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Chewing Well Modulates Pharyngeal Bolus Transit During Swallowing in Healthy Participants

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Abstract

Mastication is controlled by central pattern generator in the brainstem and can be modulated by volition. The aim of this study was to investigate the effect of chewing well on swallowing. Twenty-six healthy participants were instructed to eat 8, 12, and/or 16 g of steamed rice with barium sulphate under the following two conditions: chewing freely task (CF; chewing naturally in their usual manner) and chewing well task (CW; chewing the food with a request to “chew well”). We evaluated bolus transport and swallowing movement using videofluoroscopy and electromyography of the masseter, suprahyoid and thyrohyoid muscles. The chewing time and pharyngeal transit time (PTT) at the first swallow showed high reproducibility in both CF and CW. PTT for CW was significantly shorter and longer than CF in 12 and 16 g, respectively. In 12 g, CW increased the pharyngeal bolus velocity and decreased thyrohyoid EMG activity during swallowing compared with CF. In 16 g, the difference between CW and CF in the estimated swallowed bolus volume was positively correlated with that in upper esophageal sphincter transit duration. We speculate that CW modulates PTT during swallowing depending on the mouthful volume.

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Data Availability

All data generated or analyzed during this study are available from the corresponding author T.T. upon reasonable request.

Abbreviations

CW:

Chewing well

CF:

Chewing freely

EMG:

Electromyography

PTT:

Pharyngeal transit time

ICC:

Intraclass correlation coefficient

Mas:

Masseter

SD:

Standard deviation

SH:

Suprahyoid

TH:

Thyrohyoid

UES:

Upper esophageal sphincter

VF:

Videofluoroscopy

References

  1. Dellow PG, Lund JP. Evidence for central timing of rhythmical mastication. J Physiol. 1971;215:1–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Ashiga H, Takei E, Magara J, Takeishi R, Tsujimura T, Nagoya K, Inoue M. Effect of attention on chewing and swallowing behaviors in healthy humans. Sci Rep. 2019;9:6013.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Furuya J, Hara A, Nomura T, Kondo H. Volitional chewing with a conscious effort alters and facilitates swallowing during feeding sequence. J Oral Rehabil. 2014;41:191–8.

    Article  CAS  PubMed  Google Scholar 

  4. Palmer JB, Hiiemae KM, Matsuo K, Haishima H. Volitional control of food transport and bolus formation during feeding. Physiol Behav. 2007;91:66–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Shingai T, Miyaoka Y, Ikarashi R, Shimada K. Swallowing reflex elicited by water and taste solutions in humans. Am J Physiol. 1989;256:R822–6.

    CAS  PubMed  Google Scholar 

  6. Kitagawa JI, Shingai T, Takahashi Y, Yamada Y. Pharyngeal branch of the glossopharyngeal nerve plays a major role in reflex swallowing from the pharynx. Am J Physiol-Regul Integr Compar Physiol. 2002;282:R1342–7.

    Article  CAS  Google Scholar 

  7. Hiiemae KM, Palmer JB. Food transport and bolus formation during complete feeding sequences on foods of different initial consistency. Dysphagia. 1999;14:31–42.

    Article  CAS  PubMed  Google Scholar 

  8. Palmer JB, Rudin NJ, Lara G, Crompton AW. Coordination of mastication and swallowing. Dysphagia. 1992;7:187–200.

    Article  CAS  PubMed  Google Scholar 

  9. Amri M, Lamkadem M, Car A. Effects of lingual nerve and chewing cortex stimulation upon activity of the swallowing neurons located in the region of the hypoglossal motor nucleus. Brain Res. 1991;548:149–55.

    Article  CAS  PubMed  Google Scholar 

  10. Lamkadem M, Zoungrana OR, Amri M, Car A, Roman C. Stimulation of the chewing area of the cerebral cortex induces inhibitory effects upon swallowing in sheep. Brain Res. 1999;832:97–111.

    Article  CAS  PubMed  Google Scholar 

  11. Tsujimura T, Tsuji K, Ariyasinghe S, Fukuhara T, Yamada A, Hayashi H, Nakamura Y, Iwata K, Inoue M. Differential involvement of two cortical masticatory areas in modulation of the swallowing reflex in rats. Neurosci Lett. 2012;528:159–64.

    Article  CAS  PubMed  Google Scholar 

  12. Tsujimura T, Tsuji K, Magara J, Sakai S, Suzuki T, Nakamura Y, Nozawa-Inoue K, Inoue M. Differential response properties of peripherally and cortically evoked swallows by electrical stimulation in anesthetized rats. Brain Res Bull. 2016;122:12–8.

    Article  PubMed  Google Scholar 

  13. Hiraoka T, Palmer JB, Brodsky MB, Yoda M, Inokuchi H, Tsubahara A. Food transit duration is associated with the number of stage II transport cycles when eating solid food. Arch Oral Biol. 2017;81:186–91.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Yamashita S, Sugita D, Matsuo K. Relationship between stage II transport and number of chewing strokes as mastication progresses. Physiol Behav. 2013;122:100–3.

    Article  CAS  PubMed  Google Scholar 

  15. Fushida S, Kosaka T, Nakai M, Kida M, Nokubi T, Kokubo Y, Watanabe M, Miyamoto Y, Ono T, Ikebe K. Lower masticatory performance is a risk for the development of the metabolic syndrome: the Suita study. Front Cardiovasc Med. 2021;8: 752667.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Yamazaki T, Yamori M, Asai K, Nakano-Araki I, Yamaguchi A, Takahashi K, Sekine A, Matsuda F, Kosugi S, Nakayama T, Inagaki N, Bessho K. Nagahama Study Collaboration G: Mastication and risk for diabetes in a Japanese population: a cross-sectional study. PLoS ONE. 2013;8: e64113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Feinberg MJ. Radiographic techniques and interpretation of abnormal swallowing in adult and elderly patients. Dysphagia. 1993;8:356–8.

    Article  CAS  PubMed  Google Scholar 

  18. Berzlanovich AM, Fazeny-Dorner B, Waldhoer T, Fasching P, Keil W. Foreign body asphyxia: a preventable cause of death in the elderly. Am J Prev Med. 2005;28:65–9.

    PubMed  Google Scholar 

  19. Maeda R, Takei E, Ito K, Magara J, Tsujimura T, Inoue M. Inter-individual variation of bolus properties in triggering swallowing during chewing in healthy humans. J Oral Rehabil. 2020;47:1161–70.

    Article  PubMed  Google Scholar 

  20. Nakamichi A, Matsuyama M, Ichikawa T. Relationship between mouthful volume and number of chews in young Japanese females. Appetite. 2014;83:327–32.

    Article  PubMed  Google Scholar 

  21. Okada A, Honma A, Nomura S, Yamada Y. Oral behavior from food intake until terminal swallow. Physiol Behav. 2007;90:172–9.

    Article  CAS  PubMed  Google Scholar 

  22. Palmer PM, Luschei ES, Jaffe D, McCulloch TM. Contributions of individual muscles to the submental surface electromyogram during swallowing. J Speech Lang Hear Res. 1999;42:1378–91.

    Article  CAS  PubMed  Google Scholar 

  23. Park HS, Kim DK, Lee SY, Park KH. The effect of aging on mastication and swallowing parameters according to the hardness change of solid food. J Texture Stud. 2017;48:362–9.

    Article  PubMed  Google Scholar 

  24. Ertekin C, Kiylioglu N, Tarlaci S, Turman AB, Secil Y, Aydogdu I. Voluntary and reflex influences on the initiation of swallowing reflex in man. Dysphagia. 2001;16:40–7.

    Article  CAS  PubMed  Google Scholar 

  25. Pearson WG Jr, Langmore SE, Yu LB, Zumwalt AC. Structural analysis of muscles elevating the hyolaryngeal complex. Dysphagia. 2012;27:445–51.

    Article  PubMed  PubMed Central  Google Scholar 

  26. McConnel FM. Analysis of pressure generation and bolus transit during pharyngeal swallowing. Laryngoscope. 1988;98:71–8.

    Article  CAS  PubMed  Google Scholar 

  27. Pouderoux P, Kahrilas PJ. Deglutitive tongue force modulation by volition, volume, and viscosity in humans. Gastroenterology. 1995;108:1418–26.

    Article  CAS  PubMed  Google Scholar 

  28. Huckabee ML, Steele CM. An analysis of lingual contribution to submental surface electromyographic measures and pharyngeal pressure during effortful swallow. Arch Phys Med Rehabil. 2006;87:1067–72.

    Article  PubMed  Google Scholar 

  29. Anderson DJ, Hector MP, Linden RWA. The effects of unilateral and bilateral chewing, empty clenching and simulated bruxism, on the masticatory-parotid salivary reflex in man. Exp Physiol. 1996;81:305–12.

    Article  CAS  PubMed  Google Scholar 

  30. Mosca AC, Chen JS. Food-saliva interactions: mechanisms and implications. Trends Food Sci Technol. 2017;66:125–34.

    Article  CAS  Google Scholar 

  31. Ferris L, Doeltgen S, Cock C, Rommel N, Schar M, Carrion S, Scholten I, Omari T. Modulation of pharyngeal swallowing by bolus volume and viscosity. Am J Physiol Gastrointest Liver Physiol. 2021;320:G43–53.

    Article  CAS  PubMed  Google Scholar 

  32. Cock C, Jones CA, Hammer MJ, Omari TI, McCulloch TM. Modulation of upper esophageal sphincter (UES) relaxation and opening during volume swallowing. Dysphagia. 2017;32:216–24.

    Article  PubMed  Google Scholar 

  33. Nascimento WV, Cassiani RA, Santos CM, Dantas RO. Effect of bolus volume and consistency on swallowing events duration in healthy subjects. J Neurogastroenterol Motil. 2015;21:78–82.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Kochi I, Takei E, Maeda R, Ito K, Magara J, Tsujimura T, Kulvanich S, Inoue M. Changes of bolus properties and the triggering of swallowing in healthy humans. J Oral Rehabil. 2021;48:592–600.

    Article  PubMed  Google Scholar 

  35. Chi-Fishman G, Sonies BC. Effects of systematic bolus viscosity and volume changes on hyoid movement kinematics. Dysphagia. 2002;17:278–87.

    Article  PubMed  Google Scholar 

  36. Ertekin C, Aydogdu I, Yuceyar N, Pehlivan M, Ertas M, Uludag B, Celebi G. Effects of bolus volume on oropharyngeal swallowing: an electrophysiologic study in man. Am J Gastroenterol. 1997;92:2049–53.

    CAS  PubMed  Google Scholar 

  37. 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.

    CAS  PubMed  Google Scholar 

  38. Moon IY, Yi CH, Park IW, Yong JH. Effects of sitting posture and bolus volume on activation of swallowing-related muscles. J Oral Rehabil. 2020;47:577–83.

    Article  PubMed  Google Scholar 

  39. Perlman AL, Palmer PM, McCulloch TM, Vandaele DJ. Electromyographic activity from human laryngeal, pharyngeal, and submental muscles during swallowing. J Appl Physiol. 1985;86(1663–1669):1999.

    Google Scholar 

  40. Ueda N, Nohara K, Kotani Y, Tanaka N, Okuno K, Sakai T. Effects of the bolus volume on hyoid movements in normal individuals. J Oral Rehabil. 2013;40:491–9.

    Article  CAS  PubMed  Google Scholar 

  41. Woda A, Foster K, Mishellany A, Peyron MA. Adaptation of healthy mastication to factors pertaining to the individual or to the food. Physiol Behav. 2006;89:28–35.

    Article  CAS  PubMed  Google Scholar 

  42. Uehara F, Hori K, Hasegawa Y, Yoshimura S, Hori S, Kitamura M, Akazawa K, Ono T. Impact of masticatory behaviors measured with wearable device on metabolic syndrome: cross-sectional study. JMIR Mhealth Uhealth. 2022;10: e30789.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Helen Jeays, BDSc AE, from Edanz (https://jp.edanz.com/ac) for editing a draft of this manuscript.

Funding

This study was supported in part by a grant from JSPS KAKENHI (Grant Numbers 20K10069 to T.T.) and a grant from Food and Health Science Yazuya to T.T.

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Correspondence to Takanori Tsujimura.

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Ethical Approval and Consent

The Ethics Committee of Niigata University approved this study (approval number: 2020-0173). The participants provided written informed consent, and the study was performed in accordance with the Declaration of Helsinki and the Ethical Guidelines for Medical and Health Research Involving Human Subjects.

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Okubo, A., Tsujimura, T., Ueha, R. et al. Chewing Well Modulates Pharyngeal Bolus Transit During Swallowing in Healthy Participants. Dysphagia (2024). https://doi.org/10.1007/s00455-024-10689-z

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