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Association of Thigh Muscle Mass with Insulin Resistance and Incident Type 2 Diabetes Mellitus in Japanese Americans

  • Han, Seung Jin (Department of Endocrinology and Metabolism, Ajou University School of Medicine) ;
  • Boyko, Edward J. (Seattle Epidemiologic Research and Information Center, VA Puget Sound Health Care System) ;
  • Kim, Soo-Kyung (Department of Internal Medicine, CHA Bundang Medical Center, CHA University School of Medicine) ;
  • Fujimoto, Wilfred Y. (Department of Medicine, University of Washington School of Medicine) ;
  • Kahn, Steven E. (Department of Medicine, University of Washington School of Medicine) ;
  • Leonetti, Donna L. (Department of Anthropology, University of Washington)
  • Received : 2018.01.31
  • Accepted : 2018.05.17
  • Published : 2018.12.30

Abstract

Background: Skeletal muscle plays a major role in glucose metabolism. We investigated the association between thigh muscle mass, insulin resistance, and incident type 2 diabetes mellitus (T2DM) risk. In addition, we examined the role of body mass index (BMI) as a potential effect modifier in this association. Methods: This prospective study included 399 Japanese Americans without diabetes (mean age 51.6 years) who at baseline had an estimation of thigh muscle mass by computed tomography and at baseline and after 10 years of follow-up a 75-g oral glucose tolerance test and determination of homeostasis model assessment of insulin resistance (HOMA-IR). We fit regression models to examine the association between thigh muscle area and incidence of T2DM and change in HOMA-IR, both measured over 10 years. Results: Thigh muscle area was inversely associated with future HOMA-IR after adjustment for age, sex, BMI, HOMA-IR, fasting plasma glucose, total abdominal fat area, and thigh subcutaneous fat area at baseline (P=0.033). The 10-year cumulative incidence of T2DM was 22.1%. A statistically significant interaction between thigh muscle area and BMI was observed, i.e., greater thigh muscle area was associated with lower risk of incident T2DM for subjects at lower levels of BMI, but this association diminished at higher BMI levels. Conclusion: Thigh muscle mass area was inversely associated with future insulin resistance. Greater thigh muscle area predicts a lower risk of incident T2DM for leaner Japanese Americans.

Keywords

Acknowledgement

Supported by : National Institutes of Health, University of Washington

References

  1. Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 2014; 103:137-49. https://doi.org/10.1016/j.diabres.2013.11.002
  2. Janssen I, Heymsfield SB, Wang ZM, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol (1985) 2000;89:81-8. https://doi.org/10.1152/jappl.2000.89.1.81
  3. DeFronzo RA, Tripathy D. Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 2009;32 Suppl 2:S157-63. https://doi.org/10.2337/dc09-S302
  4. Srikanthan P, Karlamangla AS. Relative muscle mass is inversely associated with insulin resistance and prediabetes. Findings from the third National Health and Nutrition Examination Survey. J Clin Endocrinol Metab 2011;96:2898-903. https://doi.org/10.1210/jc.2011-0435
  5. Larsen BA, Allison MA, Laughlin GA, Araneta MR, Barrett-Connor E, Wooten WJ, Saad SD, Wassel CL. The association between abdominal muscle and type II diabetes across weight categories in diverse post-menopausal women. J Clin Endocrinol Metab 2015;100:E105-9. https://doi.org/10.1210/jc.2014-2839
  6. Atlantis E, Martin SA, Haren MT, Taylor AW, Wittert GA; Members of the Florey Adelaide Male Ageing Study. Inverse associations between muscle mass, strength, and the metabolic syndrome. Metabolism 2009;58:1013-22. https://doi.org/10.1016/j.metabol.2009.02.027
  7. Volpato S, Bianchi L, Lauretani F, Lauretani F, Bandinelli S, Guralnik JM, Zuliani G, Ferrucci L. Role of muscle mass and muscle quality in the association between diabetes and gait speed. Diabetes Care 2012;35:1672-9. https://doi.org/10.2337/dc11-2202
  8. Eastwood SV, Tillin T, Wright A, Mayet J, Godsland I, Forouhi NG, Whincup P, Hughes AD, Chaturvedi N. Thigh fat and muscle each contribute to excess cardiometabolic risk in South Asians, independent of visceral adipose tissue. Obesity (Silver Spring) 2014;22:2071-9. https://doi.org/10.1002/oby.20796
  9. Barzilay JI, Cotsonis GA, Walston J, Schwartz AV, Satterfield S, Miljkovic I, Harris TB; Health ABC Study. Insulin resistance is associated with decreased quadriceps muscle strength in nondiabetic adults aged >or=70 years. Diabetes Care 2009;32:736-8. https://doi.org/10.2337/dc08-1781
  10. Li JJ, Wittert GA, Vincent A, Atlantis E, Shi Z, Appleton SL, Hill CL, Jenkins AJ, Januszewski AS, Adams RJ. Muscle grip strength predicts incident type 2 diabetes: population-based cohort study. Metabolism 2016;65:883-92. https://doi.org/10.1016/j.metabol.2016.03.011
  11. Larsen BA, Wassel CL, Kritchevsky SB, Strotmeyer ES, Criqui MH, Kanaya AM, Fried LF, Schwartz AV, Harris TB, Ix JH; Health ABC Study. Association of muscle mass, area, and strength with incident diabetes in older adults: The Health ABC Study. J Clin Endocrinol Metab 2016;101:1847-55. https://doi.org/10.1210/jc.2015-3643
  12. Son JW, Lee SS, Kim SR, Yoo SJ, Cha BY, Son HY, Cho NH. Low muscle mass and risk of type 2 diabetes in middle-aged and older adults: findings from the KoGES. Diabetologia 2017;60:865-72. https://doi.org/10.1007/s00125-016-4196-9
  13. Dehghan M, Merchant AT. Is bioelectrical impedance accurate for use in large epidemiological studies? Nutr J 2008;7:26. https://doi.org/10.1186/1475-2891-7-26
  14. Fujimoto WY, Leonetti DL, Kinyoun JL, Newell-Morris L, Shuman WP, Stolov WC, Wahl PW. Prevalence of diabetes mellitus and impaired glucose tolerance among second-generation Japanese-American men. Diabetes 1987;36:721-9. https://doi.org/10.2337/diab.36.6.721
  15. Koppes LL, Dekker JM, Hendriks HF, Bouter LM, Heine RJ. Moderate alcohol consumption lowers the risk of type 2 diabetes: a meta-analysis of prospective observational studies. Diabetes Care 2005;28:719-25. https://doi.org/10.2337/diacare.28.3.719
  16. Paffenbarger RS Jr, Wing AL, Hyde RT. Physical activity as an index of heart attack risk in college alumni. Am J Epidemiol 1978;108:161-75. https://doi.org/10.1093/oxfordjournals.aje.a112608
  17. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985;28:412-9. https://doi.org/10.1007/BF00280883
  18. Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, Sullivan G, Quon MJ. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab 2000;85:2402-10. https://doi.org/10.1210/jcem.85.7.6661
  19. Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care 1997;20:1183-97. https://doi.org/10.2337/diacare.20.7.1183
  20. Shuman WP, Morris LL, Leonetti DL, Wahl PW, Moceri VM, Moss AA, Fujimoto WY. Abnormal body fat distribution detected by computed tomography in diabetic men. Invest Radiol 1986;21:483-7. https://doi.org/10.1097/00004424-198606000-00007
  21. Han SJ, Kim SK, Fujimoto WY, Kahn SE, Leonetti DL, Boyko EJ. Effects of combination of change in visceral fat and thigh muscle mass on the development of type 2 diabetes. Diabetes Res Clin Pract 2017;134:131-8. https://doi.org/10.1016/j.diabres.2017.10.003
  22. Olsen DB, Sacchetti M, Dela F, Ploug T, Saltin B. Glucose clearance is higher in arm than leg muscle in type 2 diabetes. J Physiol 2005;565(Pt 2):555-62. https://doi.org/10.1113/jphysiol.2004.081356
  23. Sacchetti M, Olsen DB, Saltin B, van Hall G. Heterogeneity in limb fatty acid kinetics in type 2 diabetes. Diabetologia 2005; 48:938-45. https://doi.org/10.1007/s00125-005-1727-1
  24. Borkan GA, Hults DE, Gerzof SG, Robbins AH, Silbert CK. Age changes in body composition revealed by computed tomography. J Gerontol 1983;38:673-7. https://doi.org/10.1093/geronj/38.6.673
  25. Gallagher D, Visser M, De Meersman RE, Sepulveda D, Baumgartner RN, Pierson RN, Harris T, Heymsfield SB. Appendicular skeletal muscle mass: effects of age, gender, and ethnicity. J Appl Physiol (1985) 1997;83:229-39. https://doi.org/10.1152/jappl.1997.83.1.229
  26. Jung KJ, Kimm H, Yun JE, Jee SH. Thigh circumference and diabetes: obesity as a potential effect modifier. J Epidemiol 2013; 23:329-36. https://doi.org/10.2188/jea.JE20120174
  27. Nakagami T, Qiao Q, Carstensen B, Nhr-Hansen C, Hu G, Tuomilehto J, Balkau B, Borch-Johnsen K; DECODE-DECODA Study Group. Age, body mass index and type 2 diabetes-associations modified by ethnicity. Diabetologia 2003;46:1063-70. https://doi.org/10.1007/s00125-003-1158-9
  28. Kim TN, Park MS, Lim KI, Choi HY, Yang SJ, Yoo HJ, Kang HJ, Song W, Choi H, Baik SH, Choi DS, Choi KM. Relationships between sarcopenic obesity and insulin resistance, inflammation, and vitamin D status: the Korean Sarcopenic Obesity Study. Clin Endocrinol (Oxf) 2013;78:525-32. https://doi.org/10.1111/j.1365-2265.2012.04433.x
  29. Kim TN, Choi KM. The implications of sarcopenia and sarcopenic obesity on cardiometabolic disease. J Cell Biochem 2015; 116:1171-8. https://doi.org/10.1002/jcb.25077
  30. Han SJ, Kim HJ, Kim DJ, Lee KW, Cho NH. Incidence and predictors of type 2 diabetes among Koreans: a 12-year follow up of the Korean Genome and Epidemiology Study. Diabetes Res Clin Pract 2017;123:173-80. https://doi.org/10.1016/j.diabres.2016.10.004
  31. Wander PL, Boyko EJ, Leonetti DL, McNeely MJ, Kahn SE, Fujimoto WY. Greater hand-grip strength predicts a lower risk of developing type 2 diabetes over 10 years in leaner Japanese Americans. Diabetes Res Clin Pract 2011;92:261-4. https://doi.org/10.1016/j.diabres.2011.01.007
  32. Hoyer D, Boyko EJ, McNeely MJ, Leonetti DL, Kahn SE, Fujimoto WY. Subcutaneous thigh fat area is unrelated to risk of type 2 diabetes in a prospective study of Japanese Americans. Diabetologia 2011;54:2795-800. https://doi.org/10.1007/s00125-011-2275-5
  33. Wallace TM, Levy JC, Matthews DR. Use and abuse of HOMA modeling. Diabetes Care 2004;27:1487-95. https://doi.org/10.2337/diacare.27.6.1487

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