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 swallowing were longer in the elderly subjects than in the young subjects for all beverages. Beverages that the subjects 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 beverage also influenced the subsequent swallowing of water, showing a persistent effect. It was suggested that carbonated 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: [email protected] 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 transmission 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 diseases, 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, posterior wall of the pharynx, pharyngeal surface of the epiglottis, 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 elevating neural excitability through increasing afferent input to the medulla oblongata [16–18]. Studies on the influence

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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 surface 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 associated 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 nervous system disease-associated dysphagia, in which carbonated 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 addition, 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. Carbonated 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 carbonated 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

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carbonated beverages, and we have actually had patients who do not readily aspirate their favorite food. In studies on swallowing, the therapeutic videoradiographic swallowing study (TVSS) and a simple two-step swallowing provocation test (SST) are frequently used. Using TVSS, bolus dynamics in the oral cavity, the pharyngeal 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 sensation 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 International 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 mylohyoid 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 50–5,000Hz bandpass filter was used. Laryngeal movement was measured by attaching a strain gauge (transducer F-12IS, Star Medical, Inc.) to the laryngeal prominence with surgical tape. Signals were synchronized with the electromyography 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 difficult’’ = ?1.0, and ‘‘much more difficult’’ = ?2.0). When it was difficult for a subject to select one of the five categories, 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 beverage 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 swallow 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 measured (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 stimulation 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 laryngeal 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 elevation 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 3

Carbonated beverage (CB) 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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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 laryngeal 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 fullwave rectification, and the standard deviation was calculated. 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 maximum value during muscle contraction was determined from the waveforms smoothed every 15 ms after full-wave rectification and was regarded as the peak muscle contraction value. The rates (%) of RMS and muscle contraction 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 comparison. All data were assessed for sphericity (Mauchly’s test), and, when rejected, the F value was corrected

(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 subject group, followed by Bonferroni’s multiple comparison. For comparison between the young and elderly groups, the Mann–Whitney U test was used. The statistically significant difference level was set at p \ 0.05 in all tests.

Fig. 1 Analytical start points of laryngeal movement and electromyography 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

electromyography waveforms of the suprahyoid muscles after fullwave 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

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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-

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). Similarly, 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 shortened 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 in the elderly group compared to those in the young group, and the difference was significant for all beverages (p \ 0.05, d = 0.921–1.869). Pharyngeal Reaction Time (PRT) The PRT in the young and elderly groups is shown by 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 significantly 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 compared to the young group.

Fig. 2 Duration of laryngeal elevation 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, and marks in the graph represent the presence of a significant difference compared with water in the first session on multiple comparison of repeated-measures ANOVAs (*p \ 0.05, **p \ 0.01). DOLE duration of laryngeal elevation, CB carbonated beverage, CW carbonated water

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 shortened by the beverages in the second session, but no significant 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 contraction 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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Fig. 4 Duration of suprahyoid muscle contraction induced by each beverage. 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). 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 beverage 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.

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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 session. 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 significantly 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 sensation, 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 carbonated 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 laryngeal elevation due to efficient suprahyoid muscle activity. 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 beverage 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. Carbonated 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 palatopharyngeal arch, posterior wall of the pharynx, and posterior 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 carbonated 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 swallowing 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 thermosensitive 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 stimulation 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 laryngeal 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 stimulations 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 swallowing. The effective stimulus in our study was the carbonated beverage, which was more suitable than carbonated water,

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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

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

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 linguapalatal pressure reduction occur with aging and slow swallowing [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

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 contraction 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 carbonated 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 perceived as an unpleasant sour taste stimulation because cells

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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 beverage 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. Currently, cooling and mechanical stimulation of the anterior faucial arches by ice massage before food ingestion are generally performed, but swallowing a carbonated beverage 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 swallowed in order to measure a single swallowing activity. Swallowing a larger volume may increase chemical stimulation 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 shortening 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 subsequent 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 carbonated 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 participated 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.

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Motoyoshi Morishita Sanae Mori

PhD, RPT

RPT

Shota Yamagami

RPT

Masatoshi Mizutani

PhD

Effect of carbonated beverages on pharyngeal swallowing in young individuals and elderly inpatients.

Gustatory and chemical stimulations of the oral cavity and pharyngeal mucosa by carbonated water improve pharyngeal swallowing. We compared changes in...
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