Timing of Surgery in Traumatic Brachial Plexus Injury: a Systematic Review

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LITERATURE REVIEW J Neurosurg 130:1333–1345, 2019

Timing of surgery in traumatic brachial plexus injury: a systematic review

Enrico Martin, BS,1,2 Joeky T. Senders, BS,1,2 Aislyn C. DiRisio, BS,2 Timothy R. Smith, MD, PhD, MPH,2 and Marike L. D. Broekman, MD, PhD, JD1,2

1Department of Neurosurgery, University Medical Center Utrecht, The Netherlands; and 2Computational Neuroscience Outcomes Center, Department of Neurosurgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts

OBJECTIVE Ideal timeframes for operating on traumatic stretch and blunt brachial plexus injuries remain a topic of de- bate. Whereas on the one hand spontaneous recovery might occur, on the other hand, long delays are believed to result in poorer functional outcomes. The goal of this review is to assess the optimal timeframe for surgical intervention for traumatic brachial plexus injuries. METHODS A systematic search was performed in January 2017 in PubMed and Embase databases according to the PRISMA guidelines. Search terms related to “brachial plexus injury” and “timing” were used. Obstetric plexus palsies were excluded. Qualitative synthesis was performed on all studies. Timing of operation and motor outcome were collected from individual patient data. Patients were categorized into 5 delay groups (0–3, 3–6, 6–9, 9–12, and > 12 months). Median delays were calculated for Medical Research Council (MRC) muscle grade ≥ 3 and ≥ 4 recoveries. RESULTS Forty-three studies were included after full-text screening. Most articles showed significantly better motor outcome with delays to surgery less than 6 months, with some studies specifying even shorter delays. Pain and quality of life scores were also significantly better with shorter delays. Nerve reconstructions performed after long time intervals, even more than 12 months, can still be useful. All papers reporting individual-level patient data described a combined total of 569 patients; 65.5% of all patients underwent operations within 6 months and 27.4% within 3 months. The highest percentage of ≥ MRC grade 3 (89.7%) was observed in the group operated on within 3 months. These percentages decreased with longer delays, with only 35.7% ≥ MRC grade 3 with delays > 12 months. A median delay of 4 months (IQR 3–6 months) was observed for a recovery of ≥ MRC grade 3, compared with a median delay of 7 months (IQR 5–11 months) for ≤ MRC grade 3 recovery. CONCLUSIONS The results of this systematic review show that in stretch and blunt injury of the brachial plexus, the optimal time to surgery is shorter than 6 months. In general, a 3-month delay appears to be appropriate because while recovery is better in those operated on earlier, this must be considered given the potential for spontaneous recovery. https://thejns.org/doi/abs/10.3171/2018.1.JNS172068 KEYWORDS brachial plexus injury; surgery; timing; outcome; systematic review; trauma; peripheral nerve

raumatic brachial plexus injury is a rare yet dev- injury, which makes almost every case unique. There is astating event that is most commonly noted in an overall consensus that in brachial plexus injury, elbow young, active adult males involved in traffic ac- flexion is the first goal of repair, followed by shoulder sta- Tcidents.45,54,59 Although the injury itself is not fatal, life- bility.7,9,14,18,33,40,55,71,87 Many other aspects of treating these long disability usually follows and can be difficult to re- patients, including the ideal time for operating on stretch verse.45,54,59 Most of the knowledge about the treatment of and blunt injuries, remain a topic of discussion among pe- traumatic brachial plexus injury comes from single-center ripheral nerve surgeons.7 observational retrospective studies. This is partially due to While some authors advocate for very early repair of the large heterogeneity in presentation of brachial plexus traumatic brachial plexus injury,13,38,41,51,88 others suggest

ABBREVIATIONS AFRS = average final result of surgery; DASH = Disability of the Arm, Shoulder and Hand questionnaire; IQR = interquartile range; MRC = Medical Research Council; PRISMA = Preferred Reporting Items for Systematic Reviews and Meta-Analysis; SF-36 = 36-Item Short-Form Health Survey; VAS = visual analog scale. ACCOMPANYING EDITORIAL See pp 1330–1332. DOI: 10.3171/2018.2.JNS1881. SUBMITTED August 20, 2017. ACCEPTED January 10, 2018. INCLUDE WHEN CITING Published online June 1, 2018; DOI: 10.3171/2018.1.JNS172068.

©AANS 2019, except where prohibited by US copyright law J Neurosurg Volume 130 • April 2019 1333

Unauthenticated | Downloaded 10/06/21 09:48 AM UTC E. Martin et al. that long delays can still result in good functional recov- studies included are summarized using box and bar plots. eries.50,58,70 Many groups recommend waiting at least 3 Further subgroup analysis was performed based on surgi- months before surgery1,14,18,19,24,44,46,59,67,72 because sponta- cal delay. Level of injury groups were made, distinguish- neous recovery might occur.21 Many groups also discour- ing C5–6, C5–7, C5–T1, and infraclavicular lesions. Box age delays longer than 6 months8,18,24,33,44,53,55,67,91 because plots were made using the statistical program R (version long denervation times can decrease muscle strength. This 3.3.2, R Core Team, 2016). results from a combination of three processes: a reduced regenerative capacity in chronically axotomized proximal Results nerve stumps, a decreased capacity of distal nerve stumps After removal of duplicates, a total of 1161 citations to support regenerating axons, and an inability of atrophied 29,30,34 were identified in the PubMed and Embase databases. muscle to recover from chronic denervation. Timing One hundred ninety-four potentially relevant articles were is essential because nerve axons regenerate at a speed of selected through title/abstract screening, of which 43 stud- 81 only 1–2.5 mm per day, and denervation times include ies were selected for qualitative synthesis after full-text both the delay in surgery and also the time before a nerve screening (Fig. 1). reaches its target. The purpose of this study is to review how the length of Study Characteristics delay to surgery affects outcomes. The maximum length The majority of studies included in our study were ret- of delay at which surgeons should still be able to perform rospective observational studies, and only 7 of the includ- successful nerve repairs is also reviewed. ed studies were prospective cohort studies23,50,63,77,90,94,95 (Table 1). The studies included a total of 2204 patients, and Methods among studies that reported sex, 89.15% of patients were Literature Search male. The median age of patients in the included studies A systematic search was performed in both PubMed was 28 years, with an interquartile range (IQR) of 26–32.6 and Embase databases according to the PRISMA (Pre- years. Surgeries performed included nerve transfers using ferred Reporting Items for Systematic Reviews and Meta- donor nerves or recipient nerves, nerve grafts, simple neu- Analysis) guidelines, in order to identify all potentially rolysis, or a combination of these procedures. The median relevant articles as of January 2017. The search string was surgical delay was 6 months (IQR 5–7.65 months), with a built with the help of a professional librarian using search range of 0–240 months. Follow-up times ranged from 6 terms related to “brachial plexus injury” and “timing.” The months to more than 38 years, with a median of 3.45 years exact search syntaxes for PubMed and Embase are shown (IQR 2–5.15 years). in the Appendix. Studies were included that looked at timing of operation in traumatic brachial plexus injury and Outcomes in Motor Function Assessed by MRC Grade either showed clear conclusions on timing of operation or All studies that assessed Medical Research Council included both timing and postoperative outcome in tables. (MRC) muscle grade outcomes found a significant20,23, Exclusion criteria included lack of full text, obstetric bra- 31,41,49,57,68,78,83 or nonsignificant4,19,61,64,67,91,93 improved recov- chial plexus surgery, irrelevant data, case series with fewer ery after early operation versus late operation (Table 2). than 10 patients, review articles, patients with secondary Twelve studies dichotomized both surgical delay and MRC operations, overlapping data, and languages other than grade outcomes,4,23,31,43,49,50,57,67,68,78,91,93 whereas 3 groups English, Dutch, French, and German. The initial review dichotomized surgical delay20,41,83 or MRC grade outcome was conducted by two independent authors (E.M. and only.19,61,64 Several studies investigated if operations per- J.T.S.). Disagreements were solved through discussion, in formed even earlier than 6 months are beneficial for motor which one other author was involved (M.L.D.B.). outcome; cutoff points were 2 months,41 3 months,4,57,78,91 and 4 months.49,83 All studies showed better results for op- Data Extraction and Synthesis erations performed even earlier than 6 months after injury. 49 4 41 Data extracted from each study included year of pub- However, only Liu et al., Altaf et al., and Jivan et al. lication, study type, number of patients, range and me- were able to show statistical significance. Whereas Samii et al.67 showed no useful recovery in dian age of patients, gender percentages, levels of bra- 4 chial plexus lesion included, cause of injury, preoperative operations performed after 12 months and Altaf et al. even reported no useful recoveries after 5 months’ delay, assessment, range and median delay of surgery, type of 50 43 surgery performed, outcome of timing, outcome measure, Liverneaux et al. and Khalifa et al. showed that even and range and median follow-up. after delays of (more than) 12 months, good results can be obtained. They report recoveries to MRC grades as good Quantitative synthesis was not performed because the 43 included studies were too heterogeneous. A qualitative as MRC grade 4. Khalifa et al. suggest that following synthesis of the included studies was performed and our their results, surgeons should not be discouraged to per- findings are summarized in narrative fashion. Some stud- form nerve transfers and grafts after delays as long as 24 ies did not directly investigate the influence of surgical months. timing on outcome, but did provide individual-level patient data on both items. Their findings have been summa- Effect of Time to Surgery on Other Outcomes rized by dichotomizing the patients in those studies into All 7 studies suggested that earlier operations resulted those operated on within 6 months and after a delay of in better outcomes, yet only 3 showed statistically sig- more than 6 months. Individual-level patient data of all nificant findings (Table 2).1,22,27 Two studies examined pa-

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FIG. 1. Flowchart depicting study selection. tient-reported outcomes using the Disability of the Arm, Studies Not Reporting Effect of Timing of Surgery on Shoulder and Hand questionnaire (DASH) score and the Outcome 36-Item Short-Form Health Survey (SF-36) and conclud- Eighteen studies did not explicitly report the effect of ed that patients operated on within 6 months of their in- timing on outcome (Table 3). Eleven studies showed higher jury were more satisfied with their surgical outcome.1,22 ≥ 1 percentages of useful ( MRC grade 3) motor outcome Ahmed-Labib et al. even showed that DASH and SF-36 in patients operated on within 6 months, and all showed scores worsened with each additional month of delay. Ruch 66 69 42 a higher percentage of good functional recovery (MRC et al., Secer et al., and Kato et al. each used a sepa- grade 4 or higher).5,24,35,52,62,74,76,77,82,94,95 Two studies showed rate form of excellent/good/fair/poor results as an outcome better outcomes in patients operated on after 6 months.48,80 measure, and although none reported a statistical signifi- Ren et al.63 showed functional recovery in all patients re- cance, they all show better results in groups with earlier 42,66,69 gardless of preoperative delay, but all 6 patients who were surgery when looking at absolute numbers. Ruch et operated on within 6 months recovered to MRC grade 4 or al.66 demonstrated best results in patients who received 42 higher, unlike those with longer delays to surgery, of whom surgery within 5 months, Kato et al. within 1 month, and only 3 of 5 recovered to that level. A median of 87.3% (IQR Secer et al.69 within 4 months. Kato et al.42 also showed 78.6%–98.2%) of patients operated on within 6 months re- that patients who were operated on sooner have lower visual analog scale (VAS) pain scores. Flores27 used an av- covered to an MRC grade of 3 or higher, compared with erage final result of surgery (AFRS) score, an average of 66.7% (IQR 50.0%–96.4%) of those who had longer de- all MRC scores, to show that patients who were operated lays to surgery. Two-thirds of patients operated on within 6 on within 6 months have significantly better outcomes. Fi- months after injury even recovered to an MRC grade of 4 nally, Estrella and Favila26 looked at the influence of tim- or higher, while less than half of patients operated on after ing on range of motion and did not find statistically sig- 6 months recovered to this level. nificant differences, yet absolute values (88.07° and 77.14° of elbow flexion ≤ 6 months vs > 6 months, respectively) Individual-Level Patient Data showed that patients have greater mobility when operated Among the studies that reported individual patient– on earlier than 6 months. level data, timing of operation and motor outcome were

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Unauthenticated | Downloaded 10/06/21 09:48 AM UTC E. Martin et al. » mm (mean) mm NA NA 30–100 (90) NA No graft NA 40–80 (NA) NA 30–65 (NA) NA NA 61 (NA) No graft No graft 60–115 (88) 85–130 (NA) No graft NA (124) No graft NA NA NA–250 (NA) NA–250 NA NA (115) NA (45) NA NA NA No graft No graft No graft 65–166 (140) NA NA Graft Length in CONTINUED ON PAGE 1337 ON PAGE CONTINUED Cause of Injury MVA MVA, sport, iatrogenic MVA iatrogenic,MVA, laceration MVA NA CTI, GSW GSW Shrapnel/bullet injury MVA MVA, sport MVA, fall, sport, iatrogenic, laceration GSW, Injury MVA, work, fall, explosion sport, fall, MVA, iatrogenic MVA, CTI Trauma MVA MVA, fallMVA, open sharp injury GSW, fall, MVA, MVA NA Sport NA NA NA MVA, sport, GSW MVA MVA, CTI Trauma NA NA MVA MVA, fall, explosion fall, MVA, Preop Assessment Preop NA NA EDT, MRI, CM EDT, NA MRI, CM EMG, NCT, EMG NA NA NA NA EDT, CM, CT EDT, CM, MRI, EMG NA EMG EMG EDT, CM MRI, EDT EMG EMG, NCT NA MRI DT NA NA NA EMG, CM, x-ray neck/shoulder x-ray CM, EMG, EMG CT, MRI CT, EMG NA EMG EMG NA EMG Lesion C5–7 C5–7 C5–T1 C5–6 C5–T1 C5–T1 C5–T1 C5–6 C5–T1 C5–T1 C5–T1 C5–T1 C5–7 Axillary C5–T1 C5–T1 C5–6 C5–6 NA C5–7 C5–6 NA C5–T1 C5–T1 C5–T1 C5–T1 C5–8 C5–T1 C5–T1 C5–T1 C5–T1 C5–6 C5–7 C5–T1 Level of Level % 87.5 97.0 71.0 91.9 76.9 NA NA NA 78.6 62.5 93.3 92.5 93.1 93.5 80.6 80.8 84.4 92.0 93.8 84.6 86.7 60.0 83.3 85.0 90.5 86.6 90.0 96.2 96.2 Male 100.0 100.0 100.0 100.0 100.0 7–62 (32.7) 4–58 (26) 5–62 (32.9) 5–62 5–76 (28) 5–70 (37) 6–48 (27) NA (26) 17–40 (28.9) 17–59 (25.4) 17–53 (35) 17–74 (38) 17– 43 (27.2) 17– 47 (27.2) 14–59 (31) 13–32 (NA) 13–55 (24.9) 15–52 (35.6) (28) 15–60 (28) 15–66 18–53 (29.8) Yrs (mean) 19–30 (22) 15–54 (27) 19–55 (35) 19–66 (37) 15–49 (NA) 10–42 (21.8) 16–29 (24.3) 16–49 (25) 16–51 (29) 15–59 (26.5) 16– 44 (27.3) 16–45 (25.3) 16–49 (33.7) Age Range in 0.83–54 (24.2) 11 17 13 14 31 15 13 31 15 16 18 10 21 10 27 32 32 25 32 40 40 20 58 65 40 33 99 44 Pts 216 242 148 221 194 100 No. of Type Study Study Retro Retro Retro Retro Retro Retro Retro Prospect Retro Retro Retro Retro Retro Retro Retro Prospect Retro Prospect Retro Retro Retro Retro Retro Retro Retro Retro Retro Retro Retro Prospect Retro Retro Retro Retro Authors & Year Jivan 2009 al., et Comtet 1988 et al., Ahmed-Labib 2007 al., et Venkatramani 2008 et al., Stewart & Birch, 2001 Matsuyama 2002 et al., Secer 2009 al., et 2002 al., et Xu 2004 al., et Teboul Battiston 2006 et al., Ruch 1995 al., et Dubuisson & Kline, 2002 Coulet 2010 et al., Moor 2010 al., et Songcharoen 1996 al., et Dong 2010 al., et Dolan 2012 al., et & Saied,Zyaei 2010 Samii 1997 al., et Goubier et al., 2011 al., et Goubier Nagano, 1998 Flores, 2011 Flores, Altaf 2012 al., et Samii 2003 al., et Khalifa 2012 al., et Ricardo, 2005Ricardo, Kato 2006 et al., Terzis & Barbitsioti,Terzis 2012 Gao 2013 al., et Liverneaux 2006 al., et Estrella & Favila, 2014 2014 Liu al., et Nath 2006 et al., Xiao 2014 al., et

Studies w/ conclusionsStudies w/ surgical to timing conclusionsStudies w/o surgical to timing

TABLE 1. Demographics 1. TABLE of the reviewed studies

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collected.5,6,20,24,35,48–50,52,56,61–64,66,74,76,77,79,80,82,90,93–95 A total of 569 patients were described individually. Patients were categorized into 5 groups based on length of delay (0–3, 3–6, 6–9, 9–12, and > 12 months; Table 4): 27.4% of pa- mm (mean) mm NA NA 100–220 (NA) NA No graft NA NA 20–150 (NA) 20–150 NA Graft Length in tients were operated on within 3 months and 65.5% of all patients were operated on within 6 months. The level of injury was described in 443 brachial plexus cases. These were further subclassified into C5–6, C5–7, C5–T1, and infraclavicular lesions. Overall, the highest percentage of useful muscle grade (89.7%) was noted in the group with 0–3 months’ delay to surgery (Fig. 2A). The percentage of useful recovery dropped with longer delays, with only 35.7% recovery in patients with delays greater than 12 months. Total percentages of MRC grade 4 and 5 Cause of Injury are almost equivalent in patients with delays of less than 3 months and patients operated on after a delay of 3–6 months (Fig. 2A). With the exception of infraclavicular lesions, injuries at all levels show a clear increase in the MVA MVA NA NA MVA, fallMVA, MVA, fallMVA, MVA, fallMVA, Trauma MVA percentage of unsuccessful recoveries when the delay to surgery is greater than 6 months, and an even greater like- lihood of unsuccessful recovery in patients with longer delays (Fig. 2B–E). The best results are seen in upper brachial plexus lesions without involvement of C7 (Fig. 2B). Successful recovery in this group is, as in other groups, more likely with early intervention, with only a very small percentage of patients who do not recover to a useful MRC grade when operated on within 6 months. In patients who Preop Assessment Preop recovered to ≥ MRC grade 3, the median delay to surgery was 4 months (IQR 3–6 months), compared to a median EMG, NCT EMG EMG, NCT, MRIEMG, NCT, EMG, MRI EMG, MRI EMG, NCT, MRIEMG, NCT, NA NCT, EMG, MRINCT, EMG, MRI delay of 7 months (IQR 5–11 months) in patients with non- useful recovery (Fig. 3). Lesion C4–7 C5–T1 C5–T1 NA C5–6 C5–T1 C5–7 C5–7 C5–6 Level of Level Discussion % 81.2 75.9 94.1 90.0 86.7 90.0 96.6 96.6 The results of this systematic review indicate that the Male 100.0 best surgical outcomes for stretch and blunt injury of the brachial plexus are observed when operative delays are less than 6 months after injury. Although some studies show statistically significant better outcomes with even NA (23.9) NA (30.2) NA (30.5) 17–68 (37) 17–56 (32.5) 18–44 (27.2) 18–44

18–55 (32) shorter delays, most only demonstrated this for a cutoff Yrs (mean) 18–42 (28) 16–40 (26.8) Age Range in point at 6 months. To date, no randomized controlled trials or prospective cohort studies have been performed to as- 11 10 29 20 40 29 30 58 34

Pts sess optimal timing for brachial plexus lesions. Only ret- No. of rospective, mostly single-center data have been published. This may be partially due to the large heterogeneity in presentation and rarity of these lesions. Both Chuang17 and Type

Study Study 44 Retro Retro Retro Prospect Prospect Prospect Retro Retro Retro Kim et al. have performed a very large number of brachi-

al plexus injury cases in their centers and, from personal experience, recommend delays to be no longer than 5 and 6 months, respectively. Terzis et al. recommend delays of less than 3 months,88 but have not been able to show a statistically significant difference with delays between 3 and 6 months.83–86,89 Hems38 and Birch13 propose even shorter delays, recommending that patients undergo operations within 2 weeks after injury if they are fit for surgery. Authors & Year ) Nonmotor Outcome Values Although better motor function is most frequently de- Lin et al., 2011 Lin al., et Ray et al., 2011 al., et Ray Socolovsky 2011 al., et Sokki 2012 al., et Ren et al., 2013 Ren al., et Tu et al., 2014 al., et Tu Barthel 2014 al., et Socolovsky 2014 al., et Souza 2014 al., et scribed as an advantage of earlier operations, other out- continued comes are also affected. Kato et al.42 showed that post- ( Studies w/o conclusionsStudies w/o surgical to timing

CONTINUED FROM PAGE 1336 FROM PAGE CONTINUED TABLE 1. Demographics 1. TABLE of the reviewed studies CM = cervical myelography; CTI = compression or traction injury no other way specified;DT = diagnostic testing no other way specified;EDT = electrodiagnosticGSW = gunshottesting wound; no other = motor MVA way vehiclespecified; accident; EMG = electromyography; NA = not available; NCT = nerve conduction test; Prospect = prospective; Pts = patients; Retro = retrospective. » operative median VAS scores were the lowest among

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Unauthenticated | Downloaded 10/06/21 09:48 AM UTC E. Martin et al. » NA (mean) >1 (NA) NA (4.5) NA (6.7) 1–5.6 (2.4) 1–3 (1.3) 1–6 (1.4) 1–7.6 (NA) 2–9 (6) 2–38.2 (NA) 2–38.2 2–8.7 (4.2) 2–6 (3.4) 2–13 (6.5) 2–13 4–17 (7) 3–16 (8.0) 3–8 (5.6) 12–82 (42.9) 12–82 Years of FU Years 0.7–2 (1.3) 0.7–2 1.3–4.6 (2.7) 1.9 –7.3 (3) 0.9–7.25 (3.6) 0.9–3.9 (2.4) 0.5–3.25 (1.7) 2.5–10 (5) 0.75–14.6 (4.4) CONTINUED ON PAGE 1339 ON PAGE CONTINUED No Yes Yes Yes† Yes‡ NA No Yes No Yes No Yes NA NA No Yes§ NA NA Yes¶ Yes** No NA NA Yes Yes Statistical Significance* ≥ MRC grade 4 Outcome Measure ROM AFRS¶¶ ≥ MRC grade 3 ≥ MRC grade 3 ≥ MRC grade 3, ≥ MRC grade 3 ≥ MRC grade 4 DASH + SF-36 Good/fair§§ DASH + SF-36 ≥ MRC grade 3 ≥ MRC grade 3 ≥ MRC grade 4 ≥ MRC grade 3 ≥ MRC grade 3 Mean MRC Good or excellent†† Good/fair,‡‡ VAS Mean MRC Median MRC Mean delay Mean delay Mean delay ≥ MRC grade 3 ≥ MRC grade 3 ° , 62.86 ° Timing Outcome (mos) ; >6: 77.14 ° , 63.85 , ° 10–12: 22.0%,10–12: 13–25: 0%; 20.0%, 0% 8–10: 14.29%/66.67% 3–6: >6: 13.6%/50.0%, 4.0 (VAS); 5.3 48.1%/25.9%, (VAS) <6: 88.07 <6: better <3: 83%, 3–6: 78.8%, 6–9: 38.3% 9–12: 74.6%, <6: 61%, 7–12: 40%, >12: 12.5% 40%, >12: 7–12: <6: 61%, 0–3: 83.0%, 35.1%; 4–6: 74.4%, 24.4%; 7–9: 52.4%, 23.8%; 7–9: 52.4%, 0–3: 4–6: 24.4%; 83.0%, 74.4%, 35.1%; <6: 71%, 6–12: 43%; >12: 0% >12: 43%; 6–12: <6: 71%, All 100% <6: >6: worse better, <4: 44.97%/46.31%,<4: 4–6: 38.33%/50%, 6–8: 28.57%/57.14%, <6: >6: worse better, <3: 87.5%, >3: 85.7% >3: <3: 87.5%, 25.0% <6: 90.6%, 75.0%, >12: 6–12: <3: 100%, 0% >5: 67% >12: <6: 82.6%, >6: 57.1% <0.5: 4.2, 0.5–2: 1.1 3.8, >2: <5: 75.0%, >5: 22.2% 56.7%/25.0%,<1: 1–3: 2.6 39.3%/39.3%, (VAS); (VAS); 3.7 <6: 3.7 (IC), 3.9 (UN); >6: 1.8 (IC), 3.3 3.9 (UN) (IC), (UN); >6: 1.8 (IC), <6: 3.7 <4: 3.66,<4: 4–8: 3.33, 2.66 >8: ≥ MRC grade 3: 6.1 mos, < MRC grade 3: 11 mos mos, < MRC≥ MRC grade grade 11 6.1 3: 3: ≥ MRC grade 4.3 mos, 3: < MRC grade 6.9 3: mos MRC grade 4.8 mos, 4: < MRC grade 8.5 4: mos <6: 73.3%, >6: 30% <4: 96%,<4: 43% >4: Op Type NT NT, NG, N NT, NT, NG NT, NG NT, NG NT, NG NT, NG NT, NG NG NT NT, NG NT NA NT, NG NT NT, NG NT, NG NT, NG NG NT, NG, N NT, NT, NG, N NT, NT, NG NT, NG NT NT, NG NA (mean) 1–12 (6.0) 1–12 1–21.5 (4.6) 1–12 (5.1) 2–14 (8.0) 2–14 2–12 (6.6) 2–12 2–6 (NA) 2–15 (NA) 2–9 (5.0) 3–11 (6.5) 3–24 (7.8) 3–12 (6.0) 3–12 3–12 (NA) 3–24 (7.3) 0–25 (NA) 0–23 (7.5) 0–8 (2.0) 0–NA (14.6) 12–36 (18) 0–43.6 (3.6) Mos of Delay 0.7–17 (NA) 0.7–17 0.2–11 (5.9) 0.2–11 0.2–13 (6.6) 0.2–13 1.5–10 (NA) NA–5 (NA) Authors & Year Estrella & Favila, 2014 Flores, 2011 Flores, Songcharoen 1996 al., et Samii 1997 al., et Nagano, 1998 Samii 2003 al., et Liverneaux 2006 al., et Secer 2009 al., et Dolan 2012 al., et Dong 2010 al., et Altaf 2012 al., et Khalifa 2012 al., et Gao 2013 al., et Xiao 2014 al., et Venkatramani 2008 et al., Jivan 2009 al., et Ruch 1995 al., et Kato 2006 et al., Ahmed-Labib 2007 al., et Coulet 2010 et al., Terzis & Barbitsioti,Terzis 2012 Comtet 1988 et al., Ricardo, 2005Ricardo, Nath 2006 et al., Liu et al., 2014 Liu al., et

Outcomes in % above useful MRC values

MRC median/mean in Outcomes values outcome Other used

Mean delay for useful MRC values

TABLE 2.TABLE Surgical outcome in relation to timing

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patients operated on within 1 month, with rising median VAS scores as delays lengthened. Lower pain scores were also correlated with better rehabilitation, higher rates of returning to work, and faster return to work,42 which is again associated with higher quality of life.16 Other studies showed that better motor recovery is paired with greater pain relief.11,39 Considering that an earlier operation also results in better motor outcome, this may also be an ar- gument for earlier restoration. Furthermore, many authors argue that earlier operations are easier to perform because of extensive fibrosis that may occur in late explora- tion.4,13,38,42,47,51,59 Hems38 states from personal experience that this is one of his reasons to operate within 2 weeks after injury, but when a longer delay occurs, a delay of 2–3 months should be considered because of an inflammatory response that occurs between 2 and 8 weeks.

Factors Influencing Surgical Outcome In this review, the impact of surgical delay on surgical outcome was assessed, yet many other factors have been described to affect surgical outcome of brachial plexus injury. There is heterogeneity in the presentation and management of these injuries, and thus the conclusions that can be drawn by solely assessing the effect of surgical delay on outcomes are limited. Other factors influencing outcome after brachial plexus surgery can be related to patients, lesions, or surgical technique. In multiple series, age has been shown to affect motor outcome, with worse outcomes associated with older age.20,25,57,83 Coulet et al.20 and Nagano57 found this to be true for patients more than 30 years old compared to younger patients, and Terzis and Barbitsioti83 showed this for patients older than 40 compared to patients younger than 20. It has been suggested that higher cortical plasticity in younger patients could be a factor contributing to their better recovery.75 The level of the brachial plexus lesion also affects motor outcome. Upper brachial plexus lesions involving C5–7 have the best results, while C8 and T1 lesions have com- parably less favorable outcomes.44,45,89 Worse outcomes are noted when complete lesions occur.25,89 This is consistent ; excellent result is 3 to (Nagano). 8 kg

° with the results of our analysis. With the exception of infraclavicular lesions, however, all lesions are negatively affected by longer delays. This finding may be due to the small number of infraclavicular lesions included in this analysis, with only four patients in both the 9–12 and ≥ 12 months’ delay groups. Additionally, infraclavicular stretch lesions are more technically challenging to operate on due to frequent concomitant axillary artery injury, shoulder dislocation or fracture, or humeral fracture. Large series do not report worse results, however, in infraclavicular stretch lesions as compared with supraclavicular lesions.44,89 In contrast, the presence of root avulsion decreases the number of good outcomes.1,89 Avulsions are managed differ- ently because they usually require other restoration techniques. Unfortunately, the presence of avulsion was poorly documented in most papers, and thus the relationship between timing of surgery and surgical outcomes could not be assessed in these patients. Studies included in this review used a wide variety of Good is being able to hold 0.5- to 3.0-kg weights in elbow flexed 90 Good is restoration of functional active movement in at least 1 axis or joint; fair is nerve regeneration proven clinical by and neurophysiological examination, but of little functional worth. Good outcome was ≥ MRC grade 4 and ≥ S4; fair was MRC grade 2–3 or S2–3. The sum of all MRC grading divided number by of grades. Between < 4 and > 8 months’ delay. Between the group operated < 6 months months. and > 12 Spearman rank correlation and < 6 vs > 6 months. Both < 0.5 and 0.5–2 months compared to > 2 months. Only in IC group. All studies considered p < 0.05 as statistically significant. nerve grafts and transfers. Exact treatment strategies for CONTINUED FROM PAGE 1338 FROM PAGE CONTINUED TABLE 2.TABLE Surgical outcome in relation to timing FU = follow-up; IC = intercostal nerve transfer group; N = neurolysis; NG = nerve graft; NT = nerve transfer; ROM = range of motion; UN = ulnar nerve transfer group. Boldface type indicates statistical significance. * ‡ § ¶ ** † †† ‡‡ §§ ¶¶ » each plexus injury go beyond the scope of this paper, but

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TABLE 3. Summary of outcomes in studies without conclusions

Mos of Delay Timing Outcome (mos) Years of FU Authors & Year (mean) Op Type ≥ MRC Grade 3 ≥ MRC Grade 4 (mean) Stewart & Birch, 2001 0–36 (4) NT, NG, N ≤6: 81.4% ≤6: 23.3% >2 (NA) >6: 100.0% >6: 50.0% Dubuisson & Kline, 2002 0 to >24 (NA) NT, NG, N ≤6: 83.3% ≤6: 75.0% 1 to >3 (NA) >6: 61.5% >6: 15.4% Matsuyama et al., 2002 0–48 (NA) NT, NG ≤6: 88.9% ≤6: 55.5% 0.5–5 (NA) >6: 66.7% >6: 50.0% Xu et al., 2002 0.5–12 (5) NT ≤6: 77.7% ≤6: 44.4% NA >6: 50.0% >6: 0.0% Teboul et al., 2004 1.5–75 (9) NT, NG ≤6: 82.4% ≤6: 70.6% 0.8–6.2 (2.6) >6: 66.7% >6: 53.3% Battiston et al., 2006 0–2 (NA) NT, NG <6: 92.9% <6: 92.9% 1.2–8 (4) Moor et al., 2010 8–20 (11.25) NT, NG >6: 100% >6: 100% >2 (NA) Zyaei & Saied, 2010 5–9 (7) NT ≤6: 100% ≤6: 100% 1 (1) >6: 75% >6: 25% Goubier et al., 2011 2–9 (5) NT, NG ≤6: 100% ≤6: 88.9% 1.5–2.3 (2) >6: 0% >6: 0% Lin et al., 2011 3–9 (5.7) NT, NG ≤6: 66.7% ≤6: 33.3% 2.5–4.4 (3.5) >6: 100% >6: 50% Ray et al., 2011 0–11 (4.9) NT, NG ≤6: 100% ≤6: 95.0% 0.7–5.7 (1.6) >6: 85.7% >6: 42.9% Socolovsky et al., 2011 2–24 (NA) NT, NG ≤6: 66.7% ≤6: 36.7% >2 (NA) >6: 11.8% >6: 5.9% Sokki et al., 2012 3–18 (NA) NT, NG ≤6: 57.1 % ≤6: 35.7% 1 (1) >6: 50% >6: 10% Ren et al., 2013 4–12 (6.7) NT ≤6: 100% ≤6: 100% 1.3–3 (NA) >6: 100% >6: 60% Tu et al., 2014 2–5 (NA) NT, NG ≤6: 90% ≤6: 62.5% 4.5–8 (6) Barthel et al., 2014 2–23 (NA) NT, NG ≤6: 90% ≤6: 75% 1.3–7.8 (NA) >6: 66.7% >6: 66.7% Socolovsky et al., 2014 1–12 (7.3) NT, NG ≤6: 85.7% ≤6: 57.1% 1–6.3 (2.4) >6: 50% >6: 50% Souza et al., 2014 7–15 (NA) NT >6: 45% >6: 0% 2 (2) Median reported percentage of recovery ≤ 6 months (IQR): ≥ MRC grade 3, 87.3% (78.6%–98.2%); ≥ MRC grade 4, 66.6% (38.5%–91.9%). Median reported percentage of recovery > 6 months (IQR): ≥ MRC grade 3, 66.7% (50.0%–96.4%); ≥ MRC grade 4, 47.5% (11.4%–52.5%). differences in motor outcome have been shown to depend bination of both in upper brachial plexus palsy, favoring the on the donor nerves that are used, especially when com- former. The length of the graft also affects outcomes, with paring intra- and extraplexal donors.25,32,36,60,83,89 Intraplexal longer grafts typically yielding worse results.8,18,60,64,67,86 donors generally give better results, which is why many au- Narakas and Hentz60 and Chuang et al.18 found that grafts thors prefer using them. This may be due to a larger number longer than 10 cm were predictive of worse outcome. Samii of axons in the donor.25 Ali et al.2 demonstrated by system- et al.67 reported statistically better outcome in patients with atic review that there is a significant difference when com- grafts 12 cm or shorter compared to grafts longer than 12 paring nerve transfers to nerve graft techniques or a com- cm, while Terzis and Kostas86 found a cutoff point at 7-cm

TABLE 4. Distribution of surgical delay among levels of injury Delay (mos) All Pts C5–6 C5–7 C5–T1 Infraclavicular 0–3 156 (27.4%) 27 (16.4%) 27 (28.4%) 51 (42.5%) 33 (52.4%) 3–6 217 (38.1%) 73 (44.2%) 36 (37.9%) 47 (39.2%) 9 (14.3%) 6–9 115 (20.2%) 42 (25.5%) 22 (23.2%) 10 (8.3%) 13 (20.6%) 9–12 53 (9.3%) 18 (10.9%) 7 (7.4%) 10 (8.3%) 4 (6.3%) >12 28 (4.9%) 5 (3.0%) 3 (3.2%) 2 (1.7%) 4 (6.3%)

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FIG. 2. Surgical timing and muscle grade of individual-level patient data: all patients (A), C5–6 lesions (B), C5–7 lesions (C), C5– T1 lesions (D), and infraclavicular lesions (E). length. Aside from surgical management, postoperative tients is a delay in referral.1,22,24,28,38,45,54,70,79 Dolan et al.22 rehabilitation also plays a role in the extent of functional reported that late referral was the reason for delayed sur- outcome.12,15,37,74 Socolovsky et al.74 used a 4-point scale to gery in every one of their patients operated on at least 6 assess the quality of the rehabilitation program their pa- months after the injury. These patients made up 75% of tients were enrolled in and showed a statistically significant all patients who did not reach functional recovery.22 In the better motor outcome in patients who receive superior re- patient group reported by Souza et al.79 no one was oper- habilitation. ated on before 6 months, all due to late referrals. Dubuis- son even reported an average referral time of 6.8 months after injury.24 Concomitant injuries in multitrauma patients Late Referrals can also lead to long delays.38,69 Even though some authors A recurring barrier to optimal treatment for these pa- argue that patients do not benefit from late repairs,3,41,59 oth-

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Limitations Further limitations of this review include the heterogeneity of the studies included. Some studies only reported on certain surgical techniques used, while others included all cases of brachial plexus surgery. Length of follow-up varies markedly between studies, possibly negatively affecting the outcomes described by studies with shorter follow-up. Many studies did not report their preoperative assessment of patients, and the ones that did also differed from one another. This may have given rise to differences in preoperative functional status, indications for surgery, and timing of surgery. Lastly, most studies did not report reasons for timing of individual cases. This may result in the factors affecting clinical decisions confounding the outcome of this review. This study is the first attempt to obtain ideal timeframes for operation in stretch and blunt injury of the brachial plexus by systematically reviewing the literature. Because of heterogeneity in published studies and the nature of brachial plexus injury, no quantitative study could be performed. Results of this study may be used as reference for future research, but clinicians will still need to take several other factors into consideration to make an appropriate management plan. In an attempt to further investigate if operations should be performed with delays shorter than 3 months, using preoperative assessment to find suitable patients is essential.

FIG. 3. Box-and-whisker plot showing median delay in months for Conclusions muscle grade. In stretch and blunt injury of the brachial plexus, ideal operative timeframes appear to be less than 6 months after injury. In general, a 3-month delay is generally appropri- ers encourage surgeons to still perform nerve restoration ate. Regardless of the level of injury, recovery is improved in some patients.10,43 Although many patients operated on in those operated on earlier, yet this must be considered after more than 12 months will need secondary operations, with the potential for spontaneous recovery in mind. such as tendon transfers, muscle transfers, or arthrodesis to restore upper extremity function,17,89 pain in preganglionic Appendix ruptures can be relieved by nerve restoration even after 10 PubMed search (21-1-2017): ((“plexus brachialis injury”[Title/ longer periods of time. Abstract] OR “brachial plexus injury”[Title/Abstract] OR “plexus brachialis injuries”[Title/Abstract] OR “brachial plex- Spontaneous Recovery us injuries”[Title/Abstract] OR “brachial plexus trauma”[Title/ Abstract] OR “brachial plexus lesion”[Title/Abstract] OR “brachial Spontaneous recovery can occur in patients, which plexus lesions”[Title/Abstract] OR “brachial plexus avulsion”[Title/ means that some early operations may be unneces- Abstract] OR “plexus brachialis palsy”[Title/Abstract] OR “brachial sary. 24,38,45,65,73,92 Few studies report on exact numbers of plexus palsy”[Title/Abstract] OR “brachial plexus palsies”[Title/ spontaneous recovery after brachial plexus injury. Kline45 Abstract] OR “brachial plexus paralysis”[Title/Abstract] OR reported from personal experience that spontaneous re- “brachial plexus disruption”[Title/Abstract] OR “brachial plexus covery occurred in 40% of patients presenting with a le- dissection”[Title/Abstract] OR “Erb’s palsy”[Title/Abstract] OR sion in C5–6, but decreased to 15%–16% when C7 was “Erb’s palsies”[Title/Abstract] OR “Erb’s paralysis”[Title/Abstract] 38 OR “Erb-Duchenne palsy”[Title/Abstract] OR “Erb-Duchenne also affected, and to 4%–5% in complete lesions. Hems, paralysis”[Title/Abstract] OR “Klumpke’s palsy”[Title/Abstract] however, states that he rarely saw recovery of function af- OR “Brachial Plexus/injuries”[Mesh:NoExp] OR “Brachial Plex- ter 3 or 4 months in cases of complete loss of function us Neuropathies”[Mesh:NoExp]) AND (“timing”[Title/Abstract] from the upper plexus. In the few cases that were man- OR “time to”[Title/Abstract] OR “time management”[Title/ aged conservatively, some recovery was noted in biceps Abstract] OR delay*[Title/Abstract] OR “early”[Title/Abstract] and deltoid function after extended follow-up, but rarely in OR “management”[Title/Abstract] OR “late”[Title/Abstract] suprascapular nerve functions.38 Preoperative assessment OR “later”[Title/Abstract]) AND (“surgery”[Title/Abstract] OR plays a large role in predicting whether patients will show reconstruct*[Title/Abstract] OR “operation”[Title/Abstract] OR 73 “operate”[Title/Abstract] OR “treatment”[Title/Abstract] OR spontaneous recovery. The exact preoperative manage- explor*[Title/Abstract] OR “surgical repair”[Title/Abstract] OR ment of peripheral nerve injuries goes beyond the scope “reconstructive surgery”[Title/Abstract] OR “Brachial Plexus/ of this paper, but is discussed in a recent review of Simon surgery”[Mesh:NoExp] OR “Brachial Plexus Neuropathies/ et al.73 surgery”[Mesh:NoExp]))

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Embase search (21-1-2017): ((‘plexus brachialis injury’:ti,ab OR 15. Chalidapong P, Sananpanich K, Klaphajone J: Electromyo- ‘brachial plexus injury’:ti,ab OR ‘plexus brachialis injuries’:ti,ab graphic comparison of various exercises to improve elbow OR ‘brachial plexus injuries’:ti,ab OR ‘brachial plexus trauma’:ti,ab flexion following intercostal nerve transfer. J Bone Joint OR ‘brachial plexus lesion’:ti,ab OR ‘brachial plexus lesions’:ti,ab Surg Br 88:620–622, 2006 OR ‘brachial plexus avulsion’:ti,ab OR ‘plexus brachialis 16. Choi PD, Novak CB, Mackinnon SE, Kline DG: Quality of palsy’:ti,ab OR ‘brachial plexus palsy’:ti,ab OR ‘brachial plexus life and functional outcome following brachial plexus injury. palsies’:ti,ab OR ‘brachial plexus paralysis’:ti,ab OR ‘brachial J Hand Surg Am 22:605–612, 1997 plexus disruption’:ti,ab OR ‘brachial plexus dissection’:ti,ab OR 17. Chuang DCC: Debates to personal conclusion in periph- ‘Erb/s palsy’:ti,ab OR ‘Erb/s palsies’:ti,ab OR ‘Erb/s paralysis’:ti,ab eral nerve injury and reconstruction: A 30-year experience OR ‘Erb-Duchenne palsy’:ti,ab OR ‘Erb-Duchenne paralysis’:ti,ab at Chang Gung Memorial Hospital. Indian J Plast Surg OR ‘Klumpke/s palsy’:ti,ab OR ‘Brachial plexus injury’/exp 49:144–150, 2016 OR ‘Brachial plexus neuropathy’/exp) AND (‘timing’:ti,ab OR 18. Chuang DCC, Epstein MD, Yeh MC, Wei FC: Functional ‘time to’:ti,ab OR ‘time management’:ti,ab OR delay*:ti,ab OR restoration of elbow flexion in brachial plexus injuries: results ‘early’:ti,ab OR ‘management’:ti,ab OR ‘late’:ti,ab OR ‘later’:ti,ab) in 167 patients (excluding obstetric brachial plexus injury). J AND (‘surgery’:ti,ab OR reconstruct*:ti,ab OR ‘operation’:ti,ab OR Hand Surg Am 18:285–291, 1993 ‘operate’:ti,ab OR ‘treatment’:ti,ab OR explor*:ti,ab OR ‘surgical 19. Comtet JJ, Sedel L, Fredenucci JF, Herzberg G: Duchenne- repair’:ti,ab OR ‘reconstructive surgery’:ti,ab) AND ([article]/lim) Erb palsy. Experience with direct surgery. Clin Orthop AND ([Embase]/lim)) Relat Res (237):17–23, 1988 20. Coulet B, Boretto JG, Lazerges C, Chammas M: A comparison of intercostal and partial ulnar nerve transfers in restor- ing elbow flexion following upper brachial plexus injury (C5- C6±C7). J Hand Surg Am 35:1297–1303, 2010 References 21. de Laat EA, Visser CP, Coene LN, Pahlplatz PV, Tavy DL: 1. Ahmed-Labib M, Golan JD, Jacques L: Functional outcome Nerve lesions in primary shoulder dislocations and humeral of brachial plexus reconstruction after trauma. Neurosur- neck fractures. A prospective clinical and EMG study. J gery 61:1016–1023, 2007 Bone Joint Surg Br 76:381–383, 1994 2. Ali ZS, Heuer GG, Faught RWF, Kaneriya SH, Sheikh UA, 22. Dolan RT, Butler JS, Murphy SM, Hynes D, Cronin KJ: Syed IS, et al: Upper brachial plexus injury in adults: com- Health-related quality of life and functional outcomes fol- parative effectiveness of different repair techniques. J Neu- lowing nerve transfers for traumatic upper brachial plexus rosurg 122:195–201, 2015 injuries. J Hand Surg Eur Vol 37:642–651, 2012 3. Allieu Y, Chammas M, Picot MC: [Paralysis of the brachial 23. Dong Z, Zhang CG, Gu YD: Surgical outcome of phrenic plexus caused by supraclavicular injuries in the adult. Long- nerve transfer to the anterior division of the upper trunk in term comparative results of nerve grafts and transfers.] Rev treating brachial plexus avulsion. J Neurosurg 112:383–385, Chir Orthop Repar Appar Mot 83:51–59, 1997 (Fr) 2010 4. Altaf F, Mannan K, Bharania P, Sewell MD, Di Mascio L, 24. Dubuisson AS, Kline DG: Brachial plexus injury: a survey of Sinisi M: Severe brachial plexus injuries in rugby. Injury 100 consecutive cases from a single service. Neurosurgery 43:272–273, 2012 51:673–683, 2002 5. Barthel PY, Barbary S, Breton A, Apredoaei C, Dap F, Man- 25. El-Gammal TA, Fathi NA: Outcomes of surgical treatment of sat P, et al: [Recovery of elbow flexion in post-traumatic brachial plexus injuries using nerve grafting and nerve trans- C5-C6 and C5-C6-C7 palsy: retrospective dual-center study fers. J Reconstr Microsurg 18:7–15, 2002 comparing single and double nerve transfer.] Chir Main 26. Estrella EP, Favila AS Jr: Nerve transfers for shoulder func- 33:211–218, 2014 (Fr) tion for traumatic brachial plexus injuries. J Reconstr Mi- 6. Battiston B, Bertoldo U, Tos P, Cimino F: Primary nerve re- crosurg 30:59–64, 2014 pair in associated lesions of the axillary artery and brachial 27. Flores LP: The importance of the preoperative clinical pa- plexus. Microsurgery 26:311–315, 2006 rameters and the intraoperative electrophysiological monitor- 7. Belzberg AJ, Dorsi MJ, Storm PB, Moriarity JL: Surgi- ing in brachial plexus surgery. Arq Neuropsiquiatr 69:654– cal repair of brachial plexus injury: a multinational survey 659, 2011 of experienced peripheral nerve surgeons. J Neurosurg 28. Franzblau LE, Maynard M, Chung KC, Yang LJS: Medical 101:365–376, 2004 treatment decision making after total avulsion brachial plex- 8. Bentolila V, Nizard R, Bizot P, Sedel L: Complete traumatic us injury: a qualitative study. J Neurosurg 122:1413–1420, brachial plexus palsy. Treatment and outcome after repair. J 2015 Bone Joint Surg Am 81:20–28, 1999 29. Fu SY, Gordon T: Contributing factors to poor functional 9. Berger A, Becker MH: Brachial plexus surgery: our concept recovery after delayed nerve repair: prolonged axotomy. J of the last twelve years. Microsurgery 15:760–767, 1994 Neurosci 15:3876–3885, 1995 10. Berman J, Anand P, Chen L, Taggart M, Birch R: Pain relief 30. Fu SY, Gordon T: Contributing factors to poor functional from preganglionic injury to the brachial plexus by late inter- recovery after delayed nerve repair: prolonged denervation. J costal nerve transfer. J Bone Joint Surg Br 78:759–760, 1996 Neurosci 15:3886–3895, 1995 11. Berman JS, Birch R, Anand P: Pain following human brachi- 31. Gao K, Lao J, Zhao X, Gu Y: Outcome after transfer of in- al plexus injury with spinal cord root avulsion and the effect tercostal nerves to the nerve of triceps long head in 25 adult of surgery. Pain 75:199–207, 1998 patients with total brachial plexus root avulsion injury. J 12. Birch R: Brachial plexus injury: the London experience with Neurosurg 118:606–610, 2013 supraclavicular traction lesions. Neurosurg Clin N Am 32. Garg R, Merrell GA, Hillstrom HJ, Wolfe SW: Comparison 20:15–23, v, 2009 of nerve transfers and nerve grafting for traumatic upper 13. Birch R: Timing of surgical reconstruction for closed trau- plexus palsy: a systematic review and analysis. J Bone Joint matic injury to the supraclavicular brachial plexus. J Hand Surg Am 93:819–829, 2011 Surg Eur Vol 40:562–567, 2015 33. Giuffre JL, Kakar S, Bishop AT, Spinner RJ, Shin AY: 14. Carlsen BT, Bishop AT, Shin AY: Late reconstruction for Current concepts of the treatment of adult brachial plexus brachial plexus injury. Neurosurg Clin N Am 20:51–64, vi, injuries. J Hand Surg Am 35:678–688, 2010 (Erratum in J 2009 Hand Surg Am 35:1226, 2010)

J Neurosurg Volume 130 • April 2019 1343

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34. Gordon T, Tyreman N, Raji MA: The basis for diminished 57. Nagano A: Treatment of brachial plexus injury. J Orthop Sci functional recovery after delayed peripheral nerve repair. J 3:71–80, 1998 Neurosci 31:5325–5334, 2011 58. Narakas A, Herzberg G: Neuro-neural intraplexal transfers in 35. Goubier JN, Teboul F, Khalifa H: Reanimation of elbow traumatic radicular avulsions of the brachial plexus. Report extension with intercostal nerves transfers in total brachial on fifteen cases. Ann Chir Main 4:211–218, 1985 plexus palsies. Microsurgery 31:7–11, 2011 59. Narakas AO: The treatment of brachial plexus injuries. Int 36. Gu YD, Ma MK: Use of the phrenic nerve for brachial plexus Orthop 9:29–36, 1985 reconstruction. Clin Orthop Relat Res (323):119–121, 1996 60. Narakas AO, Hentz VR: Neurotization in brachial plexus 37. Havton LA, Carlstedt T: Repair and rehabilitation of plexus injuries. Indication and results. Clin Orthop Relat Res and root avulsions in animal models and patients. Curr Opin (237):43–56, 1988 Neurol 22:570–574, 2009 61. Nath RK, Lyons AB, Bietz G: Physiological and clinical ad- 38. Hems TEJ: Timing of surgical reconstruction for closed trau- vantages of median nerve fascicle transfer to the musculocu- matic injury to the supraclavicular brachial plexus. J Hand taneous nerve following brachial plexus root avulsion injury. Surg Eur Vol 40:568–572, 2015 J Neurosurg 105:830–834, 2006 39. Htut M, Misra P, Anand P, Birch R, Carlstedt T: Pain phe- 62. Ray WZ, Pet MA, Yee A, Mackinnon SE: Double fascicular nomena and sensory recovery following brachial plexus nerve transfer to the biceps and brachialis muscles after bra- avulsion injury and surgical repairs. J Hand Surg [Br] chial plexus injury: clinical outcomes in a series of 29 cases. 31:596–605, 2006 J Neurosurg 114:1520–1528, 2011 40. Jamieson A, Hughes S: The role of surgery in the manage- 63. Ren GH, Li RG, Xiang DY, Yu B: Reconstruction of shoulder ment of closed injuries to the brachial plexus. Clin Orthop abduction by multiple nerve fascicle transfer through poste- Relat Res (147):210–215, 1980 rior approach. Injury 44:492–497, 2013 41. Jivan S, Kumar N, Wiberg M, Kay S: The influence of pre- 64. Ricardo M: Surgical treatment of brachial plexus injuries in surgical delay on functional outcome after reconstruction adults. Int Orthop 29:351–354, 2005 of brachial plexus injuries. J Plast Reconstr Aesthet Surg 65. Robinson LR: Traumatic injury to peripheral nerves. Muscle 62:472–479, 2009 Nerve 23:863–873, 2000 42. Kato N, Htut M, Taggart M, Carlstedt T, Birch R: The ef- 66. Ruch DS, Friedman A, Nunley JA: The restoration of elbow fects of operative delay on the relief of neuropathic pain after flexion with intercostal nerve transfers. Clin Orthop Relat injury to the brachial plexus: a review of 148 cases. J Bone Res (314):95–103, 1995 Joint Surg Br 88:756–759, 2006 67. Samii A, Carvalho GA, Samii M: Brachial plexus injury: fac- 43. Khalifa H, Belkheyar Z, Diverrez JP, Oberlin C: Results tors affecting functional outcome in spinal accessory nerve of 24 nerve repairs at more than one year post-injury. Chir transfer for the restoration of elbow flexion. J Neurosurg Main 31:318–323, 2012 98:307–312, 2003 44. Kim DH, Cho YJ, Tiel RL, Kline DG: Outcomes of surgery in 68. Samii M, Carvalho GA, Nikkhah G, Penkert G: Surgical 1019 brachial plexus lesions treated at Louisiana State Univer- reconstruction of the musculocutaneous nerve in traumatic sity Health Sciences Center. J Neurosurg 98:1005–1016, 2003 brachial plexus injuries. J Neurosurg 87:881–886, 1997 45. Kline DG: Timing for brachial plexus injury: a personal ex- 69. Secer HI, Solmaz I, Anik I, Izci Y, Duz B, Daneyemez MK, perience. Neurosurg Clin N Am 20:24–26, v, 2009 et al: Surgical outcomes of the brachial plexus lesions caused 46. Kline DG, Judice DJ: Operative management of selected bra- J Brachial Plex Peripher chial plexus lesions. J Neurosurg 58:631–649, 1983 by gunshot wounds in adults. 47. Korus L, Ross DC, Doherty CD, Miller TA: Nerve transfers Nerve Inj 4:11, 2009 and neurotization in peripheral nerve injury, from surgery to 70. Sedain G, Sharma MS, Sharma BS, Mahapatra AK: Outcome rehabilitation. J Neurol Neurosurg Psychiatry 87:188–197, after delayed Oberlin transfer in brachial plexus injury. Neu- 2016 rosurgery 69:822–828, 2011 48. Lin H, Hou C, Chen A, Xu Z: Transfer of the phrenic nerve 71. Sedel L: Repair of severe traction lesions of the brachial to the posterior division of the lower trunk to recover thumb plexus. Clin Orthop Relat Res (237):62–66, 1988 and finger extension in brachial plexus palsy. J Neurosurg 72. Shin AY, Spinner RJ, Steinmann SP, Bishop AT: Adult trau- 114:212–216, 2011 matic brachial plexus injuries. J Am Acad Orthop Surg 49. Liu Y, Lao J, Gao K, Gu Y, Zhao X: Comparative study of 13:382–396, 2005 phrenic nerve transfers with and without nerve graft for 73. Simon NG, Spinner RJ, Kline DG, Kliot M: Advances in the elbow flexion after global brachial plexus injury. Injury neurological and neurosurgical management of peripheral 45:227–231, 2014 nerve trauma. J Neurol Neurosurg Psychiatry 87:198–208, 50. Liverneaux PA, Diaz LC, Beaulieu JY, Durand S, Oberlin C: 2016 Preliminary results of double nerve transfer to restore elbow 74. Socolovsky M, Di Masi G, Battaglia D: Use of long autolo- flexion in upper type brachial plexus palsies. Plast Reconstr gous nerve grafts in brachial plexus reconstruction: factors Surg 117:915–919, 2006 that affect the outcome. Acta Neurochir (Wien) 153:2231– 51. Magalon G, Bordeaux J, Legre R, Aubert JP: Emergency 2240, 2011 versus delayed repair of severe brachial plexus injuries. Clin 75. Socolovsky M, Malessy M, Lopez D, Guedes F, Flores L: Orthop Relat Res (237):32–35, 1988 Current concepts in plasticity and nerve transfers: relation- 52. Matsuyama T, Okuchi K, Akahane M, Inada Y, Murao Y: ship between surgical techniques and outcomes. Neurosurg Clinical analysis of 16 patients with brachial plexus injury. Focus 42(3):E13, 2017 Neurol Med Chir (Tokyo) 42:114–122, 2002 76. Socolovsky M, Martins RS, Di Masi G, Bonilla G, Siqueira 53. Mehta VS, Banerji AK, Tripathi RP: Surgical treatment of MG: Influence of body mass index on the outcome of bra- brachial plexus injuries. Br J Neurosurg 7:491–500, 1993 chial plexus surgery: are there any differences between elbow 54. Midha R: Epidemiology of brachial plexus injuries in a mul- and shoulder results? Acta Neurochir (Wien) 156:2337– titrauma population. Neurosurgery 40:1182–1189, 1997 2344, 2014 55. Millesi H: Brachial plexus injuries. Nerve grafting. Clin Or- 77. Sokki AM, Bhat DI, Devi BI: Cortical reorganization follow- thop Relat Res (237):36–42, 1988 ing neurotization: a diffusion tensor imaging and functional 56. Moor BK, Haefeli M, Bouaicha S, Nagy L: Results after de- magnetic resonance imaging study. Neurosurgery 70:1305– layed axillary nerve reconstruction with interposition of sural 1311, 2012 nerve grafts. J Shoulder Elbow Surg 19:461–466, 2010 78. Songcharoen P, Mahaisavariya B, Chotigavanich C: Spinal

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accessory neurotization for restoration of elbow flexion in between total and hemicontralateral C7 nerve root transfer. avulsion injuries of the brachial plexus. J Hand Surg Am Microsurgery 34:91–101, 2014 21:387–390, 1996 91. Venkatramani H, Bhardwaj P, Faruquee SR, Sabapathy SR: 79. Souza FHM, Bernardino SN, Filho HCA, Gobbato PL, Mar- Functional outcome of nerve transfer for restoration of shoul- tins RS, Martins HAL, et al: Comparison between the anteri- der and elbow function in upper brachial plexus injury. J or and posterior approach for transfer of the spinal accessory Brachial Plex Peripher Nerve Inj 3:15, 2008 nerve to the suprascapular nerve in late traumatic brachial 92. Wilbourn AJ: The electrodiagnostic examination with pe- plexus injuries. Acta Neurochir (Wien) 156:2345–2349, ripheral nerve injuries. Clin Plast Surg 30:139–154, 2003 2014 93. Xiao C, Lao J, Wang T, Zhao X, Liu J, Gu Y: Intercostal 80. Stewart MPM, Birch R: Penetrating missile injuries of the nerve transfer to neurotize the musculocutaneous nerve brachial plexus. J Bone Joint Surg Br 83:517–524, 2001 after traumatic brachial plexus avulsion: a comparison of 81. Sunderland S: Rate of regeneration in human peripheral two, three, and four nerve transfers. J Reconstr Microsurg nerves; analysis of the interval between injury and onset of 30:297–304, 2014 recovery. Arch Neurol Psychiatry 58:251–295, 1947 94. Xu WD, Gu YD, Xu JG, Tan LJ: Full-length phrenic nerve 82. Teboul F, Kakkar R, Ameur N, Beaulieu JY, Oberlin C: transfer by means of video-assisted thoracic surgery in treat- Transfer of fascicles from the ulnar nerve to the nerve to the ing brachial plexus avulsion injury. Plast Reconstr Surg biceps in the treatment of upper brachial plexus palsy. J Bone 110:104–111, 2002 Joint Surg Am 86-A:1485–1490, 2004 95. Zyaei A, Saied A: Functional outcome of ulnar nerve fascicle 83. Terzis JK, Barbitsioti A: Primary restoration of elbow flexion transfer for restoration of elbow flexion in upper brachial in adult post-traumatic plexopathy patients. J Plast Reconstr plexus injury. Eur J Orthop Surg Traumatol 20:293–297, Aesthet Surg 65:72–84, 2012 2010 84. Terzis JK, Barmpitsioti A: Axillary nerve reconstruction in 176 posttraumatic plexopathy patients. Plast Reconstr Surg 125:233–247, 2010 Disclosures 85. Terzis JK, Barmpitsioti A: Our experience with triceps nerve The authors report no conflict of interest concerning the materi- reconstruction in patients with brachial plexus injury. J Plast als or methods used in this study or the findings specified in this Reconstr Aesthet Surg 65:590–600, 2012 paper. 86. Terzis JK, Kostas I: Suprascapular nerve reconstruction in 118 cases of adult posttraumatic brachial plexus. Plast Re- Author Contributions constr Surg 117:613–629, 2006 Conception and design: Martin, Broekman. Acquisition of data: 87. Terzis JK, Kostas I, Soucacos PN: Restoration of shoulder Martin, Senders, DiRisio. Analysis and interpretation of data: function with nerve transfers in traumatic brachial plexus Martin, Senders, DiRisio, Broekman. Drafting the article: Mar- palsy patients. Microsurgery 26:316–324, 2006 tin, Senders, DiRisio. Critically revising the article: all authors. 88. Terzis JK, Vekris MD, Soucacos PN: Brachial plexus root Reviewed submitted version of manuscript: all authors. Adminis- avulsions. World J Surg 25:1049–1061, 2001 trative/technical/material support: Smith, Broekman. Study super- 89. Terzis JK, Vekris MD, Soucacos PN: Outcomes of brachial vision: Smith, Broekman. plexus reconstruction in 204 patients with devastating paralysis. Plast Reconstr Surg 104:1221–1240, 1999 90. Tu YK, Tsai YJ, Chang CH, Su FC, Hsiao CK, Tan JSW: Correspondence Surgical treatment for total root avulsion type brachial plexus Enrico Martin: University Medical Center Utrecht, The Nether- injuries by neurotization: a prospective comparison study lands. [email protected].

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