Cited by 421Dysphagia Assessment and ManagementNutrition and Health in AgingMuscle Physiology and Disorders

Sarcopenia and dysphagia: Position paper by four professional organizations

Open access
Fujishima, Ichiro, Fujiu‐Kurachi, Masako, Arai, Hidenori, Hyodo, Masamitsu, Kagaya, Hitoshi, Maeda, Keisuke, Mori, Takashi, Nishioka, Shinta +7 more·2019·Geriatrics & Gerontology International

Abstract

This report was written by the Japanese Society of Dysphagia Rehabilitation, the Japanese Association of Rehabilitation Nutrition, the Japanese Association on Sarcopenia and Frailty, and the Society of Swallowing and Dysphagia of Japan to consolidate the currently available evidence on the topics of sarcopenia and dysphagia. Histologically, the swallowing muscles are of different embryological origin from somatic muscles, and receive constant input stimulation from the respiratory center. Although the swallowing muscles are striated, their characteristics are different from those of skeletal muscles. The swallowing muscles are inevitably affected by malnutrition and disuse; accumulating evidence is available regarding the influence of malnutrition on the swallowing muscles. Sarcopenic dysphagia is defined as dysphagia caused by sarcopenia of the whole body and swallowing‐related muscles. When sarcopenia does not exist in the entire body, the term “sarcopenic dysphagia” should not be used. Additionally, sarcopenia due to neuromuscular diseases should be excluded; however, aging and secondary sarcopenia after inactivity, malnutrition and disease (wasting disorder and cachexia) are included in sarcopenic dysphagia. The treatment of dysphagia due to sarcopenia requires both dysphagia rehabilitation, such as resistance training of the swallowing muscles and nutritional intervention. However, the fundamental issue of how dysphagia caused by sarcopenia of the swallowing muscles should be diagnosed remains unresolved. Furthermore, whether dysphagia can be caused by primary sarcopenia should be clarified. Additionally, more discussion is required on issues such as the relationship between dysphagia and secondary sarcopenia, as well as the diagnostic criteria and means for diagnosing dysphagia caused by sarcopenia. Geriatr Gerontol Int 2019; 19: 91–97.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1111/ggi.13591

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Oral dysphagia becomes prevalent in high ages according to several age-related changes in the oral cavity, pharynx, and esophagus.

    “Oral dysphagia becomes prevalent in high ages according to several age-”

    From ESPEN guideline on hospital nutrition (2021) · cites this paper as [183]

    The “Mechanisms and risk factors of dysphagia caused by sarcopenia” section describes age-related atrophy of the tongue and geniohyoid muscle, thinning of the pharyngeal wall, and associations between reduced swallowing-muscle strength and dysphagia. It does not establish that oral dysphagia becomes prevalent with age or attribute it to age-related changes in the esophagus. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 76

  1. Rosenberg IH. Summary comments: Epidemiologic and methodologic problems in determining nutritional status of older persons. Am J Clin Nutr 1989; 50: 1231-1233.
  2. Cruz-Jentoft AJ, Baeyens JP, Bauer JM et al. Sarcopenia: European con- sensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing 2010; 39: 412-423.
  3. Chen LK, Liu LK, Woo J et al. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc 2014; 15: 95-101.
  4. Anker SD, Morley JE, von Haehling S. Welcome to the ICD-10 code for sarcopenia. J Cachexia Sarcopenia Muscle 2016; 7: 512-514.
  5. Akishita M, Kozaki K, Iijima K et al. Chapter 1 Definitions and diagnosis of sarcopenia. Geriatr Gerontol Int 2018; 18 (Suppl 1): 7-12.
  6. Shimokata H, Shimada H, Satake S et al. Chapter 2 Epidemiology of sarcopenia. Geriatr Gerontol Int 2018; 18 (Suppl 1): 13-22.
  7. Kuzuya M, Sugimoto K, Suzuki T et al. Chapter 3 prevention of sarco- penia. Geriatr Gerontol Int 2018; 18 (Suppl 1): 23-27.
  8. Arai H, Wakabayashi H, Yoshimura Y, Yamada M, Kim H, Harada A. Chapter 4 treatment of sarcopenia. Geriatr Gerontol Int 2018; 18 (Suppl 1): 28-44.
  9. Veldee MS, Peth LD. Can protein-calorie malnutrition cause dyspha- gia? Dysphagia 1992; 7: 86-101.
  10. Hudson HM, Daubert CR, Mills RH. The interdependency of protein- energy malnutrition, aging, and dysphagia. Dysphagia 2000; 15: 31-38.
  11. Robbins J, Gangnon RE, Theis SM, Kays SA, Hewitt AL, Hind JA. The effects of lingual exercise on swallowing in older adults. J Am Geriatr Soc 2005; 53: 1483-1489.
  12. Kuroda Y, Kuroda R. Relationship between thinness and swallowing function in Japanese older adults: implications for sarcopenic dysphagia. J Am Geriatr Soc 2012; 60: 1785-1786.
  13. Rogers MA, Evans WJ. Changes in skeletal muscle with aging: effects of exercise training. Exerc Sport Sci Rev 1993; 21: 65-102.
  14. Roubenoff R, Hughes VA. Sarcopenia: current concepts. J Gerontol A Biol Sci Med Sci 2000; 55: M716-M724.
  15. Carmeli E, Coleman R, Reznick AZ. The biochemistry of aging muscle. Exp Gerontol 2002; 37: 477-489.
  16. Kannus P, Jozsa L, Jarvinen TL et al. Free mobilization and low-to high-intensity exercise in immobilization-induced muscle atrophy. J Appl Physiol (1985) 1998; 84: 1418-1424.
  17. Appell HJ. Morphology of immobilized skeletal muscle and the effects of a pre-and postimmobilization training program. Int J Sports Med 1986; 7: 6-12.
  18. Seki K, Taniguchi Y, Narusawa M. Alterations in contractile properties of human skeletal muscle induced by joint immobilization. J Physiol 2001; 530: 521-532.
  19. Seki K, Taniguchi Y, Narusawa M. Effects of joint immobilization on firing rate modulation of human motor units. J Physiol 2001; 530: 507-519.
  20. Lexell J. Evidence for nervous system degeneration with advancing age. J Nutr 1997; 127: 1011s-1013s.
  21. Poggi P, Marchetti C, Scelsi R. Automatic morphometric analysis of skeletal muscle fibers in the aging man. Anat Rec 1987; 217: 30-34.
  22. Gundersen K. Determination of muscle contractile properties: the importance of the nerve. Acta Physiol Scand 1998; 162: 333-341.
  23. Brooks SV, Faulkner JA. Skeletal muscle weakness in old age: underly- ing mechanisms. Med Sci Sports Exerc 1994; 26: 432-439.
  24. Krishnan VS, White Z, McMahon CD et al. A neurogenic perspective of sarcopenia: Time course study of sciatic nerves from aging mice. J Neuropathol Exp Neurol 2016; 75: 464-478.
  25. Grelot L, Barillot JC, Bianchi AL. Pharyngeal motoneurones: respiratory-related activity and responses to laryngeal afferents in the decerebrate cat. Exp Brain Res 1989; 78: 336-344.
  26. Sokoloff AJ, Douglas M, Rahnert JA et al. Absence of morphological and molecular correlates of sarcopenia in the macaque tongue muscle styloglossus. Exp Gerontol. 2016; 84: 40-48.
  27. Umezaki T, Nakazawa K, Miller AD. Behaviors of hypoglossal hyoid motoneurons in laryngeal and vestibular reflexes and in deglutition and emesis. Am J Physiol 1998; 274: R950-R955.
  28. Feng X, Todd T, Lintzenich CR et al. Aging-related geniohyoid muscle atrophy is related to aspiration status in healthy older adults. J Gerontol A Biol Sci Med Sci 2013; 68: 853-860.
  29. Rhee S, Yamamoto M, Kitamura K et al. Macrophage density in pharyn- geal and laryngeal muscles greatly exceeds that in other striated mus- cles: an immunohistochemical study using elderly human cadavers. Anat Cell Biol 2016; 49: 177-183.
  30. Shaker R, Kern M, Bardan E et al. Augmentation of deglutitive upper esophageal sphincter opening in the elderly by exercise. Am J Physiol 1997; 272: G1518-G1522.
  31. Antunes EB, Lunet N. Effects of the head lift exercise on the swallow function: a systematic review. Gerodontology 2012; 29: 247-257.
  32. Komatsu R, Okazaki T, Ebihara S et al. Aspiration pneumonia induces muscle atrophy in the respiratory, skeletal, and swallowing systems. J Cachexia Sarcopenia Muscle 2018; 9: 643-653.
  33. Wakabayashi H. Presbyphagia and Sarcopenic Dysphagia: Association between Aging, Sarcopenia, and Deglutition Disorders. J Frailty Aging 2014; 3: 97-103.
  34. Mori T, Fujishima I, Wakabayashi H et al. Development and reliability of a diagnostic algorithm for sarcopenic dysphagia. JCSM Clinical Reports 2017; 2: e00017.
  35. Maeda K, Takaki M, Akagi J. Decreased skeletal muscle mass and risk factors of sarcopenic dysphagia: A prospective observational cohort study. J Gerontol A Biol Sci Med Sci 2017; 72: 1290-1294.
  36. Tamura F, Kikutani T, Tohara T, Yoshida M, Yaegaki K. Tongue thickness relates to nutritional status in the elderly. Dysphagia 2012; 27: 556-561.
  37. Molfenter SM, Amin MR, Branski RC et al. Age-related changes in pha- ryngeal lumen size: A retrospective MRI analysis. Dysphagia 2015; 30: 321-327.
  38. Shimizu S, Hanayama K, Nakato R, Sugiyama T, Tsubahara A. Ultraso- nographic evaluation of geniohyoid muscle mass in perioperative patients. Kawasaki Med J 2016; 42: 47-56.
  39. Sporns PB, Muhle P, Hanning U et al. Atrophy of swallowing muscles is associated with severity of dysphagia and age in patients with acute stroke. J Am Med Dir Assoc 2017; 18: 635.e631-635.e637.
  40. Baba T, Goto T, Fujimoto K et al. Age-related Changes in Geniohyoid Muscle Morphology Predict Reduced Swallowing Function. J Oral Health Biosci 2017; 30: 18-25.
  41. Kajisa E, Tohara H, Nakane A 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: 222-227.
  42. Robbins J, Humpal NS, Banaszynski K, Hind J, Rogus-Pulia N. Age- related differences in pressures generated during isometric presses and swallows by healthy adults. Dysphagia 2016; 31: 90-96.
  43. Yoshida M, Kikutani T, Tsuga K, Utanohara Y, Hayashi R, Akagawa Y. Decreased tongue pressure reflects symptom of dysphagia. Dysphagia 2006; 21: 61-65.
  44. Konaka K, Kondo J, Hirota N et al. Relationship between tongue pressure and dysphagia in stroke patients. Eur Neurol 2010; 64: 101-107.
  45. Hirota N, Konaka K, Ono T et al. Reduced tongue pressure against the hard palate on the paralyzed side during swallowing predicts Dysphagia in patients with acute stroke. Stroke 2010; 41: 2982-2984.
  46. Lee JH, Kim HS, Yun DH et al. The relationship between tongue pres- sure and oral dysphagia in stroke patients. Ann Rehabil Med 2016; 40: 620-628.
  47. Maeda K, Akagi J. Decreased tongue pressure is associated with sarco- penia and sarcopenic dysphagia in the elderly. Dysphagia 2015; 30: 80-87.
  48. Buehring B, Hind J, Fidler E, Krueger D, Binkley N, Robbins J. Tongue strength is associated with jumping mechanography performance and handgrip strength but not with classic functional tests in older adults. J Am Geriatr Soc 2013; 61: 418-422.
  49. Sakai K, Nakayama E, Tohara H et al. Tongue strength is associated with grip strength and nutritional status in older adult inpatients of a rehabilitation hospital. Dysphagia 2017; 32: 241-249.
  50. Machida N, Tohara H, Hara K et al. Effects of aging and sarcopenia on tongue pressure and jaw-opening force. Geriatr Gerontol Int 2017; 17: 295-301.
  51. Wakabayashi H, Matsushima M, Uwano R, Watanabe N, Oritsu H, Shimizu Y. Skeletal muscle mass is associated with severe dysphagia in cancer patients. J Cachexia Sarcopenia Muscle 2015; 6: 351-357.
  52. Saitoh M, Ishida J, Konishi M, Springer J. The concept that focuses on oral motor and feeding function in cancer patients with muscle wasting: Skeletal muscle mass is associated with severe dysphagia in cancer patients. J Cachexia Sarcopenia Muscle 2016; 7: 233-234.
  53. Wakabayashi H, Takahashi R, Watanabe N, Oritsu H, Shimizu Y. Prev- alence of skeletal muscle mass loss and its association with swallowing function after cardiovascular surgery. Nutrition 2017; 38: 70-73.
  54. Takagi D, Hirano H, Watanabe Y et al. Relationship between skeletal muscle mass and swallowing function in patients with Alzheimer's dis- ease. Geriatr Gerontol Int 2017; 17: 402-409.
  55. Shiozu H, Higashijima M, Koga T. Association of sarcopenia with swal- lowing problems, related to nutrition and activities of daily living of elderly individuals. J Phys Ther Sci 2015; 27: 393-396.
  56. Murakami M, Hirano H, Watanabe Y, Sakai K, Kim H, Katakura A. Relationship between chewing ability and sarcopenia in Japanese community-dwelling older adults. Geriatr Gerontol Int 2015; 15: 1007-1012.
  57. Sagawa K, Kikutani T, Tamura F, Yoshida M. Factors related to skeletal muscle mass in the frail elderly. Odontology 2017; 105: 91-95.
  58. Maeda K, Akagi J. Sarcopenia is an independent risk factor of dysphagia in hospitalized older people. Geriatr Gerontol Int 2016; 16: 515-521.
  59. Shimizu A, Maeda K, Tanaka K, Ogawa M, Kayashita J. Texture- modified diets are associated with decreased muscle mass in older adults admitted to a rehabilitation ward. Geriatr Gerontol Int 2018; 18: 698-704.
  60. Yoshimura Y, Wakabayashi H, Bise T, Tanoue M. Prevalence of sarco- penia and its association with activities of daily living and dysphagia in convalescent rehabilitation ward inpatients. Clin Nutr 2018; 37: 2022-2028.
  61. Wakabayashi H, Takahashi R, Watanabe N, Oritsu H, Shimizu Y. Prev- alence of sarcopenia and its association with dysphagia in cancer patients who require rehabilitation. J Rehabil Med 2017; 49: 682-685.
  62. Zhao W-T, Yang M, Wu H-M, Yang L, Zhang X-m, Huang Y. Sys- tematic review and meta-analysis of the association between sarcopenia and dysphagia. J Nutr Health Aging 2018; 22: 1003-1009.
  63. Wakabayashi H, Sakuma K. Rehabilitation nutrition for sarcopenia with disability: a combination of both rehabilitation and nutrition care man- agement. J Cachexia Sarcopenia Muscle 2014; 5: 269-277.
  64. Maeda K, Koga T, Nasu T, Takaki M, Akagi J. Predictive accuracy of calf circumference measurements to detect decreased skeletal muscle mass and European society for clinical nutrition and metabolism- defined malnutrition in hospitalized older patients. Ann Nutr Metab 2017; 71: 10-15.
  65. Nishioka S, Okamoto T, Takayama M et al. Malnutrition risk predicts recovery of full oral intake among older adult stroke patients undergo- ing enteral nutrition: Secondary analysis of a multicentre survey (the APPLE study). Clin Nutr 2017; 36: 1089-1096.
  66. Sakai K, Nakayama E, Tohara H et al. Diagnostic accuracy of lip force and tongue strength for sarcopenic dysphagia in older inpatients: A cross-sectional observational study. Clin Nutr 2018. https://doi.org/10. 1016/j.clnu.2018.01.016. · DOI
  67. Shimizu S, Hanayama K, Metani H et al. Retest reliability of ultrasonic gen- iohyoid muscle measurement. Jap J Comprehens Rehabilit Sci 2016; 7: 55-60.
  68. Ogawa N, Mori T, Fujishima I et al. Ultrasonography to measure swal- lowing muscle mass and quality in older patients with sarcopenic dys- phagia. J Am Med Dir Assoc 2018; 19: 516-522.
  69. Maeda K, Akagi J. Treatment of sarcopenic dysphagia with rehabilita- tion and nutritional support: A comprehensive approach. J Acad Nutr Diet 2016; 116: 573-577.
  70. Wakabayashi H, Uwano R. Rehabilitation nutrition for possible sarco- penic dysphagia after lung cancer surgery: A case report. Am J Phys Med Rehabil 2016; 95: e84-e89.
  71. Hashida N, Shamoto H, Maeda K, Wakabayashi H, Suzuki M, Fujii T. Rehabilitation and nutritional support for sarcopenic dysphagia and tongue atrophy after glossectomy: A case report. Nutrition 2017; 35: 128-131.
  72. Wakabayashi H, Matsushima M, Momosaki R et al. The effects of resis- tance training of swallowing muscles on dysphagia in older people: a cluster, randomized, controlled trial. Nutrition 2018; 48: 111-116.
  73. Koyama T, Maeda K, Anzai H, Koganei Y, Shamoto H, Wakabayashi H. Early commencement of oral intake and physical function are associated with early hospital discharge with oral intake in hospitalized elderly indi- viduals with pneumonia. J Am Geriatr Soc 2015; 63: 2183-2185.
  74. Momosaki R, Yasunaga H, Matsui H, Horiguchi H, Fushimi K, Abo M. Effect of early rehabilitation by physical therapists on in-hospital mor- tality after aspiration pneumonia in the elderly. Arch Phys Med Rehabil 2015; 96: 205-209.
  75. Maeda K, Koga T, Akagi J. Tentative nil per os leads to poor outcomes in older adults with aspiration pneumonia. Clin Nutr 2016; 35: 1147-1152.
  76. Wakabayashi H. Rehabilitation nutrition in general and family medi- cine. J Gen Fam Med 2017; 18: 153-154.

Cited by

Sorted by citations

Authors
Fujishima, I., Fujiu‐Kurachi, M., Arai, H., Hyodo, M., Kagaya, H., Maeda, K., Mori, T., Nishioka, S., Oshima, F., Ogawa, S., Ueda, K., Umezaki, T., Wakabayashi, H., Yamawaki, M., & Yoshimura, Y.
Affiliations
  • Seirei Hamamatsu City Rehabilitation Hospital (JP)
  • International University of Health and Welfare (JP)
  • National Center for Geriatrics and Gerontology (JP)
  • Kochi Medical School Hospital (JP)
  • Fujita Health University (JP)
  • Aichi Medical University (JP)
  • Southern Tohoku General Hospital (JP)
  • Nagasaki Rehabilitation (JP)
  • Suwa Red Cross Hospital (JP)
  • The University of Tokyo (JP)
  • Nihon University (JP)
  • Fukuoka Sanno Hospital (JP)
  • Yokohama City University Medical Center (JP)
  • Kyoto Prefectural University of Medicine (JP)
  • Kumamoto Rehabilitation Hospital (JP)
Corresponding author
Arai, Hidenori
Venue
Geriatrics & Gerontology International
Publisher
Wiley
Published
2019-01-09
Volume
19
Issue
2
Pages
91-97
ISSN
  • 1444-1586 (ISSN-L)
  • 1447-0594
OpenAlex
W2909695165
Cited by
421
References
0
Citations by year
2026: 52 · 2025: 56 · 2024: 67 · 2023: 48 · 2022: 57 · 2021: 62 · 2020: 54 · 2019: 25
FWCI
83.65
Type
journal article
Language
en
Open access
Locations
  • Geriatrics and gerontology international/Geriatrics & gerontology international (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Funders
Japan Society for the Promotion of Science (17H02137)
Topics
  • Health Sciences › Health Professions › Speech and Hearing › Dysphagia Assessment and Management
  • Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Keywords
sarcopenia, dysphagia, sarcopenic dysphagia, swallowing muscles, malnutrition, disuse, aging, cachexia, swallowing rehabilitation, resistance training, dietary intervention, diagnostic criteria, secondary sarcopenia
MeSH terms
Deglutition Disorders, Humans, Sarcopenia

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review