timing of surgery in traumatic brachial plexus injury: a ... · traumatic brachial plexus injuries....

LITERATURE REVIEWJ Neurosurg 130:1333–1345, 2019

TraumaTic brachial plexus injury is a rare yet dev-astating event that is most commonly noted in young, active adult males involved in traffic ac-

cidents.45,54,59 Although the injury itself is not fatal, life-long disability usually follows and can be difficult to re-verse.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 sta-bility.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 pe-ripheral nerve surgeons.7

While some authors advocate for very early repair of 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.

Timing of surgery in traumatic brachial plexus injury: a systematic reviewEnrico 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 collect-ed 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 de-creased 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.JNS172068KEYWORDS brachial plexus injury; surgery; timing; outcome; systematic review; trauma; peripheral nerve

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E. Martin et al.

J Neurosurg Volume 130 • April 20191334

that long delays can still result in good functional recov-eries.50,58,70 Many groups recommend waiting at least 3 months before surgery1,14,18,19,24,44,46,59,67,72 because sponta-neous recovery might occur.21 Many groups also discour-age 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.

MethodsLiterature Search

A systematic search was performed in both PubMed and Embase databases according to the PRISMA (Pre-ferred 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 tim-ing 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 bra-chial 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 SynthesisData extracted from each study included year of pub-

lication, study type, number of patients, range and me-dian age of patients, gender percentages, levels of bra-chial 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 stud-ies did not directly investigate the influence of surgical timing on outcome, but did provide individual-level pa-tient data on both items. Their findings have been summa-rized 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 surgi-cal delay. Level of injury groups were made, distinguish-ing 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).

ResultsAfter 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 stud-ies were selected for qualitative synthesis after full-text screening (Fig. 1).

Study CharacteristicsThe majority of studies included in our study were ret-

rospective observational studies, and only 7 of the includ-ed 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 neu-rolysis, 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).

Outcomes in Motor Function Assessed by MRC GradeAll 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 recov-ery 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 per-formed 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 op-erations 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.

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 per-form nerve transfers and grafts after delays as long as 24 months.

Effect of Time to Surgery on Other OutcomesAll 7 studies suggested that earlier operations resulted

in better outcomes, yet only 3 showed statistically sig-nificant findings (Table 2).1,22,27 Two studies examined pa-


J Neurosurg Volume 130 • April 2019 1335

E. Martin et al.

tient-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 conclud-ed that patients operated on within 6 months of their in-jury 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 sepa-rate form of excellent/good/fair/poor results as an outcome measure, and although none reported a statistical signifi-cance, 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 vi-sual analog scale (VAS) pain scores. Flores27 used an av-erage 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. Fi-nally, Estrella and Favila26 looked at the influence of tim-ing on range of motion and did not find statistically sig-nificant 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 re-gardless 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 re-covered to an MRC grade of 3 or higher, compared with 66.7% (IQR 50.0%–96.4%) of those who had longer de-lays 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.

Individual-Level Patient DataAmong the studies that reported individual patient–

level data, timing of operation and motor outcome were

FIG. 1. Flowchart depicting study selection.


E. Martin et al.


TABL

E 1.

Dem

ogra

phic

s of t

he re

view

ed st

udie

s

Auth

ors &

Yea

rSt

udy

Type

No. o

f Pt

sAg

e Ran

ge in

Yr

s (me

an)

%

Male

Leve

l of

Lesio

nPr

eop A

sses

smen

tCa

use o

f Injur

yGr

aft L

engt

h in

mm (m

ean)

Stud

ies w

/ con

clusio

ns to

surg

ical ti

ming

Co

mtet

et al.

, 198

8Re

tro31

17–5

9 (25

.4)93

.5C5

–6NA

CTI, G

SW40

–80 (

NA)

Ru

ch et

al., 1

995

Retro

1710

–42 (

21.8)

100.0

C5–T

1ED

T, CM

, CT

MVA

, spo

rtNA

So

ngch

aroe

n et a

l., 19

96Re

tro21

64–

58 (2

6)96

.2C5

–T1

EDT,

CMM

VA, C

TI85

–130

(NA)

Sa

mii e

t al.,

1997

Retro

6516

–49 (

25)

84.6

C5–6

EMG

MVA

NA (1

24)

Na

gano

, 199

8Re

tro22

115

–49 (

NA)

NANA

DTNA

NA–2

50 (N

A)

Sami

i et a

l., 20

03Re

tro44

6–48

(27)

NAC5

–T1

NANA

NA (1

15)

Ri

card

o, 20

05Re

tro32

16–4

4 (27

.3)NA

C5–T

1NA

NANA

(45)

Ka

to et

al., 2

006

Retro

148

13–5

5 (24

.9)91

.9C5

–T1

CT, M

RIM

VANA

Liv

erne

aux e

t al.,

2006

Pros

pect

1017

–43 (

27.2)

90.0

C5–7

NANA

65–1

66 (1

40)

Na

th et

al., 2

006

Retro

400.

83–5

4 (24

.2)60

.0C5

–6EM

GM

VANA

Ah

med-

Labib

et al

., 200

7Re

tro31

7–62

(32.7

)80

.6C5

–T1

EDT,

MRI

, CM

MVA

, spo

rt, ia

troge

nicNA

Ve

nkatr

aman

i et a

l., 20

08Re

tro15

15–5

2 (35

.6)93

.3C5

–7NA

MVA

NA

Jivan

et al

., 200

9Re

tro27

15–6

0 (28

)96

.2C5

–6NA

MVA

30–1

00 (9

0)

Sece

r et a

l., 20

09Re

tro24

219

–30 (

22)

100.0

C5–T

1NA

Shra

pnel/

bulle

t injur

y30

–65 (

NA)

Co

ulet e

t al.,

2010

Retro

4015

–54 (

27)

92.5

C5–7

NAInj

ury

No gr

aft

Do

ng et

al., 2

010

Pros

pect

4014

–59 (

31)

87.5

C5–T

1EM

GM

VA, w

ork,

fall,

explo

sion

No gr

aft

Do

lan et

al., 2

012

Retro

2118

–53 (

29.8)

90.5

C5–7

NAM

VA, fa

llNo

graf

t

Flore

s, 20

11Re

tro10

017

–53 (

35)

71.0

NAEM

G, N

CTM

VA, fa

ll, GS

W, o

pen s

harp

injur

yNA

Al

taf e

t al.,

2012

Retro

1313

–32 (

NA)

100.0

C5–T

1NA

Spor

tNA

Kh

alifa

et al.

, 201

2Re

tro18

17–7

4 (38

)83

.3C5

–8EM

GNA

NA

Terz

is &

Barb

itsiot

i, 201

2Re

tro19

4NA

(26)

86.6

C5–T

1EM

G, C

M, x-

ray n

eck/s

hould

erM

VA, s

port,

GSW

NA

Gao e

t al.,

2013

Retro

2516

–45 (

25.3)

92.0

C5–T

1EM

GM

VA, C

TINo

graf

t

Estre

lla &

Fav

ila, 2

014

Retro

2017

–47 (

27.2)

85.0

C5–T

1NA

Trau

maNo

graf

t

Liu et

al., 2

014

Retro

3315

–59 (

26.5

)97

.0C5

–T1

EMG

MVA

, fall,

explo

sion

NA

Xiao

et al

., 201

4Re

tro32

16–4

9 (33

.7)93

.8C5

–T1

EMG

NANo

graf

tSt

udies

w/o

conc

lusion

s to s

urgic

al tim

ing

Stew

art &

Birc

h, 20

01Re

tro58

5–76

(28)

93.1

C5–T

1NA

GSW

NA

Dubu

isson

& K

line,

2002

Retro

995–

70 (3

7)80

.8C5

–T1

CM, M

RI, E

MG

MVA

, fall,

spor

t, iatr

ogen

ic, G

SW, la

cera

tion

61 (N

A)

Mats

uyam

a et a

l., 20

02Re

tro16

5–62

(32.

9)62

.5C5

–T1

MRI

, EM

G, N

CT, C

MM

VA, ia

troge

nic, la

cera

tion

NA

Xu et

al., 2

002

Pros

pect

1517

–40 (

28.9)

86.7

C5–T

1EM

GM

VANo

graf

t

Tebo

ul et

al., 2

004

Retro

3215

–66 (

28)

84.4

C5–7

NANA

NA

Battis

ton et

al., 2

006

Retro

1419

–55 (

35)

78.6

C5–T

1NA

MVA

NA

Moo

r et a

l., 20

10Re

tro13

19–6

6 (37

)76

.9Ax

illary

EMG

MVA

, fall,

spor

t, iatr

ogen

ic60

–115

(88)

Zy

aei &

Saie

d, 20

10Pr

ospe

ct10

16–2

9 (24

.3)10

0.0C5

–6M

RI, E

DTTr

auma

No gr

aft

Go

ubier

et al

., 201

1Re

tro11

16–5

1 (29

)10

0.0C5

–6M

RIM

VANA

CONT

INUE

D ON

PAG

E 13

37 »



E. Martin et al.

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-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 per-centage 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 like-lihood of unsuccessful recovery in patients with longer delays (Fig. 2B–E). The best results are seen in upper bra-chial 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 non-useful recovery (Fig. 3).

DiscussionThe 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 as-sess optimal timing for brachial plexus lesions. Only ret-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 Kim et al.44 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 sta-tistically 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 ValuesAlthough better motor function is most frequently de-

scribed as an advantage of earlier operations, other out-comes are also affected. Kato et al.42 showed that post-operative median VAS scores were the lowest among TA

BLE

1. De

mog

raph

ics o

f the

revi

ewed

stud

ies

Auth

ors &

Yea

rSt

udy

Type

No. o

f Pt

sAg

e Ran

ge in

Yr

s (me

an)

%

Male

Leve

l of

Lesio

nPr

eop A

sses

smen

tCa

use o

f Injur

yGr

aft L

engt

h in

mm (m

ean)

Stud

ies w

/o co

nclus

ions t

o sur

gical

timing

(cont

inued

)

Lin

et al

., 201

1Re

tro10

18–4

4 (27

.2)90

.0C5

–T1

EMG

MVA

NA

Ra

y et a

l., 20

11Re

tro29

17–6

8 (37

)75

.9C4

–7EM

G, N

CTM

VANA

Soco

lovsk

y et a

l., 20

11Re

tro34

NA (2

3.9)

94.1

C5–T

1EM

G, N

CT, M

RINA

100–

220 (

NA)

Sokk

i et a

l., 20

12Pr

ospe

ct30

18–5

5 (32

)86

.7NA

EMG,

MRI

NANA

Ren e

t al.,

2013

Pros

pect

1117

–56 (

32.5

)81

.2C5

–6EM

G, M

RIM

VA, fa

llNo

graf

t

Tu

et al

., 201

4Pr

ospe

ct40

16–4

0 (26

.8)90

.0C5

–T1

EMG,

NCT

, MRI

MVA

, fall

NA

Ba

rthel

et al.

, 201

4Re

tro29

NA (3

0.2)

96.6

C5–7

NAM

VA, fa

llNA

Soco

lovsk

y et a

l., 20

14Re

tro58

NA (3

0.5)

96.6

C5–7

NCT,

EMG,

MRI

Trau

ma20

–150

(NA)

Souz

a et a

l., 20

14Re

tro20

18–4

2 (28

)10

0.0C5

–6EM

G, M

RIM

VANA

CM =

cerv

ical m

yelog

raph

y; CT

I = co

mpre

ssion

or tr

actio

n inju

ry no

othe

r way

spec

ified;

DT =

diag

nosti

c tes

ting n

o oth

er w

ay sp

ecifie

d; ED

T =

electr

odiag

nosti

c tes

ting n

o oth

er w

ay sp

ecifie

d; EM

G =

electr

omyo

grap

hy;

GSW

= gu

nsho

t wou

nd; M

VA =

moto

r veh

icle a

ccide

nt; N

A =

not a

vaila

ble; N

CT =

nerv

e con

ducti

on te

st; P

rosp

ect =

pros

pecti

ve; P

ts =

patie

nts;

Retro

= re

trosp

ectiv

e.

» CON

TINU

ED F

ROM

PAGE

133

6


E. Martin et al.


TABL

E 2.

Surg

ical

outc

ome i

n re

latio

n to

tim

ing

Auth

ors &

Yea

rM

os of

Dela

y (m

ean)

Op Ty

peTi

ming

Outc

ome (

mos)

Outco

me M

easu

reSt

atisti

cal

Sign

ifican

ce*

Year

s of F

U (m

ean)

Outco

mes i

n % ab

ove u

sefu

l MRC

value

s

Song

char

oen e

t al.,

1996

1–12

(6.0)

NT, N

G<3

: 83%

, 3–6

: 78.

8%, 6

–9: 7

4.6%

, 9–1

2: 38

.3%≥

MRC

grad

e 3Ye

s2–

9 (6)

Sa

mii e

t al.,

1997

2–14

(8.0)

NT, N

G<6

: 61%

, 7–1

2: 40

%, >

12: 1

2.5%

≥ M

RC gr

ade 3

Yes†

0.75–

14.6

(4.4)

Na

gano

, 199

80–

25 (N

A)NT

, NG

0–3:

83.0%

, 35.1

%; 4

–6: 7

4.4%

, 24.4

%; 7

–9: 5

2.4%

, 23.

8%;

10–1

2: 22

.0%, 0

%; 1

3–25

: 20.0

%, 0

%≥

MRC

grad

e 3,

≥ M

RC gr

ade 4

Yes‡

2–38

.2 (N

A)

Sa

mii e

t al.,

2003

3–24

(7.8)

NT, N

G<6

: 71%

, 6–1

2: 43

%; >

12: 0

%≥

MRC

grad

e 3NA

1.9–7

.3 (3

)

Liver

neau

x et a

l., 20

062–

12 (6

.6)NT

, NG

All 1

00%

≥ M

RC gr

ade 4

No0.7

–2 (1

.3)

Venk

atram

ani e

t al.,

2008

2–6 (

NA)

NT, N

G<3

: 87.5

%, >

3: 85

.7%≥

MRC

grad

e 3No

1–3 (

1.3)

Do

ng et

al., 2

010

1–21

.5 (4

.6)NT

<6: 9

0.6%

, 6–1

2: 75

.0%, >

12: 2

5.0%

≥ M

RC gr

ade 3

Yes

0.9–3

.9 (2

.4)

Alta

f et a

l., 20

12NA

–5 (N

A)NA

<3: 1

00%

, >5:

0%≥

MRC

grad

e 4NA

NA

Khali

fa et

al., 2

012

12–3

6 (18

)NT

, NG

>12:

67%

≥ M

RC gr

ade 3

NA1–

6 (1.4

)

Gao e

t al.,

2013

NANT

<6: 7

3.3%

, >6:

30%

≥ M

RC gr

ade 3

Yes

3–8 (

5.6)

Liu

et al

., 201

40.7

–17 (

NA)

NT, N

G<4

: 96%

, >4:

43%

≥ M

RC gr

ade 3

Yes

4–17

(7)

Xi

ao et

al., 2

014

1–12

(5.1)

NT<6

: 82.

6%, >

6: 57

.1%≥

MRC

grad

e 3No

2–8.7

(4.2)

Outco

mes i

n med

ian/m

ean M

RC

Jivan

et al

., 200

90–

8 (2.0

)NT

, NG

<0.5:

4.2,

0.5–

2: 3.

8, >2

: 1.1

Mea

n MRC

Yes§

2–6 (

3.4)

Co

ulet e

t al.,

2010

3–12

(NA)

NG<6

: 3.7

(IC),

3.9 (

UN);

>6: 1

.8 (I

C), 3

.3 (U

N)M

ean M

RCYe

s¶1–

7.6 (N

A)

Terz

is &

Barb

itsiot

i, 201

20–

NA (1

4.6)

NT, N

G, N

<4: 3

.66,

4–8:

3.33

, >8:

2.66

Med

ian M

RCYe

s**

NA (4

.5)

Mea

n dela

y for

usef

ul M

RC va

lues

Co

mtet

et al.

, 198

83–

24 (7

.3)NT

, NG,

N≥

MRC

grad

e 3: 6

.1 mo

s, <

MRC

grad

e 3: 1

1 mos

Mea

n dela

yNo

2–13

(6.5

)

Rica

rdo,

2005

2–15

(NA)

NT, N

G≥

MRC

grad

e 3: 4

.3 m

os, <

MRC

grad

e 3: 6

.9 mo

sM

ean d

elay

NANA

(6.7)

Na

th et

al., 2

006

2–9 (

5.0)

NT, N

GM

RC gr

ade 4

: 4.8

mos

, < M

RC gr

ade 4

: 8.5

mos

Mea

n dela

yNA

>1 (N

A)Ot

her u

sed o

utcom

e valu

es

Ruch

et al

., 199

53–

12 (6

.0)NT

, NG

<5: 7

5.0%

, >5:

22.2

%Go

od or

exce

llent

††NA

2.5–

10 (5

)

Kato

et al.

, 200

60–

43.6

(3.6)

NT, N

G<1

: 56.7

%/2

5.0%

, 2.6

(VAS

); 1–

3: 39

.3%/3

9.3%

, 3.7

(VAS

); 3–

6: 48

.1%/2

5.9%

, 4.0

(VAS

); >6

: 13.

6%/5

0.0%

, 5.3

(VAS

)Go

od/fa

ir,‡‡ V

ASNA

3–16

(8.0)

Ah

med-

Labib

et al

., 200

70–

23 (7

.5)

NT, N

G<6

: bet

ter, >

6: wo

rse

DASH

+ S

F-36

Yes

0.9–7

.25 (

3.6)

Se

cer e

t al.,

2009

1.5–1

0 (NA

)NG

<4: 4

4.97%

/46.31

%, 4

–6: 3

8.33

%/5

0%, 6

–8: 2

8.57

%/57

.14%

, 8–

10: 1

4.29

%/6

6.67

%Go

od/fa

ir§§

No0.

5–3.

25 (1

.7)

Do

lan et

al., 2

012

0.2–

13 (6

.6)NT

<6: b

etter

, >6:

wors

eDA

SH +

SF-

36Ye

s12

–82 (

42.9)

Flo

res,

2011

3–11

(6.5

)NT

, NG,

N<6

: bet

terAF

RS¶¶

Yes

1.3–4

.6 (2

.7)

Estre

lla &

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ila, 2

014

0.2–

11 (5

.9)NT

<6: 8

8.07°,

63.8

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62.8

6°RO

MNo

1–5.

6 (2.4

)CO

NTIN

UED

ON P

AGE

1339

»



E. Martin et al.

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 be-cause 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 OutcomeIn 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 in-jury. There is heterogeneity in the presentation and man-agement 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 com-pared 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 mo-tor 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 with the results of our analysis. With the exception of in-fraclavicular 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 num-ber of good outcomes.1,89 Avulsions are managed differ-ently because they usually require other restoration tech-niques. Unfortunately, the presence of avulsion was poorly documented in most papers, and thus the relationship be-tween 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 TA

BLE

2. Su

rgic

al ou

tcom

e in

rela

tion

to ti

min

g

FU =

follo

w-up

; IC

= int

erco

stal n

erve

tran

sfer g

roup

; N =

neur

olysis

; NG

= ne

rve g

raft;

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nd >

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and <

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» CON

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ROM

PAGE

133

8


E. Martin et al.


differences in motor outcome have been shown to depend on the donor nerves that are used, especially when com-paring intra- and extraplexal donors.25,32,36,60,83,89 Intraplexal donors generally give better results, which is why many au-thors prefer using them. This may be due to a larger number of axons in the donor.25 Ali et al.2 demonstrated by system-atic review that there is a significant difference when com-paring nerve transfers to nerve graft techniques or a com-

bination 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

TABLE 3. Summary of outcomes in studies without conclusions

Authors & YearMos of Delay

(mean) Op TypeTiming Outcome (mos) Years of FU

(mean)≥ MRC Grade 3 ≥ MRC Grade 4

Stewart & Birch, 2001 0–36 (4) NT, NG, N ≤6: 81.4%>6: 100.0%

≤6: 23.3%>6: 50.0%

>2 (NA)

Dubuisson & Kline, 2002 0 to >24 (NA) NT, NG, N ≤6: 83.3%>6: 61.5%

≤6: 75.0%>6: 15.4%

1 to >3 (NA)

Matsuyama et al., 2002 0–48 (NA) NT, NG ≤6: 88.9%>6: 66.7%

≤6: 55.5%>6: 50.0%

0.5–5 (NA)

Xu et al., 2002 0.5–12 (5) NT ≤6: 77.7%>6: 50.0%

≤6: 44.4%>6: 0.0%

NA

Teboul et al., 2004 1.5–75 (9) NT, NG ≤6: 82.4%>6: 66.7%

≤6: 70.6%>6: 53.3%

0.8–6.2 (2.6)

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: 75%≤6: 100%>6: 25%

1 (1)

Goubier et al., 2011 2–9 (5) NT, NG ≤6: 100%>6: 0%

≤6: 88.9%>6: 0%

1.5–2.3 (2)

Lin et al., 2011 3–9 (5.7) NT, NG ≤6: 66.7%>6: 100%

≤6: 33.3%>6: 50%

2.5–4.4 (3.5)

Ray et al., 2011 0–11 (4.9) NT, NG ≤6: 100%>6: 85.7%

≤6: 95.0%>6: 42.9%

0.7–5.7 (1.6)

Socolovsky et al., 2011 2–24 (NA) NT, NG ≤6: 66.7%>6: 11.8%

≤6: 36.7%>6: 5.9%

>2 (NA)

Sokki et al., 2012 3–18 (NA) NT, NG ≤6: 57.1 %>6: 50%

≤6: 35.7%>6: 10%

1 (1)

Ren et al., 2013 4–12 (6.7) NT ≤6: 100%>6: 100%

≤6: 100%>6: 60%

1.3–3 (NA)

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: 66.7%≤6: 75%>6: 66.7%

1.3–7.8 (NA)

Socolovsky et al., 2014 1–12 (7.3) NT, NG ≤6: 85.7%>6: 50%

≤6: 57.1%>6: 50%

1–6.3 (2.4)

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%).

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%)



E. Martin et al.

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 pa-tients were enrolled in and showed a statistically significant better motor outcome in patients who receive superior re-habilitation.

Late ReferralsA recurring barrier to optimal treatment for these pa-

tients 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 sur-gery 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 oper-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 can also lead to long delays.38,69 Even though some authors argue that patients do not benefit from late repairs,3,41,59 oth-

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).


E. Martin et al.


ers 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 RecoverySpontaneous recovery can occur in patients, which

means that some early operations may be unneces-sary.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 re-covery occurred in 40% of patients presenting with a le-sion 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 af-ter 3 or 4 months in cases of complete loss of function from the upper plexus. In the few cases that were man-aged 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 manage-ment of peripheral nerve injuries goes beyond the scope of this paper, but is discussed in a recent review of Simon et al.73

LimitationsFurther limitations of this review include the heteroge-

neity 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 af-fecting 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 per-formed. Results of this study may be used as reference for future research, but clinicians will still need to take sev-eral other factors into consideration to make an appropri-ate 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.

ConclusionsIn 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-ate. 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.

AppendixPubMed search (21-1-2017): ((“plexus brachialis injury”[Title/

Abstract] OR “brachial plexus injury”[Title/Abstract] OR “plexus brachialis injuries”[Title/Abstract] OR “brachial plex-us 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 Plex-us 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]))

FIG. 3. Box-and-whisker plot showing median delay in months for muscle grade.



E. Martin et al.

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))

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DisclosuresThe authors report no conflict of interest concerning the materi-als or methods used in this study or the findings specified in this paper.

Author ContributionsConception and design: Martin, Broekman. Acquisition of data: Martin, Senders, DiRisio. Analysis and interpretation of data: Martin, Senders, DiRisio, Broekman. Drafting the article: Mar-tin, Senders, DiRisio. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Adminis-trative/technical/material support: Smith, Broekman. Study super-vision: Smith, Broekman.

CorrespondenceEnrico Martin: University Medical Center Utrecht, The Nether-lands. [email protected].


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