Clinical Rehabilitation 2008; 22: 291–305

Impact of EMG-triggered neuromuscular stimulation

of the wrist and finger extensors of the paretic hand
after stroke: a systematic review of the literature
A Meilink Student of Human Movement Sciences and Physical Therapy, VU University, Amsterdam, B Hemmen and
HAM Seelen Rehabilitation Foundation Limburg (SRL), Hoensbroek and G Kwakkel Center of Excellence for Rehabilitation
Medicine ‘‘de Hoogstraat’’ and Department of Rehabilitation Medicine, Rudolf Magnus Institute of NeuroScience, University
Medical Centre, Utrecht, and Department of Rehabilitation Medicine, VU University Medical Center, Amsterdam, The Netherlands

Received 26th June 2007; returned for revisions 20th July 2007; revised manuscript accepted 27th July 2007.

Objective: To assess whether EMG-triggered neuromuscular electrical

stimulation (EMG-NMES) applied to the extensor muscles of the forearm
improves hand function after stroke.
Design: Systematic review of randomized controlled trials.
Methods: A computer-aided literature search up to June 2006 identified
articles comparing EMG-NMES of the upper extremity with usual care.
Methodological quality was rated on the Physiotherapy Evidence Database
scale (PEDro), and the Hedges’ g model was used to calculate the summary
effect sizes (SES) using fixed or random models depending on heterogeneity.
Results: Eight studies, selected out of 192 hits and presenting 157 patients, were
included in quantitative and qualitative analyses. The methodological quality ranged
from 2 to 6 points. The meta-analysis revealed non-significant effect sizes in favour
of EMG-NMES for reaction time, sustained contraction, dexterity measured with the
Box and Block manipulation test, synergism measured with the Fugl-Meyer Motor
Assessment Scale and manual dexterity measured with the Action Research Arm test.
Conclusion: No statistically significant differences in effects were found between
EMG-NMES and usual care. Most studies had poor methodological quality, low
statistical power and insufficient treatment contrast between experimental and
control groups. In addition, all studies except two investigated the effects of
EMG-NMES in the chronic phase after stroke, whereas the literature suggests that
an early start, within the time window in which functional outcome of the upper limb
is not fully defined, is more appropriate.

Introduction

Stroke is one of the leading causes of impairment

Address for correspondence: G Kwakkel, Department of
Rehabilitation Medicine, VU University Medical Center,
de Boelelaan 1117, 1081 HV Amsterdam, PO Box 7057,
1007 MB Amsterdam, The Netherlands.
e-mail: g.kwakkel@vumc.nl
ß SAGE Publications 2008
Los Angeles, London, New Delhi and Singapore
and disabilities in the industrialized world.1
Although prospective epidemiological studies are
lacking, it has been suggested that about 30%2 to
66%3 of the patients suffering a stroke still have
10.1177/0269215507083368
292 A Meilink et al.
impaired upper limb function after six months,
whereas only 12%4 to 18%5 regain complete
functional recovery after a stroke. The recovery
of the wrist and finger extensors is an especially
challenging aspect, because of the development of
a deficit in individual finger activation.6 According
to a clinical study by Fritz et al.,7 regaining finger
extension is essential to functional movement
of the upper limb and hence to activities of
daily living (ADL).
Several randomized controlled trials have found
that neuromuscular electrical stimulation (NMES)
has a positive effect on motor recovery of the
paretic limb following stroke.8–10 In addition,
it was found that NMES may reduce spasticity,11,12
strengthen muscles13,14 and increase range of
motion.12 In particular, it has been suggested
that the effects of NMES can be maximized
by learning to initiate muscle activity and subse-
quently to imagine the desired movement.13,15
From this perspective, it has been hypothesized
that EMG-triggered neuromuscular electrical
stimulation (EMG-NMES), first described by
van Overeem Hansen,16 would offer added value
over neuromuscular stimulation alone.
Two independent systematic reviews have
evaluated the effects of EMG-NMES on arm
and hand function after stroke.17,18 However, the
two meta-analyses showed conflicting evidence
for the effect of EMG-NMES on upper limb func-
tion after stroke. Bolton et al.17 pooled outcomes
in terms of of impairments and limitations in
activities into one effect size, and found significant
effects in favour of EMG-NMES (0.82; confidence
interval (CI) 0.10 to 1.55), whereas van Peppen
et al.18 found non-significant overall effect sizes
in terms of synergism, strength and dexterity.
The purpose of the present systematic review was
to re-investigate the effects of EMG-NMES of the
extensors of the hand on the arm/hand function
when compared with usual care in stroke patients,
as new controlled studies have been published
since the 2003 systematic review.
Methods
Search strategy for study identification
A computer-aided literature search up to June
2006 was performed in the following electronic
databases: Pubmed (MEDLINE), Cochrane
Central register of Controlled Trials, CINAHL,
DARE, PEDro, EMBASE, DocOnline and
HighWire press. The following MeSH and
key words were used: cerebrovascular disorders,
cerebrovascular accident, hemiplegia, basal
ganglia cerebrovascular disease, upper extremity,
wrist extensors, wrist flexors, neuromuscular
stimulation, electrostimulation, electromyogra-
phy, EMG-triggered and randomized controlled
trial. References in relevant studies were examined
and if more information about a trial was needed,
the author was contacted.
Studies included in the present meta-analysis
had to meet the following criteria: First, the
studies had to involve patients diagnosed with a
stroke according to the definition of the World
Health Organization (WHO). This defines stroke
as ‘a focal (at times global) neurological impair-
ment of sudden onset, and lasting more than 24
hours (or leading to death) and of presumed
vascular origin’.19 Second, the study had to inves-
tigate the effects of EMG-NMES by means of
surface electrodes as the experimental interven-
tion. For this purpose, EMG-NMES was defined,
following the studies by Bolton et al.17 and de
Kroon et al.20 as: ‘the delivery of electrostimula-
tion when volitionally generated EMG signals
exceed a pre-set threshold.’ In such a procedure,
a microprocessor connected to surface electrodes
monitors the EMG activity level generated
by patients, as well as administering the neuro-
muscular stimulation. If the threshold is not
reached, the device automatically lowers the
threshold and the patient tries again. Third,
the EMG-NMES applied had to be targeted to
activating the extensor muscles of the forearm.
Fourth, the study had to be classified as a rando-
mized controlled trial, being defined as: ‘a clinical
trial that involves at least one test treatment and
one control treatment, concurrent enrollment and
follow-up of the test- and control-treated groups,
and in which the treatments to be administered
are selected by a random process, such as the use
of a random-numbers table.’ Fifth, the publica-
tion had to be in English, German or Dutch.
Sixth, the application of EMG-NMES had to
be the experimental treatment in the randomized
controlled trial and not the control treatment.
 EMG stimulation of the wrist and finger extensors
Methodological quality assessment
The methodological quality of the selected
randomized controlled trials was rated indepen-
dently by two assessors (GK and AM) on the
Physiotherapy Evidence Database (PEDro)
scale.21,22 The PEDro scale includes 11 items.
The first item reflects the external validity of a
study, whereas the other 10 items assess character-
istics related to the internal validity of the study.
These 10 items were used to calculate PEDro
scores. All items were scored in binary terms
(i.e. yes ¼ 1/no ¼ 0), resulting in a maximum score
of 10 points. The reliability of the PEDro scale is
good.23 Inter-rater agreement regarding individual
items was assessed by calculating a Cohen’s kappa
(k). Disagreement between the review authors was
resolved by discussion.
Quantitative analysis
Pooling was considered if the methodological
quality on the PEDro scale was
3.
Statistical pooling was performed for each study
separately if the measurement instruments used
were comparable. For this purpose, the Hedges’
g model24,25 was used to analyse the individual
effect sizes. In this model, the effect size for
each individual study was calculated from the
difference between the means for the experimental
and control groups, divided by the average popula-
tion standard deviation (SDi). Second, to avoid
overestimation of the effect size, a correction was
introduced to obtain an unbiased estimator gu. The
impact of sample size was addressed by estimating
a weighting factor (wi) for each study, assigning
larger weights to effect sizes from studies with
larger study samples and thus smaller variances.
Subsequently, individual effect sizes (gu values of
individual studies) were weighted and pooled into
a summary effect size (SES). On the basis
of individual weights (wi), the variance of the SES
was estimated.26 Since the Hedges’ model assumes
that the effects are fixed, heterogeneity between
pooled studies was tested by the Q-statistic.27
However, since this statistic may be too conserva-
tive to detect significant heterogeneity between stu-
dies, I2 was also applied to test for homogeneity.28
If the SES showed heterogeneity (i.e. I2450%), a
random effects model was used.27,29
293
Post-hoc sensitivity analysis was performed
if significant heterogeneity was found between
individual effect sizes. For all outcome variables,
the critical value for rejecting H0 was tested two
sided with a P-value50.05.
Results
Study identification
A total of 192 hits were screened and 34 were
assumed on the basis of title and abstract to be
relevant for more detailed analysis. These were
further screened for eligibility using the inclusion
and exclusion criteria. The study by Hesse et al.30
was excluded because they had used EMG-NMES
as a control group intervention and compared it to
robotics as the experimental intervention.
A total of eight randomized controlled
trials involving 157 patients were included in the
present systematic review. The electronic search
strategy and selection of papers are illustrated in
Appendix 1. One randomized controlled trial
conducted in the Netherlands was known to be
submitted for publication and added to the list
of included studies.38
Tables 1 and 2 show the main characteristics
of the eight eligible studies included in the
systematic review.
Methodological quality assessment
Table 3 presents the PEDro scores of included
studies. Initially, the two reviewers disagreed on 7
of the 80 PEDro items scored, resulting in an
average Cohen’s k score for all items of 0.83.
The median PEDro score was 5, ranging from
231 to 6 points.32,33,38
Eight studies did not use an intention-to-treat
analysis.31–38 In one study the therapists were
blinded for treatment allocation38 whereas in
three studies the randomization procedure was
concealed.32,33,38
Quantitative analysis
The study by Gabr et al.31 could not be used
for pooling due to its insufficient methodological
quality. Statistical pooling of studies was possible
 294

Table 1 Clinical characteristics of included trials

Study Intervention n Lesion Age Time post Outcome Authors’

reference, location (years) stroke (SD) measures conclusions
A Meilink et al.

First author Mean

þ publication (SD or
year range)

Cauraugh E EMG-stim E¼7 10 RH 61.64 3.49 years Reaction time of wrist/ Significantly decreased
(2000)34 C no C¼4 1 LH (9.57) (2.56) finger-extensor mus- motor dysfunction and
treatment cles Sustained contrac- improved motor cap-
tion of wrist extensors abilities of the wrist and
FM of upper extremity finger extensors
MAS of hand/wrist/fin-
gers Box & Block
timed manipulation test
Cauraugh E1 EMG-stim/ E1 ¼ 10 12 RH 63.7 39.1 months Reaction time of wrist/ The two coupled motor
(2002)35 bilat E2 ¼ 10 11 LH finger-extensor recovery protocols
E2 EMG-stim C¼5 muscles Sustained (E1&E2) increased
C no treatment contraction of wrist movement capabilities
extensors Box & Block in patients with stroke.
timed manipulation test The E2 group exceeded
the control group in the
number of blocks
moved and rapid onset
of muscle contractions
Cauraugh EMG-stim/bilat E1 ¼ 10 15 RH 66.4 2.8 years Reaction time of wrist/ The 5- and 10-s active
(2003)36 E1 on time E2 ¼ 10 11 LH (9.7) (1.9) finger-extensor stimulation/bilateral
10 s E2 on time C¼6 muscles Sustained movement groups had
5 s C on time 0 s contraction of wrist decreased residual
extensors Box & block motor dysfunctions in
timed manipulation test comparison to the 0-s
control group
Cauraugh E1 EMG-stim E1 ¼ 10 E1 6 E1 63.29 E1 3.57 years Reaction time of wrist/ The E2 group showed
(2005)37 RH & (10.81) (2.42) finger-extensor positive intralimb trans-
4 LH muscles Movement fer post treatment
time Peak velocity SD when both arms moved
peak velocity simultaneously. This
Deceleration time group displayed
improvements on all
outcome measures
except for reaction time
 E2 EMG-stim/ E2 ¼ 11 E2 E2 69.37 E2 4.73 years
bilat 9 RH & 2 LH (10.14) (3.52)
C no protocol C¼5 C no stroke C 54.48 C no stroke
history (14.29) history
Francisco E EMG-stim E¼4 ? E 60.3 E 17.5 days FM of upper Subjects in the EMG-
(1998)33 C conventional C¼5 (15.6) (2.4) extremity NMES group showed
therapy C 69.6 C 18.2 days Self-care FIM significantly greater
(16.2) (2.3) gains in FM and FIM
scores compared with
controls
Hemmen E1 EMG-stim E1 ¼ 14 E1 7 RH E1 62.1 E1 44.9 days FM of upper Both EMG-NMES and
(2007)38 þ movement E2 ¼ 13 & 6 LH (12.7) (14.5) extremity ARAT conventional electrosti-
imagery E2 4 RH & 9 E2 60.7 E2 65.5 days mulation led to
E2 conventional LH (12.3) (54.0) improved arm-hand
electrostimula- ischaemic function after 12 weeks
tion of therapy. Significant
improvement was still
observed 9 months
after treatment ended
De Kroon E1 cyclic E1 ¼ 10 E1 7 RH & 3 E1 60.6 E1 16.5 ARAT Grip strength of There was no signifi-
(2004)32 electrostim E2 ¼ 11 LH (10.9) months hand MI pinch grip/ cant difference
E2 EMG-stim E2 8 RH & 3 E2 57.4 (6–48) elbow flexion/shoulder between E1 and E2
LH (8.0) E2 27 months abduction, FM of with respect to
(7–115) upper extremity improvement of the
¼median motor function of the
(range) affected arm
Gabr E1 EMG-stim E1 ¼ 8 E1 4 RH 59.75 52.75 months FM ARAT Neither participation in
(2005)31 þ exercise E2 ¼ 4 & 4 LH E2 (44–75 (range goniometry a traditional home
programme 2 RH & 2 LH ¼ range) ¼ 13–131) exercise programme
E2 exercise nor EMG-NMES use
programme conveyed changes on
þ EMG-stim the Fugl-Meyer scale or
ARAT. However, EMG-
NMES use increased
active affected limb
extension

E, experimental group; C, control group; EMG-stim, EMG-triggered electrical stimulation; FM, upper extremity: Fugl-Meyer motor assessment using the
upper extremity motor subscore; MAS, Motor Assessment Scale to evaluate the functional recovery of the hand, wrist and fingers; EMG-stim/bilat,
treatment in which subjects received EMG-stim and assistance from unimpaired hand as wrist/finger extension was executed in both limbs; SD, standard
deviation; self-care FIM, self-care components of Functional Independence Measure; conv., conventional; MRC, Medical Research Council; sh.abd., shoulder
abduction; fl./ext., flexion, extension; electrostim, electrostimulation; ARAT, Action Research Arm Test; MI, Motricity Index.
EMG stimulation of the wrist and finger extensors
295
 296
A Meilink et al.

Table 2 Stimulation characteristics of included trials

Study reference, Device Frequency Amplitude Pulse Target muscles Duration of Treatment
First author (Hz) (mA) duration stimulation parameters
þ publication (ms)
year

Cauraugh Automove 800 50 14–29 ? m. extensor digitorum 2 times a day 30 min, 1 s ramp up, 5 s
(2000)34 communis m. extensor 3 days a week, biphasic stimulation, 1 s
carpi ulnaris for 2 weeks ramp down. Rest 25 s
Cauraugh Automove 800 50 16–29 200 m. extensor digitorum 3 times a day 30 min, 1 s ramp up, 5 s biphasic
(2002)35 communis m. extensor 3 days in 2 weeks stimulation, 1 s ramp
carpi ulnaris down. Rest 25 s
Cauraugh Automove 800 50 17–28 200 m. extensor digitorum 90 min a day, 4 days 1 s ramp up, 5 or 10 s
(2003)36 communis m. extensor in 2 weeks biphasic stimulation, 1 s
carpi ulnaris ramp down. Rest 25 s
Cauraugh Neuromove 50 15–29 200 m. extensor digitorum 90 min a day, 4 days 1 s ramp up, 5 s biphasic
(2005)37 microprocessor communis m. extensor in 2 weeks stimulation, 1 s ramp
carpi ulnaris down. Rest 25 s
Francisco Automove 20–100 0–60 200 m. extensor carpi radialis 2 times a day 30 min, 5 s stimulation and 5 s off
(1998)33 AM 706 5 days a week for
the length of stay
Hemmen Automove 50 5–60 200 Wrist extensor muscles 5 days a week 30 min, 12 s stimulation, 5 s rest
(2007)38 AM 800 for 12 weeks
De Kroon Automove 35 50 mV 300 Wrist and finger extensor 3 times 30 min 1 s ramp up, 6 s biphasic
(2004)32 AM800 muscles a day for 6 weeks stimulation, 1 s ramp
down. Rest 9 s
Gabr (2005)31 Neuromove 900 ? ? 100–400 Wrist extensors 2 times a day 10 s stimulation
35 min, for 8 weeks

m.: musculus.
Table 3 PEDro scores of included studies

Author Item on PEDro scale

1 Eligibility 2 Random 3 Concealed 4 Similarity 5 Blinding 6 Blinding 7 Blinding 8 Outcome 9 Intention- 10 Between- 11 PM Total
criteriaa allocation allocation baseline patients therapists assessors 4 85% to-treat group and MV points
patients comparisons

Cauraugh 0 1 0 0 0 0 0 1 0 1 0 3
(2000)34
Cauraugh 0 1 0 0 0 0 0 1 0 1 0 3
(2002)35
Cauraugh 1 1 0 1 0 0 0 1 0 1 1 5
(2003)36
Cauraugh 1 1 0 1 0 0 0 1 0 1 1 5
(2005)37
Francisco 1 1 1 1 0 0 1 0 0 1 1 6
(1998)33
Hemmen 1 1 1 0 0 0 1 1 0 1 1 6
(2007)38
De Kroon 1 1 1 0 0 0 1 1 0 1 1 6
(2004)32
Gabr 1 1 0 0 0 0 0 1 0 0 0 2
(2005)31

a
PEDro item 1 evaluates the external validity and was not included in the PEDro sumscore. The PEDro sumscore is based on items 2–11. PM and MV: point
measures and measures of variability.
EMG stimulation of the wrist and finger extensors
297
298 A Meilink et al.

for the following common outcomes: (1) Fugl-
Meyer Motor Assessment Scale of the upper
extremity (FM)32,33,38; (2) Action Research Arm
Test (ARAT)32,38; (3) Box & Block timed manipu-
lation test (B & B)34–36; (4) reaction time35–37; and
(5) sustained contraction.35,36
Fugl-Meyer Motor Assessment Scale for
the upper extremity
The study by Cauraugh et al.34 could not be
pooled because the article provides no point
measures and measures of variability. After
intervention, a homogeneous (2 ¼ 5.85, P50.10,
I2 ¼ 48.7%) non-significant effect size was found
for three studies (N ¼ 57)32,33,38 comparing
the effect of EMG-triggered stimulation
with conventional therapy on the Fugl-Meyer
Motor Assessment Scale for the upper extremity
(SES [fixed] 0.10; CI 0.43 to 0.64; Z ¼ 0.38,
P ¼ 0.35). However, de Kroon et al.32 used cyclic
electrostimulation as a control instead of exercise
therapy (Figure 1). Excluding the study by de
Kroon and IJzerman32 by way of sensitivity ana-
lysis resulted in a heterogeneous (2 ¼ 5.7,
P50.025, I2 ¼ 65%) non-significant SES for
EMG-triggered stimulation compared to conven-
tional therapy (SES [random] 0.60; CI 1.53 to
2.73; Z ¼ 0.55, P ¼ 0.29).33,38
Action Research Arm Test
The Action Research Arm Test was evaluated
in two studies (N ¼ 48).32,38 A homogeneous
(2 ¼ 0.13, P50.10, I2 ¼ 0) non-significant SES
was found for the Action Research Arm Test
when comparing EMG-triggered stimulation with
conventional therapy (SES [fixed] 0.00; CI 0.56
to 0.57; Z ¼ 0.007, P ¼ 0.50) (Figure 2).
Box and Block timed manipulation test
Three studies (N ¼ 62) had investigated the effect
of EMG-triggered stimulation on manual dexterity
using the Box and Block timed manipulation
test.34–36 A homogeneous (2 ¼ 0.435, P ¼ 0.81,
I2 ¼ 0) non-significant SES was found for B & B
(SES [fixed] 0.37; CI 0.27 to 1.01; Z ¼ 1.15,
P ¼ 0.13) (Figure 2).
Reaction time of the wrist and finger extensor
muscles (for isometric contraction)
Pooling for reaction time was possible for three
studies. One study showed no point estimates or
estimates of dispersion.34 A homogeneous
(2 ¼ 0.30, P ¼ 0.84, I2 ¼ 0) non-significant
SES was found for three studies (N ¼ 77)35–37 com-
paring the effect of EMG-triggered reaction
time with control group reaction time

de Kroon 2005 N = 21 0.23 [−0.15−0.61]

Hemmen 2002 N = 27 −0.37 [−0.67−(−0.08)]
Francisco 1998 N=9 1.81 [0.72−2.90]

SES Fugl-Meyer N = 57 0.10 [−0.43−0.64]

(fixed effects model)

−2 −1 0 1 2
Favors usual care Favors EMG-NMES

Figure 1 Meta-analysis of EMG-triggered neuromuscular electrical stimulation (EMG-NMES) studies on Fugl-Meyer Motor
Assessment of the upper paretic limb. Effect sizes are based on Hedges’ g (and 95% confidence intervals). The centre of
each bar represents the mean effect size, whereas the length of the bar reflects the 95% confidence interval. Bars to the
right of the vertical line denote a positive effect for EMG-NMES and vice versa. When the bar of an individual study crosses
the vertical line at zero, no definite conclusions can be drawn in favour of EMG-NMES or the usual care group. The SES
value represents the overall effect size of all included studies.
 EMG stimulation of the wrist and finger extensors 299

(SES [fixed] 0.41; CI 0.20 to 1.03; Z ¼ 3.51,
P50.001) (Figure 3). In addition, combining
EMG-triggered stimulation and bilateral move-
ment resulted in a non-significant SES [fixed]
of 0.74; CI 0.02 to 1.51.35,36
A homogeneous (2 ¼ 1.04, P ¼ 0.31, I2 ¼ 0) non-
significant SES was found for two studies (N ¼ 51)
comparing the effect of EMG-triggered sustained
contraction with a conventional treatment proto-
col (SES [fixed] 0.65; CI 0.11 to 1.41; Z ¼ 1.67,
P ¼ 0.048)35,36 (Figure 3).

Sustained contraction (maximum isometric

contraction of the wrist and finger extensor
muscles for 5 seconds)
Pooling for sustained contraction was
possible for two studies. One study could not be
pooled due to a different variable of outcome.34
Discussion
The present systematic review was conducted
to evaluate the effects of EMG-triggered

Box and BLOCK test

Cauraugh 2000 N = 11
0.71 [−0.09−1,51]

Cauraugh 2002 N = 15 0.15 [−0.44−0.74]

Cauraugh 2003 N = 16 0.36 [−0.17−0.89]

SES box & block N = 42 0.37 [−0.27−1.01]

(fixed effects model)

ARAT

de Kroon 2005 N = 21 0.12 [−0.25−0.50]

Hemmen 2006 N = 27 −0.09 [−0.38−0.20]

SES ARA N = 48 0.00 [−0.56−0.57]

(fixed effects model)

−2 −1 0 1 2
Favors usual care Favors EMG-NMES

Figure 2 Meta-analysis of EMG-triggered neuromuscular electrical stimulation (EMG-NMES) studies on Box & Block
manipulation test and Action Research Arm Test. Effect sizes are based on Hedges’ g (and 95% confidence intervals).
The centre of each bar represents the mean effect size, whereas the length of the bar reflects the 95% confidence interval.
Bars to the right of the vertical line denote a positive effect for EMG-NMES and vice versa. When the bar of an individual
study crosses the vertical line at zero, no definite conclusions can be drawn in favour of EMG-NMES or the usual care
group. The SES value represents the overall effect size of all included studies.
300 A Meilink et al.

Reaction time

Cauraugh 2005 N = 15 0.26 [−0.33−0.85]

Cauraugh 2003 N = 16 0.33 [−0.20−0.85]

Cauraugh 2002 N = 15 0.66 [−0.06−1.27]

SES reaction time N = 46 0.41 [−0.20−1.03]

(fixed effects model)

Sustained contraction

Cauraugh 2003 N = 16 1.05 [0.49−1.61]

Cauraugh 2002 N = 15 0.25 [−0.34−0.85]

SES sustained contraction N = 31 0.65 [−0.11−1.41]

(fixed effects model)

−2 −1 0 1 2
Favors usual care Favors EMG-NMES

Figure 3 Meta-analysis of EMG-triggered neuromuscular electrical stimulation (EMG-NMES) studies on reaction time,
sustained contraction and Box & Block manipulation test. Effect sizes are based on Hedges’ g (and 95% confidence
intervals). The centre of each bar represents the mean effect size, whereas the length of the bar reflects the 95%
confidence interval. Bars to the right of the vertical line denote a positive effect for EMG-NMES and vice versa. When the
bar of an individual study crosses the vertical line at zero, no definite conclusions can be drawn in favour of EMG-NMES or
the usual care group. The SES value represents the overall effect size of all included studies.

neuromuscular electrical stimulation (EMG-
NMES) on the arm/hand function after stroke.
However, our meta-analysis involving 157 subject
with stroke showed no significant effects in favour
of EMG-NMES in terms of reaction time, sus-
tained contraction, synergism with the
Fugl-Meyer Motor Assessment Scale or dexterity
measured with the Box and Block manipulation
test or Action Research Arm Test.
The findings of this systematic review disagree
with the review of Bolton and colleagues,17
who found a significant overall effect size of 0.82
(CI 0.10 to 1.55). In our opinion, there are at least
two possible explanations for this difference.
First, two of the five studies included in the meta-
analysis by Bolton et al.17 were non-randomized
clinical trials.39,40 It is important to note that
non-randomized studies tend to overestimate treat-
ment effects and will consequently report higher
effect sizes.41 Second, Bolton et al.17 pooled the
outcomes of the Fugl-Meyer upper extremity test,
the Box and Block manipulation test and the
Rivermead Motor Assessment Scale in one overall
effect size, whereas the present study restricted
pooling to measurement instruments with
the same underlying construct. Theoretically, the
selection of type of fixed effects model to calculate
the overall effect sizes in the two meta-analyses
 EMG stimulation of the wrist and finger extensors
may also affect found SES. Bolton et al.17 applied
the Glass delta model to calculate individual stan-
dardized effect sizes, whereas the present study
used the Hedges’ g model. In the Glass’s delta
model the effect size is computed by taking the
difference in improvement between experimental
and control group divided by the standard devia-
tion of the control group, whereas in the Hedges’
g model the difference in improvement between
experimental and control group is divided by the
pooled standard deviation of experimental and
control group. However, even using the standard
deviation of the control group and applying Glass’s
delta, our meta-analysis yielded no significant
effect sizes. For example, applying Glass’s
delta for measuring outcome of the Fugl-Meyer
upper extremity test yielded a non-significant SES
of 0.11. This finding suggests that our results are
almost independent of the model used to calculate
individual effect sizes. Finally, most clinical trials
included in our review had poor methodological
quality, with one study scoring 2 points31 and
two studies scoring 3 points34,35 on the PEDro
scale, indicating that there is a need for studies of
higher methodological quality. It should be noted,
however, that studies with a poor methodological
quality tend to overestimate rather than underesti-
mate found effect sizes.18
The reason for the lack of statistically signifi-
cant effects in favour of EMG-NMES remains
unclear in the present study. Due to the small
samples, all randomized controlled trials relating
to EMG-NMES for the upper limb had insuffi-
cient statistical power to reject the H0 hypothesis
in terms of outcome of dexterity. This finding is
especially important in view of the large heteroge-
neity in upper limb recovery in patients with
stroke, and the small effects of treatment.4,42
Also due to low numbers included in found
RCTs, most studies did suffer from imbalances
at baseline.
Another reason for the lack of evidence for
effects of EMG-NMES may be the absence of
sufficient treatment contrast between the experi-
mental group and the control group. For example,
in the study by de Kroon and IJzerman,32 cyclic
stimulation of the wrist and finger extensor mus-
cles was used as a control group intervention and
compared with stimulation of the extensors alone.
In the same vein, there was also a lack of
301
treatment contrast in the study by Hemmen
et al.,38 which compared EMG-NMES with con-
ventional electrostimulation. In addition,
Hemmen et al.38 and de Kroon and IJzerman32
used 2–3 times fewer EMG-NMES treatments
per week than other included studies and found
small effects for EMG-NMES. Therefore, higher
treatment intensities with larger contrasts between
experimental and control group should be consid-
ered in future randomized controlled trials.43,44
Future studies should also increase the treatment
contrast between the experimental and control
groups to detect the effects of EMG-NMES,
either by increasing the dose of EMG-NMES or
by controlling the treatment in the control group.
Finally, the lack of evidence for a favourable
effect of EMG-NMES may be explained by the
fact that the EMG-NMES intervention was
restricted to patients in the chronic or subacute
phase after stroke. Thus far, only one study33
has included patients within three weeks post
stroke. Recently, we found that over 90% of the
probability of a return of upper limb function is
decided within the first five weeks post stroke,
suggesting that there is a critical time window in
which the outcome of regaining some dexterity is
defined.4 This prospective cohort study also sug-
gests that patient selection with respect to the like-
lihood of regaining dexterity is crucial for changes
observed in chronic stroke victims. The selection
of acute patients may explain why Francisco
et al.33 found a relatively larger effect size in
terms of the FM arm score when EMG-NMES
was used in the subacute phase post stroke com-
pared with studies conducted in the chronic phase
after stroke. Especially in situations where no or
insufficient motor control is possible, EMG-
NMES may serve as a substitute to stimulate
cortical sensory areas.45 Recently, the ability to
modulate motor function by applying early soma-
tosensory stimulation was supported by the study
by Conforto and colleagues.46 They showed that
increasing somatosensory stimulation by median
nerve stimulation of the affected hand results in
an improved sensorimotor function of the paretic
limb. This finding further supports the view that
somatosensory input, like EMG-NMES, can
temporarily recondition the brain, in particular
at moments when the brain is more responsive to
afferent input.47 In the absence of voluntary motor
302 A Meilink et al.
control, early stimulation by EMG-NMES may be
able to facilitate cerebral reorganization and hence
to maximize the effect of sensorimotor relearning.
In line with this hypothesis, Butefisch et al.48
showed that during the first weeks post stroke in
particular, the motor cortex is characterized by
hyperexcitability, probably due to reduced
GABA-ergic intrahemispheric and transhemi-
spheric inhibition (i.e. downregulation). The
increased predominantly excitatory activity
in the neuronal circuits found in patients with a
favourable recovery of the upper limb may be
enhanced by afferent stimulation early post
stroke.48
Another factor that may explain the differences
in individual effect sizes between the included
studies may be the differences in the criteria for
including upper limb deficits in the randomized
controlled trials. For example, Hemmen et al.38
and Francisco et al.33 did not use wrist and
finger extension ability to include or exclude
patients, even though wrist and finger extension
has predictive value for the functional use of the
hand.7 A recent study showed that it is especially
the functional integrity of the corticospinal system
which is responsible for the level of motor impair-
ment.49 Hence, it is important for future studies to
carefully select or stratify patients with an initially
poor or favourable prognosis for functional recov-
ery of the upper limb.
Recently, Cauraugh and colleagues50 have sug-
gested that bilateral upper limb training with
EMG-NMES may be more effective than unilat-
eral training.35,36 In a review from 2006, Stewart
et al.50 indicated that bilateral symmetrical
movements may enhance hand motor recovery
after stroke. Bilateral movements activate motor
synergies between limbs and facilitate movements
in the paretic limb. Bilateral movements or other
interventions like constraint-induced movement
therapy51 may thus be valuable supplements to
EMG-NMES treatment in regaining functionality
of the hand after stroke. However, the evidence for
bilateral upper limb training with EMG-NMES
above unilateral stimulation needs to be under-
pinned in a large randomized clinical trial.
The present meta-analysis had a number of
limitations. First, we may have missed relevant
studies not published in scientific journals or
published in languages other than English,
German or Dutch. Second, the present study suf-
fered from a lack of information about the exact
dosage and content of EMG-NMES therapy, due
to the lack of information in the individual articles.
Although we contacted the authors, some data
related to patient characteristics were not
available. Third, because of a lack of sufficient
numbers of randomized controlled trials, we were
not able to perform a sensitivity analysis to reveal if
voluntary motor control of wrist and finger exten-
sors at baseline is essential for finding significant
overall effects in terms of dexterity. Due to the poor
methodological quality, the low statistical power
(type II error) to reject the H0 and accept the H1
hypothesis, the low treatment contrast, and the fact
that patients were selected beyond the first weeks
post stroke, there is a need for a multicentre study
of EMG-NMES in the near future.
Clinical messages
 Return of finger extension is critical for
improvement of dexterity after stroke.
 A systematic review of the literature shows
that the surplus value of EMG-NMES
intended to improve wrist and finger exten-
sion is lacking when compared with usual
care.
 Because the return of dexterity is not fully
defined within the initial five weeks post
stroke, future studies should investigate the
effects of EMG-NMES within this critical
time window.
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 EMG stimulation of the wrist and finger extensors 305

Appendix 1 – Selection process for studies included in the meta-analysis

Electronic database search (n = 192) +
reference search (n = 4)

Articles excluded on the basis of title or

abstract (n = 162)

Articles retrieved for further evaluation

(n = 34)

Reasons for exclusion (n = 26):

1) Patients not diagnosed as stroke patients (n = 2)
2) No application of EMG-NMES (n = 13)
3) Placement of electrodes on other muscles than the
extensors of the forearm (n = 1)
4) Studies other than RCTs (n = 6)
5) Other languages than English, German or Dutch
(n = 1)
6) EMG-NMES as control group intervention (n = 1)
7) Articles using an adjunct therapy besides
EMG-NMES, such as conventional electrical stimulation
but not exercise therapy (n = 2)

RCTs included in the meta-analysis

(n = 8)

 Extensor*
Search strategy  #6 OR #7 OR #8 OR #9 OR #10
 Neuromuscular stimulat*
 Cerebrovascular accident [MeSH]  Electric stimulation therapy [MeSH]
 Cerebrovascular disorders [MeSH]  Electrostimulation
 Hemiplegia [MeSH]  Electrical stimulation [MeSH]
 Basal Ganglia Cerebrovascular Disease [MeSH]  #12 OR #13 OR #14 OR #15
 #1 OR #2 OR #3 OR #4  Electromyography [MeSH]
 Upper extremity [MeSH]  EMG-triggered
 Hand joints [MeSH]  Rehabilitation
 Muscle spasticity [MeSH]  #17 OR #18 OR #19
 Flexor*  #5 AND #11 AND #16 AND #20
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