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Journal of Speech, Language, and Hearing Research : JSLHR logoLink to Journal of Speech, Language, and Hearing Research : JSLHR
. 2023 Feb 13;66(3):863–871. doi: 10.1044/2022_JSLHR-22-00465

The Influence of Sex, Age, and Repeated Measurement on Pixel-Based Measures of Pharyngeal Area at Rest

Sana Smaoui a,b, Renata Mancopes a, Michelle M Simmons a, Melanie Peladeau-Pigeon a, Catriona M Steele a,c,d,
PMCID: PMC10205107  PMID: 36780312

Abstract

Purpose:

Videofluoroscopic (VFSS) measurements of pharyngeal swallow mechanics can differentiate age- and disease-related changes in swallowing. Pharyngeal area at rest (PhAR) may differ in people with dysphagia, although its impact is not clear. Before the role of PhAR in dysphagia can be explored, it is important to establish whether PhAR remains stable across repeated measures in healthy adults, and varies as a function of sex or age. We hypothesized that healthy adults would show stable PhAR across repeated measures, but that larger PhAR would be seen in men versus women and in older versus younger adults.

Method:

We collected VFSS data from 87 healthy adults (44 men, M age = 46 years, range: 21–82). Trained raters identified the swallow rest frame after the initial swallow of each bolus and measured unobliterated pharyngeal area on these frames, in %(C2–4)2 units. Repeated-measures analyses of variance with a factor of sex, a covariate of age, and a repeated factor of task repetition were performed across the first 12 available measures per participant (N = 1,044 swallows).

Results:

There were no significant variations in PhAR across repeated measures. A significant Sex × Age interaction was seen (p = .04): Males had significantly larger PhAR than females (p = .001), but females showed larger PhAR with advancing age (R = .47).

Conclusions:

These data confirm stability in PhAR across repeated measurements in healthy individuals. However, significant sex and age differences should be taken into consideration in future studies exploring the role of PhAR in people with dysphagia.

Supplemental Material:

https://doi.org/10.23641/asha.22043543


During swallowing, both the longitudinal and laterally oriented constrictor muscles of the pharynx contract, creating a high pressure zone that facilitates bolus movement and clearance through the pharyngoesophageal segment into the esophagus (Hoffman et al., 2010; Kahrilas et al., 1992; Leonard et al., 2006). Impairment in pharyngeal constriction has become a focus in recent literature, with metrics capturing either the degree to which the pharynx remains partially constricted (Steele et al., 2019; Stokely et al., 2015; Waito et al., 2018), or expressing the two-dimensional lateral area of the unobliterated pharynx relative to the area of the pharynx at rest (i.e., the pharyngeal constriction ratio or PCR; Kendall & Leonard, 2001; Leonard et al., 2006, 2011). This latter approach has drawn attention to the fact that pharyngeal volume, represented by the proxy measurement of two-dimensional lateral view area, may change as a function of disease or senescence. Smaller pharyngeal area may be expected in the context of postsurgical or postradiation edema, whereas larger area may be expected with age-related changes in muscle bulk (Aminpour et al., 2011; Kendall & Leonard, 2001; Molfenter et al., 2015, 2019) or in clinical conditions involving pharyngeal muscle atrophy. Although the impact of differences in pharyngeal area at rest on pharyngeal constriction or bolus clearance remain unclear, one study by Molfenter et al. (2019) reported a significant relationship between age-related increases in pharyngeal volume as measured with acoustic pharyngometry, and videofluoroscopic findings of poor pharyngeal constriction and vallecular residue.

Pixel-based measurements of the two-dimensional area of the pharynx, the bolus, or of pharyngeal residue are recommended in several approaches to quantitative analysis of pharyngeal swallowing on lateral view videofluoroscopy (Kendall & Leonard, 2001; Leonard, 2010, 2019; Leonard et al., 2006, 2011; Molfenter & Steele, 2014; Steele et al., 2019, 2020). While some of these area-based parameters are known to vary as a function of bolus volume or consistency (Steele et al., 2019), pharyngeal area at rest (henceforth, PhAR) is a parameter that should remain stable within a participant across repeated measurement, provided that a standard method of selecting a representative rest frame is clearly described. The aim of this study was to confirm this hypothesis by exploring within-participant variations across measures of PhAR.

Two known sources of between-participants variation in measures of pharyngeal area are sex and age. As a rule, the size of the neck (and, therefore, the pharynx) is known to be larger in males than females, with the source of this variation attributed to height (Molfenter & Steele, 2014). To correct for this difference, several studies have recommended normalizing two-dimensional area measures of the pharynx or of bolus area to an anatomical reference scalar defined as the squared length of the C2–C4 cervical spine (Brates et al., 2020; Molfenter & Steele, 2014; Steele et al., 2019, 2020). Although this normalization method neutralizes sex-associated height differences in pixel-based measures of hyoid movement (Brates et al., 2020), our previous work suggests that spine-referenced measures of pharyngeal area at rest may continue to show larger values in males (Mancopes et al., 2021). Previous studies using MRI, acoustic pharyngometry, and videofluorocopy suggest that there may be age-related atrophy of the pharyngeal musculature leading to dilation of the pharyngeal airspace and larger two-dimensional area at rest (Aminpour et al., 2011; Kendall & Leonard, 2001; Molfenter et al., 2015, 2019).

A key source of potential within-participant variability in image-based measures of PhAR lies in selection of the swallow rest frame, which is not a trivial matter. In some studies, such as those of Leonard and colleagues leading to development of the PCR measure, a preswallow bolus-hold position with a standard volume of thin liquid barium has been used (Leonard et al., 2004, 2006, 2011). In other studies, the frame selected for PhAR measures, as well as measures of lowest hyoid position and residue has been a postswallow rest frame (e.g., Molfenter & Steele, 2014; Stokely et al., 2015). This has been the tradition in our lab, where we typically collect data for noncued swallows (i.e., without a bolus hold). We use an operational definition for the “swallow rest” frame as the first frame at the end of the initial swallow of a bolus (regardless of bolus type or volume), showing the pyriform sinuses at their lowest position, relative to the spine, within 30 frames (approx. 1 s) of upper esophageal sphincter (UES) closure (Steele et al., 2019). This definition is further qualified by requirements that the selected swallow rest frame must occur before the end of the fluoroscopy clip or recording, before onset of the hyoid burst for a subsequent swallow, and before nonswallow events such as coughing, talking, or UES reopening. In cases where UES closure cannot be confirmed, the swallow rest frame must be chosen within 30 frames following the first frame of pharyngeal relaxation (Steele et al., 2019). Using this approach to identifying frames of postswallow rest state, our research questions for this study were as follows:

  • 1)  What is the range of PhAR measures seen in a population of adults without dysphagia?

  • 2)  Are there significant sex differences in measures of PhAR?

  • 3)  How much variation in measures of PhAR is explained by age?

  • 4)  Do measures of PhAR show significant variation across repeated measures?

In addition to our hypothesis that PhAR would remain stable across repeated measures, we hypothesized that PhAR would be larger in males than females and would increase with age.

Method

Data Collection

These data were collected as part of a larger project exploring quantitative measures of swallowing from videofluoroscopy in adults without dysphagia (henceforth called “healthy adults”; Steele et al., 2019). Human subjects approval was obtained from the University Health Network Research Ethics Board (CAPCR #15–9431). Community dwelling adult volunteers were recruited to participate in the study. Telephone screening was completed prior to enrolment in the study to confirm absence of the following: history of dysphagia; neurological difficulties or diseases; self-reported difficulties with swallowing, taste, or smell; history of major surgery to the head, neck, or mouth (other than tonsillectomy, adenoidectomy, or routine dental procedures); history of head and neck cancer; history of X-ray to the neck in the past 6 months (other than routine dental X-ray); allergy to latex; and current pregnancy. Participants who met the eligibility criteria then attended a session with study staff where the study procedures were reviewed before signing informed consent and proceeding to a videofluoroscopic swallow study (VFSS).

Videofluoroscopy

Across the course of the larger project, there were two different VFSS protocols, denoted here as VFSS A (May 2016 to December 2019) and VFSS B (January, 2020 to October, 2021). VFSS A involved a series of 27 boluses of 20% w/v barium (Bracco E-Z-Paque powder), prepared in five consistencies (thin, slightly thick, mildly thick, moderately thick, and extremely thick liquids) according to the definitions of the International Dysphagia Diet Standardization Initiative (IDDSI; Barbon & Steele, 2019). Two different thickeners were used, one starch based and one xanthan gum based (Resource ThickenUp and Resource ThickenUp Clear, both sourced from Nestlé Health Science). Participants were instructed to self-administer all boluses using naturally sized sips or teaspoon amounts and to swallow when ready, without a cue. All stimuli were served in 40-ml volumes in 120-ml capacity styrofoam cups. Administration method was determined based on the thickness of the consistency used: Thin, slightly thick, and mildly thick, liquids were taken by comfortable sip, whereas moderately and extremely thick liquids were taken by teaspoons. To control for possible order effects relative to thickener type, participants were randomly assigned to one of two bolus administration sequences, beginning with three naturally sized sips of thin liquid barium, followed by blocks of three boluses of the thicker stimuli, arranged by increasing consistency from slightly thick to extremely thick, and with the order of thickener type within consistency differing (i.e., starch preceding xanthan gum, or vice versa).

VFSS B was designed as a follow-up experiment to probe a variety of bolus conditions beyond those included in VFSS A and comprised 22 bolus swallows including:

  • a)  comfortable noncued sips of thin liquid barium prepared using different barium products (Bracco E-Z-HD in 20% w/v concentration, and Bracco E-Z-Paque powder and Bracco Polibar Plus liquid suspension in 20% and 40% w/v concentrations). Two boluses of each stimulus were taken, served in 40-ml volumes in 120-ml capacity styrofoam cups (Steele et al., 2022);

  • b)  two boluses of teaspoon-administered 20% w/v mildly thick barium prepared using Bracco E-Z-Paque powder and thickened with Nestlé Resource ThickenUp Clear; and

  • c)  two boluses each of solid foods prepared to represent IDDSI Level 5 Minced and Moist, Level 6 Soft and Bite-sized, and Level 7 Regular consistencies. The recipes used for preparing these barium stimuli are included in Supplemental Material S1.

As with VFSS A, participants who completed the VFSS B protocol were randomly assigned to one of two bolus administration sequences to control for possible order effects relative to thickener type. All videofluoroscopies for both the VFSS A and VFSS B protocols were performed at 30 pulses per second and recorded at 30 frames per second for post hoc analysis and rating.

Data Processing and Rating

Full-length VFSS recordings were spliced to produce a series of single bolus clips for each participant and stripped of audio to remove any information that might bias raters. These bolus clips were then randomized and assigned for duplicate blinded rating by trained raters using the ASPEKT Method (Steele et al., 2019). This method has been described in detail elsewhere (Steele et al., 2019) and includes a process of frame identification for key events, including the swallow rest frame for every swallow in each bolus clip. Interrater agreement for frame selection is inspected (and interrater agreement statistics are calculated) across duplicate blinded ratings. Discrepancies in frame selection are then resolved before proceeding to pixel-based measurement. For the frame of swallow rest, any discrepancies greater than five frames across duplicate ratings were flagged and sent to a consensus meeting for resolution. Where rater differences in frame selection were smaller than five frames, the later frame was selected as the frame of record. Pixel-based measures of pharyngeal area were then performed on the swallow rest frames after the initial swallow for each bolus using ImageJ software as follows:

  • 1)  Raters used the ImageJ line tool to draw and measure the C2–C4 reference scalar length, defined as the distance (in pixels) between the anterior–inferior corners of the C2 and C4 vertebrae (see Figure 1A).

  • 2)  A second line, perpendicular to the first was then drawn using the ImageJ angle tool (see Figure 1B) and moved upward, to align with the anterior–superior corner of the C2 vertebra (see Figure 1C).

  • 3)  The area tool of ImageJ was then used to trace unobliterated pharyngeal space (including both air and any visible bolus material) between the following boundaries: superiorly, the top of the C2 vertebra; posteriorly, the posterior pharyngeal wall; inferiorly, the pit of the pyriform sinuses; and anteriorly, the base of tongue, pharyngeal surface of the epiglottis, aryepiglottic folds, and anterior wall of the pyriform sinus (see Figure 1D).

  • 4)  The pharyngeal area measure in pixels was converted into %(C2–4)2 units by dividing the area measure by the (C2–4)2 reference scalar and multiplying by 100%.

Figure 1.

Figure 1.

Stepwise illustration of the method for tracing pharyngeal area at rest (PhAR) in ImageJ software: (A) The line tool is used to trace and measure the length of the C2–4 reference scalar, in pixels; (B) the angle tool is used to draw a line perpendicular to the C2–4 reference scalar; (C) this perpendicular line is moved up to align with the bottom of the C2 vertebra to serve as the upper boundary for pharyngeal area tracing; (D) the area tool is traced between the boundaries of the top of the C2 vertebra superiorly; posteriorly, the posterior pharyngeal wall; inferiorly, the pit of the pyriform sinuses; and anteriorly, the base of tongue, pharyngeal surface of the epiglottis, aryepiglottic folds, and anterior wall of the pyriform sinus. The pixel-based measures of pharyngeal area and reference scalar length are then entered into the equation shown on the right, to yield an anatomically scaled measure of PhAR in %(C2–4)2 units.

Pixel-tracing of pharyngeal area was completed in duplicate, and interrater agreement statistics were calculated on the blinded ratings. Due to the fact that PhAR is calculated as an equation involving two steps in pixel-tracing (i.e., pharyngeal area and the cervical spine scalar), our experience is that interrater differences can be quite large. In order to determine measures of record for use in subsequent analysis, we select thresholds for discrepancy resolution with the intent of reviewing at least the top 10% of the discrepancy distribution based on prior projects in our lab. Using this approach, PhAR discrepancies greater than 20%(C2–4)2 were resolved by consensus. Below this threshold, the smaller value was taken as the rating of record.

Statistical Analyses

The number and types of swallowing tasks differed between the VFSS A and VFSS B protocols. Additionally, measures of PhAR could not be made for some participants on some tasks due to image quality concerns such as interference from shoulder shadows. Across the available data, the minimum number of postswallow PhAR measures available for each participant was 12; we, therefore, decided to explore our questions regarding variations in measures of PhAR using the first 12 available measures per participant. Given our hypothesis that PhAR would remain stable across repeated measures, we did not factor bolus type into the analysis. Interrater reliability for preconsensus identification of frame of PhAR was inspected using measures of % absolute agreement, mean absolute difference, and the frequency of discrepancies > 5 frames. For pixel-based measures of pharyngeal area and C2–4 scalar length, we calculated intraclass correlations, using a mean-rating (k = 2) two-way mixed effects model for consistency (Koo & Li, 2016). Descriptive statistics for all variables were calculated (range, median, and percentile values). A general linear model repeated-measures analysis of variance (ANOVA) was used to study variations in continuous parameter data with post hoc Sidak tests for pairwise comparisons, and post hoc Pillai's trace to evaluate the multivariate effect of task repetition. The model included a factor of sex, a covariate of age, and a repeated factor of task repetition. Alpha level for all statistical analyses was set at .05. Post hoc Cohen's d measures were calculated to determine effect size for statistically significant sex differences (Kotrlik & Williams, 2003). To further explore the magnitude of age effects, we performed post hoc Spearman correlations using each participant's median PhAR measure, both overall and within sex group.

Results

Participants

In total, the data for this analysis came from 87 healthy adults (44 men). Of these, 68 (33 men, 35 women) aged 21–82 years (M age = 50 years) completed VFSS A. The remaining 19 participants completed VFSS B and comprised nine women and 10 men, aged 22–54 years (M age = 28). Overall, the study sample mean age was 46 years (range: 21–82 years). With respect to racial distribution, the sample included 17 people of Asian descent, five people of African/Afro-American descent, one person of North American indigenous descent, and one Pacific Islander; the remaining 63 participants were White. Three participants reported Hispanic ethnicity.

Interrater Reliability

Preconsensus, 70% of the ratings for swallow rest frame identification showed discrepancies of five frames or less across raters. This translated to an intraclass correlation of 0.946 (95% confidence interval [.94, .95]). Pixel-based measures of PhAR showed a preconsensus intraclass correlation of .864 (95% confidence interval [.85, .88]) with 66% of ratings showing a discrepancy of 10%(C2–4)2 or less.

Range of PhAR Values

The first 12 available PhAR measures per participant were included in the analysis, regardless of bolus type, forming a total dataset of 1,044 swallows. Overall, measures of PhAR ranged from 25% to 135% of the C2–42 reference scalar in this sample. Mean PhAR was 62% C2–42 (Mdn = 60%; interquartile range: 49%–73%).

Between-Participants Effects

The repeated-measures ANOVAs identified significant main effects of sex and age, and a significant Sex × Age interaction, F(1, 83) = 4.45, p = .04. Significantly larger PhAR with a medium effect size was found in males compared with females, F(1, 83) = 11.38, p = .001, Cohen's d = .48. A significant covariate effect but only a small positive correlation was seen between age and PhAR, F(1, 83) = 5.67, p = .02, R 2 = .01, R = .11. The significant Sex × Age interaction took the form of a larger sex difference in younger participants, as illustrated in Figure 2, which plots each participant's median PhAR across the 12 repeated measurements as a function of age, with separate symbols for males and females. Overall, the relationship between participant median PhAR and age showed a weak Spearman correlation of ρ = .24, p = .03. When this analysis was performed within sex group, the females showed a significant relationship with age (ρ = .47, p = .002) that was not present in the male data (ρ = .06, p = .68).

Figure 2.

Figure 2.

Scatter plot of participant median values for pharyngeal area at rest (PhAR) in %(C2–4)2 units, across the 12 repeated measurements, with data for male participants shown in black and data for female participants shown in gray. Trend lines for the relationship between age and PhAR are shown by sex: for males (in black) ρ = .06; for females (in gray) ρ = .47.

Within-Participant Effects

The magnitude of within-participant variation between minimum and maximum PhAR measures across the 12 repeated boluses ranged from 12% to 83% (C2–4)2, with a mean value of 30% (C2–4)2 (SD = 12%). The repeated-measures ANOVA found no significant effect of task repetition on PhAR: Pillai's trace, F(11, 73) = 1.53, p = .14. This is illustrated in Figure 3.

Figure 3.

Figure 3.

Box plots for pharyngeal area at rest (PhAR) in %(C2–4)2 units, across the first 12 boluses for each participant. The overall median, that is, 60% (C2–4)2, and boundaries of the interquartile range, that is, 49%–73% (C2–4)2, are shown by the solid and dashed black lines, respectively.

Discussion

The primary goal of this study was to explore the stability (or degree of variation) seen in pixel-based measures of PhAR across repeated measurements in healthy adults, with those PhAR measures taken at the end of the initial swallow of a variety of different boluses. Measures of pharyngeal area, both at rest and at maximum constriction, may help us to understand the mechanisms behind swallowing impairment, and particularly behind pharyngeal residue (Stokely et al., 2015; Waito et al., 2018). The literature suggests that pharyngeal area measurements vary between healthy individuals and those with dysphagia (Kendall & Leonard, 2001; Leonard et al., 2006, 2011). It is also thought that the natural aging process may lead to muscle atrophy in healthy older individuals, with resulting dilation or enlargement of pharyngeal lumen area (Aminpour et al., 2011; Kendall & Leonard, 2001; Molfenter et al., 2015 , 2019). In this study of healthy adults aged 21–82 years, we expected to see larger PhAR in males compared with females and larger PhAR measures in older participants, but a lack of significant variation in PhAR across repeated measures within individual participants. The results confirm our primary expectation that a single measure of PhAR during a videofluoroscopy can be considered representative, without the need to expressly explore variations in PhAR across different swallowing tasks. The results also supported our hypothesis of larger PhAR measures in males. However, the predicted finding of increasing PhAR as a function of advancing age was only seen in the female participants.

One finding that deserves discussion is the fact that sex differences, with larger PhAR in males, were found in this study, despite the use of C2–C4 scalar normalization. Although previous studies have shown that this normalization method corrects for sex differences in participant height and neck length (Molfenter & Steele, 2014), the current data suggest that there are additional sex-based variations in pharyngeal dimensions. These may include variations in lateral view measures of lumen width and possibly differences in pharyngeal circumference and muscle mass-related measures of pharyngeal wall thickness, all of which could impact measures of pharyngeal area.

It is challenging to draw direct comparisons of PhAR measures across different studies in the literature, due to differences in the operational definitions of rest frame used, and differences in the methods and units of measurement reported. Additionally, it should be noted that the literature to date has paid more attention to measures of pharyngeal area at maximum constriction than it has to area at rest. As mentioned previously, Leonard and colleagues have reported measures of unconstricted pharyngeal area using a standardized context of a 1-ml bolus hold as a proxy for rest (Leonard, 2010; Leonard et al., 2004, 2006, 2011), and taken once at the beginning of their videofluoroscopy protocol. Their measures of pharyngeal constriction have been reported in metric units, and also as a ratio (%) of area during bolus hold, which cannot be directly compared with the spine-referenced area measures reported in this article. A further difference in methods between the studies of Leonard and colleagues and other methods is the fact that the region anterior to the laryngeal aditus/aryepiglottic fold is included in the pharyngeal area tracings used by the Leonard group, but excluded in our method. In previous work from our lab, we defined the rest frame as “the earliest frame following upper esophageal sphincter closure when the hyoid was observed to have descended and moved posteriorly to reach its original, preswallow position” (Stokely et al., 2015). In that study, we pooled data across 20 healthy adults under age 40 years and a clinical sample of 40 adults with suspected neurogenic dysphagia. For swallows displaying good bolus clearance and an absence of residue of concern, mean PhAR was 67% (C2–4)2, with a 95% confidence interval from 63% to 72%. The values seen in the current analysis are similar in magnitude and dispersion.

Despite a lack of statistically significant variation across repeated measures of PhAR, it should be noted that the range of measures depicted in Figure 3 is still quite large, spanning 25%–135% of the (C2–4)2 area with an interquartile range of 49%–73%. There are a number of possible sources of this variation. First, although we adopted a standard operational definition for the swallow rest frame, we acknowledge that the degree of pharyngeal relaxation seen at the end of an initial swallow may differ between scenarios where that initial swallow is the only swallow for a bolus (and, therefore, both the initial and the terminal swallow) and those that are followed by subsequent clearing swallows. In this study, we chose not to factor the type of bolus into the analysis, and also did not classify observations as coming from the initial swallow of single versus multiple swallow sequences. Incorporating these details into future studies may help to further narrow the variation seen in healthy measures of PhAR and inform the selection of a standard context to use for PhAR measurement. Similarly, in determining the ideal context for PhAR measurement, it would be interesting to compare postswallow measures to static measures taken either prior to any bolus administration or adopting the convention of a 1-ml bolus hold (Kendall & Leonard, 2001; Leonard et al., 2004, 2006, 2011). Additionally, given that altered head positions such as the chin down posture are described to narrow the pharyngeal lumen (Shanahan et al., 1993), quantifying the degree of variation in PhAR attributable to different static head positions would be of interest.

To date, there is very little evidence to illustrate whether or not differences in PhAR exist in people with dysphagia or impact swallowing in a predictable way. Molfenter et al. (2019) identified poor pharyngeal constriction and worse vallecular residue in older adults with larger pharyngeal volume, based on acoustic pharyngometry. However, whether enlarged pharyngeal area at rest predicts worse constriction or bolus clearance remains to be confirmed. It is also possible that individuals with unusually small pharyngeal area, secondary to post-surgical edema or to radiation treatment, might display difficulties with pharyngeal motility and bolus clearance. These relationships require further study. The current data do, however, provide a foundation for studying within-participant changes in measures of PhAR over time, such as those that may develop as a consequence of surgery, radiation, or neurodegenerative disease, or as an outcome of interventions intended to limit or reverse atrophy.

Limitations

This study is not without limitations. Although correlations with age are included in the analysis, we acknowledge that we did not purposefully recruit equal numbers of participants for decade or other age-bins across the range studied. Consequently, as seen in Figure 2, there is a relative sparsity of data for participants aged 40–60 years in this sample, compared with ages below 40 years and above 60 years. For this reason, we chose to use Spearman rather than Pearson correlations for post hoc exploration of age effects. It should also be noted that the mean age and age range of participants who completed VFSS Protocol B was lower than that of the larger sample who completed VFSS Protocol A.

Further issues that need to be acknowledged and considered in future research studies include the lack of normalization for factors other than cervical spine length, and the impact of aging on the C2–4 cervical spine scalar used for normalizing measures of PhAR. Aging has been shown to influence spinal morphology, with known changes in cervical spine curvature, cervical disc degeneration, vertebral body height changes, and osteophytes (Benoist, 2003; Brates et al., 2020; Ezra et al., 2017; Fujimori et al., 2017; Malcolm, 2002; Nojiri et al., 2003; Resnick, 1985; Swann, 2009). These changes in the spine may alter the length of the C2–4 scalar, therefore creating false impressions of changes in PhAR due to changes in the denominator of the normalization equation. The most likely change in this regard is that the length of the cervical spine scalar will be smaller in older people, thereby contributing to apparently larger measures of parameters like pharyngeal area (Brates et al., 2020). Therefore, we cannot definitely rule out the possibility that the larger pharyngeal area measures seen in the older participants in our study reflect some degree of inflation related to age-related cervical spine changes.

Conclusions

In conclusion, these data confirm our hypothesis that measures of pharyngeal area at rest, taken on the frame of swallow rest at the end of the initial swallow for a bolus, show stability across repeated measurements (i.e., boluses) within the same individual. The data also show significant sex differences in PhAR, with larger measures in males, and an age-related increase in pharyngeal area in females. These results identify factors that require experimental control in future studies of PhAR and the implications of variations in PhAR for pharyngeal constriction and bolus clearance in people with dysphagia.

Data Availability Statement

Additional data are available on request from the authors.

Supplementary Material

Supplemental Material S1. Recipes for radio-opaque food stimuli used in VFSS B.

Acknowledgments

Funding for this project was provided from the National Institute on Deafness and Other Communication Disorders (grant R01DC011020) to Catriona M. Steele. The authors also gratefully acknowledge assistance from Emily Barrett, Kristyn Emmerzael, Pooja Gandhi, Vanessa Panes, Todd Reesor, and Danielle Sutton with data collection and videofluoroscopy rating.

Funding Statement

Funding for this project was provided from the National Institute on Deafness and Other Communication Disorders (grant R01DC011020) to Catriona M. Steele. The authors also gratefully acknowledge assistance from Emily Barrett, Kristyn Emmerzael, Pooja Gandhi, Vanessa Panes, Todd Reesor, and Danielle Sutton with data collection and videofluoroscopy rating.

References

  1. Aminpour, S. , Leonard, R. , Fuller, S. C. , & Belafsky, P. C. (2011). Pharyngeal wall differences between normal younger and older adults. Ear, Nose & Throat Journal, 90(4), E1. https://doi.org/10.1177/014556131109000412 [DOI] [PubMed] [Google Scholar]
  2. Barbon, C. E. A. , & Steele, C. M. (2019). Characterizing the flow of thickened barium and non-barium liquid recipes using the IDDSI flow test. Dysphagia, 34(1), 73–79. https://doi.org/10.1007/s00455-018-9915-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benoist, M. (2003). Natural history of the aging spine. European Spine Journal, 12(0), S86–S89. https://doi.org/10.1007/s00586-003-0593-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Ezra, D. , Masharawi, Y. , Salame, K. , Slon, V. , Alperovitch-Najenson, D. , & Hershkovitz, I. (2017). Demographic aspects in cervical vertebral bodies' size and shape (C3-C7): A skeletal study. The Spine Journal, 17(1), 135–142. https://doi.org/10.1016/j.spinee.2016.08.022 [DOI] [PubMed] [Google Scholar]
  6. Fujimori, T. , Le, H. , Schairer, W. , Inoue, S. , Iwasaki, M. , Oda, T. , & Hu, S. S. (2017). The relationship between cervical degeneration and global spinal alignment in patients with adult spinal deformity. Clinical Spine Surgery, 30(4), E423–E429. https://doi.org/10.1097/BSD.0000000000000327 [DOI] [PubMed] [Google Scholar]
  7. Hoffman, M. R. , Ciucci, M. R. , Mielens, J. D. , Jiang, J. J. , & McCulloch, T. M. (2010). Pharyngeal swallow adaptations to bolus volume measured with high-resolution manometry. The Laryngoscope, 120(12), 2367–2373. https://doi.org/10.1002/lary.21150 [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kahrilas, P. J. , Logemann, J. A. , Lin, S. , & Ergun, G. A. (1992). Pharyngeal clearance during swallowing: A combined manometric and videofluoroscopic study. Gastroenterology, 103(1), 128–136. https://doi.org/10.1016/0016-5085(92)91105-D [DOI] [PubMed] [Google Scholar]
  9. Kendall, K. A. , & Leonard, R. J. (2001). Pharyngeal constriction in elderly dysphagic patients compared with young and elderly nondysphagic controls. Dysphagia, 16(4), 272–278. https://doi.org/10.1007/s00455-001-0086-4 [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Kotrlik, J. W. , & Williams, H. A. (2003). The incorporation of effect size in information technology, learning, and performance research. Information Technology, Learning, and Performance Journal, 21(1), 1–7. [Google Scholar]
  12. Leonard, R. (2010). Swallowing in the elderly: Evidence from fluoroscopy. SIG 13 Perspectives on Swallowing and Swallowing Disorders (Dysphagia), 19(4), 103–114. https://doi.org/10.1044/sasd19.4.103 [Google Scholar]
  13. Leonard, R. (2019). Predicting aspiration risk in patients with dysphagia: Evidence from fluoroscopy. Laryngoscope Investigative Otolaryngology, 4(1), 83–88. https://doi.org/10.1002/lio2.226 [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Leonard, R. , Belafsky, P. C. , & Rees, C. J. (2006). Relationship between fluoroscopic and manometric measures of pharyngeal constriction: The pharyngeal constriction ratio. Annals of Otology, Rhinology & Laryngology, 115(12), 897–901. https://doi.org/10.1177/000348940611501207 [DOI] [PubMed] [Google Scholar]
  15. Leonard, R. , Kendall, K. A. , & McKenzie, S. (2004). Structural displacements affecting pharyngeal constriction in nondysphagic elderly and nonelderly adults. Dysphagia, 19(2), 133–141. https://doi.org/10.1007/s00455-003-0508-6 [DOI] [PubMed] [Google Scholar]
  16. Leonard, R. , Rees, C. J. , Belafsky, P. , & Allen, J. (2011). Fluoroscopic surrogate for pharyngeal strength: The Pharyngeal Constriction Ratio (PCR). Dysphagia, 26(1), 13–17. https://doi.org/10.1007/s00455-009-9258-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Malcolm, G. P. (2002). Surgical disorders of the cervical spine: Presentation and management of common disorders. Journal of Neurology, Neurosurgery, & Psychiatry, 73(Suppl. 1), i34–i41. https://doi.org/10.1136/jnnp.73.suppl_1.i34 [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mancopes, R. , Gandhi, P. , Smaoui, S. , & Steele, C. M. (2021). Which physiological swallowing parameters change with healthy aging? OBM Geriatrics, 5(1). https://doi.org/10.21926/obm.geriatr.2101153 [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Molfenter, S. M. , Amin, M. R. , Branski, R. C. , Brumm, J. D. , Hagiwara, M. , Roof, S. A. , & Lazarus, C. L. (2015). Age-related changes in pharyngeal lumen size: A retrospective MRI analysis. Dysphagia, 30(3), 321–327. https://doi.org/10.1007/s00455-015-9602-9 [DOI] [PubMed] [Google Scholar]
  20. Molfenter, S. M. , Lenell, C. , & Lazarus, C. L. (2019). Volumetric changes to the pharynx in healthy aging: Consequence for pharyngeal swallow mechanics and function. Dysphagia, 34(1), 129–137. https://doi.org/10.1007/s00455-018-9924-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Nojiri, K. , Matsumoto, M. , Chiba, K. , Maruiwa, H. , Nakamura, M. , Nishizawa, T. , & Toyama, Y. (2003). Relationship between alignment of upper and lower cervical spine in asymptomatic individuals. Journal of Neurosurgery: Spine, 99(1), 80–83. https://doi.org/10.3171/spi.2003.99.1.0080 [DOI] [PubMed] [Google Scholar]
  23. Resnick, D. (1985). Degenerative diseases of the vertebral column. Radiology, 156(1), 3–14. https://doi.org/10.1148/radiology.156.1.3923556 [DOI] [PubMed] [Google Scholar]
  24. Shanahan, T. K. , Logemann, J. A. , Rademaker, A. W. , Pauloski, B. R. , & Kahrilas, P. J. (1993). Chin-down posture effect on aspiration in dysphagic patients. Archives of Physical Medicine and Rehabilitation, 74(7), 736–739. https://doi.org/10.1016/0003-9993(93)90035-9 [DOI] [PubMed] [Google Scholar]
  25. Steele, C. M. , Barrett, E. , & Peladeau-Pigeon, M. (2022). Which videofluoroscopy parameters are susceptible to the influence of differences in barium product and concentration? American Journal of Speech-Language Pathology, 31(5), 2145–2158. https://doi.org/10.1044/2022_AJSLP-22-00017 [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Steele, C. M. , Peladeau-Pigeon, M. , Barbon, C. A. E. , Guida, B. T. , Namasivayam-MacDonald, A. M. , Nascimento, W. V. , Smaoui, S. , Tapson, M. S. , Valenzano, T. J. , Waito, A. A. , & Wolkin, T. S. (2019). Reference values for healthy swallowing across the range from thin to extremely thick liquids. Journal of Speech, Language, and Hearing Research, 62(5), 1338–1363. https://doi.org/10.1044/2019_JSLHR-S-18-0448 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Steele, C. M. , Peladeau-Pigeon, M. , Nagy, A. , & Waito, A. A. (2020). Measurement of pharyngeal residue from lateral view videofluoroscopic images. Journal of Speech, Language, and Hearing Research, 63(5), 1404–1415. https://doi.org/10.1044/2020_JSLHR-19-00314 [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Stokely, S. L. , Peladeau-Pigeon, M. , Leigh, C. , Molfenter, S. M. , & Steele, C. M. (2015). The relationship between pharyngeal constriction and post-swallow residue. Dysphagia, 30(3), 349–356. https://doi.org/10.1007/s00455-015-9606-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Swann, J. (2009). Cervical spondylosis part 1: Osteoarthritis of the cervical spine. British Journal of Healthcare Assistants, 3(2), 81–84. https://doi.org/10.12968/bjha.2009.3.2.39392 [Google Scholar]
  30. Waito, A. A. , Tabor-Gray, L. C. , Steele, C. M. , & Plowman, E. K. (2018). Reduced pharyngeal constriction is associated with impaired swallowing efficiency in amyotrophic lateral sclerosis (ALS). Neurogastroenterology & Motility, 30(12), Article e13450. https://doi.org/10.1111/nmo.13450 [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplemental Material S1. Recipes for radio-opaque food stimuli used in VFSS B.

Data Availability Statement

Additional data are available on request from the authors.


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