Skip to main content
Top
Published in: Dysphagia 5/2023

Open Access 27-04-2023 | Dysphagia | Original Article

Surface Electromyography for Evaluating the Effect of Aging on the Coordination of Swallowing Muscles

Authors: Wei-Han Chang, Mei-Hui Chen, Jen-Fang Liu, Wei Li Chung, Li-Ling Chiu, Yi-Fang Huang

Published in: Dysphagia | Issue 5/2023

Login to get access

Abstract

Swallowing function can deteriorate with age, leading to a risk of dysphagia. Swallowing evaluation by surface electromyography (sEMG) can be easily and extensively applied for an elderly population. This study evaluated the temporal events observed by sEMG to clarify how aging affects the coordination among the masticatory and suprahyoid muscles. We recruited elderly individuals (over 65 years old) who denied dysphagia. The sEMG activities of anterior temporalis, masseter, and suprahyoid muscles were recorded during 3, 15, and 30 ml water swallowing tests (WST). We calculated the time interval between anterior temporalis and suprahyoid peak activity (T-SH interval) and masseter and suprahyoid peak activity (M-SH interval) and analyzed their correlation with age. The subjects who could and could not swallow 30 ml of water in one gulp were further assigned into the one-gulp and piecemeal groups, respectively, for subgroup analysis. We recruited 101 subjects, among whom 75 (26 males and 49 females) were analyzed after excluding those with suspected dysphagia or low-quality sEMG recordings. Age was significantly correlated with the bilateral T-SH (left: r = 0.249, p = 0.031; right: r = 0.412, p < 0.01) and right M-SH (r = 0.242, p = 0.037) intervals in the 30 ml WST. The correlation between intervals and age were observed in both subgroups. sEMG can be used to investigate the effect of aging on the temporal coordination between masticatory and suprahyoid contraction. Further studies are needed to verify the validity of screening subclinical dysphagia in the elderly.
Literature
1.
go back to reference Wirth R, Dziewas R, Beck AM, Clave P, Hamdy S, Heppner HJ, Langmore S, Leischker AH, Martino R, Pluschinski P. Oropharyngeal dysphagia in older persons–from pathophysiology to adequate intervention: a review and summary of an international expert meeting. Clin Interv Aging. 2016;11:189.PubMedPubMedCentralCrossRef Wirth R, Dziewas R, Beck AM, Clave P, Hamdy S, Heppner HJ, Langmore S, Leischker AH, Martino R, Pluschinski P. Oropharyngeal dysphagia in older persons–from pathophysiology to adequate intervention: a review and summary of an international expert meeting. Clin Interv Aging. 2016;11:189.PubMedPubMedCentralCrossRef
3.
go back to reference Leonard R. Swallowing in the elderly: evidence from fluoroscopy. Perspectives on Swallowing and Swallowing Disorders (Dysphagia). 2010;19:103–14.CrossRef Leonard R. Swallowing in the elderly: evidence from fluoroscopy. Perspectives on Swallowing and Swallowing Disorders (Dysphagia). 2010;19:103–14.CrossRef
4.
go back to reference Aslam M, Vaezi MF. Dysphagia in the elderly. Gastroenterol Hepatol. 2013;9:784. Aslam M, Vaezi MF. Dysphagia in the elderly. Gastroenterol Hepatol. 2013;9:784.
5.
go back to reference Butler SG, Stuart A, Leng X, Rees C, Williamson J, Kritchevsky SB. Factors influencing aspiration during swallowing in healthy older adults. Laryngoscope. 2010;120:2147–52.PubMedPubMedCentralCrossRef Butler SG, Stuart A, Leng X, Rees C, Williamson J, Kritchevsky SB. Factors influencing aspiration during swallowing in healthy older adults. Laryngoscope. 2010;120:2147–52.PubMedPubMedCentralCrossRef
6.
go back to reference Muhle P, Wirth R, Glahn J, Dziewas R. Age-related changes in swallowing. Physiol pathophysiol Der Nervenarzt. 2015;86:440–51. Muhle P, Wirth R, Glahn J, Dziewas R. Age-related changes in swallowing. Physiol pathophysiol Der Nervenarzt. 2015;86:440–51.
7.
go back to reference Lin C-W, Chang Y-C, Chen W-S, Chang K, Chang H-Y, Wang T-G. Prolonged swallowing time in dysphagic Parkinsonism patients with aspiration pneumonia. Arch Phys Med Rehabil. 2012;93:2080–4.PubMedCrossRef Lin C-W, Chang Y-C, Chen W-S, Chang K, Chang H-Y, Wang T-G. Prolonged swallowing time in dysphagic Parkinsonism patients with aspiration pneumonia. Arch Phys Med Rehabil. 2012;93:2080–4.PubMedCrossRef
8.
go back to reference Johnson ER, McKenzie SW, Sievers A. Aspiration pneumonia in stroke. Arch Phys Med Rehabil. 1993;74:973–6.PubMed Johnson ER, McKenzie SW, Sievers A. Aspiration pneumonia in stroke. Arch Phys Med Rehabil. 1993;74:973–6.PubMed
9.
go back to reference Rofes L, Arreola V, Romea M, Palomera E, Almirall J, Cabré M, Serra-Prat M, Clavé P. Pathophysiology of oropharyngeal dysphagia in the frail elderly. Neurogastroenterol Motil. 2010;22:851-e230.PubMedCrossRef Rofes L, Arreola V, Romea M, Palomera E, Almirall J, Cabré M, Serra-Prat M, Clavé P. Pathophysiology of oropharyngeal dysphagia in the frail elderly. Neurogastroenterol Motil. 2010;22:851-e230.PubMedCrossRef
10.
go back to reference Butler SG, Stuart A, Leng X, Wilhelm E, Rees C, Williamson J, Kritchevsky SB. The relationship of aspiration status with tongue and handgrip strength in healthy older adults. J Gerontol Series A: Biomed Sci Med Sci. 2011;66:452–8.CrossRef Butler SG, Stuart A, Leng X, Wilhelm E, Rees C, Williamson J, Kritchevsky SB. The relationship of aspiration status with tongue and handgrip strength in healthy older adults. J Gerontol Series A: Biomed Sci Med Sci. 2011;66:452–8.CrossRef
11.
go back to reference Feng X, Todd T, Lintzenich CR, Ding J, Carr JJ, Ge Y, Browne JD, Kritchevsky SB, Butler SG. Aging-related geniohyoid muscle atrophy is related to aspiration status in healthy older adults. J Gerontol Series A: Biomed Sci Med Sci. 2013;68:853–60.CrossRef Feng X, Todd T, Lintzenich CR, Ding J, Carr JJ, Ge Y, Browne JD, Kritchevsky SB, Butler SG. Aging-related geniohyoid muscle atrophy is related to aspiration status in healthy older adults. J Gerontol Series A: Biomed Sci Med Sci. 2013;68:853–60.CrossRef
12.
go back to reference Feng X, Todd T, Hu Y, Lintzenich CR, Carr JJ, Browne JD, Kritchevsky SB, Butler SG. Age-related changes of hyoid bone position in healthy older adults with aspiration. Laryngoscope. 2014;124:E231-6.PubMedCrossRef Feng X, Todd T, Hu Y, Lintzenich CR, Carr JJ, Browne JD, Kritchevsky SB, Butler SG. Age-related changes of hyoid bone position in healthy older adults with aspiration. Laryngoscope. 2014;124:E231-6.PubMedCrossRef
13.
go back to reference Ekberg O, Feinberg MJ. Altered swallowing function in elderly patients without dysphagia: radiologic findings in 56 cases. AJR Am J Roentgenol. 1991;156:1181–4.PubMedCrossRef Ekberg O, Feinberg MJ. Altered swallowing function in elderly patients without dysphagia: radiologic findings in 56 cases. AJR Am J Roentgenol. 1991;156:1181–4.PubMedCrossRef
14.
go back to reference Wakabayashi H. Presbyphagia and sarcopenic dysphagia: association between aging, sarcopenia, and deglutition disorders. J Frailty Aging. 2014;3:97.PubMed Wakabayashi H. Presbyphagia and sarcopenic dysphagia: association between aging, sarcopenia, and deglutition disorders. J Frailty Aging. 2014;3:97.PubMed
15.
go back to reference de Lima Alvarenga EH. Dall’Oglio GP, Murano EZ, Abrahão M: continuum theory: presbyphagia to dysphagia? Functional assessment of swallowing in the elderly. Eur Arch Otorhinolaryngol. 2018;275:443–9.PubMedCrossRef de Lima Alvarenga EH. Dall’Oglio GP, Murano EZ, Abrahão M: continuum theory: presbyphagia to dysphagia? Functional assessment of swallowing in the elderly. Eur Arch Otorhinolaryngol. 2018;275:443–9.PubMedCrossRef
16.
go back to reference Speyer R. Oropharyngeal dysphagia: screening and assessment. Otolaryngol Clin North Am. 2013;46:989–1008.PubMedCrossRef Speyer R. Oropharyngeal dysphagia: screening and assessment. Otolaryngol Clin North Am. 2013;46:989–1008.PubMedCrossRef
17.
go back to reference Rommel N, Hamdy S. Oropharyngeal dysphagia: manifestations and diagnosis. Nat Rev Gastroenterol Hepatol. 2016;13:49–59.PubMedCrossRef Rommel N, Hamdy S. Oropharyngeal dysphagia: manifestations and diagnosis. Nat Rev Gastroenterol Hepatol. 2016;13:49–59.PubMedCrossRef
18.
go back to reference Hashimoto H, Hirata M, Takahashi K, Kameda S, Katsuta Y, Yoshida F, Hattori N, Yanagisawa T, Palmer J, Oshino S. Non-invasive quantification of human swallowing using a simple motion tracking system. Sci Rep. 2018;8:1–9.CrossRef Hashimoto H, Hirata M, Takahashi K, Kameda S, Katsuta Y, Yoshida F, Hattori N, Yanagisawa T, Palmer J, Oshino S. Non-invasive quantification of human swallowing using a simple motion tracking system. Sci Rep. 2018;8:1–9.CrossRef
20.
go back to reference Poorjavad M, Talebian S, Ansari NN, Soleymani Z. Surface electromyographic assessment of swallowing function. Iran J Med Sci. 2017;42:194.PubMedPubMedCentral Poorjavad M, Talebian S, Ansari NN, Soleymani Z. Surface electromyographic assessment of swallowing function. Iran J Med Sci. 2017;42:194.PubMedPubMedCentral
21.
go back to reference Vaiman M, Eviatar E, Segal S. Surface electromyographic studies of swallowing in normal subjects: a review of 440 adults. Report 1. Quantitative data: timing measures. Otolaryngol-Head Neck Surg. 2004;131:548–55.PubMedCrossRef Vaiman M, Eviatar E, Segal S. Surface electromyographic studies of swallowing in normal subjects: a review of 440 adults. Report 1. Quantitative data: timing measures. Otolaryngol-Head Neck Surg. 2004;131:548–55.PubMedCrossRef
22.
go back to reference Hiraoka K. Changes in masseter muscle activity associated with swallowing. J Oral Rehabil. 2004;31:963–7.PubMedCrossRef Hiraoka K. Changes in masseter muscle activity associated with swallowing. J Oral Rehabil. 2004;31:963–7.PubMedCrossRef
23.
go back to reference Takeda H, Saitoh K. Impact of proprioception during the oral phase on initiating the swallowing reflex. Laryngoscope. 2016;126:1595–9.PubMedCrossRef Takeda H, Saitoh K. Impact of proprioception during the oral phase on initiating the swallowing reflex. Laryngoscope. 2016;126:1595–9.PubMedCrossRef
24.
go back to reference Yoneda M, Saitoh K. Modification of masticatory rhythmicity leading to the initiation of the swallowing reflex in humans. Dysphagia. 2018;33:358–68.PubMedCrossRef Yoneda M, Saitoh K. Modification of masticatory rhythmicity leading to the initiation of the swallowing reflex in humans. Dysphagia. 2018;33:358–68.PubMedCrossRef
25.
go back to reference Vaiman M, Eviatar E, Segal S. Surface electromyographic studies of swallowing in normal subjects: a review of 440 adults. Report 2. Quantitative data: amplitude measures. Otolaryngol-Head Neck Surg. 2004;131:773–80.PubMedCrossRef Vaiman M, Eviatar E, Segal S. Surface electromyographic studies of swallowing in normal subjects: a review of 440 adults. Report 2. Quantitative data: amplitude measures. Otolaryngol-Head Neck Surg. 2004;131:773–80.PubMedCrossRef
26.
go back to reference Corti G, Ghiggi A, Murelli M, Tettamanti A. Surface electromyographic pattern of masseter, orbicularis oris and submental muscles during swallowing of different cosisitencies in healthy subject. J Physiother. 2012;2:65–73. Corti G, Ghiggi A, Murelli M, Tettamanti A. Surface electromyographic pattern of masseter, orbicularis oris and submental muscles during swallowing of different cosisitencies in healthy subject. J Physiother. 2012;2:65–73.
27.
go back to reference Gaszynska E, Kopacz K, Fronczek-Wojciechowska M, Padula G, Szatko F. Electromyographic activity of masticatory muscles in elderly women–a pilot study. Clin Interv Aging. 2017;12:111.PubMedPubMedCentralCrossRef Gaszynska E, Kopacz K, Fronczek-Wojciechowska M, Padula G, Szatko F. Electromyographic activity of masticatory muscles in elderly women–a pilot study. Clin Interv Aging. 2017;12:111.PubMedPubMedCentralCrossRef
28.
go back to reference Kang AJ, Kim D-K, Kang SH, Seo KM, Park HS, Park K-H. EMG activity of masseter muscles in the elderly according to rheological properties of solid food. Ann Rehabil Med. 2016;40:447.PubMedPubMedCentralCrossRef Kang AJ, Kim D-K, Kang SH, Seo KM, Park HS, Park K-H. EMG activity of masseter muscles in the elderly according to rheological properties of solid food. Ann Rehabil Med. 2016;40:447.PubMedPubMedCentralCrossRef
29.
go back to reference Cecilio F, Regalo S, Palinkas M, Issa J, Siéssere S, Hallak J, Machado-de-Sousa J, Semprini M. Ageing and surface EMG activity patterns of masticatory muscles. J Oral Rehabil. 2010;37:248–55.PubMedCrossRef Cecilio F, Regalo S, Palinkas M, Issa J, Siéssere S, Hallak J, Machado-de-Sousa J, Semprini M. Ageing and surface EMG activity patterns of masticatory muscles. J Oral Rehabil. 2010;37:248–55.PubMedCrossRef
30.
go back to reference Endo H, Ohmori N, Chikai M, Miwa H, Ino S. Effects of age and gender on swallowing activity assessed by electromyography and laryngeal elevation. J Oral Rehabil. 2008;47(11):1358–67.CrossRef Endo H, Ohmori N, Chikai M, Miwa H, Ino S. Effects of age and gender on swallowing activity assessed by electromyography and laryngeal elevation. J Oral Rehabil. 2008;47(11):1358–67.CrossRef
31.
go back to reference Chen M-Y, Lin L-C. Nonimaging clinical assessment of impaired swallowing in community-dwelling older adults in Taiwan. J Nurs Res. 2012;20:272–80.PubMedCrossRef Chen M-Y, Lin L-C. Nonimaging clinical assessment of impaired swallowing in community-dwelling older adults in Taiwan. J Nurs Res. 2012;20:272–80.PubMedCrossRef
33.
go back to reference Morita K, Tsuka H, Kato K, Mori T, Nishimura R, Yoshida M, Tsuga K. Factors related to masticatory performance in healthy elderly individuals. J Prosthodont Res. 2018;62:432–5.PubMedCrossRef Morita K, Tsuka H, Kato K, Mori T, Nishimura R, Yoshida M, Tsuga K. Factors related to masticatory performance in healthy elderly individuals. J Prosthodont Res. 2018;62:432–5.PubMedCrossRef
34.
go back to reference Bokare B, Singh S. Physiology of swallowing Textbook of Laryngology. New Delhi: Jaypee Brothers Medical Publishers (P) Ltd; 2017. p. 31. Bokare B, Singh S. Physiology of swallowing Textbook of Laryngology. New Delhi: Jaypee Brothers Medical Publishers (P) Ltd; 2017. p. 31.
35.
go back to reference Ding R, Larson CR, Logemann JA, Rademaker AW. Surface electromyographic and electroglottographic studies in normal subjects under two swallow conditions: normal and during the Mendelsohn manuever. Dysphagia. 2002;17:1–12.PubMedCrossRef Ding R, Larson CR, Logemann JA, Rademaker AW. Surface electromyographic and electroglottographic studies in normal subjects under two swallow conditions: normal and during the Mendelsohn manuever. Dysphagia. 2002;17:1–12.PubMedCrossRef
36.
go back to reference Seta H, Hashimoto K, Inada H, Sugimoto A, Abo M. Laterality of swallowing in healthy subjects by AP projection using videofluoroscopy. Dysphagia. 2006;21:191–7.PubMedCrossRef Seta H, Hashimoto K, Inada H, Sugimoto A, Abo M. Laterality of swallowing in healthy subjects by AP projection using videofluoroscopy. Dysphagia. 2006;21:191–7.PubMedCrossRef
37.
go back to reference Rofes L, Arreola V, Clavé P. The volume-viscosity swallow test for clinical screening of dysphagia and aspiration. Stepping Stones to Living Well with Dysphagia. Basel: Karger Publishers; 2012. p. 33–42.CrossRef Rofes L, Arreola V, Clavé P. The volume-viscosity swallow test for clinical screening of dysphagia and aspiration. Stepping Stones to Living Well with Dysphagia. Basel: Karger Publishers; 2012. p. 33–42.CrossRef
38.
go back to reference Lawless HT, Bender S, Oman C, Pelletier C. Gender, age, vessel size, cup vs. straw sipping, and sequence effects on sip volume. Dysphagia. 2003;18:196–202.PubMedCrossRef Lawless HT, Bender S, Oman C, Pelletier C. Gender, age, vessel size, cup vs. straw sipping, and sequence effects on sip volume. Dysphagia. 2003;18:196–202.PubMedCrossRef
39.
40.
go back to reference Mistry S, Hamdy S. Neural control of feeding and swallowing. Phys Med Rehabil Clin N Am. 2008;19:709–28.PubMedCrossRef Mistry S, Hamdy S. Neural control of feeding and swallowing. Phys Med Rehabil Clin N Am. 2008;19:709–28.PubMedCrossRef
41.
go back to reference Teismann IK, Steinstraeter O, Schwindt W, Ringelstein EB, Pantev C, Dziewas R. Age-related changes in cortical swallowing processing. Neurobiol Aging. 2010;31:1044–50.PubMedCrossRef Teismann IK, Steinstraeter O, Schwindt W, Ringelstein EB, Pantev C, Dziewas R. Age-related changes in cortical swallowing processing. Neurobiol Aging. 2010;31:1044–50.PubMedCrossRef
43.
go back to reference Humbert IA, Fitzgerald ME, McLaren DG, Johnson S, Porcaro E, Kosmatka K, Hind J, Robbins J. Neurophysiology of swallowing: effects of age and bolus type. Neuroimage. 2009;44:982–91.PubMedCrossRef Humbert IA, Fitzgerald ME, McLaren DG, Johnson S, Porcaro E, Kosmatka K, Hind J, Robbins J. Neurophysiology of swallowing: effects of age and bolus type. Neuroimage. 2009;44:982–91.PubMedCrossRef
44.
go back to reference Perlman A, Palmer P, McCulloch T, Vandaele D. Electromyographic activity from human laryngeal, pharyngeal, and submental muscles during swallowing. J Appl Physiol. 1999;86:1663–9.PubMedCrossRef Perlman A, Palmer P, McCulloch T, Vandaele D. Electromyographic activity from human laryngeal, pharyngeal, and submental muscles during swallowing. J Appl Physiol. 1999;86:1663–9.PubMedCrossRef
45.
go back to reference Ertekin C, Aydogdu I, Yüceyar N, Pehlivan M, Estas M, Uludag B, Çelebi G: Effects of bolus volume on oropharyngeal swallowing: an electrophysiologic study in man. American Journal of Gastroenterology (Springer Nature) 92, 1997. Ertekin C, Aydogdu I, Yüceyar N, Pehlivan M, Estas M, Uludag B, Çelebi G: Effects of bolus volume on oropharyngeal swallowing: an electrophysiologic study in man. American Journal of Gastroenterology (Springer Nature) 92, 1997.
46.
go back to reference Miyaoka Y, Ashida I, Kawakami S, Tamaki Y, Miyaoka S. Activity patterns of the suprahyoid muscles during swallowing of different fluid volumes. J Oral Rehabil. 2010;37:575–82.PubMed Miyaoka Y, Ashida I, Kawakami S, Tamaki Y, Miyaoka S. Activity patterns of the suprahyoid muscles during swallowing of different fluid volumes. J Oral Rehabil. 2010;37:575–82.PubMed
48.
go back to reference Naeije M, McCarroll R, Weijs W. Electromyographic activity of the human masticatory muscles during submaximal clenching in the inter-cuspal position. J Oral Rehabil. 1989;16:63–70.PubMedCrossRef Naeije M, McCarroll R, Weijs W. Electromyographic activity of the human masticatory muscles during submaximal clenching in the inter-cuspal position. J Oral Rehabil. 1989;16:63–70.PubMedCrossRef
Metadata
Title
Surface Electromyography for Evaluating the Effect of Aging on the Coordination of Swallowing Muscles
Authors
Wei-Han Chang
Mei-Hui Chen
Jen-Fang Liu
Wei Li Chung
Li-Ling Chiu
Yi-Fang Huang
Publication date
27-04-2023
Publisher
Springer US
Published in
Dysphagia / Issue 5/2023
Print ISSN: 0179-051X
Electronic ISSN: 1432-0460
DOI
https://doi.org/10.1007/s00455-023-10572-3

Other articles of this Issue 5/2023

Dysphagia 5/2023 Go to the issue