Diabetes Metab J.  2021 Mar;45(2):183-194. 10.4093/dmj.2019.0171.

Age- and Sex-Related Differential Associations between Body Composition and Diabetes Mellitus

• Roh E
• Hwang SY
• Kim JA
• Lee YB
• Hong Sh
• Kim NH
• Seo JA
• Kim SG
• Kim NH
• Choi KM
• Baik SH
• Yoo HJ

• KMID: 2514195
• DOI: http://doi.org/10.4093/dmj.2019.0171

Abstract

The age- and sex-related differences on the impacts of body composition on diabetes mellitus (DM) remain uncertain.

The fourth and fifth Korea National Health and Nutrition Examination Survey included 15,586 subjects over 30 years of age who completed dual-energy X-ray absorptiometry. We conducted a cross-sectional study to investigate whether muscle mass index (MMI), defined as appendicular skeletal muscle divided by body mass index (BMI), and fat mass index (FMI), defined as trunk fat mass divided by BMI, were differently associated with DM according to age and sex.

In multivariate logistic regression, the risk for DM significantly increased across quartiles of FMI in men aged ≥70. Meanwhile, MMI showed a protective association with DM in men of the same age. The odds ratios (ORs) for the highest quartile versus the lowest quartile of FMI and MMI were 3.116 (95% confidence interval [CI], 1.405 to 6.914) and 0.295 (95% CI, 0.157 to 0.554), respectively. In women, the ORs of DM was significantly different across FMI quartiles in those over age 50. The highest quartile of FMI exhibited increased ORs of DM in subjects aged 50 to 69 (OR, 1.891; 95% CI, 1.229 to 2.908) and ≥70 (OR, 2.275; 95% CI, 1.103 to 4.69) compared to lowest quartile. However, MMI was not significantly associated with DM in women of all age groups.

Both FMI and MMI were independent risk factors for DM in men aged 70 years or more. In women over 50 years, FMI was independently associated with DM. There was no significant association between MMI and DM in women.

Keyword

Abdominal fat; Body composition; Diabetes mellitus; Muscle, skeletal

Figure

• 

  Fig. 1 Flowchart of the study population. KNHANES, Korean National Health and Nutrition Examination Survey; DXA, dual-energy X-ray absorptiometry; BMI, body mass index.

• 

  Fig. 2 Age and body mass index, adjusted odds ratio (ORs) (95% confidence intervals [CIs]) for diabetes mellitus by quartiles of (A) fat mass index (FMI) and (B) muscle mass index (MMI) stratified by age groups (30 to 49, 50 to 69, and ≥70 years) in men and women.

• 

Reference

1. Baumgartner RN, Stauber PM, McHugh D, Koehler KM, Garry PJ. Cross-sectional age differences in body composition in persons 60+ years of age. J Gerontol A Biol Sci Med Sci. 1995; 50:M307–M316.

2. Kyle UG, Genton L, Hans D, Karsegard L, Slosman DO, Pichard C. Age-related differences in fat-free mass, skeletal muscle, body cell mass and fat mass between 18 and 94 years. Eur J Clin Nutr. 2001; 55:663–672.

3. Yamada M, Moriguch Y, Mitani T, Aoyama T, Arai H. Age-dependent changes in skeletal muscle mass and visceral fat area in Japanese adults from 40 to 79 years-of-age. Geriatr Gerontol Int. 2014; 14 Suppl 1:8–14.

4. Gastaldelli A, Miyazaki Y, Pettiti M, Matsuda M, Mahankali S, Santini E, et al. Metabolic effects of visceral fat accumulation in type 2 diabetes. J Clin Endocrinol Metab. 2002; 87:5098–5103.

5. Yatagai T, Nagasaka S, Taniguchi A, Fukushima M, Nakamura T, Kuroe A, et al. Hypoadiponectinemia is associated with visceral fat accumulation and insulin resistance in Japanese men with type 2 diabetes mellitus. Metabolism. 2003; 52:1274–1278.

6. Fontana L, Eagon JC, Trujillo ME, Scherer PE, Klein S. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes. 2007; 56:1010–1013.

7. Gabriely I, Ma XH, Yang XM, Atzmon G, Rajala MW, Berg AH, et al. Removal of visceral fat prevents insulin resistance and glucose intolerance of aging: an adipokine-mediated process? Diabetes. 2002; 51:2951–2958.

8. 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.

9. 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.

10. Son JW, Lee SS, Kim SR, Yoo SJ, Cha BY, Son HY, et al. Low muscle mass and risk of type 2 diabetes in middle-aged and older adults: findings from the KoGES. Diabetologia. 2017; 60:865–872.

11. 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; 89:81–88.

12. Fantin F, Di Francesco V, Fontana G, Zivelonghi A, Bissoli L, Zoico E, et al. Longitudinal body composition changes in old men and women: interrelationships with worsening disability. J Gerontol A Biol Sci Med Sci. 2007; 62:1375–1381.

13. Fan B, Shepherd JA, Levine MA, Steinberg D, Wacker W, Barden HS, et al. National Health and Nutrition Examination Survey whole-body dual-energy X-ray absorptiometry reference data for GE Lunar systems. J Clin Densitom. 2014; 17:344–377.

14. Hong S, Oh HJ, Choi H, Kim JG, Lim SK, Kim EK, et al. Characteristics of body fat, body fat percentage and other body composition for Koreans from KNHANES IV. J Korean Med Sci. 2011; 26:1599–1605.

15. Carr MC. The emergence of the metabolic syndrome with menopause. J Clin Endocrinol Metab. 2003; 88:2404–2411.

16. Auro K, Joensuu A, Fischer K, Kettunen J, Salo P, Mattsson H, et al. A metabolic view on menopause and ageing. Nat Commun. 2014; 5:4708.

17. Lim S, Meigs JB. Ectopic fat and cardiometabolic and vascular risk. Int J Cardiol. 2013; 169:166–176.

18. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972; 18:499–502.

19. Cawthon PM, Peters KW, Shardell MD, McLean RR, Dam TT, Kenny AM, et al. Cutpoints for low appendicular lean mass that identify older adults with clinically significant weakness. J Gerontol A Biol Sci Med Sci. 2014; 69:567–575.

20. American Diabetes Association. 15. Diabetes care in the hospital: standards of medical care in diabetes-2019. Diabetes Care. 2019; 42(Suppl 1):S173–S181.

21. Goodpaster BH, Krishnaswami S, Harris TB, Katsiaras A, Kritchevsky SB, Simonsick EM, et al. Obesity, regional body fat distribution, and the metabolic syndrome in older men and women. Arch Intern Med. 2005; 165:777–783.

22. Goodpaster BH, Krishnaswami S, Resnick H, Kelley DE, Haggerty C, Harris TB, et al. Association between regional adipose tissue distribution and both type 2 diabetes and impaired glucose tolerance in elderly men and women. Diabetes Care. 2003; 26:372–379.

23. Snijder MB, Dekker JM, Visser M, Bouter LM, Stehouwer CD, Yudkin JS, et al. Hoorn study. Trunk fat and leg fat have independent and opposite associations with fasting and postload glucose levels: the Hoorn study. Diabetes Care. 2004; 27:372–377.

24. Van Pelt RE, Evans EM, Schechtman KB, Ehsani AA, Kohrt WM. Contributions of total and regional fat mass to risk for cardiovascular disease in older women. Am J Physiol Endocrinol Metab. 2002; 282:E1023–E1028.

25. Tanko LB, Bagger YZ, Alexandersen P, Larsen PJ, Christiansen C. Peripheral adiposity exhibits an independent dominant antiatherogenic effect in elderly women. Circulation. 2003; 107:1626–1631.

26. Arner P. Insulin resistance in type 2 diabetes: role of fatty acids. Diabetes Metab Res Rev. 2002; 18 Suppl 2:S5–S9.

27. Bjorntorp P. Metabolic implications of body fat distribution. Diabetes Care. 1991; 14:1132–1143.

28. Frayn KN. Adipose tissue as a buffer for daily lipid flux. Diabetologia. 2002; 45:1201–1210.

29. Arner P. Differences in lipolysis between human subcutaneous and omental adipose tissues. Ann Med. 1995; 27:435–438.

30. Choi SI, Chung D, Lim JS, Lee MY, Shin JY, Chung CH, et al. Relationship between regional body fat distribution and diabetes mellitus: 2008 to 2010 Korean National Health and Nutrition Examination Surveys. Diabetes Metab J. 2017; 41:51–59.

31. DeFronzo RA. Pathogenesis of type 2 diabetes mellitus. Med Clin North Am. 2004; 88:787–835.

32. Abdul-Ghani MA, DeFronzo RA. Pathogenesis of insulin resistance in skeletal muscle. J Biomed Biotechnol. 2010; 2010:476279.

33. Hong S, Chang Y, Jung HS, Yun KE, Shin H, Ryu S. Relative muscle mass and the risk of incident type 2 diabetes: a cohort study. PLoS One. 2017; 12:e0188650.

34. Kim HK, Lee MJ, Kim EH, Bae SJ, Choe J, Kim CH, et al. Longitudinal changes of body composition phenotypes and their association with incident type 2 diabetes mellitus during a 5-year follow-up in Koreans. Diabetes Metab J. 2019; 43:627–639.

35. Tatsukawa Y, Misumi M, Kim YM, Yamada M, Ohishi W, Fujiwara S, et al. Body composition and development of diabetes: a 15-year follow-up study in a Japanese population. Eur J Clin Nutr. 2018; 72:374–380.

36. Saad F, Rohrig G, von Haehling S, Traish A. Testosterone deficiency and testosterone treatment in older men. Gerontology. 2017; 63:144–156.

37. O'Reilly MW, House PJ, Tomlinson JW. Understanding androgen action in adipose tissue. J Steroid Biochem Mol Biol. 2014; 143:277–284.

38. Lee HJ, Hwang SY, Hong HC, Ryu JY, Seo JA, Kim SG, et al. Waist-to-hip ratio is better at predicting subclinical atherosclerosis than body mass index and waist circumference in postmenopausal women. Maturitas. 2015; 80:323–328.

39. Moon JH, Roh E, Oh TJ, Kim KM, Moon JH, Lim S, et al. Increased risk of metabolic disorders in healthy young adults with family history of diabetes: from the Korea National Health and Nutrition Survey. Diabetol Metab Syndr. 2017; 9:16.

40. Lear SA, Kohli S, Bondy GP, Tchernof A, Sniderman AD. Ethnic variation in fat and lean body mass and the association with insulin resistance. J Clin Endocrinol Metab. 2009; 94:4696–4702.