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Coordination of tongue pressure production, hyoid movement, and suprahyoid muscle activity during squeezing of gels
Archives of Oral Biology 111 (2020) 104631
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Coordination of tongue pressure production, hyoid movement, and suprahyoid muscle activity during squeezing of gels
T
Kazuhiro Murakamia, Kazuhiro Horib,*, Yoshitomo Minagia, Fumiko Ueharab, Simonne E. Salazarb, Sayaka Ishiharac, Makoto Nakaumac, Takahiro Funamic, Kazunori Ikebea, Yoshinobu Maedaa, Takahiro Onob a
Department of Prosthodontics, Gerodontology and Oral Rehabilitation, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka, 565-0871, Japan Division of Comprehensive Prosthodontics, Niigata University Graduate School of Medical and Dental Sciences, 2-5274 Gakkocho-dori, Niigata, Niigata, 951-8514, Japan c San-Ei Gen F. F. I., Inc., 1-1-11 Sanwa-cho, Toyonaka, Osaka, 561-8588, Japan b
A R T I C LE I N FO
A B S T R A C T
Keywords: Squeezing Gels Tongue movement Tongue pressure Hyoid movement Electromyography
Objective: The aim of this study was to evaluate tongue movement and its biomechanical effects during squeezing, one of the oral strategies for processing soft foods, by tongue pressure sensors, videofluorography, and surface electromyography. Design: Fifteen healthy men (mean age, 31.0 ± 4.1 years) without dysphagia were recruited. A 0.1-mm-thick pressure sensor sheet with five measuring points, videofluorography, and surface electromyography were used for synchronous measurements of tongue pressure, hyoid movement, and suprahyoid muscles activity, respectively, while squeezing 5 mL of gels. Amplitude, duration, area, and their sequential order during initial squeezing were analyzed. Differences in hyoid position at the onset, peak, and offset of hyoid movement were also analyzed. Results: At the beginning of initial squeezing, tongue pressure at the middle area of the hard palate, hyoid movement, and suprahyoid muscle activity appeared simultaneously, followed by tongue pressure at the anterior area and then at the posterior area. When the hyoid was in an elevated position, the amplitude of suprahyoid muscle activity and tongue pressure peaked. At the end of initial squeezing, the hyoid position at the offset of hyoid excursion was superior to that at the onset. All evaluation items of tongue pressure, hyoid movement, and suprahyoid muscle activity were modulated according to the texture of gels. Conclusions: During initial squeezing, tongue pressure, hyoid movement, and suprahyoid muscle activity were coordinated while being modulated by the food texture. At the end of initial squeezing, the hyoid was maintained in an elevated position, which might be beneficial for subsequent squeezing.
1. Introduction As the aging population increases, the proportion of older individuals with mastication and swallowing problems has been increasing, resulting in eating-related aspiration and choking problems (Ministry of Health, Labour & Welfare, 2015; Teramoto et al., 2008). Since aspiration and choking are life-threatening and decrease quality of life, ensuring safety during meals is extremely important in older people. Adjusting the food form is one of the ways to prevent these
problems during meals, and various care foods have been developed to facilitate safe eating without aspiration and choking in older people. Older individuals commonly have decreased masticatory ability due to a reduction in remaining teeth (Ikebe et al., 2012). To improve their masticatory ability, dentists perform prosthetic treatment with dentures; actually, however, many older individuals do not wear dentures even if they require them due to poor dentition (Matsuyama et al., 2017). Thus, when selecting care food for older people, it is necessary to consider not only the masticatory ability of the teeth and dentures, but
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Corresponding author. E-mail addresses: [email protected] (K. Murakami), [email protected] (K. Hori), [email protected] (Y. Minagi), [email protected] (F. Uehara), [email protected] (S.E. Salazar), sayaka-ishihara@saneigenffi.co.jp (S. Ishihara), m-nakauma@saneigenffi.co.jp (M. Nakauma), tfunami@saneigenffi.co.jp (T. Funami), [email protected] (K. Ikebe), [email protected] (Y. Maeda), [email protected] (T. Ono). https://doi.org/10.1016/j.archoralbio.2019.104631 Received 12 September 2019; Received in revised form 16 November 2019; Accepted 3 December 2019 0003-9969/ © 2019 Elsevier Ltd. All rights reserved.
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also the “compensatory mastication” ability to squeeze the food with the tongue and palate (“tongue squeezing”) or with the gums (Ministry of Agriculture, Forestry & Fishes, 2019; The Dysphagia Diet Committee of the Japanese Society of Dysphagia Rehabilitation, 2013). Tongue squeezing is one of the methods to process and consume soft food such as gels and is thought to occur frequently when eating care food that tends to be soft (Ishihara et al., 2014). However, while there are numerous reports on food mastication with teeth, only a few studies have examined food processing with tongue squeezing. We previously focused on the tongue pressure, or the pressure that arises when the tongue squeezes food against the palate, which is the driving force that propels the food bolus while swallowing (Ono, Hori, & Nokubi, 2004), and we developed a 0.1-mm-thick sensor sheet which could measure the tongue pressure production at the five points on the hard palate without affecting the dynamics of swallowing (Hori et al., 2009). Using this sensor sheet, we quantitatively elucidated how different eating strategies affect tongue pressure (Yokoyama et al., 2014) and how the gel texture influences tongue pressure during tongue squeezing and swallowing (Hayashi et al., 2013; Hori et al., 2015; Yokoyama et al., 2014). Based on these findings, measuring tongue pressure could clarify tongue movement during food intake and swallowing from the aspect of contact between the tongue surface and palate. However, it is difficult to determine the changes in the movement of the tongue when it is not in contact with the palate with a tongue pressure sensor. Therefore, to more comprehensively evaluate tongue movement during tongue squeezing, simultaneous measurements with devices such as electromyography and videofluorography (VF) are necessary. Previous studies using electromyography showed suprahyoid muscle activity during the tongue squeezing of gels and during the elevation of the tongue to the palate (Ishihara et al., 2011), and that the suprahyoid muscle activity is modulated by gel texture (Ishihara et al., 2013). It has been reported that the hyoid bone is connected to the tongue via the suprahyoid muscle, forming the tongue platform (Dodds, Stewart, & Logemann, 1990) and moves in a coordinated manner with suprahyoid muscle activity during swallowing (Crary et al., 2006). In addition, tongue pressure production and hyoid movement were temporally coordinated during swallowing water (Hori et al., 2013). From these reports, it can be considered that tongue pressure is generated in a coordinated manner with hyoid movement and with suprahyoid muscle activity during tongue squeezing. However, it is still unclear how the suprahyoid muscles, which function during both of mouth opening and swallowing, are associated with tongue squeezing. Based on previous findings, we hypothesized that tongue pressure against hard palate and suprahyoid muscle activity reached to be the highest when hyoid bone was at the elevated position during initial squeezing. We also postulated that tongue pressure production, hyoid movement, and suprahyoid muscle activity during tongue squeezing are influenced by the texture of the food that is squeezed by the tongue. Therefore, the aim of the present study was to evaluate tongue pressure, hyoid movement, and suprahyoid muscle activity specifically during the initial tongue squeezing.
Fig. 1. Tongue Pressure Measuring System (Swallow scan system, Nitta, Japan). Overview of the swallow scan system (A). The sensor sheet with five measuring points is attached to the hard palate (B).
2.2. Measurement methods 2.2.1. Tongue pressure measurement (TP) Tongue pressure was measured using a T-shaped sensor sheet consisting of five measurement points (Swallow Scan System, Nitta, Osaka, Japan, Fig. 1A). Chs. 1–3 were placed at the palate median (1, anteriormedian position; 2, mid-median position; 3, posterior-median position), and Chs. 4 and 5 were placed at the left and right posterior-circumferential regions respectively(Fig. 1B). The production of tongue pressure was recorded at each channel over time, and the synchronization signal was input into the AD board (Power Lab ML880, AD Instruments, Bella Vista, Australia). The sampling rate was set at 100 Hz. To measure tongue pressure, the sensor sheet was affixed to the palate using sheet-form denture adhesive (Touch Correct II, Shionogi Co., Osaka, Japan). Subsequently, the sensor system was calibrated by applying a specific amount of negative pressure with a vacuum pump through the air hole created at the exit point of the tongue pressure sensor sheet.
2. Methods 2.1. Participants The study participants were 15 healthy adult men (mean age, 31.0 ± 4.1 years) without mastication and swallowing problems, neuromuscular disease, or a history of temporomandibular joint disease or orthodontic treatment, who understood the objectives of the experiment and gave informed consent to participate in the study. This study was approved by the Ethics Committee of Niigata University Faculty of Dentistry (28-R2-4-14) and conformed with the Declaration of Helsinki.
2.2.2. Videofluorography (VF) Hyoid movement (HM) was measured using a sagittal projection on videofluorography (ARCADIS Avantic Gen2, Siemens, Munich, Germany). Before recording, an 11-mm-diameter iron ball was fixed to the midline of the chin of the participant and used as a reference for actual length for the measurements. The obtained VF movie was processed at 30 frames/s and recorded on a computer through an AD board 2
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C10, and fracture strain was set at approximately 45 % for A10 and A30 and approximately 75 % for C10 and C30. In other words, samples were prepared such that A10 and C10 (A30 and C30) had a similar fracture force, and A10 and A30 (C10 and C30) had a similar fracture strain.
(Power Lab ML880, AD Instruments). The upper limit of radiation exposure from VF was 89.77 mSv per participant, and the upper limit of imaging time was 120 s. 2.2.3. Surface electromyography (sEMG) To the participants’ skin surface of the bilateral anterior bellies of the digastric muscles, 8-mm-diameter surface electrodes (NT-211 u, Nihon Kohden, Tokyo, Japan) were attached 20 mm apart, and the suprahyoid muscles activity during tongue squeezing was recorded. The ear lobe was used as a reference point. Subsequently, the obtained signals were filtered (low cut, 30 Hz and high cut, 1000 Hz) and amplified (AB611-J, Nihon Kohden). These signals were recorded onto a computer through an AD board (Power Lab ML880, AD Instruments). The sampling rate was set at 1000 Hz.
2.3. Data collection and analysis 2.3.1. Data collection Participants were asked to sit in an examination chair with reclining function, and the head was fixed by positioning a headrest in the occipital region such that the Frankfurt plane was parallel to the floor according to VF images. Measurements were performed in the sitting position. The participants first placed the 5 mL of cylindrical gel sample (20 mm diameter ×16 mm height) onto the mouth floor, and the participants were subsequently instructed to squeeze the gel sample in the mouth with the tongue, without masticating with their teeth after the que of the examiner, and to swallow when they deemed the gel to be swallowable. The measurements were made twice for each of the four types of gels, and the order was randomized.
2.2.4. Synchronizing system Tongue pressure, VF imaging, and EMG data during tongue squeezing were recorded simultaneously. To synchronize these data, synchronization signals from the Swallow scan system were recorded on another computer through an AD board (Power Lab ML880, AD Instruments). In the preliminary test, the temporal characteristics of the tongue pressure sensor, VF, and EMG measurements were analyzed, and the time was corrected when synchronizing the output signal.
2.3.2. Tongue pressure (TP) The first waveform of tongue pressure was specified as the initial tongue squeezing, and the maximum value, duration, and area of the waveform from tongue pressure production to disappearance were analyzed at each tongue pressure sensor measurement site (Chs. 1–5). Furthermore, the onset, peak, and offset timings of tongue pressure at each channel were analyzed at initial tongue squeezing.
2.2.5. Food sample Gel samples contained two types of gelling agents (KELCOGEL®, KELCOGEL® LT100; San-Ei Gen F.F.I., Inc., Osaka, Japan) as the primary component. KELCOGEL® consists of a “brittle” property of lowacylated gellan gum (Morris, 2006), and KELCOGEL® LT100 consists of a “deformable” property with loading of high-acylated gellan gum. By modulating the concentrations and proportions of these two gels, it is possible to change the properties of fracture force and fracture strain. the mechanical properties of four types of gels (A10, A30, C10, C30) (Table 1) corresponded to “easy-to-chew” for A30, “can be crushed with gums” for A10 and C30, and “can be crushed with tongue” for C10 (Ministry of Agriculture, Forestry & Fishes, 2019). Pre-mixture of each gellan gum, sucrose (granulated-type sugar) and food grade sucralose sweetener (SAN SWEET® SU-100, San-Ei Gen F.F.I., Inc.) were dissolved in de-ionized water containing iopamiron 370® (Bracco imaging, Milan, Italy) at 90℃ for 10 min with mechanical stirring, followed by the addition of calcium lactate as pentahydrate and food color (SAN GREEN® GC-EM, San-Ei Gen F.F.I., Inc.). The solutions obtained were heated further at 85℃ for 30 min in a container of 60 mm in dia. and 25 mm in height, followed by curing at 8℃ for 2 h to form gels. Gels were refrigerated at 5℃ before use. SAN SWEET® SU-100, whose sweetness is equivalent of 100 times of sucrose, was added to mask the bitter taste of iopamiron. For evaluations of the initial mechanical properties of the gel samples, a texture analyzer (TA XT-plus, Stable Micro System, Surrey, UK) was used. Samples (20 mm diameter ×10 mm height) were compressed with a 50-mm-diameter aluminum probe at a speed of 10 mm/s, and the fracture force was set at 30 N for A30 and C30 and 10 N for A10 and
2.3.3. Hyoid movement (HM) Motion capture software (Dipp Motion Pro ver. 2.24d, Ditect, Tokyo, Japan) was used for VF image analysis. Based on a method described by Logemann et al. (Logemann et al., 2000), the anteriorinferior corner of the fourth cervical vertebra was set as the origin, and the line connecting the anterior-inferior corners of the second and fourth cervical vertebrae was set as the Y-axis. The line that passed through the origin and perpendicular to the Y-axis was set as the X-axis. The anterior-inferior corner of the hyoid bone was the measurement point of the hyoid bone, and the trajectory of the hyoid bone was analyzed from start to end of hyoid bone movement during initial tongue squeezing (Fig. 2). The start of hyoid bone movement during initial tongue squeezing were defined as the time when the hyoid moving distance exceeded 1 mm/frame after the que of the examiner. The time when the Y-coordinate reached a minimum between the first and the second waveform was designated as the end of hyoid movement. The hyoid moving distance and duration in the analysis interval were analyzed. The sequential order of the onset of hyoid movement, the onset and offset of the phase in which the hyoid bone was elevated, and the offset of hyoid movement were analyzed. The hyoid bone positions at the onset of it's movement, highest position (i.e., peak), and the offset of it's movement were also analyzed. The hyoid bone position at the start of measurement before the que of the examiner was used as a reference.
Table 1 Formulation and mechanical characteristics of gels. Gel
A10 A30 C10 C30
Concentration of gellan gum (% w/w)
Mechanical property
Texture characteristics
Low acylated
High acylated
Fracture force
Fracture strain
0.25 0.65 0.06 0.15
0 0 0.14 0.35
9.71 ± 0.13 28.7 ± 1.00 9.73 ± 0.94 29.4 ± 0.99
43.3 ± 0.34 46.2 ± 1.08 74.3 ± 1.67 78.7 ± 1.19
Soft - Brittle Hard - Brittle Soft - Deformable Hard - Deformable
Mechanical characteristics of agar gels were measured using a TA XT plus texture analyzer (Stable Micro Systems, Surrey, UK). Fracture force and strain were determined by compressing these gels on a metal stage using an aluminum plate of 50 mm in diameter at a crosshead speed of 10 mm/s at 20 °C. The gel size was 20 mm in diameter and 10 mm in height. 3
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Fig. 2. Reference plane and points of VF image. The anterior-inferior corner of the 4th cervical vertebra (C4) is defined as the origin. The C2-C4 axis is defined as the Y-axis. The anterior-inferior margin of the hyoid bone is defined as the reference point of hyoid movement. VF images were recorded at 30 frames per second.
synchronization. Using the onset time of hyoid movement during initial tongue squeezing as a reference, time points of tongue pressure, hyoid movement, and suprahyoid muscle activity were compared on a time series graph. Tongue pressure amplitude and duration were compared among channels. The changes in hyoid bone position were separated into anteroposterior and vertical components and compared among onset, peak, and offset. The maximum amplitude, duration, and area of tongue pressure, distance and duration of hyoid movement, and maximum amplitude, duration, and area of EMG at each channel were compared among the gel samples. For each evaluation item, the mean of two attempts was used as the representative value. Shapiro-Wilk test was applied to check normality of each evaluation item. Friedman’s test was used for comparisons among time points, channels, and gel samples during initial tongue squeezing, and the Wilcoxon signed-rank test with Bonferroni correction was used for post hoc analysis when Friedman’s test was significant. P < 0.05 was considered significant. SPSS Statistics software ver. 25 (IBM Japan, Tokyo, Japan) was used for analysis.
2.3.4. Suprahyoid muscle activity First, rectification and smoothing of the original waveform were performed. Using the mean ± 2 standard deviations of the amplitude during the first 3 s of measurement as a reference, the timing when the electromyography value exceeded the reference was specified as the onset of suprahyoid muscle activity for initial tongue squeezing. Then, between the peaks of the first and second waveforms, the timing when the amplitude reached a minimum was designated as the offset of initial tongue squeezing. The maximum amplitude, duration, area, and the timing of onset, peak, and offset of muscle activity were analyzed between the onset and offset of suprahyoid muscle activity. The mean of left and right values was used as the representative value for the maximum, duration, and area of muscle activity. 2.3.5. Data analysis Fig. 3 shows an example waveform of tongue pressure, hyoid movement, and suprahyoid muscle activity from the start of squeezing to the end of swallowing the gel after correcting the time for
3. Results 3.1. Coordination of TP, HM, and EMG during initial squeezing Fig. 4 shows the time coordination of tongue pressure, hyoid movement, and suprahyoid muscle activity during initial tongue squeezing for A30. At the start of tongue squeezing, there were not significant differences among the onset of tongue pressure at the midmedian position of the palate (Ch. 2), hyoid movement, and suprahyoid muscle activity. The onset of tongue pressure at the anterior-median position of the palate (Ch. 1) appeared, followed by the posterior palate (Chs. 3–5). Subsequently, at the phase when the hyoid bone was elevated, the suprahyoid muscle activity reached a maximum, and the tongue pressure at all channels (Chs. 1–5) reached a maximum. The offset of tongue pressure and suprahyoid muscle activity was followed by the offset of hyoid movement, and the initial tongue squeezing was concluded. Results for A10, C10, and C30 are shown in the Appendix and are similar to those of A30 (Figures S1, S2, and S3).
Fig. 3. Sample waveform of tongue pressure, hyoid position, and suprahyoid muscle activity during squeezing and swallowing gels. 4
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Fig. 4. Time sequences of tongue pressure, hyoid movement, and suprahyoid muscle activity during initial squeezing (A30). ●Onset time of tongue pressure ▲Peak time of tongue pressure ×Offset time of tongue pressure. ◼Onset time of hyoid movement ◆Onset time of the phase when the hyoid is the elevated position◇ Offset time of the phase when the hyoid is the elevated position □Offset time of hyoid movement ○ Onset time of EMG △ Peak time of EMG ＊Offset time of EMG. Time “0” was set at the onset of hyoid movement. *p < 0.05 (Friedman test with post hoc test). SHy: Suprahyoid muscles.
smaller fracture strain (A10 < C10, A30 < C30) resulted in a significantly greater tongue pressure amplitude at Chs. 1–3. Tongue pressure duration were longer at all channels with greater fracture force of the gel, but it was not significant (Fig. 6B). Tongue pressure area, similarly to tongue pressure amplitude, became greater at all channels with greater fracture force and smaller fracture strain (Fig. 6C). Comparisons of tongue pressure amplitude between each channel for each gel showed that gels with a small fracture strain (A10, A30) had greater amplitude at Ch. 2 than at the posterior Chs. 3–5, though gels with a large fracture strain (C10, C30) did not have different amplitudes between channels (Fig. 7A). On the other hand, tongue pressure duration was greater at Ch. 2 than at posterior Chs. 3–5 for all gels (Fig. 7B), and tongue pressure area was greater at Ch. 2 than at other channels (Fig. 7C). For suprahyoid muscle activity, gels with a large fracture force (A30) had greater maximum amplitude significantly, compared to gels with a small fracture force (A10, C10). Gels with a large fracture force also had greater muscle activity duration and area, and there was a significant difference between A30 and A10 (Fig. 8). For hyoid movement, gels with a large fracture force (A30, C30), compared to gels with a small fracture force (A10, C10), had a significantly greater hyoid moving distance (Fig. 9A) In addition, gels with a large fracture force had a longer hyoid moving duration than those with a small fracture force, and there were significant differences between C30 and A10 and C10. (Fig. 9B).
3.2. Position of the hyoid bone during initial squeezing During the initial tongue squeezing, there was a phase in which the hyoid bone was stationary at an elevated position. Although the anteroposterior position of the hyoid bone did not show a specific trend at onset, peak, and offset of initial tongue squeezing (Fig. 5A), the vertical position was significantly higher at peak or offset than at onset (Fig. 5B). The hyoid bone position was significantly lower at offset than at peak. These results were observed for all sample types. 3.3. Differences in TP, HM, and EMG during initial squeezing due to the mechanical properties of gels Tongue pressure, hyoid movement, and suprahyoid muscle activity during initial tongue squeezing differed depending on mechanical properties of the gels. Gels with a greater fracture force (A10 < A30, C10 < C30) resulted in a significantly greater tongue pressure amplitude at all channels (Fig. 6A). For gels with the same fracture force, a
4. Discussion In the present study, we have successfully described the sequential coordination of tongue pressure production, suprahyoid muscle activity, and hyoid movement as well as their spatial and mechanical modulation according to texture of gels during initial tongue squeezing. To the best of our knowledge, this is the first report that provides the biomechanical features of tongue squeezing as a strategy of food oral processing. Since this study used radiation for VF, there are temporal limitations in the number of experimental tasks. The experimental tasks required the participants to freely squeeze the test sample with their tongue without masticating with their teeth and to subsequently swallow at their own timing, such that the process was as natural as possible. Based on the time required for one task determined in the preliminary experiment, four types of gels with two trials each were used. Although it is necessary to change the fracture force and fracture strain by at least three levels to evaluate the changes in tongue squeezing by different food textures, this was not possible in the present study due to limitations of radiation exposure. The number of the participants was fifteen in this study, which might be the small sample size. However, the design of this study was not an interventional study
Fig. 5. Comparison of hyoid position at the onset, peak, and offset of initial squeezing. 5
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Fig. 6. Comparisons among four gels in maximum amplitude (A), duration (B), and area (C) of tongue pressure at each measuring point during initial squeezing. The maximum amplitude and area of tongue pressure at each measuring point tend to increase with fracture force, while the maximum amplitude and area tend to decrease with fracture strain. *p < 0.05 (Friedman test with post hoc test).
4.1. Coordination of TP, HM, and EMG during initial squeezing
but an exploratory and observational study with several outcomes (tongue pressure, hyoid movement and suprahyoid muscle activity). In addition, considering the risk of radiation exposure to the examiners, it is quite difficult to collect a large number of participants. For these reasons, we set the sample size in this study to fifteen like as our previous studies (Hori et al., 2013, 2015; Taniguchi, Tsukada, Ootaki, Yamada, & Inoue, 2008).
The results of the present study demonstrated that tongue pressure at the mid-median palate, suprahyoid muscle activity, and hyoid movement occurred simultaneously at the start of tongue squeezing. Previous studies showed that the onset of tongue pressure during liquid swallowing appeared after the onset of suprahyoid muscle activity (Taniguchi et al., 2008). Hori et al. reported that, during initial tongue squeezing, tongue pressure first appeared at the mid-median position of the palate (Ch. 2) where it is most affected by gel hardness, and that the Fig. 7. Comparisons among the five measuring points of the pressure sensor of maximum amplitude (A), duration (B), and area (C) of tongue pressure during initial squeezing of four gels. The maximum amplitude, duration and area of tongue pressure at Ch.2 (mid-median area of hard palate) tend to be higher than at the other channels. *p < 0.05 (Friedman test with post hoc test).
6
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Fig. 8. Comparisons among the four gels in maximum amplitude (A), duration (B), and area (C) of suprahyoid muscle activity during initial squeezing.
Furthermore, because the hyoid bone position was higher at the end than at the start of initial tongue squeezing, we believe that the whole tongue maintains a moderately elevated position to prepare for the subsequent tongue squeezing rather than returning to its original position for every tongue squeezing.
contact between the tongue at Ch. 2 and the palate played an important role in the recognition of food texture (Hori et al., 2015); similar results were observed in the present study. Furthermore, because the onset of tongue pressure at the mid-median palate appears around the same time as the onset of suprahyoid muscle activity and hyoid movement, it is postulated that, at the start of tongue squeezing, the suprahyoid muscle activity begins in order to squeeze the food against the midmedian palate, and the hyoid bone is elevated upward. During the initial tongue squeezing, there was a phase when the hyoid bone was virtually stationary in an elevated position. During this phase, the peak of tongue pressure and the peak of suprahyoid muscles appeared at all channels. In other words, the timing of maximum contact pressure at the palate and the timing of maximum suprahyoid muscle activity were during a phase in which the hyoid bone was in an elevated position. Since it has been previously reported that the hyoid bone is connected to the tongue via the hyoglossus muscle, forming the tongue platform (Dodds et al., 1990), tongue squeezing occurs not only with the morphological change of the tongue, but it is also affected by the hyoid movement and suprahyoid muscle activity with the whole tongue elevated upward.
4.2. Differences in TP, HM, and EMG during initial squeezing caused by the mechanical properties of gels In this study, we controlled fracture strain and fracture force which was measured by full compression of gels, though hardness of gels which was measured by partial compression was controlled in the previous studies (Hayashi et al., 2013; Hori et al., 2015; Yokoyama et al., 2014). Fracture force and strain are evaluated as the characteristics of deformation and fracture by compressing foods between a flat aluminum plate and stage. These parameters have been considered to be more reasonable than hardness to explain the breaking behavior of semi-solid food between tongue and hard palate (Ishihara et al., 2013, 2014), which was the reason why we employed them. During tongue squeezing, all parameters of tongue pressure, hyoid
Fig. 9. Comparisons among the four gels in moving distance (A) and duration (B) of hyoid movement during initial squeezing. 7
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2008), and that the hyoid bone position droops in older individuals compared to younger individuals (Feng et al., 2014). For these reasons, we also have to compare tongue squeezing between healthy young people, older people and those with mastication and swallowing problems in the future.
movement, and suprahyoid muscle activity became greater with gels with large fracture force (A30, C30) than with gels with small fracture force (A10, C10). Fracture force is the strength required to fracture food and is one of the mechanical properties in food engineering. We previously reported that the tongue pressure amplitude, duration, and number of tongue squeezing increase with greater gel hardness (Hori et al., 2015; Yokoyama et al., 2014). The present study also showed that tongue pressure amplitude and area during initial tongue squeezing were significantly greater with gels with a larger fracture force. Moreover, a larger fracture force increased the tongue pressure duration at initial tongue squeezing. In other words, when the fracture force of the gel increases, the pressure applied to the palate is large and continues for a long duration. These are similar to the results from our previous study involving adjusted hardness (Hori et al., 2015). Suprahyoid muscle activity had an increased maximum amplitude, muscle activity duration, and area with greater gel fracture force. Ishihara et al. previously reported that the muscle activity of the suprahyoid muscles increases with increasing fracture force of gels during oral processing (Ishihara et al., 2013), consistent with the results of the present study. Furthermore, because hyoid moving distance and duration increased with greater fracture force, it is likely that a greater fracture force of the gel increases the movement of the whole tongue. Summarizing these findings, when the fracture force of the gel increases, the contact pressure against the palate and the amplitude and duration of suprahyoid muscle activity increase, resulting in an increase in the movement of the whole tongue. Fracture strain is the strain of the food when food is crushed, and a larger value indicates a more deformable property. In gels with the same fracture force, a smaller fracture strain resulted in increased tongue pressure amplitude and area at Chs. 1–3; however, tongue pressure duration and other items related to hyoid movement and suprahyoid muscle activity were not significantly different. In addition, comparing the tongue pressure amplitudes between channels for each gel, the tongue pressure amplitude at the mid-median palate became higher than at the other channels during squeezing of brittle gels with a small fracture strain (A10, A30), and deformable gels with a large fracture strain (C10, C30) did not show significant differences in tongue pressure amplitude among channels. The reason for this may be that the gel shape during tongue squeezing differs depending on the fracture strain. When the fracture strain is small, the gel has less deformation until the gel is crushed, and tongue pressure can be focused specifically to the gel location during tongue squeezing; however, when the fracture strain is large, the tongue pressure per unit area is dispersed because the gel spreads. Summarizing these findings, when the fracture strain increases, the contact pressure to the palate decreases, changing the tongue pressure amplitude pattern.
5. Conclusion Time coordination of tongue pressure production, hyoid movement, and suprahyoid muscle activity was observed during initial tongue squeezing. Furthermore, tongue pressure, hyoid movement, and suprahyoid muscle activity during initial tongue squeezing appeared to change depending on the properties of the food to be processed. Moreover, the hyoid bone did not return to its original position at the end of initial tongue squeezing, but rather maintained an elevated position, which was suggestive of preparation for the next tongue squeezing. Author contributions Study design: K. Hori, K. Murakami. Data collection: K. Murakami, K. Hori, Y. Minagi, F. Uehara, S.E. Salazar. Data analysis: K. Murakami, Y. Minagi. Manuscript writing: K. Murakami, K. Hori. Manuscript editing: Y. Maeda, T. Ono, K. Ikebe. Sample supply: T. Funami, M. Nakauma, S. Ishihara. Funding This work was supported by JSPS KAKENHI Grant Number JP18K17116. Declaration of Competing Interest There are no conflict of interests in connection with this article. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.archoralbio.2019. 104631. References Crary, M. A., Carnaby-Mann, G. D., & Groher, M. E. (2006). Biomechanical correlates of surface electromyography signals obtained during swallowing by healthy adults. Journal of Speech, Language, and Hearing Research, 49, 186–193. Dodds, W. J., Stewart, E. T., & Logemann, J. A. (1990). Physiology and radiology of the normal oral and pharyngeal phases of swallowing. American Journal of Roentgenology, 154, 953–963. Feng, X., Todd, T., Lintzenich, C. R., Ding, J., Carr, J. J., Ge, Y., et al. (2013). Agingrelated geniohyoid muscle atrophy is related to aspiration status in healthy older adults. The Journal of Gerontology Series A: Biological Sciences and Medical Sciences, 68, 853–860. Feng, X., Todd, T., Hu, Y., Lintzenich, C. R., Carr, J. J., Browne, J. D., et al. (2014). Agerelated changes of hyoid bone position in healthy older adults with aspiration. Laryngoscope, 124, E231–236. Hayashi, H., Hori, K., Taniguchi, H., Nakamura, Y., Tsujimura, T., Ono, T., et al. (2013). Biomechanics of human tongue movement during bolus compression and swallowing. Journal of Oral Science, 55, 191–198. Hori, K., Ono, T., Tamine, K., Kondoh, J., Hamanaka, S., Maeda, Y., et al. (2009). A newly developed sensor sheet for measuring tongue pressure in swallowing. Journal of Prosthodontic Research, 53, 28–32. Hori, K., Taniguchi, H., Hayashi, H., Magara, J., Minagi, Y., Li, Q., et al. (2013). Role of tongue pressure production in oropharyngeal swallow biomechanics. Physiological Reports, 1, e00167. Hori, K., Hayashi, H., Yokoyama, S., Ono, T., Ishihara, S., Magara, J., et al. (2015). Comparison of mechanical analysis and tongue pressure analyses during squeezing and swallowing of gel agents. Food Hydrocolloids, 44, 145–155. Ikebe, K., Matsuda, K., Kagawa, R., Enoki, K., Okada, T., Yoshida, M., et al. (2012). Masticatory performance in older subjects with varying degrees of tooth loss. Journal
4.3. Clinical implications The present findings are the foundation of kinematics of tongue squeezing, which is a compensatory mastication process. They indicate that suprahyoid muscle plays a role of elevation of whole tongue in tongue squeezing in addition to mouth opening and swallowing. It is known that suprahyoid muscle is decreased by aging and dysphagia (Feng et al., 2013). Therefore, these findings may become important information for establishing criteria for selecting the food form for the elderly population declined masticatory and /or swallowing function. However, tongue function during tongue squeezing is not only to process soft food against hard palate, but also to accumulate and transport food bolus into pharynx. In the future, we have to evaluate the entire tongue squeezing process and swallowing, rather than just the initial tongue squeezing, to determine the relationship between tongue squeezing and the subsequent swallowing. As for the age related decline in tongue and hyolaryngeal motor function, It has been reported that tongue pressure at maximum tongue squeezing decreases with age or existing diseases (Utanohara et al., 8
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requestSender=estat. Morris, V. J. (2006). Bacterial polysaccharide. Food polysaccharides and their applications. London: Taylor & Francis. Ono, T., Hori, K., & Nokubi, T. (2004). Pattern of tongue pressure on hard palate during swallowing. Dysphagia, 19, 259–264. Taniguchi, H., Tsukada, T., Ootaki, S., Yamada, Y., & Inoue, M. (2008). Correspondence between food consistency and suprahyoid muscle activity, tongue pressure, and bolus transit times during the oropharyngeal phase of swallowing. Journal of Applied Physiology, 105, 791–799. Teramoto, S., Fukuchi, Y., Sasaki, H., Sato, K., Sekizawa, K., & Matsuse, T. (2008). High incidence of aspiration pneumonia in community- and hospital-acquired pneumonia in hospitalized patients: A multicenter, prospective study in Japan. Journal of the American Geriatrics Society, 56, 577–579. The Dysphagia Diet Committee of the Japanese Society of Dysphagia Rehabilitation (2013). The Japanese Dysphagia diet 2013. The Japanese Journal of Dysphagia Rehabilitation, 17, 255–267. Utanohara, Y., Hayashi, R., Yoshikawa, M., Yoshida, M., Tsuga, K., & Akagawa, Y. (2008). Standard values of maximum tongue pressure taken using newly developed disposable tongue pressure measurement device. Dysphagia, 23, 286–290. Yokoyama, S., Hori, K., Tamine, K., Fujiwara, S., Inoue, M., Maeda, Y., et al. (2014). Tongue pressure modulation for initial gel consistency in a different oral strategy. PLoS One, 9, e91920.
of Dentistry, 40, 71–76. Ishihara, S., Nakauma, M., Funami, T., Tanaka, T., Nishinari, K., & Kohyama, K. (2011). Electromyography during oral processing in relation to mechanical and sensory properties of soft gels. Journal of Texture Studies, 42, 254–267. Ishihara, S., Nakao, S., Nakauma, M., Funami, T., Hori, K., Ono, T., et al. (2013). Compression test of food gels on artificial tongue and its comparison with human test. Journal of Texture Studies, 44, 104–114. Ishihara, S., Isono, M., Nakao, S., Nakauma, M., Funami, T., Hori, K., et al. (2014). Instrumental uniaxial compression test of gellan gels of various mechanical properties using artificial tongue and its comparison with human oral strategy for the first size reduction. Journal of Texture Studies, 45, 354–366. Logemann, J. A., Pauloski, B. R., Rademaker, A. W., Colangelo, L. A., Kahrilas, P. J., & Smith, C. H. (2000). Temporal and biomechanical characteristics of oropharyngeal swallow in younger and older men. Journal of Speech Language and Hearing Research, 43, 1264–1274. Matsuyama, Y., Aida, J., Watt, R. G., Tsuboya, T., Koyama, S., Sato, Y., et al. (2017). Dental status and compression of life expectancy with disability. Journal of Dental Research, 96, 1006–1013. Ministry of Agriculture, Forestry and Fishes (2019). Effort relating to “smile care food” – Introduction of new mark system. http://www.maff.go.jp/e/policies/food_ind/attach/ pdf/index-9.pdf. Ministry of Health, Labour and Welfare (2015). Vital statistics. https://www.e-stat.go.jp/ SG1/estat/GL08020103.do?_toGL08020103_&listID=000001158057&disp=Other&
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Coordination of tongue pressure production, hyoid movement, and suprahyoid muscle activity during squeezing of gels
T
Kazuhiro Murakamia, Kazuhiro Horib,*, Yoshitomo Minagia, Fumiko Ueharab, Simonne E. Salazarb, Sayaka Ishiharac, Makoto Nakaumac, Takahiro Funamic, Kazunori Ikebea, Yoshinobu Maedaa, Takahiro Onob a
Department of Prosthodontics, Gerodontology and Oral Rehabilitation, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka, 565-0871, Japan Division of Comprehensive Prosthodontics, Niigata University Graduate School of Medical and Dental Sciences, 2-5274 Gakkocho-dori, Niigata, Niigata, 951-8514, Japan c San-Ei Gen F. F. I., Inc., 1-1-11 Sanwa-cho, Toyonaka, Osaka, 561-8588, Japan b
A R T I C LE I N FO
A B S T R A C T
Keywords: Squeezing Gels Tongue movement Tongue pressure Hyoid movement Electromyography
Objective: The aim of this study was to evaluate tongue movement and its biomechanical effects during squeezing, one of the oral strategies for processing soft foods, by tongue pressure sensors, videofluorography, and surface electromyography. Design: Fifteen healthy men (mean age, 31.0 ± 4.1 years) without dysphagia were recruited. A 0.1-mm-thick pressure sensor sheet with five measuring points, videofluorography, and surface electromyography were used for synchronous measurements of tongue pressure, hyoid movement, and suprahyoid muscles activity, respectively, while squeezing 5 mL of gels. Amplitude, duration, area, and their sequential order during initial squeezing were analyzed. Differences in hyoid position at the onset, peak, and offset of hyoid movement were also analyzed. Results: At the beginning of initial squeezing, tongue pressure at the middle area of the hard palate, hyoid movement, and suprahyoid muscle activity appeared simultaneously, followed by tongue pressure at the anterior area and then at the posterior area. When the hyoid was in an elevated position, the amplitude of suprahyoid muscle activity and tongue pressure peaked. At the end of initial squeezing, the hyoid position at the offset of hyoid excursion was superior to that at the onset. All evaluation items of tongue pressure, hyoid movement, and suprahyoid muscle activity were modulated according to the texture of gels. Conclusions: During initial squeezing, tongue pressure, hyoid movement, and suprahyoid muscle activity were coordinated while being modulated by the food texture. At the end of initial squeezing, the hyoid was maintained in an elevated position, which might be beneficial for subsequent squeezing.
1. Introduction As the aging population increases, the proportion of older individuals with mastication and swallowing problems has been increasing, resulting in eating-related aspiration and choking problems (Ministry of Health, Labour & Welfare, 2015; Teramoto et al., 2008). Since aspiration and choking are life-threatening and decrease quality of life, ensuring safety during meals is extremely important in older people. Adjusting the food form is one of the ways to prevent these
problems during meals, and various care foods have been developed to facilitate safe eating without aspiration and choking in older people. Older individuals commonly have decreased masticatory ability due to a reduction in remaining teeth (Ikebe et al., 2012). To improve their masticatory ability, dentists perform prosthetic treatment with dentures; actually, however, many older individuals do not wear dentures even if they require them due to poor dentition (Matsuyama et al., 2017). Thus, when selecting care food for older people, it is necessary to consider not only the masticatory ability of the teeth and dentures, but
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Corresponding author. E-mail addresses: [email protected] (K. Murakami), [email protected] (K. Hori), [email protected] (Y. Minagi), [email protected] (F. Uehara), [email protected] (S.E. Salazar), sayaka-ishihara@saneigenffi.co.jp (S. Ishihara), m-nakauma@saneigenffi.co.jp (M. Nakauma), tfunami@saneigenffi.co.jp (T. Funami), [email protected] (K. Ikebe), [email protected] (Y. Maeda), [email protected] (T. Ono). https://doi.org/10.1016/j.archoralbio.2019.104631 Received 12 September 2019; Received in revised form 16 November 2019; Accepted 3 December 2019 0003-9969/ © 2019 Elsevier Ltd. All rights reserved.
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also the “compensatory mastication” ability to squeeze the food with the tongue and palate (“tongue squeezing”) or with the gums (Ministry of Agriculture, Forestry & Fishes, 2019; The Dysphagia Diet Committee of the Japanese Society of Dysphagia Rehabilitation, 2013). Tongue squeezing is one of the methods to process and consume soft food such as gels and is thought to occur frequently when eating care food that tends to be soft (Ishihara et al., 2014). However, while there are numerous reports on food mastication with teeth, only a few studies have examined food processing with tongue squeezing. We previously focused on the tongue pressure, or the pressure that arises when the tongue squeezes food against the palate, which is the driving force that propels the food bolus while swallowing (Ono, Hori, & Nokubi, 2004), and we developed a 0.1-mm-thick sensor sheet which could measure the tongue pressure production at the five points on the hard palate without affecting the dynamics of swallowing (Hori et al., 2009). Using this sensor sheet, we quantitatively elucidated how different eating strategies affect tongue pressure (Yokoyama et al., 2014) and how the gel texture influences tongue pressure during tongue squeezing and swallowing (Hayashi et al., 2013; Hori et al., 2015; Yokoyama et al., 2014). Based on these findings, measuring tongue pressure could clarify tongue movement during food intake and swallowing from the aspect of contact between the tongue surface and palate. However, it is difficult to determine the changes in the movement of the tongue when it is not in contact with the palate with a tongue pressure sensor. Therefore, to more comprehensively evaluate tongue movement during tongue squeezing, simultaneous measurements with devices such as electromyography and videofluorography (VF) are necessary. Previous studies using electromyography showed suprahyoid muscle activity during the tongue squeezing of gels and during the elevation of the tongue to the palate (Ishihara et al., 2011), and that the suprahyoid muscle activity is modulated by gel texture (Ishihara et al., 2013). It has been reported that the hyoid bone is connected to the tongue via the suprahyoid muscle, forming the tongue platform (Dodds, Stewart, & Logemann, 1990) and moves in a coordinated manner with suprahyoid muscle activity during swallowing (Crary et al., 2006). In addition, tongue pressure production and hyoid movement were temporally coordinated during swallowing water (Hori et al., 2013). From these reports, it can be considered that tongue pressure is generated in a coordinated manner with hyoid movement and with suprahyoid muscle activity during tongue squeezing. However, it is still unclear how the suprahyoid muscles, which function during both of mouth opening and swallowing, are associated with tongue squeezing. Based on previous findings, we hypothesized that tongue pressure against hard palate and suprahyoid muscle activity reached to be the highest when hyoid bone was at the elevated position during initial squeezing. We also postulated that tongue pressure production, hyoid movement, and suprahyoid muscle activity during tongue squeezing are influenced by the texture of the food that is squeezed by the tongue. Therefore, the aim of the present study was to evaluate tongue pressure, hyoid movement, and suprahyoid muscle activity specifically during the initial tongue squeezing.
Fig. 1. Tongue Pressure Measuring System (Swallow scan system, Nitta, Japan). Overview of the swallow scan system (A). The sensor sheet with five measuring points is attached to the hard palate (B).
2.2. Measurement methods 2.2.1. Tongue pressure measurement (TP) Tongue pressure was measured using a T-shaped sensor sheet consisting of five measurement points (Swallow Scan System, Nitta, Osaka, Japan, Fig. 1A). Chs. 1–3 were placed at the palate median (1, anteriormedian position; 2, mid-median position; 3, posterior-median position), and Chs. 4 and 5 were placed at the left and right posterior-circumferential regions respectively(Fig. 1B). The production of tongue pressure was recorded at each channel over time, and the synchronization signal was input into the AD board (Power Lab ML880, AD Instruments, Bella Vista, Australia). The sampling rate was set at 100 Hz. To measure tongue pressure, the sensor sheet was affixed to the palate using sheet-form denture adhesive (Touch Correct II, Shionogi Co., Osaka, Japan). Subsequently, the sensor system was calibrated by applying a specific amount of negative pressure with a vacuum pump through the air hole created at the exit point of the tongue pressure sensor sheet.
2. Methods 2.1. Participants The study participants were 15 healthy adult men (mean age, 31.0 ± 4.1 years) without mastication and swallowing problems, neuromuscular disease, or a history of temporomandibular joint disease or orthodontic treatment, who understood the objectives of the experiment and gave informed consent to participate in the study. This study was approved by the Ethics Committee of Niigata University Faculty of Dentistry (28-R2-4-14) and conformed with the Declaration of Helsinki.
2.2.2. Videofluorography (VF) Hyoid movement (HM) was measured using a sagittal projection on videofluorography (ARCADIS Avantic Gen2, Siemens, Munich, Germany). Before recording, an 11-mm-diameter iron ball was fixed to the midline of the chin of the participant and used as a reference for actual length for the measurements. The obtained VF movie was processed at 30 frames/s and recorded on a computer through an AD board 2
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C10, and fracture strain was set at approximately 45 % for A10 and A30 and approximately 75 % for C10 and C30. In other words, samples were prepared such that A10 and C10 (A30 and C30) had a similar fracture force, and A10 and A30 (C10 and C30) had a similar fracture strain.
(Power Lab ML880, AD Instruments). The upper limit of radiation exposure from VF was 89.77 mSv per participant, and the upper limit of imaging time was 120 s. 2.2.3. Surface electromyography (sEMG) To the participants’ skin surface of the bilateral anterior bellies of the digastric muscles, 8-mm-diameter surface electrodes (NT-211 u, Nihon Kohden, Tokyo, Japan) were attached 20 mm apart, and the suprahyoid muscles activity during tongue squeezing was recorded. The ear lobe was used as a reference point. Subsequently, the obtained signals were filtered (low cut, 30 Hz and high cut, 1000 Hz) and amplified (AB611-J, Nihon Kohden). These signals were recorded onto a computer through an AD board (Power Lab ML880, AD Instruments). The sampling rate was set at 1000 Hz.
2.3. Data collection and analysis 2.3.1. Data collection Participants were asked to sit in an examination chair with reclining function, and the head was fixed by positioning a headrest in the occipital region such that the Frankfurt plane was parallel to the floor according to VF images. Measurements were performed in the sitting position. The participants first placed the 5 mL of cylindrical gel sample (20 mm diameter ×16 mm height) onto the mouth floor, and the participants were subsequently instructed to squeeze the gel sample in the mouth with the tongue, without masticating with their teeth after the que of the examiner, and to swallow when they deemed the gel to be swallowable. The measurements were made twice for each of the four types of gels, and the order was randomized.
2.2.4. Synchronizing system Tongue pressure, VF imaging, and EMG data during tongue squeezing were recorded simultaneously. To synchronize these data, synchronization signals from the Swallow scan system were recorded on another computer through an AD board (Power Lab ML880, AD Instruments). In the preliminary test, the temporal characteristics of the tongue pressure sensor, VF, and EMG measurements were analyzed, and the time was corrected when synchronizing the output signal.
2.3.2. Tongue pressure (TP) The first waveform of tongue pressure was specified as the initial tongue squeezing, and the maximum value, duration, and area of the waveform from tongue pressure production to disappearance were analyzed at each tongue pressure sensor measurement site (Chs. 1–5). Furthermore, the onset, peak, and offset timings of tongue pressure at each channel were analyzed at initial tongue squeezing.
2.2.5. Food sample Gel samples contained two types of gelling agents (KELCOGEL®, KELCOGEL® LT100; San-Ei Gen F.F.I., Inc., Osaka, Japan) as the primary component. KELCOGEL® consists of a “brittle” property of lowacylated gellan gum (Morris, 2006), and KELCOGEL® LT100 consists of a “deformable” property with loading of high-acylated gellan gum. By modulating the concentrations and proportions of these two gels, it is possible to change the properties of fracture force and fracture strain. the mechanical properties of four types of gels (A10, A30, C10, C30) (Table 1) corresponded to “easy-to-chew” for A30, “can be crushed with gums” for A10 and C30, and “can be crushed with tongue” for C10 (Ministry of Agriculture, Forestry & Fishes, 2019). Pre-mixture of each gellan gum, sucrose (granulated-type sugar) and food grade sucralose sweetener (SAN SWEET® SU-100, San-Ei Gen F.F.I., Inc.) were dissolved in de-ionized water containing iopamiron 370® (Bracco imaging, Milan, Italy) at 90℃ for 10 min with mechanical stirring, followed by the addition of calcium lactate as pentahydrate and food color (SAN GREEN® GC-EM, San-Ei Gen F.F.I., Inc.). The solutions obtained were heated further at 85℃ for 30 min in a container of 60 mm in dia. and 25 mm in height, followed by curing at 8℃ for 2 h to form gels. Gels were refrigerated at 5℃ before use. SAN SWEET® SU-100, whose sweetness is equivalent of 100 times of sucrose, was added to mask the bitter taste of iopamiron. For evaluations of the initial mechanical properties of the gel samples, a texture analyzer (TA XT-plus, Stable Micro System, Surrey, UK) was used. Samples (20 mm diameter ×10 mm height) were compressed with a 50-mm-diameter aluminum probe at a speed of 10 mm/s, and the fracture force was set at 30 N for A30 and C30 and 10 N for A10 and
2.3.3. Hyoid movement (HM) Motion capture software (Dipp Motion Pro ver. 2.24d, Ditect, Tokyo, Japan) was used for VF image analysis. Based on a method described by Logemann et al. (Logemann et al., 2000), the anteriorinferior corner of the fourth cervical vertebra was set as the origin, and the line connecting the anterior-inferior corners of the second and fourth cervical vertebrae was set as the Y-axis. The line that passed through the origin and perpendicular to the Y-axis was set as the X-axis. The anterior-inferior corner of the hyoid bone was the measurement point of the hyoid bone, and the trajectory of the hyoid bone was analyzed from start to end of hyoid bone movement during initial tongue squeezing (Fig. 2). The start of hyoid bone movement during initial tongue squeezing were defined as the time when the hyoid moving distance exceeded 1 mm/frame after the que of the examiner. The time when the Y-coordinate reached a minimum between the first and the second waveform was designated as the end of hyoid movement. The hyoid moving distance and duration in the analysis interval were analyzed. The sequential order of the onset of hyoid movement, the onset and offset of the phase in which the hyoid bone was elevated, and the offset of hyoid movement were analyzed. The hyoid bone positions at the onset of it's movement, highest position (i.e., peak), and the offset of it's movement were also analyzed. The hyoid bone position at the start of measurement before the que of the examiner was used as a reference.
Table 1 Formulation and mechanical characteristics of gels. Gel
A10 A30 C10 C30
Concentration of gellan gum (% w/w)
Mechanical property
Texture characteristics
Low acylated
High acylated
Fracture force
Fracture strain
0.25 0.65 0.06 0.15
0 0 0.14 0.35
9.71 ± 0.13 28.7 ± 1.00 9.73 ± 0.94 29.4 ± 0.99
43.3 ± 0.34 46.2 ± 1.08 74.3 ± 1.67 78.7 ± 1.19
Soft - Brittle Hard - Brittle Soft - Deformable Hard - Deformable
Mechanical characteristics of agar gels were measured using a TA XT plus texture analyzer (Stable Micro Systems, Surrey, UK). Fracture force and strain were determined by compressing these gels on a metal stage using an aluminum plate of 50 mm in diameter at a crosshead speed of 10 mm/s at 20 °C. The gel size was 20 mm in diameter and 10 mm in height. 3
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Fig. 2. Reference plane and points of VF image. The anterior-inferior corner of the 4th cervical vertebra (C4) is defined as the origin. The C2-C4 axis is defined as the Y-axis. The anterior-inferior margin of the hyoid bone is defined as the reference point of hyoid movement. VF images were recorded at 30 frames per second.
synchronization. Using the onset time of hyoid movement during initial tongue squeezing as a reference, time points of tongue pressure, hyoid movement, and suprahyoid muscle activity were compared on a time series graph. Tongue pressure amplitude and duration were compared among channels. The changes in hyoid bone position were separated into anteroposterior and vertical components and compared among onset, peak, and offset. The maximum amplitude, duration, and area of tongue pressure, distance and duration of hyoid movement, and maximum amplitude, duration, and area of EMG at each channel were compared among the gel samples. For each evaluation item, the mean of two attempts was used as the representative value. Shapiro-Wilk test was applied to check normality of each evaluation item. Friedman’s test was used for comparisons among time points, channels, and gel samples during initial tongue squeezing, and the Wilcoxon signed-rank test with Bonferroni correction was used for post hoc analysis when Friedman’s test was significant. P < 0.05 was considered significant. SPSS Statistics software ver. 25 (IBM Japan, Tokyo, Japan) was used for analysis.
2.3.4. Suprahyoid muscle activity First, rectification and smoothing of the original waveform were performed. Using the mean ± 2 standard deviations of the amplitude during the first 3 s of measurement as a reference, the timing when the electromyography value exceeded the reference was specified as the onset of suprahyoid muscle activity for initial tongue squeezing. Then, between the peaks of the first and second waveforms, the timing when the amplitude reached a minimum was designated as the offset of initial tongue squeezing. The maximum amplitude, duration, area, and the timing of onset, peak, and offset of muscle activity were analyzed between the onset and offset of suprahyoid muscle activity. The mean of left and right values was used as the representative value for the maximum, duration, and area of muscle activity. 2.3.5. Data analysis Fig. 3 shows an example waveform of tongue pressure, hyoid movement, and suprahyoid muscle activity from the start of squeezing to the end of swallowing the gel after correcting the time for
3. Results 3.1. Coordination of TP, HM, and EMG during initial squeezing Fig. 4 shows the time coordination of tongue pressure, hyoid movement, and suprahyoid muscle activity during initial tongue squeezing for A30. At the start of tongue squeezing, there were not significant differences among the onset of tongue pressure at the midmedian position of the palate (Ch. 2), hyoid movement, and suprahyoid muscle activity. The onset of tongue pressure at the anterior-median position of the palate (Ch. 1) appeared, followed by the posterior palate (Chs. 3–5). Subsequently, at the phase when the hyoid bone was elevated, the suprahyoid muscle activity reached a maximum, and the tongue pressure at all channels (Chs. 1–5) reached a maximum. The offset of tongue pressure and suprahyoid muscle activity was followed by the offset of hyoid movement, and the initial tongue squeezing was concluded. Results for A10, C10, and C30 are shown in the Appendix and are similar to those of A30 (Figures S1, S2, and S3).
Fig. 3. Sample waveform of tongue pressure, hyoid position, and suprahyoid muscle activity during squeezing and swallowing gels. 4
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Fig. 4. Time sequences of tongue pressure, hyoid movement, and suprahyoid muscle activity during initial squeezing (A30). ●Onset time of tongue pressure ▲Peak time of tongue pressure ×Offset time of tongue pressure. ◼Onset time of hyoid movement ◆Onset time of the phase when the hyoid is the elevated position◇ Offset time of the phase when the hyoid is the elevated position □Offset time of hyoid movement ○ Onset time of EMG △ Peak time of EMG ＊Offset time of EMG. Time “0” was set at the onset of hyoid movement. *p < 0.05 (Friedman test with post hoc test). SHy: Suprahyoid muscles.
smaller fracture strain (A10 < C10, A30 < C30) resulted in a significantly greater tongue pressure amplitude at Chs. 1–3. Tongue pressure duration were longer at all channels with greater fracture force of the gel, but it was not significant (Fig. 6B). Tongue pressure area, similarly to tongue pressure amplitude, became greater at all channels with greater fracture force and smaller fracture strain (Fig. 6C). Comparisons of tongue pressure amplitude between each channel for each gel showed that gels with a small fracture strain (A10, A30) had greater amplitude at Ch. 2 than at the posterior Chs. 3–5, though gels with a large fracture strain (C10, C30) did not have different amplitudes between channels (Fig. 7A). On the other hand, tongue pressure duration was greater at Ch. 2 than at posterior Chs. 3–5 for all gels (Fig. 7B), and tongue pressure area was greater at Ch. 2 than at other channels (Fig. 7C). For suprahyoid muscle activity, gels with a large fracture force (A30) had greater maximum amplitude significantly, compared to gels with a small fracture force (A10, C10). Gels with a large fracture force also had greater muscle activity duration and area, and there was a significant difference between A30 and A10 (Fig. 8). For hyoid movement, gels with a large fracture force (A30, C30), compared to gels with a small fracture force (A10, C10), had a significantly greater hyoid moving distance (Fig. 9A) In addition, gels with a large fracture force had a longer hyoid moving duration than those with a small fracture force, and there were significant differences between C30 and A10 and C10. (Fig. 9B).
3.2. Position of the hyoid bone during initial squeezing During the initial tongue squeezing, there was a phase in which the hyoid bone was stationary at an elevated position. Although the anteroposterior position of the hyoid bone did not show a specific trend at onset, peak, and offset of initial tongue squeezing (Fig. 5A), the vertical position was significantly higher at peak or offset than at onset (Fig. 5B). The hyoid bone position was significantly lower at offset than at peak. These results were observed for all sample types. 3.3. Differences in TP, HM, and EMG during initial squeezing due to the mechanical properties of gels Tongue pressure, hyoid movement, and suprahyoid muscle activity during initial tongue squeezing differed depending on mechanical properties of the gels. Gels with a greater fracture force (A10 < A30, C10 < C30) resulted in a significantly greater tongue pressure amplitude at all channels (Fig. 6A). For gels with the same fracture force, a
4. Discussion In the present study, we have successfully described the sequential coordination of tongue pressure production, suprahyoid muscle activity, and hyoid movement as well as their spatial and mechanical modulation according to texture of gels during initial tongue squeezing. To the best of our knowledge, this is the first report that provides the biomechanical features of tongue squeezing as a strategy of food oral processing. Since this study used radiation for VF, there are temporal limitations in the number of experimental tasks. The experimental tasks required the participants to freely squeeze the test sample with their tongue without masticating with their teeth and to subsequently swallow at their own timing, such that the process was as natural as possible. Based on the time required for one task determined in the preliminary experiment, four types of gels with two trials each were used. Although it is necessary to change the fracture force and fracture strain by at least three levels to evaluate the changes in tongue squeezing by different food textures, this was not possible in the present study due to limitations of radiation exposure. The number of the participants was fifteen in this study, which might be the small sample size. However, the design of this study was not an interventional study
Fig. 5. Comparison of hyoid position at the onset, peak, and offset of initial squeezing. 5
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Fig. 6. Comparisons among four gels in maximum amplitude (A), duration (B), and area (C) of tongue pressure at each measuring point during initial squeezing. The maximum amplitude and area of tongue pressure at each measuring point tend to increase with fracture force, while the maximum amplitude and area tend to decrease with fracture strain. *p < 0.05 (Friedman test with post hoc test).
4.1. Coordination of TP, HM, and EMG during initial squeezing
but an exploratory and observational study with several outcomes (tongue pressure, hyoid movement and suprahyoid muscle activity). In addition, considering the risk of radiation exposure to the examiners, it is quite difficult to collect a large number of participants. For these reasons, we set the sample size in this study to fifteen like as our previous studies (Hori et al., 2013, 2015; Taniguchi, Tsukada, Ootaki, Yamada, & Inoue, 2008).
The results of the present study demonstrated that tongue pressure at the mid-median palate, suprahyoid muscle activity, and hyoid movement occurred simultaneously at the start of tongue squeezing. Previous studies showed that the onset of tongue pressure during liquid swallowing appeared after the onset of suprahyoid muscle activity (Taniguchi et al., 2008). Hori et al. reported that, during initial tongue squeezing, tongue pressure first appeared at the mid-median position of the palate (Ch. 2) where it is most affected by gel hardness, and that the Fig. 7. Comparisons among the five measuring points of the pressure sensor of maximum amplitude (A), duration (B), and area (C) of tongue pressure during initial squeezing of four gels. The maximum amplitude, duration and area of tongue pressure at Ch.2 (mid-median area of hard palate) tend to be higher than at the other channels. *p < 0.05 (Friedman test with post hoc test).
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Fig. 8. Comparisons among the four gels in maximum amplitude (A), duration (B), and area (C) of suprahyoid muscle activity during initial squeezing.
Furthermore, because the hyoid bone position was higher at the end than at the start of initial tongue squeezing, we believe that the whole tongue maintains a moderately elevated position to prepare for the subsequent tongue squeezing rather than returning to its original position for every tongue squeezing.
contact between the tongue at Ch. 2 and the palate played an important role in the recognition of food texture (Hori et al., 2015); similar results were observed in the present study. Furthermore, because the onset of tongue pressure at the mid-median palate appears around the same time as the onset of suprahyoid muscle activity and hyoid movement, it is postulated that, at the start of tongue squeezing, the suprahyoid muscle activity begins in order to squeeze the food against the midmedian palate, and the hyoid bone is elevated upward. During the initial tongue squeezing, there was a phase when the hyoid bone was virtually stationary in an elevated position. During this phase, the peak of tongue pressure and the peak of suprahyoid muscles appeared at all channels. In other words, the timing of maximum contact pressure at the palate and the timing of maximum suprahyoid muscle activity were during a phase in which the hyoid bone was in an elevated position. Since it has been previously reported that the hyoid bone is connected to the tongue via the hyoglossus muscle, forming the tongue platform (Dodds et al., 1990), tongue squeezing occurs not only with the morphological change of the tongue, but it is also affected by the hyoid movement and suprahyoid muscle activity with the whole tongue elevated upward.
4.2. Differences in TP, HM, and EMG during initial squeezing caused by the mechanical properties of gels In this study, we controlled fracture strain and fracture force which was measured by full compression of gels, though hardness of gels which was measured by partial compression was controlled in the previous studies (Hayashi et al., 2013; Hori et al., 2015; Yokoyama et al., 2014). Fracture force and strain are evaluated as the characteristics of deformation and fracture by compressing foods between a flat aluminum plate and stage. These parameters have been considered to be more reasonable than hardness to explain the breaking behavior of semi-solid food between tongue and hard palate (Ishihara et al., 2013, 2014), which was the reason why we employed them. During tongue squeezing, all parameters of tongue pressure, hyoid
Fig. 9. Comparisons among the four gels in moving distance (A) and duration (B) of hyoid movement during initial squeezing. 7
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2008), and that the hyoid bone position droops in older individuals compared to younger individuals (Feng et al., 2014). For these reasons, we also have to compare tongue squeezing between healthy young people, older people and those with mastication and swallowing problems in the future.
movement, and suprahyoid muscle activity became greater with gels with large fracture force (A30, C30) than with gels with small fracture force (A10, C10). Fracture force is the strength required to fracture food and is one of the mechanical properties in food engineering. We previously reported that the tongue pressure amplitude, duration, and number of tongue squeezing increase with greater gel hardness (Hori et al., 2015; Yokoyama et al., 2014). The present study also showed that tongue pressure amplitude and area during initial tongue squeezing were significantly greater with gels with a larger fracture force. Moreover, a larger fracture force increased the tongue pressure duration at initial tongue squeezing. In other words, when the fracture force of the gel increases, the pressure applied to the palate is large and continues for a long duration. These are similar to the results from our previous study involving adjusted hardness (Hori et al., 2015). Suprahyoid muscle activity had an increased maximum amplitude, muscle activity duration, and area with greater gel fracture force. Ishihara et al. previously reported that the muscle activity of the suprahyoid muscles increases with increasing fracture force of gels during oral processing (Ishihara et al., 2013), consistent with the results of the present study. Furthermore, because hyoid moving distance and duration increased with greater fracture force, it is likely that a greater fracture force of the gel increases the movement of the whole tongue. Summarizing these findings, when the fracture force of the gel increases, the contact pressure against the palate and the amplitude and duration of suprahyoid muscle activity increase, resulting in an increase in the movement of the whole tongue. Fracture strain is the strain of the food when food is crushed, and a larger value indicates a more deformable property. In gels with the same fracture force, a smaller fracture strain resulted in increased tongue pressure amplitude and area at Chs. 1–3; however, tongue pressure duration and other items related to hyoid movement and suprahyoid muscle activity were not significantly different. In addition, comparing the tongue pressure amplitudes between channels for each gel, the tongue pressure amplitude at the mid-median palate became higher than at the other channels during squeezing of brittle gels with a small fracture strain (A10, A30), and deformable gels with a large fracture strain (C10, C30) did not show significant differences in tongue pressure amplitude among channels. The reason for this may be that the gel shape during tongue squeezing differs depending on the fracture strain. When the fracture strain is small, the gel has less deformation until the gel is crushed, and tongue pressure can be focused specifically to the gel location during tongue squeezing; however, when the fracture strain is large, the tongue pressure per unit area is dispersed because the gel spreads. Summarizing these findings, when the fracture strain increases, the contact pressure to the palate decreases, changing the tongue pressure amplitude pattern.
5. Conclusion Time coordination of tongue pressure production, hyoid movement, and suprahyoid muscle activity was observed during initial tongue squeezing. Furthermore, tongue pressure, hyoid movement, and suprahyoid muscle activity during initial tongue squeezing appeared to change depending on the properties of the food to be processed. Moreover, the hyoid bone did not return to its original position at the end of initial tongue squeezing, but rather maintained an elevated position, which was suggestive of preparation for the next tongue squeezing. Author contributions Study design: K. Hori, K. Murakami. Data collection: K. Murakami, K. Hori, Y. Minagi, F. Uehara, S.E. Salazar. Data analysis: K. Murakami, Y. Minagi. Manuscript writing: K. Murakami, K. Hori. Manuscript editing: Y. Maeda, T. Ono, K. Ikebe. Sample supply: T. Funami, M. Nakauma, S. Ishihara. Funding This work was supported by JSPS KAKENHI Grant Number JP18K17116. Declaration of Competing Interest There are no conflict of interests in connection with this article. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.archoralbio.2019. 104631. References Crary, M. A., Carnaby-Mann, G. D., & Groher, M. E. (2006). Biomechanical correlates of surface electromyography signals obtained during swallowing by healthy adults. Journal of Speech, Language, and Hearing Research, 49, 186–193. Dodds, W. J., Stewart, E. T., & Logemann, J. A. (1990). Physiology and radiology of the normal oral and pharyngeal phases of swallowing. American Journal of Roentgenology, 154, 953–963. Feng, X., Todd, T., Lintzenich, C. R., Ding, J., Carr, J. J., Ge, Y., et al. (2013). Agingrelated geniohyoid muscle atrophy is related to aspiration status in healthy older adults. The Journal of Gerontology Series A: Biological Sciences and Medical Sciences, 68, 853–860. Feng, X., Todd, T., Hu, Y., Lintzenich, C. R., Carr, J. J., Browne, J. D., et al. (2014). Agerelated changes of hyoid bone position in healthy older adults with aspiration. Laryngoscope, 124, E231–236. Hayashi, H., Hori, K., Taniguchi, H., Nakamura, Y., Tsujimura, T., Ono, T., et al. (2013). Biomechanics of human tongue movement during bolus compression and swallowing. Journal of Oral Science, 55, 191–198. Hori, K., Ono, T., Tamine, K., Kondoh, J., Hamanaka, S., Maeda, Y., et al. (2009). A newly developed sensor sheet for measuring tongue pressure in swallowing. Journal of Prosthodontic Research, 53, 28–32. Hori, K., Taniguchi, H., Hayashi, H., Magara, J., Minagi, Y., Li, Q., et al. (2013). Role of tongue pressure production in oropharyngeal swallow biomechanics. Physiological Reports, 1, e00167. Hori, K., Hayashi, H., Yokoyama, S., Ono, T., Ishihara, S., Magara, J., et al. (2015). Comparison of mechanical analysis and tongue pressure analyses during squeezing and swallowing of gel agents. Food Hydrocolloids, 44, 145–155. Ikebe, K., Matsuda, K., Kagawa, R., Enoki, K., Okada, T., Yoshida, M., et al. (2012). Masticatory performance in older subjects with varying degrees of tooth loss. Journal
4.3. Clinical implications The present findings are the foundation of kinematics of tongue squeezing, which is a compensatory mastication process. They indicate that suprahyoid muscle plays a role of elevation of whole tongue in tongue squeezing in addition to mouth opening and swallowing. It is known that suprahyoid muscle is decreased by aging and dysphagia (Feng et al., 2013). Therefore, these findings may become important information for establishing criteria for selecting the food form for the elderly population declined masticatory and /or swallowing function. However, tongue function during tongue squeezing is not only to process soft food against hard palate, but also to accumulate and transport food bolus into pharynx. In the future, we have to evaluate the entire tongue squeezing process and swallowing, rather than just the initial tongue squeezing, to determine the relationship between tongue squeezing and the subsequent swallowing. As for the age related decline in tongue and hyolaryngeal motor function, It has been reported that tongue pressure at maximum tongue squeezing decreases with age or existing diseases (Utanohara et al., 8
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requestSender=estat. Morris, V. J. (2006). Bacterial polysaccharide. Food polysaccharides and their applications. London: Taylor & Francis. Ono, T., Hori, K., & Nokubi, T. (2004). Pattern of tongue pressure on hard palate during swallowing. Dysphagia, 19, 259–264. Taniguchi, H., Tsukada, T., Ootaki, S., Yamada, Y., & Inoue, M. (2008). Correspondence between food consistency and suprahyoid muscle activity, tongue pressure, and bolus transit times during the oropharyngeal phase of swallowing. Journal of Applied Physiology, 105, 791–799. Teramoto, S., Fukuchi, Y., Sasaki, H., Sato, K., Sekizawa, K., & Matsuse, T. (2008). High incidence of aspiration pneumonia in community- and hospital-acquired pneumonia in hospitalized patients: A multicenter, prospective study in Japan. Journal of the American Geriatrics Society, 56, 577–579. The Dysphagia Diet Committee of the Japanese Society of Dysphagia Rehabilitation (2013). The Japanese Dysphagia diet 2013. The Japanese Journal of Dysphagia Rehabilitation, 17, 255–267. Utanohara, Y., Hayashi, R., Yoshikawa, M., Yoshida, M., Tsuga, K., & Akagawa, Y. (2008). Standard values of maximum tongue pressure taken using newly developed disposable tongue pressure measurement device. Dysphagia, 23, 286–290. Yokoyama, S., Hori, K., Tamine, K., Fujiwara, S., Inoue, M., Maeda, Y., et al. (2014). Tongue pressure modulation for initial gel consistency in a different oral strategy. PLoS One, 9, e91920.
of Dentistry, 40, 71–76. Ishihara, S., Nakauma, M., Funami, T., Tanaka, T., Nishinari, K., & Kohyama, K. (2011). Electromyography during oral processing in relation to mechanical and sensory properties of soft gels. Journal of Texture Studies, 42, 254–267. Ishihara, S., Nakao, S., Nakauma, M., Funami, T., Hori, K., Ono, T., et al. (2013). Compression test of food gels on artificial tongue and its comparison with human test. Journal of Texture Studies, 44, 104–114. Ishihara, S., Isono, M., Nakao, S., Nakauma, M., Funami, T., Hori, K., et al. (2014). Instrumental uniaxial compression test of gellan gels of various mechanical properties using artificial tongue and its comparison with human oral strategy for the first size reduction. Journal of Texture Studies, 45, 354–366. Logemann, J. A., Pauloski, B. R., Rademaker, A. W., Colangelo, L. A., Kahrilas, P. J., & Smith, C. H. (2000). Temporal and biomechanical characteristics of oropharyngeal swallow in younger and older men. Journal of Speech Language and Hearing Research, 43, 1264–1274. Matsuyama, Y., Aida, J., Watt, R. G., Tsuboya, T., Koyama, S., Sato, Y., et al. (2017). Dental status and compression of life expectancy with disability. Journal of Dental Research, 96, 1006–1013. Ministry of Agriculture, Forestry and Fishes (2019). Effort relating to “smile care food” – Introduction of new mark system. http://www.maff.go.jp/e/policies/food_ind/attach/ pdf/index-9.pdf. Ministry of Health, Labour and Welfare (2015). Vital statistics. https://www.e-stat.go.jp/ SG1/estat/GL08020103.do?_toGL08020103_&listID=000001158057&disp=Other&
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