Archives of Physical Medicine and Rehabilitation

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Archives of Physical Medicine and Rehabilitation 2016;97:355-62

ORIGINAL RESEARCH

Effectiveness of Neuromuscular Electrical Stimulation

on Patients With Dysphagia With Medullary Infarction
Ming Zhang, MS,a,b Tao Tao, MD,c Zhao-Bo Zhang, MS,b Xiao Zhu, PhD,d
Wen-Guo Fan, PhD,e Li-Jun Pu, MB,b Lei Chu, MB,f Shou-Wei Yue, PhDa
From the aDepartment of Physical Medicine and Rehabilitation, Qilu Hospital, Medical School of Shandong University, Jinan, Shandong;
b
Department of Physical Medicine and Rehabilitation, Zibo Central Hospital, Zibo, Shandong; cDepartment of Gastroenterology, Zibo Central
Hospital, Zibo, Shandong; dGuangdong Provincial Key Laboratory of Medical Molecular Diagnostics, Guangdong Medical University, Dongguan,
Guangdong; eDepartment of Oral Anatomy and Physiology, Guanghua School of Stomatology, Sun Yat-sen University, Guangzhou; and
f
Department of Medical Examination Center, Zaozhuang Mining Group General Hospital, Zaozhuang, China.

Abstract
Objective: To evaluate and compare the effects of neuromuscular electrical stimulation (NMES) acting on the sensory input or motor muscle in
treating patients with dysphagia with medullary infarction.
Design: Prospective randomized controlled study.
Setting: Department of physical medicine and rehabilitation.
Participants: Patients with dysphagia with medullary infarction (NZ82).
Interventions: Participants were randomized over 3 intervention groups: traditional swallowing therapy, sensory approach combined with
traditional swallowing therapy, and motor approach combined with traditional swallowing therapy. Electrical stimulation sessions were for 20
minutes, twice a day, for 5d/wk, over a 4-week period.
Main Outcome Measures: Swallowing function was evaluated by the water swallow test and Standardized Swallowing Assessment, oral intake
was evaluated by the Functional Oral Intake Scale, quality of life was evaluated by the Swallowing-Related Quality of Life (SWAL-QOL) Scale,
and cognition was evaluated by the Mini-Mental State Examination (MMSE).
Results: There were no statistically significant differences between the groups in age, sex, duration, MMSE score, or severity of the swallowing
disorder (P>.05). All groups showed improved swallowing function (P
.01); the sensory approach combined with traditional swallowing therapy
group showed significantly greater improvement than the other 2 groups, and the motor approach combined with traditional swallowing therapy
group showed greater improvement than the traditional swallowing therapy group (P<.05). SWAL-QOL Scale scores increased more significantly
in the sensory approach combined with traditional swallowing therapy and motor approach combined with traditional swallowing therapy groups
than in the traditional swallowing therapy group, and the sensory approach combined with traditional swallowing therapy and motor approach
combined with traditional swallowing therapy groups showed statistically significant differences (PZ.04).
Conclusions: NMES that targets either sensory input or motor muscle coupled with traditional therapy is conducive to recovery from dysphagia
and improves quality of life for patients with dysphagia with medullary infarction. A sensory approach appears to be better than a motor approach.
Archives of Physical Medicine and Rehabilitation 2016;97:355-62
ª 2016 by the American Congress of Rehabilitation Medicine

Dysphagia is common in patients with stroke and is an indepen-
dent predictor of outcome.1,2 It typically refers to difficulty in
eating as a result of disruption in the swallowing process and
shows an increased risk of complications (eg, malnutrition,
Disclosures: none.
aspiration pneumonia).1-4 This may increase mortality and length
of hospital stay.5,6 Dysphagia caused by brainstem stroke has a
greater occurrence than that caused by hemispheric stroke and
shows signs of the most severe form.7
It has been well established that the sequential and rhythmic
patterns of swallowing are produced and organized by a central
pattern generator (CPG)8-10 located in the lower brainstem

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356
(medulla oblongata)11,12 and that this includes 2 main groups of
neurons (nucleus tractus solitarius and nucleus ambiguous). In
animal experiments, these neurons can be excited by the repetitive
stimulation of the superior laryngeal nerve.13,14 Once the
sequential and rhythmic patterns of swallowing have been initi-
ated, an irreversible motor event is observed in the pharyngeal
phase of swallowing.11,12
Recently, neuromuscular electrical stimulation (NMES) has
been widely studied in the clinical setting and shown to be an
effective and safe treatment for dysphagia.15-19 It has been
assumed that the electrical stimulation assists swallowing either
by eliciting muscle contractions20-24 or by increasing the sensory
input to the central nervous system.25,26 Most of the randomized
controlled studies20-23 applied NMES at a frequency of 80Hz for
60m/d for 5d/wk. Kushner et al19 administered NMES at fixed
pulse rates in the range of 5 to 120Hz (mean, 80Hz), with a pulse
duration of 100 to 300ms. They adjusted the frequency to <80Hz
(range, 5e80Hz) to minimize fatigue, and the frequency of high
voltage treatment was set at up to 120Hz. They reported that
NMES with traditional dysphagia therapy was significantly more
effective than traditional therapy alone in reducing feeding tube-
dependent dysphagia in patients with acute stroke.19 A supra-
liminal stimulus has been used to elicit muscle contractions,
which may improve and enhance laryngeal elevation19,27 and
may also protect the muscles from atrophy.28 It is believed that
the sensory approach may stimulate the sensory pathways and
that the sensory stimulation may have a long-term effect in
reorganization of the cortex.29-31 Power et al26 applied faucial
pillar stimulation on 10 healthy subjects at 3 frequencies (0.2, 1,
and 5Hz); they found stimulation at 5Hz lengthened swallow
response time and inhibited the corticobulbar projection, stimu-
lation at 0.2Hz did not enhance swallowing behavior but facili-
tated the corticobulbar projection, and stimulation at 1Hz had no
effect on swallow response time or corticobulbar projection.26
Fraser et al32 discovered electrical stimulation at 1 or 5Hz
increased cortical excitability as determined by the greater
response amplitude of pharyngeal electromyography, whereas
stimulation at 10, 20, and 40Hz suppressed the excitability.32
Wang et al33 administered NMES to patients with severe
dysphagia caused by lower brainstem infarction at a frequency of
0.25Hz for 20 minutes per session, twice a day, for 5d/wk; the
authors indicated that this schedule could facilitate the recovery
of the swallow function and that this may be because of
involvement with the sensory input, particularly the integration
of signals at the nucleus tractus solitarius.33 These results suggest
that the treatment effect is frequency-related for neurogenic
swallowing dysfunction.
In this article we selected 0.25Hz for sensory approach and
120Hz for motor approach. We then evaluated and compared the
effects of NMES in 2 different modes, acting on the sensory input
or the motor muscle, in treating patients with dysphagia with
medullary infarction.
List of abbreviations:
CPG central pattern generator
FOIS Functional Oral Intake Scale
MMSE Mini-Mental State Examination
NMES neuromuscular electrical stimulation
SSA Standardized Swallowing Assessment
SWAL-QOL Swallowing-Related Quality of Life
WST water swallow test
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M. Zhang et al
Methods
Ethics statement
The study protocol was approved by the Ethics Committee of Zibo
Central Hospital. After all the procedures in this study were
explained, written informed consent was obtained from
each patient.
Participants
Study participants were recruited from Zibo Central Hospital.
Between January 2012 and January 2015, 97 participants with
dysphagia who had been diagnosed with medullary infarction
within 1 month and who had no muscular disorders or contrain-
dications to the electrical stimulation were assessed for inclusion.
Five participants were excluded, and 2 declined to participate; 8
participants dropped out for personal reasons unrelated to the
intervention. Therefore, there were 82 participants (fig 1). Par-
ticipants were randomized over 3 intervention groups: traditional
swallowing therapy, a sensory approach combined with traditional
swallowing therapy, and a motor approach combined with tradi-
tional swallowing therapy. The participants were assigned
sequentially to the groups, including the first to the traditional
swallowing therapy group, the second to the sensory approach
combined with traditional swallowing therapy, the third to the
motor approach combined with traditional swallowing therapy
group, the fourth to the traditional swallowing therapy group, and
so forth.
Inclusion and exclusion criteria
The inclusion criteria were as follows: (1) a primary diagnosis of
medullary infarction with brain computed tomography or mag-
netic resonance imaging; (2) disease onset <1 month previously;
(3) presence of oropharyngeal dysphagia confirmed by video-
fluoroscopic swallowing study, including different levels of water
choke to cough, choking, prolonged eating time, difficulty with
swallowing, and nasal regurgitation after swallowing34; (4) age
within the range of 40 to 80 years; (5) no severe cognitive
degeneration that could restrict cooperation with the checks and
treatment, with a Mini-Mental State Examination (MMSE) score
21; and (6) 30-mL water swallow test (WST) level of 3, 4, or 5.
The exclusion criteria were as follows: (1) unstable vital signs
caused by highly inflammatory, severe cardiopulmonary disease or
carotid sinus syndrome (ie, temperature >38.5 C or <35.5 C,
systolic blood pressure >180 or <90mmHg, diastolic blood
pressure >110 or <60mmHg, heart rate >100 or <60 times per
min, respiratory rate >25 or <12 times per min); (2) a cardiac
pacemaker or other electrically sensitive implanted stimulator; (3)
dysphagia caused by structural lesions (eg, radiotherapy, extensive
surgery of the head and neck region); (4) skin lesions of the area to
be treated or implants containing metal parts within the area of
treatment; (5) a history of epilepsy, malignancies, or other
neurologic disease; (6) pregnancy; or (7) spastic paralysis.
Equipment and interventions
All treatments were performed by an occupational therapist.
Traditional swallowing therapy involves compensation strategies
to augment the impaired aspects of oropharyngeal swallowing
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Treatment of dysphasia 357

97 participants with medullary infarction were

assessed for eligibility

5 excluded

2 did not give

informed consent

Qualified and randomized=90

TT group, n=30 SA+TT group, n=30 MA+TT group, n=30

Dropped out Dropped out Dropped out

n=3(10%) due to n=2(6.7%) due to n=3(10%) due to
personal reason. personal reason personal reason
unrelated to unrelated to
intervention. intervention.

Final assessment Final assessment Final assessment

(4weeks) n=27. (4weeks) n=28. (4weeks) n=27.

Fig 1 Flow diagram of the study. Abbreviations: MAþTT, motor approach combined with traditional swallowing therapy; SAþTT, sensory
approach combined with traditional swallowing therapy; TT, traditional swallowing therapy.

(eg, postural adjustment or diet modification, increasing the sen-

sory input through thermal-tactile stimulation, strengthening weak
oropharyngeal musculature through oral exercise, swallow-
ing maneuvers).
The electrical stimulations were performed for 20 minutes per
session, twice a day, 5d/wk, for >4 weeks.

Sensory approach
This approach used a vocaSTIM-Mastera and a pair of 2 surface
electrodes.

Parameter settings
Parameter settings included the following: T/R exponential cur-
rent; triangle wave (ascending: 750ms, descending: 250ms); pulse
width of 1 second, pulse time of 1 second, and release time of 3
seconds; and frequency of .25Hz. The cathode was placed on the
submental region (fig 2), and the anode was placed on the occipital
skin. The intensity of the electrode stimulation ranged from 0 to
15mA, increasing the intensity gradually up to a sensory input
level expected to lead to swallowing. Fig 2 Position of the electrodes. Abbreviations: MA, motor approach,
where the cathode and anode were placed in parallel on the skin of the
Motor approach anterior belly of the digastric muscle in the submental region above the
This approach used a multifunctional nerve rehabilitation and hyoid bone; SA, sensory approach, where the cathode was placed on
treatment systemb and a pair of 2 surface electrodes. the submental region and the anode was placed on the occipital skin.

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358
Parameter settings
Parameter settings included the following: transcutaneous electrical
nerve stimulation mode; bipolar index wave, square wave; pulse
width of 100ms; pulse time of 10 seconds and release time of 5
seconds; and frequency of 120Hz. The cathode and anode were
placed in parallel on the skin of the anterior belly of the digastric
muscle in the submental region above the hyoid bone (see fig 2).16
The intensity of electrode stimulation ranged from 0 to 60mA,
increasing the intensity gradually to a level expected to elicit a
contraction of the target muscle.
The current intensity was started at 2mA and increased by 1-mA
intervals. When the patient expressed slight discomfort, their reac-
tion was observed for a few seconds to allow for possible adaptation
by the patient; if the patient continued to indicate discomfort or pain,
we defined the current intensity used prior to the patient’s indica-
tion as the maximal tolerable intensity.35 The maximal tolerable
current was subsequently administered as the stimulation intensity.
Outcome measures
All baseline characteristics were evaluated by an experienced certi-
fied physical therapist who was not involved in the design of the
study or the treatment of the patients. The MMSE was used to assess
cognition36; its score ranged from 0 to 30. The WST37,38 (table 1)
and Standardized Swallowing Assessment (SSA)39-41 were used to
evaluate swallowing function. In the WST, the subject drank 30mL of
warm water in a sitting position, and the frequency of swallow and
choking cough when subjects were drinking water were observed,
with level 1 indicating a normative swallowing function and level 5
indicating the worst swallowing function. The SSA consisted of 3
sections. The first section included the level of responsiveness, trunk
and head control, lip closure, breathing, sound intensity, pharyngeal
reflex, and voluntary cough and was scored in the range 8 to 23
points. The second section assessed salivary management, laryngeal
movement, repetitive swallowing, choking, and stridor and vocal
quality, with subjects swallowing 5mL of water 3 times (score range,
5e11 points). If all items of the first 2 sections were achieved, the
third section was undertaken, with the subject swallowing 60mL of
water (score range, 5e12 points). The total score for the SSA is in
the range of 18 to 46 points, with higher scores indicating worse
swallowing function. The Functional Oral Intake Scale (FOIS)42 was
used to evaluate oral intake. It used an ordinal series of 7 swallowing
function levels that ranged from no oral intake (level 1) to total oral
intake with no restriction (level 7).
In addition, the Swallowing-Related Quality of Life (SWAL-
QOL)43,44 Scale was used to assess the participants’ quality of life.
This is a 44-item tool constructed for use in clinical research for
patients with oropharyngeal dysphagia that assesses 11 aspects of
quality of life, including burden, eating duration, eating desire,
symptom frequency, food selection, communication, fear, mental
health, social, fatigue, and sleep. Each scale was constructed using
a Likert method of summated ratings, weighting each item equally
Table 1 Water swallow test
Score Performance Deficit
1 Can swallow the water smoothly, once in 5s Normative
2 Can swallow without cough, twice Minimal
3 Can swallow once, but with cough Mild
4 Swallow more than twice, with cough Severe
5 Cough frequently, cannot swallow Profound
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M. Zhang et al
and summing all the ratings into an overall scale score that was
then transformed into a scale of 0 to 100,43,44 with zero indicating
extremely impaired quality of life and 100 indicating no impair-
ment experienced by the individual.
Data and statistical analyses
SPSS software version 22.0 for Windowsc was used to analyze all
the collected data. All data were formally tested for normality prior
to further analysis, and nonparametric tests were used for data that
were not normally distributed. Descriptive data were reported as
mean  SD for normally distributed or median (interquartile range)
for discrete variables for baseline characteristics. One-way analysis
of variance and Kruskal-Wallis test were used to assess differences
between the 3 groups in age, sex, disease duration, MMSE score,
and initial swallowing function. The WST, SSA, FOIS, and SWAL-
QOL Scale were administered before and after treatment, and the
differences between the post- and pretreatment scores were tested
for significance using the Wilcoxon signed-rank test. The Kruskal-
Wallis test (K independent samples) was used to assess differences
between all 3 groups. Differences were considered to be statistically
significant when P<.05.
Results
Participant characteristics
In total, 82 participants were randomized into 3 groups, as pre-
viously described. The traditional swallowing therapy group was
comprised of 17 men and 10 women, with a mean age of 62.68.7
years and disease duration of 21.34.1 days. The sensory
approach combined with traditional swallowing therapy group
was comprised of 16 men and 12 women, with a mean age of
61.37.1 years and disease duration of 22.14.0 days. The motor
approach combined with traditional swallowing therapy group
was comprised of 19 men and 8 women, with a mean age of
62.29.2 years and disease duration of 20.64.3 days. There were
no statistically significant differences between the 3 groups in age,
sex, duration, MMSE score, or severity of the swallowing disorder
in the baseline evaluation (P>.05) (table 2).
Treatment effects
Table 3 and figure 3 present the descriptive statistics for pre- and
posttreatment results of the WST, SSA, FOIS, and SWAL-QOL
Scale. The effect data (posttreatment data minus pretreatment
data) showed statistically significant positive treatment effects for
all 3 groups (P
.01).
There were significant differences between the 3 groups in the
size of treatment effect (P<.05). Table 4 shows the sensory
approach combined with traditional swallowing therapy group had
a significantly greater improvement in swallowing function than
the other 2 groups, and the motor approach combined with
traditional swallowing therapy group improved more significantly
than the traditional swallowing therapy group (P<.05).
Quality of life
The SWAL-QOL Scale scores increased to a significantly greater
extent in the sensory approach combined with traditional swal-
lowing therapy and motor approach combined with traditional
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Treatment of dysphasia 359

Table 2 Baseline characteristics

Characteristic TT Group SAþTT Group MAþTT Group Total F H P
n 27 28 27 82 e e e
Male, n 17 16 19 52 .51 e .60
Female, n 10 12 8 30
Age (y) 62.68.7 61.37.1 62.29.2 62.08.3 .17 e .85
Time since brain injury (d) 21.34.1 22.14.0 20.64.3 21.34.1 .98 e .38
MMSE 25.81.4 25.91.4 26.11.5 25.91.4 .37 e .69
WST 4.40.6 4.40.7 4.30.8 4.40.7 .20 e .82
SSA 35.33.1 36.43.9 35.34.0 35.73.7 .87 e .42
FOIS 2 (1) 1 (1) 2 (1) 1.5 (1) e .40 .82
SWAL-QOL 43.6 (7.4) 43.6 (8.1) 42.8 (9.1) 43.6 (6.6) e .13 .94
NOTE. Values are presented as mean  SD, median (interquartile range), or as otherwise indicated.
Abbreviations: MAþTT, motor approach combined with traditional swallowing therapy; SAþTT, sensory approach combined with traditional swallowing
therapy; TT, traditional swallowing therapy.

swallowing therapy groups than those in the traditional swallow-
ing therapy group; simultaneously, the difference between the
sensory approach combined with traditional swallowing therapy
and motor approach combined with traditional swallowing therapy
groups was also statistically significant (PZ.04).
Safety
In this study, no significant side effects were observed, including
skin burns, laryngeal muscle spasms, bradycardia, or sharp fluc-
tuations in blood pressure. Only a few patients (3 in the sensory
approach combined with traditional swallowing therapy group and
4 in the motor approach combined with traditional swallowing
therapy group) experienced local skin redness or allergic reaction
in the electrode placement area; this disappeared soon after the
cessation of the electrical stimulation, and no one dropped out
because of the skin reaction. We observed that as their swallowing
function recovered, the target stimulus current decreased gradually
in some patients.
Discussion
NMES is a noninvasive intervention technology for the manage-
ment of swallowing disorders. Recently, it has been widely
applied in the clinical setting and shown to be effective in treating
dysphagia in poststroke patients. A meta-analysis concluded that
the electrical stimulation may improve swallowing function.45
Leelamanit et al24 reported that the electrical stimulation can
improve dysphagia by increasing synchronous contraction of the
thyrohyoid muscle. Freed et al22 considered the electrical stimu-
lation to be an effective and safe treatment for poststroke
dysphagia that improves swallowing function better than tradi-
tional thermal-tactile stimulation treatment. Kushner19 suggested
that supplementing traditional dysphagia therapy and progressive
resistance training with NMES during inpatient rehabilitation was
significantly more effective than those 2 therapies alone in
reducing feeding tube-dependent dysphagia in patients who have
had an acute stroke.19
The present study suggests that NMES added to traditional
therapy is more effective than traditional therapy alone in treating
patients with dysphagia with lower brainstem infarction. It also
indicates that it is more effective to target NMES at the sensory
input rather than at the motor muscles. Possible explanations for
the efficacy of NMES observed in this study may be as follows.
First, the sensory approach may increase the local sensory input to
the central nervous system via the CPG to induce the action of
swallowing, therefore eliciting both sensory and motor effects, and
the sensory stimulation may have a long-term effect in reorgani-
zation of the human cortex, resulting in the enhancement of brain
plasticity/recovery in swallowing control.29-31 Second, it is known
that even a few days without normative daily swallowing can
result in disuse atrophy of the oropharyngeal muscles; the motor
approach may elicit local muscle contractions, which may
improve and enhance laryngeal elevation22,27 and protect the
muscles from atrophy.28
Swallowing is composed of highly complex sensorimotor
neuronal components and is programmed by the CPG in the
brainstem.46-49 During swallowing, the sensory inputs arising
from the posterior oral, pharyngeal, and some laryngeal mucosae

Table 3 Comparisons before and after treatment (Wilcoxon signed-rank test)

Pretreatment Posttreatment P
Assessment TT SAþTT MAþTT TT SAþTT MAþTT TT SAþTT MAþTT
WST 4 (1) 4.5 (1) 4 (1) 4 (2) 2 (1) 3 (1)
.01
.01
.01
SSA 35 (5) 37 (6.5) 36 (5) 32 (8) 25 (3.8) 28 (3)
.01
.01
.01
FOIS 2 (1) 1 (1) 2 (1) 3 (3) 6 (2) 4 (3)
.01
.01
.01
SWAL-QOL 43.6 (7.4) 43.6 (8.1) 42.8 (9.1) 52.7 (18.9) 77.4 (26.5) 63.5 (23.9)
.01
.01
.01
NOTE. Values are presented as median (interquartile range).
Abbreviations: MAþTT, motor approach combined with traditional swallowing therapy; SAþTT, sensory approach combined with traditional swallowing
therapy; TT, traditional swallowing therapy.

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360 M. Zhang et al

Fig 3 Assessment of pre- and posttreatment. Abbreviations: MAþTT, motor approach combined with traditional swallowing therapy; SAþTT,
sensory approach combined with traditional swallowing therapy; TT, traditional swallowing therapy.

are transmitted to the medullary nucleus tractus solitarius and
nucleus ambiguus, with reticular formation linking synaptically to
the cranial motor neuron pools bilaterally.46-48 However, many
researchers have found that a complex array of cortical repre-
sentations, including the frontal operculum, sensorimotor cortices,
cingulate, premotor cortex, parietal cortex, insular, basal ganglia,
thalamus, and cerebellum, also play an important role in swal-
lowing control.49-53 The sensory approach for dysphagia in stroke
targets the enhancement of sensory feedback from the oropharynx
to the CPG, and the motor approach targets the strengthening of
the oropharyngeal musculature. The efficacy of the sensory
approach observed in this study may also be explained by its ef-
fects on stimulating brain plasticity/recovery in swallow-
ing control.
This study also demonstrated that NMES could not only
improve the swallowing function but also increase the quality of
life in these patients. Dysphagia affects the most basic of human
functions, the ability to eat and drink. The SWAL-QOL Scale was
constructed for use in clinical research for patients with oropha-
ryngeal dysphagia.43 The quality of life improved to a signifi-
cantly greater extent in the sensory approach combined with
traditional swallowing therapy group than in the motor approach
combined with traditional swallowing therapy and traditional
swallowing therapy groups. Traditional therapy combined with the
sensory approach, therefore, seems to be the most effective
approach to adopt.
Study limitations
The absence of a sham group without any treatment could be
considered a significant limitation of this study. Studies involving
a larger number of participants are needed, and the long-term
curative effects warrant further investigation.
Conclusions
NMES that targets either the sensory input or motor muscles,
combined with traditional therapy, is conducive to recovery from
dysphagia and improves quality of life for patients with dysphagia
with medullary infarction. The sensory approach appears to be
more effective than the motor approach.
Suppliers
a. vocaSTIM-Master; Physiomed Elektromedizin.
b. WOND2000F; Guangzhou TopMedi Co. Ltd.
c. SPSS software version 22.0 for Windows; IBM.

Table 4 Comparisons of treatment effect

Mean Rank Keywords
Assessment TT SAþTT MAþTT H P
Brain stem infarctions; Deglutition disorders; Electric stimulation;
WST 25.48 59.43 38.93 37.96 .01
Quality of life; Rehabilitation
SSA 60.204 19.29 45.83 42.19 .01
FOIS 25.06 61.77 36.93 35.26 .02
SWAL-QOL 25.48 59.43 38.93 28.40 .04
Abbreviations: MAþTT, motor approach combined with traditional
Corresponding author
swallowing therapy; SAþTT, sensory approach combined with tradi-
tional swallowing therapy; TT, traditional swallowing therapy.
Shou-Wei Yue, PhD, Department of Physical Medicine and
Rehabilitation, Qilu Hospital of Shandong University, No 107,

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Treatment of dysphasia
Wenhua Xi Rd, Jinan, Shandong Province, PR China, 250012.
E-mail address: shouweiy@126.com.
References
1. Daniels SK, Ballo LA, Mahoney MC, Foundas AL. Clinical pre-
dictors of dysphagia and aspiration risk: outcome measures in acute
stroke patients. Arch Phys Med Rehabil 2000;81:1030-3.
2. Smithard DG, O’Neill PA, Parks C, Morris J. Complications and
outcome after acute stroke. Does dysphagia matter? Stroke 1996;27:
1200-4.
3. Martino R, Foley N, Bhogal S, Diamant N, Speechley M, Teasell R.
Dysphagia after stroke: incidence, diagnosis, and pulmonary com-
plications. Stroke 2005;36:2756-63.
4. Guillen-Sola A, Chiarella SC, Martinez-Orfila J, et al. Usefulness of
citric cough test for screening of silent aspiration in subacute stroke
patients: a prospective study. Arch Phys Med Rehabil 2015;96:1277-
83.
5. Altman KW, Yu GP, Schaefer SD. Consequence of dysphagia in the
hospitalized patient: impact on prognosis and hospital resources.
Arch Otolaryngol Head Neck Surg 2010;136:784-9.
6. Wang Y, Lim LL, Heller RF, Fisher J, Levi CR. A prediction model
of 1-year mortality for acute ischemic stroke patients. Arch Phys
Med Rehabil 2003;84:1006-11.
7. Teasell R, Foley N, Doherty T, Finestone H. Clinical characteristics
of patients with brainstem strokes admitted to a rehabilitation unit.
Arch Phys Med Rehabil 2002;83:1013-6.
8. Meltzer SJ. On the causes of the orderly progress of the peristaltic
movements in the oesophagus. Am J Physiol 1899;2:266-72.
9. Meltzer SJ. Secondary peristalsis of the oesophagus, a demonstration
on a dog with a permanent fistula. Proc Soc Exp Biol Med 1907;4:35-7.
10. Meltzer SJ. Deglutition through an oesophagus partly deprived of its
muscularis, with demonstration. Proc Soc Exp Biol Med 1907;4(4):
40-3.
11. Jean A. Brain stem control of swallowing: neuronal network and
cellular mechanisms. Physiol Rev 2001;81:929-69.
12. Aida S, Takeishi R, Magara J, et al. Peripheral and central control of
swallowing initiation in healthy humans. Physiol Behav 2015;151:
404-11.
13. Jean A. [Localization and activity of medullary swallowing neuro-
nes] [French]. J Physiol (Paris) 1972;64:227-68.
14. Kessler JP, Jean A. Identification of the medullary swallowing re-
gions in the rat. Exp Brain Res 1985;57:256-63.
15. Bulow M, Speyer R, Baijens L, Woisard V, Ekberg O. Neuromus-
cular electrical stimulation (NMES) in stroke patients with oral and
pharyngeal dysfunction. Dysphagia 2008;23:302-9.
16. Heijnen BJ, Speyer R, Baijens LW, Bogaardt HC. Neuromuscular
electrical stimulation versus traditional therapy in patients with
Parkinson’s disease and oropharyngeal dysphagia: effects on quality
of life. Dysphagia 2012;27:336-45.
17. Lee KW, Kim SB, Lee JH, Lee SJ, Ri JW, Park JG. The effect of
early neuromuscular electrical stimulation therapy in acute/subacute
ischemic stroke patients with dysphagia. Ann Rehabil Med 2014;38:
153-9.
18. Tan C, Liu Y, Li W, Liu J, Chen L. Transcutaneous neuromuscular
electrical stimulation can improve swallowing function in patients
with dysphagia caused by non-stroke diseases: a meta-analysis.
J Oral Rehabil 2013;40:472-80.
19. Kushner DS, Peters K, Eroglu ST, Perless-Carroll M, Johnson-
Greene D. Neuromuscular electrical stimulation efficacy in acute
stroke feeding tube-dependent dysphagia during inpatient rehabili-
tation. Am J Phys Med Rehabil 2013;92:486-95.
20. Permsirivanich W, Tipchatyotin S, Wongchai M, et al. Comparing the
effects of rehabilitation swallowing therapy vs. neuromuscular
electrical stimulation therapy among stroke patients with persistent
www.archives-pmr.org
Downloaded for Anonymous User (n/a) at University of Indonesia from ClinicalKey.com by Elsevier on September 27,
2023. For personal use only. No other uses without permission. Copyright ©2023. Elsevier Inc. All rights reserved.
361
pharyngeal dysphagia: a randomized controlled study. J Med Assoc
Thai 2009;92:259-65.
21. Gallas S, Marie JP, Leroi AM, Verin E. Sensory transcutaneous
electrical stimulation improves post-stroke dysphagic patients.
Dysphagia 2010;25:291-7.
22. Freed ML, Freed L, Chatburn RL, Christian M. Electrical stimula-
tion for swallowing disorders caused by stroke. Respir Care 2001;
46:466-74.
23. Xia W, Zheng C, Lei Q, et al. Treatment of post-stroke dysphagia by
vitalstim therapy coupled with conventional swallowing training.
J Huazhong Univ Sci Technolog Med Sci 2011;31:73-6.
24. Leelamanit V, Limsakul C, Geater A. Synchronized electrical stim-
ulation in treating pharyngeal dysphagia. Laryngoscope 2002;112:
2204-10.
25. Park CL, O’Neill PA, Martin DF. A pilot exploratory study of oral
electrical stimulation on swallow function following stroke: an
innovative technique. Dysphagia 1997;12:161-6.
26. Power M, Fraser C, Hobson A, et al. Changes in pharyngeal corti-
cobulbar excitability and swallowing behavior after oral stimulation.
Am J Physiol Gastrointest Liver Physiol 2004;286:G45-50.
27. Lim KB, Lee HJ, Yoo J, Kwon YG. Effect of low-frequency rTMS
and NMES on subacute unilateral hemispheric stroke with dysphagia.
Ann Rehabil Med 2014;38:592-602.
28. Blumenfeld L, Hahn Y, Lepage A, Leonard R, Belafsky PC.
Transcutaneous electrical stimulation versus traditional dysphagia
therapy: a nonconcurrent cohort study. Otolaryngology 2006;135:
754-7.
29. Hamdy S, Rothwell JC, Aziz Q, Singh KD, Thompson DG. Long-
term reorganization of human motor cortex driven by short-term
sensory stimulation. Nat Neurosci 1998;1:64-8.
30. Hamdy S, Rothwell JC, Aziz Q, Thompson DG. Organization and
reorganization of human swallowing motor cortex: implications for
recovery after stroke. Clin Sci 2000;99:151-7.
31. Steele CM, Miller AJ. Sensory input pathways and mechanisms in
swallowing: a review. Dysphagia 2010;25:323-33.
32. Fraser C, Power M, Hamdy S, et al. Driving plasticity in human adult
motor cortex is associated with improved motor function after brain
injury. Neuron 2002;34:831-40.
33. Wang J, Wu D, Song W, Zhang H, Wang Z. Treatment and mechanism
of surface electrical stimulation for severe dysphagia caused by lower
brainstem infarction. Chin J Rehabil Theory Pract 2009;15:54-7.
34. Gonzalez-Fernandez M, Ottenstein L, Atanelov L, Christian AB.
Dysphagia after stroke: an overview. Curr Phys Med Rehabil Rep
2013;1:187-96.
35. Beom J, Kim SJ, Han TR. Electrical stimulation of the suprahyoid
muscles in brain-injured patients with dysphagia: a pilot study. Ann
Rehabil Med 2011;35:322-7.
36. Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A
practical method for grading the cognitive state of patients for the
clinician. J Psychiatr Res 1975;12:189-98.
37. Suiter DM, Leder SB. Clinical utility of the 3-ounce water swallow
test. Dysphagia 2008;23:244-50.
38. Wu MC, Chang YC, Wang TG, Lin LC. Evaluating swallowing
dysfunction using a 100-ml water swallowing test. Dysphagia 2004;
19:43-7.
39. Yang EJ, Kim MH, Lim JY, Paik NJ. Oropharyngeal dysphagia in a
community-based elderly cohort: the Korean longitudinal study on
health and aging. J Korean Med Sci 2013;28:1534-9.
40. Perry L. Screening swallowing function of patients with acute stroke.
Part two: detailed evaluation of the tool used by nurses. J Clin Nurs
2001;10:474-81.
41. Perry L. Screening swallowing function of patients with acute stroke.
Part one: identification, implementation and initial evaluation of a
screening tool for use by nurses. J Clin Nurs 2001;10:463-73.
42. Crary MA, Mann GD, Groher ME. Initial psychometric assessment
of a functional oral intake scale for dysphagia in stroke patients. Arch
Phys Med Rehabil 2005;86:1516-20.
362 M. Zhang et al

43. McHorney CA, Bricker DE, Robbins J, Kramer AE, Rosenbek JC,
Chignell KA. The SWAL-QOL outcomes tool for oropharyngeal
dysphagia in adults: II. Item reduction and preliminary scaling.
Dysphagia 2000;15:122-33.
44. McHorney CA, Robbins J, Lomax K, et al. The SWAL-QOL and
SWAL-CARE outcomes tool for oropharyngeal dysphagia in
adults: III. Documentation of reliability and validity. Dysphagia
2002;17:97-114.
45. Carnaby-Mann GD, Crary MA. Examining the evidence on neuro-
muscular electrical stimulation for swallowing: a meta-analysis. Arch
Otolaryngol Head Neck Surg 2007;133:564-71.
46. Jean A. Brainstem organization of the swallowing network. Brain
Behav Evol 1984;25:109-16.
47. Jean A. Control of the central swallowing program by inputs from the
peripheral receptors. A review. J Auton Nerv Syst 1984;10:225-33.
48. Broussard DL, Altschuler SM. Brainstem viscerotopic organization
of afferents and efferents involved in the control of swallowing. Am J
Med 2000;108(Suppl 4a):79S-86S.
49. Hamdy S, Mikulis DJ, Crawley A, et al. Cortical activation during
human volitional swallowing: an event-related fMRI study. Am J
Physiol 1999;277:G219-25.
50. Mosier K, Bereznaya I. Parallel cortical networks for volitional
control of swallowing in humans. Exp Brain Res 2001;140:280-9.
51. Huckabee ML, Deecke L, Cannito MP, Gould HJ, Mayr W. Cortical
control mechanisms in volitional swallowing: the Bereitschaftspo-
tential. Brain Topogr 2003;16:3-17.
52. Martin R, Barr A, MacIntosh B, et al. Cerebral cortical processing of
swallowing in older adults. Exp Brain Res 2007;176:12-22.
53. Martin RE. Neuroplasticity and swallowing. Dysphagia 2009;24:
218-29.

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