Effect of EMG-triggered neuromuscular electrical stimulation with bilateral arm training on hemiplegic shoulder pain and arm function after stroke: a randomized controlled trial
Chuang et al. Journal of NeuroEngineering and Rehabilitation
Effect of EMG-triggered neuromuscular electrical stimulation with bilateral arm training on hemiplegic shoulder pain and arm function after stroke: a randomized controlled trial
Li-Ling Chuang 1 3 4
You-Lin Chen 1
Chih-Chung Chen 1 3 4
Yen-Chen Li 7
Alice May-Kuen Wong 1 3
An-Lun Hsu 0 2
0 Equal contributors
1 Department of Physical Therapy and Graduate Institute of Rehabilitation Science, College of Medicine, Chang Gung University , Taoyuan , Taiwan
2 Department of Physical Therapy, Mackay Memorial Hospital , Taipei , Taiwan
3 Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Linkou Medical Center , Taoyuan , Taiwan
4 Healthy Aging Research Center, Chang Gung University , Taoyuan , Taiwan
5 No. 259, Wenhua 1st Rd., Guishan Dist., Taoyuan 33302 , Taiwan
6 Neuroscience Research Center, Chang Gung Memorial Hospital, Linkou Medical Center , Taoyuan , Taiwan
7 Physical therapy, Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital , Taoyuan , Taiwan
Background: Hemiplegic shoulder pain is a frequent complication after stroke, leading to limited use of the affected arm. Neuromuscular electrical stimulation (NMES) and transcutaneous electrical nerve stimulation (TENS) are two widely used interventions to reduce pain, but the comparative efficacy of these two modalities remains uncertain. The purpose of this research was to compare the immediate and retained effects of EMG-triggered NMES and TENS, both in combination with bilateral arm training, on hemiplegic shoulder pain and arm function of stroke patients. Methods: A single-blind, randomized controlled trial was conducted at two medical centers. Thirty-eight patients (25 males and 13 females, 60.75 ± 10.84 years old, post stroke duration 32.68 ± 53.07 months) who had experienced a stroke more than 3 months ago at the time of recruitment and hemiplegic shoulder pain were randomized to EMG-triggered NMES or TENS. Both groups received electrical stimulation followed by bilateral arm training 3 times a week for 4 weeks. The primary outcome measures included a vertical Numerical Rating Scale supplemented with a Faces Rating Scale, and the short form of the Brief Pain Inventory. The secondary outcome measures were the upper-limb subscale of the Fugl-Meyer Assessment, and pain-free passive shoulder range of motion. All outcomes were measured pretreatment, posttreatment, and at 1-month after post-treatment. Two-way mixed repeated measures ANOVAs were used to examine treatment effects. Results: Compared to TENS with bilateral arm training, the EMG-triggered NMES with bilateral arm training was associated with lower pain intensity during active and passive shoulder movement (P =0.007, P =0.008), lower worst pain intensity (P = 0.003), and greater pain-free passive shoulder abduction (P =0.001) and internal rotation (P =0.004) at follow-up. Both groups improved in pain at rest (P =0.02), pain interference with daily activities, the Fugl-Meyer Assessment, and pain-free passive shoulder flexion and external rotation post-treatment (P < 0.001) and maintained the improvement at follow-up (P < 0.001), except for resting pain (P =0.08). (Continued on next page)
(Continued from previous page)
Conclusions: EMG-triggered NMES with bilateral arm training exhibited greater immediate and retained effects than
TENS with bilateral arm training with respect to pain and shoulder impairment for chronic and subacute stroke patients
with hemiplegic shoulder pain.
Trial registration: NCT01913509.
Hemiplegic shoulder pain is a common complication
following stroke that restricts shoulder mobility and may
interfere with rehabilitation [
]. Initial post-stroke
weakness and spasticity lead to shoulder instability and
immobility, which can cause pain directly or place the
capsule at risk for trauma, subsequently leading to pain
]. The etiology of hemiplegic shoulder pain is
multifactorial, including shoulder subluxation, spasticity in the
pectoralis major and subscapularis, adhesive capsulitis,
bursitis, tendonitis, and shoulder-hand syndrome [
Accordingly, a wide variety of current treatment
regimens have been used, such as shoulder positioning,
slings and support aids, strapping and taping, surgical
interventions, triamcinolone acetonide injections,
electrical stimulation, and so on [
The most promising interventions for hemiplegic
shoulder pain are surface or percutaneous neuromuscular
electrical stimulation (NMES) and intraarticular corticosteroid
]. Although corticosteroid injections may
give satisfactory results, potential side effects include
postinjection flare and tendon rupture . Percutaneous NMES
requires invasive procedures to implant electrodes and
poses the risk of electrode-related infections, which makes
clinical implementation difficult [
]. Given the potential
adverse effects of percutaneous NMES, it is more
conservative to use surface NMES for hemiplegic shoulder pain.
NMES and transcutaneous electrical nerve stimulation
(TENS) are two widely used interventions to reduce pain
in clinical practice [
]. The distinction between these
two interventions is that NMES is used to produce muscle
tetany to improve pain, whereas TENS is specifically used
for pain relief at the sensory level, with no muscle
]. Theoretically, NMES helps contract and
strengthen muscles to prevent disuse atrophy, relax
muscle spasm, increase blood circulation and nutrition of
the muscles, and reeducate muscles [
2, 9, 10
Eight controlled trials of surface NMES for hemiplegic
shoulder pain have been reported [
stimulation was applied over periods ranging from 4 weeks to
3 months. Some of these studies demonstrated that
NMES not only reduced shoulder pain and subluxation
11, 12, 16, 18
], but also improved shoulder abduction
and arm function in patients with acute stroke [
In contrast, Church et al. found no difference in
upperlimb pain and arm function between NMES and placebo
groups after acute stroke . The authors proposed
that surface NMES may interfere with upper-limb motor
recovery by producing artificial proximal stimulation
]. Wang et al. found that a NMES program
significantly improved motor function for patients with acute
stroke, but had no effect on pain-free passive external
shoulder rotation [
]. However, significant differences
in the severity of baseline disability between groups
made their interpretations uncertain. The disparity in
these studies could be due to many factors, among
which are the heterogeneity of study populations,
interventions, and outcome measures used; inconsistent
definitions of hemiplegic shoulder pain [
]; inclusion of
subjects without shoulder pain [
]; and lack of an
appropriate guide for treatment modality selection [
Moreover, the existence of different treatment doses
may have generated bias in some studies, in which the
experimental group received NMES therapy in addition
to conventional rehabilitation and had more attention to
their shoulder than the control group [
12, 14, 15, 18
Finally, most of the studies did not examine the effects of
NMES beyond the termination of treatment.
Recently, surface NMES has been applied in
combination with other approaches to create a task-specific
training paradigm [
]. Chan et al. found that surface NMES
with bilateral arm training produced significant
improvements in arm function and active wrist extension when
compared with placebo stimulation with bilateral arm
]. Cauraugh and Kim combined
electromyography (EMG)-triggered NMES with bilateral arm training
and showed improved motor control in a bimanual task
]. De Kroon et al. found EMG-triggered NMES
may be more effective than non-triggered stimulation in
producing improvements in motor control of the
hemiparetic arm . EMG-triggered NMES is unique in that it
requires subjects’ active participation in the training via
cognitive intent to trigger electrical stimulation and
activate the corresponding NMES-induced muscle
]. Accordingly, it would be interesting to
investigate the effects of EMG-triggered NMES with
bilateral arm training on hemiplegic shoulder pain. However,
there is a lack of research on the combined effects of
EMG-triggered NMES and functional training to identify
the most effective strategy for reducing hemiplegic
shoulder pain and improving arm function. Therefore, the
primary aim of this study was to investigate the effects of
EMG-triggered NMES combined with bilateral arm
training on hemiplegic shoulder pain and arm function, as
compared with TENS combined with bilateral arm
training, in subacute and chronic stroke patients. The
secondary aim was to evaluate the retention of the treatment
effect at 1 month after the intervention. The primary
hypothesis was that NMES combined with bilateral arm
training would improve pain and arm function more than
TENS combined with bilateral arm training, and the
secondary hypothesis was that the therapeutic effects of
NMES combined with bilateral arm training would be
retained more than those of TENS combined with
bilateral arm training.
Subjects were recruited from two medical centers
(Mackay Memorial Hospital and Chang Gung Memorial
Hospital). The recruitment criteria were as follows: (1)
firstever stroke with onset >3 months prior at time of
recruitment; (2) at least mild intensity of hemiplegic shoulder
pain with activity in the past 7 days (Numerical Rating
Scale score ≥ 1); (3) no other neurological disorders, such
as Parkinson’s disease, epilepsy, multiple sclerosis, etc.; (4)
adequate cognitive ability (Mini-Mental State Examination
score ≥ 24). The exclusion criteria were (1)
contraindications for electrical stimulation (e.g., metal implants,
cardiac pacemaker); (2) pre-existing pathology of the
shoulder, such as rotator cuff injury or tendonitis, frozen
shoulder, etc.; (3) participation in any experimental
rehabilitation or drug studies during the study period; (4)
change of pain medication during the study period; (5)
treatment of upper limb spasticity, including botulinum
toxin injection or neurolytic or surgical procedures; (6)
aphasia; and (7) severe cognitive deficits.
The study was approved by the Institutional Review
Boards of the participating sites. All participants
provided written informed consent and were informed of
the study’s purpose, the process, and their right to
withdraw from the study at any time.
Study design and randomization
This study was a single-blind, randomized controlled trial.
The ClinicalTrials.gov identifier number is NCT01913509.
The Consolidated Standards of Reporting Trials
(CONSORT) flow chart is presented in Fig. 1. After obtaining
written informed consent, the eligible participants were
randomly assigned to one of two training groups
according to a computer-generated list, with stratification by side
of brain lesion. The stratification was performed since
recovery profile is influenced by the initial stage, such as side
of lesion and motor severity. The two training groups
included: (1) EMG-triggered NMES with bilateral arm
training; (2) TENS with bilateral arm training. The allocation
sequence was carried out by a research assistant and
concealed in opaque, sealed envelopes. Participants were
blinded to the type of treatment.
The participants received the interventions for 12 sessions
(3 days/week for 4 weeks). Participants in the
experimental group received EMG-triggered NMES and
those in the control group received TENS for 20 min.
After the EMG-triggered NMES or TENS, all participants
received 20 min of bilateral arm training, including
bilateral arm raises, bilateral arm reaching forward, bilateral
shoulder abduction, and bilateral shoulder horizontal
abduction at pain-free range. The number of repetitions of
the bilateral arm training exercises was based on each
individual’s capability and was gradually increased
throughout the treatment sessions.
A portable, two-channel neuromuscular stimulator
(PAS System™ GD601: OG GIKEN Company, Okayama,
Japan) with trigger mode was used to deliver
EMGtriggered NMES for the experimental group. Trigger
mode was used to start the low frequency output when
EMG feedback was detected. The system uses a
threeelectrode format and EMG feedback detection to allow
EMG-triggered electrical stimulation of the target
muscles (i.e., supraspinatus and posterior deltoid). The gain
dial was used to adjust the sensitivity of EMG feedback
detection and the EMG monitor lit up when EMG
feedback was detected. When EMG feedback over the level
set with the gain dial was detected, the output voltage
was gradually increased. After a certain duration, the
output voltage was gradually decreased to allow the
muscle to return to a resting state. After the rest time
passed, the next EMG feedback detection was enabled.
The supraspinatus and posterior deltoid muscles were
selected as the targets for treatment, as they are key
muscles in maintaining correct shoulder alignment and
providing stabilization of the shoulder joint [
10, 25, 26
Therapeutic electrical stimulation to the supraspinatus
and posterior deltoid muscles has been shown to
effectively reduce shoulder subluxation and pain, increase
muscle force, and facilitate shoulder stability [
]. Electrode placement for the supraspinatus and
posterior deltoid muscles was assisted by palpation,
visual inspection of the muscles, and skin markings for the
spine of the scapula and the acromion process. Two
active electrodes were placed over the palpated muscle
belly along the length of the muscle. Electrode
placement for the supraspinatus was 1.5 cm superior to the
midpoint of the spine of the scapula. Electrode
placement for the muscle belly of the posterior deltoid was
two fingerwidths inferior to the posterior margin of the
acromion process [
]. Participants were instructed to
initiate a voluntary isotonic contraction of the shoulder
abductors and horizontal abductors with effort,
respectively. Surface electrodes detected the EMG feedback
signal at the target muscle and then the target muscle was
electrically stimulated. A stimulation frequency of 30 Hz
was used to generate a tetanized contraction, and the
intensity was individually adjusted to produce significant
muscle contraction within the maximum tolerance level.
The range of intensities used to stimulate the muscles
was 3–5 out of 10. The contraction-relaxation ratio of
EMG-triggered NMES was adjusted progressively from
10/10 s to 30/10 s [
]. There were no adverse events,
such as burns or skin allergic responses, during the
The control group received TENS on the supraspinous
fossa and posterior deltoid muscles of the painful
shoulder, which was performed by a portable stimulator unit
(SW320, Shining World Health Care Co., LTD., Taiwan)
at a frequency of 30 Hz. TENS was applied using a similar
treatment protocol, electrode placement, and stimulation
frequency as the experimental group. According to the
manufacturer’s instructions, the level of intensity was set
from 1 through 5 at the highest comfortable setting but
below the motor threshold, as the intensity setting varies
individually. To find the electrode placement for the target
muscles, the participants in the TENS group initiated a
voluntary movement and received higher level of
stimulation intensity at the beginning. Then the intensity of
stimulation was adjusted gradually to lower level to the
maximum tolerable sensory level without muscle
All outcomes were measured pretreatment,
posttreatment, and 1 month after posttreatment. Hemiplegic
shoulder pain can interfere with activities of daily living
and subsequently lead to disability and poor functional
recovery of the affected arm. To determine pain intensity
and pain interference with daily activities, two pain
measures (a vertical Numerical Rating Scale supplemented
with a Faces Rating Scale [NRS-FRS] and the short form
of the Brief Pain Inventory [BPI-SF]) were chosen as the
primary outcome measures. Regarding the extent of
upper-limb impairment and dysfunction, two measures
(the upper-limb subscale of the Fugl-Meyer Assessment
[FMA-UL] and pain-free passive shoulder range of
motion) were chosen as the secondary outcome measures.
Pain intensity was measured on a 10-point vertical
NRS with word anchors supplemented with the six facial
expressions of the FRS, facilitating the scoring of pain.
Participants were asked to rate the intensity of their
hemiplegic shoulder pain at rest, and during active and
passive range of motion of the affected shoulder.
Shoulder pain was significantly more frequent in subjects with
limitation of flexion, abduction, and external rotation of
]. For the assessment of shoulder pain
during movement, immediately following the
performance of active and passive shoulder range of motion,
subjects were asked to mark the vertical NRS-FRS at the
point that corresponded to the level of pain they
experienced during shoulder flexion, abduction, and external
rotation, respectively. The vertical NRS-FRS is a reliable
measure of pain after stroke, with good test-retest
The BPI-SF is a 9 item questionnaire for the assessment
of worst, least, average, and current pain intensity and the
degree that pain interferences with daily activities on a 10
point scale [
]. The statement of question 3 of the
BPISF was as follows: “Please rate your pain by marking the
number that best describes your pain at its worst in the
last 24 hours.” Question 3 of the BPI-SF was used to ask
participants to rate the worst shoulder pain intensity in
the past 24 h, with 0 being “no pain” and 10 being “pain
as bad as you can imagine.” The statement of question 9
of the BPI-SF was as follows: “Mark the number that
describes how, during the past 24 hours, pain has interfered
with your general activity, mood, walking ability, normal
work, relations with other people, sleep, and enjoyment of
life, respectively.” Question 9 of the BPI-SF was used to
estimate the degree to which shoulder pain interfered with
daily life in the past week, with 0 being “no interference”
and 10 being “interferes completely.” The BPI-SF has
demonstrated good reliability and validity for clinical pain
assessment across cultures and languages. A Chinese
version of the BPI-SF was developed and proven to be a
reliable and valid measure of both the severity and impact of
pain among Taiwanese cancer patients [
The FMA-UL was used to measure motor impairment
]. The FMA-UL includes 33 items (total score: 0–66
points) and is scored on a 3-point ordinal scale (0
=cannot perform, 1 =performs partially, 2 =performs
completely), with good reliability and validity [
FMA-UL can be divided into 21 proximal (0–42 points)
and 12 distal (0–24 points) items. A higher score on the
FMA-UL indicates better motor function. Limited range
of passive shoulder external rotation and abduction was
correlated highly with hemiplegic shoulder pain [
]. Motor impairment and pain were also assessed by
measuring the pain-free passive range of motion of the
hemiplegic shoulder using a clinical goniometer, where a
loss of range indicated an increase in pain .
Sample size calculation
The sample size calculation was performed with G*Power
3 (a statistical power analysis program) [
]. The effect
size computation was based on Cohen’s d, with an
expected effect of 0.2 to 0.5. Two-way mixed repeated
measures ANOVA indicated that a total sample size of 28 was
needed to reach 80% power to detect an interaction effect
size of 0.25 at the 0.05 level of significance. The sample
size requirement for each group in a 2-group study design
was 14 subjects. With a potential 20% attrition rate, a total
of 34 subjects were targeted for this study.
The independent t-test and χ2 test were used to compare
the baseline characteristics between groups. Descriptive
statistics were presented using the mean (standard
deviation) or median (range) for continuous variables, or
numbers for categorical variables. The effect of the
interventions on the primary and secondary outcomes was
analyzed using 2 × 3 mixed repeated measures ANOVAs
with group (i.e. NMES combined with bilateral arm
training, TENS combined with bilateral arm training) as the
between-subject factor and time (i.e. pretreatment,
posttreatment, 1-month follow-up) as the within-subject
factor. Effect sizes were calculated as partial eta squared
(η2) for ANOVA results. Post hoc planned pairwise
comparisons through t-tests, with Bonferroni correction
for multiple comparisons, were performed when
significant interactions or main effects for factors were observed.
In addition, subgroup analysis was used to compare the
changes in outcomes over time from pretreatment to
post-treatment and follow-up in subjects with or without
subluxation (i.e., NMES combined with bilateral arm
training group without subluxation, NMES combined with
bilateral arm training group with subluxation, TENS
combined with bilateral arm training group without
subluxation, TENS combined with bilateral arm training group
with subluxation) by using ANOVAs. The significance
level was set at 0.05. Statistical analyses were performed
with SPSS 20.
This study was conducted from December 2013 to June
2017. Thirty-eight participants were randomized, 19 in
NMES combined with bilateral arm training and 19 in
TENS combined with bilateral arm training. No
participant was lost to follow-up, and none were excluded after
randomization, such that all 19 participants in each
group were included in the final analysis according to
their originally assigned groups. The baseline
characteristics of the 38 participants are summarized in Table 1.
Nine subjects (47%) in the NMES combined with
bilateral arm training group and 8 subjects (42%) in TENS
combined with bilateral arm training group had shoulder
subluxation, which was measured by palpation of the
space between the acromion and the humeral head. The
size of the space was quantified by how many fingers
could be placed between the acromion and the humerus
]. There was no statistically significant difference
between the 2 groups at pretreatment. No harms or
unintended effects were reported in either group.
Effect of interventions on primary outcomes
Two-way mixed ANOVA revealed a significant time effect
(F1.17, 42.04 =4.65, P =0.03, partial η2 =0.11, observed power
=0.60), and no significant interaction and group effects
(P > 0.05) on the vertical NRS-FRS for assessing pain at
rest (Table 2). Both groups had significantly decreased
shoulder pain at rest after the interventions (P =0.02).
There was a significant interaction of time and group on
the vertical NRS-FRS for assessing pain during active
shoulder range of motion (F1.45, 52.22 =5.84, P =0.01, partial
η2 =0.14, observed power =0.77) and during passive
shoulder range of motion (F2, 72 =11.83, P < 0.001, partial η2
=0.25, observed power =0.99). Significant between-group
differences were found in pain during active and passive
shoulder range of motion at follow-up (P < 0.05) (Fig. 2).
The NMES combined with bilateral arm training group
had lower pain intensity during active and passive
shoulder movement than the TENS combined with bilateral
Abbreviations: SD indicates standard deviation; n, subgroup number, NMES
neuromuscular electrical stimulation, TENS transcutaneous electrical nerve
stimulation, BAT bilateral arm training
aShoulder subluxation was defined as incorrect alignment between the
scapula and the humerus, as compared with the unaffected shoulder
NRS-FRS during shoulder 3.89 ± 3.00
NRS-FRS during shoulder 5.79 ± 2.10
BPI-SF question 3 worst pain BPI-SF question 9 pain interference
arm training group. Both groups showed significant
reductions in pain intensity during shoulder movement after
the interventions (P < 0.05). However, the NMES
combined with bilateral arm training group maintained the
improvement in pain reduction during passive shoulder
range of motion at follow-up, whereas the TENS
combined with bilateral arm training group had increased pain
intensity at follow-up compared with post-treatment (P =
0.01) (Fig. 2b). These results suggest that the NMES
combined with bilateral arm training intervention produced
longer-lasting pain relief than TENS combined with
bilateral arm training.
There was a significant time-group interaction on
question 3 of the BPI-SF (F1.47, 52.94 = 10.84, P < 0.001, partial
η2 = 0.23, observed power = 0.96). Both groups showed
significant reductions in the worst pain intensity
posttreatment, but only the NMES combined with bilateral
arm training group maintained pain reduction at follow-up
(P < 0.05). A significant difference was found between
groups on question 3 of the BPI-SF post-treatment and at
follow-up (P = 0.033 and P = 0.003, respectively). The
NMES combined with bilateral arm training group had
significantly greater reductions in the worst pain than the
TENS combined with bilateral arm training group
posttreatment and at follow-up (from 5.95 to 2.58 and 2.11
with NMES combined with bilateral arm training vs. from
5.21 to 3.95 and 4.05 with TENS combined with bilateral
Table 1 Baseline characteristics of the participants
NMES-BAT TENS-BAT (n = 19) (n = 19) Age (mean years ± SD) 58.89 ± 11.93 62.61 ± 9.59
arm training) (Fig. 3). A significant time effect on question
9 of the BPI-SF for assessing pain interference was found
(F1.27, 45.62 = 20.62, P < 0.001, partial η2 = 0.36, observed
power = 1.00). Both groups showed significant reductions
in pain interference post-treatment and at follow-up (P <
0.05) (Table 2).
Effect of interventions on secondary outcome measures
For total, proximal, and distal scores on the FMA-UL,
repeated measures ANOVA showed a significant time effect
(total: F1.27, 45.58 = 12.60, P < 0.001, partial η2 = 0.26,
observed power = 0.97; proximal: F1.39, 50.13 = 12.98,
P < 0.001, partial η2 = 0.27, observed power = 0.98; distal:
F1.23, 44.21 = 3.88, P = 0.05, partial η2 = 0.10, observed
power = 0.54), but no group-time interaction or group
effects (P > 0.05) (Table 3). Both groups showed significant
improvements in the total score and proximal score of the
FMA-UL post-treatment and maintained the
improvement at follow-up (P < 0.05). There was no significant
group effect, but the NMES combined with bilateral arm
training group had a numerically larger increase in the
total score of upper-limb subscale of the FMA-UL than
the TENS combined with bilateral arm training group
post-treatment and at follow-up. The mean changes in
overall scores from pretreatment to post-treatment and
follow-up were 4.06 and 4.37 points (proximal: 3 and 3.27
points; distal: 1.06 and 1.11 points) for the NMES
combined with bilateral arm training group and 1.63 and 1.31
points (proximal: 1.21 and 0.89 points; distal: 0.42 and
0.42 points) for the TENS combined with bilateral arm
training group, respectively.
There was no significant group-time interaction in
painfree passive shoulder range of motion except for passive
shoulder internal rotation (F2, 72 = 4.74, P = 0.01, partial
η2 = 0.12, observed power = 0.78) (Table 3). A significant
difference was found between groups on passive shoulder
internal rotation at follow-up (P = 0.004). Moreover, there
was a significant group effect on pain-free passive
shoulder abduction (F1, 36 = 5.23, P = 0.03, partial η2 = 0.13,
observed power = 0.61) (Table 3). The NMES combined with
bilateral arm training group had better pain-free passive
shoulder abduction than the TENS combined with
bilateral arm training group at follow-up. A significant time
effect was found in pain-free passive shoulder abduction,
flexion, and external rotation (P < 0.001). Both groups
showed significant improvements in pain-free passive
shoulder abduction, flexion, and external rotation
posttreatment and at follow-up (P < 0.05) (Table 3).
Comparative effectiveness of interventions in subjects with and without subluxation
Subgroup analyses showed that a significant group effect
was identified only for the change in score on the
vertical NRS-FRS during active (from pretreatment to
follow-up: F3, 34 = 3.42, P = 0.03) and passive shoulder
range of motion (from pretreatment to post-treatment:
F3, 34 = 3.42, P = 0.03; from pretreatment to follow-up:
F3, 34 = 7.97, P < 0.001). NMES combined with bilateral
arm training, in patients both with and without
subluxation, produced greater reductions in pain during active
shoulder movement at follow-up than the TENS
combined with bilateral arm training in patients with
subluxation (P = 0.02; P = 0.01, respectively). The NMES
combined with bilateral arm training group with
subluxation improved more on pain during passive shoulder
movement at post-treatment and follow-up than the
TENS combined with bilateral arm training group with
or without subluxation (P < 0.05).
There was no significant group effect on the change in
scores on the FMA-UL and or on pain-free passive
shoulder flexion, abduction, or external rotation except for
shoulder internal rotation (F3, 34 = 6.22, P = 0.002). Both
the NMES combined with bilateral arm training groups
with and without subluxation improved more in terms of
pain-free range of shoulder internal rotation at follow-up
than the TENS combined with bilateral arm training
group with subluxation (P < 0.001 and P = 0.01,
respectively). The mean change in overall scores of the
FMA-UL from pretreatment to post-treatment was 4.44
and 3.70 points for the NMES combined with bilateral
arm training group with and without subluxation,
respectively, and 1.88 and 1.45 points for the TENS combined
with bilateral arm training group with and without
To our knowledge this is the first randomized controlled
study that examined the effects of NMES combined with
bilateral arm training on hemiplegic shoulder pain. In
support of our hypotheses, this randomized controlled
trial provides evidence that the immediate and retained
effects of NMES combined with bilateral arm training in
reducing pain and improving arm function were better
than TENS combined with bilateral arm training for
stroke patients with hemiplegic shoulder pain. The results
demonstrated that EMG-triggered NMES with bilateral
arm training was superior to TENS with bilateral arm
training in reducing hemiplegic shoulder pain during
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shoulder movement, lessening the worst shoulder pain,
and increasing pain-free shoulder abduction and internal
rotation at follow-up. Both groups improved on pain
interference, motor impairment, and pain-free shoulder
abduction, flexion, and external rotation.
Pain reduction in people with stroke
Our results are consistent with previous studies showing
positive effects of NMES on pain reduction in stroke
12, 14, 16, 18
]. Our previous study showed that the
smallest real difference in the vertical NRS-FRS for
measuring pain after stroke was 1.87 points . In this study,
the NMES combined with bilateral arm training group’s
scores on the vertical Numerical Rating Scale
supplemented with a Faces Rating Scale decreased by 2.94 points
during active shoulder range of motion and by 3.53 points
during passive shoulder range of motion at
posttreatment. The mean changes from pretreatment to
posttreatment exceeded the measurement error and were real
at the 90% confidence level.
It is noteworthy that the effects of NMES combined
with bilateral arm training on pain reduction during
movement were maintained for 1 month after the
intervention ceased for subjects both with and without
subluxation. It is possible that the active participation of the
NMES group during the intervention further motivated
them to continue using the paretic arm, producing
longlasting effects on pain reduction and pain-free passive
shoulder abduction and internal rotation. Conversely,
the score on the vertical NRS-FRS in the TENS
combined with bilateral arm training group increased at the
follow-up assessment, approaching pretreatment levels,
especially for subjects with subluxation.
Hemiplegic shoulder pain is a complex phenomenon.
Its pathophysiology is not yet fully understood, which
results in uncertainty regarding the optimal management
strategy for hemiplegic shoulder pain. The cause of
hemiplegic shoulder pain is a subject of debate due to its
multifactorial etiology. Shoulder subluxation is
considered an important risk factor for shoulder pain [
this study, 45% of subjects (17 out of 38) had shoulder
subluxation and shoulder pain. Subjects with shoulder
subluxation in the EMG-triggered NMES combined with
bilateral arm training group had more improvement on
pain reduction during shoulder movement than those
with subluxation who received TENS combined with
bilateral arm training. The participants that improved
more on the pain scale were those who received
EMGtriggered NMES combined with bilateral arm training,
regardless of whether they had subluxation.
Previous studies showed that NMES did not decrease
upper-limb pain and improve arm function in patients
with acute stroke [
], and that NMES did not improve
arm recovery and pain-free passive shoulder external
rotation in patients with chronic stroke [
]. In the
present study, NMES combined with bilateral arm
training significantly relieved shoulder pain and increased the
painless range of motion in chronic and subacute stroke
patients. Such differences could be attributed to
differences in stroke chronicity, measurement tools, treatment
dose, and the use of bilateral arm training in this study.
The current study recruited subjects much later than
the previous studies [
13, 16, 18
], i.e., after the onset of
stroke and development of shoulder pain. It has been
proposed that early intervention with NMES in acute
stroke may be more beneficial in patients with mild
upper-limb impairment, but may interfere with arm
recovery in patients with severe impairment [
addition, the most common pain measure used in
previous studies was the VAS, which is not recommended for
measuring pain after stroke [
]. Finally, the stimulation
protocol in this study differed from previous studies in
frequency and duration. Investigation of the optimal
dosage of the treatment program to maximize the effects
of NMES needs to be determined in future research.
Both groups experienced significant reductions in the
worst pain intensity post-treatment and pain
interference with daily activities. Only the NMES combined
with bilateral arm training group maintained the
improvement in the worst pain intensity at follow-up.
These results were in line with a previous study that
showed peripheral nerve stimulation therapy
significantly improved pain interference and lessened pain
]. The retention of the effects of NMES
combined with bilateral arm training was similar to that
reported in a previous study of intramuscular electrical
stimulation in reducing hemiplegic shoulder pain at
12 months post-treatment [
]. Chae et al. defined
treatment success as a minimum 2-point reduction in the
BPI-SF question 3 post-treatment [
]. In the current
study, the mean change in scores on the BPI-SF question
3 from pretreatment to post-treatment in the NMES
combined with bilateral arm training group exceeded 2
points (3.37 points), while those in the TENS combined
with bilateral arm training group failed to reach this
threshold (1.26 points). Given these results, we suggest
that short-term EMG-triggered NMES may be a good
alternative to long-duration intramuscular electrical
stimulation for inducing voluntary contraction and
providing pain relief.
Advantages of bilateral arm training
In the current study, both groups improved significantly
on the FMA-UL. Lin et al. found that bilateral arm
training significantly reduced motor impairment of the
affected upper limb in stroke patients [
]. Bilateral arm
training comprises repetitive bilateral arm movements in
symmetrical or alternating patterns [
] by which
participants learn to shape the movement trajectory of
the affected arm as symmetrically as the non-affected
arm. Bilateral arm training can induce concurrent
activation of the ipsilateral tracts, cortical disinhibition, and
other neural cross-talk, resulting in improved motor
control in the affected limb [
]. Thus, bilateral arm
training has been proposed to be a potential
rehabilitation intervention for upper-limb hemiparesis, especially
in the proximal region [
Benefits of EMG-triggered NMES with bilateral arm training
Although there was no significant between-group
difference on the FMA-UL, the mean changes in the total score
of the FMA-UL from pretreatment to post-treatment and
follow-up were 4.06 and 4.37 points for the NMES
combined with bilateral arm training group and 1.63 and 1.31
points for the TENS combined with bilateral arm training
group, respectively. The estimated minimal clinically
important difference on the total score of the FMA-UL in
patients with chronic stroke is 4.25 points, and only the
NMES combined with bilateral arm training group
experienced changes close to this threshold [
improvement of the total score of the FMA-UL after NMES
combined with bilateral arm training was mainly on the
proximal score of the FMA-UL (3 and 3.27 points from
pretreatment to post-treatment and follow-up,
respectively). The benefit on the upper-limb subscale of the
FMA-UL was probably attributed to an augmented
intervention effect of NMES and bilateral arm training.
EMGtriggered NMES can augment movement of the
hemiparetic arm, increase cognitive attention through
proprioceptive sensory feedback, and may enhance arm function in
stroke patients [
]. Bilateral arm training was reported to
produce greater gains in the proximal score of the
FMAUL than a control intervention in patients with chronic
]. The additional facilitation in the affected arm
is probably because concurrent activation of both arms
facilitates intracortical activity and decreases inhibition in
both hemispheres [
]. Given this perspective, it is
hypothesized that repetitive muscle contraction and
cognitive involvement in generating repetitive movements are
critical for redeveloping spontaneous motor control [
Limitations of this study were a lack of placebo control
and the short duration of follow-up. Perhaps a longer
period of evaluation would have generated proportionately
different outcomes between the treatment groups.
Moreover, research that compares the intervention effects of
EMG-triggered NMES combined with bilateral arm
training, EMG-triggered NMES only, and bilateral arm training
only would provide more insight into the benefits of the
EMG-triggered NMES combined with bilateral arm
training was better than TENS with bilateral arm
training for reducing hemiplegic shoulder pain during
movement, lessening the worst shoulder pain, and improving
pain-free shoulder abduction and internal rotation for
stroke patients with hemiplegic shoulder pain. Such
improvements appear to be sustained beyond the
immediate time frame of the treatment.
BPI-SF: Short form of the brief pain inventory; FMA-UL: Upper-limb subscale
of the Fugl-Meyer Assessment; NMES: Neuromuscular electrical stimulation;
NRS-FRS: Numerical rating scale supplemented with a faces rating scale;
TENS: Transcutaneous electrical nerve stimulation
We thank Melissa Stauffer for editorial assistance and Chun-Yi Tsai for assistance with the interventions.
This work was partially supported by the Ministry of Science and Technology
(MOST-102-2314-B-182-003, 104–2314-B-182-035-MY3, and
104–2314-B-182007-MY3) and the Healthy Aging Research Center at Chang Gung University
(EMRPD1E1711), and the Chang Gung Memorial Hospital (CMRPD3E0331,
CMRPD1G0041, and CMRPD3E113) in Taiwan.
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author upon request.
LLC and YJC helped acquire funding. YLC, ALH, CCC, and YCL acquired data
and were responsible for training subjects. AMW screened and referred
eligible subjects. LLC and YJC conceived, designed, and coordinated the
study. LLC analyzed and interpreted the data, and was a major contributor in
writing the manuscript. All authors read and approved the final manuscript.
Ethics approval and consent to participate
The study was approved by the Institutional Review Boards of Chang Gung
Medical Foundation (103-7272B) and Mackay Memorial Hospital
(15MMHIS063). All participants provided written informed consent and were
informed of the study’s purpose, the process, and their right to withdraw
from the study at any time.
Consent for publication
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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