Sex differences in sarcopenia and frailty among community-dwelling Korean older adults with diabetes: The Korean Frailty and Aging Cohort Study

Sunyoung Kang, Tae Jung Oh, Be Long Cho, Yong Soon Park, Eun Roh, Hyeon Ju Kim, Sam-Gyu Lee, Bong Jo Kim, Miji Kim, Chang Won Won, Hak Chul Jang, Sunyoung Kang, Tae Jung Oh, Be Long Cho, Yong Soon Park, Eun Roh, Hyeon Ju Kim, Sam-Gyu Lee, Bong Jo Kim, Miji Kim, Chang Won Won, Hak Chul Jang

Abstract

Aims/introduction: We aimed to examine the prevalence of sarcopenia and frailty in Korean older adults with diabetes compared with individuals without diabetes.

Materials and methods: We analyzed the data of 2,403 participants aged 70-84 years enrolled in the Korean Frailty and Aging Cohort Study. Sarcopenia was defined using the Asian Working Group for Sarcopenia and the Foundation for the National Institutes of Health. Frailty was assessed by the Cardiovascular Health Study frailty phenotype criteria.

Results: The mean age of the participants was 76.0 ± 3.9 years, and 47.2% were men. The prevalence of diabetes was 30.2% in men and 25.8% in women. Adults with diabetes showed a lower muscle mass index (appendicular skeletal muscle mass/body mass index) and handgrip strength in both sexes, but only the women showed decreased physical performance. Women with diabetes presented a higher prevalence of sarcopenia diagnosed by the Foundation for the National Institutes of Health criteria, and frailty compared with participants without diabetes (sarcopenia 14.7% vs 8.5%, P = 0.001; frailty 9.5% vs 4.9%, P = 0.003). Men in the high and middle tertiles for homeostatic model assessment of insulin resistance presented a significantly higher prevalence of sarcopenia, compared with men in the low tertile homeostatic model assessment of insulin resistance (high tertile 16.6%, middle tertile 13.3%, low tertile 8.6%).

Conclusions: In older adults with diabetes, muscle mass index and muscle strength were lower than in those without diabetes. However, the prevalence of sarcopenia and frailty was higher and physical performance was lower only in women with diabetes.

Keywords: Frailty; Sarcopenia; Type 2 diabetes.

Conflict of interest statement

The authors declare no conflict of interest.

© 2020 The Authors. Journal of Diabetes Investigation published by Asian Association for the Study of Diabetes (AASD) and John Wiley & Sons Australia, Ltd.

Figures

Figure 1
Figure 1
Flow diagram showing the number of participants who were enrolled in the Korean Frailty and Aging Cohort Study (KFACS) study. Of a total 3,014 enrolled participants, 2,403 participants were finally included for analysis. BIA, bioimpedance analysis; DXA, dual‐energy X‐ray absorptiometry; HGS, handgrip strength.

References

    1. Korean Statistical Information Service . Available from:
    1. Jang HC. How to diagnose sarcopenia in Korean older adults? Ann Geriat Med Res 2018; 22: 73–79.
    1. Cruz‐Jentoft AJ, Bahat G, Bauer J, et al Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48: 601.
    1. 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.
    1. Kim JH, Lim S, Choi SH, et al Sarcopenia: an independent predictor of mortality in community‐dwelling older Korean men. J Gerontol A Biol Sci Med Sci 2014; 69: 1244–1252.
    1. Delmonico MJ, Harris TB, Lee JS, et al Alternative definitions of sarcopenia, lower extremity performance, and functional impairment with aging in older men and women. J Am Geriatr Soc 2007; 55: 769–774.
    1. Goodpaster BH, Park SW, Harris TB, et al The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci 2006; 61: 1059–1064.
    1. Kalyani RR, Corriere M, Ferrucci L. Age‐related and disease‐related muscle loss: the effect of diabetes, obesity, and other diseases. Lancet Diabetes Endocrinol 2014; 2: 819–829.
    1. Won JC, Lee JH, Kim JH, et al Diabetes fact sheet in Korea, 2016: an appraisal of current status. Diabetes Metab J 2018; 42: 415–424.
    1. Kim TN, Park MS, Yang SJ, et al Prevalence and determinant factors of sarcopenia in patients with type 2 diabetes: the Korean Sarcopenic Obesity Study (KSOS). Diabetes Care 2010; 33: 1497–1499.
    1. Park SW, Goodpaster BH, Lee JS, et al Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care 2009; 32: 1993–1997.
    1. Kalyani RR, Tra Y, Yeh HC, et al Quadriceps strength, quadriceps power, and gait speed in older U.S. adults with diabetes mellitus: results from the National Health and Nutrition Examination Survey, 1999–2002. J Am Geriatr Soc 2013; 61: 769–775.
    1. 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: 1507–1512.
    1. Barzilay JI, Cotsonis GA, Walston J, et al Insulin resistance is associated with decreased quadriceps muscle strength in nondiabetic adults aged >or=70 years. Diabetes Care 2009; 32: 736–738.
    1. Kuo CK, Lin LY, Yu YH, et al Inverse association between insulin resistance and gait speed in nondiabetic older men: results from the U.S. National Health and Nutrition Examination Survey (NHANES) 1999–2002. BMC Geriatr 2009; 9: 49.
    1. Xu L, Hao YT. Effect of handgrip on coronary artery disease and myocardial infarction: a Mendelian randomization study. Sci Rep 2017; 7: 954.
    1. Leong DP, Teo KK, Rangarajan S, et al Prognostic value of grip strength: findings from the Prospective Urban Rural Epidemiology (PURE) study. Lancet 2015; 386: 266–273.
    1. Abellan van Kan G. Epidemiology and consequences of sarcopenia. J Nutr Health Aging. 2009; 13: 708–712.
    1. Kim KS, Park KS, Kim MJ, et al Type 2 diabetes is associated with low muscle mass in older adults. Geriatr Gerontol Int 2014; 14(Suppl 1): 115–121.
    1. Lee MR, Jung SM, Bang H, et al Association between muscle strength and type 2 diabetes mellitus in adults in Korea: data from the Korea national health and nutrition examination survey (KNHANES) VI. Medicine (Baltimore) 2018; 97: e10984.
    1. Won CW, Lee S, Kim J, et al Korean frailty and aging cohort study (KFACS): cohort profile. BMJ Open 2020; 10: e035573.
    1. American Diabetes Association . 2. Classification and diagnosis of diabetes: standards of medical care in diabetes‐2018. Diabetes Care 2018; 41(Suppl 1): S13–S27.
    1. Guralnik JM, Simonsick EM, Ferrucci L, et al A short physical performance battery assessing lower extremity function: association with self‐reported disability and prediction of mortality and nursing home admission. J Gerontol 1994; 49: M85–M94.
    1. Podsiadlo D, Richardson S. The timed "Up & Go": a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 1991; 39: 142–148.
    1. Studenski SA, Peters KW, Alley DE, et al The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci 2014; 69: 547–558.
    1. Fried LP, Tangen CM, Walston J, et al Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci 2001; 56: M146–M157.
    1. Saum KU, Dieffenbach AK, Muller H, et al Frailty prevalence and 10‐year survival in community‐dwelling older adults: results from the ESTHER cohort study. Eur J Epidemiol 2014; 29: 171–179.
    1. Bouillon K, Kivimaki M, Hamer M, et al Diabetes risk factors, diabetes risk algorithms, and the prediction of future frailty: the Whitehall II prospective cohort study. J Am Med Dir Assoc 2013; 14: e851–e856.
    1. Baumgartner RN, Koehler KM, Gallagher D, et al Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 1998; 147: 755–763.
    1. Newman AB, Kupelian V, Visser M, et al Sarcopenia: alternative definitions and associations with lower extremity function. J Am Geriatr Soc 2003; 51: 1602–1609.
    1. 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.
    1. Therkelsen KE, Pedley A, Hoffmann U, et al Intramuscular fat and physical performance at the Framingham Heart Study. Age (Dordr) 2016; 38: 31.
    1. Karastergiou K, Smith SR, Greenberg AS, et al Sex differences in human adipose tissues ‐ the biology of pear shape. Biol Sex Differ 2012; 3: 13.
    1. Beavers KM, Beavers DP, Houston DK, et al Associations between body composition and gait‐speed decline: results from the Health, Aging, and Body Composition study. Am J Clin Nutr 2013; 97: 552–560.
    1. Pereira S, Marliss EB, Morais JA, et al Insulin resistance of protein metabolism in type 2 diabetes. Diabetes 2008; 57: 56–63.
    1. Abdulla H, Smith K, Atherton PJ, et al Role of insulin in the regulation of human skeletal muscle protein synthesis and breakdown: a systematic review and meta‐analysis. Diabetologia 2016; 59: 44–55.
    1. Wang X, Hu Z, Hu J, et al Insulin resistance accelerates muscle protein degradation: Activation of the ubiquitin‐proteasome pathway by defects in muscle cell signaling. Endocrinology 2006; 147: 4160–4168.
    1. Rolland Y, Czerwinski S, Abellan Van Kan G, et al Sarcopenia: its assessment, etiology, pathogenesis, consequences and future perspectives. J Nutr Health Aging 2008; 12: 433–450.
    1. Dimitriadis G, Mitrou P, Lambadiari V, et al Insulin effects in muscle and adipose tissue. Diabetes Res Clin Pract 2011; 93(Suppl 1): S52–S59.
    1. Newman AB, Kupelian V, Visser M, et al Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort. J Gerontol A Biol Sci Med Sci 2006; 61: 72–77.
    1. Moore AZ, Caturegli G, Metter EJ, et al Difference in muscle quality over the adult life span and biological correlates in the Baltimore Longitudinal Study of Aging. J Am Geriatr Soc 2014; 62: 230–236.
    1. Visser M, Goodpaster BH, Kritchevsky SB, et al 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.
    1. Oh TJ, Song Y, Moon JH, et al Diabetic peripheral neuropathy as a risk factor for sarcopenia. Ann Geriatr Med Res 2019; 23: 170–175.
    1. Gougeon R, Marliss EB, Jones PJ, et al Effect of exogenous insulin on protein metabolism with differing nonprotein energy intakes in Type 2 diabetes mellitus. Int J Obesity Relat Metab Dis 1998; 22: 250–261.
    1. Gougeon R, Styhler K, Morais JA, et al Effects of oral hypoglycemic agents and diet on protein metabolism in type 2 diabetes. Diabetes Care 2000; 23: 1–8.
    1. Lee CG, Boyko EJ, Barrett‐Connor E, et al Insulin sensitizers may attenuate lean mass loss in older men with diabetes. Diabetes Care 2011; 34: 2381–2386.
    1. Kang ES, Yun YS, Park SW, et al Limitation of the validity of the homeostasis model assessment as an index of insulin resistance in Korea. Metabolism 2005; 54: 206–211.
    1. Katsuki A, Sumida Y, Gabazza EC, et al Homeostasis model assessment is a reliable indicator of insulin resistance during follow‐up of patients with type 2 diabetes. Diabetes Care 2001; 24: 362–365.
    1. Shepherd JA, Fan B, Lu Y, et al A multinational study to develop universal standardization of whole‐body bone density and composition using GE Healthcare Lunar and Hologic DXA systems. J Bone Miner Res 2012; 27: 2208–2216.

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