Diabetes Metab J.  2020 Jun;44(3):446-457. 10.4093/dmj.2019.0110.

Association between the Thigh Muscle and Insulin Resistance According to Body Mass Index in Middle-Aged Korean Adults

• Heo JE
• Shim JS
• Lee H
• Kim HC

• KMID: 2513002
• DOI: http://doi.org/10.4093/dmj.2019.0110

Abstract

We examined the associations between thigh muscle area (TMA) and insulin resistance (IR) according to body mass index (BMI) in middle-aged Korean general population.

TMA was measured using quantitative computed tomography and corrected by body weight (TMA/Wt) in 1,263 men, 788 premenopausal women, and 1,476 postmenopausal women all aged 30 to 64 years. The tertiles of TMA/Wt were calculated separately for men and for premenopausal and postmenopausal women. Homeostatic model assessment for insulin resistance (HOMA-IR) was performed using fasting blood glucose and insulin levels, and increased IR was defined according to sex-specific, top quartiles of HOMA-IR. Associations between the TMA/Wt tertiles and increased IR according to the BMI categories (<25 and ≥25 kg/m²) were assessed using multivariable logistic regression analysis.

In men with higher BMIs, but not in those with lower BMIs, the presence of an increased IR had significantly higher odds ratios in the lower TMA/Wt tertiles, even after adjustment for visceral fat area. However, in premenopausal and postmenopausal women, there was no significant inverse association between TMA/Wt tertiles and increased IR, regardless of BMI category.

Our findings suggest that the thigh muscle is inversely associated with IR in men, particularly in those with higher BMIs.

Keyword

Body composition; Insulin resistance; Muscles; Sarcopenia; Tomography, X-ray computed

Reference

1. 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; 22:2071–2079. PMID: 24862429.

2. Moon SS. Low skeletal muscle mass is associated with insulin resistance, diabetes, and metabolic syndrome in the Korean population: the Korea National Health and Nutrition Examination Survey (KNHANES) 2009-2010. Endocr J. 2014; 61:61–70. PMID: 24088600.

3. Heo JE, Shim JS, Song BM, Bae HY, Lee HJ, Lee E, Kim HC. Association between appendicular skeletal muscle mass and depressive symptoms: review of the cardiovascular and metabolic diseases etiology research center cohort. J Affect Disord. 2018; 238:8–15. PMID: 29852344.

4. Lee SW, Youm Y, Lee WJ, Choi W, Chu SH, Park YR, Kim HC. Appendicular skeletal muscle mass and insulin resistance in an elderly Korean population: the Korean social life, health and aging project-health examination cohort. Diabetes Metab J. 2015; 39:37–45. PMID: 25729711.

5. Hirasawa Y, Matsuki R, Ebisu T, Kurose T, Hamamoto Y, Seino Y. Evaluation of skeletal muscle mass indices, assessed by bioelectrical impedance, as indicators of insulin resistance in patients with type 2 diabetes. J Phys Ther Sci. 2019; 31:190–194. PMID: 30858661.

6. Wells CE, Polkey MI, Baker EH. Insulin resistance is associated with skeletal muscle weakness in COPD. Respirology. 2016; 21:689–696. PMID: 26678022.

7. Wang HL, Ding TT, Lu S, Xu Y, Tian J, Hu WF, Zhang JY. Muscle mass loss and intermuscular lipid accumulation were associated with insulin resistance in patients receiving hemodialysis. Chin Med J (Engl). 2013; 126:4612–4617. PMID: 24342298.

8. Lee J, Hong YP, Shin HJ, Lee W. Associations of sarcopenia and sarcopenic obesity with metabolic syndrome considering both muscle mass and muscle strength. J Prev Med Public Health. 2016; 49:35–44. PMID: 26841883.

9. Poehlman ET, Dvorak RV, DeNino WF, Brochu M, Ades PA. Effects of resistance training and endurance training on insulin sensitivity in nonobese, young women: a controlled randomized trial. J Clin Endocrinol Metab. 2000; 85:2463–2468. PMID: 10902794.

10. Grontved A, Ried-Larsen M, Ekelund U, Froberg K, Brage S, Andersen LB. Independent and combined association of muscle strength and cardiorespiratory fitness in youth with insulin resistance and β-cell function in young adulthood: the European Youth Heart Study. Diabetes Care. 2013; 36:2575–2581. PMID: 23579180.

11. 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; 96:2898–2903. PMID: 21778224.

12. Kim KM, Jang HC, Lim S. Differences among skeletal muscle mass indices derived from height-, weight-, and body mass index-adjusted models in assessing sarcopenia. Korean J Intern Med. 2016; 31:643–650. PMID: 27334763.

13. Dmitruk A, Czeczelewski J, Czeczelewska E, Golach J, Parnicka U. Body composition and fatty tissue distribution in women with various menstrual status. Rocz Panstw Zakl Hig. 2018; 69:95–101. PMID: 29519121.

14. Moon HU, Ha KH, Han SJ, Kim HJ, Kim DJ. The association of adiponectin and visceral fat with insulin resistance and β-cell dysfunction. J Korean Med Sci. 2018; 34:e7. PMID: 30618514.

15. Cheng YH, Tsao YC, Tzeng IS, Chuang HH, Li WC, Tung TH, Chen JY. Body mass index and waist circumference are better predictors of insulin resistance than total body fat percentage in middle-aged and elderly Taiwanese. Medicine (Baltimore). 2017; 96:e8126. PMID: 28953643.

16. Peplies J, Bornhorst C, Gunther K, Fraterman A, Russo P, Veidebaum T, Tornaritis M, De Henauw S, Marild S, Molnar D, Moreno LA, Ahrens W. IDEFICS consortium. Longitudinal associations of lifestyle factors and weight status with insulin resistance (HOMA-IR) in preadolescent children: the large prospective cohort study IDEFICS. Int J Behav Nutr Phys Act. 2016; 13:97. PMID: 27590045.

17. Shim JS, Song BM, Lee JH, Lee SW, Park JH, Choi DP, Lee MH, Ha KH, Kim DJ, Park S, Lee WW, Kim HC. Cardiovascular and Metabolic Diseases Etiology Research Center (CMERC) cohort: study protocol and results of the first 3 years of enrollment. Epidemiol Health. 2017; 39:e2017016. PMID: 28395401.

18. Park JT, Kim BG, Jhun HJ. Alcohol consumption and the CAGE questionnaire in Korean adults: results from the Second Korea National Health and Nutrition Examination Survey. J Korean Med Sci. 2008; 23:199–206. PMID: 18437000.

19. 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; 28:412–419. PMID: 3899825.

20. Yun KJ, Han K, Kim MK, Park YM, Baek KH, Song KH, Kwon HS. Insulin resistance distribution and cut-off value in Koreans from the 2008-2010 Korean National Health and Nutrition Examination Survey. PLoS One. 2016; 11:e0154593. PMID: 27128847.

21. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2012; 35 Suppl 1:S64–S71. PMID: 22187472.

22. Ochi M, Tabara Y, Kido T, Uetani E, Ochi N, Igase M, Miki T, Kohara K. Quadriceps sarcopenia and visceral obesity are risk factors for postural instability in the middle-aged to elderly population. Geriatr Gerontol Int. 2010; 10:233–243. PMID: 20199590.

23. Huang L, Tepaamorndech S, Kirschke CP, Newman JW, Keyes WR, Pedersen TL, Dumnil J. Aberrant fatty acid metabolism in skeletal muscle contributes to insulin resistance in zinc transporter 7 (znt7)-knockout mice. J Biol Chem. 2018; 293:7549–7563. PMID: 29555680.

24. Srikanthan P, Hevener AL, Karlamangla AS. Sarcopenia exacerbates obesity-associated insulin resistance and dysglycemia: findings from the National Health and Nutrition Examination Survey III. PLoS One. 2010; 5:e10805. PMID: 22421977.

25. Kim J. Gender difference in association between appendicular skeletal muscle mass and cardiometabolic abnormalities in normal-weight and obese adults: Korea National Health and Nutrition Examination Survey (KNHANES) IV-3 and V-1. Asia Pac J Public Health. 2015; 27:NP468–NP475. PMID: 23188881.

26. Han SJ, Boyko EJ, Kim SK, Fujimoto WY, Kahn SE, Leonetti DL. Association of thigh muscle mass with insulin resistance and incident type 2 diabetes mellitus in Japanese Americans. Diabetes Metab J. 2018; 42:488–495. PMID: 30302961.

27. Aleman-Mateo H, Lopez Teros MT, Ramirez FA, Astiazaran-Garcia H. Association between insulin resistance and low relative appendicular skeletal muscle mass: evidence from a cohort study in community-dwelling older men and women participants. J Gerontol A Biol Sci Med Sci. 2014; 69:871–877. PMID: 24325896.

28. Tonks KT, Coster AC, Christopher MJ, Chaudhuri R, Xu A, Gagnon-Bartsch J, Chisholm DJ, James DE, Meikle PJ, Greenfield JR, Samocha-Bonet D. Skeletal muscle and plasma lipidomic signatures of insulin resistance and overweight/obesity in humans. Obesity (Silver Spring). 2016; 24:908–916. PMID: 26916476.

29. Fu X, Zhu F, Zhao X, Ma X, Zhu S. Central fat accumulation associated with metabolic risks beyond total fat in normal BMI Chinese adults. Ann Nutr Metab. 2014; 64:93–100. PMID: 24943409.

30. Gueugneau M, Coudy-Gandilhon C, Theron L, Meunier B, Barboiron C, Combaret L, Taillandier D, Polge C, Attaix D, Picard B, Verney J, Roche F, Feasson L, Barthelemy JC, Bechet D. Skeletal muscle lipid content and oxidative activity in relation to muscle fiber type in aging and metabolic syndrome. J Gerontol A Biol Sci Med Sci. 2015; 70:566–576. PMID: 24939997.

31. Adams JM 2nd, Pratipanawatr T, Berria R, Wang E, DeFronzo RA, Sullards MC, Mandarino LJ. Ceramide content is increased in skeletal muscle from obese insulin-resistant humans. Diabetes. 2004; 53:25–31. PMID: 14693694.

32. Boden G. Ceramide: a contributor to insulin resistance or an innocent bystander? Diabetologia. 2008; 51:1095–1096. PMID: 18458870.

33. Coen PM, Dube JJ, Amati F, Stefanovic-Racic M, Ferrell RE, Toledo FG, Goodpaster BH. Insulin resistance is associated with higher intramyocellular triglycerides in type I but not type II myocytes concomitant with higher ceramide content. Diabetes. 2010; 59:80–88. PMID: 19833891.

34. Haugaard SB, Vaag A, Hoy CE, Madsbad S. Sex and muscle structural lipids in obese subjects: an impact on insulin action? Eur J Clin Invest. 2008; 38:494–501. PMID: 18578691.

35. Stubbins RE, Najjar K, Holcomb VB, Hong J, Nunez NP. Oestrogen alters adipocyte biology and protects female mice from adipocyte inflammation and insulin resistance. Diabetes Obes Metab. 2012; 14:58–66. PMID: 21834845.

36. Bredella MA. Sex differences in body composition. Adv Exp Med Biol. 2017; 1043:9–27. PMID: 29224088.

37. Wu CH, Yao WJ, Lu FH, Yang YC, Wu JS, Chang CJ. Sex differences of body fat distribution and cardiovascular dysmetabolic factors in old age. Age Ageing. 2001; 30:331–336. PMID: 11509312.

38. Schorr M, Dichtel LE, Gerweck AV, Valera RD, Torriani M, Miller KK, Bredella MA. Sex differences in body composition and association with cardiometabolic risk. Biol Sex Differ. 2018; 9:28. PMID: 29950175.

39. 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; 101:1847–1855. PMID: 26930180.

40. Brochu M, Starling RD, Tchernof A, Matthews DE, Garcia-Rubi E, Poehlman ET. Visceral adipose tissue is an independent correlate of glucose disposal in older obese postmenopausal women. J Clin Endocrinol Metab. 2000; 85:2378–2384. PMID: 10902782.

41. Toth MJ, Tchernof A, Sites CK, Poehlman ET. Menopause-related changes in body fat distribution. Ann N Y Acad Sci. 2000; 904:502–506. PMID: 10865795.

42. Zanchetti A, Facchetti R, Cesana GC, Modena MG, Pirrelli A, Sega R. SIMONA participants. Menopause-related blood pressure increase and its relationship to age and body mass index: the SIMONA epidemiological study. J Hypertens. 2005; 23:2269–2276. PMID: 16269969.

43. Wang N, Qin MZ, Cui J. Lipid profile comparison between pre- and post-menopausal women. Zhonghua Xin Xue Guan Bing Za Zhi. 2016; 44:799–804. PMID: 27667280.

44. Kasai T, Ishiguro N, Matsui Y, Harada A, Takemura M, Yuki A, Kato Y, Otsuka R, Ando F, Shimokata H. Sex- and age-related differences in mid-thigh composition and muscle quality determined by computed tomography in middle-aged and elderly Japanese. Geriatr Gerontol Int. 2015; 15:700–706. PMID: 25244543.

45. Visser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, Simonsick EM, Harris TB. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci Med Sci. 2005; 60:324–333. PMID: 15860469.

46. Ikeda Y, Suehiro T, Nakamura T, Kumon Y, Hashimoto K. Clinical significance of the insulin resistance index as assessed by homeostasis model assessment. Endocr J. 2001; 48:81–86. PMID: 11403106.