Neuromodulation: Technology at the Neural Interface

Received: February 22, 2019 Revised: August 21, 2019 Accepted: August 29, 2019

(onlinelibrary.wiley.com) DOI: 10.1111/ner.13057

Repetitive Peripheral Magnetic Stimulation

for Strengthening of the Suprahyoid Muscles:
A Randomized Controlled Trial
Mao Ogawa, MD*; Hitoshi Kagaya, MD, DMSc* ; Yuki Nagashima, DDS*†;
Shino Mori, MD, DMSc*; Seiko Shibata, MD, DMSc*;
Yoko Inamoto, SLHT, DMSc‡; Yoichiro Aoyagi, MD, PhD*;
Fumi Toda, MD, DMSc*; Megumi Ozeki, MD, DMSc‡;
Eiichi Saitoh, MD, DMSc*
Objective: Head lift exercise is a widely known form of training in the rehabilitation of patients with dysphagia. This study
aimed to compare muscular strength reinforcement training of the suprahyoid muscles using repetitive peripheral magnetic
stimulation (rPMS) with head lift exercises in a randomized controlled trial.
Materials and Methods: Twenty-four healthy adults were randomly assigned to either the magnetic stimulation group
(M group) or the head lift exercise group (H group). Both groups underwent training five days a week for two weeks. The pri-
mary outcome was the cervical flexor strength, and secondary outcomes were jaw-opening force, tongue pressure, muscle
fatigue of the hyoid and laryngeal muscles, displacement of the hyoid bone and opening width of the upper esophageal
sphincter (UES) while swallowing 10 mL of liquid, training performance rate, and pain.
Results: No dropouts were reported during the two-week intervention period. Cervical flexor strength significantly increased
solely in the M group. Tongue pressure significantly improved in both groups. There were no significant differences in the
jaw-opening force, median frequency rate of the anterior belly of the digastric muscle, sternohyoid muscle,
sternocleidomastoid muscle, anterior and superior hyoid bone displacement, and UES opening width in both groups.
Conclusions: Two-week rPMS of the suprahyoid muscles increased the strength of these muscles compared with the head lift
exercise during the same period.

Keywords: Dysphagia, head lift exercise, repetitive peripheral magnetic stimulation, Shaker exercise, suprahyoid muscles
Conflict of Interest: The new coil for magnetic stimulation is patent-pending and Dr. Kagaya is one of the inventors. The
remaining authors have no conflicts of interest to disclose.

INTRODUCTION
During the rehabilitation of patients with dysphagia, the head lift
exercise, also known as Shaker exercise (1), is a widely utilized reha-
bilitation method. The Shaker exercise consists of two exercises
performed in the supine position. The first exercise is an isometric
exercise in which the head is kept raised for 1 min and is repeated
three times at 1-min intervals. The second exercise is an isotonic
exercise in which the head is repeatedly raised 30 times. Three sets
are performed daily for six weeks. The Shaker exercise improves
the hyoid laryngeal elevation by strengthening the suprahyoid
muscles, thereby increasing the opening of the upper esophageal
sphincter (UES) (2–4). A systematic review has also shown the
improvement of dysphagia (5). However, it has been previously
reported that in the Shaker exercise, completing the protocol is dif-
ficult because of significant exercise burden, often resulting in
dropouts (3,6). In a study using surface electromyography (EMG),
fatigue occurred faster in the sternocleidomastoid muscle than in
the suprahyoid muscle group, which was the original target, affect-
ing the quality and efficacy of the training (7,8). Therefore, several
to date. In the chin tuck against resistance exercise, the subject is
placed in a sitting position holding an inflatable 12-cm rubber ball
trapped between the base of the chin and the manubrium sterni.
This exercise consists of alternating isometric and isotonic exercises
and has been reported to generate increased activity of the
Address correspondence to: Hitoshi Kagaya, MD, DMSc, Department of
Rehabilitation Medicine I, School of Medicine, Fujita Health University, 1-98
Dengakugakubo, Kutsukake, Toyoake, Aichi 470-1192, Japan. Email:
hkagaya2@fujita-hu.ac.jp
* Department of Rehabilitation Medicine I, School of Medicine, Fujita Health
University, Toyoake, Aichi, Japan;
†
Department of Dysphagia Rehabilitation, Nihon University School of
Dentistry, Tokyo, Japan; and
‡
Faculty of Rehabilitation, School of Health Sciences, Fujita Health University,
Toyoake, Aichi, Japan
For more information on author guidelines, an explanation of our peer review
process, and conflict of interest informed consent policies, please go to http://
www.wiley.com/WileyCDA/Section/id-301854.html
Source(s) of financial support: This work was supported in part by JSPS
1

training methods that modify Shaker exercise have been proposed KAKENHI Grant Number 16 K01475.

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 OGAWA ET AL.

suprahyoid muscles than the Shaker exercise (9,10). Moreover, it

was reported to be effective when the frequency of the Shaker
exercise is reduced to once a day (11), or even when performed at
a 45 reclining position with a smaller exercise load than in the
supine position (12). Further, a four-weeks jaw-opening exercise
has shown significant improvement in the superior movement of
the hyoid bone, the UES opening width, and bolus pharyngeal
transit time in patients with dysphagia (13).
However, in all the above-mentioned training, patients are
required to perform muscle strengthening exercises actively, and in
patients with dysphagia, who have difficulties in following instruc-
tions during acute or subacute periods, or patients with complica-
tions of sarcopenia or frailty make it difficult to maintain them as
active participants. On the other hand, electrical stimulation of sup-
rahyoid muscles, using surface electrodes for patients with dyspha-
gia, has already been established as an evidence-based therapy in
meta-analyses (14,15). Nevertheless, employing sufficiently intense
Figure 1. Trial profile. Included subjects were randomly assigned to a mag-
electrical stimulation was considered difficult due to the painful sen- netic stimulation group or head lift exercise group.
sation on the skin during stimulation. We specifically designed a
smaller coil for magnetic stimulation of the suprahyoid muscles and
hyoid displacement of <5.3 mm were excluded. Included subjects
succeeded in obtaining the same extent of hyoid elevation as that in
were then randomly assigned to a magnetic stimulation group
the case of a healthy individual swallowing 10 mL of liquid (16,17).
(M group) or head lift exercise group (H group) by a computer-
Magnetic stimulation induces eddy currents in an organism by elec-
generated random number table. Both groups performed the
tromagnetic induction without stimulation of the nociceptors in the
training for five days per week for two weeks (Fig. 1).
skin, because of which skin pain is less likely to occur and sufficiently
The M group underwent rPMS of the suprahyoid muscles via a
intense stimulation is possible (18,19). If large muscle contractions
specifically designed coil placed submentally (Fig. 2). Using Path-
are possible, muscle-strengthening training may be employed (20);
leader (IFG Corporation, Sendai, Japan), the stimulation intensity
therefore, we hypothesized that repetitive peripheral magnetic stim-
was set to 70% of the maximum (approximately 0.7 T), with a fre-
ulation (rPMS) to the suprahyoid muscles can be an alternative to
quency of 30 Hz and stimulation time of 2 s, as well as a pause time
the Shaker exercise. The purpose of this study was to compare mus-
of 8 s consecutively for 10 times; the process was repeated three
cular strength reinforcement training using rPMS of the suprahyoid
times with a 1-min interval. Stimulation was performed in three sets
muscles with head lift exercise in a randomized controlled trial.
daily, that is, 90 times daily. In the H group, as an isometric portion,
the subject was in the supine position and kept the head elevated
for 1 min. This exercise was repeated three times with a 1-min inter-
METHODS
val. In an isotonic portion, the subject performed 30 consecutive
This study was approved by the institutional review board repetitions of head raising in the same supine position. These exer-
(approval no. HM17-383) and was registered in the UMIN Clinical cises are performed three times daily. In the H group, the subjects
Trials Registry (UMIN000031824). The protocol was a prospective, performed the same exercise as the Shaker exercise, but the imple-
randomized, open, blinded-endpoint manner (21). The target indi- mentation period was two weeks instead of six weeks.
vidual and training instructor knew which group the subjects
were assigned to, but the evaluator was blinded to the grouping.
The inclusion criteria were as follows: healthy men aged Outcome Measures
≥20 years who had no history of stroke, neuromuscular disease, All subjects were evaluated twice before the beginning of the
organic disease of pharynx/larynx, respiratory disease, and upper intervention and after the end of the intervention as well, the
gastrointestinal disease. Exclusion criteria were as follows: individ-
uals who had difficulty performing head lift exercises due to dis-
ease of the neck, and so on; those with a history of epilepsy;
those with a pacemaker; and those with magnetic substances that
cannot be removed at a site proximal to the stimulation site. Writ-
ten informed consent was obtained from all the subjects.
All enrolled subjects underwent magnetic stimulation per-
formed for 2 s at a frequency of 30 Hz with a specially designed
coil placed submentally. The movement of the hyoid bone during
magnetic stimulation was evaluated using X-ray fluoroscopy at
30 frames/s. In addition, pain during stimulation was evaluated
using a numerical rating scale (NRS; 0: no pain and 10: the most
severe pain). As magnetic stimulation to the suprahyoid muscles
of healthy individuals led to anterior movement of the hyoid
bone of 10.9  2.8 mm (mean  SD) (17), when the value was
less than the mean value −2 SD, sufficient hyoid movement due Figure 2. rPMS of the suprahyoid muscles. The coil was placed submentally.
2

to magnetic stimulation could not be obtained, and cases with a [Color figure can be viewed at wileyonlinelibrary.com]

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primary outcome was cervical flexor strength. Cervical flexor
strength was measured in the supine position using a handheld
dynamometer (μTas F-1, Anima Corporation, Chofu, Japan). The
subject’s head was fixed to the bed with a non-stretchable belt.
The subjects were then asked to raise their heads. Three measure-
ments were taken with a 1-min interval in between, and the mean
value was used as the cervical flexor strength.
The secondary outcomes were jaw-opening force, tongue pres-
sure, muscle fatigue of the hyoid and laryngeal muscles, displace-
ment of the hyoid bone and opening width of the UES while
swallowing 10 mL liquid, training performance rate, and pain. The
jaw-opening force was measured by having the subjects open the
mouth maximally while in the sitting position, using a jaw-
opening force measurement device (KT2016, Livet Inc., Hachioji,
Japan) (22,23). Measurements were performed three times, with a
1-min interval between each measurement, and the mean value
was subsequently calculated. To measure tongue pressure, a
tongue pressure-measuring device (Orarize, JMS Co., Ltd. Hiro-
shima, Japan) was used; a balloon was placed in the oral cavity
while the subject was in the sitting position, and the subject was
instructed to raise the tongue and apply maximum pressure for
7 s to the balloon with the anterior part of the hard palate
(23–25). A 1-min interval was employed between each measure-
ment. Three measurements were recorded, and the mean value
was subsequently calculated.
Muscle fatigue of the hyoid and laryngeal muscles was mea-
sured using surface EMG during head elevation for 1 min. Dispos-
able electrodes (LecTrode NP Sekisui Plastics Co., Ltd. Osaka,
Japan) were fixed along the muscle fibers of the anterior belly of
the digastric muscle, considered a suprahyoid muscle; the
sternohyoid muscle, considered an infrahyoid muscle; and the
sternocleidomastoid muscle. After A/D conversion at a sampling
frequency of 1000 Hz, each waveform was analyzed using a data
integration analysis program (Kine Analyzer, Kissei Comtec Co.,
Ltd. Matsumoto, Japan). The frequency band was 20-500 Hz, and
the frequency attenuation was calculated based on the study by
White et al. (8). The transition of the median frequency of the
power spectrum was obtained after fast Fourier transformation
was plotted. The slope of the change in the median frequency,
which gradually decreased due to fatigue over time, was calcu-
lated as the rate of change in the median frequency (MF rate).
The MF rate is indicated by a negative value, and a larger value
indicates less muscle fatigue.
Displacement of the hyoid bone and the opening width of the
UES during swallowing of 10 mL of liquid were evaluated in the
lateral view of the videofluoroscopic examination of swallowing.
With the subjects in the sitting position, 10 mL of thin liquid bar-
ium was added to the oral vestibule through a syringe, and sub-
jects discretely swallowed the liquid. Recording was performed
twice at 30 frames/s, and the larger value was used for analysis.
The straight line connecting the lower anterior corners of the
second and fifth cervical vertebral bodies was defined as a verti-
cal line, the line perpendicular thereto was regarded as the hori-
zontal line, and the horizontal component at the time of
maximal hyoid bone elevation during swallowing was considered
as the anterior displacement and the vertical component as the
superior displacement. Moreover, when the 10 mL of thin liquid
barium was swallowed, the UES opening was defined as the
anteroposterior diameter of the narrowest part between the third
and sixth cervical vertebrae at the maximal opening of UES.
ImageJ (National Institutes of Health, Bethesda, MD) was used for
measurement.
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RPMS FOR STRENGTHENING OF SUPRAHYOID MUSCLES
During the intervention period, we evaluated the sets of train-
ing that were performed, which consisted of three sets daily for
10 days (a total of 30 sets). The pain in the cervical region imme-
diately before the start of the first set of training and just after
the end of the third set was recorded every training day using
NRS, and the mean values of NRS both before the first set and
after the third set were calculated.
Statistical Analysis
Based on our preliminary examination, we hypothesized that
the cervical flexor strength, which is the primary outcome, would
be increased by 10 N due to rPMS, assuming an SD of 8, a signifi-
cance level of 5%, a detection power of 80%, and a dropout rate
of 10%. The sample size was set as 24 cases. Values are presented
as mean  SD in tables. The paired-t test was used to compare
values before and after the intervention, and the M and H groups
were compared using an unpaired t-test. However, regarding the
number of training sets and pain, the M and H groups were com-
pared using the Mann-Whitney U test. The significance level was
set at 5%, and JMP ver. 13 (SAS Institute Japan Ltd. Tokyo, Japan)
was used for analysis.
RESULTS
When a magnetic stimulus was applied to all subjects, the ante-
rior displacement measured using X-ray fluoroscopy showed a
minimum value of 5.6 mm and a maximum value of 14.1 mm
(mean, 9.7 mm), and as the anterior displacement was ≥5.3 mm
in all patients, it did not fall under the exclusion criteria. In terms
of NRS during magnetic stimulation, 17 subjects reported a rating
of 0, 3 subjects reported a rating of 1, 2 subjects reported a
rating of 2, and 2 subjects reported a rating of 3. The data of both
groups are shown in Table 1. There were no significant differ-
ences in the M and H groups prior to intervention.
No dropouts were recorded during the two-week intervention.
The cervical flexor strength, which was the primary outcome,
improved significantly in the M group. In the H group, an improv-
ing trend was observed, but no significant difference was demon-
strated. The jaw-opening force result showed an improving trend
in both groups, but no significant difference was noted. The
tongue pressure test significantly improved in both groups
(Table 2). The MF rate of the hyoid and laryngeal muscles in two
cases in the M group and in one case in the H group were
excluded from the analysis due to the EMG measurements not
being recorded adequately. No significant difference was found in
Table 1. Subject Characteristics.
M group H group p value
Number of subjects 12 12
Age (y/o) 30  6 29  5 0.549
Height (cm) 169  7 174  6 0.066
Weight (kg) 63  7 62  11 0.744
Anterior hyoid displacement 10.3  2.2 9.0  2.1 0.202
by magnetic stimulation (mm)
Superior hyoid displacement 4.4  3.9 6.1  4.4 0.345
by magnetic stimulation (mm)
Mean  SD.
3
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Table 2. Changes in Cervical Flexor Strength, Jaw-Opening Force, and Tongue Pressure.

Outcome measurements M group (N = 12) H group (N = 12)

Pre Post p value Pre Post p value

Cervical flexor strength (N) 82.4  23.8 92.6  20.2 0.009** 78.3  19.6 85.0  22.0 0.082
Jaw-opening force (N) 85.8  19.2 91.6  15.9 0.097 84.3  15.2 89.1  19.3 0.178
Tongue pressure (kPa) 40.4  7.5 43.1  8.5 0.006** 43.8  6.6 47.1  7.2 0.006**
Mean  SD.
**p < 0.01.

Table 3. Rate of Change in the Median Frequency.

Rate of change in the median frequency (Hz/s) M group (N = 10) H group (N = 11)

Pre Post p value Pre Post p value

Anterior belly of digastric muscle −0.66  0.37 −0.66  0.38 0.991 −0.68  0.27 −0.80  0.57 0.542
Sternohyoid muscle −0.43  0.15 −0.52  0.36 0.276 −0.53  0.23 −0.49  0.36 0.718
Sternocleidomastoid muscle −0.32  0.26 −0.34  0.23 0.875 −0.26  0.10 −0.19  0.14 0.151
Mean  SD.

Table 4. Changes in Displacement of Hyoid Bone and UES Opening Width During 10 mL of Liquid Swallowing.

Outcome measurements (mm) M group (N = 12) H group (N = 12)

Pre Post p value Pre Post p value

Anterior hyoid displacement 14.2  2.5 13.5  3.0 0.326 12.9  2.9 13.8  3.4 0.099
Superior hyoid displacement 7.4  4.6 7.6  5.0 0.788 7.2  5.3 8.4  4.9 0.284
UES opening width 8.2  2.1 8.7  2.1 0.179 7.9  1.8 8.2  1.9 0.171
UES, upper esophageal sphincter.
Mean  SD.

the MF rates of the anterior belly of digastric muscle, sternohyoid
muscle, and sternocleidomastoid muscle in both groups (Table 3).
In addition, no significant differences were observed in the ante-
rior and superior displacement of the hyoid bone, and UES open-
ing width while swallowing 10 mL of liquid in both groups
(Table 4). No significant differences were found between the M
and H groups both pre- and post-intervention in cervical flexor
strength, jaw-opening force, tongue pressure, MF rates, displace-
ment of hyoid bone, and UES opening width.
The mean number of training sessions implemented was 28 for
the M group and 29 for the H group, and no statistically signifi-
cant differences were observed between the two groups. Pain,
immediately before the first set of training, was significantly lesser
in the M group than in the H group. After the third set of training,
the M group reported milder pain than H group, but no statisti-
cally significant difference was observed (Table 5).
DISCUSSION
The results of this study indicate that cervical flexor strength
significantly improved only in the M group, and tongue pressure
improved in both groups. Moreover, pain just before the start of
training was significantly milder in the M group than that in the H
group. However, no significant improvement was noted for jaw-
opening force; fatigue of the anterior belly of digastric muscle,
sternohyoid muscle, or sternocleidomastoid muscle. The anterior
and superior displacement of the hyoid bone and UES opening

Table 5. Adherence and Pain Around Cervical Area.

M group (N = 12) H group (N = 12) p value

The number of sets of training performed 28  4 29  2 0.890
Pain immediately before the first set of training (NRS) 0 0.3  0.4 0.037*
Pain just after the third set of training (NRS) 0.5  0.6 1.0  1.3 0.589
NRS, numerical rating scale.
Mean  SD.
4

*p < 0.05.

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width during swallowing 10 mL of liquid also showed no signifi-
cant differences.
The measurement of suprahyoid muscle strength is not always
easy, but the intraclass correlation coefficient (1,2) of cervical
flexor strength using a handheld dynamometer in the supine
position showed favorable intra-rater (0.89) and inter-rater (0.82)
reliability (26), and it was reported to increase, due to muscle
strengthening training of the suprahyoid muscles (27). Therefore,
in this study, we evaluated cervical muscle strength in the supine
position using a handheld dynamometer. Many studies have
reported that suprahyoid muscle strengthening can be achieved
through Shaker exercise, but a training period of six weeks is
required. In this study, improvement of cervical flexor strength
was observed in the H group; however, the reason no significant
change occurred is probably the short training period
(two weeks). In contrast, attaining muscle strengthening in the M
group for two weeks was possible. Woo et al. (11) reported that
an equivalent efficacy was obtained by performing Shaker exer-
cise once daily for six weeks. In the H group in our study, training
exercises were equivalent to those performed in the study by
Woo et al. at three times daily for two weeks. Muscle strengthen-
ing initially increased the muscle strength per unit cross-sectional
area due to neural factors, followed by muscle hypertrophy; mus-
cle hypertrophy dominates after three to five weeks (28). In the
present study, the increase in muscle strength obtained in two
weeks appears to be mainly due to the involvement of neural fac-
tors. However, the recruitment pattern of the muscle in the elec-
trical stimulation is said to be the inverse of the voluntary
contractions (29); therefore, results should be interpreted with
caution. Importantly, cervical flexor strength could have signifi-
cantly improved, if the H group training had continued for
six weeks, however at least in the M group, suprahyoid muscle
strengthening was realized earlier than in the H group, which
may be useful for patients in acute and sub-acute periods.
The mylohyoid and the anterior belly of the digastric muscle
among the suprahyoid muscles contributed to tongue-to-palate
pressure generation (30), while the hyoglossus muscle that
belonged to the tongue muscles was activated during head lift
(12). Hence, the improvement of tongue pressure can potentially
be obtained by rPMS and head lift exercise. Even though in the
present study, tongue pressure significantly improved in both
groups, in the past studies using the Shaker exercise, unlike the
recline exercise, could not improve tongue pressure (12); thus, fur-
ther studies are needed to clarify this finding. On the other hand,
no significant change was noted in the jaw-opening force. Among
the suprahyoid muscles, the mylohyoid muscle, the anterior belly
of digastric muscle, and the geniohyoid muscle adhered to the
hyoid bone, pulling down the mandible, but because the hyoid
bone was not fixed in either group, no change in the jaw-opening
force was observed.
In this study, no significant improvement was found in muscle
fatigue, anterior and superior displacement of the hyoid bone,
and UES opening width during swallowing in both groups. The
Shaker exercise was performed by healthy elderly subjects, and
fatigue resistance of the sternocleidomastoid muscle was
improved; however, fatigue resistance in the suprahyoid and
infrahyoid muscles reportedly did not improve (8). In addition, the
Shaker exercise was reported to significantly improve the anterior
movement of the hyoid bone and the UES opening width in
healthy elderly subjects, but no significant change in superior
movement of the hyoid bone was noted (3,6). Because the train-
ing period was two weeks and the subjects were young and
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RPMS FOR STRENGTHENING OF SUPRAHYOID MUSCLES
healthy in this study, the 1-min head lift exercise may have been
too short to evaluate muscle fatigue. Even if an increase in sup-
rahyoid muscle strength was obtained, perhaps increasing the
movement of the hyoid bone and the UES opening width during
swallowing is not necessary, as there was no dysphagia. In this
regard, further investigation of elderly individuals or patients with
dysphagia is necessary.
The training performance rate was favorable in both groups.
No dropout cases were reported in the H group, which included
only healthy young subject and the training period was short
(two weeks). Pain, just before the first set of training, showed pain
remaining after training of the next day. In the M group, all
patients reported NRS ratings of 0, and pain was significantly
milder in the M group than in the H group. Regarding pain imme-
diately after completion of set 3, pain due to training on that day
was noted and there was no significant difference between both
groups. Therefore, with rPMS, pain was not felt on the following
day, and better adherence than head lift exercise can be
expected.
This study has several limitations. We tried healthy individuals
rather than patients in this study to avoid ethical issues. In
elderly patients with dysphagia, differences may occur in regard
to the movement of the hyoid bone and UES opening width dur-
ing swallowing, and muscle fatigue in both groups. The Shaker
exercise was shown to be effective in increasing the muscle
strength of the suprahyoid muscles and improving the UES
opening and dysphagia. In this study, rPMS was found to
enhance suprahyoid muscle strength; however, whether an
increase in UES opening width and improvement in dysphagia
can be realized in patients with dysphagia warrants further
investigation. Moreover, the low numbers of participants and
short duration of rPMS may have affected the results in this
study. Similar to the Shaker exercise, it is necessary to consider
the effects of the six-week training for rPMS. It would also be
interesting to evaluate how long the training effects last after
rPMS, in future studies.
In conclusion, the results of this study suggest that two weeks
of rPMS of the suprahyoid muscles was useful for strengthening
them, compared to the head lift exercise during the same period.
Authorship Statements
Drs. Kagaya, Ogawa, Shibata, and Inamoto designed the study.
Drs. Ogawa, Nagashima, Mori, Toda, and Ozeki conducted the
study, data collection, and data analysis. Dr. Ogawa prepared the
manuscript draft with important intellectual input from Drs.
Kagaya, Saitoh, and Aoyagi. All authors approved the final
manuscript.
How to Cite this Article:
Ogawa M., Kagaya H., Nagashima Y., Mori S., Shibata S.,
Inamoto Y., Aoyagi Y., Toda F., Ozeki M., Saitoh E. 2019.
Repetitive Peripheral Magnetic Stimulation
for Strengthening of the Suprahyoid Muscles: A Rando-
mized Controlled Trial.
Neuromodulation 2019; E-pub ahead of print.
DOI:10.1111/ner.13057
5
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 OGAWA ET AL.
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