Association Between Relative Quadriceps Strength and Type 2 Diabetes Mellitus in Older Adults: The Yangpyeong Cohort of the Korean Genome and Epidemiology Study

in Journal of Physical Activity and Health

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Bong Kil Song
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Geon Hui Kim
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Jung Woon Kim
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Elizabeth C. Lefferts
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Angelique G. Brellenthin
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Duck-Chul Lee
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Yu-Mi Kim
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Mi Kyung Kim
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Bo Youl Choi
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Yeon Soo Kim
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Background: To examine the independent and combined association between relative quadriceps strength and the prevalence of type 2 diabetes mellitus (T2DM) in older adults. Methods: Among 1441 Korean older adults aged ≥65 years (71 [4.7] y) recruited between 2007 and 2016, 1055 older adults with no history of myocardial infarction, stroke, or cancer were included in the analysis. Cases of T2DM were identified by self-reported physician diagnosis, use antihyperglycemic medication or insulin, or fasting blood glucose ≥126 mg/dL. Logistic regression was used to calculate the odds ratios and 95% confidence intervals of T2DM by quartiles of relative quadriceps strength. Results: There were 162 T2DM cases (15%). Compared with the lowest quartile (weakest), the odds ratios (95% confidence intervals) of T2DM were 0.56 (0.34–0.90), 0.60 (0.37–0.96), and 0.47 (0.28–0.80) in the second, third, and fourth quartiles, respectively, after adjusting for possible confounders, including body mass index. In the joint analysis, compared with the “weak and overweight/obese” group, the odds (odds ratios [95% confidence intervals]) of T2DM was only lower in the “strong and normal weight” group (0.36 [0.22–0.60]) after adjusting for possible confounders. Conclusions: Greater relative quadriceps strength is associated with reduced odds of T2DM in older adults after adjusting for potential confounders including body mass index.

Song, G.H. Kim, and Y.S. Kim are with the Department of Physical Education, College of Education, Seoul National University, Seoul, South Korea. Song, Lefferts, Brellenthin, and Lee are with the Department of Kinesiology, College of Human Sciences, Iowa State University, Ames, IA, USA. J.W. Kim is with the Department of Aero Fitness, Korea Air Force Academy, Cheong-Ju, South Korea. Y.-M. Kim, M.K. Kim, and Choi are with the Department of Preventive Medicine, College of Medicine, Hanyang University, Seoul, South Korea; and the Institute for Health and Society, Hanyang University, Seoul, South Korea. Y.S. Kim is also with the Institute of Sports Science, Seoul National University, Seoul, South Korea.

Y.S. Kim (kys0101@snu.ac.kr) is corresponding author.
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  • Expand
  • 1.

    International Diabetes Federation. IDF Diabetes Atlas (9th ed.). Brussels, Belgium: International Diabetes Federation; 2019.

  • 2.

    World Health Organization. Classification of Diabetes Mellitus. Geneva, Switzerland: World Health Organization; 2019.

  • 3.

    Verma S, Hussain ME. Obesity and diabetes: an update. Diabetes Metab Syndr: Clin Res Rev. 2017;11(1):7379. doi:10.1016/j.dsx.2016.06.017

  • 4.

    Nair KS. Aging muscle. Am J Clin Nutr. 2005;81(5): 953963. PubMed ID: 15883415 doi:10.1093/ajcn/81.5.953

  • 5.

    Sinclair A, Dunning T, Rodriguez-Mañas L. Diabetes in older people: new insights and remaining challenges. Lancet Diabetes Endocrinol. 2015;3(4):275285. PubMed ID: 25466523 doi:10.1016/S2213-8587(14)70176-7

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Morley JE, Baumgartner RN, Roubenoff R, Mayers J, Nair KS. Sarcopenia. J Lab Clin Med. 2001;137(4);231243. PubMed ID: 11283518 doi:10.1067/mlc.2001.113504

  • 7.

    Li R, Xia J, Zhang XI, et al. Associations of muscle mass and strength with all-cause mortality among US older adults. Med Sci Sports Exerc. 2018;50(3):458. PubMed ID: 28991040 doi:10.1249/MSS.0000000000001448

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Cetinus E, Buyukbese MA, Uzel M, Ekerbicer H, Karaoguz A. Hand grip strength in patients with type 2 diabetes mellitus. Diabetes Res Clin Pract. 2005;70(3):278286. PubMed ID: 15878215 doi:10.1016/j.diabres.2005.03.028

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Mainous AG III, Tanner RJ, Anton SD, Jo A. Grip strength as a marker of hypertension and diabetes in healthy weight adults. Am J Prev Med. 2015;49(6):850858. PubMed ID: 26232901 doi:10.1016/j.amepre.2015.05.025

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Kunutsor SK, Isiozor NM, Khan H, Laukkanen JA. Handgrip strength—A risk indicator for type 2 diabetes: systematic review and meta-analysis of observational cohort studies. Diabetes Metab Res Rev. 2020;37(2):e3365. doi:10.1002/dmrr.3365

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Hughes VA, Frontera WR, Wood M, et al. Longitudinal muscle strength changes in older adults: influence of muscle mass, physical activity, and health. J Gerontol A Biol Sci Med Sci. 2001;56(5):B209B217. doi:10.1093/gerona/56.5.B209

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Buchman AS, Wilson RS, Boyle PA, Tang Y, Fleischman DA, Bennett DA. Physical activity and leg strength predict decline in mobility performance in older persons. J Am Geriatr Soc. 2007;55(10):16181623. PubMed ID: 17697103 doi:10.1111/j.1532-5415.2007.01359.x

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Meigs JB, Wilson PW, Fox CS, et al. Body mass index, metabolic syndrome, and risk of type 2 diabetes or cardiovascular disease. J Clin Endocrinol Metab. 2006;91(8):29062912. PubMed ID: 16735483 doi:10.1210/jc.2006-0594

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Castaneda C, Layne JE, Munoz-Orians L, et al. A randomized controlled trial of resistance exercise training to improve glycemic control in older adults with type 2 diabetes. Diabetes Care. 2002;25(12):23352341. PubMed ID: 12453982 doi:10.2337/diacare.25.12.2335

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Rhi SY, Lee O, Kim YS, Chung JS. Reliability of isometric maximal voluntary contraction test and regression equations to predict one repetition maximal strength in women. Korean J Phys Educ. 2011;50:433439.

    • Search Google Scholar
    • Export Citation
  • 16.

    Ishigaki N, Kimura T, Usui Y, et al. Analysis of pelvic movement in the elderly during walking using a posture monitoring system equipped with a triaxial accelerometer and a gyroscope. J Biomech. 2011;44(9):17881792. PubMed ID: 21546026 doi:10.1016/j.jbiomech.2011.04.016

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    American Diabetes Association. 2. Classification and diagnosis of diabetes. Diabetes Care. 2017;40(Suppl 1):S11S24. doi:10.2337/dc16-S005

  • 18.

    Oh JM, Woo HW, Kim MK, et al. Dietary total, animal, vegetable calcium and type 2 diabetes incidence among Korean adults: the Korean Multi-Rural Communities Cohort (MRCohort). Nutr Metab Cardiovasc Dis. 2017;27(12):11521164. PubMed ID: 29167059 doi:10.1016/j.numecd.2017.10.005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Hong SM, Woo HW, Kim MK, et al. A prospective association between dietary folate intake and type 2 diabetes risk among Korean adults aged 40 years or older: the Korean Multi-Rural Communities Cohort (MRCohort) Study. Br J Nutr. 2017;118(12):10781088. doi:10.1017/S0007114517003087

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Son JW, Lee SS, Kim SR, et al. Low muscle mass and risk of type 2 diabetes in middle-aged and older adults: findings from the KoGES. Diabetologia. 2017;60(5):865872. PubMed ID: 28102434 doi:10.1007/s00125-016-4196-9

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Fink A, Buchmann N, Tegeler C, Steinhagen-Thiessen E, Demuth I, Doblhammer G. Physical activity and cohabitation status moderate the link between diabetes mellitus and cognitive performance in a community-dwelling elderly population in Germany. PLoS One. 2017;12(10):e0187119. PubMed ID: 29073237 doi:10.1371/journal.pone.0187119

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Daya R, Bayat Z, Raal FJ. Prevalence and pattern of dyslipidaemia in type 2 diabetes mellitus patients at a tertiary care hospital. JEMDSA. 2017;22(3):3135. doi:10.1080/16089677.2017.1360064

    • Search Google Scholar
    • Export Citation
  • 23.

    World Health Organization. Global database on Body Mass Index: BMI Classification 2006. Geneva, Switzerland: World Health Organization; 2015.

    • Search Google Scholar
    • Export Citation
  • 24.

    Whelton PK, Carey RM, Aronow WS, et al. 2017 ACC/AHA/AAPA/ABC/ACPM/AGS/APhA/ASH/ASPC/NMA/PCNA guideline for the prevention, detection, evaluation, and management of high blood pressure in adults: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. J Am Coll Cardiol. 2018;71(19):e127e248. PubMed ID: 29146535 doi:10.1016/j.jacc.2017.11.006

    • Search Google Scholar
    • Export Citation
  • 25.

    Na W, Chung B, Sohn C. A relationship between dietary patterns and dyslipidemia in urban-dwelling middle-aged Korean men: using Korean Genome and Epidemiology Study (KoGES). Clin Nutr Res. 2019;8(3):219228. PubMed ID: 31384600 doi:10.7762/cnr.2019.8.3.219

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Artero EG, Lee DC, Ruiz JR, et al. A prospective study of muscular strength and all-cause mortality in men with hypertension. J Am Coll Cardiol. 2011;57(18):18311837. PubMed ID: 21527158 doi:10.1016/j.jacc.2010.12.025

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Ruiz JR, Sui X, Lobelo F, et al. Association between muscular strength and mortality in men: prospective cohort study. BMJ. 2008;337:a439. PubMed ID: 18595904 doi:10.1136/bmj.a439

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    World Health Organization. Obesity: Preventing and Managing the Global Epidemic. Geneva, Switzerland: World Health Organization; 2000.

  • 29.

    Visser M, Deeg DJ, Lips P, Harris TB, Bouter LM. Skeletal muscle mass and muscle strength in relation to lower-extremity performance in older men and women. J Am Geriatr Soc. 2000;48(4):381386. PubMed ID: 10798463 doi:10.1111/j.1532-5415.2000.tb04694.x

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Wang Y, Lee DC, Brellenthin AG, et al. Association of muscular strength and incidence of type 2 diabetes. Mayo Clin Proc. 2019;94(4):643651. PubMed ID: 30871784 doi:10.1016/j.mayocp.2018.08.037

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Carbone S, Kirkman DL, Garten RS, et al. Muscular strength and cardiovascular disease: an updated state-of-the-art narrative review. J Cardiopulm Rehabil Prev. 2020;40(5):302309. PubMed ID: 32796492 doi:10.1097/HCR.0000000000000525

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Wang Y, Lee DC, Brellenthin AG, et al. Leisure-time running reduces the risk of incident type 2 diabetes. Am J Med. 2019;132(10):12251232. PubMed ID: 31103650 doi:10.1016/j.amjmed.2019.04.035

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Larsen BA, Wassel CL, Kritchevsky SB, et al. Association of muscle mass, area, and strength with incident diabetes in older adults: the health abc study. J Clin Endocrinol Metab. 2016;101(4):18471855. PubMed ID: 26930180 doi:10.1210/jc.2015-3643

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Kalyani RR, Metter EJ, Xue QL, et al. The relationship of lean body mass with aging to the development of diabetes. J Endocr Soc. 2020;4(7):bvaa043. doi:10.1210/jendso/bvaa043

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Wade KH, Carslake D, Sattar N, Davey Smith G, Timpson NJ. BMI and mortality in UK Biobank: revised estimates using mendelian randomization. Obesity. 2018;26(11):17961806. PubMed ID: 30358150 doi:10.1002/oby.22313

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Asia Pacific Cohort Studies Collaboration. Body mass index and cardiovascular disease in the Asia-Pacific region: an overview of 33 cohorts involving 310,000 participants. Int J Epidemiol. 2004;33(4):751758. doi:10.1093/ije/dyh163

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Meigs JB, Wilson PWF, Fox CS, et al. Body mass index, metabolic syndrome, and risk of type 2 diabetes or cardiovascular disease. J Clin Endocrinol Metab. 2006;91(8):29062912. PubMed ID: 16735483 doi:10.1210/jc.2006-0594

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Hossain P, Kawar B, Nahas ME. Obesity and diabetes in the developing world—A growing challenge. N Engl J Med. 2007;356(3):213215. doi:10.1056/NEJMp068177

  • 39.

    Park SW, Goodpaster BH, Strotmeyer ES, et al. Decreased muscle strength and quality in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes. 2006;55(6):18131818. PubMed ID: 16731847 doi:10.2337/db05-1183

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Kim KS, Park KS, Kim MJ, Kim SK, Cho YW, Park SW. Type 2 diabetes is associated with low muscle mass in older adults. Geriatr Gerontol Int. 2014;14:115121. PubMed ID: 24450569 doi:10.1111/ggi.12189

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Kalyani RR, Tra Y, Yeh HC, Egan JM, Ferrucci L, Brancati FL. Quadriceps strength, quadriceps power, and gait speed in older US adults with diabetes mellitus: results from the National Health and Nutrition Examination Survey, 1999–2002. J Am Geriatr Soc. 2013;61(5):769775. PubMed ID: 23617584 doi:10.1111/jgs.12204

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42.

    IJzerman TH, Schaper NC, Melai T, Meijer K, Wiliems PBJ, Savelberg HHCM. Lower extremity muscle strength is reduced in people with type 2 diabetes, with and without polyneuropathy, and is associated with impaired mobility and reduced quality of life. Diabetes Res Clin Pract. 2012;95(3):345351. PubMed ID: 22104262 doi:10.1016/j.diabres.2011.10.026

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Park SW, Goodpaster BH, Strotmeyer ES, et al. Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes Care. 2007;30(6):15071512. PubMed ID: 22104262 doi:10.2337/dc06-2537x

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Andersen H, Nielsen S, Mogensen CE, Jakobsen J. Muscle strength in type 2 diabetes. Diabetes. 2004;53(6):15431548. PubMed ID: 15161759 doi:10.2337/diabetes.53.6.1543

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    Russell ST, Rajani S, Dhadda RS, Tisdale MJ. Mechanism of induction of muscle protein loss by hyperglycaemia. Exp Cell Res. 2009;315(1):1625. PubMed ID: 18973755 doi:10.1016/j.yexcr.2008.10.002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    Pereira S, Marliss EB, Morais JA, Chevalier S, Gougeon R. Insulin resistance of protein metabolism in type 2 diabetes. Diabetes. 2008;57(1):5663. PubMed ID: 17940118 doi:10.2337/db07-0887

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    Figaro MK, Kritchevsky SB, Resnick HE, et al. Diabetes, inflammation, and functional decline in older adults: findings from the Health, Aging and Body Composition (ABC) study. Diabetes Care. 2006;29(9):20392045. PubMed ID: 16936150 doi:10.2337/dc06-0245

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Goyal R, Faizy AF, Siddiqui SS, Singhai M. Evaluation of TNF-α and IL-6 levels in obese and non-obese diabetics: pre- and postinsulin effects. N Am J Med Sci. 2012;4(4):180. PubMed ID: 22536561 doi:10.4103/1947-2714.94944

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49.

    Anderson LJ, Liu H, Garcia JM. Sex differences in muscle wasting. Adv Exp Med Biol. 2017;1043:153197. PubMed ID: 29224095 doi:10.1007/978-3-319-70178-3_9

  • 50.

    Sénéchal M, Dionne IJ, Brochu M. Dynapenic abdominal obesity and metabolic risk factors in adults 50 years of age and older. J Aging Health. 2012;24(5):812826. PubMed ID: 22451528 doi:10.1177/0898264312440324

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
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