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Associations of swallowing-related muscle quantity and quality with sarcopenic parameters

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Key summary points

AbstractSection Aim

To elucidate the relationship between swallowing-related muscle characteristics and sarcopenic parameters in community-dwelling older adults.

AbstractSection Findings

The cross-sectional area of the geniohyoid muscle was significantly associated with the grip strength, and tongue characteristics were significantly associated with the skeletal muscle mass index. Sarcopenic parameters were associated with swallowing-related muscle characteristics.

AbstractSection Message

This research may increase our understanding of the pathophysiology of sarcopenic dysphagia and muscle physiology.

Abstract

Purpose

To examine the associations between swallowing-related muscle characteristics and sarcopenic parameters.

Methods

We included 147 community-dwelling older adults (age: 71.6 ± 4.7 years, body mass index: 23.0 ± 2.7 kg/m2 (mean ± standard deviation), men: 50; women: 97) and categorized them into robust (n = 125), low-function (n = 17), and sarcopenia (n = 5) groups based on the diagnostic criteria of the Asia Working Group for Sarcopenia 2019. We evaluated the geniohyoid muscle (GHM) and tongue characteristics (muscle quantity and quality). The cross-sectional area (CSA) indicated the muscle quantity, and echo intensity (EI) values indicated the muscle quality. A multiple regression analysis was performed to clarify the relationship of swallowing-related muscle characteristics and strength with sarcopenic parameters.

Results

The grip strength (CSA of GHM: β = 1.64, p = 0.03) and skeletal muscle mass index (CSA of tongue: β = 74.81, p = 0.003, EI of tongue: β = 1.92, p = 0.009) were better indicators of swallowing-related muscle characteristics.

Conclusion

These findings may facilitate the early detection of aging-related deterioration in swallowing-related musculature through the diagnostic process of sarcopenia and increase our understanding of muscle physiology.

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Data availability

All data generated or analyzed during this study are included in this article. Further inquiries can be directed to the corresponding author.

References

  1. Lynch NA, Metter EJ, Lindle RS, Fozard JL, Tobin JD, Roy TA et al (1999) Muscle quality. I. Age-associated differences between arm and leg muscle groups. J Appl Physiol (1985) 86:188–94. https://doi.org/10.1152/jappl.1999.86.1.188

    Article  CAS  Google Scholar 

  2. Utanohara Y, Hayashi R, Yoshikawa M, Yoshida M, Tsuga K, Akagawa Y (2008) Standard values of maximum tongue pressure taken using newly developed disposable tongue pressure measurement device. Dysphagia 23:286–290. https://doi.org/10.1007/s00455-007-9142-z

    Article  Google Scholar 

  3. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T et al (2019) Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 48:16–31. https://doi.org/10.1093/ageing/afy169. (Erratum in 10.1093/ageing/afz046)

    Article  Google Scholar 

  4. Fırat Ozer F, Akın S, Soysal T, Gokcekuyu BM, Erturk ZG (2021) Relationship between dysphagia and sarcopenia with comprehensive geriatric evaluation. Dysphagia 36:140–146. https://doi.org/10.1007/s00455-020-10120-3

    Article  Google Scholar 

  5. Maeda K, Ishida Y, Nonogaki T, Shimizu A, Yamanaka Y, Matsuyama R et al (2019) Development and predictors of sarcopenic dysphagia during hospitalization of older adults. Nutrients 12:70. https://doi.org/10.3390/nu12010070

    Article  Google Scholar 

  6. Maeda K, Akagi J (2016) Sarcopenia is an independent risk factor of dysphagia in hospitalized older people. Geriatr Gerontol Int 16:515–521. https://doi.org/10.1111/ggi.12486

    Article  Google Scholar 

  7. Maeda K, Takaki M, Akagi J (2017) Decreased skeletal muscle mass and risk factors of sarcopenic dysphagia: a prospective observational cohort study. J Gerontol A Biol Sci Med Sci 72:1290–1294. https://doi.org/10.1093/gerona/glw190

    Article  Google Scholar 

  8. Fujishima I, Fujiu-Kurachi M, Arai H, Hyodo M, Kagaya H, Maeda K et al (2019) Sarcopenia and dysphagia: position paper by four professional organizations. Geriatr Gerontol Int 19:91–97. https://doi.org/10.1111/ggi.13591

    Article  Google Scholar 

  9. Yamaguchi K, Hara K, Nakagawa K, Yoshimi K, Ariya C, Nakane A et al (2021) Ultrasonography shows age-related changes and related factors in the tongue and suprahyoid muscles. J Am Med Dir Assoc 22:766–772. https://doi.org/10.1016/j.jamda.2020.10.012

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  11. Feng X, Todd T, Lintzenich CR, Ding J, Carr JJ, Ge Y et al (2013) Aging-related geniohyoid muscle atrophy is related to aspiration status in healthy older adults. J Gerontol A Biol Sci Med Sci 68:853–860. https://doi.org/10.1093/gerona/gls225

    Article  Google Scholar 

  12. Ogawa N, Mori T, Fujishima I, Wakabayashi H, Itoda M, Kunieda K et al (2018) Ultrasonography to measure swallowing muscle mass and quality in older patients with sarcopenic dysphagia. J Am Med Dir Assoc 19:516–522. https://doi.org/10.1016/j.jamda.2017.11.007

    Article  Google Scholar 

  13. Komatsu R, Okazaki T, Ebihara S, Kobayashi M, Tsukita Y, Nihei M et al (2018) Aspiration pneumonia induces muscle atrophy in the respiratory, skeletal, and swallowing systems. J Cachexia Sarcopenia Muscle 9:643–653. https://doi.org/10.1002/jcsm.12297

    Article  Google Scholar 

  14. Yamaguchi K, Tohara H, Hara K, Nakane A, Kajisa E, Yoshimi K et al (2018) Relationship of aging, skeletal muscle mass, and tooth loss with masseter muscle thickness. BMC Geriatr 18:67. https://doi.org/10.1186/s12877-018-0753-z

    Article  Google Scholar 

  15. Suzuki M, Koyama S, Kimura Y, Ishiyama D, Otobe Y, Nishio N et al (2018) Relationship between characteristics of skeletal muscle and oral function in community-dwelling older women. Arch Gerontol Geriatr 79:171–175. https://doi.org/10.1016/j.archger.2018.09.003

    Article  Google Scholar 

  16. Yoshimi K, Nakagawa K, Hara K, Yamaguchi K, Nakane A, Kubota K et al (2020) Relationship between tongue pressure and back muscle strength in healthy elderly individuals. Aging Clin Exp Res 32:2549–2555. https://doi.org/10.1007/s40520-020-01484-5

    Article  Google Scholar 

  17. Chen LK, Woo J, Assantachai P, Auyeung TW, Chou MY, Iijima K et al (2020) Asian working group for sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J Am Med Dir Assoc 21:300-307.e2. https://doi.org/10.1016/j.jamda.2019.12.012

    Article  Google Scholar 

  18. Young HJ, Jenkins NT, Zhao Q, Mccully KK (2015) Measurement of intramuscular fat by muscle echo intensity. Muscle Nerve 52:963–971. https://doi.org/10.1002/mus.24656

    Article  Google Scholar 

  19. Kajisa E, Tohara H, Nakane A, Wakasugi Y, Hara K, Yamaguchi K et al (2018) The relationship between jaw-opening force and the cross-sectional area of the suprahyoid muscles in healthy elderly. J Oral Rehabil 45:222–227. https://doi.org/10.1111/joor.12596

    Article  CAS  Google Scholar 

  20. Wakasugi Y, Tohara H, Machida N, Nakane A, Minakuchi S (2017) Can grip strength and/or walking speed be simple indicators of the deterioration in tongue pressure and jaw opening force in older individuals? Gerodontology 34:455–459. https://doi.org/10.1111/ger.12292

    Article  Google Scholar 

  21. Feng X, Cartwright MS, Walker FO, Bargoil JH, Hu Y, Butler SG (2015) Ultrasonographic evaluation of geniohyoid muscle and hyoid bone during swallowing in young adults. Laryngoscope 125:1886–1891. https://doi.org/10.1002/lary.25224

    Article  Google Scholar 

  22. Korfage JA, Schueler YT, Brugman P, Van Eijden TM (2001) Differences in myosin heavy-chain composition between human jaw-closing muscles and supra- and infrahyoid muscles. Arch Oral Biol 46:821–827. https://doi.org/10.1016/s0003-9969(01)00042-5

    Article  CAS  Google Scholar 

  23. Klein CS, Marsh GD, Petrella RJ, Rice CL (2003) Muscle fiber number in the biceps brachii muscle of young and old men. Muscle Nerve 28:62–68. https://doi.org/10.1002/mus.10386

    Article  Google Scholar 

  24. Lexell J, Taylor CC, Sjöström M (1988) What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84:275–294. https://doi.org/10.1016/0022-510x(88)90132-3

    Article  CAS  Google Scholar 

  25. Sanders I, Mu L, Amirali A, Su H, Sobotka S (2013) The human tongue slows down to speak: muscle fibers of the human tongue. Anat Rec (Hoboken) 296:1615–1627. https://doi.org/10.1002/ar.22755

    Article  Google Scholar 

  26. Ciciliot S, Rossi AC, Dyar KA, Blaauw B, Schiaffino S (2013) Muscle type and fiber type specificity in muscle wasting. Int J Biochem Cell Biol 45:2191–2199. https://doi.org/10.1016/j.biocel.2013.05.016

    Article  CAS  Google Scholar 

  27. VanRavenhorst-Bell HA, Mefferd AS, Coufal KL, Scudder R, Patterson J (2017) Tongue strength and endurance: comparison in active and non-active young and older adults. Int J Speech Lang Pathol 19:77–86. https://doi.org/10.3109/17549507.2016.1154983

    Article  Google Scholar 

  28. Takae R, Hatamoto Y, Yasukata J, Kose Y, Komiyama T, Ikenaga M et al (2019) Physical activity and/or high protein intake maintains fat-free mass in older people with mild disability; the Fukuoka Island City study: a cross-sectional study. Nutrients 11:2595. https://doi.org/10.3390/nu11112595

    Article  CAS  Google Scholar 

  29. Nagayoshi M, Higashi M, Takamura N, Tamai M, Koyamatsu J, Yamanashi H et al (2017) Social networks, leisure activities and maximum tongue pressure: cross-sectional associations in the Nagasaki Islands Study. BMJ Open 7:e014878. https://doi.org/10.1136/bmjopen-2016-014878

    Article  Google Scholar 

  30. Nakao Y, Yamashita T, Honda K, Katsuura T, Hama Y, Nakamura Y et al (2021) Association among age-related tongue muscle abnormality, tongue pressure, and presbyphagia: a 3D MRI study. Dysphagia 36:483–491. https://doi.org/10.1007/s00455-020-10165-4

    Article  Google Scholar 

  31. Arakawa-Kaneko I, Watarai Y, Schimmel M, Abou-Ayash S (2022) Relationship between tongue pressure and handgrip strength: a systematic review and meta-analysis. J Oral Rehabil 49:1087–1105. https://doi.org/10.1111/joor.13362

    Article  Google Scholar 

  32. Wiedmer P, Jung T, Castro JP, Pomatto LCD, Sun PY, Davies KJA et al (2021) Sarcopenia—molecular mechanisms and open questions. Ageing Res Rev 65:101200. https://doi.org/10.1016/j.arr.2020.101200

    Article  CAS  Google Scholar 

  33. Pillen S, Tak RO, Zwarts MJ, Lammens MM, Verrijp KN, Arts IM et al (2009) Skeletal muscle ultrasound: correlation between fibrous tissue and echo intensity. Ultrasound Med Biol 35:443–446. https://doi.org/10.1016/j.ultrasmedbio.2008.09.016

    Article  Google Scholar 

  34. Cadore EL, Izquierdo M, Conceição M, Radaelli R, Pinto RS, Baroni BM et al (2012) Echo intensity is associated with skeletal muscle power and cardiovascular performance in elderly men. Exp Gerontol 47:473–478. https://doi.org/10.1016/j.exger.2012.04.002

    Article  Google Scholar 

  35. Akazawa N, Kishi M, Hino T, Tsuji R, Tamura K, Hioka A et al (2022) Relationship between muscle mass and fraction of intramuscular adipose tissue of the quadriceps in older inpatients. PLoS One 17:e0263973. https://doi.org/10.1371/journal.pone.0263973

    Article  CAS  Google Scholar 

  36. Uezumi A, Fukada S, Yamamoto N, Takeda S, Tsuchida K (2010) Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol 12:143–152. https://doi.org/10.1038/ncb2014

    Article  CAS  Google Scholar 

  37. Joe AWB, Yi L, Natarajan A, Le Grand F, So L, Wang J et al (2010) Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol 12:153–163. https://doi.org/10.1038/ncb2015

    Article  CAS  Google Scholar 

  38. Papadopoulou SK, Tsintavis P, Potsaki P, Papandreou D (2020) Differences in the prevalence of sarcopenia in community-dwelling, nursing home and hospitalized individuals. A systematic review and meta-analysis. J Nutr Health Aging 24:83–90. https://doi.org/10.1007/s12603-019-1267-x

    Article  CAS  Google Scholar 

  39. Wakabayashi H (2014) Presbyphagia and sarcopenic dysphagia: association between aging, sarcopenia, and deglutition disorders. J Frailty Aging 3:97–103. https://doi.org/10.14283/jfa.2014.8

    Article  CAS  Google Scholar 

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Acknowledgements

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

Funding

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

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Authors and Affiliations

  1. Department of Dysphagia Rehabilitation, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo, 113-8510, Japan

    Kohei Yamaguchi, Kazuharu Nakagawa, Kanako Yoshimi, Ayako Nakane, Miki Ishii, Shohei Hasegawa & Haruka Tohara

  2. Department of Preventive Dentistry, Naresuan University, 99 Moo 9, Phitsanulok-Nakhon Sawan Road, Tha Pho, Mueang Phitsanlok, 65000, Thailand

    Chantaramanee Ariya

Authors
  1. Kohei Yamaguchi
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  2. Kazuharu Nakagawa
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Contributions

Conceptualization, methodology, formal analysis, writing—original draft, review, and editing: KYa. Validation, data curation, writing—review, and editing: KN. Investigation, data curation, and resources: KYo, CA, and MI. Formal analysis, resources: AN, MI, and SH. Supervision, project administration, and writing—review and editing: HT.

Corresponding author

Correspondence to Kohei Yamaguchi.

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The authors declare no competing interests.

Ethical approval

This study was approved by the Ethics Committee of the Tokyo Medical and Dental University (ref: D2014-047) and met the guidelines of the Declaration of Helsinki.

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Yamaguchi, K., Nakagawa, K., Yoshimi, K. et al. Associations of swallowing-related muscle quantity and quality with sarcopenic parameters. Eur Geriatr Med 14, 195–201 (2023). https://doi.org/10.1007/s41999-023-00747-4

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