Neuromodulation: Technology at the Neural Interface

Received: July 2, 2013 Revised: September 30, 2013 Accepted: October 25, 2013

(onlinelibrary.wiley.com) DOI: 10.1111/ner.12137

Functional Magnetic Stimulation Using a

Parabolic Coil for Dysphagia After Stroke
Ryo Momosaki, MD, PhD; Masahiro Abo, MD, PhD; Shu Watanabe, MD, PhD;
Wataru Kakuda, MD, PhD; Naoki Yamada, MD; Kenjiro Mochio, MD
Objectives: Recently, the usefulness of neuromuscular electrical stimulation and repetitive transcranial magnetic stimulation for
poststroke dysphagia has been reported. However, there is no report that describes the effectiveness of functional magnetic
stimulation (FMS) for dysphagia. The purpose of this study is to clarify the effectiveness of FMS for poststroke dysphagia.
Methods: Twenty poststroke dysphagic patients (age at treatment: 51–80 years; interval between onset of stroke and treatment:
6 to 36 months) were randomly assigned to a real group or a sham group. In the real group, FMS of 30 Hz was applied for
suprahyoid muscles in a 20-sec train using a parabolic coil for 10 min (total 1200 pulses). In the sham group, sham stimulation was
applied for 10 min at the same site. Swallowing function was evaluated by the timed water swallow test, interswallow interval (ISI),
swallowing volume velocity (speed), and volume per swallow (capacity) were measured before and after stimulation.
Results: All patients completed the stimulation and none showed any adverse reactions throughout the stimulation. The
improvement of speed and capacity of swallowing after stimulation was significantly larger in the real group compared with the
sham group (all p < 0.05). However, no significant difference in the ISI was found between the groups.
Conclusions: FMS using a parabolic coil can potentially improve swallowing function in poststroke dysphagic patients.

Keywords: Dysphagia, functional magnetic stimulation, rehabilitation, stroke

Conflicts of Interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of
the paper.

BACKGROUND to a coil to generate a magnetic field perpendicular to it, causing

eddy currents inside the body that selectively stimulate nerves and
Dysphagia is a common complication in stroke patients, with a muscles. The principles behind FMS can be thought of as largely
reported incidence of approximately 55% during the acute phase of similar to those for electrical stimulation, but FMS is characterized
a stroke (1). Dealing with dysphagia is clinically important because it by a greater range of depth and less pain and almost no side effects
can affect the activities of daily living (ADL), quality of life, and due to its noninvasiveness (15).
prognosis of stroke patients. Effective dysphagia rehabilitation tech- There have been successful reports to date of FMS targeting
niques are relatively limited and include the Shaker exercise (2), respiratory muscles improving respiratory function (16), of stimula-
lingual exercise (3), pronunciation training (4), and expiratory tion of the digestive tract improving intestinal peristalsis (17), and of
muscle strength training (5). stimulation of the stomach improving gastric emptying (18), among
In recent years, research has been conducted on noninvasive others. For dysphagia too, it may be possible to induce improved
stimulation methods as novel treatments for patients with dyspha- contractility of pharyngeal muscle groups and neuromodulation of
gia. For example, the efficacy of electrical stimulation of the neck swallowing-related muscle groups by stimulation of the pharyngeal
has been validated in several comparative studies (6–9). However, muscles and their dominant nerves through FMS, but no past
that improvement is limited, and moreover, the affixing of wiring studies have been performed using FMS to treat dysphagia. If its
and electrodes for stimulation is labor intensive; for the elderly in efficacy could be confirmed, FMS could contribute to the field of
particular, wrinkles and the slackening of skin make their placement
difficult. In addition, as the distance to muscles increases, so does
electrical resistance. Furthermore, as the neck region is a place that Address correspondence to: Masahiro Abo, MD, PhD, Department of Rehabilita-
does not delapidate easily and where skin electrical resistance also tion Medicine, Jikei University School of Medicine, 3-25-8, Nishi-Shimbashi,
Minato-Ku, Tokyo 105-8461, Japan. Email: [email protected]
is present to a certain degree, stimulation can easily produce pain.
Several repetitive transcranial magnetic stimulation (rTMS) thera- Department of Rehabilitation Medicine, Jikei University School of Medicine,
pies targeting dysphagia also have been reported (10–13) but have Tokyo, Japan.
been limited to small-scale studies. Settings where such interven-
tions cannot be performed safely due to contraindications (epilepsy, For more information on author guidelines, an explanation of our peer review
process, and conflict of interest informed consent policies, please go to http://
intracranial metal) (14) also exist. www.wiley.com/bw/submit.asp?ref=1094-7159&site=1
Functional magnetic stimulation (FMS) is a safer, minimally inva-
637

Source of financial support: This work was supported by Japan Society for the
sive stimulation therapy. FMS is a method where a current is applied Promotion of Science KAKENHI Grant Number 70439800.

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 MOMOSAKI ET AL.

Table 1. Patient Characteristics (N = 20).

Value Sham (N = 10) Real (N = 10)

Age (years) Mean ± SD 66 ± 9 61 ± 22
Male Number 6 8
Duration after stroke (months) Mean ± SD 21 ± 8 19 ± 8
Ischemic lesion Number
Cerebrum 1 2
Cerebellum 3 2
Brainstem 2 5
Mixed 4 1
Functional Oral Intake Scale Median (IQR) 8 (7,8) 7 (7,8)
Modified Rankin Scale Median (IQR) 1 (1,2) 2 (1,2)
Functional independence measure Mean ± SD 88 ± 10 84 ± 8
IQR, Inter Quartile Range; SD, standard deviation.

swallowing rehabilitation as a novel therapeutic modality for

patients with dysphagia. The purpose of the study is to provide an
initial evaluation of the safety, feasibility, and efficacy of FMS for
dysphagic patients.

METHOD
The purpose of this study was to clarify the effectiveness of FMS
for poststroke dysphagic patients. The study was performed in the
Outpatient Rehabilitation Clinic of the Third Hospital of the Jikei
University School of Medicine. The study population was 20 patients
who had experienced a cerebral infarction more than six months
ago, or who had only mild dysphagia (Table 1). They were aware of
difficulty in swallowing and sometimes observed choking during
meals. However, almost all of them were able to orally intake regular
diets and thin liquids. In addition, we excluded patients with
contraindications to magnetic stimulation (cardiac pacemaker, epi-
lepsy, metal in the neck or skull, dental implants, and pregnancy Figure 1. MMC-90 parabolic coil.
(14)) and with cognitive impairment such as they could not under- The coil is parabolic in shape and suitable for stimulation of the jaw and neck.
stand the research contents, patients with general health problems
(disturbed consciousness and major complications such as fever, (MagVenture Company, Farum, Denmark); the magnetic stimulation
infectious disease, severe heart disease, etc.), patients under 20 coil was the MMC-90 Parabolic Coil (Fig. 1) from the same company.
years of age, patients with malignant tumors or skin disease of the The coil was parabolic in shape to provide powerful and focused
neck, and patients with carotid vein thrombosis. The study popula- stimulation, and it was suitable for stimulation of the jaw and neck
tion was assigned to two groups (real and sham, N = 10 each) with a regions. The inner diameter of the transducer head was 25 mM, the
method of randomization to validate the effectiveness of FMS. The outer diameter was 87 mM, and the winding height was 11 mM. The
sample size was determined through calculations using G*Power3 max initial dB/dt was 40 kT/s near the coil surface on the convex
software (v 3.1.6; Franz Faul, Kiel University, Kiel, Germany) (19) side. The active pulse width was 280 μsec (biphasic). As the stimu-
under the following settings to establish swallowing speed gain as lation frequency of 20–30 Hz was provided in most previous study
the main outcome: α = 0.05, power = 0.8, mean of real group = 2.5, of FMS (16–18), we applied a high-frequency stimulation of 30 Hz in
mean of sham group = 1.0, standard deviation of real group = 1.5, this study accordingly. The suprahyoid muscle group above, at the
and standard deviation of sham group = 0.4. The Ethical Committee midpoint of the hyoid bone and the chin, was chosen as the stimu-
of the Jikei University School of Medicine approved the study. In lation site, and the stimulation strength was set at 90% of the
addition, the study has been registered in the Japan Medical Asso- minimal intensity at which the patient subjectively feel local pain.
ciation Clinical Trial Registration. The site was stimulated at 30 Hz for two seconds followed by 28 sec
of rest, repeated for ten minutes (1200 pulses in total). Sham stimu-
lation was performed by setting the coil on its lateral side while
Functional Magnetic Stimulation using the same protocol as for FMS: i.e., the coil was turned on, but
We performed stimulation after informed consent was obtained the target site was not stimulated.
from the dysphagic patients and evaluated functional swallowing
ability pre- and postintervention. The FMS intervention consisted of Timed Water-Swallow Test
one session of FMS performed on a single day. The stimulation The timed water-swallow test was carried out to evaluate swal-
638

device used for the study was the MagVenture MagProR30 lowing ability. It was conducted according to the protocol described

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 FUNCTIONAL MAGNETIC STIMULATION FOR DYSPHAGIA

Figure 2. Change of interswallow interval. Figure 3. Change of speed.

No significant difference could be seen between groups in the change of The change of speed from pre- to poststimulation was significantly larger for the
interswallow interval from pre- to poststimulation. real group.

by Hughes and Wiles (20). Each patient was asked to drink water
(50 mL) from one cup as quickly and as comfortably as possible
while being precisely timed. Any residual water in the cup was mea-
sured afterward. The number of laryngeal elevations (swallows) was
counted during this task. A stopwatch was started when the first
drop of water touched the lip and stopped when the volunteer
breathed after the last swallow. The mean interswallow interval (ISI)
was calculated as completion time divided by the number of swal-
lows. Mean swallowing volume velocity (speed) was then calculated
as volume drunk (mL) divided by time taken (sec). Mean swallowing
volume capacity was calculated as volume drunk (mL) divided by
number of swallows. Basically, the smaller the ISI, the larger the
speed and capacity, signifying good swallowing function.

Figure 4. Change of capacity.

Statistical Analysis The change of capacity from pre- to poststimulation was significantly larger for
The Mann–Whitney U-test was used to conduct between-group the real group.
comparisons between the sham and real groups. All swallowing
data are expressed as mean ± SD. A p-value of 0.05 was used to
indicate statistical significance. there were between-group differences, and returned respective
p-values of 0.3, 0.9, and 0.5: no significant differences were
observed. The mean values for poststimulation ISI, speed, and
RESULTS capacity for the sham group were 2.7 ± 0.2, 5.2 ± 3.8, and 11.9 ± 2.9,
respectively; for the real group, they were 2.5 ± 0.2, 6.6 ± 4.8, and
Table 1 summarizes the clinical characteristics of the study popu- 14.1 ± 4.5. The mean amounts of change caused by the stimulation
lation. The mean of age at study entry was 63 ± 16 years. The mean procedure for ISI, speed, and capacity were −0.3 ± 0.4, 0.9 ± 1.4, and
time between stroke onset and study entry (i.e., duration after 0.4 ± 0.9, respectively, for the sham group and −0.4 ± 0.5, 2.3 ± 2.7,
stroke) was 20 ± 8 months. The mean Functional Independence and 3.3 ± 2.7, respectively, for the real group. Examination of
Measure (21), which evaluates ADL, was 86.3 ± 9.1 at study entry. between-group differences showed a significant improvement in
The median score of the modified Rankin Scale (22) and the Func- speed (p = 0.008) and capacity (p = 0.005) for the real group com-
tional Oral Intake Scale (23), which respectively evaluate stroke pared with the sham group. However, no significant difference in ISI
severity and oral intake state, were 1 and 7, respectively. No signifi- (p = 0.76) could be found between the groups. Patients in the real
cant differences were observed between the sham and real groups group expressed feelings of diminished anxiety about choking
for demographic variables, including age (p = 0.40), duration after during water swallowing and easier production of the swallowing
stroke (p = 0.94), and the Function Independence Measure (p = 0.40). reflex after FMS.
FMS procedures were all completed without deterioration of
adverse reactions. Values for ISI, speed, and capacity before and
after FMS and the amount of change are shown in Figures 2–4. The DISCUSSION
mean values for prestimulation ISI, speed, and capacity for the sham
group were 3.0 ± 0.8, 4.2 ± 2.5, and 11.5 ± 3.1, respectively; for the FMS was feasible and conducted without significant adverse
real group, they were 2.8 ± 0.9, 4.3 ± 2.3, and 10.8 ± 3.2, respectively. events. Swallowing volume velocity and volume per swallow were
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The Mann–Whitney U-test was used to examine whether or not improved for the real group compared with the sham group. Speed

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 MOMOSAKI ET AL.

is the total time it takes to swallow 50 mL; it reflects the overall rate a manometry is expensive and is not commonly performed in Japan.
of serial swallowing and includes the speed from the end of one Therefore, we were unable to take data on pharyngeal contractions.
swallow to the elicitation of the next. Capacity represents the In addition, we did not measure motor-evoked potentials, as we were
amount of water corresponding to one swallow; it reflects the reac- unable to make suitable preparations in time.
tion speed of a single swallowing reflex. By elevating the smooth
continuity and the motor reflex speed of swallowing, FMS improved
both swallowing volume velocity and volume per swallow. On the CONCLUSION
other hand, ISI represents the time a single swallow takes; because
a decrease in the number of swallows necessary to swallow 50 mL The results suggest that FMS improves swallowing reaction speed
accompanied the improvement in capacity, no significant differ- for poststroke dysphagia patients. This could lead to novel interven-
ence in ISI could be observed. tions for dysphagia and will be a necessary methodology to con-
It can safely be said that action mechanism of FMS is similar to sider in the future.
electrical stimulation (15). For example, Lim et al. performed electri-
cal stimulation through surface electrodes on the neck region and
reported significant improvement of swallowing function (24). Elec- Authorship Statements
trical stimulation is thought to assist in the improvement of swal-
lowing function by causing muscle contraction, acting to increase Drs. Momosaki, Yamada, and Mochio designed and conducted
muscle and potentiate endurance (25). In addition, afferent input the study, including patient recruitment, data collection, and data
brings about a certain change in the reflex mechanism in the central analysis. Dr. Momosaki prepared the manuscript draft with impor-
nervous system. This demonstrates the neuromodulatory effect of tant intellectual input from Drs. Abo, Watanabe, and Kakuda. All
electrical stimulation, as typified by the improvement of overactive authors approved the final manuscript.
bladder syndrome through stimulation of the sacral region (26).
One of the afferent pathways of the swallowing reflex is the sensory
branch of the vagus nerve from the pharyngeal mucosa. If the vagus How to Cite this Article:
nerve were stimulated, it is possible that afferent input from the Momosaki R., Abo M., Watanabe S., Kakuda W., Yamada
oropharynx could act on the swallowing reflex center in the medulla N., Mochio K. 2014. Functional Magnetic Stimulation
oblongata and on the cerebral cortex, causing neuromodulation as Using a Parabolic Coil for Dysphagia After Stroke.
excitation of the swallowing response (27). The results of this study Neuromodulation 2014; 17: 637–641
show that FMS improves swallowing reaction speed. There is no
previous studies concerning FMS for dysphagia; it is speculated that
neuromodulation over nerve stimulation causes the effect.
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***
This is an interesting study showing a new application of
neuromodulation. The major strength of the study is the use of a
noninvasive method of functional magnetic stimulation for dysphagia.
However, the study was preliminary and limited in a number of issues:
1) no optimization process was applied to obtain the most effective
parameters for stimulation; and 2) no physiological or mechanistic data
were provided to support the conclusion. A chronic and comprehen-
sive study is needed to truly establish the clinical relevance of this
approach in treating dysphagia.

Jiande Chen, PhD

Galveston, TX, USA

Comments not included in the Early View version of this paper. 641

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