Pharyngeal Swallowing Mechanics Secondary to Hemispheric Stroke
Introduction
Dysphagia commonly follows stroke and is a predictor of poor outcomes including aspiration, lengthened hospital stay, need for institutional care, pneumonia, and even mortality.1, 2, 3, 4, 5 During pharyngeal swallowing, the pharynx is transformed from a respiratory channel into an alimentary conduit. In the current study, pharyngeal swallowing mechanics of dysphagic ischemic stroke patients are compared to those of healthy controls to better appreciate the impact of stroke on swallowing. We compared left and right hemispheric stroke groups to understand the impact of each on swallowing mechanics. Furthermore, we investigated the sample's pharyngeal mechanics associated with penetration and aspiration.
Current literature of the functional changes in stroke-related dysphagia emphasizes delays in timing,6, 7, 8 aspiration risk associated with timing,9, 10, 11 and related sensorineural deficits12, 13, 14 with mechanistic deficits receiving less attention. Reports suggest differences in hyoid and laryngeal displacements but are mixed (Table 1).11, 15, 16, 17, 18 A more comprehensive understanding of covariant swallowing mechanics including hyoid and laryngeal movements, tongue base retraction, pharyngeal shortening, and head and neck extensions could not only highlight the dysfunction underlying stroke-associated penetration and aspiration but also suggest which treatment goals would be more salient.19, 20
Another important factor that could be contributing to dysfunction of swallowing mechanics is the impact of left versus right hemispheric lesions. Although the consensus in the literature supports the idea that swallowing is bilaterally innervated,21, 22, 23, 24 some studies suggest that 1 hemisphere is more dominant, varying by person.25, 26, 27, 28, 29 Increasingly, recent studies indicate that right hemisphere lesion is associated with deficits in the pharyngeal stage of swallowing.30, 31, 32 Teismann et al and Mihai et al showed a shift of neural activity to the right hemisphere during the pharyngeal stage of swallowing in healthy subjects.33, 34 Other authors support the notion that the 2 hemispheres do, in fact, control different aspects of swallowing.35 Support for this theory dates back to 1993 when Robbins et al found right hemispheric strokes to be associated with longer pharyngeal transit and response times as well as increased risk of penetration and aspiration when compared to left hemispheric strokes.36 However, consensus on whether there is a dominant hemisphere, varying by person, or whether there are instead distinct roles assigned to each hemisphere remains unclear. Furthermore, the specific impact of hemispheric stroke on the multiple muscle group actions underlying pharyngeal swallowing mechanics is unreported.
Conventional univariate displacement measurements from videofluoroscopic swallowing studies are helpful to quantify stroke impact, for example, on hyoid movement. The impact of multiple stroke variables, however, on multiple interacting elements of swallowing mechanics requires a different approach. Pharyngeal swallowing is complex. Computational analysis of swallowing mechanics (CASM) utilizes geometric morphometrics to quantify overall shape differences associated with variables of interest. Once these overall differences are determined, eigenvectors are used to visualize the impact of variables on covariant pharyngeal swallowing mechanics. As such, the traditional outcome of distance measurements is replaced by eigenvectors that provide information characterizing the direction and magnitude of variations in shape.
CASM maps anatomical landmarks of the swallowing apparatus. These landmarks can be reliably obtained from imaging data including hyoid movement, laryngeal elevation, tongue base retraction, pharyngeal shortening, and head and neck posture (Fig 1).37, 38 Configurations of coordinates represent the interaction of multiple muscle groups underlying pharyngeal swallowing mechanics as these landmarks are displaced. Hence, shape analysis of landmarks throughout the swallow permits statistical evaluation and statistical visualization of elements of pharyngeal swallowing. Sets of coordinates are compared mathematically to determine differences in shape by variables of interest (group, lesion site, bolus type, penetration–aspiration status, etc.).39 Eigenvectors show the magnitude and direction of variation for each coordinate. The impact of a named variable on the action of multiple muscle groups is therefore inferred, allowing for an approach to quantify and visualize the gestalt mechanics of pharyngeal swallowing using imaging data.
Herein we consider the independent variables of the test group, hemispheres affected by stroke, and penetration–aspiration status. The goal of the present study was to analyze and visualize pharyngeal swallowing mechanics associated with these variables. The authors hypothesized that (H1) multiple elements of pharyngeal swallowing mechanics of dysphagic stroke patients are reduced when compared with age- and gender-matched controls; (H2) right-sided lesions more negatively impact pharyngeal stage swallowing mechanics than left-sided lesions; and (H3) within the stroke cohort, impaired pharyngeal swallowing mechanics are associated with penetration–aspiration status.
Section snippets
Subjects and Imaging
The study included 18 supratentorial ischemic stroke subjects (averaged 70.1 ± 15.4 years of age, ranged from 40 to 90 years, and included 11 females and 7 males) and 18 age- and gender-matched healthy control subjects. All stroke subjects were right handed; 6 had right hemispheric infarcts and 12 had left hemispheric infarcts. Local institutional review boards approved the study and all participants gave written informed consent.
Inclusion criteria for the stroke patients were unilateral,
Results
H1 Stroke versus controls.
Canonical variate analysis of the test group, swallowing stage, and hemisphere affected showed highly significant differences (P < .0001) across all comparisons. DFA pairwise comparisons of stroke versus controls groups showed significant differences in pharyngeal swallowing mechanics between the cohorts (D = 2.17, P < .0001). DFA eigenvectors (Fig 3) indicate reduced hyoid elevation, reduced tongue base retraction, and reduced pharyngeal shortening, as well as
Discussion
In the present study, differences in pharyngeal swallowing mechanics were evaluated and visualized using CASM to assess associations with stroke, lesion site (left versus right hemisphere), and penetration–aspiration status. These findings suggest that mechanical changes resulting from stroke are an important consideration in dysphagia management and knowing the specific mechanical impairment will allow for more specific therapy goals, possibly hastening and increasing the chances of recovery.
Conclusions
Our results from this limited data set show a global impairment of swallowing mechanics after stroke. Moreover, these data suggest that the sidedness of stroke lesions meaningfully affects the resulting mechanical changes with right-sided hemispheric strokes having a greater negative impact on pharyngeal swallowing mechanics than left-sided hemispheric strokes when compared to controls. CASM is a method that provides new insight into impaired swallowing mechanics associated with stroke
Acknowledgments
The authors would like to acknowledge Dr. Kendrea Garand and Dr. Bonnie Martin-Harris for the contribution of the control data.
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Cited by (29)
Cerebral control of swallowing: An update on neurobehavioral evidence
2022, Journal of the Neurological SciencesCitation Excerpt :Most of these studies report that right hemispheric lesions result in more severe dysphagia involving pharyngeal impairments [47,51,52]. The symptoms associated with right hemispheric lesions include altered swallowing mechanics characterized by prominent pharyngeal dysmotility and reduced hyolaryngeal elevation [47,52], prolonged pharyngeal events [51], increased pharyngeal residue, impaired swallow response, increased risk of aspiration [39–41,51,53]. Moreover, Li et al., [54] reported that right hemispheric lesions were associated with pharyngeal dysfunction whereas left hemispheric lesions were associated with oral dysfunction.
Age-related alterations in swallowing biomechanics
2019, Experimental GerontologyCitation Excerpt :Baum and Bodner, 1983; Clark et al., 2003; Clark and Solomon, 2012) Swallowing function is typically examined using an instrumental evaluation, such as the modified barium swallow study that uses videofluoroscopy and allows for visualization of the bolus as it moves through the oral cavity and pharynx. Methodologies have been developed to assess and quantify swallowing impairment (Modified Barium Swallowing Tool [MBSImp])(Martin-Harris et al., 2008) and biomechanics (Computational Analysis of Swallowing Mechanics [CASM]) in humans,(Ellis et al., 2018; Garand et al., 2018; May et al., 2017; Pearson Jr. et al., 2016a; Pearson Jr. et al., 2016b; Pearson Jr. and Zumwalt, 2013; Schwertner et al., 2016; Thi Tu Anh et al., 2018) but underlying physiological and biological mechanisms of age-related swallow dysfunction have not yet been identified. Because use of human subjects is often precluded in examination of age-related muscular degeneration in the cranial motor system, aging rodent models have been used to study underlying biochemical, molecular, and cellular mechanisms contributing to age-related dysphagia.
Mapping acute lesion locations to physiological swallow impairments after stroke
2019, NeuroImage: ClinicalCitation Excerpt :In terms of side of the lesion, most of the significant voxels or ROIs were in the right hemisphere and only comparably few in the left hemisphere. This is in line with previous studies linking right hemisphere strokes to pharyngeal impairment or to more severe dysphagia in general (Daniels et al., 1996; May et al., 2016; Robbins, 1993; Suntrup et al., 2015; Suntrup-Krueger et al., 2017; Wilmskoetter et al., 2018). However, two (anterior hyoid movement, laryngeal vestibular closure) of the four (laryngeal elevation, anterior hyoid movement, laryngeal vestibular closure, pharyngeal residue) significant pharyngeal components were associated with lesions in the left hemisphere; thus, our findings are in line with our previous research emphasizing that lesions in the left hemisphere can also impair pharyngeal swallow physiology (Wilmskoetter et al., 2018).
Differences in swallow physiology in patients with left and right hemispheric strokes
2018, Physiology and BehaviorCitation Excerpt :Both patients with left and right hemisphere strokes showed pharyngeal impairment, but patients with right hemisphere strokes showed worse pharyngeal impairment than patients with left hemisphere strokes. This is in line with results from previous [12–14,46] and contradictory to other studies [15,24,25]. The observed differences occurred especially in thin and nectar thick liquid swallows, where patients with right hemisphere strokes showed worse pharyngeal impairment than patients with left hemisphere strokes.
Swallowing Disorders After Stroke
2018, Stroke Rehabilitation
Grant support: Grant support for stroke data from the National Institute on Deafness and Other Communication Disorders of the National Institutes of Health (NIH) under Award Number R01DC012584 (Kumar). The Grant Support for Control Data from Veterans Affairs, Rehabilitation Research and Development under award number CDA-1 1IK1RX001628-01A1 (PI: [Focht] Garand), the National Institute on Deafness and Other Communication Disorders of the National Institutes of Health under award number K24DC12801 (PI: Martin-Harris), and the South Carolina Clinical & Translational Research Institute, with an academic home at the Medical University of South Carolina, NIH/National Center for Advancing Translational Sciences grant number TL1 TR000061 (PI: Brady, Project PI: Garand).
The content of this work is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.