NeuroRehabilitation 42 (2018) 457–463 457

DOI:10.3233/NRE-172306
IOS Press

Effects of neuromuscular electrical

stimulation in patients with Parkinson’s
disease and dysphagia: A randomized,
single-blind, placebo-controlled trial
Ji-Su Parka, Dong-Hwan Ohb, Na-Kyoung Hwangc and Jung-Hoon Leed,∗
a Departmentof Rehabilitation Science, Graduate School, Inje University, Gimhae, Republic of Korea
bDepartment of Occupational Therapy, Kyung-dong University, Wonju, Republic of Korea
cDepartment of Occupational Therapy, Seoul North Municipal Hospital, Seoul, Republic of Korea
d Department of Physical Therapy, College of Nursing, Healthcare Sciences and Human Ecology,

Dong-Eui University, Busan, Republic of Korea

Abstract.
BACKGROUND: Neuromuscular electrical stimulation has been used to improve swallowing function in neurologic patients
with dysphagia, but its effect on patients with dysphagia and Parkinson’s disease remains unclear.
OBJECTIVES: This study aimed to identify the effect of effortful swallowing combined with neuromuscular electrical
stimulation as a novel treatment approach in dysphagic patients with Parkinson’s disease.
METHODS: Participants were randomly allocated to an experimental group (n = 9) or a placebo group (n = 9). The exper-
imental group simultaneously received neuromuscular electrical stimulation with effortful swallowing, while the placebo
group received sham neuromuscular electrical stimulation with effortful swallowing. All participants received the treatment
for 30 min/day at five sessions per week for 4 weeks. Both groups also received the same conventional dysphagia therapy.
RESULTS: The experimental group showed significant differences in horizontal movement (p = 0.038) and vertical movement
(p = 0.042) compared to the placebo group, but showed no significant differences in the oral (p = 0.648) or pharyngeal phase
(p = 0.329) of the Videofluoroscopic Dysphagia Scale compared to the placebo group, except for the Penetration-Aspiration
Scale (p = 0.039).
CONCLUSIONS: We demonstrated that neuromuscular electrical stimulation applied to the infrahyoid region combined
with effortful swallowing effectively increased hyoid bone movement and reduced aspiration in dysphagic patients with
Parkinson’s disease.

Keywords: Dysphagia, Parkinson’s disease, swallowing, neuromuscular electrical stimulation

1. Introduction oropharyngeal transit time, reduced hyoid bone

movement, decreased muscle strength, and aspiration
Dysphasic patients with Parkinson’s disease pneumonia (Kim et al., 2015). The main causes of
(PD) have common symptoms such as delayed these are bradykinesia and rigidity in the oropharyn-
∗ geal phase, incomplete cricopharyngeal relaxation,
Address for correspondence: Jung-Hoon Lee, Department of
Physical Therapy, College of Nursing and Healthcare Sciences, reduced cricopharyngeal opening, and delayed initi-
Dong-Eui University, 176, Eomgwangno, Busanjin-gu, Busan, ation of the swallowing reflex in the pharyngeal phase
47340, Republic of Korea. E-mail: dreampt@hanmail.net. (Ertekin et al., 2002; Jost, 2016; Nagaya, Kachi, &

1053-8135/18/$35.00 © 2018 – IOS Press and the authors. All rights reserved
458 J.-S. Park et al. / Effects of neuromuscular electrical stimulation in patients with Parkinson’s disease
Yamada, 2000). There are disturbances throughout
the oral, pharyngeal, and esophageal phases, partic-
ularly the first two.
Neuromuscular electrical stimulation (NMES) is
widely used in clinical practice to improve the
swallowing function of patients with various neu-
rological diseases. NMES is a therapeutic method
that delivers stimulation to the muscles through sur-
face electrodes. It is used in facilitation techniques
to increase swallowing muscle strength and sensory
awareness, thereby improving or recovering the swal-
lowing function. Several studies reported the effects
of NMES on patients with dysphagia after neurologic
disorder (Baijens et al., 2013; Calabro et al., 2016;
Park, Oh, Hwang, & Lee, 2016). As a result, improved
hyoid bone movement, decreased pharyngeal residue,
and reduced aspiration were observed.
Humbert et al. (2006) reported various elec-
trode placement methods for NMES. The electrode
arrangement of the NMES is based on the hyoid bone
and is applied to muscle groups such as the suprahy-
oid and infrahyoid muscles. Recently, Park et al.
(2012) introduced a new electrode placement method
of applying two pairs of electrodes to the infrahyoid
muscles. This is a concept that provides electrical
stimulation to the infrahyoid muscles to deliberately
pull down the hyoid bone, overcome it, and lift it again
through effortful swallowing. In other words, resis-
tance is known to offer more intense training. Thus,
NMES combined with effortful swallowing can be an
alternative approach for dysphasia. Park et al. (2016)
reported improved hyoid movement and swallowing
function after use of this method in patients with dys-
phagia after stroke. However, no study has reported
on electrical stimulation applied to the infrahyoid
muscles in PD patients with dysphagia. Therefore,
it is important to use the new electrode placement
method in patients with PD. This study aimed to
investigate the effect of a new NMES placement
method on hyoid bone movement and swallowing
function in dysphagic patients with PD.
2. Methods
2.1. Participants
This study was conducted from July 2016 to
December 2016. Patients with PD and dysphagia,
treated (n = 21) at a university hospital and local
rehabilitation centre in the Republic of Korea were
recruited. The inclusion criteria were as follows:
1) oropharyngeal dysphagia after PD confirmed by
a videofluoroscopic swallowing study (VFSS), (2)
no significant cognitive deficit (Mini-Mental State
Examination score >20), (3) age <75 years, (4) ability
to swallow voluntarily, and (5) Hoehn and Yahr scale
<3 points. The exclusion criteria were as follows:
(1) other neurological disease, (2) having undergone
deep brain stimulation, (3) neck pain or neck surgery,
(4) implanted electronic devices including cardiac
pacemakers or defibrillators, (5) severe communica-
tion problem, (6) severe dyskinesia of the head and
neck, and (7) history of seizure or epilepsy. Three
participants did not meet the criteria for inclusion and
were excluded from the study. Therefore, this study
involved a total of 18 participants. Written informed
consent was obtained from all patients. The study
was approved by the Institutional Review Board of
Dong-eui University.
2.2. Procedures
This study had a prospective two-group (experi-
mental and placebo group) randomized trial design.
Participants were randomly allocated to an experi-
mental group (n = 9) or a placebogroup (n = 9) by
blocked randomization to ensure an equal number
in both groups by an occupational therapist blinded
to the patients.
The experimental group received NMES using a
VitalStim (Chattanooga Group, Hixson, TN, USA)
with effortful swallowing, whereas the placebo group
received sham NMES with effortful swallowing. Two
pairs of electrodes were placed in the anterior neck
region. The electrodes were placed in the infrahyoid
area targeting the sternohyoid muscles (omohyoid,
sternohyoid, and sternothyroid) (Fig. 1).
The electrical stimulation unit provided two chan-
nels of bipolar electrical stimulation at a fixed 80-Hz
pulse rate and a fixed biphasic pulse duration of
Fig. 1. Electrode placement.
 J.-S. Park et al. / Effects of neuromuscular electrical stimulation in patients with Parkinson’s disease
700 µs. In the experimental group, the electrical
stimulation was applied to induce a strong muscle
contraction; in the placebo group, sham stimulation
was used at an intensity of 1.0 mA. The duration of the
electrical stimulation in this study was set at 30 min
per session. The intensity was gradually increased in
0.5 mA intervals for the experimental group. All par-
ticipants were asked to perform an effortful swallow
using their saliva during the stimulation. Except for
stimulation intensity, the procedure for the placebo
group was the same.
Both groups received the same conventional dys-
phagia therapy (CDT) for 30 minutes after the NMES
intervention that comprised orofacial muscle exer-
cises, thermal tactile stimulation, and therapeutic or
compensatory maneuvers. An experienced occupa-
tional therapist performed the CDT in all participants
for 30 min/day, five days a week, for 4 weeks. A
flowchart of this study is shown in Fig. 2.
2.3. Outcome measurement
We assessed hyoid bone movement using the
Image J program (National Institutes of Health,
Bethesda, MD, USA). The analysis was conducted
Fig. 2. Flowchart of this study.
459
of the VFSS image using the same method described
in a previous study (Park et al., 2016). The swal-
lowing process was captured using a frame during
the VFSS. Two picture frames of the VFSS were
used for the analysis: 1) rest position of the hyoid,
and 2) maximal excursion of the hyoid bone. The
application of the vertical C2–C4 axis used an image
rotation technique. A straight line was drawn between
the most antero-inferior points, C2 and C4, and the
images were rotated to the true vertical 90◦. The
antero-inferior corner of C4 was identified on each
image and used as an “anchor point,” which repre-
sents a stable point (resting position) of the hyoid
before swallowing from the distance of the moving
hyoid. Hyoid displacement represents the distance
from the resting position to the maximal excursion
position during swallowing; the most supero-anterior
point of the hyoid indicates maximum displacement
after swallowing. Horizontal and vertical displace-
ment of the hyoid were calculated by subtracting the
point values (x, y) measured on the resting position
image (pre-swallow image) from that measured on
the maximal excursion image: anterior displacement,
(x2-x1)-(Ox2-Ox1); vertical displacement: (y2-y1)-
(Oy2-Oy1). The pre-swallow image coordinates were
460 J.-S. Park et al. / Effects of neuromuscular electrical stimulation in patients with Parkinson’s disease
x1 and y1, while the maximal excursion image coor-
dinates were x2 and y2. The coordinates of the anchor
point of the pre-swallow image were Ox1 and Oy1,
while those of the excursion image were Ox2 and
Oy2.
The Videofluoroscopic Dysphagia Scale (VDS) is
a comprehensive swallowing assessment based on
the VFSS findings. The VDS is divided into the
oral stage (seven items: lip closure, bolus forma-
tion, tongue-to-palate contact, mastication, apraxia,
premature bolus loss, and oral transit time) and the
pharyngeal stage (seven items: pharyngeal triggering,
vallecular residues, pyriform sinus residues, laryn-
geal elevation, pharyngeal wall coating, pharyngeal
transit time, and aspiration) (Kim et al., 2012).
The Penetration-Aspiration Scale (PAS) is a
standard tool that reflects airway penetration and
aspiration. Penetration is defined as the passage of
material into the larynx that does not pass below the
vocal folds, while aspiration refers to the action of
material penetrating the larynx and entering the air-
way below the true vocal folds (Rosenbek, Robbins,
Roecker, Coyle, & Wood, 1996).
2.4. Statistical analysis
The statistical analyses were performed using
SPSS version 15.0 (IBM Corporation, Armonk, NY,
USA). Descriptive statistics are presented as means
with standard deviations. To evaluate the intervention
effects, the Wilcoxon signed-rank test was used to
compare measures pre- and post-intervention in each
group. The Mann-Whitney U test was used to com-
pare the intergroup changes in outcome measures.
Significance level was set at p < 0.05. Effect sizes
(Cohen d) of changed scores comparing experimental
and placebo group were calculated. Effect size of 0.2,
0.5 and 0.8 represent a small, moderate or large effect
respectively.
Table 1
Characteristics of participants
Characteristics
Age (year), mean ± SD (range)
Gender, male/female
ICH
Infarction
Time since onset of stroke, weeks, mean ± SD (range)
Stimulation intensity (mA)
SD: standard deviation. ICH: Intra cerebral hemorrhage.
3. Results
3.1. General characteristics of participants
The patients’ general characteristics are described
in Table 1 with no significant between the two groups
(p > 0.05).
3.2. Effects on kinematics of the hyoid bone
The experimental group showed significant
improvement in horizontal and vertical movements
of the hyoid bone (p = 0.015 and p = 0.008 respec-
tively), and the placebo group also showed significant
improvement (p = 0.05 and p = 0.043 respectively).
After the intervention, the experimental group
showed significantly different values in horizon-
tal movement (p = 0.038) and vertical movement
(p = 0.042) compared to the placebo group (Table 2).
In a comparison of the extent of change in the groups,
both groups showed significant differences in ver-
tical movement but not in horizontal movement of
the hyoid bone (p = 0.009 and p = 0.093, respectively)
(Table 3). Effect sizes were observed for the horizon-
tal (0.9) and vertical movement (0.9) of the hyoid
bone.
3.3. Effects on swallowing function
The experimental group showed a significant
improvement in the total score (p = 0.021), the pha-
ryngeal phase of VDS (p = 0.028), and the PAS
(P = 0.007); the placebo group showed a significant
improvement only in the total score (p = 0.041). After
the intervention, the experimental group showed no
significant differences in the oral (p = 0.648) and pha-
ryngeal (p = 0.329) phase of VDS compared to the
placebo group, except in PAS (p = 0.039) (Table 2).
A comparison of the extent of change in the groups
revealed significant differences in PAS except for
Experimental group Placebo group
(n = 9) (n = 9)
63.44 ± 13.55 54.67 ±13.82
5/4 3/6
4 5
5 4
36.44 ± 7.5 (29–48) 36.11 ± 7.94 (28–50)
13.2 ± 1.52 3.5 ± 1.12
 J.-S. Park et al. / Effects of neuromuscular electrical stimulation in patients with Parkinson’s disease 461

Table 2
Changes in parameters before and after treatment
Experimental group Placebo group Between
(Mean ± SD) (Mean ± SD) group
Before After p-value Before After p-value p-values
treatment treatment treatment treatment
VDS-total 59.22 ± 6.26 54.11 ± 5.62 0.021∗ 56.28 ± 9.35 53.28 ± 10.21 0.041∗ 0.690
VDS-oral phase 17.83 ± 1.64 17.39 ± 1.36 0.18 15.11 ± 6.35 14.22 ± 6.22 0.18 0.648
VDS-pharyngeal phase 41.39 ± 5.92 36.72 ± 5.67 0.028∗ 41.17 ± 4.38 39.06 ± 4.73 0.093 0.329
Horizontal displacement 1.36 ± 0.26 1.65 ± 0.17 0.015∗ 1.32 ± 0.13 1.41 ± 0.22 0.05∗ 0.038†
of the hyoid bone (cm)
Vertical displacement 1.39 ± 0.18 1.71 ± 0.25 0.008∗ 1.4 ± 0.18 1.5 ± 0.26 0.043∗ 0.042†
of the hyoid bone (cm)
PAS 5.11 ± 1.45 2.33 ± 0.71 0.007∗ 4.11 ± 1.27 3.67 ± 1.32 0.429 0.039†
SD: standard deviation. VDS: videofluoroscopic dysphagia scale, PAS: penetration-aspiration scale, ∗p < 0.05 by Wilcoxon test, †p < 0.05
by Mann-Whitney U test.

Table 3
Comparison of the differences after the 6-week treatment in the two groups
Experimental group Placebo group Between group
(Mean ± SD) (Mean ± SD) p-value
VDS-total 5.11 ± 5.12 3 ± 3.44 0.426
VDS-oral phase 0.44 ± 0.92 0.89 ± 2.03 0.903
VDS-pharyngeal phase 4.67 ± 5.31 2.11 ± 3.38 0.308
Horizontal displacement 0.29 ± 0.2 0.12 ± 0.17 0.093
of the hyoid bone (cm)
Vertical displacement 0.32 ± 0.17 0.09 ± 0.14 0.009†
of the hyoid bone (cm)
PAS 2.78 ± 1.2 0.44 ± 1.59 0.006†
SD: standard deviation. VDS: videofluoroscopic dysphagia scale, PAS: penetration-aspiration
scale, †p < 0.05 by Mann-Whitney U test.

the oral and pharyngeal phase of VDS (p = 0.006,
0.903, and 0.308, respectively) (Table 3). Effect sizes
were observed for the oral phase (0.1) and pharyngeal
phase (0.5) of VDS and PAS (2.0).
4. Discussion
This study examined the effects of NMES com-
bined with effortful swallowing for patients with PD
and dysphagia. We first attempted a new electrode
placement method with proven efficacy in patients
with PD.
The results of this study confirm that the experi-
mental treatment was more effective for improving
hyoid bone antero-superior movement than the
placebo treatment. Therefore, we demonstrated that
effortful swallowing with NMES applied to the
infrahyoid muscles is an effective method for improv-
ing hyoid bone movement.
The results of this study can be attributed to the fol-
lowing reasons. First, effortful swallowing is known
to be effective at increasing the antero-superior
movement of the hyolaryngeal complex and respond-
ing to epiglottic tilt (Jang, Leigh, Seo, Han, & Oh,
2015). However, when the NMES is applied to the
infrahyoid muscles, the hyoid bone is lowered due
to infrahyoid muscle contraction. When the effort-
ful swallowing is overcome, the hyoid bone move
up again (Park et al., 2012). In other words, since
resistance occurs during effort swallowing, it can
be more effective in raising the hyoid bone than
performing effort swallowing only. Previous studies
(Baijens et al., 2012, 2013; Heijnen, Speyer, Baijens,
& Bogaardt, 2012) using NMES for patients with
PD did not measure hyoid movement; thus, direct
comparison with this study is difficult. However, the
results of this study are similar to those of previ-
ous studies using NMES and effortful swallowing in
stroke patients (Park et al., 2012).
Improved hyoid bone movement is an important
factor for patients with dysphagia. This is because
the hyolaryngeal movement directly affects the pha-
ryngeal phase during swallowing. Therefore, we
evaluated swallowing function using VDS based on
VFSS. There was no significant difference between
462 J.-S. Park et al. / Effects of neuromuscular electrical stimulation in patients with Parkinson’s disease
the two groups in swallowing function during the
oral and pharyngeal phase. Interestingly, for a more
accurate and sensitive assessment of penetration-
aspiration, the PAS score on the 8-point scale showed
a significant intergroup difference, indicating that this
intervention method is helpful for decreasing aspira-
tion. In other words, this study showed that effortful
swallowing and NMES did not improve the over-
all swallowing function but was helpful for reducing
aspiration.
The reduction in aspiration observed in this study
may be due to several reasons. First, the reduc-
tion of aspiration is probably due to improvement
of the antero-superior movement of the hyolaryn-
geal complex. Enhancement of the antero-superior
movement of the hyolaryngeal complex affects the
pharyngeal phase and is closely related to the airway
protection mechanism such as epiglottic tilt. More
precisely, anterior and upward movement of the hyoid
bone affects the upper esophageal sphincter open-
ing and airway protection, respectively (Park et al.,
2016).
Second, from a different point of view, a change in
the central nervous system induced by NMES can be
explained to some extent. NMES has a central as well
as peripheral effect, such as a change in skeletal mus-
cles. NMES provides afferent input to the swallowing
center in the brain stem or pharyngeal motor cortex
and activates it (Guillen-Sola et al., 2016). Apply-
ing electrical stimulation to the pharynx changes the
excitability of the pharyngeal motor cortex, i.e., facil-
itation of neural plasticity possibly has a positive
effect on improved swallowing function.
Third, it can be explained by the synergistic effect
of NMES and effortful swallowing. NMES is known
to be effective in selectively stimulating type 2 fibers
as a treatment that is known to effectively strengthen
muscles, prevent atrophy, and retrain the neuromus-
cular system by inducing muscle contraction via
nerve fiber depolarization (Freed, Freed, Chatburn,
& Christian, 2001; Permsirivanich et al., 2009; Shaw
et al., 2007). However, unlike NMES, effortful swal-
lowing spontaneously induces muscle contraction,
which further stimulates type 1 fibers (Shaw et al.,
2007). Swallowing-related muscles, like other skele-
tal muscles, are composed of type 1 and 2 muscle
fibers, but type 2 fibers tend to be heavier. The syn-
chronous recruitment of both type I and type II fibres
can generate greater swallowing muscle force during
combined therapy and is more effective than effortful
swallowing alone in muscle re-education for dyspha-
gia (Park et al., 2016). Therefore, the application
of these two methods is theoretically superior to
effortful swallowing only (Guillen-Sola et al., 2016).
A three patients in the experimental group showed
signs of fatigue after a 30-minute treatment session,
which was due to the decrease of tolerance during the
intervention by elevation of the hyoid bone through
continuous swallowing. Careful observation of the
patient’s level of fatigue is needed, but we believe
that to elicit a therapeutic response such as improved
swallowing function, patients need to be challenged
to reach beyond the range of tolerable fatigue.
This study applied NMES with effortful swallow-
ing to patients with PD and dysphagia. As a result,
hyoid bone movement was increased and the aspi-
ration was reduced. Therefore, we recommend this
intervention to improve swallowing in patients with
PD and dysphagia.
This study has some limitations. First, sample
size may have influenced the results, therefore these
results cannot be generalized. Second, absence of
follow-up after the end of intervention did not
allow for determination of the durability of effects.
Third, brain imaging was not performed; hence,
swallowing-related cortical change could not be
confirmed.
5. Conclusion
This study demonstrated that NMES is effective
in improving the oropharyngeal swallowing function
in patients with Parkinson’s disease and dysphagia.
Therefore, NMES can be recommended as a medical
treatment.
Conflict of interest
This research was performed without funding. No
conflicts of interest are declared.
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