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Journal of Clinical Sleep Medicine : JCSM : Official Publication of the American Academy of Sleep Medicine logoLink to Journal of Clinical Sleep Medicine : JCSM : Official Publication of the American Academy of Sleep Medicine
. 2021 Sep 1;17(9):1793–1803. doi: 10.5664/jcsm.9286

Altered swallowing biomechanics in people with moderate-severe obstructive sleep apnea

Mistyka S Schar 1,2,✉, Taher I Omari 2, Charmaine M Woods 2,3, Lara F Ferris 4, Sebastian H Doeltgen 4, Kurt Lushington 5, Anna Kontos 6, Theodore Athanasiadis 2,3, Charles Cock 2,7, Ching-Li Chai Coetzer 8,9, Danny J Eckert 9, Eng H Ooi 2,3
PMCID: PMC8636337  PMID: 33904392

Abstract

Study Objectives:

Dysphagia is a common but under-recognized complication of obstructive sleep apnea (OSA). However, the mechanisms remain poorly described. Accordingly, the aim of this study was to assess swallowing symptoms and use high-resolution pharyngeal manometry to quantify swallowing biomechanics in patients with moderate-severe OSA.

Methods:

Nineteen adults (4 female; mean (range) age, 46 ± 26-68 years) with moderate-severe OSA underwent high-resolution pharyngeal manometry testing with 5-, 10-, and 20-mL volumes of thin and extremely thick liquids. Data were compared with 19 age- and sex-matched healthy controls (mean (range) age, 46 ± 27-68 years). Symptomatic dysphagia was assessed using the Sydney Swallow Questionnaire. Swallow metrics were analyzed using the online application swallowgateway.com. General linear mixed model analysis was performed to investigate potential differences between people with moderate-severe OSA and controls. Data presented are means [95% confidence intervals].

Results:

Twenty-six percent (5 of 19) of the OSA group but none of the controls reported symptomatic dysphagia (Sydney Swallow Questionnaire > 234). Compared with healthy controls, the OSA group had increased upper esophageal sphincter relaxation pressure (−2 [−1] vs 2 [1] mm Hg, F = 32.1, P < .0001), reduced upper esophageal sphincter opening (6 vs 5 mS, F = 23.6, P < .0001), and increased hypopharyngeal intrabolus pressure (2 [1] vs 7 [1] mm Hg, F = 19.0, P < .05). Additionally, upper pharyngeal pressures were higher, particularly at the velopharynx (88 [12] vs 144 [12] mm Hg⋅cm⋅s, F = 69.6, P < .0001).

Conclusions:

High-resolution pharyngeal manometry identified altered swallowing biomechanics in people with moderate-severe OSA, which is consistent with a subclinical presentation. Potential contributing mechanisms include upper esophageal sphincter dysfunction with associated upstream changes of increased hypopharyngeal distension pressure and velopharyngeal contractility.

Citation:

Schar MS, Omari TI, Woods CM, et al. Altered swallowing biomechanics in people with moderate-severe obstructive sleep apnea. J Clin Sleep Med. 2021;17(9):1793–1803.

Keywords: deglutition, deglutition disorders, sleep apnea obstructive, sleep apnea syndromes, manometry, fluoroscopy, patient-reported outcome measures

BRIEF SUMMARY

Current Knowledge/Study Rationale: Dysphagia is a common and under-recognized complication of obstructive sleep apnea, but the biomechanics remain poorly described. High-resolution pharyngeal manometry is a novel mechanistic and clinical tool used in pharyngeal swallowing assessment. Subsequently, this study aimed to quantify swallowing biomechanics using high-resolution pharyngeal manometry in people with obstructive sleep apnea.

Study Impact: This study confirms the subclinical presentation of disordered swallowing in people with obstructive sleep apnea. Altered pharyngeal function was identified, consisting of upper esophageal sphincter dysfunction with associated increased velopharyngeal contractility pressure. The upper esophageal sphincter dysfunction is suggestive of sensory neural changes, whereas the increased velopharyngeal pressures may be intrinsic or occur as a compensatory response to upper esophageal sphincter dysfunction. High-resolution pharyngeal manometry assessment of swallowing may be useful when considering device or surgical management of obstructive sleep apnea.

INTRODUCTION

Obstructive sleep apnea (OSA) is a chronic sleep-related upper respiratory condition. It is characterized by repetitive partial or complete upper airway collapse during sleep resulting in obstruction of breathing and arousal.1 Hypopnea and apnea episodes are defined by reduction and cessation of airflow, respectively. Recent population estimates indicate that 25% of women and 50% of men have moderate-severe OSA defined as an apnea/hypopnea index (AHI) > 15 events/h sleep.2 In addition to male sex, the risk of OSA increases with obesity3 and aging.4

The pathophysiologic mechanisms that contribute to OSA are multifactorial and not completely understood. Skeletal and soft tissue anatomical factors result in upper airway narrowing, collapsibility, and obstruction.5 However, there is increasing evidence that additional nonanatomical mechanisms contribute to OSA pathogenesis.6 The low-frequency vibrations that occur with snoring and the tissue stretching that occurs with repeated pharyngeal collapse episodes can result in chronic inflammation and associated edema of the pharyngeal soft tissue.7 This can lead to neuromuscular changes of the upper airway, including peripheral afferent and efferent neural injury and muscle fiber alterations, such as axonal loss, increased connective tissue and muscle fiber size, and fiber atrophy.7–9

Dysphagia is a recognized comorbidity in people with OSA, with a prevalence ranging between 16% and 78%.10 A recent pilot study reported treatment of OSA with continuous positive airway pressure was able to reverse signs of disordered swallowing.11 Subclinical bolus flow abnormalities have been identified using visual instrumental swallowing assessments such as videofluoroscopy swallowing study (VFSS) or fiberoptic endoscopic evaluation of swallowing (FEES) in people with OSA.12–14 In a recent systematic review that analyzed OSA and swallowing function, the most common swallowing impairments reported were premature spillage and/or delayed swallow initiation, followed by observed penetration and pharyngeal residue.10 As yet, however, the pathophysiology of dysphagia in patients with OSA is unclear.10,14 A possible contributing mechanism is that injury from the nightly mechanical trauma of snoring and OSA to the peripheral afferent nerves in the upper airway may impair key swallowing mechanisms in response to bolus flow properties.9,12,15–17 Indeed, oropharyngeal sensory impairment has been reported in people with OSA with prolonged latency of swallow initiation and shorter duration of inspiration after swallowing.17 This is consistent with impaired oropharyngeal swallowing modulation.16 Shah et al9 also recently reported the degree of swallowing dysfunction in people with OSA was associated with neuromuscular injuries in the soft palate, in particular, lower axon density within the nerve fascicles of the soft palate.

High-resolution pharyngeal manometry (HRPM) provides novel mechanistic and clinical insight into pharyngeal swallowing.18 This trans-nasal catheter-based assessment measures pressures generated by the pharynx simultaneously with bolus movement, detected by intraluminal impedance. Together, these measurements allow for a biomechanically based assessment of swallowing physiology.19,20 Identification of the biomechanical properties of swallowing in people with OSA is important to help elucidate the mechanisms that contribute to dysphagia in this population. Accordingly, the aim of this study was to assess swallowing biomechanics and self-reported dysphagia symptoms in people with moderate-severe OSA and compare with age and sex-matched controls.

METHODS

Participants

Ethical approval was granted by the Southern Adelaide Clinical Human Research Ethics Committee (Nos. 283.11 and 156.18). Participants were prospectively enrolled between November 2017 and September 2020. All participants provided written informed consent.

Participants with moderate-severe OSA were recruited following referral to the Otolaryngology Head and Neck Surgery Unit at Flinders Medical Centre for suitability of upper airway surgery. Inclusion criteria were moderate-severe OSA (AHI > 15 events/h sleep)21 based on an overnight polysomnography sleep study, adult (>18 years), and noncompliance with medical management of OSA. Exclusion criteria were previous upper airway or gastrointestinal surgery, self-reported laryngopharyngeal reflux/gastroesophageal reflux disease symptoms, allergy to local anesthesia, pregnancy, uncontrolled diabetes or blood pressure, and a neurologic diagnosis.

Age- and sex-matched control data were acquired from an existing laboratory database.19 Inclusion criteria were adults (>18 years). Exclusion criteria were previous upper airway or gastrointestinal surgery, self-reported swallowing difficulties, self-reported laryngopharyngeal reflux/gastroesophageal reflux disease symptoms, allergy to local anesthesia, pregnancy, uncontrolled diabetes or blood pressure, medications affecting gastrointestinal motility, and medical history consistent with OSA.

Patient-reported outcome measures

All participants completed the Sydney Swallow Questionnaire (SSQ), a validated 17-item self-report outcome measure of symptomatic dysphagia,22,23 which is accessible online (https://stgeorgeswallowcentre.org/sydney-swallow-questionnaire/). Visual analog scale ratings are used in 16 (of the 17) of the items, with a total SSQ score > 234 being abnormal and indicative of symptomatic dysphagia.22 The Epworth Sleepiness Scale, a validated self-administered questionnaire, was used to assess daytime sleepiness with sleepiness defined as a score ≥ 10.24

High-resolution pharyngeal manometry assessment

A combined high-resolution pharyngeal manometry assessment (HRPM) and VFSS was performed in the fluoroscopy suite, whereas HRPM-only studies were conducted in a clinical motility laboratory (Figure 1). An 8-Fr catheter with 32 pressure sensors (unidirectional) and 16 impedance transducers (Unisensor AG catheter, Atticon, Switzerland) was used for recording pressure and impedance data. Following a 4-hour fasting period, lignocaine spray (5%) was topically administered to the nose to maximize participant comfort for HRPM catheter placement. The catheter was positioned to span from the velopharynx to the proximal esophagus. Pressure and impedance data were acquired at 20 samples/s using the Solar GI acquisition unit (Medical Measurement System, Enschede, The Netherlands). Participants were studied in an upright seated posture with a head neutral position. Following a 5-minute accommodation period, a total of 18 test bolus swallows were administered via syringe: 3 swallows each of 5-, 10-, and 20-mL thin (International Dysphagia Diet Standardized Initiative 0) and extremely thick (International Dysphagia Diet Standardized Initiative 4) liquids. The bolus was prepared using a standard HRPM bolus medium (SBMkit, Trisco Foods Pty Ltd, Brisbane, Australia)19 with 100 mL tap water. Viscosity was tested to ensure conformance with the International Dysphagia Diet Standardization Initiative.25

Figure 1. VFSS and corresponding HRPM of a 10-mL thin liquid swallow in a healthy control.

Figure 1

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(A) Lateral VFSS image shows the 8-Fr catheter in the trans-nasal position spanning the velum to the UES, at rest. (B) HRPM pharyngeal pressure-topography plot of a complete swallow. Boxes represent regions for the velopharyngeal (VCI), mesopharyngeal (MCI), and hypopharyngeal (HPCI) contractile integrals. The corresponding regions are seen on the adjacent VFSS image. (The pharyngeal contractile integral [PhCI] is the mean of the VCI, MCI, and HPCI). (C) Hypopharyngeal derived metric, intra-bolus pressure (IBP) is represented as the peak of admittance of bolus movement (in pink). (D) UES-derived metrics, relaxation time (UES RT), opening extent (UES maximum admittance), and pressure (UES IRP) are shown in relation to UES pressure (in black) and bolus movement (in pink). (E) UES relaxation time (UES RT) is the duration from UES relaxation to UES contraction, represented by the yellow vertical lines on hypopharyngeal and UES admittance/pressure graphs and by the yellow dots on the pressure topography plot. HRPM = high-resolution pharyngeal manometry, UES = upper esophageal sphincter, VFSS = videofluoroscopy swallow study.

The HRPM recordings were analyzed by an experienced speech pathologist (author MS) and reviewed by an expert in HRPM analysis (author TO). The analysis was conducted using the web-based platform Swallow Gateway™ (swallowgateway.com, version 2020; Flinders University, Adelaide, Australia), whereby each HRPM study was exported from a Medical Measurement System in ASCII file (.asc) format containing no identifying information and uploaded for analysis. Individual swallows were selected by drawing a region of interest spanning from the velopharynx to the esophageal transition zone (inferior border of the proximal esophagus). For each selected swallow, the analyst placed anatomical markers at the velopharyngeal proximal margin, hypopharyngeal proximal margin, upper esophageal sphincter (UES) apogee, and UES distal margin, as well as timing markers of UES relaxation and closure.

Core outcome swallow biomechanical metrics (Table 1; Figure 1) were derived by algorithms consistent with the recently published International HRPM Working Group recommendations.20 Additional biomechanical metrics (Table 1) were derived through software analysis. Previous studies have demonstrated reliability of this analysis method.26 The swallow risk index (SRI) is a validated additional biomechanical metric that represents global swallow function; an SRI > 15 has been associated with swallowing dysfunction predisposing to aspiration risk.27

Table 1.

High-resolution pharyngeal manometry outcome metrics and definitions.21

Measurement Definition
HRPM core outcome metrics
 Pharyngeal lumen occlusive pressure
  Pharyngeal contractile integral (PhCI) An integral pressure measure of pharyngeal contractile vigor spanning from the velopharynx to the upper margin of the upper esophageal sphincter (UES) (mm Hg⋅cm⋅s).
  Velopharyngeal contractile integral (VCI) An integral pressure measure of pharyngeal contractile vigor spanning the velopharyngeal region only (mm Hg⋅cm⋅s).
  Mesopharyngeal contractile integral (MCI) An integral pressure measure of pharyngeal contractile vigor spanning the mesopharyngeal region only (mm Hg⋅cm⋅s).
  Hypopharyngeal contractile integral (HPCI) An integral pressure measure of pharyngeal contractile vigor spanning the hypopharyngeal region only (mm Hg⋅cm⋅s).
 Hypopharyngeal intrabolus distension pressure
  Hypopharyngeal intrabolus distension pressure (IBP) The pressure 1 cm superior to the UES apogee position at the time of maximum hypopharyngeal distension (indicated by impedance/admittance) (mmHg).
 UES relaxation and opening
  UES integrated relaxation pressure (UES IRP) A pressure measure of the extent of UES relaxation pressure, generated as the median of the lowest pressure in a nonconsecutive 0.20–0.25 second window (mm Hg).
  UES relaxation time (UES RT) A measure of the duration of UES relaxation – a pressure interval below 50% of baseline or 35 mmHg, whichever is lower, in units of seconds.
  UES maximum admittance (UES Max Ad) A measure of extent of UES opening. The highest admittance value (inverse of impedance) recorded during trans- sphincteric bolus flow, in units of millisiemens.
HRPM additional outcome metrics
 Global swallow function
  Swallow risk index (SRI) A composite score based on a mathematical formula comprising of four hypopharyngeal swallow metrics (IBP, BPT, DCL, peak pharyngeal pressure) and provides a numerical value distinguishing normal from abnormal swallow function (SRI > 15, indicates abnormal function).
 Timing measures
  Bolus presence time (BPT) Duration of the bolus in the hypopharynx prior to UES relaxation – a correlate of the dwell time of the bolus in the pharynx (s).
  Distension-contraction latency (DCL) A timing measure from maximum pharyngeal bolus distension to the pharyngeal luminal occlusive contraction – a correlate of bolus propulsion ahead of the pharyngeal stripping wave (s).
 UES pre- and postswallow and proximal esophageal measures
  UES basal pressure (UES BP) The peak pressure at the level of the UES pre swallow (mm Hg).
  UES contractile integral (UES CI) An integral pressure measure of UES contractile vigor, post swallow (mm Hg⋅cm ⋅s).
  Proximal esophageal contractile integral (Prox Es CI) An integral pressure measure of proximal esophageal contractility (mm Hg⋅cm ⋅s).
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VFSS

Simultaneous VFSS with HRPM evaluation was conducted using a standardized protocol in the radiology suite using a videofluoroscope (Artis zee multipurpose, Seimens Healthineers) and recorded at 15 frames/s in-line with Flinders Medical Centre Radiology department procedure. The standard VFSS protocol consisted of 5,10, and 20 mL of thin and extremely thick liquids observed in the lateral plane. Repeat 20 mL thin and extremely thick liquids was observed in the anterior-posterior plane. The bolus was prepared using standard HRPM bolus medium (SBMkit) with 100 mL liquid barium used in place of tap water (Polybar barium sulfate suspension; Bracco Diagnostics Inc., Monroe Township, NJ).

Premature spillage was defined as entry of the bolus into the pharynx without the initiation of a swallow, which is typically associated with poor oral containment and/or delayed swallow initiation.28 Penetration and aspiration were quantified using the 8-point penetration-aspiration scale29; a penetration-aspiration scale > 2 was considered indicative of abnormal swallowing. Vallecular and pyriform sinus residue was measured using the normalized residue ratio scale30 via open-source image analysis software (Image J, National Institute of Health, Rockville, MD). The ratio of postswallow residue relative to the outlined valleculae or pyriform sinus regions was captured. Abnormal postswallow residue was defined as normalized residue ratio scale (NRRS), valleculae (NRRSv) > 0.1, and pyriform sinus residue (NRRSp) > 0.2.30

Statistical analysis

Statistical analysis was performed using IBM SPSS Statistics Version 25.0 (Statistical Package for the Social Sciences; IBM Corp., Armonk, NY). The average of each swallow function metric was determined per participant across each volume and consistency condition (3 swallows for each bolus condition). General linear mixed model analysis was performed with bolus volume and consistency as repeated measures and group as fixed factors. Where relevant, general linear mixed model descriptive parameters (F, P value) are shown for overall comparisons. Bonferroni adjustment was applied to multiple pairwise comparisons. Nonparametric data were normalized by log transformation or compared using Mann Whitney U test. Data are presented as means (95% confidence interval) or median [interquartile range] as appropriate. Statistically significant was inferred when P < .05.

RESULTS

Demographics

Demographics of the study participants are presented in Table 2. The OSA group comprised of nineteen participants: 84% (16 of 19) had severe OSA (AHI > 30 events/h sleep) and 16% (3 of 19) had moderately severe OSA (AHI between 15 and 30 events/h sleep). Excessive daytime sleepiness was reported in 37% (7 of 19) of participants in the OSA group. Data for 19 controls were consecutively selected from the database to match the age and sex distribution of the OSA participants. The 2 groups were not body mass index (BMI) matched, and the average BMI was 6 kg/m2 higher in the OSA group compared with controls (Table 2).

Table 2.

Demographics of OSA and age-matched control groups.

Control (n = 19) OSA (n = 19)
Age (y) 46, range 27–68 46, range 26–68
Sex (male: female) 14:5 14:5
BMI (kg/m2) 25, range 18–31 31, range 22–41
AHI Not applicable 46, range 17–90
ESS Not applicable 9, range 2–16
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Data presented as mean with range or count. AHI = apnea-hypopnea index, BMI = body mass index, ESS = Epworth Sleepiness Scale, OSA = obstructive sleep apnea.

Patient-reported outcome measure of swallowing

Twenty six percent (5 of 19) of the OSA group reported symptomatic dysphagia. The total SSQ score was significantly higher in the OSA cohort compared with healthy controls (median = 116, [70, 242] vs median = 42 [20, 66], Mann Whitney U test = 3.085; P < .002; Figure 2). OSA severity (AHI) was not significantly correlated with symptomatic dysphagia (SSQ; r = .86, P = .727, Spearman rho).

Figure 2. Self-reported dysphagia symptoms in people with OSA compared with healthy controls.

Figure 2

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Scatterplot showing different distribution of SSQ scores of the control vs OSA groups. Five of 19 (26%) of the OSA group show symptomatic dysphagia. The control group have a median of 42 (IQR [20, 66]), whereas the OSA group has an increased median of 116 (IQR [70, 242]), approaching the SSQ symptomatic dysphagia cutoff value of 234. Mann-Whitney U test, 3.085; P < .002. Error bars = 95% confidence interval. GRP = group, IDDSI = international dysphagia diet standardization initiative, IQR = interquartile range, OSA = obstructive sleep apnea, OSAS = obstructive sleep apnea syndrome, SSQ = Sydney Swallow Questionnaire, UES = upper esophageal sphincter.

VFSS

VFSS was performed in a subgroup of 9 OSA participants (concurrently with HRPM). Premature spillage was observed in 11% (1 of 9). All participants with OSA presented with a penetration-aspiration scale score within normal limits (level of 1 or 2). Valleculae postswallow residue, quantified using the normalized residue ratio scale, valleculae, was within normal limits for 8 participants. One had a valleculae postswallow residue score of 0.2, considered indicative of abnormal function. Interestingly, this patient was asymptomatic for dysphagia with an SSQ score of 160. All participants had a normal pyriform sinus postswallow residue score.

HRPM core outcomes

UES relaxation and opening diameter

UES integrated relaxation pressure was statistically increased in the OSA group compared with healthy controls (P < .0001). Significant pairwise differences were present for all test combinations with the exception of 5 mL extremely thick liquids (P < .05; Figure 3; Table 3). Similarly, UES opening diameter was reduced in the OSA group compared with controls (P < .0001). Pairwise comparisons were significantly different in the OSA group vs controls, for 10 mL thin and 10 and 20 mL extremely thick liquids (P < .05; Figure 4; Table 3). UES relaxation time was reduced in the OSA group vs controls (P < .02). However, there were no significant pairwise differences.

Figure 3. UES integrated relaxation pressure in OSA cohort compared with age-matched healthy controls.

Figure 3

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Bar graph illustrating mean and 95% CI for 5-, 10-, and 20-mL bolus volumes at thin (IDDSI level 0) and extremely thick (IDDSI level 4) consistencies for the OSA group (red) and the control group (blue). UES IRP was significantly increased in the OSA group for all tested bolus conditions except 5 mL extremely thick liquid. *Statistical significance (P < .05, general linear mixed modeling). CI = confidence interval, IDDSI = international dysphagia diet standardization initiative, IRP = integrated relaxation pressure, OSA = obstructive sleep apnea, SSQ = Sydney Swallow Questionnaire, UES = upper esophageal sphincter.

Table 3.

HRPM metrics comparing the OSA group to age- and sex-matched healthy control group.

Metric Control (n = 19) OSA (n = 19) F P Pairwise comparisons of bolus volume and viscosity
HRPM core outcome measures, mean (95% CI)
 Pharyngeal contractile integral (mm Hg⋅cm ⋅s) 287 (268, 307) 377 (357, 397) 39.907 < .0001 Thin liquids 5, 10, 20 mL*
Extremely thick liquids 5, 10, 20 mL*
 Velopharyngeal contractile integral (mm Hg⋅cm ⋅s)† 87.5 (76, 99) 144 (132,156) 69.629 < .0001 Thin liquids 5, 10, 20 mL*
Extremely thick liquids 5, 10, 20 mL*
 Mesopharyngeal contractile integral (mm Hg⋅cm ⋅s) 129 (119,139) 141 (131,151) 2.559 .111 Not significant
 Hypopharyngeal contractile integral (mm Hg⋅cm ⋅s)† 71 (63, 78) 92 (84, 99) 18.203 < .0001 Extremely thick liquids 10 mL*
 Hypopharyngeal intrabolus pressure (mm Hg) 2.4 (1.1, 3.7) 6.5 (5.2, 7.8) 18.984 < .05 Thin liquids 5, 10, 20 mL*
Extremely thick liquids 5, 10, 20 mL*
 UES maximum admittance (mS) 5.7 (5.6, 5.8) 5.2 (5.0, 5.3) 23.564 < .0001 Thin liquids 5, 10, 20 mL*
Extremely thick liquids 5, 10, 20 mL*
 UES integrated relaxation pressure (mm Hg) −2.0 (−3.0, 1.0) 2.0 (1.0, 3.0) 32.152 < .0001 Thin liquids 5, 10, 20 mL*
Extremely thick liquids 5, 10, 20 mL*
 UES relaxation time (s) 0.57 (0.55, 0.58) 0.54 (0.52, 0.56) 5.085 < .025 Not significant
HRPM additional outcome measures, mean (95% CI)
 Swallow risk index† 1.9 (1.0, 2.7) 3.6 (2.7, 4.5) 20.766 < .0001 Thin liquids 5, 10, 20 mL*
Extremely thick liquids 5, 10, 20 mL*
 Bolus presence time (s)a 0.7 (0.6,0.8) 0.7 (0.6, 0.8) 0.248 .619 Not significant
 Distension-contraction latency (s) 0.51 (0.49, 0.52) 0.47 (0.46, 0.49) 10.067 < .002 Thin liquids 20 mL*
 UES basal pressure (mm Hg) 77 (71, 84) 64 (58,70) 8.866 < .003 Thin liquids 10 mL*
 UES contractile integral (mm Hg⋅cm ⋅s) 523 (483, 563) 458 (417, 598) 5.030 < .026 Not significant
 Proximal esophageal contractile integral (mm Hg⋅cm ⋅s)† 364 (326, 401) 304 (265, 342) 0.176 .675 Not significant
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Shown are main effects of general linear mixed modeling with F statistic and P values. Pairwise comparisons with Bonferroni adjustment are presented comparing the OSA group to the age-matched control group for each bolus condition. *Significance (P < .05) pairwise comparisons of tested bolus conditions across volumes (5, 10, or 20 mL) and viscosity (thin [IDDSI 0] and extremely thick [IDDSI 4] liquids). †Measures that were log transformed before GLMM. HRPM = high-resolution pharyngeal manometry, IDDSI = international dysphagia diet standardization initiative, OSA = obstructive sleep apnea, UES = upper esophageal sphincter.

Figure 4. UES opening extent measures in people with OSA compared with age-matched healthy controls.

Figure 4

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Bar graph illustrating mean and 95% CI for 5-, 10-, and 20-mL bolus volumes at thin (IDDSI level 0) and extremely thick (IDDSI level 4) consistencies for the OSA group (red) and the control group (blue). UES opening extent, measured by maximum admittance, was significantly reduced in the OSA group for 10 mL thin and extremely thick and 20 mL extremely thick bolus conditions. *Statistical significance (P < .05, general linear mixed modeling). CI = confidence interval, IDDSI = international dysphagia diet standardization initiative, OSA = obstructive sleep apnea, Max Admin = maximum admittance, UES = upper esophageal sphincter. Error bars = 95% CI.

Hypopharyngeal intrabolus distension pressure

The hypopharyngeal intrabolus pressure was significantly increased in participants with OSA compared with controls (P<.0001). Pairwise comparisons demonstrated significant increases for the OSA group for 5 and 20 mL thin liquids and 5 and 10 mL extremely thick liquids (P < .05; Table 3).

Pharyngeal contractile integrals (velo-, meso-, hypo-)

Significant increases in velopharyngeal contractile integral (P < .0001), hypopharyngeal contractile integral (P < .0001), and pharyngeal contractile integral (P < .0001) were present for the OSA group compared with healthy controls (Table 3). Pairwise comparisons were significantly increased for velopharyngeal and pharyngeal contractile integrals across all tested volumes and consistencies for the OSA group (Figure 5; Table 3). The hypopharyngeal contractile integral showed a significant increase for 10 mL extremely thick liquids (P < .0001). The mesopharyngeal contractile integral did not differ between participants with OSA and healthy controls (P = .11; Table 3).

Figure 5. Velopharyngeal contractile pressure measures in people with OSA compared with healthy controls.

Figure 5

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Bar graph illustrating mean and 95% CI for 5-, 10-, and 20-mL bolus volumes at thin (IDDSI level 0) and extremely thick (IDDSI level 4) consistencies for the OSA group (red) and the control group (blue). VCI was significantly increased in the OSA group for all tested bolus conditions. Error bars = 95% CI. *Statistical significance (P < .05, Mann Whitney U test). CI = confidence interval, IDDSI = international dysphagia diet standardization initiative, OSA = obstructive sleep apnea, OSAS = obstructive sleep apnea syndrome, VCI = velopharyngeal contractile pressure.

HRPM additional outcome measures

The SRI was significantly elevated in the OSA group compared with controls (P<.0001). Significant pairwise differences (increased SRIs) were present for all tested volumes of thin liquid and extremely thick liquids (P < .05; Table 3). There was no significant correlation between the presence of an abnormal SRI and OSA severity (AHI; r = .141, P = .565, Spearman rho).

The bolus presence time did not differ between OSA participants and controls (P = .6). The distension-contraction latency was significantly shorter in participants with OSA compared with controls (P < .002). Significant pairwise differences were present only for 20 mL thin liquid. UES basal pressure, which measures the UES pressure before swallow initiation, was reduced in the OSA group vs controls (P < .003). Pairwise differences were present in 10 mL thin liquid only. When comparing the difference of thin vs thickened liquid, there were no differences observed in the OSA group compared with controls, who showed a significantly higher UES basal pressure during thin liquid swallows (Table 3).

The postswallow UES contractility was reduced in the OSA group vs controls (P < .026). However, no significant pairwise differences were identified. Proximal esophageal contractility was not significantly different for the participants with OSA compared with controls (P = .6; Table 3).

DISCUSSION

This is the first study to investigate dysphagia symptoms and swallowing physiology in people with moderate to severe OSA using HRPM technology. The main findings were (1) 26% of OSA participants were symptomatic of dysphagia, and (2) the OSA group displayed altered swallowing physiology compared with age- and sex-matched controls. The main biomechanical differences identified included (i) reduced UES relaxation and opening extent, (ii) elevated hypopharyngeal intrabolus pressures, and (iii) increased velopharyngeal contractile pressures. These findings suggest that people with moderate-severe OSA have evidence of UES dysfunction with associated upstream changes in distension pressure and contractility.

Self-reported dysphagia scores were elevated in the OSA cohort compared with matched controls, with 26% symptomatic of dysphagia. This is consistent with the literature.31 Despite the increased prevalence of self-reported dysphagia symptoms in people with OSA, this has not been reported to impact health-related quality of life,11 suggesting this may be minor and subclinical in nature. However, these OSA-related changes may compound the known age-related deterioration of the swallowing mechanism,32 potentially resulting in an earlier onset of symptomatic dysphagia. Consistent with existing literature, no correlation was found between OSA severity and self-reported/objective measures of dysphagia.12,14,15

Compared with healthy controls, people with moderate-severe OSA had reduced UES opening. This may correlate with reported findings of reduced hyolaryngeal contraction times,33 as hyolaryngeal movement is biomechanically coupled with increased traction and opening of the UES.34 Additionally, the OSA group had the biomechanical hallmarks of UES dysfunction, evidenced by increased UES relaxation pressures, shorter UES relaxation times, and elevated hypopharyngeal intrabolus pressures. UES dysfunction may be the result of (1) noncompliance of the cricopharyngeal muscle, (2) weak/ineffective pharyngeal propulsion, or (3) a neuroregulatory impairment.35 Controls were age matched to allow for age-related UES dysfunctions.35 In the VFSS, there was no evidence of structural pathology (eg, stricture, cricopharyngeal bar). Likewise, pharyngeal contractility was within or above normal limits in the OSA group. Thus, our findings support altered neuroregulatory swallowing modulation as the basis of UES dysfunction, resulting in less efficient accommodation of bolus volume and consistency. These results need to be considered in light of BMI, because fat deposits in the lateral pharyngeal wall and posterior tongue are known to cause upper airway narrowing in people with OSA.6,36 This may result in propulsion of liquid through a reduced space with associated increased intrabolus pressures in the hypopharynx and UES regardless of the UES opening. However, altered UES biomechanics, together with known peripheral sensory neural injury in people with OSA,7–9,14 are suggestive of sensory inputs to the brainstem central pattern generator potentially being attenuated in people with OSA.

Previous studies support this notion of sensory impairment associated with swallowing dysfunction in people with OSA.12,16 Teramoto et al17 found that patients with OSA have prolonged latency of swallow initiation, consistent with peripheral sensory impairment affecting the swallowing mechanism. In the current study, altered HRPM timing-based metrics, such has UES relaxation time and distension-contraction latency, may be in accordance with a putative impairment of swallowing modulation by mucosal mechano-receptors, which detect bolus stimuli facilitating effective bolus accommodation.37 Additionally, the preswallow UES basal pressure that, in controls, displays a reflex-like activation to swallowing liquids,19,38 did not show similar activation in this OSA cohort.

Increased velopharyngeal contractility in people with OSA may be representative of increased tissue volume of the retropalatal region or an upstream compensatory response to UES restriction during bolus flow. Given that velum collapsibility is highly prevalent in the OSA population with a reported incidence of 81%,39 this may account for the observed increased velopharyngeal contractile pressure in this OSA cohort. Velopharyngeal contractile pressure and duration increases with swallow volume and contributes to the configuration of an enclosed pharyngeal chamber that assists with bolus propulsion.40 It is plausible that reduced UES opening and restricted bolus flow through the UES may cause a compensatory response of increased velopharyngeal pressures to augment bolus propulsion and clearance. This biomechanical relationship has previously been described during neck flexion maneuvers and inverted body position in healthy participants.40,41 It is also noteworthy that people with obesity have shown increased pharyngeal length and closing pressure, resulting from increased fat deposit in the tongue base and associated altered hyoid bone location with the epiglottis positioned superiorly toward the soft palate.42

It is important to note that many of the altered swallowing findings observed in the current study align with those reported in a previous OSA cohort after upper airway surgery.43 The previous study assessed swallowing in patients following upper airway surgery for treatment of OSA without a comparative preoperative assessment. The current study adds to this previous report and suggests that the abnormal measures of swallowing may be associated with OSA per se and not necessarily a result of surgical intervention. In contrast to the increased pharyngeal contraction observed in the current study, people with OSA after surgical intervention did not have altered pharyngeal contraction. This suggests that the surgical intervention may impair the capacity for compensation to downstream UES resistance, potentially leading to an increased risk of dysphagia. Thus, it is conceivable that altered UES function may be a feature of moderate-severe OSA in general, whereas a reduction in pharyngeal contractility is an additional feature following upper airway surgical intervention. Further investigations of dysphagia following upper airway surgery are needed to differentiate the mechanisms associated with OSA and upper airway surgical intervention.

The current study also contributes to further establishing HRPM technology as a useful adjunct to the assessment and management of swallowing in people with OSA. High-resolution manometry has long been considered the gold-standard diagnostic assessment of esophageal motility disorders in clinical and research settings.44 The application of high-resolution manometry technology in the evaluation of oropharyngeal disorders can advance the swallowing physiology assessment as it can detect subtle, subclinical, levels of impairment.45 In a recently published systematic review that investigated OSA and the association with dysphagia, approximately one-half of the studies used visual instrumental assessments and primarily reported bolus flow outcomes of penetration, aspiration, and bolus residue.10 However, identification of the associated pathophysiologic impairments are limited, resulting in increased variability in the interpretation of visual instrumental findings and subsequent treatment planning.46 Therefore, HRPM technology can identify contributing pathophysiologic mechanisms to abnormal bolus flow findings, thereby improving the diagnostic specificity of visual instrumental swallowing assessment interpretation in people with OSA.

The following limitations are acknowledged. Given the high prevalence of laryngopharyngeal reflux/gastroesophageal reflux disease in people with OSA, exclusion based on a validated questionnaire, rather than self-report, would have provided more confidence that patients were indeed asymptomatic of gastroesophageal reflux disease. Although there was a wide range of body mass indices in both groups, the 2 groups were not BMI matched, with a higher BMI in people with OSA being a common observation. It is important to consider that in people who are obese, changes in pharyngeal swallowing function have been identified, including increased premature spillage and increased pharyngeal clearance time.47 Although there are few published data on pharyngeal HRPM in relation to BMI, one pediatric study did not find a correlation.48 Nonetheless, in future studies, it will be important to carefully investigate the potential influence of BMI and symptomatic laryngopharyngeal reflux (with use validated self-report symptomatic measures) and dysphagia in people with OSA. Currently, VFSS is considered a gold-standard of oropharyngeal swallowing assessment and was conducted in a subgroup of participants with OSA and not available for controls. The testing of solid textured foods and use of standardized quantified VFSS criteria may have identified subtle changes enabling correlation of the VFSS quantified measures with the HRPM biomechanical measures. Future studies may consider correlating VFSS physiologic parameters with HRPM metrics. Finally, as swallowing dysfunction seen was subtle with most patients not reporting dysphagia, a much larger study sample would be required to determine any relationships between biomechanical changes and symptoms.

CONCLUSIONS

People with moderate-severe OSA have biomechanical features consistent with UES dysfunction and associated upstream changes with increased hypopharyngeal distension pressure and velopharyngeal contractility. These differences may be intrinsic or occur as a compensatory response to UES flow restriction and reduced UES opening. These novel observations contribute to increased understanding of the potential mechanisms of dysphagia in the OSA population. Further studies to extend these findings and determine the relationship between altered swallowing biomechanics, patient symptoms, and the effects of OSA treatments are warranted.

DISCLOSURE STATEMENT

All authors have seen and approved this manuscript. M. Schar was awarded a joint SA Health/University of South Australia grant and author T. Omari was awarded the Flinders Seeding Grant, which supported data collection. T. Omari and D. J. Eckert (1116942) are supported by National Health & Medical Research Council of Australia Senior Research Fellowships. The development of the swallowgateway.com website was supported by grants from the College of Medicine and Public Health, Flinders University. The other authors report no external funding for this manuscript. T. Omari holds inventorship of the patent family that covers the analytical methods described. The Swallow Gateway web application is owned by Flinders University. D. J. Eckert has a Cooperative Research Centre (CRC)-P grant and a joint Australian Government, Academia and Industry collaboration (Industry partner Oventus Medical); receives research income from Bayer and Apnimed; and serves as a consultant outside the submitted work. All other authors report no conflict of interest.

ABBREVIATIONS

AHI

apnea-hypopnea index

BMI

body mass index

HRPM

high-resolution pharyngeal manometry

OSA

obstructive sleep apnea

SRI

swallow risk index

SSQ

Sydney Swallow Questionnaire

UES

upper esophageal sphincter

VFSS

videofluoroscopy swallow study

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