexus injury. J Brachial Plex Peripher Nerve Inj 3:152008

    • Search Google Scholar
    • Export Citation
  • 79

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