Archives of Physical Medicine and Rehabilitation

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Archives of Physical Medicine and Rehabilitation 2018;-:-------

ORIGINAL RESEARCH

Efficiency of Neuromuscular Electrical Stimulation

and Transcutaneous Nerve Stimulation on Hemiplegic
Shoulder Pain: A Prospective Randomized Controlled
Trial
Meimei Zhou, MS,a Fang Li, PhD, MD,b,c Weibo Lu, MD,d Junfa Wu, MD, PhD,b
Song Pei, BScc
From the aDepartment of Rehabilitation, Huadong Hospital, Fudan University, Shanghai; bDepartment of Rehabilitation, Huashan Hospital,
Fudan University, Shanghai; cDepartment of Rehabilitation, Renhe Hospital, Baoshan District, Shanghai; and dDepartment of Rehabilitation,
the First Rehabilitation Hospital, Shanghai, China.

Abstract
Objective: To compare the efficacy of neuromuscular electrical stimulation (NMES) and transcutaneous nerve stimulation (TENS) on hemiplegic
shoulder pain (HSP).
Design: This is a prospective randomized controlled trial.
Setting: A rehabilitation hospital.
Participants: Participants (NZ90) were randomized into NMES (nZ36), TENS (nZ36), or control groups (nZ18).
Interventions: NMES (15Hz, pulse width 200ms) was applied to supraspinatus and deltoids (medial and posterior parts), whereas TENS (100Hz,
pulse width 100ms) was used on the same areas. The surface electrodes were placed near the motor points of the supraspinatus and medial or posterior
bundle of deltoids. The 4-week treatment consisted of 20 sessions, each session composed of 1 hour of stimulation per day. Routine rehabilitation
program without any stimulation was administered to the control and the NMES/TENS groups. Numerical rating scale (NRS), active/passive range of
motion (AROM/PROM) of shoulder, upper extremity Fugl-Meyer Assessment (FMA), modified Ashworth scale (MAS), Barthel Index (BI), and
stroke-specific quality of life scale (SSQOLS) were assessed in a blinded manner at baseline, 2, 4, and 8 weeks after treatment, respectively.
Main Outcome Measures: The primary endpoint was the improvement from baseline in NRS for HSP at 4 weeks.
Results: NRS scores in NMES, TENS, and control groups had decreased by 2.03, 1.44, and 0.61 points, respectively after 4 weeks of treatment, with
statistically significant differences among the 3 groups (P<.001). The efficacy of the NMES group was significantly better than that of the TENS
group (PZ.043). Moreover, the efficacy of NMES and TENS groups was superior to that of the control group (P<.001, PZ.044, respectively).
The differences in the therapeutic efficacy on shoulder AROM/PROM, FMA, MAS, BI, and SSQOLS scores were not significant among the 3 groups.
Conclusions: TENS and NMES can effectively improve HSP, the efficacy of NMES being distinctly superior to that of TENS in maintaining
long-term analgesia. However, NMES was not more efficacious than the TENS or control group in improving the shoulder joint mobility, upper
limb function, spasticity, the ability of daily life activity, and stroke-specific quality of life in HSP patients.
Archives of Physical Medicine and Rehabilitation 2018;-:-------
ª 2018 by the American Congress of Rehabilitation Medicine

Hemiplegic shoulder pain (HSP) is a common poststroke
complication with a reported incidence of 16%-84%.1-3 HSP was
found to be associated with intensified pain, poor functional
Supported by the Research Fund of the Baoshan district committee of science and technology,
Shanghai, China (grant no. 12-E-30).
Clinical Trial Registration No.: ChiCTR-TRC-13004272.
Disclosures: none.
recovery, reduced quality of life, depression, sleeping disorders,
and prolonged hospital stay.1-5
However, the precise pathogenesis of HSP is presently unclear.
Some studies showed that diverse potential etiologies were involved
in the development of HSP. Pong et al found different mechanisms
and contributing factors for HSP at various motor recovery stages.6
The common factors include soft-tissue lesions (shoulder

0003-9993/18/$36 - see front matter ª 2018 by the American Congress of Rehabilitation Medicine
https://doi.org/10.1016/j.apmr.2018.04.020
2 M. Zhou et al
subluxation, rotator cuff injury, adhesive capsulitis),5-8 impaired
motor control (muscle weakness, flaccidity, or spasticity),6,9-12
other peripheral and central nervous system dysfunctions (periph-
eral nerve entrapment, brachial plexus injury, complex regional pain
syndrome, central poststroke pain),2,13-16 and psychological factors
(depression and anxiety).17 These etiologies may be presented
independently or coexist simultaneously.1
Multiple factors are involved in the pathophysiology of HSP,
which includes soft-tissue injury, neuromuscular dysfunction, and
circulatory disturbance.5-17 Correspondingly, the neuromuscular
electrical stimulation (NMES) and transcutaneous nerve stimula-
tion (TENS) are theoretically recommended for treating HSP, due
to their multiple physiological effects such as increasing muscle
strength, improving circulation, promoting wound healing, and
inhibiting pain fibers. NMES is often used at a frequency of 15-50
Hz and a pulse width of 200-400 ms18,19 to alleviate pain, boost
muscle contraction, promote motor relearning,20 and increase the
range of motion. In NMES, 0-100 mA current is used for surface
electrodes and <20 mA for the intramuscular electrodes. TENS is
a noninvasive treatment, based on the gate control theory, that
stimulates the peripheral nerve crude fibers.21 It specifically tar-
gets the sensory nerve fibers and does not activate the motor fibers
with low frequencies, refraining from discernible muscle
contraction.22 Commonly, the conventional TENS is used to
alleviate pain, reduce edema, and repair wounds, with 75-100 Hz,
pulse width of <200 ms, and low amplitude with the sen-
sory threshold.
NMES and TENS are associated with excellent tolerance and
exhibit few adverse effects. Although NMES activates muscle fi-
bers, Baker and Parker23 adopted surface NMES, for the first time,
to treat poststroke shoulder dysfunction and concluded that NMES
could be recommended for treating HSP. Furthermore, Chae
et al24 applied 6 hours of intramuscular electrical stimulation into
the supraspinatus, medial and posterior deltoids, and upper
trapezius daily for 6 weeks, and found a significant relief in
poststroke shoulder pain. The application of TENS in pain relief
could be traced back to the 1960s, and until recently, was useful in
treating HSP. Ekim et al25 used TENS in patients with HSP and
found a remarkable alleviation in HSP and improved passive
external abduction of the shoulder. As demonstrated in another
randomized clinical trial, TENS was more effective than, safer
than, and superior to ultrasonic therapy in treating HSP.26
Although most of the previous studies focused on describing
and evaluating the efficacy of isolated interventions to control
HSP in acute stroke, few investigations compared the different
modalities of treatment in chronic stroke. In addition, because of
the lack of controls and small sample sizes, strong evidence-based
studies regarding the effectiveness of NMES and TENS in treating
HSP are yet limited.
List of abbreviations:
AROM/PROM active/passive range of motion
BI Barthel Index
FMA Fugl-Meyer Assessment
HSP hemiplegic shoulder pain
MAS modified Ashworth scale
NMES neuromuscular electrical stimulation
NRS numerical rating scale
SSQOLS stroke-specific quality of life scale
TENS transcutaneous nerve stimulation
Compared with TENS, NMES is more effective in
improving muscle strength and joint mobility by recruiting a
large number of muscle fibers that might play a critical role in
HSP treatment. The studies addressing the analgesic efficacy of
NMES on HSP have been published in recent years. However,
whether NMES is superior to TENS in alleviating HSP remains
uncertain. The comparison of the effectiveness of these 2
therapies is helpful in understanding the mechanism underlying
the therapy-induced analgesia. According to this study, we
aimed to offer a better option for the electrical stimulation
treatment of HSP.
Methods
Participants
A total of 184 HSP patients, aged 18-80 years, were recruited in the
First Rehabilitation Hospital of Shanghai, China from February
2014 to July 2016. All patients were diagnosed with first stroke. Of
these, 90 were randomized into NMES (nZ36), TENS (nZ36), or
control groups (nZ18). The inclusion criteria were as follows: (1)
hemiplegia in unilateral limb and pain in the hemiplegic shoulder
poststroke; (2) a stable condition and suitability for physical
training; and (3) Mini-Mental State Examination score >24 points
and being able to understand the requirements of test and training.
The exclusion criteria were as follows: (1) a history of shoulder
pain prior to stroke; (2) an unstable medical condition or uncon-
trolled systemic diseases (such as respiratory failure, congestive
heart failure, liver and kidney dysfunction, or any other disorders
affecting neuromuscular function); (3) quadriplegia; (4) those
demanding cardiac pacemakers; (5) administering any nonsteroidal
anti-inflammatory drugs for shoulder pain prior to the study; and
(6) disturbance of awareness, severe visual, and cognitive
impairment.
The patient (and/or caretaker) was informed about the purpose
of the study prior to obtaining the signed consent form. The ethics
approval was obtained from the Institutional Review Board of the
hospital. This study was conducted in accordance with the
Declaration of Helsinki. The trial was registered at http://www.
chictr.org.cn, number ChiCTR-TRC-13004272.
Randomization, Treatment Allocation, and Blinding
A computer-generated randomized number sequence allocated
participants to either the NMES or TENS group and the control
group. The randomization ratio was NMES: TENS: control
groupZ2:2:1. Randomization was managed by clinicians external
to the study. The principal investigator (M.Z.) was responsible for
eligibility assessment, consent, baseline assessment, and treat-
ment. Allocation was assigned after baseline assessment. All
outcomes were measured by a physiatrist who was blinded to the
treatment allocation. Participants remained blinded to allocation.
Outcome Measurements
Demographic data including age, gender, type of stroke, lesion
side, and days poststroke were recorded at baseline. The patients
were assessed at 0 (baseline), 2, 4, and 8 weeks after treatment.
The primary endpoint was the improvement from baseline in the
numerical rating scale (NRS) for HSP at 4 weeks.27
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Efficiency of NMES and TENS on HSP 3

The severity of pain was assessed by a 10-point numeric rating rehabilitation kitb) was used in the same area; the amplitude was
scale (0 representing no pain, 10 meaning unbearable pain, and adjusted to cause minimal discomfort without any discernible
between 0 and 10 indicate a gradual increase in pain). Patients muscle contraction. A total of 20 sessions of 1-hour stimulation
were asked to describe the severity of shoulder pain during passive were conducted daily for 4 weeks, consecutively. Patients in the
forward flexion, abduction, and external rotation of the shoulder 3 groups underwent a standardized rehabilitation program,
joint, and the maximal NRS scores were recorded. The range of which was delivered by occupational therapists and physical
motions were measured in a sitting position using a universal therapists.
goniometry. During measuring of the active/passive range of
motion (AROM/PROM) of shoulder forward flexion and abduc-
tion, the humerus was regarded as the mobile arm, acromion as the Statistics
axis, and the body sideline as the fixed arm. For AROM/PROM of
The objective of this study was to test whether the efficacy of
shoulder lateral external rotation, the forearm served as the mobile
TENS was different from NMES while treating HSP. The primary
arm for measurement, olecranon as the axis, the gravity line as the
efficacy endpoint and improvement between NMES and TENS in
fixed arm, and hemiplegic shoulder position at 0
abduction. The
NRS for HSP at week 4 was used for the estimation of sample
arm function was measured by upper extremity Fugl-Meyer
size. Because NRS is grade data rather than continuous count, for
Assessment28 (FMA, range 0-66, 0: no function; 66: normal
our consideration, 1-point reduction in NRS meant 1-level decline;
function). The tone of shoulder adductors and internal rotators was
hence, the NMES was more efficacious than the TENS. A sample
measured according to the modified Ashworth scale29 (MAS,
size of 72 eligible participants, 30 for the NMES group, 30 for the
range 0-5, 0: no spasticity; 5: joint is rigid). The daily activities
TENS group, and 12 for the control group, was required to achieve
were evaluated by the Barthel Index30 (BI, 0: severe disability;
90% power at the 2-sided 5% significance level to detect a clin-
100: no disability). The quality of life was assessed by stroke-
ically significant treatment difference of 1 point at the common
specific quality of life scale31 (SSQOLS, range 49-245, higher
standard deviation of 0.9. Considering a 20% withdrawal or
scores indicating better quality of life).
nonevaluable rate, the total sample size increased to 90, with 36
participants for the NMES group, 36 for the TENS group, and 18
Treatments for the control group.
SPSS 20.0 softwarea was used for statistical analysis. Statis-
All patients were randomly assigned into the NMES or TENS
tical significance level was set at P<.05. Statistically significant
group and the control group. NMES (15Hz and pulse width 200ms,
differences in demographic data among the 3 groups were
dual channel stimulators, rehabilitation kitb) was applied to
compared using the Pearson chi-square test or Fisher exact test
supraspinatus and deltoids (middle and posterior bundles) in the
for categorical variables, as appropriate. The effective rate,
NMES group. Previous studies showed that stimulating trapezius
which was defined as the proportion exhibiting a reduction of 1
could stabilize the scapula in stroke patients.24,32,33 Because the
point in NRS of 2, 4, and 8 weeks after treatment relative to
scapula only articulates with the clavicle (at the acromioclavicular
baseline, was compared using the Fisher’s exact test among the
joint), the upper trapezius contraction contributes to raising the
groups. The rank-sum test (Kruskal-Wallis test) had been used to
scapula, thereby resulting in an external rotation of the scapula
adjust for baseline and outcome measures among the groups.
with the acromioclavicular joint acting as the pivot. This, in turn,
And analysis of covariance with NRS as a covariate had been
could initiate or worsen subluxation and impingement, thereby
used for analysis when the baseline had a statistically significant
resulting in HSP.34 Therefore, trapezius stimulation is unnecessary
difference. Wilcoxon signed-rank test or Kruskal-Wallis test was
and should be avoided. The supraspinatus can stabilize the hu-
used to analyze the differences within each group before and
merus in the glenoid fossa and coordinate the deltoids to shoulder
after treatment.
abduction. Previous studies postulated that the contraction of the
Full analysis set was used for summarizing the demographic
middle and posterior deltoids was responsible for the observed
and baseline characteristics. Per protocol set referred to those
therapeutic effects on HSP.35 The middle and posterior deltoids
participants in the full analysis set who had completed all the
were adjacent to one another. Therefore, a single surface electrode
visits and had no major protocol violations. The per protocol set
positioned between the motor points of these muscles contribute to
was used for efficacy analyses in this study.
the activation of both muscles simultaneously.
In this study, the surface electrodes were placed near the
motor points of the supraspinatus and medial or posterior bundle
of deltoids. The motor points have been defined as the superficial Results
points of stimulation with the lowest motor threshold, that is, the
points on the skin over the muscle belly, on which a minimal Participants and Baseline Characteristics
amount of current is required to produce muscle contraction.36,37
Therefore, we located the surface electrode (areaZ22cm2) on A total of 184 HSP patients underwent initial screening before
the target muscle belly where the minimal current could induce a enrollment; 90 were randomized into 3 groups (NMESZ36,
visible muscle contraction in this study.38 Moreover, the current TENSZ36, control groupZ18). Nine patients dropped out, 6
intensity was adjusted to produce visible contractions of shoul- were lost to follow-up, 1 refused treatment, 6 discontinued treat-
der abductors (not trapezius) without any discomfort, usually ment because of early discharge, and 2 presented poor general
tens of milliamps (between 20 and 50mA). During stimulation condition during the trial; 5 were from the NMES group and 4
therapy, the stimulator completed a cycle every 30 seconds belonged to the TENS group. Of these, the 2 cases with poor
consisting of 5 seconds to ramp up, 10 seconds at maximum general condition used the nonsteroidal anti-inflammatory drugs
stimulation, 5 seconds to ramp down, and 10 seconds of no during the follow-up period, and the improper care aggravated the
stimulation.35,39 TENS (100Hz and pulse width 100ms, shoulder pain. Finally, a total of 81 patients completed all

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4 M. Zhou et al

evaluations after 4 weeks of treatment, and 19 participants with-
drew at 8 weeks of follow-up. The schematic representation of
patient selection is shown in fig 1. No adverse events were
observed in either of the groups during the 8-week follow-up.
Pathologically, after 1-2 weeks of stroke onset, an acute phase
has passed; and 6 months later, the condition has entered a rela-
tively slow phase of chronic change. Our patients are basically
sorted to the period between these 2 points. A comparison of the
demographic characteristics NRS, AROM/PROM, FMA, MAS,
BI, and SSQOLS scores did not exhibit statistically significant
differences at baseline between the 3 groups (table 1).
Primary Outcome Measurements
The primary outcome measurements, that is, NRS scores, were
decreased by an average of 2.03, 1.44, and 0.61 points in NMES,
TENS, and the control groups after 20 sessions. All differences
were statistically significant among the 3 groups (P<.001)

184 patients received initial screening assessment

54 patients were excluded:

1. Severe cognitive impairment (MMSE<24)

2. Suffered from cerebrovascular disease and left dysfunction

3. Implantation of pacemakers

127 patients met the inclusion criteria 4. Any other disorder that affects neuromuscular function

37 patients were excluded:

1. Unwilling to sign informed consent

2. An unstable medical condition

90 subjects were randomized into NMES, TENS, or control

NMES group (n=36): TENS group (n=36): Control group (n=18):

NMES + conventional TENS + conventional Conventional

rehabilitation program rehabilitation program rehabilitation program

9 patients dropped out:

1. Refused treatment (n=1)

2. Used nonsteroidal antiinflammatory drugs (n=2)

3. Discontinued treatment because of early discharge (n=6)

81 patients (NMES=31, TENS=32, control group=18) completed all

evaluations (NRS, AROM/PROM, FMA, MAS, BI, SSQOLS) at
0 (baseline), 2, and 4 weeks after 4 weeks of treatment

19 patients were lost to follow-up at 8 weeks

(NMES=10, TENS=4, control group=5)

62 patients completed all evaluations at 8 weeks

Fig 1 Schematic of the study design.

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Efficiency of NMES and TENS on HSP 5

Table 1 Baseline characteristics

Characteristics NMES (nZ31) TENS (nZ32) Control (nZ18) P Value
Mean age  SD (y) 59.3510.78 58.509.07 63.7811.17 .180
Sex, % female 33.33 18.75 16.67 .334
Stroke onset to enrollment (d), 73.6153.40 100.88103.32 105.89142.80 .814
mean  SD
Stroke type, % hemorrhagic 38.71 59.38 33.33 .127
Right hemiparesis (%) 48.39 40.63 38.89 .755
NRS assessment, mean  SD 4.231.28 4.411.24 3.721.02 .100
AROM/PROM, degrees, mean  SD
Forward flexion 22.1040.94/104.6832.51 35.6354.00/106.0937.58 28.3342.04/98.0637.19 .608/.874
Abduction 20.6532.24/89.8419.26 25.7840.08/83.4432.09 25.2834.92/85.8321.37 .917/.412
External rotation 0.973.75/18.8718.06 11.2520.44/32.0325.40 6.6715.34/24.7217.19 .050/.110
FMA (0-66), mean  SD 11.0010.58 19.9720.09 17.2819.07 .266
MAS (0-6), mean  SD
Adductors 0.190.65 0.280.52 0.220.65 .299
Internal rotators 0.771.06 0.941.27 0.941.11 .853
BI (0-100), mean  SD 46.1311.08 37.5019.39 39.4419.17 .115
SSQOLS assessment, mean  SD 137.5517.97 130.00 31.07 132.6131.90 .382

(table 2). Of these, the efficacy of the NMES group was superior
to that of the TENS group (PZ.043), and that of the NMES and
TENS group was superior to that of the control group (P<.001,
PZ.044) (table 3).
Secondary Outcome Measurements
The mean  SD NRS scores at baseline were 4.231.283,
4.411.241, and 3.721.018 points for NMES, TENS, and con-
trol groups, respectively, which dropped to 3.261.460,
3.591.478, and 3.441.338, respectively, at 2 weeks and
remained at 2.001.844, 2.791.618, and 2.381.325 points,
respectively, at 8 weeks (table 4). The Kruskal-Wallis test revealed
significant differences among the 3 groups at 2 weeks (PZ.011)
and 8 weeks (PZ.013) (see table 2), but the differences in the
therapeutic efficacy of the NMES and TENS group (2 weeks:
PZ.188; 8 weeks: PZ.052) as well as the TENS and control
group (2 weeks: PZ.054; 8 weeks: PZ1.000) were not statisti-
cally significant. Moreover, the efficacy in the NMES group was
superior to that in the control group (2 weeks: PZ.008; 8 weeks:
PZ.024) (see table 3). Figure 2 exhibits the effective rates
assessed at each time point. The Pearson chi-square or Fisher
exact tests of the proportion of NRS scores yielded a remarkably
higher effective rate in the NMES group than TENS and control
groups at 2 weeks (75.0% vs 50.0% vs 22.2%, P<.001), 4 weeks
(100% vs 78.1% vs 44.4%, P<.001), and 8 weeks (100% vs 82.1%
vs 84.6%, P<.001) when the 1-point reduction criterion was used.
During the current study, all groups displayed significant im-
provements in the mean shoulder AROM/PROM, FMA, BI, and
SSQOLS scores at each assessment posttreatment (see table 2)
(fig 3). However, the improvements were not significantly
different between the 3 groups (P>.05) (see table 2). Moreover,
the MAS scores of the shoulder adductors and internal rotators had
not improved (see table 2).
In table 4, the treatment groups, including NMES and TENS,
experienced significantly reduced NRS scores at 2 weeks, which
were even further reduced at 4 weeks and maintained at 8 weeks
compared to baseline (P<.05). A gradual reduction could also be
seen in the control group throughout the entire phase, with a
significant difference at 4 and 8 weeks (P<.05) but not at 2 weeks
(P>.05). Similarly, the differences in the improvements of mean
shoulder AROM/PROM, FMA, BI, and SSQOLS scores were
statistically significant as compared to the baseline levels within
each group. However, the improvements in the PROM of shoulder
external rotation in the control group throughout all the phases
exhibited a slight difference (P>.05). And there were no im-
provements in the MAS of shoulder adductors and internal rota-
tors after treatment within the group (P>.05).
Discussion
To our knowledge, this is the first study comparing the efficacy of
NMES and TENS on HSP. Pain relief can be observed in each
group, which is significantly different after 2, 4, and 8 weeks. The
main finding is that NMES and TENS can effectively improve
HSP, and the therapeutic efficacy of NMES is superior to that of
TENS. Effects of low-frequency electrical stimulation for
reducing HSP lie in decreasing the excitability of nerve C fibers,40
and antidromic conduction stimulation of Ab fibers in the dorsal
columns in the stimulated segment.41 In addition, they seem to
modify the release of g-aminobutyric acid, calcitonin gene-related
peptide, substance P, adrenaline, serotonin, and alanine.42
Specifically, the pain relief in the TENS group (low amplitude,
100Hz, pulse width 100ms) might be attributed to the gate control
theory proposed by Melzak and Wall. TENS can specifically
stimulate the peripheral sensory fibers, not the motor fibers,22 to
activate the dorsal horn of the glial cells to close the valve. Also, it
can inhibit the pain signal input to the same segment of the small
afferent sensory fibers and reduce the stimulation of the projected
neurons, resulting in an immediate analgesic effect.21,41 Further-
more, TENS can stimulate the sensory receptors in the skin to
cause reflex or regeneration of axons,43 improving the local blood
circulation.44 Unlike TENS, NMES (high amplitude, 15Hz, pulse
width 200ms) is able to excite peripheral sensory and motor
nerves, especially to produce discernible muscle contraction
mechanisms, including those of the peripheral and central nervous
systems, without inducing significant discomfort.45 The muscle

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6 M. Zhou et al

Table 2 Improvements in the outcome assessments for NMES, TENS, and control groups at 2, 4, and 8 weeks after treatment
Time of Assessment NMES TENS Control P Value*
NRS, mean  SE
Wk 2 0.970.88 0.811.09 0.280.58 .011
Wk 4 2.030.91 1.441.22 0.610.78 <.001
Wk 8 2.241.14 1.571.29 1.230.83 .013
AROM/PROM, mean  SE
Forward flexion
Wk 2 3.7111.76/9.1916.84 10.1632.49/9.8416.04 2.507.33/9.4417.98 .992/.772
Wk 4 8.5519.11/17.5820.53 12.5036.57/17.519.96 6.9411.39/16.6715.81 .682/.967
Wk 8 14.0525.43/21.1923.92 14.6438.63/19.8219.03 13.4628.24/17.6920.78 .867/.730
Abduction
Wk 2 5.8113.30/8.0619.35 8.2822.06/7.0315.07 5.0012.37/4.729.47 .795/.847
Wk 4 10.9717.44/12.4222.39 18.9137.69/16.7225.51 7.2215.93/10.0011.25 .400/.909
Wk 8 22.8626.15/11.926.57 23.3940.83/23.7525.84 15.7733.53/18.8521.62 .458/.184
External rotation
Wk 2 1.132.80/3.559.06 1.565.60/4.228.44 1.113.66/0.285.28 .890/.140
Wk 4 0.973.01/8.3916.95 4.5313.40/5.4710.58 1.944.89/1.1113.99 .711/.178
Wk 8 1.193.84/5.4818.16 5.0014.34/8.399.53 3.089.69/5.3813.14 .666/.827
FMA, mean  SE
Wk 2 2.063.28 2.756.14 2.174.82 .710
Wk 4 3.264.27 4.198.27 3.896.34 .814
Wk 8 4.866.40 5.469.52 5.3110.40 .615
MAS, mean  SE
Adductors/internal rotators
Wk 2 0.000.00/0.100.54 0.060.50/0.060.35 0.000.00/0.170.51 .493/.277
Wk 4 0.000.00/0.350.76 0.160.63/0.160.81 0.000.00/0.390.92 .052/.432
Wk 8 0.000.00/0.480.93 0.210.69/0.110.88 0.000.00/0.000.41 .046/.151
BI, mean  SE
Wk 2 4.845.84 6.727.69 2.503.09 .211y
Wk 4 8.066.80 12.5012.95 6.945.72 .419y
Wk 8 11.678.11 14.8218.13 13.0810.71 .663y
SSQOLS, mean  SE
Wk 2 5.398.46 4.758.06 2.674.94 .432
Wk 4 9.9714.06 9.0012.58 7.068.03 .718
Wk 8 17.8121.40 12.6819.37 10.7712.56 .130
* Differences between groups were analyzed by the Kolmogorov-Smirnov test.
y
Differences between groups were analyzed by the analysis of covariance with NRS as a covariate.

contraction-mediated sensory modulation resulted in sustained
functional reorganization or neuroplasticity of the central nervous
system,36,46 which might be more critical and beneficial in
reducing HSP. The longer the patients remain inactive, the slower
the rehabilitation, and the greater and more severe the residual
damage and dysfunction. Therefore, movement is vital in
maintaining shoulder stability to alleviate pain.47 Lynch et al48
found that the continuous passive motion exhibited an apparent
benefit in shoulder stability, and none of the hemiplegic patients
receiving the continuous passive motion developed shoulder pain;
no neurologic benefit was observed in their study. Although
several studies showed the efficacy of NMES in HSP,23,24 they

Table 3 Mean changes in NRS/MAS for NMES, TENS, and control groups at 2, 4, and 8 weeks after treatment
Significance Tests*
Time of Assessment NMES TENS Control NMES vs control TENS vs Control NMES vs TENS
NRS
Wk 2 0.970.88 0.811.09 0.280.58 0.008 0.514 0.188
Wk 4 2.030.91 1.441.22 0.610.78 <0.001 0.044 0.043
Wk 8 2.241.14 1.571.29 1.230.83 0.024 1.000 0.052
MAS (adductors)
Wk 8 0.000.00 0.210.69 0.000.00 1.000 0.178 0.085
* Differences between groups were analyzed by the Kolmogorov-Smirnov test.

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Efficiency of NMES and TENS on HSP 7

Table 4 Outcome assessments for NMES, TENS, and control groups at 2, 4, and 8 weeks after treatment
Time of Assessment NMES (nZ31) TENS (nZ32) Control (nZ18)
NRS, mean SD
Wk 0 4.231.28 4.411.24 3.721.02
Wk 2 3.261.46* 3.591.48* 3.441.34
Wk 4 2.191.54* 2.971.56* 3.111.37*
Wk 8 2.001.84* 2.791.62* 2.381.33*
AROM/PROM, mean  SD
Forward flexion
Wk 0 22.1040.94/104.6832.51 35.6354.00/106.0937.58 28.3342.04/98.0637.19
Wk 2 25.8147.12*/113.8735.82* 45.7861.53/115.9436.49* 30.8346.53/107.5035.20*
Wk 4 30.6554.46*/122.2636.81* 48.1364.64*/123.5936.59* 35.2850.16*/114.7233.50*
Wk 8 39.0962.10*/128.3333.70* 49.2964.29*/127.6838.53* 41.1562.12*/111.9246.26*
Abduction
Wk 0 20.6532.24/89.8419.26 25.7840.08/83.4432.09 25.2834.92/85.8321.37
Wk 2 26.4538.50*/97.9024.08* 34.0644.62*/90.4730.88* 30.2837.04/90.5618.93*
Wk 4 31.6142.49*/102.2625.59* 44.6954.58*/100.1628.72* 32.5039.53/95.8326.14*
Wk 8 45.9549.94*/100.9526.72* 47.8657.00*/106.0729.92* 38.4656.99*/102.6938.87*
External rotation
Wk 0 0.973.75/18.8718.06 11.2520.44/32.0325.40 6.6715.34/24.7217.19
Wk 2 2.105.74*/22.4218.75* 12.8121.33/36.2524.92* 7.7815.83/25.0016.54
Wk 4 1.944.77/27.2625.88* 15.7824.79*/37.5027.24* 8.6116.34/23.6117.72
Wk 8 2.145.61/26.9022.44 16.4326.17*/42.5025.15* 9.2320.50/27.6918.55
FMA, mean  SD
Wk 0 11.0010.58 19.9720.09 17.2819.07
Wk 2 13.0612.63* 22.7221.05* 19.4420.12*
Wk 4 14.2613.26* 24.1622.29* 21.1720.55*
Wk 8 15.0515.11* 24.0022.01* 20.9223.11*
MAS, mean  SD
Adductors/internal rotators
Wk 0 0.190.65/0.771.06 0.280.52/0.941.27 0.220.65/0.941.11
Wk 2 0.190.65/0.871.06 0.340.65/0.881.26 0.220.65/1.111.18
Wk 4 0.190.65/1.131.02 0.440.72/1.091.40 0.220.65/1.331.33
Wk 8 0.000.00/1.001.10 0.540.74/1.181.36 0.150.56/0.851.21
BI, mean  SD
Wk 0 46.1311.08 37.5019.39 39.4419.17
Wk 2 50.9713.38* 44.2220.25* 41.9419.41*
Wk 4 54.1912.85* 50.0022.36* 46.3919.91*
Wk 8 58.1011.78* 51.0723.51* 50.0023.98*
SSQOLS, mean  SD
Wk 0 137.5517.97 130.0031.07 132.6131.90
Wk 2 142.9416.93* 134.7530.98* 135.2830.41*
Wk 4 147.5217.81* 139.0032.58* 139.6731.12*
Wk 8 150.8119.20* 139.6833.16* 143.4635.67*
* Statistically significant differences between each group before and after treatment, P<.05.

failed to explore the underlying mechanism. Despite various dis-
similarities between NMES and TENS, the stimulation-induced
muscle contraction and joint movement are the core factors.
Thus, we should prioritize the shoulder abductor contraction and
glenohumeral joint movement in HSP management, which can be
easily achieved through NMES. In addition, stimulation with
multiple physiological effects might increase circulation and
promote wound healing,44 which are also crucial in HSP
management.
In this study, we compared 2 interventions to the control group,
which aimed to provide further clinical evidence for the effec-
tiveness of NMES and TENS for treating HSP. The present study
demonstrated that the therapeutic efficacy of the NMES group was
superior to that of the control group in NRS scores at 2 weeks
(PZ.008), which was further notable at 4 weeks (P<.001) and
maintained at 8 weeks (PZ.024). These observations suggested
that NMES can effectively relieve pain and maintain the long-term
analgesic effect. The underlying mechanism may be that NMES
can repeatedly stimulate muscle contraction as mentioned earlier.
A correlation between the amount of motion and motor recovery
was established.49 However, whether this mechanism would result
in the long-term analgesic effect is yet unclear. We speculated that
dose and time response trials would allow us to optimize the
outcomes of the enduring treatment. Noticeably, the therapeutic
efficacy of TENS group was superior to that of the control group
as assessed by NRS scores at 4 weeks (PZ.044), but not at 2 and 8

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8 M. Zhou et al
Fig 2 Efficacy outcomes (1-point reduction in NRS at 2, 4, and 8
weeks) for the MNES, TENS, and control groups.
weeks (PZ.514, P>.99, respectively). TENS produced low-
frequency electrical analgesia and promoted local blood circula-
tion41-44; however, it could not achieve the significant cumulative
effect at 2 weeks posttreatment. At 8 weeks of follow-up, the
cumulative analgesic effect of TENS had been speculated to
disappear gradually because the treatments had been discontinued
for 4 weeks in these patients. Another possible reason may be that
the effect of rehabilitation training on HSP may start to appear.
However, statistically, the control group should still be inferior to
NMES. Therefore, we are more supportive of our early use of
NMES for HSP.
Previous studies found that spasticity played a major role in the
pathogenesis of HSP,9-11 which could be improved by electrical
stimulation.50 In this trial, we did not observe improvements in the
spasticity of shoulder adductors and internal rotators after treat-
ment. Although the MAS is not adequate for the evaluation of
spasticity, it was unlikely that NMES or TENS relieved pain by
reducing spasticity; this phenomenon was inconsistent with the
results of previous studies.2,51
Fig 3 Graphical comparison of (A) pain in NRS at 0, 2, 4, and 8 weeks; (B) arm function in FMA at 0, 2, 4, and 8 weeks; (C and D) life activity
abilities in BI and SSQOLS at 0, 2, 4, and 8 weeks, respectively.
Previous studies found that shoulder subluxation and spasticity
have negative effects on motor function recovery post-HSP.52-54
Especially, the muscle tone of the shoulder internal rotators and
adductors increased in the spastic stage, giving rise to ROM
limitation during external rotation and abduction. These results are
in accordance with our findings. Overall, the 8-week intervention
did not result in any significant difference in the AROM/PROM of
the shoulder in the 3 directions between NMES and TENS, as well
as compared to those of the control group. Thus, we should not
overestimate the efficacy of electrical stimulation on the
improvement of the shoulder ROM.
Consistent with our 8-week findings, the NMES and TENS
groups did not display any marked effects on motor impairment,
activity limitation, and quality of life as compared to the control
group after 2, 4, and 8 weeks, which could be potentially attrib-
uted to various factors. The FMA evaluates not only the shoulder
joint but also the synergic and independent movement of other
joints, which might be weakly related to HSP. The BI measures the
functional status of a patient’s daily life activities depending on
the measurements of a series of independent behaviors such as
eating, bathing, and walking, which might not be related to the
intensity of HSP. In addition, the SSQOLS is composed of 12
items involving, for example, physical fitness, family and social
roles, and personality, which might be less related to HSP. The
improvements in mean FMA, BI, and SSQOLS scores were un-
likely to be associated with stimulation of shoulder muscles,
which were caused by the whole rehabilitation program including
learning capacity to use compensatory movement strategies of the
nonaffected arm and/or increased involvement of the carer.55
Study Limitations
Nonetheless, our study was associated with some limitations.
First, the inclusion and exclusion criteria resulted in a small
sample size, thereby limiting the differences in study results.
Second, the manifestations of HSP vary at different neurologic
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Efficiency of NMES and TENS on HSP
stages of stroke recovery.56 Patients in various stages of recovery
have significantly different arm motor functions, thereby affecting
the later observation of arm movement. Consequently, the phys-
ical movement stages should be considered when assessing motor
recovery of the affected upper limb in hemiplegic patients in
future studies. Third, this study was associated with a high rate of
loss to follow-up, which might lead to information bias and
reduced reliability. Furthermore, the time, frequency, intensity,
and site of electrical stimulation treatment of HSP varied from
those proposed by previous studies.19,57,58 Whether the stimula-
tion parameters used in the current study are optimal remains to be
elucidated. Finally, the absence of uniformity in conventional
rehabilitation program might result in systemic bias.
Conclusions
TENS and NMES can effectively improve HSP; the efficacy of
NMES was distinctly superior to that of TENS with respect to the
maintenance of long-term analgesia. However, NMES has not
shown more increased efficacy than TENS on improving the
shoulder joint mobility, upper limb function, spasticity, the ability
of daily life activity, and stroke-specific quality of life in
HSP patients.
Supplier
a. SPSS, version 20.0; IBM.
b. 100Hz and pulse width 100ms; Shanghai National Electronic
Co, Ltd.
Keywords
Rehabilitation; Transcutaneous nerve stimulation
Corresponding author
Fang Li, PhD, MD, Department of Rehabilitation, Huashan
Hospital, Fudan University, 12 Wulumuqi Middle Rd, Jingan
Qu, Shanghai, China. E-mail address: fangl@fudan.edu.cn.
Acknowledgments
We thank Bingchen An, PhD, MD, and Dalin Cai, PhD, MD, for
statistical advices. We also thank the Research Fund of the
Baoshan district committee of science and technology,
Shanghai, China.
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