Dysphagia
DOI 10.1007/s00455-013-9493-6
ORIGINAL ARTICLE
Effect of Carbonated Beverages on Pharyngeal Swallowing
in Young Individuals and Elderly Inpatients
Motoyoshi Morishita • Sanae Mori •
Shota Yamagami • Masatoshi Mizutani
Received: 9 March 2013 / Accepted: 25 September 2013
Ó Springer Science+Business Media New York 2013
Abstract Gustatory and chemical stimulations of the oral
cavity and pharyngeal mucosa by carbonated water
improve pharyngeal swallowing. We compared changes in
pharyngeal swallowing and sensory aspects induced by a
carbonated beverage preferred by Japanese with those
induced by carbonated water, a sports drink, and tap water
in healthy young subjects and elderly inpatients with no
swallowing problems. The duration of laryngeal elevation
(DOLE) for swallowing the carbonated beverage and water
in the second session was shorter compared to that for
water in the first session in the elderly subjects. The DOLE
and the duration of suprahyoid muscle activity for swal-
lowing were longer in the elderly subjects than in the
young subjects for all beverages. Beverages that the sub-
jects subjectively felt were easy to swallow were the sports
drink and carbonated beverage, whereas they stated that
carbonated water was less easy to swallow. In the elderly
subjects, swallowing ability latently decreased, even
though they had no problem swallowing in their daily lives,
and it was assumed that the carbonated beverage improved
pharyngeal swallowing. In addition, the carbonated bev-
erage also influenced the subsequent swallowing of water,
showing a persistent effect. It was suggested that carbon-
ated beverages are easy to swallow and effective for the
improving pharyngeal swallowing.
M. Morishita (&)
M. Mizutani
Department of Physical Therapy, Kibi International University, 8
Iga-machi, Takahashi, Okayama 716-8508, Japan
e-mail: m_mori@kiui.ac.jp
M. Morishita
S. Mori
S. Yamagami
Rehabilitation Center, Watanabe Hospital, Shiseikai Medical
Corporation, 2032-15 Niimi, Niimi, Okayama 718-0011, Japan
Keywords Deglutition
Deglutition disorders
Sensory
stimulation
Carbonated beverages
The swallowing reflex is normally induced by the trans-
mission of sensory stimulation of the oral cavity, pharynx,
and larynx to the medulla oblongata [1–3]. Reportedly, the
swallowing reflex delays in the elderly due to anatomical
[4–6] and functional [6–9] changes in the oral cavity,
pharynx, larynx, and upper esophagus reduced sensory
receptor thresholds [10–12], and reduced nerve conduction
velocity [13]. In patients with central nervous system dis-
eases, the swallowing reflex is impaired due to pharyngeal
and laryngeal sensory disturbance, motor paralysis, and the
reduction of substance P synthesis associated with a
reduction of dopamine synthesis in the basal ganglia [14,
15]. Poor oral ingestion due to a delayed and impaired
swallowing reflex leads to nutritional disturbance and
exacerbation of the general condition, and increases the
risk of aspiration pneumonia. Therefore, it is necessary to
investigate a method to induce an appropriate swallowing
reflex.
Sensory stimulation is frequently applied to facilitate the
pharyngeal swallowing reflex, and, reportedly, mechanical
stimulation of the soft palate, anterior faucial pillars, pos-
terior wall of the pharynx, pharyngeal surface of the epi-
glottis, and pharyngoesophageal junction is effective in
inducing the swallowing reflex [1–3]. In particular, cold
thermal tactile stimulation is frequently applied to the oral
cavity and pharynx for treatment of dysphagia patients with
problems with the pharyngeal and laryngeal phases. It is
believed to facilitate the swallowing reflex by reducing the
receptor threshold in the anterior faucial pillars and ele-
vating neural excitability through increasing afferent input
to the medulla oblongata [16–18]. Studies on the influence
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 M. Morishita et al.: Effect of Carbonated Beverages on Pharyngeal Swallowing
of carbonated water on swallowing have recently been
performed, focusing on the stimulation of receptors in the
oral mucosa by carbonic acid. Muscle activity was not
influenced in some reports [19], but a shorter pharyngeal
transit time and little pharyngeal retention of carbonated
water compared to those of normal water [20] and an
increase in the high-frequency content of submental sur-
face electromyography (sEMG) [21] were observed in
others. Shortening of the pharyngeal transit time of tablets
swallowed with carbonated water has also been reported
[22]. A very recent study reported that cooled carbonated
water activated afferent input to the central nervous system
and improved water swallowing movement [23]. Jennings
et al. [24] reported that water ingestion using carbonated
beverages was possible in patients with dysphagia associ-
ated with oropharyngeal dysfunction following skull base
tumor resection. The linguapalatal pressure of swallowing
a carbonated beverage (ginger ale) has been investigated
[25]. Ginger ale is thought to stimulate chemoreceptors in
the oral cavity and pharynx with carbonic acid and gingerol
and improve the linguapalatal pressure compared to plain
water. There was also an investigation of reactions while
swallowing carbonated water of patients with central ner-
vous system disease-associated dysphagia, in which car-
bonated water was less aspirated and retained in the
pharynx compared to noncarbonated, thin liquid, but no
differences were noted in the oral or pharyngeal transit
time, initiation of the pharyngeal swallow, or pharyngeal
retention [26].
Reportedly, the swallowing reflex is also altered by
gustatory stimulation. Among gustatory stimulations, sour
taste stimulation is expected to increase the linguapalatal
pressure and suprahyoid muscle activity [27–29]. In addi-
tion, salty and sweet taste stimulations have been reported
to improve the linguapalatal pressure and suprahyoid
muscle activity compared to those tastes without gustatory
stimulation [19, 28, 29]. However, the ingestion of very
sour or salty food to induce swallowing is unpleasant with
regard to the taste or ease of eating, although they are
edible [27], and the introduction of these foods into meals
is practically difficult.
Previous studies on swallowing with carbonated water
were performed mostly in the Western countries. Carbon-
ated mineral water is commercially available in these
countries, and it is common to drink sugarless carbonated
water. However, Japanese are not familiar with drinking
sugarless carbonated water. Considering the preference of
dysphagia patients, this situation may be a problem with
respect to introducing the continuous ingestion of carbon-
ated water. Investigation of tasty food stimulating the oral
cavity and pharynx is important to increase volition for
ingestion and improve the swallowing reflex in patients.
We heard that dysphagia patients do not aspirate beer and
123
carbonated beverages, and we have actually had patients
who do not readily aspirate their favorite food.
In studies on swallowing, the therapeutic videoradio-
graphic swallowing study (TVSS) and a simple two-step
swallowing provocation test (SST) are frequently used.
Using TVSS, bolus dynamics in the oral cavity, the pha-
ryngeal transit time, and pharyngolaryngeal and upper
esophageal movement during swallowing can be analyzed,
but the preparation of contrast imaging-applicable physical
properties and an X-ray device are necessary. In SST, a
thin tube is inserted into the oropharynx through the nasal
cavity and swallowing reactions to liquid infusion are
observed. This is considered a useful swallowing reflex test
[30, 31]. However, the medical procedure of placing a tube
through the nasal cavity is necessary but stressful for the
patient, and it is not always doable at places other than
medical facilities. Analyses of laryngeal prominence and
swallowing movements on sEMG are used to study the
muscle activity pattern and contraction intensity during
swallowing and the oral and pharyngeal transit time of the
bolus and water [32, 33]. Although the transit time is less
reliable than that from TVSS, it can be measured by simply
applying electrodes and sensors to the skin of the face and
neck, which is less stressful to the patient.
Using a carbonated beverage familiar for Japanese, we
investigated differences in the swallowing reflex pattern
with stimulation from carbonic acid alone, gustatory sen-
sation alone, and water based on surface electromyograms,
laryngeal movement, and sensory aspects. The goal was to
find a beverage that is easy to swallow and safely and
effectively induces the swallowing reflex in both young
and elderly subjects.
Methods
Participants
The subjects were 14 healthy young individuals attending
Kibi International University [mean age 21.1 ± 0.3 years
(range = 21–22 years)] and 14 elderly inpatients [mean age
79.6 ± 9.0 years (55–90 years)] admitted for fracture and
internal diseases and who consented to participate in the
study. The mean duration of hospitalization was
40.7 ± 35.5 days (7–110 days). The elderly inpatients who
met the following three criteria were selected with respect to
the risk of aspiration: (1) not diagnosed with dysphagia, (2)
oral food ingestion was permitted by their physician, and (3)
normal repetitive saliva swallowing test (i.e. able to swallow
saliva three times or more within 30 s) [34]. Subjects with a
communicative disorder or dementia, otorhinolaryngeal and
dental diseases, and spinal deformity that affected oral
ingestion were excluded. The study was initiated after
M. Morishita et al.: Effect of Carbonated Beverages on Pharyngeal Swallowing
explaining the content to all subjects using documents and
obtaining consent. The study was approved by Kibi Inter-
national University’s Institutional Ethics Board.
Instrumentation
Bipolar lead electromyography was performed using Bio
Amp (FE-136, AD Instruments Pty, Ltd., Australia) and
44.8-mm 9 22-mm oval disposable Ag/AgCl electrodes
(Blue sensor N-00-S, Ambu, Denmark). Electrodes were
applied to a site slightly posterior to the mandibular mental
protuberance and the middle point between the mental
protuberance and hyoid bone. The muscle action potential
from the sites represented the total muscle activity of the
suprahyoid muscles comprising the geniohyoid and mylo-
hyoid muscles and anterior belly of the digastric. The
ground electrode was attached to the antebrachial protruded
region. The sampling frequency was 1 kHz, and a 50–5,000-
Hz bandpass filter was used. Laryngeal movement was
measured by attaching a strain gauge (transducer F-12IS,
Star Medical, Inc.) to the laryngeal prominence with sur-
gical tape. Signals were synchronized with the electromy-
ography signals using a bridge box (FB-01, Star Medical,
Inc.), strain amplifier (FS-04M, Star Medical, Inc.), and
PowerLab (AD Instruments Pty, Ltd.). In regard to sensory
aspects, using the subjective difficulty of swallowing (SDS)
reported by Miyaoka et al. [33], individual subjects stated
their SDS for each beverage with respect to conveying the
beverage to the pharynx compared to swallowing water in
the first session using a five-step scale (‘‘much easier’’ =
-2.0, ‘‘easier’’ = -1.0, ‘‘equal’’ = 0.0, ‘‘more diffi-
cult’’ = ?1.0, and ‘‘much more difficult’’ = ?2.0). When
it was difficult for a subject to select one of the five cate-
gories, we allowed an in-between rating such as -1.5 or
?0.5.
Procedure
The subjects were instructed to avoid eating and drinking
2 h before measurements would be taken. The subject sat
on a backed chair in a comfortable posture, and a desk was
placed in front. The examiner held 3 ml of the test bev-
erage in a syringe, instructed the subject to open the mouth
while minimally extending the neck, and rapidly infused
the beverage under the tongue. The subject was instructed
to close his/her mouth and swallow the beverage as rapidly
as possible; the examiner sent a signal to the PowerLab at
the moment he visually confirmed that the lips were closed.
To reduce mixing of electromyography signals associated
with neck movement and strain amplifier signals of the
laryngeal prominence, the subject was instructed to swal-
low the infused beverage with as little neck movement as
possible.
Stimuli
The test beverages were tap water, a carbonated beverage
(Mitsuya-Cider, Asahi soft drinks, Co., Ltd., Japan), a
sports drink (Aquarius, Coca-Cola, Co., Ltd., Japan) as a
gustatory stimulation without carbonic acid, and sugarless
carbonated water (Suntory-Soda, Suntory Holdings, Ltd.,
Japan) as stimulation by carbonic acid alone. All beverages
were similarly chilled in a refrigerator to prevent the
influence of temperature, and the temperature was mea-
sured (set at about 10 °C). To minimize the influence of
drinking intervals, a 1-min rest period was allowed before
swallowing the next beverage; the subjects were allowed to
swallow saliva.
The beverages were swallowed in the order shown in
Table 1. Carbonated water was used as stimulation by
carbonic acid alone, the sports drink was used as stimula-
tion by sweet taste alone, and water was used as a condition
with no stimulation.
Data Analysis and Reduction
The strain gauge waveforms, electromyography waveforms
after full-wave rectification, and waveforms after 15-ms
smoothing were analyzed. The baseline points of analyses
are shown in Fig. 1. In the strain gauge attached to the
laryngeal prominence, waveforms appeared when the lar-
yngeal prominence rose and fell. In this study, the interval
between the peaks at the rise and fall of the laryngeal
prominence was designated as the duration of laryngeal
elevation. Also, the beginning of the first rise of the
waveform after lip closure was regarded as the beginning
of laryngeal movement, and the interval between this point
and the peak of laryngeal elevation was defined as the
pharyngeal reaction time. The duration of laryngeal ele-
vation is considered to be the time when the esophageal
entrance is relaxed and the beverage is transported into the
esophagus [35–37]. While it is not equivalent to the
Table 1 Order of stimulus presentation of beverages
Trial Beverages
1st session
1 Tap water
2 Carbonated beverage (CB)
3 Sports drink
4 Carbonated water (CW)
2nd session
5 Tap water
6 Carbonated water (CW)
7 Sports drink
8 Carbonated beverage (CB)
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 M. Morishita et al.: Effect of Carbonated Beverages on Pharyngeal Swallowing
pharyngeal transit time in a strict sense, we considered it to
be an index of the smoothness of beverage transit. The
pharyngeal reaction time is an index of the speed of lar-
yngeal elevation in the initial phase of the swallowing
reflex.
In regard to the electromyography waveform, the
amplitude was measured for 5 s in a resting state after full-
wave rectification, and the standard deviation was calcu-
lated. Defining the interval between when the amplitude of
the full-wave-rectified waveform immediately before the
start of laryngeal movement based on the strain gauge
waveforms exceeded 2 standard deviations (2 SD) and
when the amplitude decreased to \2 SD as the duration of
suprahyoid muscle contraction, the muscle contraction time
and root mean square (RMS) were determined. The max-
imum value during muscle contraction was determined
from the waveforms smoothed every 15 ms after full-wave
rectification and was regarded as the peak muscle con-
traction value. The rates (%) of RMS and muscle con-
traction peaks relative to those for water in the first session,
which was regarded as 100 %, were calculated in each
subject.
Statistical analysis was performed using SPSS ver. 20
(SPSS, IBM, Chicago, IL, USA). The measured values
were subjected to repeated-measures one way analysis of
variance (ANOVA) for each beverage in the young and
elderly groups, followed by Bonferroni’s multiple com-
parison. All data were assessed for sphericity (Mauchly’s
test), and, when rejected, the F value was corrected
Fig. 1 Analytical start points of laryngeal movement and electromy-
ography waveforms of the suprahyoid muscles. The vertical dotted
line represents the timing of lip closure. The upper row shows strain
gauge waveforms during laryngeal movement. The first waveform
appeared when the laryngeal prominence rose, and the second
waveform appeared when it fell. The middle row shows the
123
(Greenhouse–Geisser). In repeated-measures ANOVAs,
the main effect size of each beverage was determined using
the effective size (Cohen’s f) calculated from partial g2
(g2P). The resulting f value was interrupted with 0.25–0.4 as
a medium effect and 0.4 or greater as a large effect. On
multiple comparisons, Cohen’s d was determined for all
significant pairs. The resulting d value was interrupted with
0.4–0.8 as a medium effect and 0.8 or greater as a large
effect. To compare the young and elderly groups, the t test
was performed for all beverages. The SDS was compared
between the beverages using Friedman’s test in each sub-
ject group, followed by Bonferroni’s multiple comparison.
For comparison between the young and elderly groups, the
Mann–Whitney U test was used. The statistically signifi-
cant difference level was set at p \ 0.05 in all tests.
Results
Duration of Laryngeal Elevation (DOLE)
In all subjects, flat waveforms on the baseline were noted
between elevation and fall of the laryngeal prominence,
showing that the thyroid cartilage was sufficiently elevated
while swallowing the beverages. The DOLE for each
beverage in the young and elderly groups is shown in
Fig. 2. On comparison between the beverages in the young
group, no significant difference was noted in any pair of
beverage. In the elderly group, a significant between-
electromyography waveforms of the suprahyoid muscles after full-
wave rectification. Waveforms in the middle row smoothed every
15 ms are shown in the bottom row. SH suprahyoid muscles, PRT
pharyngeal reaction time, DOLE duration of laryngeal elevation, RMS
root mean square. See text for details
M. Morishita et al.: Effect of Carbonated Beverages on Pharyngeal Swallowing

beverage difference was noted on repeated-measures

ANOVAs [F(7,91) = 4.542, p \ 0.01, f = 0.591]. On
multiple comparisons, the DOLE for water in the first
session was 1.23 ± 0.34 s and that for CB in the first
session was 0.94 ± 0.37 s, which shows that the DOLE
was significantly shortened (p \ 0.01, d = 0.817). Simi-
larly, the DOLE for water in the second session was
0.95 ± 0.31 s (p \ 0.05, d = 0.861) and that for CB in the
second session was 0.86 ± 0.3 s (p \ 0.01, d = 1.154);
these values show that the DOLE was significantly short-
ened compared to that for water in the first session. No
significant difference was noted in any other pair in the
elderly group. The DOLE for all beverages was prolonged
Fig. 2 Duration of laryngeal elevation by beverage in young and
in the elderly group compared to those in the young group, elderly subjects. Numbers in parentheses following beverage names
and the difference was significant for all beverages represent the session number and error bars represent standard
(p \ 0.05, d = 0.921–1.869). deviation. Marks following beverage names represent the presence of
a significant difference between the young and elderly subjects on the
t test, and marks in the graph represent the presence of a significant
Pharyngeal Reaction Time (PRT) difference compared with water in the first session on multiple
comparison of repeated-measures ANOVAs (*p \ 0.05, **p \ 0.01).
The PRT in the young and elderly groups is shown by DOLE duration of laryngeal elevation, CB carbonated beverage, CW
carbonated water
beverage in Fig. 3. On repeated-measures ANOVA, no
significant difference was noted for any pair of beverages
in the young or elderly group. On comparison by beverage
between the young and elderly groups, the PRT was sig-
nificantly prolonged for CB and the sports drink in the first
session, for water in the second session (p \ 0.05,
d = 0.900–0.987), and for CW and CB in the second
session (p \ 0.01, d = 1.213–1.314) in the elderly com-
pared to the young group.

Duration of Muscle Contraction

The durations of suprahyoid muscle contraction in the

young and elderly groups are shown by beverage in Fig. 4.
On between-beverage comparison in the young group, the
duration induced by water in the first session was
0.73 ± 0.24 s, whereas duration induced by carbonated
water (CW) in the second session was 0.65 ± 0.23 s and
that by CB in the second session was 0.65 ± 0.22 s,
showing that the duration of muscle contraction was short-
ened by the beverages in the second session, but no signif-
icant difference was noted on repeated-measures ANOVAs.
In the elderly group, the duration of muscle contraction
induced by water in the first session was 1.27 ± 0.5 s,
whereas that by CB in the first session was 1.06 ± 0.39 s,
that by CW in the first session was 1.07 ± 0.27 s, and that
by CB in the second session was 0.95 ± 0.33 s, showing
that the duration of muscle contraction was shortened by the
beverages compared to that induced by water in the first
session, but no significant difference was detected on
repeated-measures ANOVAs. On comparison between the
young and elderly groups, the duration of muscle contrac-
tion was prolonged by all beverages in the elderly group
Fig. 3 Pharyngeal reaction time by beverage in young and elderly
subjects. Numbers in parentheses following beverage names represent
the session number and error bars represent standard deviation.
Marks following beverage names represent the presence of a
significant difference between the young and elderly subjects on the
t test (*p \ 0.05, **p \ 0.01). PRT pharyngeal reaction time, CB
carbonated beverage, CW carbonated water
compared to that in the young group, and the difference was
significant for all beverages (p \ 0.05, d = 0.936–1.377).
Root Mean Square (RMS)
The RMS rates of the suprahyoid muscles in the young and
elderly groups are shown by beverage in Fig. 5. On
between-beverage comparison in the young group, RMS
tended to decrease in the second session but no significant
difference was detected on repeated-measures ANOVAs

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 M. Morishita et al.: Effect of Carbonated Beverages on Pharyngeal Swallowing
Fig. 4 Duration of suprahyoid muscle contraction induced by each
beverage. Numbers in parentheses following beverage names repre-
sent the session number and error bars represent standard deviation.
Marks following beverage names represent the presence of a
significant difference between the young and elderly subjects on the
t test (*p \ 0.05). CB carbonated beverage, CW carbonated water
due to large individual variations. In the elderly group,
RMS tended to increase when CW and CB were swallowed
in the first and second sessions but no significant difference
was detected on repeated-measures ANOVAs due to large
individual variations. No significant difference was also
noted between the young and elderly groups for any bev-
erage on the t test.
Peak Amplitude
The peak suprahyoid muscle activity rates in the young and
elderly groups are shown in Fig. 6. On between-beverage
comparison in the young group, the peak value tended to
decrease in the second session but no significant difference
was detected on repeated-measures ANOVAs due to large
individual variations. In the elderly group, the peak value
tended to increase for all beverages in the second session but
no significant difference was detected on repeated measures
ANOVAs due to large individual variations. No significant
difference was noted on comparison between the young and
elderly groups for each beverage using the t test.
Sensory Aspects
The SDS values in the young and elderly groups are shown
by beverage in Fig. 7. The beverage with the highest SDS
value (most difficult to swallow) in the young group was
CW in the first and second sessions and that with the lowest
value (easiest to swallow) was the sports drink in the
second session. A significant difference was noted between
the beverages on Friedman’s test (v2 = 14.938, p \ 0.05)
but not on multiple comparison. Similarly, the beverage
with the highest SDS value (most difficult to swallow) was
CW in the first and second sessions in the elderly group.
123
Fig. 5 RMS rate of suprahyoid muscle contraction induced by
beverage. The rates (%) relative to RMS of muscle contraction
induced by water in the first session are presented. Numbers in
parentheses following beverage names represent the session number
and error bars represent standard deviation. No significant differences
were noted between the beverages or between the young and elderly
groups. RMS root mean square, CB carbonated beverage, CW
carbonated water
Those with the lowest value (easiest to swallow) were CB
in the first session and the sports drink in the second ses-
sion. A significant difference between the beverages was
noted on Friedman’s test (v2 = 39.568, p \ 0.01). On
multiple comparison, compared to those of CW in the first
and second sessions, the SDS values of CB in the first
session (p \ 0.05) and the sports drink in the first
(p \ 0.05) and second (p \ 0.01) sessions were signifi-
cantly lower (easier to swallow). No significant difference
was noted between the young and elderly groups for any
beverage on the Mann–Whitney U test.
Discussion
Differences in the patterns of the swallowing reflex
induced by stimulation with carbonic acid, gustatory sen-
sation, and both, compared to that induced by water, were
evaluated based on the surface electromyograms of the
suprahyoid muscles, records of laryngeal movement, and
SDS, and the swallowing reflex-inducing effect of car-
bonated beverages was investigated in healthy young and
elderly subjects.
In this study, the DOLE, defined as the interval between
the peaks of waveforms at the rise and fall of the laryngeal
prominence, was used as an index of the smoothness of the
passage of a beverage into the esophagus. The PRT reflects
the speed of laryngeal elevation in an initial phase of
swallowing. A short PRT indicates rapid and smooth lar-
yngeal elevation due to efficient suprahyoid muscle activ-
ity. In contrast, its prolongation is considered to indicate an
increased risk of aspiration due to inefficient muscle
M. Morishita et al.: Effect of Carbonated Beverages on Pharyngeal Swallowing
Fig. 6 Rate of peak suprahyoid muscle contraction by beverage. The
rates (%) relative to the peak muscle contraction value induced by
water in the first session are presented. Numbers in parentheses
following beverage names represent the session number and error
bars represent standard deviation. No significant differences were
noted between the beverages or between the young and elderly
groups. CB carbonated beverage, CW carbonated water
activities. In this study, no difference in the PRT by bev-
erage was observed, but the DOLE was shortened in the
elderly group for CB in the first and second sessions and
for water in the second session compared with water in the
first session. Similarly, in studies in which the pharyngeal
transit time of CW was measured using videofluorography,
the pharyngeal transit time of carbonated water was shorter
than those of thin and thickened liquids [20], showing that
our findings support the results of earlier studies. Carbon-
ated water stimulates nociceptors of the oral mucosa when
carbon dioxide (CO2) dissolved in beverages reacts with
carbonic anhydrase IV (CA-IV) in salivary enzymes and
produces carbonic acid (H2CO3) [38, 39]. Regarding the
gustatory receptors sensing stimuli of carbonated water,
when carbonic acid in carbonated water is dissociated into
bicarbonate ions and free protons in the oral cavity, the free
protons stimulate sour-sensitive taste receptor cells through
the facial nerve [40]. The most stimulation-sensitive
regions for the induction of swallowing are the palato-
pharyngeal arch, posterior wall of the pharynx, and pos-
terior border of the soft palate, and stimulation of the
superior laryngeal nerve (SLN) and pharyngeal branch of
the glossopharyngeal nerve (GPN-ph) induces swallowing
[41]. In our study, carbonic acid may have chemically
stimulated the nerves through nociceptors in these regions
and promoted swallowing. In a recent study, chilled car-
bonated water markedly shortened the swallowing reaction
time [23]. The authors discussed that chemical stimulation
of the pharynx by carbonic acid induced afferent sensory
input and activated the central swallow-inducing nerve
network.
Mechanical and cooling stimulations are widely used to
induce the swallowing reflex in the pharyngeal phase.
Lazzara et al. [17] reported that a single stimulation of the
anterior faucial arches reduced the threshold of oral
mucosal receptors for temperature and tactile stimulations,
and, following five to six inductions, pharyngeal swal-
lowing remained improved. Kaatzke-MacDonald et al. [42]
investigated the effects of cooling, gustatory, and
mechanical stimulations on the anterior faucial pillar based
on the latency time of swallowing and frequency of
repetitive swallowing, and they discussed that thermosen-
sitive receptors induce swallowing in response to cooling
mechanical stimulation. Since in one report [23] chilled
carbonated water markedly shortened the swallowing
reaction time, it was thought that the shortening of the
duration of laryngeal elevation by complex stimulation of
the oral cavity and pharyngeal mucosa by using chilled
beverages and carbonic acid was the result of the 10 °C
beverage. However, since the beverage volume was only
3 ml and it was infused under the tongue, the beverage may
have been warmed before transport to the pharynx and the
effect of the chilled beverage stimulation was lost. The
shortening effect by water in the second session was also
observed, but this may have been due to persistence of the
pharyngeal swallow-inducing effect of chemical stimula-
tion by carbonic acid, not an effect of chilled beverage
stimulation, suggesting the possibility of a therapeutic
approach using carbonic acid in addition to water ingestion
for dysphagia patients.
Carbonated water did not shorten the duration of lar-
yngeal elevation, and shortening was noted only with the
carbonated beverage and water in the second session,
suggesting that gustatory stimulation was involved, in
addition to mechanical stimulation by carbonic acid. Sour
taste stimulation is widely used as an effective gustatory
stimulation to improve pharyngeal swallowing. Sour taste
stimulation reportedly improves the swallowing reflex by
increasing sensory input from the SLN and GPN-ph [43,
44]. Neurologically, the facial nerve activity level increases
when salty and sweet materials are tasted [45, 46]. Facial
and glossopharyngeal nerve activation enhances sensory
nerve activation in the nucleus tractus solitarius (NTS)
[19], and sweet and bitter taste stimulations are important
swallow-facilitating factors regulating the cerebral cortical
swallowing movement pathway by exciting and inhibiting
the NTS and transmitting sensory stimulation to the NTS
through the brainstem pathway [47]. Babaei et al. [48]
performed a study using functional magnetic resonance
imaging in which gustatory, olfactory, and visual stimula-
tions with the subjects’ favorite food, such as popcorn and
chocolate, activated swallowing-related cerebral cortical
regions. Therefore, stimulations by sweet taste and one’s
favorite food may also neurologically facilitate swallow-
ing. The effective stimulus in our study was the carbonated
beverage, which was more suitable than carbonated water,
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 M. Morishita et al.: Effect of Carbonated Beverages on Pharyngeal Swallowing
Fig. 7 Changes in subjective difficulty on swallowing beverages.
Numbers in parentheses following beverage names represent the
session number. The upper and lower ends of columns represent the
upper (75 %) and lower (25 %) quartiles, respectively. The upper and
suggesting that this beverage also neurologically facilitates
swallowing through both factors: sweet taste stimulation
and preference. Preference for the sports drink was similar
to that for sweet taste, but the difference in the effect from
that of water was unclear. The carbonated beverage may
have shortened the duration of laryngeal elevation through
a synergistic effect with chemical stimulation by carbonic
acid.
The duration of laryngeal elevation and duration of
muscle contraction were longer in the elderly than in the
young subjects. The PRT was also prolonged except for
some beverages. Physiological changes such as linguapal-
atal pressure reduction occur with aging and slow swal-
lowing [49]. It has been reported [50] that the threshold
volume of pharyngeal swallows induced by pharyngeal
stimulation with water is increased in the elderly. Since
sensory functions, i.e., perceptions of viscosity and tastes in
the oral cavity, decline with aging, when the intensities of
gustatory and somatic sensory stimulations are similar, the
effect related to swallowing is lower in elderly than in
young individuals [51], indicating that strong gustatory and
somatic sensory stimulations are necessary for the elderly
because the sensitivity threshold is decreased. Since the
baseline muscle activity level is decreased in the elderly, it
may be possible to regulate pharyngeal swallowing by
applying sufficient stimulation, and our study suggested
that the duration of laryngeal elevation was altered.
Changes in sensory motor physiology start in middle age
123
lower ends of error bars represent the maximum and minimum
values, respectively, and the cross bar represents the median. In
beverages without columns, the upper and lower quartiles and median
were identical. CB carbonated beverage, CW carbonated water
and increase with aging [52]. In our elderly subjects,
swallowing problems were not actualized in daily living
activities, but age-related anatomical and physiological
changes in sensation and movement had occurred, through
which pharyngeal swallowing slowed and muscle con-
traction was prolonged in the test with water in the first
session, and these may have been altered by stimulation.
Regarding suprahyoid muscle activity, since muscle
strength and contraction morphology are altered in the
elderly, muscle activity enhancement by chemical and
gustatory stimulations with carbonic acid indicates the
improvement of pharyngeal swallowing. Muscle activity
enhancement was expected, but no significant differences
were noted among the beverages due to large individual
variations. In contrast, in the young subjects, reduction in
muscle activity level by stimulation indicates efficient
pharyngeal swallowing because the baseline muscle
activity level is sufficiently high. However, no significant
differences were noted due to large individual variations,
similar to those in the elderly subjects.
On the evaluation using SDS, the beverage most difficult
to swallow by both young and elderly subjects was car-
bonated water. One reason for this is that Japanese may not
be familiar with chemical stimulation by carbonic acid not
accompanied by gustatory stimulation because they do not
have much occasion to drink sugarless carbonated water. It
was also possible that carbonic acid stimulation was per-
ceived as an unpleasant sour taste stimulation because cells
M. Morishita et al.: Effect of Carbonated Beverages on Pharyngeal Swallowing
detecting gas and dissolved carbon dioxide also perceive a
sour taste [40]. In contrast, the beverages easy to swallow
were the sports drink and carbonated beverage. Miyaoka
et al. [33] investigated feelings of difficulty in swallowing
umami, salty, bitter, sour, and sweet taste samples and
observed that the sweet taste sample tended to be easy to
swallow. The sports drink and carbonated beverage were
more preferred, suggesting that swallowing these was easy
due to both neurological factors and gustatory preference.
This study showed not only changes in the pharyngeal
and laryngeal responses on swallowing carbonated water,
which had been reported, but also shortening of the DOLE
on swallowing water in the second session, suggesting that
chemical and gustatory stimulation by the carbonated
beverage affected subsequent drinking of other beverages.
Therefore, drinking a small amount of a carbonated bev-
erage before a meal as well as modification of the water
ingestion method may have favorable effects on dysphagia
patients such as reducing the risk of food aspiration. Cur-
rently, cooling and mechanical stimulation of the anterior
faucial arches by ice massage before food ingestion are
generally performed, but swallowing a carbonated bever-
age is a simple method requiring no special technique and
is easy to do, even for caregivers not specialized in medical
work. In addition, a synergistic effect may be expected
when a carbonated beverage is combined with mechanical
stimulation. However, only 3 ml of beverage was swal-
lowed in order to measure a single swallowing activity.
Swallowing a larger volume may increase chemical stim-
ulation and exhibit a cooling stimulation of the anterior
faucial arches. Changes were noted upon pharyngeal
swallowing of water in the second session, but the basis for
the persistent effect of the carbonated beverage is still
unknown. The duration of the effect must be investigated
in detail by increasing the swallowing volume.
Conclusion
The influence of swallowing a small volume of a carbonated
beverage on pharyngeal swallowing was investigated by
comparing it with that of water, carbonated water, and a
sports drink using the duration of laryngeal elevation,
suprahyoid muscle activity, and subjective difficulty in
swallowing as indices. The DOLE, based on the movements
of the laryngeal prominence, was shortened in the elderly
subjects by drinking a carbonated beverage, and this short-
ening was also observed on drinking water in the second
session. These effects may have been due to chemical
stimulation by carbonic acid and gustatory stimulation by a
sweet taste, and a persistent effect that influenced the sub-
sequent swallowing of beverages was also suggested. The
effect may have been readily exhibited in the elderly subjects
because their swallowing function had latently declined. The
carbonated beverage was the easiest to swallow in both
young and elderly subjects on the evaluation of ease of
swallowing, showing that carbonated beverages are readily
accepted by Japanese and may improve swallowing. We are
planning to increase the swallowing volume of the carbon-
ated beverages used and closely investigate the persistent
effect when cooling and chemical stimulations of the oral
cavity and pharynx are increased.
Acknowledgments We are grateful to the 28 subjects who partici-
pated in the study and Ms. Mariko Kobayashi at Watanabe Hospital
for her supervision of and instruction for the study.
Conflict of interest The authors have no conflict of interest or
financial ties to disclose.
References
1. Miller RF, Sherrington CS. Some observations on the bucco-
pharyngeal stage of reflex deglutition in the cat. Q J Exp Physiol.
1916;9:147–86.
2. Pommerenke WT. A study of the sensory areas eliciting the
swallowing reflex. Am J Physiol. 1928;84:36–41.
3. Storey AT. Laryngeal initiation of swallowing. Exp Neurol.
1968;20:359–65.
4. Bassler R. Histopathology of different types of atrophy of the
human tongue. Pathol Res Pract. 1987;182:87–97.
5. Malmgren LT, Fisher PJ, Bookman LM, Uno T. Age-related
changes in muscle fiber types in the human thyroarytenoid
muscle: an immunohistochemical and stereological study using
confocal laser scanning microscopy. Otolaryngol Head Neck
Surg. 1999;121:441–51.
6. Bardan E, Xie P, Brasseur J, et al. Effect of ageing on the upper
and lower oesophageal sphincters. Eur J Gastroenterol Hepatol.
2000;12:1221–5.
7. Newton J, Yemm R. Age changes in contractile properties of
masseter muscle in man. J Oral Rehabil. 1990;17:204–5.
8. Vaiman M, Eviatar E, Segal S. Surface electromyographic studies
of swallowing in normal subjects: a review of 440 adults. Report
1. Quantitative data: timing measures. Otolaryngol Head Neck
Surg. 2004;131:548–55.
9. Takeda N, Thomas GR, Ludlow CL. Aging effects on motor units in
the human thyroarytenoid muscle. Laryngoscope. 2000;110:1018–25.
10. Wohlert AB. Tactile perception of spatial stimuli on the lip
surface by young and older adults. J Speech Hear Res.
1996;39:1191–8.
11. Smith CH, Logemann JA, Burghardt WR, Zecker SG, Rademaker
AW. Oral and oropharyngeal perceptions of fluid viscosity across
the age span. Dysphagia. 2006;21:209–17.
12. Chauhan J, Hawrysh ZJ. Suprathreshold sour taste intensity and
pleasantness perception with age. Physiol Behav. 1988;43:601–7.
13. LaFratta CW, Canestrari R. A comparison of sensory and motor
nerve conduction velocities as related to age. Arch Phys Med
Rehabil. 1966;47:286–90.
14. Veis SL, Logemann JA. Swallowing disorders in persons with
cerebrovascular accident. Arch Phys Med Rehabil. 1985;66:372–5.
15. Arai T, Yoshimi N, Fujiwara H, Sekizawa K. Serum substance P
concentrations and silent aspiration in elderly patients with
stroke. Neurology. 2003;61:1625–6.
123
 M. Morishita et al.: Effect of Carbonated Beverages on Pharyngeal Swallowing
16. Sciortino K, Liss JM, Case JL, Gerritsen KG, Katz RC. Effects of
mechanical, cold, gustatory, and combined stimulation to the
human anterior faucial pillars. Dysphagia. 2003;18:16–26.
17. Lazzara G, Lazarus C, Logemann JA. Impact of thermal stimu-
lation on the triggering of the swallowing reflex. Dysphagia.
1986;1:73–7.
18. Rosenbek JC, Roecker EB, Wood JL, Robbins J. Thermal
application reduces the duration of stage transition in dysphagia
after stroke. Dysphagia. 1996;11:225–33.
19. Ding R, Logemann JA, Larson CR, Rademaker AW. The effects
of taste and consistency on swallow physiology in younger and
older healthy individuals: a surface electromyographic study.
J Speech Lang Hear Res. 2003;46:977–89.
20. Bülow M, Olsson R, Ekberg O. Videoradiographic analysis of
how carbonated thin liquids and thickened liquids affect the
physiology of swallowing in subjects with aspiration on thin
liquids. Acta Radiol. 2003;44:366–72.
21. Miura Y, Morita Y, Koizumi H, Shingai T. Effects of taste solu-
tions, carbonation, and cold stimulus on the power frequency
content of swallowing submental surface electromyography. Chem
Senses. 2009;34:325–31.
22. Hasselbalch H, Jørgensen F, Wamberg T, Hey H. Alternatives to
optimal administration of tablets. Acta Med Scand. 1985;217:
527–30.
23. Michou E, Mastan A, Ahmed S, Mistry S, Hamdy S. Examining
the role of carbonation and temperature on water swallowing
performance: a swallowing reaction-time study. Chem Senses.
2012;37:799–807.
24. Jennings KS, Siroky D, Jackson CG. Swallowing problems after
excision of tumors of the skull base: diagnosis and management
in 12 patients. Dysphagia. 1992;7:40–4.
25. Krival K, Bates C. Effects of club soda and ginger brew on lin-
guapalatal pressures in healthy swallowing. Dysphagia. 2012;27:
228–39.
26. Sdravou K, Walshe M, Dagdilelis L. Effects of carbonated liquids
on oropharyngeal swallowing measures in people with neuro-
genic dysphagia. Dysphagia. 2012;27:240–50.
27. Logemann JA, Pauloski BR, Colangelo L, Lazarus C, Fujiu M,
Kahrilas PJ. Effects of a sour bolus on oropharyngeal swallowing
measures in patients with neurogenic dysphagia. J Speech Hear
Res. 1995;38:556–63.
28. Palmer PM, McCulloch TM, Jaffe D, Neel AT. Effects of a sour
bolus on the intramuscular electromyographic (EMG) activity of
muscles in the submental region. Dysphagia. 2005;20:210–7.
29. Pelletier CA, Dhanaraj GE. The effect of taste and palatability on
lingual swallowing pressure. Dysphagia. 2006;21:121–8.
30. Teramoto S, Matsuse T, Fukuchi Y, Ouchi Y. Simple two-step
swallowing provocation test for elderly patients with aspiration
pneumonia. Lancet. 1999;353:1243.
31. Teramoto S, Fukuchi Y. Detection of aspiration and swallowing
disorder in older stroke patients: simple swallowing provocation
test versus water swallowing test. Arch Phys Med Rehabil.
2000;81:1517–9.
32. Takagi M, Miyaoka Y, Haishima K, Haishima H, Matsunaga K,
Yamada Y. Analysis of swallowing movement using a simple and
safe device. J Jpn Soc Stomatognath Funct. 2001;8:25–30.
33. Miyaoka Y, Haishima K, Takagi M, Haishima H, Asari J, Yamada
Y. Influences of thermal and gustatory characteristics on sensory
and motor aspects of swallowing. Dysphagia. 2006;21:38–48.
34. Oguchi K, Saitoh E, Mizuno M, Baba M, Okui M, Suzuki M. The
repetitive saliva swallowing test (RSST) as a screening test of
functional dysphagia (1) normal values of RSST. Jpn J Rehabil
Med. 2000;37:375–82 [in Japanese].
35. Miller AJ. Deglutition. Physiol Rev. 1982;62:129–84.
123
36. Jacob P, Kahrilas PJ, Logemann JA, Shah V, Ha T. Upper
esophageal sphincter opening and modulation during swallowing.
Gastroenterology. 1989;97:1469–78.
37. Gay T, Rendell JK, Spiro J, Mosier K, Lurie AG. Coordination of
oral cavity and laryngeal movements during swallowing. J Appl
Physiol. 1994;77:357–65.
38. Simons CT, Dessirier JM, Carstens MI, O’Mahony M, Carstens
E. Neurobiological and psychophysical mechanisms underlying
the oral sensation produced by carbonated water. J Neurosci.
1999;19:8134–44.
39. Dessirier JM, Simons CT, Carstens MI, O’Mahony M, Carstens
E. Psychophysical and neurobiological evidence that the oral
sensation elicited by carbonated water is of chemogenic origin.
Chem Senses. 2000;25:277–84.
40. Chandrashekar J, Yarmolinsky D, von Buchholtz L, et al. The
taste of carbonation. Science. 2009;326:443–5.
41. Kitagawa J, Shingai T, Takahashi Y, Yamada Y. Pharyngeal
branch of the glossopharyngeal nerve plays a major role in reflex
swallowing from the pharynx. Am J Physiol Regul Integr Comp
Physiol. 2002;282:R1342–7.
42. Kaatzke-McDonald MN, Post E, Davis PJ. The effects of cold,
touch, and chemical stimulation of the anterior faucial pillar on
human swallowing. Dysphagia. 1996;11:198–206.
43. Shingai T, Miyaoka Y, Ikarashi R, Shimada K. Swallowing reflex
elicited by water and taste solutions in humans. Am J Physiol.
1989;256:R822–6.
44. Kajii Y, Shingai T, Kitagawa J, et al. Sour taste stimulation
facilitates reflex swallowing from the pharynx and larynx in the
rat. Physiol Behav. 2002;77:321–5.
45. Nejad MS. The neural activities of the greater superficial petrosal
nerve of the rat in response to chemical stimulation of the palate.
Chem Senses. 1986;11:283–93.
46. Frank ME, Bieber SL, Smith DV. The organization of taste
sensibilities in hamster chorda tympani nerve fibers. J Gen
Physiol. 1988;91:861–96.
47. Mistry S, Rothwell JC, Thompson DG, Hamdy S. Modulation of
human cortical swallowing motor pathways after pleasant and
aversive taste stimuli. Am J Physiol Gastrointest Liver Physiol.
2006;291:G666–71.
48. Babaei A, Kern M, Antonik S, et al. Enhancing effects of flavored
nutritive stimuli on cortical swallowing network activity. Am J
Physiol Gastrointest Liver Physiol. 2010;299:G422–9.
49. Humbert IA, Robbins J. Dysphagia in the elderly. Phys Med
Rehabil Clin N Am. 2008;19:853–66.
50. Shaker R, Ren J, Zamir Z, Sarna A, Liu J, Sui Z. Effect of aging,
position, and temperature on the threshold volume triggering
pharyngeal swallows. Gastroenterology. 1994;107:396–402.
51. Shaker R, Ren J, Bardan E, et al. Pharyngoglottal closure reflex:
characterization in healthy young, elderly and dysphagic patients
with predeglutitive aspiration. Gerontology. 2003;49:12–20.
52. Robbins J, Hamilton JW, Lof GL, Kempster GB. Oropharyngeal
swallowing in normal adults of different ages. Gastroenterology.
1992;103:823–9.
Motoyoshi Morishita PhD, RPT
Sanae Mori RPT
Shota Yamagami RPT
Masatoshi Mizutani PhD