Clinical Rehabilitation2015, Vol. 29(1) 3 –13© The Author(s) 2014Reprints and permissions: sagepub.co.uk/journalsPermissions.navDOI: 10.1177/0269215514536411cre.sagepub.com

CLINICALREHABILITATION

IntroductionOver the last few decades, various interventions have evolved in an attempt to improve arm and hand function in individuals with spinal cord injury.1–3 Loss of arm and hand function is one of the most devastating consequences of tetraplegia and it has been shown to be the priority of recovery for this population. Even a small improvement in

Effects of training on upper limb function after cervical spinal cord injury: a systematic review

Xiao Lu1, Camilla R Battistuzzo2, Maryam Zoghi2 and Mary P Galea2

AbstractObjective: To summarize the evidence for the effectiveness of exercise training in promoting recovery of upper extremity function after cervical spinal cord injury.Data sources: Medline, Cochrane, CINAHL, EMBASE and PEDro were used to search the literature.Review methods: Two reviewers independently selected and summarized the included studies. Methodological quality of the selected articles was scored using the Downs and Black checklist.Results: A total of 16 studies were included, representing a total of 426 participants. Overall, the internal validity and reporting of the studies was fair to good, while power and external validity were poor. Interventions included exercise therapy, electrical stimulation, functional electrical stimulation, robotic training and repetitive transcranial magnetic stimulation. Most of the studies reported improvements in muscle strength, arm and hand function, activity of daily living or quality of life after intervention.Conclusions: Training including exercise therapy, electrical stimulation, functional electrical stimulation of the upper limb following cervical spinal cord injury leads to improvements in muscle strength, upper limb function and activity of daily living or quality of life. Further research is needed into the effects of repetitive transcranial magnetic stimulation and robotic training on upper limb function.

KeywordsSpinal cord injury, systematic review, training, upper limb

Received: 24 March 2013; accepted: 27 April 2014

1 Department of Rehabilitation, The First Affiliated Hospital of Nanjing Medical University, Nanjing, China

2 Physiotherapy Department, The University of Melbourne, Parkville, Victoria 3010, Australia

Corresponding author:Xiao Lu, Department of Rehabilitation, The First Affiliated Hospital of Nanjing Medical University, Nanjing, China. Email: luxiao1972@163.com

536411 CRE0010.1177/0269215514536411Clinical RehabilitationLu et al.research-article2014

Article

4 Clinical Rehabilitation 29(1)

arm and hand function may lead to increased inde-pendence in daily activities, improving independ-ence and quality of life.4,5

Interventions, such as tendon transfer surgery, implanted neuroprostheses and re-training of arm and hand function, are currently used to improve upper limb function.6,7 Among these methods, re-training is the most common as it is non-invasive and relatively inexpensive. However, studies assessing the effects of training on upper limb or hand function following cervical spinal cord injury are scarce and results are somewhat diverse.8 Identifying the value and efficacy of these inter-ventions can help clinicians and also future clinical trials, and there are few existing systematic reviews of this topic. Thus, the aim of this review was to summarize the evidence for the effectiveness of training aimed at promoting recovery of upper limb/hand function from clinical trials involving people with cervical spinal cord injury.

MethodsA systematic literature search of studies published from January 1950 to November 2013 was con-ducted using Medline, Web of Science, EMBASE, Cumulative Index to Nursing and Allied Health Literature (CINAHL), the Physiotherapy Evidence Database (PEDro) databases. In the search strat-egy, MeSH-terms and text words for participants (tetraplegia, quadriplegia, spinal cord injury, spinal cord lesion), interventions (exercise, strength, robotic, repetitive transcranial magnetic stimula-tion, electric* stimulation, task specific training, virtual reality, biofeedback) and outcomes (hand function, arm function, upper limb function, upper extremity function) were combined (Appendix I). Reference lists of all selected trials were also screened to identify additional studies.

Randomized controlled trials, quasi-randomized controlled trials, crossover and controlled trials published in peer-reviewed journals were included if they compared therapy intervention to a control group in patients with complete or incomplete cer-vical spinal cord injury and hand function or upper limb function were an outcome measured. The fol-lowing therapy interventions were included in this

study: robotic training, repetitive transcranial mag-netic stimulation, functional electrical stimulation, electrical stimulation, resistance training task- specific repetitive functional training, virtual real-ity and biofeedback. Case studies, reviews, book chapters and letters were excluded, as well as studies using surgery, orthoses, splints, implants or drugs. All searches were limited to English language articles.

Two investigators (XL and CRB) independently evaluated the title and abstract of indentified stud-ies according to selection criteria. Thereafter, the full-text articles of all eligible studies were obtained and evaluated for in/exclusion by the two investi-gators. In case of disagreement, consensus was reached by discussion between all the authors.

The following data were extracted from each included study: (1) patient characteristics (group, number of participants, time since injury, American Spinal Injury Association (ASIA) grade, level of injury, age); (2) intervention(s) implemented in the study (type of therapy, intensity, duration and fre-quency); (3) outcome measures (strength, hand or arm function, activities of daily living and quality of life); and (4) conclusions. For studies that included paraplegic and tetraplegic patients, only data about tetraplegic participants were extracted.

A 27-item checklist developed by Downs and Black was used to assess the methodological qual-ity of included studies. This checklist contains items for reporting (10 items), external validity (three items), internal validity (bias and confound-ing 13 items) and power (one items). Answers are scored 0 or 1, except for one single item on power, which was scored 0 to 5. The total maximum score was therefore 31.9

Agreement between investigators on inclusion of studies was assessed using the Kappa statistic and percentage agreement (SPSS software version 17.0, Chicago, Illinois, USA). Findings were sum-marized using descriptive statistics.

ResultsA total of 15 eligible studies were identified after searching the databases. After full text screening, one article was excluded because no intervention

Lu et al. 5

was provided and two further articles were added after checking the references of relevant publica-tions, resulting in 16 studies being included in this systematic review10–25 (Figure 1). A 99% (Kappa 0.73) inter-rater agreement was found for the study selection.

Out of 16 included studies, 13 (81%) were ran-domized controlled trials, two (12%) were cohort studies and one (6%) was a cross-over study. The results of quality assessment of these studies are listed in Table 1. Overall, scores for reporting and

internal validity, which includes bias and con-founding, were good, however the scores for exter-nal validity and power were poor. Five studies included blinded outcome measures (Table 1).

The sizes of the experimental and control groups were comparable in the selected studies ranging from five to 32 participants in each group.10–25 There was a wide range of time between injury of participants included (2.5 weeks to 28.5 years). The ASIA classification ranging from grades A to D (Table 2).

Figure 1. Flowchart of screened, excluded and analyzed articles.

6 Clinical Rehabilitation 29(1)

Table 1. Methodological quality assessment of included studies.

Number of studiesmedian (quartile range)

Reporting (10 items) 8 (2)External validity (3 items) 2 (2)Bias (7 items) 6 (1)Confounding (6 items) 3 (3)Power (1 item) 0 (1)

In terms of the type of therapy investigated, the effects of aerobic ergometry, resistance training, massed practice training, task-oriented training, somatosensory stimulation, electrical stimulation and functional electrical stimulation were studied in 14 studies.10–23 The two most recent published studies24–25 focused on the effect of more advanced technology, such as robotic training and repetitive transcranial magnetic stimulation. The length of the training programs ranged from two weeks to nine months, with the majority (56%) lasting between 6–8 weeks (Table 3).

Six studies focused on the effect of exercise ther-apy10–12,15,16,23 (Table 4). The overall results of exer-cise therapy on muscle strength and upper limb/hand function seemed positive. Three studies12,15,23 observed the impact of exercise therapy on activities of daily living or quality of life. Only one study15 assessed quality of life and reported positive results. A positive change in activities of daily living meas-ured by the Quadriplegia Index of Function and the Functional Independence Measure was reported by one study,23 whereas no change was observed in activities of daily living when assessed using the Canadian Occupational Performance Measure.12

Four studies investigating the effect of electrical stimulation13,14,18,20 focused on the change in upper limb muscle strength. Most studies13,14,18 measured change in wrist extensor strength and showed signifi-cant improvement after electrical stimulation (ES) therapy. None of these four studies reported changes in upper limb function and only one study18 evalu-ated self-feeding abilities, but showed no positive results (Table 4).

All four studies investigating functional electri-cal stimulation17,19,21,22 showed positive results on

upper limb function. Among them two studies17,21 showed that compared with conventional therapy alone, conventional therapy combined with func-tional electrical stimulation was more effective in improving upper limb function, while one study22 showed no extra benefit. One of the four studies19 showed a significant increase in grasp force after functional electrical stimulation combined with exercise therapy, but there was no improvement of pinch force. A combination of functional electrical stimulation and conventional therapy resulted in significant improvement in activities of daily living17,19,21and the gains were maintained at six months follow-up.17

Robotic training combined with conventional therapy had no significant effect on muscle strength and functional task performance in the patients with partial hand function.25 Compared with sham stimulation, repetitive transcranial magnetic stimu-lation for five days increased upper extremity func-tion assessed by the Action Research Arm Test, but that was not significantly different from control group24 (Table 4).

DiscussionIn general, the results of this systematic review demonstrate that there are a limited number of studies investigating effects of training on arm and hand function in people with cervical spinal cord injury. The studies included in this review had a wide range of functional levels of participants, training, methodology and outcome parameters. Interestingly, these studies revealed that improve-ment in arm and hand muscle strength and function was possible with training in both the acute and chronic phases.

According to the checklist developed by Down and Black,9 studies included in this systematic review showed fair to good results for reporting and internal validity, but external validity and power was poor. Most studies did not include a sample size calculation and the sample sizes were small, which impacted on the power of the studies. The limited sample sizes might be explained by several factors. First, cervical spinal cord injury have low incidence. Second, patients with cervical

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8 Clinical Rehabilitation 29(1)

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tren

gth

trai

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0 m

in e

lect

rica

l stim

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FES

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exe

rcise

on

the

ReJo

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per

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(201

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Lu et al. 9T

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e pa

ram

eter

s of

incl

uded

stu

dies

.

Aut

hor

(yea

r)Re

sults

Stre

ngth

Endu

ranc

eU

pper

lim

b an

d ha

nd fu

nctio

nA

DL

or Q

oL

Exer

cise

ther

apy

Hic

ks e

t al.

(200

3)15

IE

of c

hest

, bic

eps,

ante

rior

del

toid

pr

e vs

. pos

t(+)

Arm

erg

omet

ry

perf

orm

ance

pre

vs.

post

(+)

Not

ass

esse

dQ

oLET

vs.

cont

rol(+

)N

ot a

sses

sed

Beek

huiz

en e

t al.

(200

5)10

M

axim

al p

inch

gri

p fo

rce

: MP+

SS(+

)N

ot a

sses

sed

WM

FT: M

P+SS

(+)

Not

ass

esse

dJH

FT: M

P+SS

(+),

MP(

+)N

ot a

sses

sed

Glin

sky

et a

l. (2

008)

12IE

of w

rist

ext

enso

rET

vs.

cont

rol(=

)Fa

tigue

res

istan

ce o

f w

rist

ext

enso

r: E

T vs

. con

trol

(=)

Not

ass

esse

dC

OPM

: ET

vs. c

ontr

o(=)

Not

ass

esse

d

Beek

huiz

en e

t al.

(200

8)11

M

axim

al p

inch

gri

p fo

rce

: M

P+SS

(+),

SS(+

)N

ot a

sses

sed

WM

FT: M

P+SS

(+),

SS(+

)N

ot a

sses

sed

JHFT

: MP+

SS(+

), M

P(+)

, SS

(+)

Not

ass

esse

d

Hof

fman

et a

l. (2

010)

16

pinc

h gr

ip s

tren

gth

Bi-M

P+SS

(=),

Uni

-MP+

SS(=

)N

ot a

sses

sed

JHFT

, CA

HA

I: Bi

-MP+

SS(+

), U

ni-M

P+SS

(+)

Not

ass

esse

d

Not

ass

esse

dSp

oore

n et

al.

(201

1)23

N

ot a

sses

sed

Not

ass

esse

dVa

n Li

esho

ut T

est:

pre

vs.

post

or

pre

vs. 3

mon

th: (

+),

ToC

UES

T vs

. sta

ndar

d(=)

QIF

, FIM

: pre

vs.

post

or

pre

vs. 3

m

onth

(+),

ToC

UES

T vs

. sta

ndar

d(=)

, C

OPM

: pre

vs.

post

or

pre

vs. 3

mon

th(+

)N

ot a

sses

sed

Elec

trica

l stim

ulat

ion

Koh

lmey

er e

t al.

(199

6)18

W

rist

ext

enso

r, d

elto

id a

nd b

icep

s: am

ong

4 gr

oups

(=),

pre

vs. p

ost(

+)

(4 g

roup

s to

geth

er)

Not

ass

esse

dN

ot a

sses

sed

Self-

feed

ing

abili

ties:

amon

g fo

ur g

roup

s (=

). Pr

e vs

. pos

t(+)

(fou

r gr

oups

to

geth

er)

Not

ass

esse

dN

eedh

am e

t al.

(199

7)20

Tr

icep

s m

uscl

e gr

ades

ES+v

olun

tary

vs.

volu

ntar

y(+)

Not

ass

esse

dN

ot a

sses

sed

Not

ass

esse

dN

ot a

sses

sed

Har

tkop

p et

al.

(200

3)14

St

reng

th o

f wri

st e

xten

sors

Hr(

+), L

r(=)

Fatig

ue r

esist

ance

of

wri

st e

xten

sor:

H

r(+)

, Lr(

+)

Not

ass

esse

dN

ot a

sses

sed

Not

ass

esse

d

Glin

sky

et a

l. (2

009)

13

W

rist

ext

enso

r IE

: Pre

vs.

post

bo

th(+

), ES

+ET

vs. E

T(=)

Fatig

ue r

esist

ance

: pr

e vs

. pos

t bot

h(=)

, ES

+ E

T vs

. ET(

=)

Not

ass

esse

dN

ot a

sses

sed

Not

ass

esse

d

(Con

tinue

d)

10 Clinical Rehabilitation 29(1)

Aut

hor

(yea

r)Re

sults

Stre

ngth

Endu

ranc

eU

pper

lim

b an

d ha

nd fu

nctio

nA

DL

or Q

oL

Func

tiona

l ele

ctric

al s

timul

atio

nPo

povi

c et

al.

(200

6)22

N

ot a

sses

sed

Not

ass

esse

dRE

L te

st: p

re v

s. po

st b

oth(

+)C

OT+

FES

vs. C

OT(

=)FI

M, S

CIM

: pre

vs.

post

bot

h(+)

CO

T+FE

S vs

. CO

T(=)

Not

ass

esse

dK

apad

ia e

t al.

(201

1)21

N

ot a

sses

sed

Not

ass

esse

dTR

I-HFT

: pre

vs.

post

or

pre

vs. 6

mon

th: b

oth(

+),

CO

T+FE

S vs

.: C

OT(

+)

FIM

, SC

IM: p

re v

s. po

st o

r pr

e vs

. 6

mon

th: b

oth(

+), C

OT+

FES

vs.:

CO

T(+)

Not

ass

esse

d

Kow

alcz

ewsk

i et a

l. (2

011)

19

G

rasp

and

pin

ch fo

rce:

ReJ

oyce

ET

vs. c

onve

ntio

nal E

T(=)

. Pre

vs.

post

: gr

asp

both

(+),

pinc

h bo

th(=

)

ARA

T, R

AH

FT: p

re v

s. po

st

both

(+)

Not

ass

esse

d

ReJo

yce

ET v

s. co

nven

tiona

l ET

(+)

Not

ass

esse

d

Popo

vic

et a

l. (2

011)

21

Not

ass

esse

dN

ot a

sses

sed

TRI-H

FT: p

re v

s. po

st

both

(+)

CO

T+FE

S vs

. CO

T(+)

FIM

, SC

IM: p

re v

s. po

st b

oth(

+)C

OT+

FES

vs. C

OT(

+)N

ot a

sses

sed

rTM

S an

d ro

botic

Kup

pusw

amy,

et a

l. (2

011)

24

Not

ass

esse

dN

ot a

sses

sed

ARA

T; p

re v

s. po

st(+

), rT

MS

vs. s

ham

rTM

S(=)

Not

ass

esse

dN

ot a

sses

sed

Zar

iffa

et a

l. (2

012)

25

10

upp

er li

mb

mus

cles

: pre

vs.

post

(=),

robo

tic v

s. co

ntro

l(=)

Not

ass

esse

dA

RAT

and

GRA

SSP;

pre

vs

. pos

t(=)

, rob

otic

vs.

cont

rol(=

)

Not

ass

esse

dN

ot a

sses

sed

ARA

T: A

ctio

n Re

sear

ch A

rm T

est;

Bi-:

bim

anua

l; C

AH

AI:

Che

doke

Arm

and

Han

d A

ctiv

ity In

vent

ory;

CO

PM: T

he C

anad

ian

Occ

upat

iona

l Per

form

ance

Mea

sure

; CO

T: c

onve

ntio

nal o

ccup

atio

nal

ther

apy;

ET:

exe

rcise

ther

apy;

FES

: fun

ctio

nal e

lect

rica

l stim

ulat

ion;

FIM

: Fun

ctio

nal I

ndep

ende

nce

Mea

sure

; GRA

SSP:

Gra

ded

and

rede

fined

ass

essm

ent o

f str

engt

h, s

ensib

ility

and

pre

hens

ion;

Hr:

hi

gh r

esist

ance

; IE:

isom

etric

exe

rcise

; JH

FT: J

ebse

n H

and

Func

tion

Test

; Lr:

low

er r

esist

ance

; MP:

mas

sed

prac

tice;

RA

HFT

: ReJ

oyce

aut

omat

ed h

and

func

tion

test

; REL

test

: Reh

abili

tatio

n En

gine

erin

g La

bora

tory

Han

d Fu

nctio

n Te

st; r

TMS:

rep

etiti

ve tr

ansc

rani

al m

agne

tic s

timul

atio

n; S

CIM

: Spi

nal C

ord

Inde

pend

ence

Mea

sure

; SS:

som

atos

enso

ry s

timul

atio

n; T

oCU

EST:

task

-ori

ente

d cl

ient

- ce

nter

ed u

pper

ext

rem

ity s

kille

d pe

rfor

man

ce tr

aini

ng; T

RI-H

FT: T

oron

to R

ehab

ilita

tion

Inst

itute

Han

d Fu

nctio

n Te

st; U

ni-:

unim

anua

l; W

MFT

: Wol

f Mot

or F

unct

iona

l Tes

t; A

DL:

act

ivity

of d

aily

liv

ing;

QoL

: qua

lity

of li

fe; Q

IF: q

uadr

iple

gia

inde

x of

func

tion;

ES:

elec

tric

al s

timul

atio

n.

(=):

no s

igni

fican

t cha

nge;

(+):

signi

fican

t im

prov

emen

t; bo

th (+

): sig

nific

ant i

mpr

ovem

ent i

n bo

th g

roup

s; bo

th (=

): no

sig

nific

ant c

hang

e in

bot

h gr

oups

.

Tab

le 4

. (C

ontin

ued)

Lu et al. 11

spinal cord injury have, among the total population with spinal cord injury, the most secondary compli-cations, leading to frequent drop-outs and poorer adherence to trial training specifications. Third, these patients are difficult to match owing to the complexity of their pathology. Fourth, both in spi-nal cord injury and non-spinal cord injury patients, arm and hand function is a complex issue. It encompasses a wide variety of highly non-cyclic movements, which are not always easy to measure objectively, especially at the activity level.26

Some studies in the literature indicate that early initiation of spinal cord injury-specific rehabilita-tion is extremely important. A delay in starting these interventions may negatively influence ulti-mate functional capability.27,28 However, studies included in this review showed that training initi-ated in the chronic stage still resulted in improve-ment of muscle strength, hand function and activities of daily living or quality of life. These findings indicated that improvement in arm and hand muscle strength and function was possible with training in both the acute and chronic phases.

The outcome of included studies showed that exer-cise therapy and functional electrical stimulation improved muscle strength, arm and hand function, activities of daily living or quality of life in patients with cervical spinal cord injury. Studies that focused on electrical stimulation showed improvements in muscle strength of upper extremity, but there were few reports about whether it could improve arm and hand function, activities of daily living or quality of life. New techno-logical innovations, such as repetitive transcranial stimulation, robotic training and virtual reality, have been introduced in rehabilitation in recent years. But most studies were case series, with only two studies on repetitive transcranial stimulation and robotic training, which were included in this review, including a control group.24,25 Neither of the two studies reported muscle strength improvement after training, only repetitive transcranial magnetic stimulation (rTMS) showed an arm function increase after training. The negative results be owing to the small sample size.

In this review, we only included English-language articles, which may cause bias owing to missing some published studies in this area in another language. Most of the studies did not include a sample size

calculation. The small sample size means that the power of the studies to detect an effect, if the effect actually exists, is compromised. Therefore, conclu-sions drawn from these studies should be made with caution. A meta-analysis was not possible because of the variety of outcome measures. Comparison of results across studies would be improved by stand-ardization of outcome measures. There are initiatives in the field of spinal cord injury rehabilitation to develop international standards and data sets for spi-nal cord injury. The Functional Independence Measure and the Spinal Cord Independence Measure are recommended in these guidelines to assess activi-ties of daily living in patients with spinal cord injury.29,30 Other tests, such as the Jebsen test and the Sollerman test have also been suggested in these guidelines. However, at the present time, there is a lack of consensus on what might be the most useful tests of arm and hand function after spinal cord injury.

In conclusion, the results of this systematic review suggest that training of the upper limb following spinal cord injury, including exercise therapy, electrical stim-ulation and functional electrical stimulation, leads to improvements in muscle strength, upper limb function and activities of daily living or quality of life. Further research is needed on the use of new technology, such as repetitive transcranial stimulation in improving upper limb function. Future studies should be carefully designed to increase trial power and external validity. The routine use of a series of standardized objective tests would allow future meta-analyses of the effective-ness of exercise interventions on upper limb function from a number of smaller studies.

Clinical messages

x� Training, including exercise therapy, elec-trical stimulation and functional electrical stimulation, could improve arm and hand muscle strength and function after spinal cord injury.

x� The use of standardized outcome meas-ures of upper limb function in future clini-cal trials would facilitate meta-analyses on the effectiveness of training interven-tions on upper limb function.

12 Clinical Rehabilitation 29(1)

Conflict of interestThe authors declare that there is no conflict of interest.

FundingThis research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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Appendix 1

Search strategyMEDLINE search strategy (the search strategy uses MeSH terms unless indicated otherwise): Set A terms (combined by OR) tetraplegia quadriplegia spinal cord injury spinal cord lesion; Set B terms (combined by OR) hand function arm function upper limb function upper extremity function; Set C (combined by OR) exercise strength robotic electric* stimulation task specific training repetitive transcranial magnetic stimu-lation virtual reality.

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