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

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

Ideal timeframes for operating on traumatic stretch and blunt brachial plexus injuries remain a topic of debate. 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.

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.

OBJECTIVE

Ideal timeframes for operating on traumatic stretch and blunt brachial plexus injuries remain a topic of debate. 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.

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.

Traumatic brachial plexus injury is a rare yet devastating event that is most commonly noted in young, active adult males involved in traffic accidents.45,54,59 Although the injury itself is not fatal, lifelong disability usually follows and can be difficult to reverse.45,54,59 Most of the knowledge about the treatment of traumatic brachial plexus injury comes from single-center observational retrospective studies. This is partially due to the large heterogeneity in presentation of brachial plexus injury, which makes almost every case unique. There is an overall consensus that in brachial plexus injury, elbow flexion is the first goal of repair, followed by shoulder stability.7,9,14,18,33,40,55,71,87 Many other aspects of treating these patients, including the ideal time for operating on stretch and blunt injuries, remain a topic of discussion among peripheral nerve surgeons.7

While some authors advocate for very early repair of traumatic brachial plexus injury,13,38,41,51,88 others suggest that long delays can still result in good functional recoveries.50,58,70 Many groups recommend waiting at least 3 months before surgery1,14,18,19,24,44,46,59,67,72 because spontaneous recovery might occur.21 Many groups also discourage delays longer than 6 months8,18,24,33,44,53,55,67,91 because long denervation times can decrease muscle strength. This results from a combination of three processes: a reduced regenerative capacity in chronically axotomized proximal nerve stumps, a decreased capacity of distal nerve stumps to support regenerating axons, and an inability of atrophied muscle to recover from chronic denervation.29,30,34 Timing is essential because nerve axons regenerate at a speed of only 1–2.5 mm per day,81 and denervation times include both the delay in surgery and also the time before a nerve reaches its target.

The purpose of this study is to review how the length of delay to surgery affects outcomes. The maximum length of delay at which surgeons should still be able to perform successful nerve repairs is also reviewed.

Methods

Literature Search

A systematic search was performed in both PubMed and Embase databases according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analysis) guidelines, in order to identify all potentially relevant articles as of January 2017. The search string was built with the help of a professional librarian using search terms related to “brachial plexus injury” and “timing.” The exact search syntaxes for PubMed and Embase are shown in the Appendix. Studies were included that looked at timing of operation in traumatic brachial plexus injury and either showed clear conclusions on timing of operation or included both timing and postoperative outcome in tables. Exclusion criteria included lack of full text, obstetric brachial plexus surgery, irrelevant data, case series with fewer than 10 patients, review articles, patients with secondary operations, overlapping data, and languages other than English, Dutch, French, and German. The initial review was conducted by two independent authors (E.M. and J.T.S.). Disagreements were solved through discussion, in which one other author was involved (M.L.D.B.).

Data Extraction and Synthesis

Data extracted from each study included year of publication, study type, number of patients, range and median age of patients, gender percentages, levels of brachial plexus lesion included, cause of injury, preoperative assessment, range and median delay of surgery, type of surgery performed, outcome of timing, outcome measure, and range and median follow-up.

Quantitative synthesis was not performed because the included studies were too heterogeneous. A qualitative synthesis of the included studies was performed and our findings are summarized in narrative fashion. Some studies did not directly investigate the influence of surgical timing on outcome, but did provide individual-level patient data on both items. Their findings have been summarized by dichotomizing the patients in those studies into those operated on within 6 months and after a delay of more than 6 months. Individual-level patient data of all studies included are summarized using box and bar plots. Further subgroup analysis was performed based on surgical delay. Level of injury groups were made, distinguishing C5–6, C5–7, C5–T1, and infraclavicular lesions. Box plots were made using the statistical program R (version 3.3.2, R Core Team, 2016).

Results

After removal of duplicates, a total of 1161 citations were identified in the PubMed and Embase databases. One hundred ninety-four potentially relevant articles were selected through title/abstract screening, of which 43 studies were selected for qualitative synthesis after full-text screening (Fig. 1).

FIG. 1.
FIG. 1.

Flowchart depicting study selection.

Study Characteristics

The majority of studies included in our study were retrospective observational studies, and only 7 of the included studies were prospective cohort studies23,50,63,77,90,94,95 (Table 1). The studies included a total of 2204 patients, and among studies that reported sex, 89.15% of patients were male. The median age of patients in the included studies was 28 years, with an interquartile range (IQR) of 26–32.6 years. Surgeries performed included nerve transfers using donor nerves or recipient nerves, nerve grafts, simple neurolysis, or a combination of these procedures. The median surgical delay was 6 months (IQR 5–7.65 months), with a range of 0–240 months. Follow-up times ranged from 6 months to more than 38 years, with a median of 3.45 years (IQR 2–5.15 years).

TABLE 1.

Demographics of the reviewed studies

Authors & YearStudy TypeNo. of PtsAge Range in Yrs (mean)% MaleLevel of LesionPreop AssessmentCause of InjuryGraft Length in mm (mean)
Studies w/ conclusions to surgical timing
 Comtet et al., 1988Retro3117–59 (25.4)93.5C5–6NACTI, GSW40–80 (NA)
 Ruch et al., 1995Retro1710–42 (21.8)100.0C5–T1EDT, CM, CTMVA, sportNA
 Songcharoen et al., 1996Retro2164–58 (26)96.2C5–T1EDT, CMMVA, CTI85–130 (NA)
 Samii et al., 1997Retro6516–49 (25)84.6C5–6EMGMVANA (124)
 Nagano, 1998Retro22115–49 (NA)NANADTNANA–250 (NA)
 Samii et al., 2003Retro446–48 (27)NAC5–T1NANANA (115)
 Ricardo, 2005Retro3216–44 (27.3)NAC5–T1NANANA (45)
 Kato et al., 2006Retro14813–55 (24.9)91.9C5–T1CT, MRIMVANA
 Liverneaux et al., 2006Prospect1017–43 (27.2)90.0C5–7NANA65–166 (140)
 Nath et al., 2006Retro400.83–54 (24.2)60.0C5–6EMGMVANA
 Ahmed-Labib et al., 2007Retro317–62 (32.7)80.6C5–T1EDT, MRI, CMMVA, sport, iatrogenicNA
 Venkatramani et al., 2008Retro1515–52 (35.6)93.3C5–7NAMVANA
 Jivan et al., 2009Retro2715–60 (28)96.2C5–6NAMVA30–100 (90)
 Secer et al., 2009Retro24219–30 (22)100.0C5–T1NAShrapnel/bullet injury30–65 (NA)
 Coulet et al., 2010Retro4015–54 (27)92.5C5–7NAInjuryNo graft
 Dong et al., 2010Prospect4014–59 (31)87.5C5–T1EMGMVA, work, fall, explosionNo graft
 Dolan et al., 2012Retro2118–53 (29.8)90.5C5–7NAMVA, fallNo graft
 Flores, 2011Retro10017–53 (35)71.0NAEMG, NCTMVA, fall, GSW, open sharp injuryNA
 Altaf et al., 2012Retro1313–32 (NA)100.0C5–T1NASportNA
 Khalifa et al., 2012Retro1817–74 (38)83.3C5–8EMGNANA
 Terzis & Barbitsioti, 2012Retro194NA (26)86.6C5–T1EMG, CM, x-ray neck/shoulderMVA, sport, GSWNA
 Gao et al., 2013Retro2516–45 (25.3)92.0C5–T1EMGMVA, CTINo graft
 Estrella & Favila, 2014Retro2017–47 (27.2)85.0C5–T1NATraumaNo graft
 Liu et al., 2014Retro3315–59 (26.5)97.0C5–T1EMGMVA, fall, explosionNA
 Xiao et al., 2014Retro3216–49 (33.7)93.8C5–T1EMGNANo graft
Studies w/o conclusions to surgical timing
 Stewart & Birch, 2001Retro585–76 (28)93.1C5–T1NAGSWNA
 Dubuisson & Kline, 2002Retro995–70 (37)80.8C5–T1CM, MRI, EMGMVA, fall, sport, iatrogenic, GSW, laceration61 (NA)
 Matsuyama et al., 2002Retro165–62 (32.9)62.5C5–T1MRI, EMG, NCT, CMMVA, iatrogenic, lacerationNA
 Xu et al., 2002Prospect1517–40 (28.9)86.7C5–T1EMGMVANo graft
 Teboul et al., 2004Retro3215–66 (28)84.4C5–7NANANA
 Battiston et al., 2006Retro1419–55 (35)78.6C5–T1NAMVANA
 Moor et al., 2010Retro1319–66 (37)76.9AxillaryEMGMVA, fall, sport, iatrogenic60–115 (88)
 Zyaei & Saied, 2010Prospect1016–29 (24.3)100.0C5–6MRI, EDTTraumaNo graft
 Goubier et al., 2011Retro1116–51 (29)100.0C5–6MRIMVANA
 Lin et al., 2011Retro1018–44 (27.2)90.0C5–T1EMGMVANA
 Ray et al., 2011Retro2917–68 (37)75.9C4–7EMG, NCTMVANA
 Socolovsky et al., 2011Retro34NA (23.9)94.1C5–T1EMG, NCT, MRINA100–220 (NA)
 Sokki et al., 2012Prospect3018–55 (32)86.7NAEMG, MRINANA
 Ren et al., 2013Prospect1117–56 (32.5)81.2C5–6EMG, MRIMVA, fallNo graft
 Tu et al., 2014Prospect4016–40 (26.8)90.0C5–T1EMG, NCT, MRIMVA, fallNA
 Barthel et al., 2014Retro29NA (30.2)96.6C5–7NAMVA, fallNA
 Socolovsky et al., 2014Retro58NA (30.5)96.6C5–7NCT, EMG, MRITrauma20–150 (NA)
 Souza et al., 2014Retro2018–42 (28)100.0C5–6EMG, MRIMVANA

CM = cervical myelography; CTI = compression or traction injury no other way specified; DT = diagnostic testing no other way specified; EDT = electrodiagnostic testing no other way specified; EMG = electromyography; GSW = gunshot wound; MVA = motor vehicle accident; NA = not available; NCT = nerve conduction test; Prospect = prospective; Pts = patients; Retro = retrospective.

Outcomes in Motor Function Assessed by MRC Grade

All studies that assessed Medical Research Council (MRC) muscle grade outcomes found a significant20,23,31,41,49,57,68,78,83 or nonsignificant4,19,61,64,67,91,93 improved recovery after early operation versus late operation (Table 2). Twelve studies dichotomized both surgical delay and MRC grade outcomes,4,23,31,43,49,50,57,67,68,78,91,93 whereas 3 groups dichotomized surgical delay20,41,83 or MRC grade outcome only.19,61,64 Several studies investigated if operations performed even earlier than 6 months are beneficial for motor outcome; cutoff points were 2 months,41 3 months,4,57,78,91 and 4 months.49,83 All studies showed better results for operations performed even earlier than 6 months after injury. However, only Liu et al.,49 Altaf et al.,4 and Jivan et al.41 were able to show statistical significance.

TABLE 2.

Surgical outcome in relation to timing

Authors & YearMos of Delay (mean)Op TypeTiming Outcome (mos)Outcome MeasureStatistical Significance*Years of FU (mean)
Outcomes in % above useful MRC values
 Songcharoen et al., 19961–12 (6.0)NT, NG<3: 83%, 3–6: 78.8%, 6–9: 74.6%, 9–12: 38.3%≥ MRC grade 3Yes2–9 (6)
 Samii et al., 19972–14 (8.0)NT, NG<6: 61%, 7–12: 40%, >12: 12.5%≥ MRC grade 3Yes0.75–14.6 (4.4)
 Nagano, 19980–25 (NA)NT, NG0–3: 83.0%, 35.1%; 4–6: 74.4%, 24.4%; 7–9: 52.4%, 23.8%; 10–12: 22.0%, 0%; 13–25: 20.0%, 0%≥ MRC grade 3, ≥ MRC grade 4Yes2–38.2 (NA)
 Samii et al., 20033–24 (7.8)NT, NG<6: 71%, 6–12: 43%; >12: 0%≥ MRC grade 3NA1.9–7.3 (3)
 Liverneaux et al., 20062–12 (6.6)NT, NGAll 100%≥ MRC grade 4No0.7–2 (1.3)
 Venkatramani et al., 20082–6 (NA)NT, NG<3: 87.5%, >3: 85.7%≥ MRC grade 3No1–3 (1.3)
 Dong et al., 20101–21.5 (4.6)NT<6: 90.6%, 6–12: 75.0%, >12: 25.0%≥ MRC grade 3Yes0.9–3.9 (2.4)
 Altaf et al., 2012NA–5 (NA)NA<3: 100%, >5: 0%≥ MRC grade 4NANA
 Khalifa et al., 201212–36 (18)NT, NG>12: 67%≥ MRC grade 3NA1–6 (1.4)
 Gao et al., 2013NANT<6: 73.3%, >6: 30%≥ MRC grade 3Yes3–8 (5.6)
 Liu et al., 20140.7–17 (NA)NT, NG<4: 96%, >4: 43%≥ MRC grade 3Yes4–17 (7)
 Xiao et al., 20141–12 (5.1)NT<6: 82.6%, >6: 57.1%≥ MRC grade 3No2–8.7 (4.2)
Outcomes in median/mean MRC
 Jivan et al., 20090–8 (2.0)NT, NG<0.5: 4.2, 0.5–2: 3.8, >2: 1.1Mean MRCYes§2–6 (3.4)
 Coulet et al., 20103–12 (NA)NG<6: 3.7 (IC), 3.9 (UN); >6: 1.8 (IC), 3.3 (UN)Mean MRCYes1–7.6 (NA)
 Terzis & Barbitsioti, 20120–NA (14.6)NT, NG, N<4: 3.66, 4–8: 3.33, >8: 2.66Median MRCYes**NA (4.5)
Mean delay for useful MRC values
 Comtet et al., 19883–24 (7.3)NT, NG, N≥ MRC grade 3: 6.1 mos, < MRC grade 3: 11 mosMean delayNo2–13 (6.5)
 Ricardo, 20052–15 (NA)NT, NG≥ MRC grade 3: 4.3 mos, < MRC grade 3: 6.9 mosMean delayNANA (6.7)
 Nath et al., 20062–9 (5.0)NT, NGMRC grade 4: 4.8 mos, < MRC grade 4: 8.5 mosMean delayNA>1 (NA)
Other used outcome values
 Ruch et al., 19953–12 (6.0)NT, NG<5: 75.0%, >5: 22.2%Good or excellent††NA2.5–10 (5)
 Kato et al., 20060–43.6 (3.6)NT, NG<1: 56.7%/25.0%, 2.6 (VAS); 1–3: 39.3%/39.3%, 3.7 (VAS); 3–6: 48.1%/25.9%, 4.0 (VAS); >6: 13.6%/50.0%, 5.3 (VAS)Good/fair,‡‡ VASNA3–16 (8.0)
 Ahmed-Labib et al., 20070–23 (7.5)NT, NG<6: better, >6: worseDASH + SF-36Yes0.9–7.25 (3.6)
 Secer et al., 20091.5–10 (NA)NG<4: 44.97%/46.31%, 4–6: 38.33%/50%, 6–8: 28.57%/57.14%, 8–10: 14.29%/66.67%Good/fair§§No0.5–3.25 (1.7)
 Dolan et al., 20120.2–13 (6.6)NT<6: better, >6: worseDASH + SF-36Yes12–82 (42.9)
 Flores, 20113–11 (6.5)NT, NG, N<6: betterAFRS¶¶Yes1.3–4.6 (2.7)
 Estrella & Favila, 20140.2–11 (5.9)NT<6: 88.07°, 63.85°; >6: 77.14°, 62.86°ROMNo1–5.6 (2.4)

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.

All studies considered p < 0.05 as statistically significant.

Between the group operated < 6 months and > 12 months.

Spearman rank correlation and < 6 vs > 6 months.

Both < 0.5 and 0.5–2 months compared to > 2 months.

Only in IC group.

Between < 4 and > 8 months’ delay.

Good is being able to hold 0.5- to 3.0-kg weights in elbow flexed 90°; excellent result is 3 to 8 kg (Nagano).

Good is restoration of functional active movement in at least 1 axis or joint; fair is nerve regeneration proven by clinical 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 by number of grades.

Whereas Samii et al.67 showed no useful recovery in operations performed after 12 months and Altaf et al.4 even reported no useful recoveries after 5 months’ delay, Liverneaux et al.50 and Khalifa et al.43 showed that even after delays of (more than) 12 months, good results can be obtained. They report recoveries to MRC grades as good as MRC grade 4. Khalifa et al.43 suggest that following their results, surgeons should not be discouraged to perform nerve transfers and grafts after delays as long as 24 months.

Effect of Time to Surgery on Other Outcomes

All 7 studies suggested that earlier operations resulted in better outcomes, yet only 3 showed statistically significant findings (Table 2).1,22,27 Two studies examined patient-reported outcomes using the Disability of the Arm, Shoulder and Hand questionnaire (DASH) score and the 36-Item Short-Form Health Survey (SF-36) and concluded that patients operated on within 6 months of their injury were more satisfied with their surgical outcome.1,22 Ahmed-Labib et al.1 even showed that DASH and SF-36 scores worsened with each additional month of delay. Ruch et al.,66 Secer et al.,69 and Kato et al.42 each used a separate form of excellent/good/fair/poor results as an outcome measure, and although none reported a statistical significance, they all show better results in groups with earlier surgery when looking at absolute numbers.42,66,69 Ruch et al.66 demonstrated best results in patients who received surgery within 5 months, Kato et al.42 within 1 month, and Secer et al.69 within 4 months. Kato et al.42 also showed that patients who were operated on sooner have lower visual analog scale (VAS) pain scores. Flores27 used an average final result of surgery (AFRS) score, an average of all MRC scores, to show that patients who were operated on within 6 months have significantly better outcomes. Finally, Estrella and Favila26 looked at the influence of timing on range of motion and did not find statistically significant differences, yet absolute values (88.07° and 77.14° of elbow flexion ≤ 6 months vs > 6 months, respectively) showed that patients have greater mobility when operated on earlier than 6 months.

Studies Not Reporting Effect of Timing of Surgery on Outcome

Eighteen studies did not explicitly report the effect of timing on outcome (Table 3). Eleven studies showed higher percentages of useful (≥ MRC grade 3) motor outcome in patients operated on within 6 months, and all showed a higher percentage of good functional recovery (MRC grade 4 or higher).5,24,35,52,62,74,76,77,82,94,95 Two studies showed better outcomes in patients operated on after 6 months.48,80 Ren et al.63 showed functional recovery in all patients regardless of preoperative delay, but all 6 patients who were operated on within 6 months recovered to MRC grade 4 or higher, unlike those with longer delays to surgery, of whom only 3 of 5 recovered to that level. A median of 87.3% (IQR 78.6%–98.2%) of patients operated on within 6 months recovered to an MRC grade of 3 or higher, compared with 66.7% (IQR 50.0%–96.4%) of those who had longer delays to surgery. Two-thirds of patients operated on within 6 months after injury even recovered to an MRC grade of 4 or higher, while less than half of patients operated on after 6 months recovered to this level.

TABLE 3.

Summary of outcomes in studies without conclusions

Timing Outcome (mos)
Authors & YearMos of Delay (mean)Op Type≥ MRC Grade 3≥ MRC Grade 4Years of FU (mean)
Stewart & Birch, 20010–36 (4)NT, NG, N≤6: 81.4%≤6: 23.3%>2 (NA)
>6: 100.0%>6: 50.0%  
Dubuisson & Kline, 20020 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., 20020–48 (NA)NT, NG≤6: 88.9%≤6: 55.5%0.5–5 (NA)
>6: 66.7%>6: 50.0%  
Xu et al., 20020.5–12 (5)NT≤6: 77.7%≤6: 44.4%NA
>6: 50.0%>6: 0.0%  
Teboul et al., 20041.5–75 (9)NT, NG≤6: 82.4%≤6: 70.6%0.8–6.2 (2.6)
>6: 66.7%>6: 53.3%  
Battiston et al., 20060–2 (NA)NT, NG<6: 92.9%<6: 92.9%1.2–8 (4)
Moor et al., 20108–20 (11.25)NT, NG>6: 100%>6: 100%>2 (NA)
Zyaei & Saied, 20105–9 (7)NT≤6: 100%≤6: 100%1 (1)
>6: 75%>6: 25%  
Goubier et al., 20112–9 (5)NT, NG≤6: 100%≤6: 88.9%1.5–2.3 (2)
>6: 0%>6: 0%  
Lin et al., 20113–9 (5.7)NT, NG≤6: 66.7%≤6: 33.3%2.5–4.4 (3.5)
>6: 100%>6: 50%  
Ray et al., 20110–11 (4.9)NT, NG≤6: 100%≤6: 95.0%0.7–5.7 (1.6)
>6: 85.7%>6: 42.9%  
Socolovsky et al., 20112–24 (NA)NT, NG≤6: 66.7%≤6: 36.7%>2 (NA)
>6: 11.8%>6: 5.9%  
Sokki et al., 20123–18 (NA)NT, NG≤6: 57.1 %≤6: 35.7%1 (1)
>6: 50%>6: 10%  
Ren et al., 20134–12 (6.7)NT≤6: 100%≤6: 100%1.3–3 (NA)
>6: 100%>6: 60%  
Tu et al., 20142–5 (NA)NT, NG≤6: 90%≤6: 62.5%4.5–8 (6)
Barthel et al., 20142–23 (NA)NT, NG≤6: 90%≤6: 75%1.3–7.8 (NA)
>6: 66.7%>6: 66.7%  
Socolovsky et al., 20141–12 (7.3)NT, NG≤6: 85.7%≤6: 57.1%1–6.3 (2.4)
>6: 50%>6: 50%  
Souza et al., 20147–15 (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%).

Individual-Level Patient Data

Among the studies that reported individual patient–level data, timing of operation and motor outcome were 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 patients 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 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 percentage of unsuccessful recoveries when the delay to surgery is greater than 6 months, and an even greater likelihood 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 recovered to ≥ MRC grade 3, the median delay to surgery was 4 months (IQR 3–6 months), compared to a median delay of 7 months (IQR 5–11 months) in patients with nonuseful recovery (Fig. 3).

TABLE 4.

Distribution of surgical delay among levels of injury

Delay (mos)All PtsC5–6C5–7C5–T1Infraclavicular
0–3156 (27.4%)27 (16.4%)27 (28.4%)51 (42.5%)33 (52.4%)
3–6217 (38.1%)73 (44.2%)36 (37.9%)47 (39.2%)9 (14.3%)
6–9115 (20.2%)42 (25.5%)22 (23.2%)10 (8.3%)13 (20.6%)
9–1253 (9.3%)18 (10.9%)7 (7.4%)10 (8.3%)4 (6.3%)
>1228 (4.9%)5 (3.0%)3 (3.2%)2 (1.7%)4 (6.3%)
FIG. 2.
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).

FIG. 3.
FIG. 3.

Box-and-whisker plot showing median delay in months for muscle grade.

Discussion

The results of this systematic review indicate that the 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 shorter delays, most only demonstrated this for a cutoff point at 6 months. To date, no randomized controlled trials or prospective cohort studies have been performed to assess optimal timing for brachial plexus lesions. Only retrospective, 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 Kim et al.44 have performed a very large number of brachial 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.

Nonmotor Outcome Values

Although better motor function is most frequently described as an advantage of earlier operations, other outcomes are also affected. Kato et al.42 showed that postoperative median VAS scores were the lowest among 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 argument for earlier restoration. Furthermore, many authors argue that earlier operations are easier to perform because of extensive fibrosis that may occur in late exploration.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 comparably less favorable outcomes.44,45,89 Worse outcomes are noted when complete lesions occur.25,89 This is consistent 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 differently 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 nerve grafts and transfers. Exact treatment strategies for each plexus injury go beyond the scope of this paper, but differences in motor outcome have been shown to depend on the donor nerves that are used, especially when comparing intra- and extraplexal donors.25,32,36,60,83,89 Intraplexal donors generally give better results, which is why many authors prefer using them. This may be due to a larger number of axons in the donor.25 Ali et al.2 demonstrated by systematic review that there is a significant difference when comparing nerve transfers to nerve graft techniques or a combination of both in upper brachial plexus palsy, favoring the former. The length of the graft also affects outcomes, with longer grafts typically yielding worse results.8,18,60,64,67,86 Narakas and Hentz60 and Chuang et al.18 found that grafts longer than 10 cm were predictive of worse outcome. Samii et al.67 reported statistically better outcome in patients with grafts 12 cm or shorter compared to grafts longer than 12 cm, while Terzis and Kostas86 found a cutoff point at 7-cm length. Aside from surgical management, postoperative rehabilitation also plays a role in the extent of functional outcome.12,15,37,74 Socolovsky et al.74 used a 4-point scale to assess the quality of the rehabilitation program their patients were enrolled in and showed a statistically significant better motor outcome in patients who receive superior rehabilitation.

Late Referrals

A recurring barrier to optimal treatment for these patients is a delay in referral.1,22,24,28,38,45,54,70,79 Dolan et al.22 reported that late referral was the reason for delayed surgery in every one of their patients operated on at least 6 months after the injury. These patients made up 75% of all patients who did not reach functional recovery.22 In the patient group reported by Souza et al.79 no one was operated on before 6 months, all due to late referrals. Dubuisson even reported an average referral time of 6.8 months after injury.24 Concomitant injuries in multitrauma patients can also lead to long delays.38,69 Even though some authors argue that patients do not benefit from late repairs,3,41,59 others encourage surgeons to still perform nerve restoration in some patients.10,43 Although many patients operated on after more than 12 months will need secondary operations, such as tendon transfers, muscle transfers, or arthrodesis to restore upper extremity function,17,89 pain in preganglionic ruptures can be relieved by nerve restoration even after longer periods of time.10

Spontaneous Recovery

Spontaneous recovery can occur in patients, which means that some early operations may be unnecessary.24,38,45,65,73,92 Few studies report on exact numbers of spontaneous recovery after brachial plexus injury. Kline45 reported from personal experience that spontaneous recovery occurred in 40% of patients presenting with a lesion in C5–6, but decreased to 15%–16% when C7 was also affected, and to 4%–5% in complete lesions. Hems,38 however, states that he rarely saw recovery of function after 3 or 4 months in cases of complete loss of function from the upper plexus. In the few cases that were managed conservatively, some recovery was noted in biceps and deltoid function after extended follow-up, but rarely in suprascapular nerve functions.38 Preoperative assessment plays a large role in predicting whether patients will show spontaneous recovery.73 The exact preoperative management of peripheral nerve injuries goes beyond the scope of this paper, but is discussed in a recent review of Simon et al.73

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.

Conclusions

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 appropriate. Regardless of the level of injury, recovery is improved in those operated on earlier, yet this must be considered with the potential for spontaneous recovery in mind.

Appendix

PubMed search (21-1-2017): ((“plexus brachialis injury”[Title/Abstract] OR “brachial plexus injury”[Title/Abstract] OR “plexus brachialis injuries”[Title/Abstract] OR “brachial plexus injuries”[Title/Abstract] OR “brachial plexus trauma”[Title/Abstract] OR “brachial plexus lesion”[Title/Abstract] OR “brachial plexus lesions”[Title/Abstract] OR “brachial plexus avulsion”[Title/Abstract] OR “plexus brachialis palsy”[Title/Abstract] OR “brachial plexus palsy”[Title/Abstract] OR “brachial plexus palsies”[Title/Abstract] OR “brachial plexus paralysis”[Title/Abstract] OR “brachial plexus disruption”[Title/Abstract] OR “brachial plexus dissection”[Title/Abstract] OR “Erb’s palsy”[Title/Abstract] OR “Erb’s palsies”[Title/Abstract] OR “Erb’s paralysis”[Title/Abstract] OR “Erb-Duchenne palsy”[Title/Abstract] OR “Erb-Duchenne paralysis”[Title/Abstract] OR “Klumpke’s palsy”[Title/Abstract] OR “Brachial Plexus/injuries”[Mesh:NoExp] OR “Brachial Plexus Neuropathies”[Mesh:NoExp]) AND (“timing”[Title/Abstract] OR “time to”[Title/Abstract] OR “time management”[Title/Abstract] OR delay*[Title/Abstract] OR “early”[Title/Abstract] OR “management”[Title/Abstract] OR “late”[Title/Abstract] OR “later”[Title/Abstract]) AND (“surgery”[Title/Abstract] OR reconstruct*[Title/Abstract] OR “operation”[Title/Abstract] OR “operate”[Title/Abstract] OR “treatment”[Title/Abstract] OR explor*[Title/Abstract] OR “surgical repair”[Title/Abstract] OR “reconstructive surgery”[Title/Abstract] OR “Brachial Plexus/surgery”[Mesh:NoExp] OR “Brachial Plexus Neuropathies/surgery”[Mesh:NoExp]))

Embase search (21-1-2017): ((‘plexus brachialis injury’:ti,ab OR ‘brachial plexus injury’:ti,ab OR ‘plexus brachialis injuries’:ti,ab OR ‘brachial plexus injuries’:ti,ab OR ‘brachial plexus trauma’:ti,ab OR ‘brachial plexus lesion’:ti,ab OR ‘brachial plexus lesions’:ti,ab OR ‘brachial plexus avulsion’:ti,ab OR ‘plexus brachialis palsy’:ti,ab OR ‘brachial plexus palsy’:ti,ab OR ‘brachial plexus palsies’:ti,ab OR ‘brachial plexus paralysis’:ti,ab OR ‘brachial plexus disruption’:ti,ab OR ‘brachial plexus dissection’:ti,ab OR ‘Erb/s palsy’:ti,ab OR ‘Erb/s palsies’:ti,ab OR ‘Erb/s paralysis’:ti,ab OR ‘Erb-Duchenne palsy’:ti,ab OR ‘Erb-Duchenne paralysis’:ti,ab OR ‘Klumpke/s palsy’:ti,ab OR ‘Brachial plexus injury’/exp OR ‘Brachial plexus neuropathy’/exp) AND (‘timing’:ti,ab OR ‘time to’:ti,ab OR ‘time management’:ti,ab OR delay*:ti,ab OR ‘early’:ti,ab OR ‘management’:ti,ab OR ‘late’:ti,ab OR ‘later’:ti,ab) AND (‘surgery’:ti,ab OR reconstruct*:ti,ab OR ‘operation’:ti,ab OR ‘operate’:ti,ab OR ‘treatment’:ti,ab OR explor*:ti,ab OR ‘surgical repair’:ti,ab OR ‘reconstructive surgery’:ti,ab) AND ([article]/lim) AND ([Embase]/lim))

Disclosures

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

Author Contributions

Conception and design: Martin, Broekman. Acquisition of data: Martin, Senders, DiRisio. Analysis and interpretation of data: Martin, Senders, DiRisio, Broekman. Drafting the article: Martin, Senders, DiRisio. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Administrative/technical/material support: Smith, Broekman. Study supervision: Smith, Broekman.

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Illustration from Ferrareze Nunes et al. (pp 1304–1314). Copyright Juan C. Fernandez-Miranda. Published with permission.

  • View in gallery

    Flowchart depicting study selection.

  • View in gallery

    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).

  • View in gallery

    Box-and-whisker plot showing median delay in months for muscle grade.

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