Skip to main content
Top
Published in: Dysphagia 4/2020

01-08-2020 | Foreign Body Aspiration | Original Article

Impaired Movement Scaling and Reduced Synchrony with Vestibule Closure Characterize Swallowing in Severe Dysphagia

Authors: Seng Mun Wong, Erin Kamarunas, Christy L. Ludlow

Published in: Dysphagia | Issue 4/2020

Login to get access

Abstract

The contribution of hyoid and laryngeal movement deficits to penetration or aspiration in dysphagia is unclear, partly due to large variations in normal hyolaryngeal kinematics for swallowing. In healthy volunteers, laryngeal and hyoid kinematics relate to the requirements for laryngeal vestibule closure suggesting a central schematic control of movement magnitude and patterning for airway protection. Our first aim was to determine if patients with severe dysphagia showed evidence of an impaired swallowing schema, by examining if their kinematic measures were related to their hyolaryngeal space before swallow onset, and if hyolaryngeal movement synchrony for vestibule closure was disrupted. Our second aim was to determine the kinematic measures that predicted bolus penetration and aspiration in dysphagia. The methods included two-dimensional measures of the hyoid and laryngeal anterior and superior displacement and velocity, and the change in laryngeal vestibule area made from videofluoroscopic swallow recordings of 21 healthy volunteers and 21 patients with dysphagia on tube feeding secondary to the stroke or head and neck cancer. The results demonstrated that the patients did not adapt their hyolaryngeal movements during swallowing to their initial hyolaryngeal space. Further, none of the patients’ measures of hyoid or laryngeal peak velocity timing were synchronized with vestibule closure, demonstrating a disorganized movement patterning. Laryngeal elevation peak velocity independently predicted penetration and aspiration. In conclusion, the central schema for swallowing patterning was disturbed, impairing the integration of kinematic actions for airway protection in severe dysphagia, while laryngeal peak elevation velocity predicted penetration and aspiration on patient swallows.
Literature
1.
go back to reference Molfenter SM, Steele CM. Physiological variability in the deglutition literature: hyoid and laryngeal kinematics. Dysphagia. 2011;26:67–74.CrossRef Molfenter SM, Steele CM. Physiological variability in the deglutition literature: hyoid and laryngeal kinematics. Dysphagia. 2011;26:67–74.CrossRef
2.
go back to reference Kim YH, Oh BM, Jung IY, Lee JC, Lee GJ, Han TR. Spatiotemporal characteristics of swallowing in Parkinson's disease. Laryngoscope. 2014;125(2):389–95.CrossRef Kim YH, Oh BM, Jung IY, Lee JC, Lee GJ, Han TR. Spatiotemporal characteristics of swallowing in Parkinson's disease. Laryngoscope. 2014;125(2):389–95.CrossRef
3.
go back to reference Kendall KA, Leonard RJ. Hyoid movement during swallowing in older patients with dysphagia. Arch Otolaryngol Head Neck Surg. 2001;127:1224–9.CrossRef Kendall KA, Leonard RJ. Hyoid movement during swallowing in older patients with dysphagia. Arch Otolaryngol Head Neck Surg. 2001;127:1224–9.CrossRef
4.
go back to reference Bingjie L, Tong Z, Xinting S, Jianmin X, Guijun J. Quantitative videofluoroscopic analysis of penetration-aspiration in post-stroke patients. Neurol India. 2010;58:42–7.CrossRef Bingjie L, Tong Z, Xinting S, Jianmin X, Guijun J. Quantitative videofluoroscopic analysis of penetration-aspiration in post-stroke patients. Neurol India. 2010;58:42–7.CrossRef
5.
go back to reference Paik NJ, Kim SJ, Lee HJ, Jeon JY, Lim JY, Han TR. Movement of the hyoid bone and the epiglottis during swallowing in patients with dysphagia from different etiologies. J Electromyogr Kinesiol. 2008;18:329–35.CrossRef Paik NJ, Kim SJ, Lee HJ, Jeon JY, Lim JY, Han TR. Movement of the hyoid bone and the epiglottis during swallowing in patients with dysphagia from different etiologies. J Electromyogr Kinesiol. 2008;18:329–35.CrossRef
6.
go back to reference Sundgren P, Maly P, Gullberg B. Elevation of the larynx on normal and abnormal cineradiogram. Br J Radiol. 1993;66:768–72.CrossRef Sundgren P, Maly P, Gullberg B. Elevation of the larynx on normal and abnormal cineradiogram. Br J Radiol. 1993;66:768–72.CrossRef
7.
go back to reference Molfenter SM, Steele CM. Use of an anatomical scalar to control for sex-based size differences in measures of hyoid excursion during swallowing. J Speech Lang Hear Res. 2014;57:768–78.CrossRef Molfenter SM, Steele CM. Use of an anatomical scalar to control for sex-based size differences in measures of hyoid excursion during swallowing. J Speech Lang Hear Res. 2014;57:768–78.CrossRef
8.
go back to reference Wong SM, Domangue RJ, Fels S, Ludlow CL. Evidence that an internal schema adapts swallowing to upper airway requirements. J Physiol. 2017;595:1793–814.CrossRef Wong SM, Domangue RJ, Fels S, Ludlow CL. Evidence that an internal schema adapts swallowing to upper airway requirements. J Physiol. 2017;595:1793–814.CrossRef
9.
go back to reference Steele CM, Cichero JA. Physiological factors related to aspiration risk: a systematic review. Dysphagia. 2014;29:295–304.CrossRef Steele CM, Cichero JA. Physiological factors related to aspiration risk: a systematic review. Dysphagia. 2014;29:295–304.CrossRef
10.
go back to reference Kraaijenga SA, van der Molen L, Heemsbergen WD, Remmerswaal GB, Hilgers FJ, van den Brekel MW. Hyoid bone displacement as parameter for swallowing impairment in patients treated for advanced head and neck cancer. Eur Arch Otorhinolaryngol. 2017;274:597–606.CrossRef Kraaijenga SA, van der Molen L, Heemsbergen WD, Remmerswaal GB, Hilgers FJ, van den Brekel MW. Hyoid bone displacement as parameter for swallowing impairment in patients treated for advanced head and neck cancer. Eur Arch Otorhinolaryngol. 2017;274:597–606.CrossRef
11.
go back to reference Molfenter SM, Steele CM. Kinematic and temporal factors associated with penetration-aspiration in swallowing liquids. Dysphagia. 2014;29:269–76.CrossRef Molfenter SM, Steele CM. Kinematic and temporal factors associated with penetration-aspiration in swallowing liquids. Dysphagia. 2014;29:269–76.CrossRef
13.
go back to reference Kahrilas PJ, Lin S, Rademaker AW, Logemann JA. Impaired deglutitive airway protection: a videofluoroscopic analysis of severity and mechanism. Gastroenterology. 1997;113:1457–64.CrossRef Kahrilas PJ, Lin S, Rademaker AW, Logemann JA. Impaired deglutitive airway protection: a videofluoroscopic analysis of severity and mechanism. Gastroenterology. 1997;113:1457–64.CrossRef
14.
go back to reference Wang TG, Chang YC, Chen WS, Lin PH, Hsiao TY. Reduction in hyoid bone forward movement in irradiated nasopharyngeal carcinoma patients with dysphagia. Arch Phys Med Rehabilit. 2010;91:926–31.CrossRef Wang TG, Chang YC, Chen WS, Lin PH, Hsiao TY. Reduction in hyoid bone forward movement in irradiated nasopharyngeal carcinoma patients with dysphagia. Arch Phys Med Rehabilit. 2010;91:926–31.CrossRef
15.
go back to reference Zhang J, Zhou Y, Wei N, Yang B, Wang A, Zhou H, Zhao X, Wang Y, Liu L, Ouyoung M, Villegas B, Groher M. Laryngeal elevation velocity and aspiration in acute ischemic stroke patients. PLoS ONE. 2016;11:e0162257.CrossRef Zhang J, Zhou Y, Wei N, Yang B, Wang A, Zhou H, Zhao X, Wang Y, Liu L, Ouyoung M, Villegas B, Groher M. Laryngeal elevation velocity and aspiration in acute ischemic stroke patients. PLoS ONE. 2016;11:e0162257.CrossRef
16.
go back to reference Pearson WG Jr, Taylor BK, Blair J, Martin-Harris B. Computational analysis of swallowing mechanics underlying impaired epiglottic inversion. Laryngoscope. 2016;126:1854–8.CrossRef Pearson WG Jr, Taylor BK, Blair J, Martin-Harris B. Computational analysis of swallowing mechanics underlying impaired epiglottic inversion. Laryngoscope. 2016;126:1854–8.CrossRef
17.
go back to reference Vose A, Humbert I. “Hidden in Plain Sight”: a descriptive review of laryngeal vestibule closure. Dysphagia. 2018;34(3):281–9.CrossRef Vose A, Humbert I. “Hidden in Plain Sight”: a descriptive review of laryngeal vestibule closure. Dysphagia. 2018;34(3):281–9.CrossRef
18.
go back to reference van der Kruis JG, Baijens LW, Speyer R, Zwijnenberg I. Biomechanical analysis of hyoid bone displacement in videofluoroscopy: a systematic review of intervention effects. Dysphagia. 2011;26:171–82.CrossRef van der Kruis JG, Baijens LW, Speyer R, Zwijnenberg I. Biomechanical analysis of hyoid bone displacement in videofluoroscopy: a systematic review of intervention effects. Dysphagia. 2011;26:171–82.CrossRef
19.
go back to reference Veljan D. The 2500-year-old Pythagorean Theorem. Math Mag. 2000;73:259–72.CrossRef Veljan D. The 2500-year-old Pythagorean Theorem. Math Mag. 2000;73:259–72.CrossRef
20.
go back to reference Kang BS, Oh BM, Kim IS, Chung SG, Kim SJ, Han TR. Influence of aging on movement of the hyoid bone and epiglottis during normal swallowing: a motion analysis. Gerontology. 2010;56:474–82.CrossRef Kang BS, Oh BM, Kim IS, Chung SG, Kim SJ, Han TR. Influence of aging on movement of the hyoid bone and epiglottis during normal swallowing: a motion analysis. Gerontology. 2010;56:474–82.CrossRef
21.
go back to reference Martin-Harris B, Brodsky MB, Michel Y, Lee F, Walters B. Delayed initiation of the pharyngeal swallow: normal variability in adult swallows. J Speech Lang Hear Res. 2007;50:585–94.CrossRef Martin-Harris B, Brodsky MB, Michel Y, Lee F, Walters B. Delayed initiation of the pharyngeal swallow: normal variability in adult swallows. J Speech Lang Hear Res. 2007;50:585–94.CrossRef
22.
go back to reference Stephen JR, Taves DH, Smith RC, Martin RE. Bolus location at the initiation of the pharyngeal stage of swallowing in healthy older adults. Dysphagia. 2005;20:266–72.CrossRef Stephen JR, Taves DH, Smith RC, Martin RE. Bolus location at the initiation of the pharyngeal stage of swallowing in healthy older adults. Dysphagia. 2005;20:266–72.CrossRef
23.
go back to reference Mendell DA, Logemann JA. Temporal sequence of swallow events during the oropharyngeal swallow. J Speech Lang Hear Res. 2007;50:1256–71.CrossRef Mendell DA, Logemann JA. Temporal sequence of swallow events during the oropharyngeal swallow. J Speech Lang Hear Res. 2007;50:1256–71.CrossRef
24.
go back to reference Logemann JA, Pauloski BR, Rademaker AW, Colangelo LA, Kahrilas PJ, Smith CH. Temporal and biomechanical characteristics of oropharyngeal swallow in younger and older men. J Speech Lang Hear Res. 2000;43:1264–74.CrossRef Logemann JA, Pauloski BR, Rademaker AW, Colangelo LA, Kahrilas PJ, Smith CH. Temporal and biomechanical characteristics of oropharyngeal swallow in younger and older men. J Speech Lang Hear Res. 2000;43:1264–74.CrossRef
25.
go back to reference Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996;11:93–8.CrossRef Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996;11:93–8.CrossRef
26.
go back to reference Steele CM, Grace-Martin K. Reflections on clinical and statistical use of the penetration-aspiration scale. Dysphagia. 2017;32:601–16.CrossRef Steele CM, Grace-Martin K. Reflections on clinical and statistical use of the penetration-aspiration scale. Dysphagia. 2017;32:601–16.CrossRef
27.
go back to reference Jacob P, Kahrilas PJ, Logemann JA, Shah V, Ha T. Upper esophageal sphincter opening and modulation during swallowing. Gastroenterology. 1989;97:1469–78.CrossRef Jacob P, Kahrilas PJ, Logemann JA, Shah V, Ha T. Upper esophageal sphincter opening and modulation during swallowing. Gastroenterology. 1989;97:1469–78.CrossRef
28.
go back to reference Yokoyama M, Mitomi N, Tetsuka K, Tayama N, Niimi S. Role of laryngeal movement and effect of aging on swallowing pressure in the pharynx and upper esophageal sphincter. Laryngoscope. 2000;110:434–9.CrossRef Yokoyama M, Mitomi N, Tetsuka K, Tayama N, Niimi S. Role of laryngeal movement and effect of aging on swallowing pressure in the pharynx and upper esophageal sphincter. Laryngoscope. 2000;110:434–9.CrossRef
29.
go back to reference Cook IJ, Dodds WJ, Dantas RO, Massey B, Kern MK, Lang IM, Brasseur JG, Hogan WJ. Opening mechanisms of the human upper esophageal sphincter. Am J Physiol. 1989;257:G748–G759759.PubMed Cook IJ, Dodds WJ, Dantas RO, Massey B, Kern MK, Lang IM, Brasseur JG, Hogan WJ. Opening mechanisms of the human upper esophageal sphincter. Am J Physiol. 1989;257:G748–G759759.PubMed
30.
go back to reference Pearson WG Jr, Davidoff AA, Smith ZM, Adams DE, Langmore SE. Impaired swallowing mechanics of post radiation therapy head and neck cancer patients: a retrospective videofluoroscopic study. World J Radiol. 2016;8:192–9.CrossRef Pearson WG Jr, Davidoff AA, Smith ZM, Adams DE, Langmore SE. Impaired swallowing mechanics of post radiation therapy head and neck cancer patients: a retrospective videofluoroscopic study. World J Radiol. 2016;8:192–9.CrossRef
31.
go back to reference Kahrilas PJ, Logemann JA, Krugler C, Flanagan E. Volitional augmentation of upper esophageal sphincter opening during swallowing. Am J Physiol. 1991;260:G450–G456456.PubMed Kahrilas PJ, Logemann JA, Krugler C, Flanagan E. Volitional augmentation of upper esophageal sphincter opening during swallowing. Am J Physiol. 1991;260:G450–G456456.PubMed
32.
go back to reference Kahrilas PJ, Lin S, Chen J, Logemann JA. Oropharyngeal accommodation to swallow volume. Gastroenterology. 1996;111:297–306.CrossRef Kahrilas PJ, Lin S, Chen J, Logemann JA. Oropharyngeal accommodation to swallow volume. Gastroenterology. 1996;111:297–306.CrossRef
33.
go back to reference Vandaele DJ, Perlman AL, Cassell MD. Intrinsic fibre architecture and attachments of the human epiglottis and their contributions to the mechanism of deglutition. J Anat. 1995;186(Pt 1):1–15.PubMedPubMedCentral Vandaele DJ, Perlman AL, Cassell MD. Intrinsic fibre architecture and attachments of the human epiglottis and their contributions to the mechanism of deglutition. J Anat. 1995;186(Pt 1):1–15.PubMedPubMedCentral
34.
go back to reference Logemann JA, Kahrilas PJ, Cheng J, Pauloski BR, Gibbons PJ, Rademaker AW, Lin S. Closure mechanisms of laryngeal vestibule during swallow. Am J Physiol. 1992;262:G338–G34444.PubMed Logemann JA, Kahrilas PJ, Cheng J, Pauloski BR, Gibbons PJ, Rademaker AW, Lin S. Closure mechanisms of laryngeal vestibule during swallow. Am J Physiol. 1992;262:G338–G34444.PubMed
35.
go back to reference Ludlow CL, Humbert I, Saxon K, Poletto C, Sonies B, Crujido L. Effects of surface electrical stimulation both at rest and during swallowing in chronic pharyngeal Dysphagia. Dysphagia. 2007;22:1–10.CrossRef Ludlow CL, Humbert I, Saxon K, Poletto C, Sonies B, Crujido L. Effects of surface electrical stimulation both at rest and during swallowing in chronic pharyngeal Dysphagia. Dysphagia. 2007;22:1–10.CrossRef
36.
go back to reference Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81:929–69.CrossRef Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81:929–69.CrossRef
Metadata
Title
Impaired Movement Scaling and Reduced Synchrony with Vestibule Closure Characterize Swallowing in Severe Dysphagia
Authors
Seng Mun Wong
Erin Kamarunas
Christy L. Ludlow
Publication date
01-08-2020
Publisher
Springer US
Published in
Dysphagia / Issue 4/2020
Print ISSN: 0179-051X
Electronic ISSN: 1432-0460
DOI
https://doi.org/10.1007/s00455-019-10067-0

Other articles of this Issue 4/2020

Dysphagia 4/2020 Go to the issue