Skip to main content
NCBI home page
Journal of Speech, Language, and Hearing Research : JSLHR logoLink to Journal of Speech, Language, and Hearing Research : JSLHR
. 2020 Sep 23;63(10):3408–3418. doi: 10.1044/2020_JSLHR-20-00125

Determining the Underlying Relationship Between Swallowing and Maximum Vocal Pitch Elevation: A Preliminary Study of Their Hyoid Biomechanics in Healthy Adults

Anumitha Venkatraman a, Robert Brinton Fujiki a, Bruce A Craig b, M Preeti Sivasankar a,c, Georgia A Malandraki a,c,✉
PMCID: PMC8582751  PMID: 32966145

Abstract

Purpose

Deficiencies in swallowing (aspiration) and in maximum vocal pitch elevation have been shown to correlate in dysphagia. However, the underlying mechanisms that may explain this relationship are not known. In this study, we compare hyoid kinematics between swallowing and maximum vocal pitch elevation in healthy adults.

Method

Ten young (M = 21 ± 1.33 years) and eight older (M = 72.85 ± 5.59 years) healthy adults completed trials of maximum vocal pitch elevation (vowels /a/ and /i/) and swallowing (thin liquid and pudding) under videofluoroscopy. Superior and anterior hyoid excursions were obtained using kinematic analysis. Two-way analyses of variance and Spearman rho correlations were used to examine differences and relationships between swallowing and maximum pitch elevation biomechanics.

Results

Superior hyoid excursion was significantly greater for liquid swallows compared to pitch elevation tasks (/a/ and /i/; p = .002; Cohen's d = 1.28; p = .0179, Cohen's d = 1.03, respectively) and for pudding swallows compared to pitch tasks (p = .000, Cohen's d = 1.64; p = .001, Cohen's d = 1.38, respectively). Anterior hyoid excursion was not significantly different between the two functions, but was overall reduced in the older group (p = .0231, Cohen's d = .90). Furthermore, there was a moderate positive correlation between the degree of superior excursion during liquid swallows and maximum pitch elevation for both vowels (r s = .601, p = .001; r s = .524, p = .003) in young adults, and between the degree of anterior excursion during liquid swallows and pitch elevation for both vowels (r s = .688, p = .001; r s = .530, p = .008) in older adults.

Conclusions

Swallowing and maximum pitch elevation require similar anterior, but not superior, hyoid excursion in healthy adults. Differential correlations between the two tasks for each age group may be associated with age-related muscle changes. We provide evidence of partially shared biomechanics between swallowing and maximum pitch elevation.

Swallowing and maximum vocal pitch elevation are distinct functions of the head and neck that share neurophysiological and anatomical substrates. Recent evidence suggests a potential relationship between reduced maximum vocal pitch elevation abilities and swallowing dysfunction (specifically aspiration) in patients with neurogenic dysphagia (primarily due to stroke; Rajappa et al., 2017) and in patients with respiratory disease (Mavrea & Regan, 2019). However, the underlying mechanisms that may explain this relationship have not been extensively investigated. Identifying potential shared and distinct biomechanics between swallowing and maximum vocal pitch elevation in the healthy mechanism may enable a better understanding of the potential cross-system interactions between these functions. The purpose of this study is to start determining these mechanisms.

From a neurophysiological perspective, the external branch of the superior laryngeal nerve (SLN) motorically innervates the cricothyroid (CT) muscle and the inferior pharyngeal constrictor, and the internal branch of the SLN provides sensation to the laryngo-pharyngeal region. The CT is one of the primary muscles responsible for raising vocal pitch (Mu & Sanders, 2009). Therefore, it has been hypothesized that lesions affecting the SLN may result in both reduced vocal pitch elevation and silent aspiration (or absent sensation when foreign particles enter the airway). Indeed, studies have provided evidence indicating that reduced vocal pitch elevation abilities may be correlated or even predictive of aspiration (Malandraki et al., 2011; Mavrea & Regan, 2019; Rajappa et al., 2017).

From a mechanical point of view, swallowing requires both the vertical and anterior movement of the hyoid and larynx, to facilitate airway closure (Pearson et al., 2013; Ragland et al., 2016; Steele et al., 2011; Zoratto et al., 2010). This hyolaryngeal excursion is achieved primarily by the suprahyoid muscles, but also partially by the contraction of the long pharyngeal muscles (Pearson et al., 2013). With specific regard to suprahyoid muscles, the geniohyoid and mylohyoid assist in anterior and superior hyoid movements, respectively (Pearson et al., 2011). Overall, hyoid excursion ensures adequate airway closure and bolus clearance during swallowing and is an extensively studied event (Nagy et al., 2014; Steele et al., 2011).

Two studies provide similar evidence for tasks that involve vocal pitch, such as the effortful pitch glide or maximum vocal pitch elevation (Hong et al., 2015; Miloro et al., 2014). Both studies reported increased superior hyoid excursion with rising pitch (Hong et al., 2015; Miloro et al., 2014). An association between suprahyoid muscle activity (specifically the geniohyoid) and increasing fundamental frequency was initially postulated in the 1970s–1980s (Erickson et al., 1976; Honda et al., 1981; Sapir et al., 1981). Alternate pitch-raising mechanisms such as thyroarytenoid muscle contraction and increasing lung pressure have been previously reported (Shipp, 1975; Titze, 1989, 1994); however, the role of supralaryngeal musculature in pitch elevation has not been clearly delineated (Vilkman et al., 1996).

In addition, there is emerging evidence that supports a potential cross-system interaction between swallowing and maximum vocal pitch elevation. A recent study showed that gains in the higher frequency range were observed in healthy older adults after implementing two exercises that targeted improved hyolaryngeal excursion, that is, the recline and head lift exercises (Fujiki et al., 2019). Additionally, healthy older adults who completed the head lift exercise had improved voice outcomes, as measured using the Dysphonia Severity Index, when compared to healthy controls (Easterling, 2008). Finally, a group of patients with Parkinson's disease self-reported significant improvement in swallowing-related symptoms following the Lee Silverman Voice Treatment, which includes pitch glides as one of its components (Miles et al., 2017). Albeit the preliminary nature of this evidence, clinically vocal pitch elevation (i.e., pitch glides) is often used as an exercise aimed at improving hyolaryngeal excursion.

Although these earlier findings point to a potential relationship between the two functions, the underlying shared and separate biomechanical mechanisms of these two systems have not been delineated. Better understanding of these mechanisms in healthy physiology first may shed light on whether and how these two systems interact and form a basis for comparison with patient populations in the future. Therefore, the overarching purpose of this preliminary study is to identify the shared and distinct underlying biomechanical mechanisms—specifically hyoid excursion—of swallowing and maximum vocal pitch elevation in healthy young and older adults. Specifically, we aimed to determine if superior and anterior hyoid excursions were significantly different when comparing maximum vocal pitch elevation and swallowing. Based on the findings of a preliminary study investigating the comparative hyoid and laryngeal excursion between swallowing and pitch glide tasks in young adults (Miloro et al., 2014), we hypothesized that superior hyoid excursion would be significantly greater for swallowing, but anterior hyoid excursion would be similar for both functions in young and older adults. Because data on older adults are sparse, it is critical to include older adults in this investigation, as age-related changes in laryngeal physiology can increase the risk of dysphagia in this population (Mulheren et al., 2018), and to allow for comparisons with elderly individuals with dysphagia in the future. Second, we aimed to explore potential correlations between hyoid excursion during both tasks.

Method

All procedures and protocols were approved by our university institutional review board before initiation of this study.

Participants

Two groups of participants were recruited, a healthy young adult group (18–35 years old) and a healthy older group (> 65 years old). All participants were recruited from the West Lafayette and Lafayette areas (IN, United States) from January 2019 to June 2019. To participate, individuals had to satisfy the following inclusionary criteria: (a) be between the ages of 18–35 years or above the age of 65 years; (b) have no significant medical history including neurological diseases, stroke, asthma or respiratory illness, head–neck surgery, or cancer; (c) no history of voice or swallowing difficulty; (d) no pregnancy at the time of the study as confirmed with a pregnancy test before the session for young adults, and (e) no professional singing or voice training. Additionally, young adults were not taking any prescription medication at the time of the study (with the exception of birth control).

This study was a preliminary study that was designed as a first step to a future clinical trial. Knowing the study would be of limited size, we determined the sample size based on detecting relatively large differences among the tasks. Specifically, we determined that a sample size of n = 20 subjects was needed to detect a large effect size (Cohen's d = 0.9) between any two tasks with a power of 80%. We divided this number between young and old participants in order to also better understand interaction.

Screening Procedures

All participants were screened with rigid videostroboscopy (Model 9310 HD, Pentax Medical). No overt lesions were observed. Glottal competence was observed in all participants. All participants obtained normative scores on the following questionnaires: on the Functional, Physical, and Emotional subsections of the Vocal Handicap Index (Jacobson et al., 1997); the Eating Assessment Tool-10 (scores of < 3; Belafsky et al., 2002); and the Montréal Cognitive Assessment (< 26; Nasreddine et al., 2005) as shown in Table 1. A cranial nerve examination and a bedside swallowing assessment were also performed to ensure functional clinical swallowing function. This examination includes a detailed assessment of the sensory and/or motor functions of cranial nerves V–XII, that is, the cranial nerves involved in the phases of swallowing and voice production (Carnaby, 2012; Perlman, 1996) and few oral trials of liquids and solids (McCullough & Martino, 2013).

Table 1.

Demographic and screening data for study participants.

Number Gender Age Group EAT-10 MoCA VHI score
Functional Emotional Physical
1 M 22 Young 1 27 0 0 1
2 M 21 Young 1 29 1 0 3
3 F 21 Young 1 29 1 0 2
4 F 21 Young 0 28 3 0 3
5 F 20 Young 1 27 0 0 0
6 M 19 Young 0 28 0 0 0
7 F 19 Young 0 29 0 0 0
8 F 23 Young 0 29 0 0 0
9 M 22 Young 1 28 4 0 1
10 M 22 Young 1 30 8 7 4
11 M 79 Older 0 30 0 0 0
12 M 74 Older 0 28 7 4 5
13 F 65 Older 0 29 0 0 0
14 M 79 Older 1 30 2 0 1
15 F 77 Older 0 29 0 0 0
16 M 65 Older 0 30 0 0 0
17 F 72 Older 0 28 6 1 2
18 F 72 Older 0 26 0 0 0
Open in a new tab

Note. EAT-10 = Eating Assessment Tool-10; MoCA = Montréal Cognitive Assessment; VHI = Vocal Handicap Index; M = male; F = female.

Experimental Protocol

This is a prospective crossover study with two groups of participants. Each participant completed four tasks in one experimental session that lasted approximately 2 hr.

Pre-Experiment Training

A customized training video was created for tasks of maximum vocal pitch elevation on the vowels /i/ and /a/ and swallowing barium contrast. The training video ensured that the same instructions and models were provided for every task. After shown a model in the training video, each participant was then asked to glide to their highest pitch at a comfortable loudness and maintain that pitch for 2–3 s. Each participant completed two practice trials of maximum vocal pitch elevation (one on each vowel, /i/ and /a/) and was given verbal feedback (if needed). If the participant stated that they could sustain a higher pitch, they were asked to repeat a practice trial. The video also instructed participants to swallow barium contrast in a single swallow, and they completed one practice trial using 10-ml Varibar Thin Liquid barium (CAT. NO. 105, E-Z-EM Canada Inc.). This ensured participants were familiar with both tasks before the actual experiment took place. The participants were asked to practice completing the tasks with minimal movement of the head and neck.

Data Collection (Videofluoroscopy)

The experiment was completed in the videofluoroscopy suite of our lab using a videofluoroscopic C-arm system (OEC 9800 Plus Digital Mobile 12 in. GE). The C-arm system recorded images at 30 frames per second at the highest resolution (30 pulses per second). Patients were seated upright next to the image intensifier such that the following anatomical structures were visible in lateral view: oral and nasal cavities, upper vertebrae, upper esophagus, and hyoid and laryngeal areas.

Patients first completed three trials of maximum vocal pitch elevation on vowels /i/ and /a/. Audio recordings were collected simultaneously with videofluoroscopy using an audio recorder with a built-in omnidirectional, condenser microphone (DR-05 Audio recorder, TAScom) with a 44.1-kHz sampling rate that was placed on a stand at a constant distance of exactly 1 ft from the participant (measured using a ruler). After each maximum vocal pitch elevation task, participants were asked, “Do you think you reached your highest pitch?” and then rated their self-perceived highest pitch on a 5-point visual analogue scale (left anchor = 1 being not the highest pitch, and right anchor = 5 being the highest pitch; Rajappa et al., 2017). This task was completed so that participants would be encouraged to reach their highest pitch. Then, all participants self-fed three trials of the following bolus consistencies: 10-ml Varibar thin liquid barium (CAT. NO. 105, E-Z-EM Canada Inc.) and 5-cc Varibar barium pudding (CAT. NO. 125, E-Z-EM Canada Inc.). The order of tasks was not counterbalanced because we wanted to prevent any potential impact of the barium taste or residue on oropharyngeal movements during maximum pitch elevation. The participants were instructed and reminded to maintain an upright posture with minimum movement of the head and neck during the tasks.

Data Analysis

Swallowing and vocal pitch biomechanics. Biokinematic analysis on all trials of swallowing and vocal pitch elevation was conducted using Image J software (https://imagej.nih.gov/ij/index.html; Rasband, 1997–2018). Superior and anterior hyoid excursions on swallowing trials were analyzed using an algorithm and protocol established by Molfenter and Steele (2014). Specifically, hyoid excursion was calculated using an algorithm that maps hyoid position in relation to the C2-C4 vertebrae (as an anatomical scalar). This measurement was used to control for subject size, height, and sex (Brates et al., 2020; Molfenter & Steele, 2014) and reduce measurement variability. Hyoid excursion analysis was chosen instead of hyoid peak position analysis in order to compare the magnitude of hyoid displacement observed in both swallowing and maximum vocal pitch elevation. In swallowing trials, the hyoid rest frame was defined as the lowest position of the hyoid within 10 frames of epiglottic inversion postswallow (Fujiki et al., 2019). If the hyoid continued to descend after 10 frames following epiglottic inversion, another 10 frames were considered in order to obtain the lowest point of the hyoid in this range (Fujiki et al., 2019). In order to adapt this protocol to analyze trials of maximum vocal pitch elevation, the hyoid “rest” frame for the pitch trials was defined as the lowest position of the hyoid after jaw opening and start of phonation. This “rest or low” frame was chosen as the hyoid is vertically lower during phonation tasks than at rest in healthy participants (Lowell et al., 2012). Once the hyoid rest frame was identified for each trial, the following anatomical positions were marked in the following order: the most anterior–inferior position of (a) the C2 vertebra, (b) the C4 vertebra, and (d) the hyoid bone.

Next, the frame with maximum hyoid displacement (hyoid max frame) was defined in each trial. The maximal superior and anterior position of the hyoid bone was identified during swallowing and maximum vocal pitch elevation trials. For maximum vocal pitch elevation and because the maximum hyoid position was maintained for several seconds, the first frame corresponding to the highest superior and anterior hyoid position was recorded. If the frame corresponding to the maximal superior position of the hyoid differed from the maximal anterior position, then different hyoid max frames were used in calculation of these measures. The data were then transferred to an Excel sheet containing the algorithm developed by Molfenter and Steele (2014), to obtain the superior and anterior hyoid excursion data for all trials of swallowing and maximum vocal pitch elevation. Analysis of tasks was not blinded, as it was obvious which trial (swallowing or pitch) was being analyzed, but analyzers were blinded to group (young vs. old). The analysis of the kinematic videofluoroscopic data was completed by the first author, who is a doctoral student in speech and language pathology. Ten percent of all data were re-analyzed by another and the same rater to enable inter- and intrareliability measures. The second author (also a doctoral student in speech and language pathology) completed the analysis for interrater reliability measures. Both raters had reached > 80% agreement with the principal investigator (last author) on these measurements before the analysis for this project was initiated.

Acoustic and self-perceptual outcome measures. Maximum vocal pitch elevation samples from the audio recorder (DR-05 Audio recorder, TAScom) were extracted as .wav files. Acoustic analysis on all six trials of maximum vocal pitch elevation (three on each vowel) was completed using the Praat software (Version 6.1; Boersma & Weenink, 2019). In each maximum vocal pitch elevation sample, the pitch and intensity contours were first obtained. Approximately 1 s of the sample that corresponded to the maximum fundamental frequency was selected in accordance with established procedures (Goy et al., 2013; Lortie et al., 2015). The vocal intensity (in dB) and maximum fundamental frequency (in Hz) were then recorded. Although no specific cues regarding vocal register were provided to the participants, they each were perceived to transition between the “modal” and “falsetto” register during their maximum vocal pitch elevation productions.

Statistical Analysis

Statistical analysis was completed using SPSS (Version 23) and SAS software (Version 9.4). In order to determine if superior and anterior hyoid excursions were significantly different between the tasks of maximum vocal pitch elevation and swallowing, two-way linear mixed analyses of variance (ANOVAs) were performed for the between-subjects factor (age; i.e., old, young) and within-subject factor (task; 5-cc pudding swallow, 10-ml thin liquid, vowels /a/ and /i/) on each dependent measure with effect sizes reported in partial eta squared. All residuals from the model were tested with Shapiro–Wilk test of normality for parametric test assumptions. Post hoc mean comparisons were used for further post hoc analysis of significant effects, and effect sizes are reported in Cohen's d.

In order to explore potential relationships between both superior and anterior hyoid excursions during swallowing and maximum vocal pitch elevation, Spearman correlation coefficient was used for all four tasks (5-cc pudding swallow, 10-ml thin liquid, vowel /a/, and vowel /i/). Spearman correlation coefficient was selected because not all data followed a normal distribution. In addition, during tasks of vocal pitch elevation, the transition between the modal to the falsetto register may prevent a linear increase in superior and anterior hyoid excursions with increasing pitch.

Results

Reliability

Inter- and intrarater reliability was computed on 10% of the biokinematic and acoustic data using intraclass correlation coefficients (ICCs) that are reported according to established criteria (Koo & Li, 2016). For superior hyoid excursion, intrarater reliability was excellent with an ICC of .934 (p = .00, 95% CI [.853, .971]) and interrater reliability was in the good range with an ICC of .873 (p = .000, 95% CI [.730, .943]). For anterior hyoid excursion, intrarater reliability was in the good range with an ICC of .889 (p = .000, 95% CI [.729, .957]). Interrater reliability was also in the good range with an ICC of .822 (p =.000, 95% CI [.632, .919]). For maximum fundamental frequency, intrarater reliability was excellent with an ICC of .953 (p = .000, 95% CI, [.846, .986]). Interrater reliability was also excellent with an ICC of .909 (p = .000, 95% CI [.716, .973]). For vocal intensity, intrarater reliability was excellent with an ICC of .964 (p = .000, 95% CI, [.881, .990]). Interrater reliability for vocal intensity was also excellent with an ICC of .946 (p = .00, 95% CI [.824, .984]).

Participants–Demographics

The demographic and screening information for each participant are shown in Table 1. Twenty participants (10 young adults and 10 older adults) were screened for the study. Two older adults did not qualify due to their scores on the Montréal Cognitive Assessment (Nasreddine et al., 2005). Additionally, one young adult and one older adult had a hypersensitive gag reflex and could not be screened with rigid videostroboscopy. However, both of these participants had no complaints or history of voice-related problems and obtained normative scores on the Vocal Handicap Index and, thus, were included in the study. As a result, 10 healthy young adults (M = 21 ± 1.33 years; five females and five males) and eight healthy older adults (M = 72.85 ± 5.59 years; four females and four males) completed the experiment.

Acoustic and Self-Perceptual Analysis

The mean and standard errors for maximum fundamental frequency, vocal intensity, and self-perceived vocal maximum pitch elevation ability are reported in Table 2. The self-perceptual ratings reported are average values across the maximum vocal pitch elevation tasks for each vowel. The self-perceptual ratings were generally 4 or higher, indicating that each participant perceived that they reached their highest pitch on tasks of maximum vocal pitch elevation for both vowels /a/ and /i/.

Table 2.

Mean and standard deviations of the acoustic and self-perceptual measures collected during tasks of vocal pitch elevation tasks.

Group Vowel /a/
 Vowel /i/
Fundamental frequency (Hz) Self-perceived pitch elevation ability (Scale 1–5) Intensity (dB) Fundamental frequency (Hz) Self-perceived pitch elevation ability (Scale 1–5) Intensity (dB)
Young males 553.86 ± 93.86 4.63 ± 0.51 71.2 ± 1.87 579 ± 100.7 4.82 ± 0.44 71.2 ± 3.74
Young females 937.46 ± 154.23 4.53 ± 0.61 81.33 ± 3.39 921.4 ± 143.27 4.63 ± 0.516 78.2 ± 7.39
Older males 383. 58 ± 76.7 4.54 ± 0.62 74 ± 8.99 400.16 ± 74.17 4.675 ± 0.43 75.83 ± 7.2
Older females 634.166 ± 241.27 4.27 ± 0.63 67.16 ± 4.10 700.66 ± 262.55 4.20 ± 0.68 67.33 ± 2.99
Open in a new tab

Differences in Hyoid Excursion Between Maximum Vocal Pitch Elevation and Swallowing

Superior Hyoid Excursion

Two-way ANOVA results revealed a significant main effect of task, swallowing and maximum pitch, F(3, 48) = 11.02, p = .000, partial η2 = .408. Age was not significant, F(1, 16) = 3.47, p = .0811, partial η2 = .178, and there were no significant interaction effects, F(3, 48) = .8049, p = .540. Post hoc analysis comparing tasks revealed significant differences between the degree of superior hyoid excursion for 10-ml thin liquid swallows and for maximum vocal pitch elevation on the vowel /a/, t(48) = 3.81, p = .002, Cohen's d = 1.28, large effect size, and the vowel /i/, t(48) = 3.07, p = .0179, Cohen's d = 1.03, large effect size. Superior hyoid excursion on 5-cc pudding swallows was also significantly greater when compared to vowel /a/, t(48) = 4.86, p = .000, Cohen's d = 1.64, large effect size and vowel /i/, t(48) = 4.11, p = .001, Cohen's d = 1.38, large effect size. These results are shown in Figure 1.

Figure 1.

Figure 1.

Open in a new tab

Means and standard errors of superior hyoid excursion (%C2-C4 distance) in tasks of swallowing and maximum vocal pitch elevation in younger and older adults. *Indicates a significant difference between tasks of swallowing and maximum vocal pitch elevation (p < .05).

Anterior Hyoid Excursion

For anterior hyoid excursion, two-way ANOVA results revealed a significant main effect of age, F(1, 16) = 6.31, p = .002, partial η2 = .283. Task was not significant, F(3, 48) = 1.60, p = .201), and there were no significant interaction effects, F(3, 48) = 0.32, p = .809. With regard to age, anterior hyoid excursion values for younger adults were greater when compared to older adults (p = .0231, Cohen's d = 0.90) across tasks. These results are depicted in Figure 2.

Figure 2.

Figure 2.

Open in a new tab

Means and standard errors of anterior hyoid excursion (%C2-C4 distance) in tasks of swallowing and vocal pitch elevation in younger and older adults. *Indicates significant differences between older and younger adults (p < .05).

Exploring Correlations Between Hyoid Kinematics During Maximum Vocal Pitch Elevation and Swallowing

Superior Hyoid Excursion for Young Adults

For young adults, there were significant moderate positive correlations between the degree of superior hyoid excursion during liquid swallows and during maximum pitch elevation of the vowel /a/ (r s = .601, p = .001; see Figure 3a) and the vowel /i/ (r s = .524, p = .003; see Figure 3b). Also, there was a significant moderate positive correlation between the degree of superior hyoid excursion during pudding swallows and during maximum pitch elevation of the vowel /a/ (r s = .603, p = .001; see Figure 3c). These results suggest that, in young healthy adults, higher magnitudes of superior hyoid excursion in tasks of swallowing moderately correlate with higher magnitudes of superior hyoid excursion in maximum vocal pitch elevation.

Figure 3.

Figure 3.

Open in a new tab

Significant correlations for superior hyoid excursion in young adults.

Superior Hyoid Excursion for Older Adults

There were no significant correlations between the degree of superior hyoid excursion during liquid or pudding swallows and during maximum pitch elevation of either vowel for the older group.

Anterior Hyoid Excursion for Young Adults

Similarly, there were no significant correlations between the degree of anterior hyoid excursion during liquid or pudding swallows and during maximum pitch elevation of either vowel for the younger group.

Anterior Hyoid Excursion for Older Adults

For the older group, there were significant moderate positive correlations between the degree of anterior hyoid excursion during liquid swallows and during maximum pitch elevation of the vowel /a/ (r s = .688, p = .001; see Figure 4a) and the vowel /i/ (r s = .530, p = .008; see Figure 4b). In addition, there was also a significant moderate positive correlation between the degree of anterior hyoid excursion during pudding swallows and during maximum pitch elevation of the vowel /a/ (r s = .575, p = .003; see Figure 4c). This suggests that, in older healthy adults, higher magnitudes of anterior hyoid excursion in tasks of swallowing moderately correlate with higher magnitudes of anterior hyoid excursion in tasks of maximum vocal pitch elevation.

Figure 4.

Figure 4.

Open in a new tab

Significant correlations for anterior hyoid excursion in older adults.

Discussion

The overarching purpose of this preliminary study was to start uncovering the shared and distinct underlying hyoid excursion biomechanics of swallowing and maximum vocal pitch elevation in healthy adults. Investigating these mechanisms in healthy adults first is an important step in providing insights on the potential interactions of these two functions and in forming normative data that will enable comparisons with patient populations in the future.

Our results indicated that superior hyoid excursion was significantly greater in magnitude for swallows when compared to tasks of maximum vocal pitch elevation in both age groups. It is well documented that superior hyoid excursion assists in protecting the airway and facilitating adequate bolus clearance (Pearson et al., 2013; Ragland et al., 2016; Steele et al., 2011; Zoratto et al., 2010). This hyoid excursion during swallowing is primarily achieved by suprahyoid muscle contraction with some assistance from the long pharyngeal muscles (Pearson et al., 2011). While some evidence suggests maximum vocal pitch elevation is also associated with superior hyoid excursion (Hong et al., 2015), it is primarily achieved by the CT muscle and other physiological mechanisms (e.g., thyroarytenoid muscle contraction and lung pressure increases; Shipp, 1975; Titze, 1989, 1994) and may not require suprahyoid muscle contraction to the same extent as swallowing. Therefore, our results are not surprising and are in agreement with a recent study that suggests that laryngeal lift is also greater in tasks of swallowing when compared to pitch elevation in patients with dysphagia (Kennedy et al., 2019).

Exploration of the relative role of the suprahyoid musculature in each function may elucidate the increased degree of superior hyoid excursion during tasks of swallowing when compared to tasks of maximum vocal pitch elevation and may provide insights on our age-specific correlation results, as well. Specifically, we found that the degree of this excursion during swallows was moderately positively correlated with the degree of excursion during tasks of vocal pitch elevation in younger, but not older, adults. This finding may be explained by the different muscle properties underlying the main muscles involved in these functions. In terms of suprahyoid musculature, the mylohyoid primarily facilitates superior hyoid excursion (Matsubara et al., 2018; Pearson et al., 2013). The mylohyoid has a greater percentage of Type I (slow twitch) muscle fibers (Ren & Mu, 2005), which are relatively spared from sarcopenia or age-related muscle atrophy (Cobos et al., 2001; Matsubara et al., 2018). However, the CT muscle—which is primarily responsible for elevating vocal pitch—undergoes significant muscle fiber changes with age (Nishida et al., 2013). The relative contributions of the CT versus suprahyoid musculature in maximum vocal pitch elevation and the differential age-related changes in these muscle groups may explain the positive correlation in superior hyoid excursion during the examined tasks in younger, but not older, adults, who experience sarcopenia-related muscle changes. It should be noted that a small number of studies have reported age-related differences in superior hyoid excursion during swallows (Kim & McCullough, 2010; Logemann et al., 2000); however, the literature on these findings remains mixed (Kang et al., 2010; Logemann et al., 2002; Molfenter & Steele, 2011). Our study did not reveal significant age-related differences in superior hyoid excursion, but given the relatively large effect size (partial η2 = .178), we believe this may be deserving of further investigation.

The second important finding of our study was that anterior hyoid excursion was not significantly different across the two types of tasks. This anterior hyoid movement is essential for adequate airway closure and bolus clearance during swallowing (Nagy et al., 2014; Steele et al., 2011). In our study, comparable (i.e., not significantly different) degrees of anterior hyoid displacement were observed across tasks of swallowing and maximum vocal pitch elevation across groups. However, anterior excursion was significantly reduced in the older group compared to the younger group across tasks. This finding may partially explain the results of prior research, which included primarily older adults, that has found associations between reduced maximum vocal pitch elevation abilities and the occurrence of aspiration (Malandraki et al., 2011; Mavrea & Regan, 2019; Rajappa et al., 2017).

Furthermore, we also found a significant moderate positive correlation in the degree of anterior hyoid excursion during swallows and maximum vocal pitch elevation in older but not younger adults. It has been postulated that the suprahyoid muscles (primarily the geniohyoid) facilitate anterior hyoid excursion during tasks of swallowing (Matsubara et al., 2018; Pearson et al., 2013). The geniohyoid muscle has been shown to play a role in pitch elevation as well (Sapir et al., 1981). Both the geniohyoid and CT muscles undergo significant sarcopenia or age-related muscle atrophy in the elderly (Cobos et al., 2001; Matsubara et al., 2018), which could partially explain this finding. Further research is required to parse out the relative contributions of the suprahyoid versus CT (and pharyngeal) musculature in facilitating anterior hyoid excursion in tasks of maximum vocal pitch elevation and swallowing.

Limitations and Future Directions

This study was a preliminary study designed as a first step for a future clinical trial and, thus, involved a relatively small sample size (10 younger adults and eight older adults). Fortunately, many of the effect sizes were large enough to be found statistically significant. This study also provided us with measures of between-subjects and within-subject variabilities with intraclass correlations ranging between .4 and .5 that can be used for designing our future clinical trial. Furthermore, future studies should include analysis of additional kinematic and morphometric parameters to examine additional potential shared mechanisms between the two functions. For example, exploring kinematic measures of pharyngeal constriction (Schwertner et al., 2016) and general morphometric changes in the pharynx could be of high interest, because recent evidence suggests that the long pharyngeal muscles may also partially contribute to hyoid excursion during swallowing (Pearson et al., 2011). Also, the incorporation of surface electromyography may further shed valuable insight on contributions of the suprahyoid musculature on both tasks of interest. In this study, we did not have the ability to calibrate for dB SPL, which means that our ability to control for loudness was reduced. This should be addressed in future studies, since there is overlap in the underlying biomechanics between frequency and intensity regulation. Finally, in this study, we did not incorporate a target pitch during maximum vocal pitch elevation tasks. That is because regular pitch glides (i.e., highest perceived pitch possible), and not pitch glides with target pitches, are commonly used as therapeutic or evaluation parameters during swallowing management and our aim was to compare the underlying mechanism of this clinical task with the swallowing mechanism. We acknowledge that this may have resulted in varied average maximum fundamental frequency values across age groups and should be considered in future work.

Conclusions

The purpose of this study was to compare hyoid excursion biomechanics between tasks of maximum vocal pitch elevation and swallowing. Superior hyoid excursion was significantly greater during swallowing when compared to vocal pitch elevation in both old and young healthy adults. However, anterior hyoid excursion was similar across both tasks, but overall reduced in the older group. In addition, superior hyoid excursion was moderately positively correlated between swallows and pitch elevation for younger, but not older, adults. Anterior hyoid excursion was moderately positively correlated between swallows and pitch elevation in older, but not younger, adults. Taken together, these findings shed initial insights into the shared and distinct hyoid biomechanics of these two critical aerodigestive tasks and will inform future work on cross-system interactions between these two functions.

Acknowledgments

Funding was provided by an internal departmental grant awarded to the first author in the Department of Speech, Language, and Hearing Sciences at Purdue University. We thank the following individuals for their contributions to data collection and analysis: Nicole DeJong, Mackenzie Zorn, Jennine Bryan, Samantha Mitchell, Paige Cornille, and Cagla Kantarcigil. We also thank our radiology technicians, Maureen Vasquez and Richard Culbertson. We are also grateful to Hilda. S. Ibriga at the Purdue University Statistical Consulting Services who assisted with statistical analysis.

Funding Statement

Funding was provided by an internal departmental grant awarded to the first author in the Department of Speech, Language, and Hearing Sciences at Purdue University. We thank the following individuals for their contributions to data collection and analysis: Nicole DeJong, Mackenzie Zorn, Jennine Bryan, Samantha Mitchell, Paige Cornille, and Cagla Kantarcigil.

References

  1. Belafsky, P. , Postma, G. , & Koufman, J. (2002). Validity and reliability of the reflux symptom index (RSI). Journal of Voice, 16(2), 274–277. https://doi.org/10.1016/S0892-1997(02)00097-8 [DOI] [PubMed] [Google Scholar]
  2. Boersma, P. , & Weenink, D. (2019). Praat: Doing phonetics by computer (Version 6.1) [Computer program] . Retrieved July 25, 2019, from http://www.praat.org/
  3. Brates, D. , Steele, C. M. , & Molfenter, S. M. (2020). Measuring hyoid excursion across the life span: Anatomical scaling to control for variation. Journal of Speech, Language, and Hearing Research, 63(1), 125–134. https://doi.org/10.1044/2019_JSLHR-19-00007 [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carnaby, G. (2012). Food for thought: Importance of a clinical exam/cranial nerve assessment. SIG 13 Perspectives on Swallowing and Swallowing Disorders (Dysphagia), 21(4), 143–149. https://doi.org/10.1044/sasd21.4.143 [Google Scholar]
  5. Cobos, A. R. , Segade, L. A. , & Fuentes, I. (2001). Muscle fibre types in the suprahyoid muscles of the rat. Journal of Anatomy, 198(3), 283–294. https://doi.org/10.1046/j.1469-7580.2001.19830283.x [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Easterling, C. (2008). Does an exercise aimed at improving swallow function have an effect on vocal function in the healthy elderly. Dysphagia, 23(3), 317–326. https://doi.org/10.1007/s00455-008-9158-z [DOI] [PubMed] [Google Scholar]
  7. Erickson, D. M. , Liberman, M. Y. , & Niimi, S. (1976). The geniohyoid and the role of the strap muscles in pitch control. The Journal of the Acoustical Society of America, 60(S1), S63–S63. https://doi.org/10.1121/1.2003454 [Google Scholar]
  8. Fujiki, R. B. , Oliver, A. J. , Malandraki, J. B. , Wetzel, D. , Craig, B. A. , & Malandraki, G. A. (2019). The recline and head lift exercises: A randomized clinical trial comparing biomechanical swallowing outcomes and perceived effort in healthy older adults. Journal of Speech, Language, and Hearing Research, 62(3), 631–643. https://doi.org/10.1044/2018_JSLHR-S-18-0117 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Goy, H. , Fernandes, D. , Pichora-Fuller, M. , & van Lieshout, P. (2013). Normative voice data for younger and older adults. Journal of Voice, 27(5), 545–555. https://doi.org/10.1016/j.jvoice.2013.03.002 [DOI] [PubMed] [Google Scholar]
  10. Honda, K. , Baer, T. , Hirose, H. , & Sawashima, M. (1981). Relationship between vowel articulation and pitch control. The Journal of the Acoustical Society of America, 69(S1), S67–S67. https://doi.org/10.1121/1.386169 [Google Scholar]
  11. Hong, Y. T. , Hong, K. H. , Jun, J.-P. , & Hwang, P. H. (2015). The effects of dynamic laryngeal movements on pitch control. American Journal of Otolaryngology, 36(5), 660–665. https://doi.org/10.1016/j.amjoto.2015.05.002 [DOI] [PubMed] [Google Scholar]
  12. Jacobson, B. , Johnson, A. , Grywalski, C. , Silbergleit, A. , Jacobson, G. , Benninger, M. , & Newman, C. (1997). The Voice Handicap Index (VHI): Development and validation. American Journal of Speech-Language Pathology, 6(3), 66–70. https://doi.org/10.1044/1058-0360.0603.66 [Google Scholar]
  13. Kang, B.-S. , Oh, B.-M. , Kim, I. S. , Chung, S. G. , Kim, S. J. , & Han, T. R. (2010). Influence of aging on movement of the hyoid bone and epiglottis during normal swallowing: A motion analysis. Gerontology, 56(5), 474–482. https://doi.org/10.1159/000274517 [DOI] [PubMed] [Google Scholar]
  14. Kennedy, S. , Pisegna, J. M. , Kim, K. , Parker, L. , & Langmore, S. (2019). The pitch glide speech task lacks clinical utility to infer laryngeal lift during swallowing. International Journal of Speech-Language Pathology. Advance online publication. https://doi.org/10.1080/17549507.2019.1679258 [DOI] [PubMed] [Google Scholar]
  15. Kim, Y. , & McCullough, G. H. (2010). Maximal hyoid excursion in poststroke patients. Dysphagia, 25(1), 20–25. https://doi.org/10.1007/s00455-009-9224-1 [DOI] [PubMed] [Google Scholar]
  16. Koo, T. K. , & Li, M. Y. (2016). A guideline of selecting and reporting intraclass correlation coefficients for reliability research. Journal of Chiropractic Medicine, 15(2), 155–163. https://doi.org/10.1016/j.jcm.2016.02.012 [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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(5), 1264–1274. https://doi.org/10.1044/jslhr.4305.1264 [DOI] [PubMed] [Google Scholar]
  18. Logemann, J. A. , Pauloski, B. R. , Rademaker, A. W. , & Kahrilas, P. J. (2002). Oropharyngeal swallow in younger and older women: Videofluoroscopic analysis. Journal of Speech, Language, and Hearing Research, 45(3), 434–445. https://doi.org/10.1044/1092-4388(2002/034) [DOI] [PubMed] [Google Scholar]
  19. Lortie, C. L. , Thibeault, M. , Guitton, M. J. , & Tremblay, P. (2015). Effects of age on the amplitude, frequency and perceived quality of voice. AGE, 37(6), 117. https://doi.org/10.1007/s11357-015-9854-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lowell, S. Y. , Kelley, R. T. , Colton, R. H. , Smith, P. B. , & Portnoy, J. E. (2012). Position of the hyoid and larynx in people with muscle tension dysphonia. The Laryngoscope, 122(2), 370–377. https://doi.org/10.1002/lary.22482 [DOI] [PubMed] [Google Scholar]
  21. Malandraki, G. A. , Hind, J. A. , Gangnon, R. , Logemann, J. A. , & Robbins, J. (2011). The utility of pitch elevation in the evaluation of oropharyngeal dysphagia: Preliminary findings. American Journal of Speech-Language Pathology, 20(4), 262–268. https://doi.org/10.1044/1058-0360(2011/10-0097) [DOI] [PubMed] [Google Scholar]
  22. Matsubara, M. , Tohara, H. , Hara, K. , Shinozaki, H. , Yamazaki, Y. , Susa, C. , Nakane, A. , Wakasugi, Y. , & Minakuchi, S. (2018). High-speed jaw-opening exercise in training suprahyoid fast-twitch muscle fibers. Clinical Interventions in Aging, 13, 125–131. https://doi.org/10.2147/CIA.S152821 [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mavrea, S. , & Regan, J. (2019). The diagnostic accuracy of the pitch glide to identify aspiration in patients with respiratory diseases: A pilot study. Folia Phoniatrica et Logopaedica: Official Organ of the International Association of Logopedics and Phoniatrics. Advance online publication. https://doi.org/10.1159/000501451 [DOI] [PubMed] [Google Scholar]
  24. McCullough, G. H. , & Martino, R. (2013). Clinical evaluation of patients with dysphagia: Importance of history taking and physical exam. In Shaker, R. , Belafsky, P. , Postma, G. , & Easterling , C. (Eds.), Manual of diagnostic and therapeutic techniques for disorders of deglutition (pp. 11–30). Springer. [Google Scholar]
  25. Miles, A. , Jardine, M. , Johnston, F. , de Lisle, M. , Friary, P. , & Allen, J. (2017). Effect of Lee Silverman Voice Treatment (LSVT LOUD) on swallowing and cough in Parkinson's disease: A pilot study. Journal of the Neurological Sciences, 383, 180–187. https://doi.org/10.1016/j.jns.2017.11.015 [DOI] [PubMed] [Google Scholar]
  26. Miloro, K. V. , Pearson, W. G. , & Langmore, S. E. (2014). Effortful pitch glide: A potential new exercise evaluated by dynamic MRI. Journal of Speech, Language, and Hearing Research, 57(4), 1243–1250. https://doi.org/10.1044/2014_JSLHR-S-13-0168 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Molfenter, S. M. , & Steele, C. M. (2011). Physiological variability in the deglutition literature: Hyoid and laryngeal kinematics. Dysphagia, 26(1), 67–74. https://doi.org/10.1007/s00455-010-9309-x [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Molfenter, S. M. , & Steele, C. M. (2014). Use of an anatomical scalar to control for sex-based size differences in measures of hyoid excursion during swallowing. Journal of Speech, Language, and Hearing Research, 57(3), 768–778. https://doi.org/10.1044/2014_JSLHR-S-13-0152 [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mu, L. , & Sanders, I. (2009). The human cricothyroid muscle: Three muscle bellies and their innervation patterns. Journal of Voice, 23(1), 21–28. https://doi.org/10.1016/j.jvoice.2007.08.001 [DOI] [PubMed] [Google Scholar]
  30. Mulheren, R. W. , Azola, A. M. , Kwiatkowski, S. , Karagiorgos, E. , Humbert, I. , Palmer, J. B. , & González-Fernández, M. (2018). Swallowing changes in community-dwelling older adults. Dysphagia, 33(6), 848–856. https://doi.org/10.1007/s00455-018-9911-x [DOI] [PubMed] [Google Scholar]
  31. Nagy, A. , Molfenter, S. M. , Péladeau-Pigeon, M. , Stokely, S. , & Steele, C. M. (2014). The effect of bolus volume on hyoid kinematics in healthy swallowing. BioMed Research International, 2014, 1–6. https://doi.org/10.1155/2014/738971 [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Nasreddine, Z. S. , Phillips, N. A. , Bédirian, V. , Charbonneau, S. , Whitehead, V. , Collin, I. , Cummings, J. L. , & Chertkow, H. (2005). The Montréal Cognitive Assessment, MoCA: A brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society, 53(4), 695–699. https://doi.org/10.1111/j.1532-5415.2005.53221.x [DOI] [PubMed] [Google Scholar]
  33. Nishida, N. , Taguchi, A. , Motoyoshi, K. , Hyodo, M. , Gyo, K. , & Desaki, J. (2013). Age-related changes in rat intrinsic laryngeal muscles: Analysis of muscle fibers, muscle fiber proteins, and subneural apparatuses. European Archives of Oto-Rhino-Laryngology, 270(3), 975–984. https://doi.org/10.1007/s00405-012-2231-0 [DOI] [PubMed] [Google Scholar]
  34. Pearson, W. G. , Hindson, D. F. , Langmore, S. E. , & Zumwalt, A. C. (2013). Evaluating swallowing muscles essential for hyolaryngeal elevation by using muscle functional magnetic resonance imaging. International Journal of Radiation Oncology, Biology, Physics, 85(3), 735–740. https://doi.org/10.1016/j.ijrobp.2012.07.2370 [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Pearson, W. G. , Langmore, S. E. , & Zumwalt, A. C. (2011). Evaluating the structural properties of suprahyoid muscles and their potential for moving the hyoid. Dysphagia, 26(4), 345–351. https://doi.org/10.1007/s00455-010-9315-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Perlman, A. L. (1996). Neuroanatomy and neurophysiology: Implications for swallowing. Topics in Stroke Rehabilitation, 3(3), 1–13. https://doi.org/10.1080/10749357.1996.11754118 [DOI] [PubMed] [Google Scholar]
  37. Ragland, M. C. , Park, T. , McCullough, G. , & Kim, Y. (2016). The speed of the hyoid excursion in normal swallowing. Clinical Archives of Communication Disorders, 1(1), 30–35. https://doi.org/10.21849/cacd.2016.00010 [Google Scholar]
  38. Rajappa, A. T. , Soriano, K. R. , Ziemer, C. , Troche, M. S. , Malandraki, J. B. , & Malandraki, G. A. (2017). Reduced maximum pitch elevation predicts silent aspiration of small liquid volumes in stroke patients. Frontiers in Neurology, 8, 436. https://doi.org/10.3389/fneur.2017.00436 [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Rasband, W. S. (1997–2018). ImageJ. U.S. National Institutes of Health, Bethesda, MD, United States . https://imagej.nih.gov/ij/
  40. Ren, M. , & Mu, L. (2005). Intrinsic properties of the adult human mylohyoid muscle: Neural organization, fiber-type distribution, and myosin heavy chain expression. Dysphagia, 20(3), 182–194. https://doi.org/10.1007/s00455-005-0015-z [DOI] [PubMed] [Google Scholar]
  41. Sapir, S. , Campbell, C. , & Larson, C. (1981). Effect of geniohyoid, cricothyroid and sternothyroid muscle stimulation on voice fundamental frequency of electrically elicited phonation in rhesus macaque. The Laryngoscope, 91(3), 457–468. https://doi.org/10.1288/00005537-198103000-00017 [DOI] [PubMed] [Google Scholar]
  42. Schwertner, R. W. , Garand, K. L. , & Pearson, W. G., Jr. (2016). A novel imaging analysis method for capturing pharyngeal constriction during swallowing. Journal of Imaging Science, 1(1). [PMC free article] [PubMed] [Google Scholar]
  43. Shipp, T. (1975). Vertical laryngeal position during continuous and discrete vocal frequency change. Journal of Speech and Hearing Research, 18(4), 707–718. https://doi.org/10.1044/jshr.1804.707 [DOI] [PubMed] [Google Scholar]
  44. Steele, C. M. , Bailey, G. L. , Chau, T. , Molfenter, S. M. , Oshalla, M. , Waito, A. A. , & Zoratto, D. C. B. H. (2011). The relationship between hyoid and laryngeal displacement and swallowing impairment. Clinical Otolaryngology, 36(1), 30–36. https://doi.org/10.1111/j.1749-4486.2010.02219.x [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Titze, I. (1989). On the relation between subglottal pressure and fundamental frequency in phonation. The Journal of the Acoustical Society of America, 85(2), 901–906. https://doi.org/10.1121/1.397562 [DOI] [PubMed] [Google Scholar]
  46. Titze, I. (1994). Principles of voice production. Prentice-Hall. [Google Scholar]
  47. Vilkman, E. , Sonninen, A. , Hurme, P. , & Körkkö, P. (1996). External laryngeal frame function in voice production revisited: A review. Journal of Voice: Official Journal of the Voice Foundation, 10(1), 78–92. https://doi.org/10.1016/S0892-1997(96)80021-X [DOI] [PubMed] [Google Scholar]
  48. Zoratto, D. C. B. , Chau, T. , & Steele, C. M. (2010). Hyolaryngeal excursion as the physiological source of swallowing accelerometry signals. Physiological Measurement, 31(6), 843–855. https://doi.org/10.1088/0967-3334/31/6/008 [DOI] [PubMed] [Google Scholar]

Articles from Journal of Speech, Language, and Hearing Research : JSLHR are provided here courtesy of American Speech-Language-Hearing Association

RESOURCES