Effects of chemoradiation and tongue exercise on swallow biomechanics and bolus kinematics

Nicole E Schaen‐Heacock; Linda M Rowe; Michelle R Ciucci; John A Russell

doi:10.1002/hed.27899

. 2024 Aug 16;47(1):355–370. doi: 10.1002/hed.27899

Effects of chemoradiation and tongue exercise on swallow biomechanics and bolus kinematics

Nicole E Schaen‐Heacock ^1,^2,^✉, Linda M Rowe ^1,², Michelle R Ciucci ^1,^2,³, John A Russell ²

PMCID: PMC11635752 NIHMSID: NIHMS2011624 PMID: 39150237

Abstract

Background

Common treatments for head and neck cancer (radiation and chemotherapy) can lead to dysphagia; tongue exercise is a common intervention. This study aimed to assess swallow biomechanics and bolus kinematics using a well‐established rat model of radiation or chemoradiation treatment to the tongue base, with or without tongue exercise intervention.

Methods

Pre‐ and post‐treatment videofluoroscopy was conducted on 32 male Sprague–Dawley rats treated with radiation/chemoradiation and exercise/no exercise. Rats in the exercise groups completed a progressive resistance tongue training paradigm. Swallow biomechanics, bolus kinematics, jaw opening, and post‐swallow respiration were assessed.

Results

Both treatments impacted outcome measures; the addition of exercise intervention showed benefit for some measures, particularly in rats treated with radiation, vs. chemoradiation.

Conclusions

Radiation and chemoradiation can significantly affect aspects of deglutition; combined treatment may result in worse outcomes. Tongue exercise intervention can mitigate deficits; more intensive intervention may be warranted in proportion to combined treatment.

Keywords: chemoradiation, deglutition, dysphagia, murine, radiation

1. INTRODUCTION

Swallowing impairments are a significant sequelae of head and neck cancer interventions, affecting up to 60% of patients receiving radiotherapy (RT), chemotherapy (CT), or concurrent chemoradiotherapy (CCRT). ¹ , ² , ³ , ⁴ , ⁵ , ⁶ Commonly, acute toxicities (i.e., during and/or shortly after HNC treatment) can cause side effects such as mucositis, xerostomia, odynophagia, and dysgeusia, leading to functional impairments in deglutition known as radiation‐associated dysphagia (RAD) and late radiation‐associated dysphagia (LRAD—occurring at least 5 years post‐treatment). ⁷ , ⁸ Both RAD and LRAD cause significant detriment to patients' overall health and quality of life, including increased risk for aspiration pneumonia, malnutrition, reliance on alternative means of nutrition, and feelings of isolation. ¹ , ² , ³ , ⁹ , ¹⁰

Functional deglutition requires precise coordination of oral, laryngeal, and pharyngeal structures. Treatment‐related toxicities may result in direct or indirect damage to the composition and movement of structures necessary for safe and efficient mastication. ¹¹ , ¹² Trismus, edema, fibrosis, issues with dentition, and mucositis can impact mandibular motion/masticatory cycles, as well as preparation and propulsion of the bolus. ⁸ , ¹² , ¹³ , ¹⁴ , ¹⁵ Previous clinical studies in HNC using morphometric analysis software to study swallowing kinematics (computational analysis of swallowing mechanics [CASM]) have reported increased flexion of the head and neck during swallowing, reduced base of tongue retraction, ¹⁶ and reduced pharyngeal shortening. ¹⁷

Coordinated orolingual movements also play a significant role in oropharyngeal swallow safety, including respiratory–swallow coordination. Prior research has demonstrated that dysregulated tongue movements can have negative impacts on swallowing and thus the coordination between swallowing and breathing, and the addition of lingual exercise improved respiratory–swallow coordination. ¹⁸ , ¹⁹ Clinical studies evaluating respiratory–swallow coordination in HNC have identified disruption to the stable, protective post‐swallow exhale pattern, with reports of increased frequency of post‐swallow inhales in post‐intervention HNC, ²⁰ , ²¹ and decreased stability of respiratory–swallow pattern within treated individuals. ²² These deficits significantly elevate patient risk of aspiration, and potential medical complications including pneumonia and malnutrition. ²⁰ , ²¹ , ²² Although aerodigestive dysfunction post‐treatment in HNC is becoming increasingly well‐characterized, the underlying mechanisms of impairment, and of potential rescue interventions, are not well understood.

As survivorship in the HNC population increases, critical gaps in knowledge remain regarding the relationship between HNC treatments and changes to swallow physiology and function, as well as the role of exercise‐based swallow interventions in mitigating these changes. While clinical practice is moving towards a proactive approach to intervention for this patient population, many diagnosed with HNC continue to receive intervention reactively following patient‐reported symptoms of dysphagia, or signs such as weight loss or aspiration pneumonia. ²³ , ²⁴ , ²⁵ This may be due to barriers such as rurality, access difficulties to relevant providers, lack of a Speech‐Language Pathologist on the multidisciplinary cancer care team, and treatment burden. Although several exercise‐based intervention programs have shown promise at improving swallow‐related outcomes in post‐treatment HNC, ²⁶ optimal parameterization (e.g., frequency, intensity, onset relative to radiation treatment) of these programs is not forthcoming. Clinical investigations into effectiveness of exercise‐based dysphagia interventions are subject to limitations such as variability in treatment dose/location and adherence to intervention strategies. ²⁶ In addition, exercise‐based interventions employed in clinical practice for patients with HNC often include a myriad of maneuvers to engage several swallow‐related structures simultaneously, thus the biomechanical impact of a particular exercise is unclear. ²³ , ²⁷ , ²⁸ , ²⁹ , ³⁰ , ³¹ , ³² Further, interrogating the impact of dysphagia exercise on underlying peripheral and central nervous system biology is challenging in clinical studies, limiting our understanding of their relative contributions to functional changes in deglutition. Many of these shortcomings can be accounted for in a validated, controlled translational rat model of treatment and tongue exercise, as this enables investigation and correlation of functional changes to underlying biology. ³³ , ³⁴

Preclinical investigation of the impacts of RT and CCRT treatment to the tongue base in the rat model show similarities to human clinical findings, including altered chewing, tongue function, respiratory patterns, and bolus movement in the pharynx. ³³ , ³⁴ The ability to analyze treatment‐induced effects in an otherwise healthy system allows for controlled investigation without tumor‐related interference on swallow muscle function and underlying muscle biology. Numerous confounds present in clinical treatment of HNC can be accounted for in an animal model, including control of dosing/treatment plan, targeted structures involved, adherence to treatment and related interventions, and continuance of oral intake. Further, targeted tongue training has been successfully used in a number of translational studies showing increases in force generation models of healthy aging ³⁵ , ³⁶ , ³⁷ , ³⁸ and Parkinson's disease. ³⁹ This progressive resistance training paradigm is similar to tongue strength exercises employed in the clinical setting. ³⁵ , ³⁶ , ³⁷ , ⁴⁰ , ⁴¹ , ⁴² , ⁴³ Therefore, assessing the impacts of tongue‐based exercise intervention on swallow function following treatment in a controlled translational rat model can provide insight and subsequent refinement of clinical intervention methods for this patient population.

The purpose of this study was to investigate how RT and CCRT, with and without the addition of progressive resistance tongue exercise, would affect 1) swallow biomechanics; 2) bolus kinematics and bolus area; 3) related functions including jaw aperture (opening) and respiratory–swallow coordination. We hypothesized that both RT and CCRT would 1) impact the magnitude and directionality of change of swallow‐related musculoskeletal structures similar to clinical HNC CASM findings (i.e., altered head/neck posture and pharyngeal shortening) ¹⁶ , ¹⁷ ; 2) decrease efficiency (bolus speed, bolus area, mastication rate); and 3) increase instances of post‐swallow inhalation, with more pronounced effects in CCRT compared to RT alone. We further hypothesized that the addition of tongue exercise intervention would mitigate the negative impacts of HNC treatment, thus resulting in no significant differences compared to healthy baseline on these parameters in both treatment groups receiving tongue exercise.

2. MATERIALS AND METHODS

Thirty‐two male Sprague–Dawley rats were randomized into four groups: concurrent chemoradiotherapy without exercise (CCRT), radiotherapy without exercise (RT), CCRT + tongue exercise (CCRT + TE), and radiotherapy + tongue exercise (RT + TE), with eight animals per group based on a priori power calculations. All rats underwent videofluoroscopic swallow studies (VFSS) at baseline (prior to treatment administration/exercise intervention) and 12 weeks post‐treatment ± exercise intervention, thus serving as their own controls. Treatment consisted of RT delivered to an 8 × 12 mm² area of the tongue base over the course of 10 days using methods previously described (Xstrahl Small Animal Radiation Research Platform [SARRP] Irradiator). ³³ Administration of radiotherapy to this area targets a structure crucial for swallowing and allows exploration of how treatment may impact swallow function. ¹⁴ , ⁴⁴ , ⁴⁵ , ⁴⁶

Each rat received 4.5 Gy/day, totaling 45 Gy—thus the biological effective dose was approximately 112 Gy. ³³ , ⁴⁷ , ⁴⁸ This fraction size was calculated using methods previously described, and allowed for maintenance of clinical relevance in the protocol of treatment delivery. ³³ , ⁴⁷ , ⁴⁸ In addition, rats in the CCRT groups received two doses of cisplatin (3 mg/kg) in addition to RT—one dose prior to the first fraction of RT, and another prior to the sixth fraction. Cisplatin is a common chemotherapy drug and is often considered the standard of care in this patient population. ⁴⁹ , ⁵⁰ Rats in the TE groups underwent an 8‐week progressive resistance tongue training paradigm following treatment administration and a recovery period. Baseline and final VFSS recordings were used for data analysis via ImageJ. Rats were pair‐housed in standard polycarbonate cages in the vivarium on a reversed 12:12 light/dark cycle. All animal work was done in accordance with NIH and university animal‐use guidelines and approved by the University of Wisconsin School of Medicine and Public Health Animal Care and Use Committee (IACUC Protocol M005828).

2.1. Progressive resistance tongue training paradigm

The progressive resistance tongue training paradigm is a well‐established tool, analogous to lingual strengthening exercises employed in the clinical setting, in translational models such as aging, Parkinson disease, and stroke. ⁴¹ , ⁴³ , ⁵¹ , ⁵² Intervention involves training the rat to press a disc connected to a force transducer with a specified amount of force to obtain a water reward (Figure 1). To avoid adding undue stress during treatment administration, rats were not water restricted until after treatment. Following a 1‐week (7 days) gradual water restriction, rats were acclimated to the apparatus and underwent an 8‐week training paradigm. Maximum force (g) was calculated at baseline, and individualized force requirements were initiated at 20% and increased by 20% every 2 weeks, ending with 80% maximum force required at 8 weeks. Rats were water restricted over the training period to motivate their participation in the exercise, and given access to water ad libitum for 3 hours/day, 7 days/week.

Tongue force apparatus. The rat is trained to press the disc (connected to the force transducer) with a certain amount of force, using their tongue. A water reward is then dispensed from the motorized water reservoir. This figure was originally published in Connor et al. ³⁶ Reprint with minor editing permission was obtained: https://marketplace.copyright.com/rs‐ui‐web/mp/license/83147258‐fcb1‐4789‐a709‐c9379048a58a/1aeed1a9‐1948‐491b‐ac6a‐bb3ef70d97ce. [Color figure can be viewed at wileyonlinelibrary.com]

2.2. Videofluoroscopy

Videofluoroscopic swallow study (VFSS) allows for radiographic imagining of bolus movement and swallowing physiology from the oral cavity to the esophagus. ³⁴ , ³⁵ , ⁴⁰ , ⁵³ , ⁵⁴ , ⁵⁵ Quantitative measures of deglutition including bolus speed, bolus area, and mastication rate have been validated in prior animal studies as clinically relevant measures of oral phase efficiency. Such outcomes provide information on potential physiological changes, thus enabling translation to human studies given anatomical similarities present between this model and humans. ³⁴ , ³⁵ , ⁴⁰ Further, assessment of swallow biomechanics and post‐swallow respiration using VFSS recordings provide critical information regarding deglutition. ³⁴ , ⁵⁶ , ⁵⁷ Analysis of these outcomes can provide clinically relevant insight into aspects of swallow physiology in both the oral and pharyngeal phases of swallowing.

All rats underwent baseline and post‐treatment/intervention recordings to compare potential changes both within and between groups. Rats were food restricted prior to recording and acclimated to smooth peanut butter placed on the side of the home cage prior to recording day. To conduct VFSS, rats were individually placed in their home cage on an L‐shaped platform perpendicular to the C‐arm fluoroscope (Genoray ZEN‐7000 C‐Arm 3rd Gen Fluoroscope; Origin Republic of Korea, Vendor Mulit Inc., Ontario, CA). A mixture of peanut butter and barium was placed on a stage affixed to the side of the home cage; rats were allowed to consume the mixture ad libitum for approximately 5 min (Figure 2). X‐ray was only initiated when the rat began to consume the mixture, as to avoid unnecessary radiation exposure. Swallows were recorded at 30 frames/s and analyzed offline, using MorphoJ for swallowing biomechanics, and ImageJ for all other measures.

Videofluoroscopic still image of rat consuming peanut butter and barium mixture.

2.3. Computational analysis of swallow mechanics adapted for the rodent model

Computational Analysis of Swallowing Mechanics (CASM) is a morphometric analysis software that has been used for studying swallowing biomechanics in humans with dysphagia, and has been adapted for use in rodents (CASM‐R). ⁵⁶ , ⁵⁸ CASM‐R tracks markers at skeletal levers formed by the hard palate, first and fourth cervical vertebrae, and mandible (Figure 3A) at each frame, in order to describe body and jaw movements during the swallow. Skeletal lever tracking also serves to re‐axis/“anchor” the position of soft tissue structures relative to the skeletal landmarks, allowing for more specific analysis of the isolated movement of swallowing structures, including the upper esophageal sphincter (UES) and base of tongue (BOT), without interference of gross body/jaw movements.

Representation of CASM‐R findings. Chemoradiation causes increased head and neck flexion (1, 7), and decreased pharyngeal shortening (4), and more inferior base of tongue positioning (8) during pharyngeal phase of swallowing in rats, consistent with reports in humans with HNC (D = 2.47, p < 0.0001). 1 = hard palate; 2 = 1st cervical vertebra; 3 = 4th cervical vertebra; 4 = upper esophageal sphincter (UES); 5–7 = mandible; 8 = base of tongue (BOT). Both RT and CCRT significantly altered pharyngeal phase swallowing kinematics (RT − D = 2.12, p < 0.0001, CV % variance = 31.6%; CCRT − D = 2.56, p < 0.0001, CV % variance = 57.3%). [Color figure can be viewed at wileyonlinelibrary.com]

Assessment of swallow biomechanics can provide information on potential musculoskeletal dysfunction through analysis of key muscular and skeletal landmarks affiliated with swallowing, thereby guiding investigation of the underlying mechanisms treatment may have on swallow physiology. ⁵⁶ An initial group of 16 male Sprague–Dawley rats (n = 4/group) were included for a preliminary pilot analysis, following methods previously described in Kletzien et al. and in alignment with published clinical work supporting significant outcomes with limited sample size, ¹⁶ , ¹⁷ to determine the impacts of treatment and exercise intervention on swallow biomechanics. ⁵⁶ Briefly, three VFSS recorded swallows were selected for analysis. Eight muscular and skeletal landmarks were identified—the hard palate, C1, C4, the UES, three mandibular points (anterior, mid, and posterior), and tongue base—and mapped in each frame of the individual swallow for multivariate morphometric analysis. The pharyngeal phase was defined as the frame immediately preceding swallow onset until the bolus head made contact with the UES. Swallows in which the rat's positioning was suboptimal for data analysis (i.e., obliqued, extraneous movement, or upper extremities blocking structures) were identified as outliers by MorphoJ ⁵⁹ and were subsequently excluded from final analysis, as inadequate positioning could provide incorrect data related to the positioning and movement of the key anatomical landmarks. In these cases, said excluded swallow was replaced with another from the same rat, selected at random. Following this preliminary pilot multivariate morphometric analysis, analysis of bolus kinematics and bolus area was completed to study the dynamic interaction on swallow function in a larger sample size. Given interpretation of CASM‐R findings is limited, the subsequent inclusion of kinematic analysis allowed for more robust assessment and subsequent conclusions of the relationship between HNC treatment, tongue exercise intervention, and physiologic outcomes.

2.4. Bolus kinematics and bolus area

Prior to analysis, three swallows were selected per rat. Selection was based on the following criteria: unobstructed sagittal view, adequate positioning during recording (ideally little to no movement, rat positioned straight without curvature of body/movement of limbs), and visualization of bolus from oral cavity (mastication) through esophagus. To measure bolus speed (mm/s), a marker was placed at the leading edge of the bolus (referred to as the head of the bolus), beginning at the frame immediately preceding swallow onset, and at each subsequent frame until the head of the bolus made contact with the UES. A marker was placed on the skull (rostral and posterior to the eye) at the frame before swallow onset, and again at the final frame of the swallow, in order to account for whole body movement. Bolus area was measured at the final frame of the swallow (when bolus head first encounters UES) as the slowed transit caused by impedance of the UES permits greater visualization of the bolus, with less interference of movement artifact on bolus edges. To further reduce measurement variability, the same bolus frame was measured 3 times, with the average used for final analysis. Pixel area was converted to mm² using a calibration factor derived from a 17.9 cm metal disc.

Mastication rate (cycles/s) was calculated from the frame of minimum jaw opening (jaw closure) following bolus acquisition, through five complete cycles of jaw opening‐closing, until the closure of the fifth cycle. All videos were analyzed by rater 1 (NSH), and a random subset of videos (10%) was analyzed by a second rater (AFP) to calculate inter‐rater reliability. Agreement among the raters was excellent (ICC = 0.99).

2.5. Jaw opening

Following results obtained from assessment of mastication rate, the length of jaw opening (aperture) was measured to investigate effects of treatment and intervention on mandibular range of motion. Three mastication cycles were selected, analyzed, and averaged per rat. The point of maximum jaw opening in a cycle was identified, and a line was drawn from the lowest point of the mandible (mid‐anterior) to the highest point of the hard palate. Measurements were taken pre‐ and post‐treatment/tongue exercise intervention for all groups.

2.6. Respiratory–swallow coordination

The typical process of deglutition involves a post‐swallow exhalation immediately following the swallow apnea period. ³⁴ , ⁶⁰ HNC treatments can impact coordination of breathing and swallowing, resulting in an unsafe post‐swallow inhale that elevates the risk of aspiration. ²⁰ A previous study in our lab confirmed the presence of this aberrant post‐swallow inhale pattern in a rat model of combined chemoradiation treatment, using a validated diaphragm tracking measure as a proxy for respiration. ³⁴ In the present study, an abbreviated version of this assay was used to determine the differential effects of CCRT, RT, and tongue exercise on respiratory–swallow coordination. The position of the diaphragm was visually tracked during the breathing cycle associated with each analyzed swallow, and a binary code was assigned for statistical analysis: post‐swallow exhale (0; Ex) or post‐swallow inhale (1; In). Raters, blinded to rat ID, group assignment, and time point, identified the onset frame and directionality of each phase: pre‐swallow respiration (In/Ex), swallow apnea (cessation of movement), and post‐swallow respiration (In/Ex). All files were analyzed by NSH, and 10% of all videos were analyzed by a second rater (LMR) for inter‐rater reliability (IRR = 90%).

3. STATISTICAL ANALYSIS

3.1. Swallow biomechanics

Procrustes fit was generated to evaluate the distribution of shape change among rats and highlight potential outliers. Following identification and removal of outliers, a canonical variate (CV) analysis was conducted to determine biomechanical differences between the groups. A discriminant function post hoc analysis was completed to visualize said changes through corrected eigenvectors. Mahalanobis distance (D) was used to indicate significance. To account for multiple comparisons across eight coordinates, a post hoc Bonferroni correction was performed with a corresponding set critical value of α < 0.006.

3.2. Bolus kinematics, bolus area, jaw opening, and post‐swallow respiration

To compare the effects of treatment and tongue exercise on bolus speed, bolus area, mastication rate, and jaw aperture within (pre vs. post time points) and between groups, a two‐way repeated measures analysis of variance (ANOVA; assumptions met) with pairwise comparisons and post hoc Bonferroni correction was conducted using SPSS (IBM, Chicago, IL). To assess potential changes in post‐swallow respiration patterns, descriptive statistics were generated (frequency and percentage of post‐swallow inhales across three trials per rat) to compare the two time points and four groups—RT without exercise, RT + TE, CCRT without exercise, and CCRT + TE. Given there were no aberrant post‐swallow inhales during the pre‐treatment and pre‐intervention time point (as expected for healthy controls), McNemar's test to assess repeated measures of a binary outcome could not be completed. As such, Fisher's exact test was conducted to assess the differences between groups in the post‐treatment and intervention time point. Further, to determine how bolus area and post‐swallow respiration impacted post‐bolus speed, an ANCOVA was conducted on post‐bolus speed data, with the covariates being pre‐treatment bolus speed, post‐treatment bolus area, and post‐swallow respiration using SAS. A critical value of α = 0.05 indicated significance.

4. RESULTS

A complete list of all variables and statistics is reported in Table 1.

TABLE 1.

Variables and results.

Outcome	Group	Result
	RT pre vs. post (pharyngeal phase)	D = 2.12; p < 0.0001
	CCRT pre vs. post (pharyngeal phase)	D = 2.56; p < 0.0001
	RT vs. CCRT (pharyngeal phase)	D = 2.20; p < 0.0001
	CCRT exercise vs. no exercise (pharyngeal phase)	D = 3.12; p < 0.0001
	CCRT exercise pre vs. post (pharyngeal phase)	D = 2.47; p < 0.0001
Bolus speed (covarying for bolus area)	Pre vs. post (time)	p = 0.043
	Time*treatment (pre vs. post)	p = 0.047
	Time*exercise (pre vs. post)	p = 0.019
	Timetreatmentexercise (pre vs. post)	p = 0.155
	CCRT vs. RT	p = 0.734
	Exercise vs. no exercise	p = 0.501
	Treatment*exercise	p = 0.948
Post‐bolus speed (covarying for pre‐ bolus speed, post‐bolus area, and post‐swallow respiration)	CCRT vs. RT (treatment)	p = 0.0329
	Exercise vs. no exercise	p = 0.0727
Bolus area	Pre vs. post (time)	p = 0.015
	Time*treatment (pre vs. post)	p = 0.124
	Time*exercise (pre vs. post)	p = 0.888
	Timetreatmentexercise (pre vs. post)	p = 0.334
	CCRT vs. RT (treatment)	p = 0.528
	Exercise vs. no exercise	p = 0.011
	Treatment*exercise	p = 0.009
Mastication rate	Pre vs. post (time)	p < 0.001
	Time*treatment (pre vs. post)	p = 0.073
	Time*exercise (pre vs. post)	p = 0.397
	Timetreatmentexercise (pre vs. post)	p = 0.102
	CCRT vs. RT (treatment)	p = 0.957
	Exercise vs. no exercise	p = 0.233
	Treatment*exercise	p = 0.043; pairwise comparison: p = 0.027
Jaw opening	Pre vs. post (time)	p < 0.001
	Time*treatment (pre vs. post)	p = 0.605
	Time*exercise (pre vs. post)	p = 0.433
	Timetreatmentexercise (pre vs. post)	p = 0.397
	CCRT vs. RT (treatment)	p = 0.078
	Exercise vs. no exercise	p = 0.222
	Treatment*exercise	p = 0.610
Post‐swallow respiration	Fischer's exact test comparing four groups (RT, RT + TE, CCRT, CCRT + TE)	p = 0.0394

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Note: Complete list of results for all outcomes. p < 0.05 indicates significance, significant results in bold.

Abbreviations: CCRT, chemoradiation treatment without exercise; CCRT + TE, chemoradiation treatment and tongue exercise; RT, radiation treatment without exercise; RT + TE, radiation treatment and tongue exercise.

4.1. Swallow biomechanics

Both RT and CCRT treatments significantly altered pharyngeal phase swallowing kinematics (RT − D = 2.12, p < 0.0001, 31.6% variance associated with RT; CCRT − D = 2.56, p < 0.0001, 57.3% variance associated with CCRT) (Figure 3B). CCRT group swallowing kinematics significantly differed from RT group (D = 2.20, p < 0.0001), with greater magnitude of positional change in those treated with CCRT compared with RT alone. Eigenvectors indicated rats treated with CCRT demonstrated increased head/neck flexion, reduced pharyngeal shortening, and impaired base of tongue retraction to posterior pharyngeal wall, which occurred lower in the pharynx compared to baseline (Figure 3C).

Rats that completed tongue exercise following chemoradiation treatment (CCRT + TE group) differed significantly from CCRT without tongue exercise (D = 3.12, p < 0.0001). Notably, post hoc eigenvectors indicated that while CCRT without exercise demonstrated increased head/neck flexion during pharyngeal swallow, as reported in clinical HNC studies using CASM, tongue exercise in CCRT increased head/neck extension (D = 2.47, p < 0.0001).

4.2. Bolus kinematics and bolus area

Kinematic analysis revealed an overall significant decrease in bolus speed (F _1,28 = 4.5, p = 0.043) pre‐ to post‐treatment overall, when accounting for bolus area (Figure 4) in rats treated with RT; significant within‐subject interactions between time and treatment (F _1,28 = 4.321, p = 0.047) as well as time and exercise (F _1,28 = 6.192, p = 0.019) were found pre‐ to post‐treatment. No significant differences between RT and CCRT and exercise versus no exercise intervention were observed.

Comparison of bolus speed (mm/s) pre‐ vs. post‐treatment. There was a significant decrease in bolus speed pre‐ to post‐treatment overall (p = 0.043). [Color figure can be viewed at wileyonlinelibrary.com]

There was a significant interaction between treatment and exercise for bolus area (F _1,28 = 7.835, p = 0.009). Rats in the RT + TE group swallowed significantly larger boluses than rats in the RT without exercise group (Figure 5). To assess how bolus area and post‐swallow respiration may impact bolus speed, a general linear regression model covarying for pre‐bolus speed, post‐bolus area, and post‐swallow respiration was conducted on post‐treatment/intervention bolus speed data. There was a significant main effect of treatment on bolus speed (F _1,31 = 5.10, p = 0.0329). Post hoc comparisons revealed rats treated with CCRT had significantly faster bolus speed compared to rats treated with RT. There was not a significant difference between exercise groups or post‐swallow respiration patterns for this outcome.

Comparison of bolus area (mm²) pre‐ vs. post‐treatment. Rats in the RT + TE group had significantly larger bolus area compared to the RT without exercise group (p = 0.009). [Color figure can be viewed at wileyonlinelibrary.com]

4.3. Jaw kinematics

Analysis revealed a main effect of time pre‐ to post‐treatment overall (F _1,28 = 17.345, p < 0.001) as well as a significant interaction between treatment and exercise post‐treatment (F _1,28 = 4.322, p = 0.047). Pairwise comparisons further revealed rats in the CCRT without exercise group had significantly faster mastication rates compared to rats in the CCRT + TE group (F _1,28 = 5.44, p = 0.027) (Figure 6). There was no significant change in mastication rate for rats in the CCRT + TE group when comparing baseline measures to measures recorded post‐treatment and intervention; interestingly, rats in this group maintained mastication rates similar to their baseline measures (pre‐mean rate = 4.99 cycles/s, post‐mean rate = 5.18 cycles/s).

Comparison of mastication rate (cycles/s) between CCRT without exercise and CCRT + TE groups. Rats in the CCRT without exercise group had significantly faster mastication rates compared to rats in the CCRT + TE group (p = 0.027). [Color figure can be viewed at wileyonlinelibrary.com]

Given these findings, and that trismus is a common occurrence post‐definitive treatment for HNC, we analyzed jaw opening to determine whether the unexpected finding of the CCRT without exercise group having faster mastication rate relative to CCRT + TE group could be attributable to reduced mandibular displacement. We hypothesized (1) rats treated with CCRT who did not undergo tongue exercise intervention would have reduced jaw opening compared to rats who did undergo tongue exercise intervention, and (2) rats who were treated with CCRT without exercise would have reduced jaw opening compared to rats treated with RT without exercise. There was a significant increase in jaw opening pre‐ to post‐treatment and intervention overall, regardless of treatment type or exercise condition (F _1,28 = 27.87, p < 0.001).

4.4. Swallowing and respiration

Fisher's exact test revealed a significant difference in respiratory–swallow coordination between the four groups post‐treatment/intervention (p = 0.0394). Descriptive statistics are provided in Table 2. Rats treated with CCRT exhibited comparable percentages of aberrant post‐swallow inhale both with tongue exercise intervention (25% of swallows) and without tongue exercise intervention (24% of swallows). Rats in the RT without exercise group exhibited aberrant post‐swallow inhale pattern in 29% of swallows. However, rats in the RT + TE group exhibited post‐swallow inhale in 0% of swallows.

TABLE 2.

Post‐swallow respiration descriptive statistics.

Group	Post‐swallow inhale frequency	Post‐swallow inhale percentage
CCRT without exercise	5/21^*	24%
CCRT + TE	6/24	25%
RT without exercise	7/24	29%
RT + TE	0/24	0%

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Note: Descriptive statistics. Frequency and percentage of post‐swallow inhale following treatment/intervention out of 24 trials (three swallows/rat) per group.

Abbreviations: CCRT, chemoradiation treatment; CCRT + TE, chemoradiation treatment and tongue exercise; RT, radiation treatment; RT + TE, radiation treatment and tongue exercise.

*One rat in the CCRT without exercise group did not have data at the post‐time point due to poor positioning and subsequent lack of diaphragm visualization.

5. DISCUSSION

Common treatments for head and neck cancer—RT and CCRT—have deleterious effects on swallowing and quality of life. ¹ , ² , ³ , ⁴ , ⁵ , ⁹ , ¹⁰ , ²⁵ , ⁶¹ Often, tongue press is one of a myriad of deglutition‐focused exercises recommended for patients during treatment, yet the isolated effects of lingual strengthening in this population are unclear. ²⁷ , ⁶² Prior research has demonstrated positive impacts of lingual strengthening on swallow function, particularly related to quality of life, bolus propulsion, and decreased residue and airway invasion. ⁶² , ⁶³ , ⁶⁴ In the current study, we assessed the impacts of RT and CCRT on: swallow biomechanics, bolus kinematics, jaw kinematics, and respiratory–swallow coordination, as well as the potential benefit of targeted tongue exercise intervention in the presence of treatment.

The purpose of this study was to characterize the effects of treatment and exercise on deglutition‐related kinematics in a translational model of radiation, with and without adjunctive chemotherapy, using clinically relevant outcome measures. We hypothesized that swallowing mechanics would differ from healthy baseline following RT and CCRT, with greater magnitude changes in CCRT. Our findings from CASM‐R analysis of rats treated with chemoradiation were consistent with clinical reports from CASM studies, ¹⁶ , ¹⁷ including increased head/neck flexion, reduced pharyngeal shortening, and impaired base of tongue retraction to posterior pharyngeal wall, which occurred lower in the pharynx compared to baseline. Further, morphometric analysis indicated greater magnitude of change in the chemoradiation treatment group compared to radiation treatment alone. Kinematic analysis also revealed clinical agreement in increased frequency of post‐swallow inhale events in RT and CCRT groups without tongue exercise, indicating this is an adequately representative model of aerodigestive discoordination.

Additionally, we hypothesized that tongue exercise would mitigate changes to swallowing kinematics following HNC treatment. Morphometric analysis of the relationship between treatment, swallow function, and exercise intervention in this translational rat model revealed significant impacts from both HNC treatment and tongue exercise intervention. Our CASM‐R analysis indicated that while the CCRT without exercise group presented with increased head/neck flexion during pharyngeal swallow, as reported in clinical HNC studies, CCRT with tongue exercise intervention resulted in increased head/neck extension (D = 2.47, p < 0.0001). These findings suggest HNC treatment has significant impacts on the underlying biomechanics of swallowing, and the addition of tongue exercise may be beneficial in mitigating such changes.

There was a significant decrease in bolus speed pre‐ to post‐treatment overall, suggesting mechanistic changes leading to alterations of efficient bolus movement through the pharynx. Clinical findings showing changes in mechanistic functions, including reduced pharyngeal stripping wave, bolus propulsion, tongue base retraction, and thus may correlate to observations from the current study. ⁴⁴ , ⁶⁵ , ⁶⁶ , ⁶⁷ , ⁶⁸ When co‐varying for baseline bolus speed, post‐treatment bolus area, and post‐treatment respiratory–swallow patterns, HNC treatment was found to significantly affect bolus speed post‐treatment. Specifically, rats treated with CCRT had significantly faster bolus speeds compared to rats treated with RT. However, faster bolus speed does not necessarily indicate a positive outcome, and could suggest a lack of regulation/structural control in this model. Similar findings of increased bolus speed have been noted in other translational models that assess swallow function (e.g., rat models of Parkinson disease), including similar conclusions of reduced bolus control and impaired efficiency. ⁶⁹ , ⁷⁰ Given that the current tongue exercise intervention paradigm did not significantly impact bolus speed, more intensive intervention may be warranted to observe a measurable benefit for this outcome in the presence of treatment.

Though not significant, bolus speed was slower in the RT + TE group compared to the CCRT + TE group. As noted in comparing means between the four groups, the addition of tongue exercise may help prevent significant dysregulation, potentially more so in the less severe treatment (RT) compared to CCRT given noted slower bolus speeds and less change between baseline and post‐treatment findings. Further, alterations in post‐swallow respiratory phase reset, though not found to be significantly correlated with post‐bolus speed in this study, can contribute to changes in sensory‐motor integration and thus impact functional deglutition. HNC treatments can lead to changes in sensory‐motor integration, particularly with regard to altered sensory input and related patterned response in the setting of changes to taste and oropharyngeal tissue, thereby impacting sequential structural functions involved in the deglutition process. ⁷ , ⁶⁵ , ⁷¹ , ⁷² A lack of regulated sequential movements of key structures involved in the process of swallowing can lead to airway compromise, reduced bolus clearance and subsequent, significant health consequences that have been observed clinically (e.g., aspiration pneumonia, weight loss, nutritional deficiency). ⁵ , ⁶⁵ , ⁶⁸ , ⁷³ , ⁷⁴ Overall, the differences between treatment groups observed in this study validate that CCRT is a more severe treatment and thus may lead to more dysregulation compared to RT. Further research is warranted to investigate such relationships.

There was an overall decrease in bolus area following RT and CCRT. Rats in the RT + TE group swallowed significantly larger boluses compared to rats in the RT without exercise group. This suggests the addition of tongue exercise intervention is beneficial in preserving function in the presence of treatment for rats treated with RT. The lack of similar benefit in the CCRT + TE group could therefore indicate 1) chemoradiation is a harsher treatment and thus 2) more intensive intervention may be warranted to observe a significant benefit for this outcome. Further, the decrease in bolus size observed in the RT group may relate to treatment‐induced alterations in sensory‐motor integration, or may demonstrate a behavioral response similar to patients self‐selecting a smaller bolus. ⁷⁵

Mastication rate is a common, robustly reliable measure used in both clinical and translational studies to represent mandibular coordination at the functional level. ⁵⁷ , ⁶⁹ , ⁷⁰ , ⁷⁶ Unexpectedly, we found that mastication rate increased post‐CCRT. To determine whether this increased rate was attributable to treatment‐related decrease in mandibular range of motion, we performed a subsequent analysis of jaw opening distance pre‐ to post‐treatment, and assessed comparisons between groups post‐treatment. Contrary to clinical findings, we found an overall increase in jaw opening regardless of treatment type or inclusion of tongue exercise intervention. Clinically, trismus is common in patients post‐treatment—many present with decreased mandibular range of motion. ¹² , ¹⁵ , ⁷⁷ , ⁷⁸ , ⁷⁹ Further research is warranted to assess this in the rat model.

Previous work has demonstrated alterations to swallow‐respiration coordination following neurological events, degenerative disease progression, and HNC treatments. ²⁰ , ³⁴ , ⁷⁴ , ⁸⁰ , ⁸¹ Discoordination of this system can compromise airway safety and lead to aspiration/aspiration pneumonia. ²⁰ , ²¹ , ³⁴ Our findings are consistent with prior studies demonstrating an increase in post‐swallow inhales following treatment. ³⁴ Further, Rowe et al., demonstrated associations between post‐swallow inhales and increased pharyngoesophageal bolus speed when comparing CCRT to naïve controls. ³⁴ This current study allowed for exploration between two different treatments, providing insight into which treatment may be the driving force behind this particular finding. The lack of post‐swallow inhales in the RT + TE group suggests that tongue exercise intervention may have contributed to preservation of a coordinated post‐swallow respiratory pattern after radiation treatment. The coordination of tongue movement in relation to deglutition has significant implications for swallow safety and efficiency, including respiratory–swallow coordination. Dysregulated tongue movements can negatively impact swallow function via lack of bolus control, decreased propulsion, and thus the coordination between swallowing and breathing; however, the addition of tongue exercise has shown to improve not only oropharyngeal swallow outcomes, but respiratory–swallow coordination in previous research via models of Parkinson disease. ¹⁸ , ¹⁹ Findings from the current study further supports the notion that the addition of CT to RT leads to worse outcomes and as such, may require more intensive intervention to overcome treatment‐induced deficits. ⁸² , ⁸³

Clinically, CCRT has been highlighted as the harsher of the two treatments, with notable corresponding sequelae including odynophagia and mucositis having significant impacts on both health status (due to reduced oral intake) and quality of life. ⁷ , ¹³ , ⁸⁴ , ⁸⁵ While difficult to assess the influences of such sequelae in this preclinical model, it is plausible they may influence the preclinical outcomes of the current study, in addition to related clinical outcomes. Additionally, though such sequelae have not previously been observed in this particular model, prior research has demonstrated the development of chemotherapy‐induced oral mucositis via intraperitoneal injection ⁸⁶ and administration of combined chemotherapy and radiation ⁸⁷ in the rat model. Future preclinical work tracking oral intake during treatment and acute recovery as well as examination of oral structures may help further elucidate potential influence.

The underlying mechanism by which RT and CCRT impact swallow function is poorly understood. Swallow deficits have been attributed to radiation‐induced tissue changes, such as fibrosis or nerve injury, yet are relatively unexplored. ⁸⁸ , ⁸⁹ Further, differing presentation between the two treatment conditions (RT and CCRT), and the differential impact of tongue exercise with these treatments observed in the present study suggest potential related differences in underlying mechanistic changes. The purpose of this translational study was to characterize treatment and exercises‐related impacts on clinically relevant swallow outcomes in a controlled model. Future investigation into underlying tissue changes, relation to treatment provided, and their correlations to observed swallow outcomes is warranted.

5.1. Limitations and future directions

While this study used a validated animal model to assess the impacts of treatment and exercise intervention on swallow‐related outcomes, there were several limitations. One consideration is that rats in our study were free of oncologic tissue pathology, such as tumor or lymphedema/lymphadenopathy, present within the head and neck region, compared to human patients. ⁹⁰ , ⁹¹ The size and location of tumor(s) themselves may impact swallow function due to impedance of structure‐specific movement (e.g., the tongue), and thus is an important clinical consideration when assessing deglutition in this patient population. However, analyzing changes to an otherwise healthy system was necessary in order to isolate the specific effects of RT and CCRT, without the interference of tumor‐specific effects on swallowing muscle biology and function. Further, given the region of treatment delivery in this study (8 × 12 mm² area to the tongue base), damage to the chemoreceptors and mechanoreceptors in the tongue base may have occurred. These components of the sensory system present in the tongue base convey critical information related to bolus size, location, composition, and movement, all of which can impact deglutition and thus may have contributed to findings from this present study. ³⁴ , ⁹² , ⁹³ , ⁹⁴ Additionally, this study did not investigate potential alterations to peripheral mechanisms or structures/tissues involved in swallowing, and as such, cannot definitively state the underlying mechanism by which treatment affects swallow function. Future work will address these limitations and upcoming directions.

6. CONCLUSION

Our study supports that RT and CCRT significantly alter swallowing biomechanics, aerodigestive kinematics, and bolus transit, and proposes that the addition of tongue‐based exercise intervention may be beneficial in mitigating these changes to prevent functional decline in the acute, post‐treatment phase of care. In the context of observed differences in the effects of tongue exercise on aerodigestive kinematics observed between RT and CCRT, continued analysis of the differential impact of HNC treatments on deglutition exercises is critical to optimizing swallowing‐related therapeutic outcomes. Future studies focused on underlying mechanistic changes as a result of treatment, intensity and timing of intervention initiation, and corresponding changes to swallow physiology and function can deepen understanding of dysphagia in the head and neck cancer population, thereby informing future clinical intervention methods.

CONFLICT OF INTEREST STATEMENT

The authors declare no conflicts of interest.

ETHICS STATEMENT

This work was completed under the approved IACUC protocol (M005828) and in accordance with current NIH animal use guidelines.

ACKNOWLEDGMENTS

The authors would like to thank Dr. Glen Leverson, Adele Poser, Jared Cullen, and Dr. Tim Hacker's lab personnel for their assistance. This work was funded by National Institute of Health, National Cancer Institute (NIH NCI) 5R37CA225608‐07; National Institute of Health, National Institute on Deafness and Other Communication Disorders (NIH, NIDCD) R01DC018584‐01; National Institute of Health, National Institute on Aging (NIH, NIA) F31AG077952‐01.

Schaen‐Heacock NE, Rowe LM, Ciucci MR, Russell JA. Effects of chemoradiation and tongue exercise on swallow biomechanics and bolus kinematics. Head & Neck. 2025;47(1):355‐370. doi: 10.1002/hed.27899

Results detailed in this manuscript were presented at the Dysphagia Research Society Annual Meeting in 2020 and 2022.

Section Editor: Patrick Ha

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.

REFERENCES

1. Katherine AH. Late radiation‐associated dysphagia (RAD) in head and neck cancer survivors. Perspect Swallowing Swallowing Disord. 2013;22(2):61‐72. doi: 10.1044/sasd22.2.61 [DOI] [Google Scholar]
2. Hutcheson KA, Yuk MM, Holsinger FC, Gunn GB, Lewin JS. Late radiation‐associated dysphagia with lower cranial neuropathy in long‐term oropharyngeal cancer survivors: video case reports. Head Neck. 2015;37(4):E56‐E62. doi: 10.1002/hed.23840 [DOI] [PubMed] [Google Scholar]
3. Hutcheson KA, Lewin JS, Barringer DA, et al. Late dysphagia after radiotherapy‐based treatment of head and neck cancer. Cancer. 2012;118(23):5793‐5799. doi: 10.1002/cncr.27631 [DOI] [PMC free article] [PubMed] [Google Scholar]
4. Hutcheson KA, Abualsamh AR, Sosa A, et al. Impact of selective neck dissection on chronic dysphagia after chemo‐intensity‐modulated radiotherapy for oropharyngeal carcinoma. Head Neck. 2016;38(6):886‐893. doi: 10.1002/hed.24195 [DOI] [PubMed] [Google Scholar]
5. Hutcheson KA, Nurgalieva Z, Zhao H, et al. Two‐year prevalence of dysphagia and related outcomes in head and neck cancer survivors: an updated SEER‐Medicare analysis. Head Neck. 2019;41(2):479‐487. doi: 10.1002/hed.25412 [DOI] [PMC free article] [PubMed] [Google Scholar]
6. Aylward A, Abdelaziz S, Hunt JP, et al. Rates of dysphagia‐related diagnoses in long‐term survivors of head and neck cancers. Otolaryngol Head Neck Surg. 2019;161(4):643‐651. doi: 10.1177/0194599819850154 [DOI] [PMC free article] [PubMed] [Google Scholar]
7. Sroussi HY, Epstein JB, Bensadoun R‐J, et al. Common oral complications of head and neck cancer radiation therapy: mucositis, infections, saliva change, fibrosis, sensory dysfunctions, dental caries, periodontal disease, and osteoradionecrosis. Cancer Med. 2017;6(12):2918‐2931. doi: 10.1002/cam4.1221 [DOI] [PMC free article] [PubMed] [Google Scholar]
8. Rogers SN, Heseltine N, Flexen J, Winstanley HR, Cole‐Hawkins H, Kanatas A. Structured review of papers reporting specific functions in patients with cancer of the head and neck: 2006–2013. Br J Oral Maxillofac Surg. 2016;54(6):e45‐e51. doi: 10.1016/j.bjoms.2016.02.012 [DOI] [PubMed] [Google Scholar]
9. Davis LA. Quality of life issues related to dysphagia. Top Geriatr Rehabil. 2007;23(4):352‐365. doi: 10.1097/01.TGR.0000299163.46655.48 [DOI] [Google Scholar]
10. May AH, Hiner ED, Feldman E. Oral integrity related to head and neck cancer treatment. Perspect Swallowing Swallowing Disord. 2012;21(1):28‐33. doi: 10.1044/sasd21.1.28 [DOI] [Google Scholar]
11. Pauloski BR. Rehabilitation of dysphagia following head and neck cancer. Phys Med Rehabil Clin N Am. 2008;19(4):889‐928. doi: 10.1016/j.pmr.2008.05.010 [DOI] [PMC free article] [PubMed] [Google Scholar]
12. Sandler ML, Lazarus CL, Ru M, et al. Effects of jaw exercise intervention timing on outcomes following oral and oropharyngeal cancer surgery: pilot study. Head Neck. 2019;41(11):3806‐3817. doi: 10.1002/hed.25908 [DOI] [PubMed] [Google Scholar]
13. Moroney LB, Helios J, Ward EC, et al. Patterns of dysphagia and acute toxicities in patients with head and neck cancer undergoing helical IMRT ± concurrent chemotherapy. Oral Oncol. 2017;64:1‐8. doi: 10.1016/j.oraloncology.2016.11.009 [DOI] [PubMed] [Google Scholar]
14. Son YR, Choi KH, Kim TG. Dysphagia in tongue cancer patients. Ann Rehabil Med. 2015;39(2):210‐217. doi: 10.5535/arm.2015.39.2.210 [DOI] [PMC free article] [PubMed] [Google Scholar]
15. Ahlberg A, Engström T, Nikolaidis P, et al. Early self‐care rehabilitation of head and neck cancer patients. Acta Otolaryngol. 2011;131(5):552‐561. doi: 10.3109/00016489.2010.532157 [DOI] [PMC free article] [PubMed] [Google Scholar]
16. Tadavarthi Y, Hosseini P, Reyes SE, Focht Garand KL, Pisegna JM, Pearson WGJ. Pilot study of quantitative methods for differentiating pharyngeal swallowing mechanics by dysphagia etiology. Dysphagia. 2021;36(2):231‐241. doi: 10.1007/s00455-020-10123-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
17. Hosseini P, Tadavarthi Y, Martin‐Harris B, Pearson WGJ. Functional modules of pharyngeal swallowing mechanics. Laryngoscope Investig Otolaryngol. 2019;4(3):341‐346. doi: 10.1002/lio2.273 [DOI] [PMC free article] [PubMed] [Google Scholar]
18. Ouahchi Y, Marie JP, Verin E. Effect of lingual paralysis on swallowing and breathing coordination in rats. Respir Physiol Neurobiol. 2012;181(1):95‐98. doi: 10.1016/j.resp.2012.01.009 [DOI] [PubMed] [Google Scholar]
19. Wang C‐M, Shieh W‐Y, Ho C‐S, Hu Y‐W, Wu Y‐R. Home‐based orolingual exercise improves the coordination of swallowing and respiration in early Parkinson disease: a quasi‐experimental before‐and‐after exercise program study. Front Neurol. 2018;9:624. doi: 10.3389/fneur.2018.00624 [DOI] [PMC free article] [PubMed] [Google Scholar]
20. Martin‐Harris B, McFarland D, Hill EG, et al. Respiratory‐swallow training in patients with head and neck cancer. Arch Phys Med Rehabil. 2015;96(5):885‐893. doi: 10.1016/j.apmr.2014.11.022 [DOI] [PMC free article] [PubMed] [Google Scholar]
21. Martin‐Harris B, Garand KLF, McFarland D. Optimizing respiratory‐swallowing coordination in patients with oropharyngeal head and neck cancer. Perspect ASHA Spec Interes Groups. 2017;2(13):103‐110. doi: 10.1044/persp2.SIG13.103 [DOI] [PMC free article] [PubMed] [Google Scholar]
22. Brodsky MB, McFarland DH, Dozier TS, et al. Respiratory‐swallow phase patterns and their relationship to swallowing impairment in patients treated for oropharyngeal cancer. Head Neck. 2010;32(4):481‐489. doi: 10.1002/hed.21209 [DOI] [PMC free article] [PubMed] [Google Scholar]
23. Greco E, Simic T, Ringash J, Tomlinson G, Inamoto Y, Martino R. Dysphagia treatment for patients with head and neck cancer undergoing radiation therapy: a meta‐analysis review. Int J Radiat Oncol Biol Phys. 2018;101(2):421‐444. doi: 10.1016/j.ijrobp.2018.01.097 [DOI] [PubMed] [Google Scholar]
24. Ajmani GS, Nocon CC, Brockstein BE, et al. Association of a proactive swallowing rehabilitation program with feeding tube placement in patients treated for pharyngeal cancer. JAMA Otolaryngol Head Neck Surg. 2018;144(6):483‐488. doi: 10.1001/jamaoto.2018.0278 [DOI] [PMC free article] [PubMed] [Google Scholar]
25. Hutcheson KA, Bhayani MK, Beadle BM, et al. Eat and exercise during radiotherapy or chemoradiotherapy for pharyngeal cancers: use it or lose it. JAMA Otolaryngol Head Neck Surg. 2013;139(11):1127‐1134. doi: 10.1001/jamaoto.2013.4715 [DOI] [PMC free article] [PubMed] [Google Scholar]
26. Krekeler BN, Rowe LM, Connor NP. Dose in exercise‐based dysphagia therapies: a scoping review. Dysphagia. 2021;36(1):1‐32. doi: 10.1007/s00455-020-10104-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
27. Lazarus C. Tongue strength and exercise in healthy individuals and in head and neck cancer patients. Semin Speech Lang. 2006;27(4):260‐267. doi: 10.1055/s-2006-955116 [DOI] [PubMed] [Google Scholar]
28. Van den Steen L, Baudelet M, Tomassen P, Bonte K, De Bodt M, Van Nuffelen G. Effect of tongue‐strengthening exercises on tongue strength and swallowing‐related parameters in chronic radiation‐associated dysphagia. Head Neck. 2020;42(9):2298‐2307. doi: 10.1002/hed.26179 [DOI] [PubMed] [Google Scholar]
29. Perry A, Lee SH, Cotton S, Kennedy C. Therapeutic exercises for affecting post‐treatment swallowing in people treated for advanced‐stage head and neck cancers. Cochrane Database Syst Rev. 2016;2016(8):CD011112. doi: 10.1002/14651858.CD011112.pub2 [DOI] [PMC free article] [PubMed] [Google Scholar]
30. Constantinescu G, Rieger J, Seikaly H, Eurich D. Adherence to home‐based swallowing therapy using a mobile system in head and neck cancer survivors. Am J Speech‐Language Pathol. 2021;30(6):2465‐2475. doi: 10.1044/2021_AJSLP-21-00026 [DOI] [PubMed] [Google Scholar]
31. Govender R, Smith CH, Taylor SA, Barratt H, Gardner B. Swallowing interventions for the treatment of dysphagia after head and neck cancer: a systematic review of behavioural strategies used to promote patient adherence to swallowing exercises. BMC Cancer. 2017;17(1):43. doi: 10.1186/s12885-016-2990-x [DOI] [PMC free article] [PubMed] [Google Scholar]
32. Shinn EH, Basen‐Engquist K, Baum G, et al. Adherence to preventive exercises and self‐reported swallowing outcomes in post‐radiation head and neck cancer patients. Head Neck. 2013;35(12):1707‐1712. doi: 10.1002/hed.23255 [DOI] [PMC free article] [PubMed] [Google Scholar]
33. Russell JA, Connor NP. Effects of age and radiation treatment on function of extrinsic tongue muscles. Radiat Oncol. 2014;9:254. doi: 10.1186/s13014-014-0254-y [DOI] [PMC free article] [PubMed] [Google Scholar]
34. Rowe LM, Connor NP, Russell JA. Respiratory‐swallow coordination in a rat model of chemoradiation. Head Neck. 2021;43(10):2954‐2966. doi: 10.1002/hed.26782 [DOI] [PMC free article] [PubMed] [Google Scholar]
35. Krekeler BN, Weycker JM, Connor NP. Effects of tongue exercise frequency on tongue muscle biology and swallowing physiology in a rat model. Dysphagia. 2020;35(6):918‐934. doi: 10.1007/s00455-020-10105-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
36. Connor NP, Russell JA, Wang H, et al. Effect of tongue exercise on protrusive force and muscle fiber area in aging rats. J Speech Lang Hear Res. 2009;52(3):732‐744. doi: 10.1044/1092-4388(2008/08-0105) [DOI] [PMC free article] [PubMed] [Google Scholar]
37. Kletzien H, Russell JA, Leverson GE, Connor NP. Differential effects of targeted tongue exercise and treadmill running on aging tongue muscle structure and contractile properties. J Appl Physiol. 2012;114(4):472‐481. doi: 10.1152/japplphysiol.01370.2012 [DOI] [PMC free article] [PubMed] [Google Scholar]
38. Schaser AJ, Ciucci MR, Connor NP. Cross‐activation and detraining effects of tongue exercise in aged rats. Behav Brain Res. 2016;297:285‐296. doi: 10.1016/j.bbr.2015.10.030 [DOI] [PMC free article] [PubMed] [Google Scholar]
39. Broadfoot CK, Hoffmeister JD, Lechner SA, et al. Tongue and laryngeal exercises improve tongue strength and vocal function outcomes in a Pink1−/− rat model of early Parkinson disease. Behav Brain Res. 2024;460:114754. doi: 10.1016/j.bbr.2023.114754 [DOI] [PMC free article] [PubMed] [Google Scholar]
40. Krekeler BN, Connor NP. Age‐related changes in mastication are not improved by tongue exercise in a rat model. Laryngoscope. 2017;127(1):E29‐E34. doi: 10.1002/lary.26045 [DOI] [PMC free article] [PubMed] [Google Scholar]
41. Glass TJ, Figueroa JE, Russell JA, Krekeler BN, Connor NP. Progressive protrusive tongue exercise does not alter aging effects in retrusive tongue muscles. Front Physiol. 2021;12:740876. doi: 10.3389/fphys.2021.740876 [DOI] [PMC free article] [PubMed] [Google Scholar]
42. Cullins MJ, Krekeler BN, Connor NP. Differential impact of tongue exercise on intrinsic lingual muscles. Laryngoscope. 2018;128(10):2245‐2251. doi: 10.1002/lary.27044 [DOI] [PMC free article] [PubMed] [Google Scholar]
43. Krekeler BN, Leverson G, Connor NP. Tongue exercise and ageing effects on morphological and biochemical properties of the posterior digastric and temporalis muscles in a Fischer 344 Brown Norway rat model. Arch Oral Biol. 2018;89:37‐43. doi: 10.1016/j.archoralbio.2018.02.002 [DOI] [PMC free article] [PubMed] [Google Scholar]
44. Pauloski BR, Logemann JA. Impact of tongue base and posterior pharyngeal wall biomechanics on pharyngeal clearance in irradiated postsurgical oral and oropharyngeal cancer patients. Head Neck. 2000;22(2):120‐131. [DOI] [PubMed] [Google Scholar]
45. Wall LR, Ward EC, Cartmill B, Hill AJ. Physiological changes to the swallowing mechanism following (chemo)radiotherapy for head and neck cancer: a systematic review. Dysphagia. 2013;28(4):481‐493. doi: 10.1007/s00455-013-9491-8 [DOI] [PubMed] [Google Scholar]
46. Lalla RV, Treister N, Sollecito T, et al. Oral complications at 6 months after radiation therapy for head and neck cancer. Oral Dis. 2017;23(8):1134‐1143. doi: 10.1111/odi.12710 [DOI] [PMC free article] [PubMed] [Google Scholar]
47. Fowler JF. 21 years of biologically effective dose. Br J Radiol. 2010;83(991):554‐568. doi: 10.1259/bjr/31372149 [DOI] [PMC free article] [PubMed] [Google Scholar]
48. Fowler JF. The linear‐quadratic formula and progress in fractionated radiotherapy. Br J Radiol. 1989;62(740):679‐694. doi: 10.1259/0007-1285-62-740-679 [DOI] [PubMed] [Google Scholar]
49. Osman N, Elamin YY, Rafee S, et al. Weekly cisplatin concurrently with radiotherapy in head and neck squamous cell cancer: a retrospective analysis of a tertiary institute experience. Eur Arch Oto‐Rhino‐Laryngol. 2014;271(8):2253‐2259. doi: 10.1007/s00405-013-2749-9 [DOI] [PubMed] [Google Scholar]
50. Helfenstein S, Riesterer O, Meier UR, et al. 3‐weekly or weekly cisplatin concurrently with radiotherapy for patients with squamous cell carcinoma of the head and neck—a multicentre, retrospective analysis. Radiat Oncol. 2019;14(1):32. doi: 10.1186/s13014-019-1235-y [DOI] [PMC free article] [PubMed] [Google Scholar]
51. Cullins MJ, Wenninger JM, Cullen JS, Russell JA, Kleim JA, Connor NP. Tongue force training induces plasticity of the lingual motor cortex in Young adult and aged rats. Front Neurosci. 2019;13:1355. doi: 10.3389/fnins.2019.01355 [DOI] [PMC free article] [PubMed] [Google Scholar]
52. Ciucci MR, Russell JA, Schaser AJ, Doll EJ, Vinney LM, Connor NP. Tongue force and timing deficits in a rat model of Parkinson disease. Behav Brain Res. 2011;222(2):315‐320. doi: 10.1016/j.bbr.2011.03.057 [DOI] [PMC free article] [PubMed] [Google Scholar]
53. Hunter KU, Schipper M, Feng FY, et al. Toxicities affecting quality of life after chemo‐IMRT of oropharyngeal cancer: prospective study of patient‐reported, observer‐rated, and objective outcomes. Int J Radiat Oncol Biol Phys. 2013;85(4):935‐940. doi: 10.1016/j.ijrobp.2012.08.030 [DOI] [PMC free article] [PubMed] [Google Scholar]
54. Brooks L, Landry A, Deshpande A, Marchica C, Cooley A, Raol N. Posterior tongue tie, base of tongue movement, and pharyngeal dysphagia: what is the connection? Dysphagia. 2020;35(1):129‐132. doi: 10.1007/s00455-019-10040-x [DOI] [PubMed] [Google Scholar]
55. Knigge MA, Thibeault S, McCulloch TM. Implementation of high‐resolution manometry in the clinical practice of speech language pathology. Dysphagia. 2014;29(1):2‐16. doi: 10.1007/s00455-013-9494-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
56. Kletzien H, Connor NP. Computational analysis of swallowing mechanics in an aging rodent model. Frontiers in Optics 2017. OSA Technical Digest. Optical Society of America; 2017. doi: 10.1364/FIO.2017.JTu2A.83 [DOI] [Google Scholar]
57. Kletzien H, Cullins MJ, Connor NP. Age‐related alterations in swallowing biomechanics. Exp Gerontol. 2019;118:45‐50. doi: 10.1016/j.exger.2019.01.006 [DOI] [PMC free article] [PubMed] [Google Scholar]
58. Schwertner RW, Garand KL, Pearson WGJ. A novel imaging analysis method for capturing pharyngeal constriction during swallowing. J Imaging Sci. 2016;1:1. [PMC free article] [PubMed] [Google Scholar]
59. Klingenberg CP. MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour. 2011;11(2):353‐357. doi: 10.1111/j.1755-0998.2010.02924.x [DOI] [PubMed] [Google Scholar]
60. McFarland DH, Martin‐Harris B, Fortin A‐J, Humphries K, Hill E, Armeson K. Respiratory‐swallowing coordination in normal subjects: lung volume at swallowing initiation. Respir Physiol Neurobiol. 2016;234:89‐96. doi: 10.1016/j.resp.2016.09.004 [DOI] [PMC free article] [PubMed] [Google Scholar]
61. Goepfert RP, Lewin JS, Barrow MP, et al. Long‐term patient‐reported dysphagia in low‐risk oropharyngeal carcinoma after intensity modulated radiation therapy. Int J Radiat Oncol. 2016;94(4):963‐964. doi: 10.1016/j.ijrobp.2015.12.329 [DOI] [PMC free article] [PubMed] [Google Scholar]
62. Lazarus CL, Husaini H, Falciglia D, et al. Effects of exercise on swallowing and tongue strength in patients with oral and oropharyngeal cancer treated with primary radiotherapy with or without chemotherapy. Int J Oral Maxillofac Surg. 2014;43:523‐530. doi: 10.1016/j.ijom.2013.10.023 [DOI] [PMC free article] [PubMed] [Google Scholar]
63. Van Nuffelen G, Vanderwegen J, Guns C, Van den Steen L, de Bodt M. Effect of tongue strength training in head and neck cancer (HNC) patients treated with chemoradiation (CRT) or radiotherapy (RT). Dysphagia. 2022;28:300. [Google Scholar]
64. Smaoui S, Langridge A, Steele CM. The effect of lingual resistance training interventions on adult swallow function: a systematic review. Dysphagia. 2019;35:745‐761. doi: 10.1007/s00455-019-10066-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
65. Xinou E, Chryssogonidis I, Kalogera‐Fountzila A, Panagiotopoulou‐Mpoukla D, Printza A. Longitudinal evaluation of swallowing with videofluoroscopy in patients with locally advanced head and neck cancer after chemoradiation. Dysphagia. 2018;33(5):691‐706. doi: 10.1007/s00455-018-9889-4 [DOI] [PubMed] [Google Scholar]
66. Gharzai LA, Li P, Schipper MJ, et al. Characterization of very late dysphagia after chemoradiation for oropharyngeal squamous cell carcinoma. Oral Oncol. 2020;111:104853. doi: 10.1016/j.oraloncology.2020.104853 [DOI] [PubMed] [Google Scholar]
67. Carmignani I, Locatello LG, Desideri I, et al. Analysis of dysphagia in advanced‐stage head‐and‐neck cancer patients: impact on quality of life and development of a preventive swallowing treatment. Eur Arch Oto‐Rhino‐Laryngol. 2018;275(8):2159‐2167. doi: 10.1007/s00405-018-5054-9 [DOI] [PubMed] [Google Scholar]
68. Pisegna JM, Langmore SE, Meyer TK, Pauloski B. Swallowing patterns in the HNC population: timing of penetration‐aspiration events and residue. Otolaryngol Neck Surg. 2020;163(6):1232‐1239. doi: 10.1177/0194599820933883 [DOI] [PubMed] [Google Scholar]
69. Russell JA, Ciucci MR, Hammer MJ, Connor NP. Videofluorographic assessment of deglutitive behaviors in a rat model of aging and Parkinson disease. Dysphagia. 2013;28(1):95‐104. doi: 10.1007/s00455-012-9417-x [DOI] [PMC free article] [PubMed] [Google Scholar]
70. Cullen KP, Grant LM, Kelm‐Nelson CA, et al. Pink1 −/− rats show early‐onset swallowing deficits and correlative brainstem pathology. Dysphagia. 2018;33(6):749‐758. doi: 10.1007/s00455-018-9896-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
71. Lowell SY, Poletto CJ, Knorr‐Chung BR, Reynolds RC, Simonyan K, Ludlow CL. Sensory stimulation activates both motor and sensory components of the swallowing system. Neuroimage. 2008;42(1):285‐295. doi: 10.1016/j.neuroimage.2008.04.234 [DOI] [PMC free article] [PubMed] [Google Scholar]
72. Riantiningtyas RR, Carrouel F, Bruyas A, et al. Oral somatosensory alterations in head and neck cancer patients‐an overview of the evidence and causes. Cancers (Basel). 2023;15(3):718. doi: 10.3390/cancers15030718 [DOI] [PMC free article] [PubMed] [Google Scholar]
73. Denaro N, Merlano MC, Russi EG. Dysphagia in head and neck cancer patients: pretreatment evaluation, predictive factors, and assessment during radio‐chemotherapy, recommendations. Clin Exp Otorhinolaryngol. 2013;6(3):117‐126. doi: 10.3342/ceo.2013.6.3.117 [DOI] [PMC free article] [PubMed] [Google Scholar]
74. Leslie P, Drinnan MJ, Ford GA, Wilson JA. Swallow respiration patterns in dysphagic patients following acute stroke. Dysphagia. 2002;17(3):202‐207. doi: 10.1007/s00455-002-0053-8 [DOI] [PubMed] [Google Scholar]
75. Dziadziola J, Hamlet S, Michou G, Jones L. Multiple swallows and piecemeal deglutition; observations from normal adults and patients with head and neck cancer. Dysphagia. 1992;7(1):8‐11. doi: 10.1007/BF02493415 [DOI] [PubMed] [Google Scholar]
76. Lever TE, Gorsek A, Cox KT, et al. An animal model of oral dysphagia in amyotrophic lateral sclerosis. Dysphagia. 2008;24(2):180‐195. doi: 10.1007/s00455-008-9190-z [DOI] [PubMed] [Google Scholar]
77. de Groot RJ, Wetzels J‐W, Merkx MAW, et al. Masticatory function and related factors after oral oncological treatment: a 5‐year prospective study. Head Neck. 2019;41(1):216‐224. doi: 10.1002/hed.25445 [DOI] [PMC free article] [PubMed] [Google Scholar]
78. van der Molen L, van Rossum MA, Burkhead LM, Smeele LE, Rasch CRN, Hilgers FJM. A randomized preventive rehabilitation trial in advanced head and neck cancer patients treated with chemoradiotherapy: feasibility, compliance, and short‐term effects. Dysphagia. 2011;26(2):155‐170. doi: 10.1007/s00455-010-9288-y [DOI] [PMC free article] [PubMed] [Google Scholar]
79. Karsten RT, van der Molen L, Hamming‐Vrieze O, et al. Long‐term swallowing, trismus, and speech outcomes after combined chemoradiotherapy and preventive rehabilitation for head and neck cancer; 10‐year plus update. Head Neck. 2020;42:1907‐1918. doi: 10.1002/hed.26120 [DOI] [PubMed] [Google Scholar]
80. Hadjikoutis S, Pickersgill TP, Dawson K, Wiles CM. Abnormal patterns of breathing during swallowing in neurological disorders. Brain. 2000;123:1863‐1873. doi: 10.1093/brain/123.9.1863 [DOI] [PubMed] [Google Scholar]
81. Pinnington LL, Muhiddin KA, Ellis RE, Playford ED. Non‐invasive assessment of swallowing and respiration in Parkinson's disease. J Neurol. 2000;247(10):773‐777. doi: 10.1007/s004150070091 [DOI] [PubMed] [Google Scholar]
82. Tulunay‐Ugur OE, McClinton C, Young Z, Penagaricano JA, Maddox A‐M, Vural E. Functional outcomes of Chemoradiation in patients with head and neck cancer. Otolaryngol Neck Surg. 2012;148(1):64‐68. doi: 10.1177/0194599812459325 [DOI] [PubMed] [Google Scholar]
83. Lazarus CL. Effects of chemoradiotherapy on voice and swallowing. Curr Opin Otolaryngol Head Neck Surg. 2009;17(3):172‐178. doi: 10.1097/MOO.0b013e32832af12f [DOI] [PMC free article] [PubMed] [Google Scholar]
84. Murphy BA, Gilbert J. Dysphagia in head and neck cancer patients treated with radiation: assessment, sequelae, and rehabilitation. Semin Radiat Oncol. 2009;19:35‐42. doi: 10.1016/j.semradonc.2008.09.007 [DOI] [PubMed] [Google Scholar]
85. Lazarus CL, Logemann JA, Pauloski BR, et al. Swallowing and tongue function following treatment for oral and oropharyngeal cancer. J Speech Lang Hear Res. 2000;43:1011‐1023. doi: 10.1044/jslhr.4304.1011 [DOI] [PubMed] [Google Scholar]
86. Kim DOH, Choi J, Lim Y‐S, Huh HJ, Cho CG, Kim BH. A rat model for oral mucositis induced by a single administration of 5‐fluorouracil. In Vivo. 2023;37(1):218‐224. doi: 10.21873/invivo.13070 [DOI] [PMC free article] [PubMed] [Google Scholar]
87. Patel A, Rajesh S, Chandrashekhar VM, et al. A rat model against chemotherapy plus radiation‐induced oral mucositis. Saudi Pharm J. 2013;21(4):399‐403. doi: 10.1016/j.jsps.2012.11.003 [DOI] [PMC free article] [PubMed] [Google Scholar]
88. King SN, Dunlap NE, Tennant PA, Pitts T. Pathophysiology of radiation‐induced dysphagia in head and neck cancer. Dysphagia. 2016;31(3):339‐351. doi: 10.1007/s00455-016-9710-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
89. Zhou Y, Sheng X, Deng F, et al. Radiation‐induced muscle fibrosis rat model: establishment and valuation. Radiat Oncol. 2018;13(1):160. doi: 10.1186/s13014-018-1104-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
90. Starmer H, Sanguineti G, Marur S, Gourin CG. Multidisciplinary head and neck cancer clinic and adherence with speech pathology. Laryngoscope. 2011;121(10):2131‐2135. doi: 10.1002/lary.21746 [DOI] [PubMed] [Google Scholar]
91. Stenson KM, MacCracken E, List M, et al. Swallowing function in patients with head and neck cancer prior to treatment. Arch Otolaryngol Neck Surg. 2000;126(3):371‐377. doi: 10.1001/archotol.126.3.371 [DOI] [PubMed] [Google Scholar]
92. Steele CM, Miller AJ. Sensory input pathways and mechanisms in swallowing: a review. Dysphagia. 2010;25(4):323‐333. doi: 10.1007/s00455-010-9301-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
93. Miller AJ. Oral and pharyngeal reflexes in the mammalian nervous system: their diverse range in complexity and the pivotal role of the tongue. Crit Rev Oral Biol Med. 2002;13(5):409‐425. doi: 10.1177/154411130201300505 [DOI] [PubMed] [Google Scholar]
94. Sweazey RD, Bradley RM. Responses of neurons in the lamb nucleus tractus solitarius to stimulation of the caudal oral cavity and epiglottis with different stimulus modalities. Brain Res. 1989;480(1–2):133‐150. doi: 10.1016/0006-8993(89)91576-x [DOI] [PubMed] [Google Scholar]

Associated Data

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

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

[hed27899-bib-0001] 1. Katherine AH. Late radiation‐associated dysphagia (RAD) in head and neck cancer survivors. Perspect Swallowing Swallowing Disord. 2013;22(2):61‐72. doi: 10.1044/sasd22.2.61 [DOI] [Google Scholar]

[hed27899-bib-0002] 2. Hutcheson KA, Yuk MM, Holsinger FC, Gunn GB, Lewin JS. Late radiation‐associated dysphagia with lower cranial neuropathy in long‐term oropharyngeal cancer survivors: video case reports. Head Neck. 2015;37(4):E56‐E62. doi: 10.1002/hed.23840 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0003] 3. Hutcheson KA, Lewin JS, Barringer DA, et al. Late dysphagia after radiotherapy‐based treatment of head and neck cancer. Cancer. 2012;118(23):5793‐5799. doi: 10.1002/cncr.27631 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0004] 4. Hutcheson KA, Abualsamh AR, Sosa A, et al. Impact of selective neck dissection on chronic dysphagia after chemo‐intensity‐modulated radiotherapy for oropharyngeal carcinoma. Head Neck. 2016;38(6):886‐893. doi: 10.1002/hed.24195 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0005] 5. Hutcheson KA, Nurgalieva Z, Zhao H, et al. Two‐year prevalence of dysphagia and related outcomes in head and neck cancer survivors: an updated SEER‐Medicare analysis. Head Neck. 2019;41(2):479‐487. doi: 10.1002/hed.25412 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0006] 6. Aylward A, Abdelaziz S, Hunt JP, et al. Rates of dysphagia‐related diagnoses in long‐term survivors of head and neck cancers. Otolaryngol Head Neck Surg. 2019;161(4):643‐651. doi: 10.1177/0194599819850154 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0007] 7. Sroussi HY, Epstein JB, Bensadoun R‐J, et al. Common oral complications of head and neck cancer radiation therapy: mucositis, infections, saliva change, fibrosis, sensory dysfunctions, dental caries, periodontal disease, and osteoradionecrosis. Cancer Med. 2017;6(12):2918‐2931. doi: 10.1002/cam4.1221 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0008] 8. Rogers SN, Heseltine N, Flexen J, Winstanley HR, Cole‐Hawkins H, Kanatas A. Structured review of papers reporting specific functions in patients with cancer of the head and neck: 2006–2013. Br J Oral Maxillofac Surg. 2016;54(6):e45‐e51. doi: 10.1016/j.bjoms.2016.02.012 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0009] 9. Davis LA. Quality of life issues related to dysphagia. Top Geriatr Rehabil. 2007;23(4):352‐365. doi: 10.1097/01.TGR.0000299163.46655.48 [DOI] [Google Scholar]

[hed27899-bib-0010] 10. May AH, Hiner ED, Feldman E. Oral integrity related to head and neck cancer treatment. Perspect Swallowing Swallowing Disord. 2012;21(1):28‐33. doi: 10.1044/sasd21.1.28 [DOI] [Google Scholar]

[hed27899-bib-0011] 11. Pauloski BR. Rehabilitation of dysphagia following head and neck cancer. Phys Med Rehabil Clin N Am. 2008;19(4):889‐928. doi: 10.1016/j.pmr.2008.05.010 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0012] 12. Sandler ML, Lazarus CL, Ru M, et al. Effects of jaw exercise intervention timing on outcomes following oral and oropharyngeal cancer surgery: pilot study. Head Neck. 2019;41(11):3806‐3817. doi: 10.1002/hed.25908 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0013] 13. Moroney LB, Helios J, Ward EC, et al. Patterns of dysphagia and acute toxicities in patients with head and neck cancer undergoing helical IMRT ± concurrent chemotherapy. Oral Oncol. 2017;64:1‐8. doi: 10.1016/j.oraloncology.2016.11.009 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0014] 14. Son YR, Choi KH, Kim TG. Dysphagia in tongue cancer patients. Ann Rehabil Med. 2015;39(2):210‐217. doi: 10.5535/arm.2015.39.2.210 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0015] 15. Ahlberg A, Engström T, Nikolaidis P, et al. Early self‐care rehabilitation of head and neck cancer patients. Acta Otolaryngol. 2011;131(5):552‐561. doi: 10.3109/00016489.2010.532157 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0016] 16. Tadavarthi Y, Hosseini P, Reyes SE, Focht Garand KL, Pisegna JM, Pearson WGJ. Pilot study of quantitative methods for differentiating pharyngeal swallowing mechanics by dysphagia etiology. Dysphagia. 2021;36(2):231‐241. doi: 10.1007/s00455-020-10123-0 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0017] 17. Hosseini P, Tadavarthi Y, Martin‐Harris B, Pearson WGJ. Functional modules of pharyngeal swallowing mechanics. Laryngoscope Investig Otolaryngol. 2019;4(3):341‐346. doi: 10.1002/lio2.273 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0018] 18. Ouahchi Y, Marie JP, Verin E. Effect of lingual paralysis on swallowing and breathing coordination in rats. Respir Physiol Neurobiol. 2012;181(1):95‐98. doi: 10.1016/j.resp.2012.01.009 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0019] 19. Wang C‐M, Shieh W‐Y, Ho C‐S, Hu Y‐W, Wu Y‐R. Home‐based orolingual exercise improves the coordination of swallowing and respiration in early Parkinson disease: a quasi‐experimental before‐and‐after exercise program study. Front Neurol. 2018;9:624. doi: 10.3389/fneur.2018.00624 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0020] 20. Martin‐Harris B, McFarland D, Hill EG, et al. Respiratory‐swallow training in patients with head and neck cancer. Arch Phys Med Rehabil. 2015;96(5):885‐893. doi: 10.1016/j.apmr.2014.11.022 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0021] 21. Martin‐Harris B, Garand KLF, McFarland D. Optimizing respiratory‐swallowing coordination in patients with oropharyngeal head and neck cancer. Perspect ASHA Spec Interes Groups. 2017;2(13):103‐110. doi: 10.1044/persp2.SIG13.103 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0022] 22. Brodsky MB, McFarland DH, Dozier TS, et al. Respiratory‐swallow phase patterns and their relationship to swallowing impairment in patients treated for oropharyngeal cancer. Head Neck. 2010;32(4):481‐489. doi: 10.1002/hed.21209 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0023] 23. Greco E, Simic T, Ringash J, Tomlinson G, Inamoto Y, Martino R. Dysphagia treatment for patients with head and neck cancer undergoing radiation therapy: a meta‐analysis review. Int J Radiat Oncol Biol Phys. 2018;101(2):421‐444. doi: 10.1016/j.ijrobp.2018.01.097 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0024] 24. Ajmani GS, Nocon CC, Brockstein BE, et al. Association of a proactive swallowing rehabilitation program with feeding tube placement in patients treated for pharyngeal cancer. JAMA Otolaryngol Head Neck Surg. 2018;144(6):483‐488. doi: 10.1001/jamaoto.2018.0278 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0025] 25. Hutcheson KA, Bhayani MK, Beadle BM, et al. Eat and exercise during radiotherapy or chemoradiotherapy for pharyngeal cancers: use it or lose it. JAMA Otolaryngol Head Neck Surg. 2013;139(11):1127‐1134. doi: 10.1001/jamaoto.2013.4715 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0026] 26. Krekeler BN, Rowe LM, Connor NP. Dose in exercise‐based dysphagia therapies: a scoping review. Dysphagia. 2021;36(1):1‐32. doi: 10.1007/s00455-020-10104-3 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0027] 27. Lazarus C. Tongue strength and exercise in healthy individuals and in head and neck cancer patients. Semin Speech Lang. 2006;27(4):260‐267. doi: 10.1055/s-2006-955116 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0028] 28. Van den Steen L, Baudelet M, Tomassen P, Bonte K, De Bodt M, Van Nuffelen G. Effect of tongue‐strengthening exercises on tongue strength and swallowing‐related parameters in chronic radiation‐associated dysphagia. Head Neck. 2020;42(9):2298‐2307. doi: 10.1002/hed.26179 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0029] 29. Perry A, Lee SH, Cotton S, Kennedy C. Therapeutic exercises for affecting post‐treatment swallowing in people treated for advanced‐stage head and neck cancers. Cochrane Database Syst Rev. 2016;2016(8):CD011112. doi: 10.1002/14651858.CD011112.pub2 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0030] 30. Constantinescu G, Rieger J, Seikaly H, Eurich D. Adherence to home‐based swallowing therapy using a mobile system in head and neck cancer survivors. Am J Speech‐Language Pathol. 2021;30(6):2465‐2475. doi: 10.1044/2021_AJSLP-21-00026 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0031] 31. Govender R, Smith CH, Taylor SA, Barratt H, Gardner B. Swallowing interventions for the treatment of dysphagia after head and neck cancer: a systematic review of behavioural strategies used to promote patient adherence to swallowing exercises. BMC Cancer. 2017;17(1):43. doi: 10.1186/s12885-016-2990-x [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0032] 32. Shinn EH, Basen‐Engquist K, Baum G, et al. Adherence to preventive exercises and self‐reported swallowing outcomes in post‐radiation head and neck cancer patients. Head Neck. 2013;35(12):1707‐1712. doi: 10.1002/hed.23255 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0033] 33. Russell JA, Connor NP. Effects of age and radiation treatment on function of extrinsic tongue muscles. Radiat Oncol. 2014;9:254. doi: 10.1186/s13014-014-0254-y [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0034] 34. Rowe LM, Connor NP, Russell JA. Respiratory‐swallow coordination in a rat model of chemoradiation. Head Neck. 2021;43(10):2954‐2966. doi: 10.1002/hed.26782 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0035] 35. Krekeler BN, Weycker JM, Connor NP. Effects of tongue exercise frequency on tongue muscle biology and swallowing physiology in a rat model. Dysphagia. 2020;35(6):918‐934. doi: 10.1007/s00455-020-10105-2 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0036] 36. Connor NP, Russell JA, Wang H, et al. Effect of tongue exercise on protrusive force and muscle fiber area in aging rats. J Speech Lang Hear Res. 2009;52(3):732‐744. doi: 10.1044/1092-4388(2008/08-0105) [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0037] 37. Kletzien H, Russell JA, Leverson GE, Connor NP. Differential effects of targeted tongue exercise and treadmill running on aging tongue muscle structure and contractile properties. J Appl Physiol. 2012;114(4):472‐481. doi: 10.1152/japplphysiol.01370.2012 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0038] 38. Schaser AJ, Ciucci MR, Connor NP. Cross‐activation and detraining effects of tongue exercise in aged rats. Behav Brain Res. 2016;297:285‐296. doi: 10.1016/j.bbr.2015.10.030 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0039] 39. Broadfoot CK, Hoffmeister JD, Lechner SA, et al. Tongue and laryngeal exercises improve tongue strength and vocal function outcomes in a Pink1−/− rat model of early Parkinson disease. Behav Brain Res. 2024;460:114754. doi: 10.1016/j.bbr.2023.114754 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0040] 40. Krekeler BN, Connor NP. Age‐related changes in mastication are not improved by tongue exercise in a rat model. Laryngoscope. 2017;127(1):E29‐E34. doi: 10.1002/lary.26045 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0041] 41. Glass TJ, Figueroa JE, Russell JA, Krekeler BN, Connor NP. Progressive protrusive tongue exercise does not alter aging effects in retrusive tongue muscles. Front Physiol. 2021;12:740876. doi: 10.3389/fphys.2021.740876 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0042] 42. Cullins MJ, Krekeler BN, Connor NP. Differential impact of tongue exercise on intrinsic lingual muscles. Laryngoscope. 2018;128(10):2245‐2251. doi: 10.1002/lary.27044 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0043] 43. Krekeler BN, Leverson G, Connor NP. Tongue exercise and ageing effects on morphological and biochemical properties of the posterior digastric and temporalis muscles in a Fischer 344 Brown Norway rat model. Arch Oral Biol. 2018;89:37‐43. doi: 10.1016/j.archoralbio.2018.02.002 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0044] 44. Pauloski BR, Logemann JA. Impact of tongue base and posterior pharyngeal wall biomechanics on pharyngeal clearance in irradiated postsurgical oral and oropharyngeal cancer patients. Head Neck. 2000;22(2):120‐131. [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0045] 45. Wall LR, Ward EC, Cartmill B, Hill AJ. Physiological changes to the swallowing mechanism following (chemo)radiotherapy for head and neck cancer: a systematic review. Dysphagia. 2013;28(4):481‐493. doi: 10.1007/s00455-013-9491-8 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0046] 46. Lalla RV, Treister N, Sollecito T, et al. Oral complications at 6 months after radiation therapy for head and neck cancer. Oral Dis. 2017;23(8):1134‐1143. doi: 10.1111/odi.12710 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0047] 47. Fowler JF. 21 years of biologically effective dose. Br J Radiol. 2010;83(991):554‐568. doi: 10.1259/bjr/31372149 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0048] 48. Fowler JF. The linear‐quadratic formula and progress in fractionated radiotherapy. Br J Radiol. 1989;62(740):679‐694. doi: 10.1259/0007-1285-62-740-679 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0049] 49. Osman N, Elamin YY, Rafee S, et al. Weekly cisplatin concurrently with radiotherapy in head and neck squamous cell cancer: a retrospective analysis of a tertiary institute experience. Eur Arch Oto‐Rhino‐Laryngol. 2014;271(8):2253‐2259. doi: 10.1007/s00405-013-2749-9 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0050] 50. Helfenstein S, Riesterer O, Meier UR, et al. 3‐weekly or weekly cisplatin concurrently with radiotherapy for patients with squamous cell carcinoma of the head and neck—a multicentre, retrospective analysis. Radiat Oncol. 2019;14(1):32. doi: 10.1186/s13014-019-1235-y [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0051] 51. Cullins MJ, Wenninger JM, Cullen JS, Russell JA, Kleim JA, Connor NP. Tongue force training induces plasticity of the lingual motor cortex in Young adult and aged rats. Front Neurosci. 2019;13:1355. doi: 10.3389/fnins.2019.01355 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0052] 52. Ciucci MR, Russell JA, Schaser AJ, Doll EJ, Vinney LM, Connor NP. Tongue force and timing deficits in a rat model of Parkinson disease. Behav Brain Res. 2011;222(2):315‐320. doi: 10.1016/j.bbr.2011.03.057 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0053] 53. Hunter KU, Schipper M, Feng FY, et al. Toxicities affecting quality of life after chemo‐IMRT of oropharyngeal cancer: prospective study of patient‐reported, observer‐rated, and objective outcomes. Int J Radiat Oncol Biol Phys. 2013;85(4):935‐940. doi: 10.1016/j.ijrobp.2012.08.030 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0054] 54. Brooks L, Landry A, Deshpande A, Marchica C, Cooley A, Raol N. Posterior tongue tie, base of tongue movement, and pharyngeal dysphagia: what is the connection? Dysphagia. 2020;35(1):129‐132. doi: 10.1007/s00455-019-10040-x [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0055] 55. Knigge MA, Thibeault S, McCulloch TM. Implementation of high‐resolution manometry in the clinical practice of speech language pathology. Dysphagia. 2014;29(1):2‐16. doi: 10.1007/s00455-013-9494-5 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0056] 56. Kletzien H, Connor NP. Computational analysis of swallowing mechanics in an aging rodent model. Frontiers in Optics 2017. OSA Technical Digest. Optical Society of America; 2017. doi: 10.1364/FIO.2017.JTu2A.83 [DOI] [Google Scholar]

[hed27899-bib-0057] 57. Kletzien H, Cullins MJ, Connor NP. Age‐related alterations in swallowing biomechanics. Exp Gerontol. 2019;118:45‐50. doi: 10.1016/j.exger.2019.01.006 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0058] 58. Schwertner RW, Garand KL, Pearson WGJ. A novel imaging analysis method for capturing pharyngeal constriction during swallowing. J Imaging Sci. 2016;1:1. [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0059] 59. Klingenberg CP. MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour. 2011;11(2):353‐357. doi: 10.1111/j.1755-0998.2010.02924.x [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0060] 60. McFarland DH, Martin‐Harris B, Fortin A‐J, Humphries K, Hill E, Armeson K. Respiratory‐swallowing coordination in normal subjects: lung volume at swallowing initiation. Respir Physiol Neurobiol. 2016;234:89‐96. doi: 10.1016/j.resp.2016.09.004 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0061] 61. Goepfert RP, Lewin JS, Barrow MP, et al. Long‐term patient‐reported dysphagia in low‐risk oropharyngeal carcinoma after intensity modulated radiation therapy. Int J Radiat Oncol. 2016;94(4):963‐964. doi: 10.1016/j.ijrobp.2015.12.329 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0062] 62. Lazarus CL, Husaini H, Falciglia D, et al. Effects of exercise on swallowing and tongue strength in patients with oral and oropharyngeal cancer treated with primary radiotherapy with or without chemotherapy. Int J Oral Maxillofac Surg. 2014;43:523‐530. doi: 10.1016/j.ijom.2013.10.023 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0063] 63. Van Nuffelen G, Vanderwegen J, Guns C, Van den Steen L, de Bodt M. Effect of tongue strength training in head and neck cancer (HNC) patients treated with chemoradiation (CRT) or radiotherapy (RT). Dysphagia. 2022;28:300. [Google Scholar]

[hed27899-bib-0064] 64. Smaoui S, Langridge A, Steele CM. The effect of lingual resistance training interventions on adult swallow function: a systematic review. Dysphagia. 2019;35:745‐761. doi: 10.1007/s00455-019-10066-1 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0065] 65. Xinou E, Chryssogonidis I, Kalogera‐Fountzila A, Panagiotopoulou‐Mpoukla D, Printza A. Longitudinal evaluation of swallowing with videofluoroscopy in patients with locally advanced head and neck cancer after chemoradiation. Dysphagia. 2018;33(5):691‐706. doi: 10.1007/s00455-018-9889-4 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0066] 66. Gharzai LA, Li P, Schipper MJ, et al. Characterization of very late dysphagia after chemoradiation for oropharyngeal squamous cell carcinoma. Oral Oncol. 2020;111:104853. doi: 10.1016/j.oraloncology.2020.104853 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0067] 67. Carmignani I, Locatello LG, Desideri I, et al. Analysis of dysphagia in advanced‐stage head‐and‐neck cancer patients: impact on quality of life and development of a preventive swallowing treatment. Eur Arch Oto‐Rhino‐Laryngol. 2018;275(8):2159‐2167. doi: 10.1007/s00405-018-5054-9 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0068] 68. Pisegna JM, Langmore SE, Meyer TK, Pauloski B. Swallowing patterns in the HNC population: timing of penetration‐aspiration events and residue. Otolaryngol Neck Surg. 2020;163(6):1232‐1239. doi: 10.1177/0194599820933883 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0069] 69. Russell JA, Ciucci MR, Hammer MJ, Connor NP. Videofluorographic assessment of deglutitive behaviors in a rat model of aging and Parkinson disease. Dysphagia. 2013;28(1):95‐104. doi: 10.1007/s00455-012-9417-x [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0070] 70. Cullen KP, Grant LM, Kelm‐Nelson CA, et al. Pink1 −/− rats show early‐onset swallowing deficits and correlative brainstem pathology. Dysphagia. 2018;33(6):749‐758. doi: 10.1007/s00455-018-9896-5 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0071] 71. Lowell SY, Poletto CJ, Knorr‐Chung BR, Reynolds RC, Simonyan K, Ludlow CL. Sensory stimulation activates both motor and sensory components of the swallowing system. Neuroimage. 2008;42(1):285‐295. doi: 10.1016/j.neuroimage.2008.04.234 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0072] 72. Riantiningtyas RR, Carrouel F, Bruyas A, et al. Oral somatosensory alterations in head and neck cancer patients‐an overview of the evidence and causes. Cancers (Basel). 2023;15(3):718. doi: 10.3390/cancers15030718 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0073] 73. Denaro N, Merlano MC, Russi EG. Dysphagia in head and neck cancer patients: pretreatment evaluation, predictive factors, and assessment during radio‐chemotherapy, recommendations. Clin Exp Otorhinolaryngol. 2013;6(3):117‐126. doi: 10.3342/ceo.2013.6.3.117 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0074] 74. Leslie P, Drinnan MJ, Ford GA, Wilson JA. Swallow respiration patterns in dysphagic patients following acute stroke. Dysphagia. 2002;17(3):202‐207. doi: 10.1007/s00455-002-0053-8 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0075] 75. Dziadziola J, Hamlet S, Michou G, Jones L. Multiple swallows and piecemeal deglutition; observations from normal adults and patients with head and neck cancer. Dysphagia. 1992;7(1):8‐11. doi: 10.1007/BF02493415 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0076] 76. Lever TE, Gorsek A, Cox KT, et al. An animal model of oral dysphagia in amyotrophic lateral sclerosis. Dysphagia. 2008;24(2):180‐195. doi: 10.1007/s00455-008-9190-z [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0077] 77. de Groot RJ, Wetzels J‐W, Merkx MAW, et al. Masticatory function and related factors after oral oncological treatment: a 5‐year prospective study. Head Neck. 2019;41(1):216‐224. doi: 10.1002/hed.25445 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0078] 78. van der Molen L, van Rossum MA, Burkhead LM, Smeele LE, Rasch CRN, Hilgers FJM. A randomized preventive rehabilitation trial in advanced head and neck cancer patients treated with chemoradiotherapy: feasibility, compliance, and short‐term effects. Dysphagia. 2011;26(2):155‐170. doi: 10.1007/s00455-010-9288-y [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0079] 79. Karsten RT, van der Molen L, Hamming‐Vrieze O, et al. Long‐term swallowing, trismus, and speech outcomes after combined chemoradiotherapy and preventive rehabilitation for head and neck cancer; 10‐year plus update. Head Neck. 2020;42:1907‐1918. doi: 10.1002/hed.26120 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0080] 80. Hadjikoutis S, Pickersgill TP, Dawson K, Wiles CM. Abnormal patterns of breathing during swallowing in neurological disorders. Brain. 2000;123:1863‐1873. doi: 10.1093/brain/123.9.1863 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0081] 81. Pinnington LL, Muhiddin KA, Ellis RE, Playford ED. Non‐invasive assessment of swallowing and respiration in Parkinson's disease. J Neurol. 2000;247(10):773‐777. doi: 10.1007/s004150070091 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0082] 82. Tulunay‐Ugur OE, McClinton C, Young Z, Penagaricano JA, Maddox A‐M, Vural E. Functional outcomes of Chemoradiation in patients with head and neck cancer. Otolaryngol Neck Surg. 2012;148(1):64‐68. doi: 10.1177/0194599812459325 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0083] 83. Lazarus CL. Effects of chemoradiotherapy on voice and swallowing. Curr Opin Otolaryngol Head Neck Surg. 2009;17(3):172‐178. doi: 10.1097/MOO.0b013e32832af12f [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0084] 84. Murphy BA, Gilbert J. Dysphagia in head and neck cancer patients treated with radiation: assessment, sequelae, and rehabilitation. Semin Radiat Oncol. 2009;19:35‐42. doi: 10.1016/j.semradonc.2008.09.007 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0085] 85. Lazarus CL, Logemann JA, Pauloski BR, et al. Swallowing and tongue function following treatment for oral and oropharyngeal cancer. J Speech Lang Hear Res. 2000;43:1011‐1023. doi: 10.1044/jslhr.4304.1011 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0086] 86. Kim DOH, Choi J, Lim Y‐S, Huh HJ, Cho CG, Kim BH. A rat model for oral mucositis induced by a single administration of 5‐fluorouracil. In Vivo. 2023;37(1):218‐224. doi: 10.21873/invivo.13070 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0087] 87. Patel A, Rajesh S, Chandrashekhar VM, et al. A rat model against chemotherapy plus radiation‐induced oral mucositis. Saudi Pharm J. 2013;21(4):399‐403. doi: 10.1016/j.jsps.2012.11.003 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0088] 88. King SN, Dunlap NE, Tennant PA, Pitts T. Pathophysiology of radiation‐induced dysphagia in head and neck cancer. Dysphagia. 2016;31(3):339‐351. doi: 10.1007/s00455-016-9710-1 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0089] 89. Zhou Y, Sheng X, Deng F, et al. Radiation‐induced muscle fibrosis rat model: establishment and valuation. Radiat Oncol. 2018;13(1):160. doi: 10.1186/s13014-018-1104-0 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0090] 90. Starmer H, Sanguineti G, Marur S, Gourin CG. Multidisciplinary head and neck cancer clinic and adherence with speech pathology. Laryngoscope. 2011;121(10):2131‐2135. doi: 10.1002/lary.21746 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0091] 91. Stenson KM, MacCracken E, List M, et al. Swallowing function in patients with head and neck cancer prior to treatment. Arch Otolaryngol Neck Surg. 2000;126(3):371‐377. doi: 10.1001/archotol.126.3.371 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0092] 92. Steele CM, Miller AJ. Sensory input pathways and mechanisms in swallowing: a review. Dysphagia. 2010;25(4):323‐333. doi: 10.1007/s00455-010-9301-5 [DOI] [PMC free article] [PubMed] [Google Scholar]

[hed27899-bib-0093] 93. Miller AJ. Oral and pharyngeal reflexes in the mammalian nervous system: their diverse range in complexity and the pivotal role of the tongue. Crit Rev Oral Biol Med. 2002;13(5):409‐425. doi: 10.1177/154411130201300505 [DOI] [PubMed] [Google Scholar]

[hed27899-bib-0094] 94. Sweazey RD, Bradley RM. Responses of neurons in the lamb nucleus tractus solitarius to stimulation of the caudal oral cavity and epiglottis with different stimulus modalities. Brain Res. 1989;480(1–2):133‐150. doi: 10.1016/0006-8993(89)91576-x [DOI] [PubMed] [Google Scholar]

PERMALINK

Effects of chemoradiation and tongue exercise on swallow biomechanics and bolus kinematics

Nicole E Schaen‐Heacock, MS

Linda M Rowe, MS

Michelle R Ciucci, PhD

John A Russell, PhD

Abstract

Background

Methods

Results

Conclusions

1. INTRODUCTION

2. MATERIALS AND METHODS

2.1. Progressive resistance tongue training paradigm

FIGURE 1.

2.2. Videofluoroscopy

FIGURE 2.

2.3. Computational analysis of swallow mechanics adapted for the rodent model

FIGURE 3.

2.4. Bolus kinematics and bolus area

2.5. Jaw opening

2.6. Respiratory–swallow coordination

3. STATISTICAL ANALYSIS

3.1. Swallow biomechanics

3.2. Bolus kinematics, bolus area, jaw opening, and post‐swallow respiration

4. RESULTS

TABLE 1.

4.1. Swallow biomechanics

4.2. Bolus kinematics and bolus area

FIGURE 4.

FIGURE 5.

4.3. Jaw kinematics

FIGURE 6.

4.4. Swallowing and respiration

TABLE 2.

5. DISCUSSION

5.1. Limitations and future directions

6. CONCLUSION

CONFLICT OF INTEREST STATEMENT

ETHICS STATEMENT

ACKNOWLEDGMENTS

DATA AVAILABILITY STATEMENT

REFERENCES

Associated Data

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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