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The Cross-Sectional Area of the Middle and Base of the Tongue is Associated with Swallowing-Related Muscle Strength

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Abstract

Muscle strength and function are generally positively correlated with muscle quantity and negatively correlated with muscle quality; however, the tongue shows a unique tendency, different from limb muscles. The relationship between the characteristics of each part of the tongue, muscle strength and function, and systemic factors has been unclear. The aim of the study was to investigate the relationship between cross-sectional area (CSA) and echo intensity (EI) of the middle and base of the tongue and swallowing, articulation function, and body composition. Eighty-nine healthy individuals were included in this cross-sectional study. Swallowing was assessed using tongue pressure (TP) and jaw opening force (JOF) as they indicate swallowing-related muscle strength. Articulation function was evaluated through oral diadochokinesis (ODK). Bioelectrical impedance analysis was performed for body composition. CSAs and EIs of the middle and base of the tongue were measured using ultrasound. Multiple regression analysis was used to examine the relationship between the characteristics of the tongue, swallowing-related muscle strength, and ODK. In multiple regression analysis with TP as the dependent variable, age (β = − 0.22, P < 0.01) and CSA of the middle part (β = 0.02, P < 0.01) were significant explanatory variables. In multiple regression analysis with JOF as the dependent variable, sex (β = − 2.76, P < 0.01) and CSA of the base (β = − 0.004, P < 0.05) were significant explanatory variables. Multiple regression analysis with articulation function as the dependent variable did not yield significant results. The CSA of the tongue is a better indicator of swallowing-related muscle strength than EI. Ultrasonography may be used for assessing swallowing-related muscle strength.

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References

  1. Maeda K, Akagi J. Decreased tongue pressure is associated with sarcopenia and sarcopenic dysphagia in the elderly. Dysphagia. 2015;30:80–7. https://doi.org/10.1007/s00455-014-9577-y.

    Article  PubMed  Google Scholar 

  2. Rong P, Green JR. Predicting speech intelligibility based on spatial tongue-jaw coupling in persons with amyotrophic lateral sclerosis: the impact of tongue weakness and jaw adaptation. J Speech Lang Hear Res. 2019;62:3085–103. https://doi.org/10.1044/2018_JSLHR-S-CSMC7-18-0116.

    Article  PubMed  Google Scholar 

  3. van der Maarel-Wierink CD, Vanobbergen JN, Bronkhorst EM, Schols JM, de Baat C. Meta-analysis of dysphagia and aspiration pneumonia in frail elders. J Dent Res. 2011;90:1398–404. https://doi.org/10.1177/0022034511422909.

    Article  PubMed  Google Scholar 

  4. Maresca G, Pranio F, Naro A, De Luca R, Maggio MG, Scarcella I, et al. Augmentative and alternative communication improves quality of life in the early stages of amyotrophic lateral sclerosis. Funct Neurol. 2019;34:35–43.

    CAS  PubMed  Google Scholar 

  5. Kim AM, Keenan BT, Jackson N, Chan EL, Staley B, Poptani H, et al. Tongue fat and its relationship to obstructive sleep apnea. Sleep. 2014;37:1639–48. https://doi.org/10.5665/sleep.4072.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Bradley TD, Floras JS. Obstructive sleep apnea and its cardiovascular consequences. Lancet. 2009;373:82–93. https://doi.org/10.1016/S0140-6736(08)61622-0.

    Article  PubMed  Google Scholar 

  7. Yaggi HK, Concato J, Kernan WN, Lichtman JH, Brass LM, Mohsenin V. Obstructive sleep apnea as a risk factor for stroke and death. N Engl J Med. 2005;353:2034–41. https://doi.org/10.1056/NEJMoa043104.

    Article  CAS  PubMed  Google Scholar 

  8. Yamaguchi K, Hara K, Nakagawa K, Yoshimi K, Ariya C, Nakane A, et al. Ultrasonography shows age-related changes and related factors in the tongue and suprahyoid muscles. J Am Med Dir Assoc. 2021;22:766–72. https://doi.org/10.1016/j.jamda.2020.10.012.

    Article  PubMed  Google Scholar 

  9. Nashi N, Kang S, Barkdull GC, Lucas J, Davidson TM. Lingual fat at autopsy. Laryngoscope. 2007;117:1467–73. https://doi.org/10.1097/MLG.0b013e318068b566.

    Article  PubMed  Google Scholar 

  10. Ogawa N, Mori T, Fujishima I, Wakabayashi H, Itoda M, Kunieda K, et al. Ultrasonography to measure swallowing muscle mass and quality in older patients with sarcopenic dysphagia. J Am Med Dir Assoc. 2018;19:516–22. https://doi.org/10.1016/j.jamda.2017.11.007.

    Article  PubMed  Google Scholar 

  11. Biltz NK, Collins KH, Shen KC, Schwartz K, Harris CA, Meyer GA. Infiltration of intramuscular adipose tissue impairs skeletal muscle contraction. J Physiol. 2020;598:2669–83. https://doi.org/10.1113/JP279595.

    Article  CAS  PubMed  Google Scholar 

  12. Sanders I, Mu L, Amirali A, Su H, Sobotka S. The human tongue slows down to speak: muscle fibers of the human tongue. Anat Rec (Hoboken). 2013;296:1615–27. https://doi.org/10.1002/ar.22755.

    Article  Google Scholar 

  13. Nakao Y, Yamashita T, Honda K, Katsuura T, Hama Y, Nakamura Y, et al. Association among age-related tongue muscle abnormality, tongue pressure, and presbyphagia: a 3D MRI study. Dysphagia. 2021;36:483–91. https://doi.org/10.1007/s00455-020-10165-4.

    Article  PubMed  Google Scholar 

  14. International Phonetic Association. Handbook of the international phonetic association: a guide to the use of the international phonetic alphabet. Cambridge: Cambridge University Press; 1999.

    Google Scholar 

  15. Matsuo K, Palmer JB. Anatomy and physiology of feeding and swallowing: normal and abnormal. Phys Med Rehabil Clin N Am. 2008;19:691–707. https://doi.org/10.1016/j.pmr.2008.06.001.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2), the Extended Group for EWGSOP2, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48:16–31. https://doi.org/10.1093/ageing/afy169.

  17. Young HJ, Jenkins NT, Zhao Q, Mccully KK. Measurement of intramuscular fat by muscle echo intensity. Muscle Nerve. 2015;52:963–71. https://doi.org/10.1002/mus.24656.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Chantaramanee A, Tohara H, Nakagawa K, Hara K, Nakane A, Yamaguchi K, et al. Association between echo intensity of the tongue and its thickness and function in elderly subjects. J Oral Rehabil. 2019;46:634–9. https://doi.org/10.1111/joor.12788.

    Article  PubMed  Google Scholar 

  19. Mori T, Wakabayashi H, Ogawa N, Fujishima I, Oshima F, Itoda M, et al. The mass of geniohyoid muscle is associated with maximum tongue pressure and tongue area in patients with sarcopenic dysphagia. J Nutr Health Aging. 2021;25:356–60. https://doi.org/10.1007/s12603-020-1528-8.

    Article  CAS  PubMed  Google Scholar 

  20. Namiki C, Hara K, Tohara H, Kobayashi K, Chantaramanee A, Nakagawa K, et al. Tongue-pressure resistance training improves tongue and suprahyoid muscle functions simultaneously. Clin Interv Aging. 2019;14:601–8. https://doi.org/10.2147/CIA.S194808.

    Article  PubMed  PubMed Central  Google Scholar 

  21. 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 (1985). 2013;114:472–81. https://doi.org/10.1152/japplphysiol.01370.2012.

    Article  Google Scholar 

  22. Nagano A, Maeda K, Koike M, Murotani K, Ueshima J, Shimizu A, et al. Effects of physical rehabilitation and nutritional intake management on improvement in tongue strength in sarcopenic patients. Nutrients. 2020;12:3104. https://doi.org/10.3390/nu12103104.

    Article  CAS  PubMed Central  Google Scholar 

  23. Yamaguchi K, Nakagawa K, Yoshimi K, Ariya C, Nakane A, et al. Tohara H. Age-related changes in swallowing muscle intramuscular adipose tissue deposition and related factors. Exp Gerontol. 2021;153:111505. https://doi.org/10.1016/j.exger.2021.111505.

  24. Yoshimi K, Hara K, Tohara H, Nakane A, Nakagawa K, Yamaguchi K, et al. Relationship between swallowing muscles and trunk muscle mass in healthy elderly individuals: a cross-sectional study. Arch Gerontol Geriatr. 2018;79:21–6. https://doi.org/10.1016/j.archger.2018.07.018.

    Article  PubMed  Google Scholar 

  25. Low S, Ng TP, Lim CL, Moh A, Ang SF, Wang J, et al. Association between lower extremity skeletal muscle mass and impaired cognitive function in type 2 diabetes. Sci Rep. 2020;10:2956. https://doi.org/10.1038/s41598-020-59914-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Hara K, Tohara H, Wada S, Iida T, Ueda K, Ansai T. Jaw-opening force test to screen for Dysphagia: preliminary results. Arch Phys Med Rehabil. 2014;95:867–74. https://doi.org/10.1016/j.apmr.2013.09.005.

    Article  PubMed  Google Scholar 

  27. Sarukawa S, Noguchi T, Miyazaki K, Itoh H, Nishino H, Kusama M. Development of a tool for speech intelligibility evaluation after glossectomy: the TKR speech test. Jpn J Head Neck Cancer. 2013;39:374–8.

    Google Scholar 

  28. Utanohara Y, Hayashi R, Yoshikawa M, Yoshida M, Tsuga K, Akagawa Y. Standard values of maximum tongue pressure taken using newly developed disposable tongue pressure measurement device. Dysphagia. 2008;23:286–90. https://doi.org/10.1007/s00455-007-9142-z.

    Article  PubMed  Google Scholar 

  29. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull. 1979;86:420–8. https://doi.org/10.1037//0033-2909.86.2.420.

    Article  CAS  PubMed  Google Scholar 

  30. Nakamori M, Imamura E, Fukuta M, Tachiyama K, Kamimura T, Hayashi Y, et al. Tongue thickness measured by ultrasonography is associated with tongue pressure in the Japanese elderly. PLoS ONE. 2020;15: e0230224. https://doi.org/10.1371/journal.pone.0230224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kajisa E, Tohara H, Nakane A, Wakasugi Y, Hara K, Yamaguchi K, et al. The relationship between jaw-opening force and the cross-sectional area of the suprahyoid muscles in healthy elderly. J Oral Rehabil. 2018;45:222–7. https://doi.org/10.1111/joor.12596.

    Article  CAS  PubMed  Google Scholar 

  32. Baril AA, Carrier J, Lafrenière A, Warby S, Poirier J, Osorio RS, Canadian Sleep and Circadian Network, et al. Biomarkers of dementia in obstructive sleep apnea. Sleep Med Rev. 2018;42:139–48. https://doi.org/10.1016/j.smrv.2018.08.001.

    Article  Google Scholar 

  33. Cadore EL, Izquierdo M, Conceição M, Radaelli R, Pinto RS, Baroni BM, et al. Echo intensity is associated with skeletal muscle power and cardiovascular performance in elderly men. Exp Gerontol. 2012;47:473–8. https://doi.org/10.1016/j.exger.2012.04.002.

    Article  PubMed  Google Scholar 

  34. Sanders I, Mu L. A three-dimensional atlas of human tongue muscles. Anat Rec (Hoboken). 2013;296:1102–14. https://doi.org/10.1002/ar.22711.

    Article  Google Scholar 

  35. Mizuno T, Matsui Y, Tomida M, Suzuki Y, Nishita Y, Tange C, et al. Differences in the mass and quality of the quadriceps with age and sex and their relationships with knee extension strength. J Cachexia Sarcopenia Muscle. 2021;12:900–12. https://doi.org/10.1002/jcsm.12715.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Lopez P, Pinto MD, Pinto RS. Does rest time before ultrasonography imaging affect quadriceps femoris muscle thickness, cross-sectional area and echo intensity measurements? Ultrasound Med Biol. 2019;45:612–6. https://doi.org/10.1016/j.ultrasmedbio.2018.10.010.

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank Editage for editing and proofreading this manuscript for English language and all staff members and participants of the study.

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The authors did not receive support from any organization for the submitted work.

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Authors

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KY involved in conceptualization, methodology, formal analysis, writing-original draft, review, and editing. KN participated in validation, data curation, writing-review, and editing. KY and CA took part in investigation, data curation, and resources. AN and TO did formal analysis and resources. HT contributed in supervision, project administration, writing-review, and editing.

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Correspondence to Kohei Yamaguchi.

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The authors have no relevant financial or non-financial interests to disclose.

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This study was approved by the Tokyo Medical and Dental University Ethics Committee (Ref: D2014-047).

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Yamaguchi, K., Nakagawa, K., Yoshimi, K. et al. The Cross-Sectional Area of the Middle and Base of the Tongue is Associated with Swallowing-Related Muscle Strength. Dysphagia 37, 1723–1731 (2022). https://doi.org/10.1007/s00455-022-10431-7

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