Sex Differences in the Prevalence of Metabolic Syndrome Based on Leg Strength, Cardiorespiratory Fitness, and Skeletal Muscle Mass in Elderly

Background: Metabolic syndrome (MetS) is characterized by abdominal obesity, high blood glucose, and dyslipidemia. Low fitness, muscle mass, and strength increase the risk of MetS. The characteristics of these variables are highly interrelated. This cross-sectional study aimed to analyze the prevalence of MetS by combining leg strength (LSTR), cardiorespiratory fitness (CRF), and appendicular skeletal muscle mass (ASM) in elderly men and women. Methods: Participants included 1420 persons aged 65–79 years (men: 753, women: 667). An isokinetic dynamometer was used to measure LSTR; CRF was evaluated by measuring maximum oxygen uptake; and ASM was assessed using bio-impedance analysis. The measured CRF, LSTR, and ASM were converted to relative values by dividing by body weight and grouped into ‘high’ and ‘low’ based on the median value. The diagnosis of MetS was based on five criteria: waist circumference, blood pressure, high-density lipoprotein cholesterol, triglycerides, and fasting glucose. MetS was diagnosed when the participant fulfilled 3 or more of the criteria, and odds ratios (ORs) were analyzed using logistic regression. Results: MetS was diagnosed in 32.1% and 30.3% of men and women, respectively. The relative LSTR and ASM values were significantly higher in the non-MetS group compared to those of the MetS group in both sexes. The OR for MetS in men was 3.6-fold higher in the low LSTR group, 3.5-fold higher in the low CRF group, and 2.3-fold higher in the low ASM group than in the high groups. In women, the OR for MetS increased 1.3-fold in the group with low LSTR and 3.7-fold in the group with low CRF. The OR for MetS exhibited a 3.5-fold increase in men and a 2.4-fold increase in women for combined low LSTR and low ASM compared to those of the combined high LSTR and high ASM group. Despite high ASM, the OR for MetS was a 3.5-fold higher in men and a 3.9-fold in women for low LSTR and low CRF group. Conclusions: The prevalence of MetS increased in elderly with relatively decreased LSTR, ASM and decreased CRF. Furthermore, the prevalence of MetS is increased when both LSTR and ASM are low despite high CRF. In addition, even if ASM was low, the risk of metabolic syndrome did not increase when both CRF and LSTR were high. In conclusion, when two or more of the three variables CRF, LSTR, and ASM were low, the prevalence of MetS increased.

leg strength; cardiorespiratory fitness; appendicular skeletal muscle mass; prevalence; metabolic syndrome; sex differences

[1] McCracken E, Monaghan M, Sreenivasan S. Pathophysiology of the metabolic syndrome. Clinics in Dermatology. 2018; 36: 14–20.

[2] Saklayen MG. The Global Epidemic of the Metabolic Syn-drome. Current Hypertension Reports. 2018; 20: 12.

[3] Li X, Li X, Lin H, Fu X, Lin W, Li M, et al. Metabolic syndrome and stroke: a meta-analysis of prospective cohort studies. Jour-nal of Clinical Neuroscience. 2017; 40: 34–38.

[4] Thomsen M, Nordestgaard BG. Myocardial Infarction and Is-chemic Heart Disease in Overweight and Obesity with and with-out Metabolic Syndrome. JAMA Internal Medicine. 2014; 174: 15.

[5] Kaminsky LA, Arena R, Ellingsen Ø, Harber MP, Myers J, Oze-mek C, et al. Cardiorespiratory fitness and cardiovascular dis-ease - the past, present, and future. Progress in Cardiovascular Diseases. 2019; 62: 86–93.

[6] Grundy SM, Barlow CE, Farrell SW, Vega GL, Haskell WL. Cardiorespiratory fitness and metabolic risk. The American Journal of Cardiology. 2012; 109: 988–993.

[7] Cho KK, Kim YH, Kim YH. Association of fitness, body cir-cumference, muscle mass, and exercise habits with metabolic syndrome. Journal of Men’s Health. 2019; 15: 46–55.

[8] Puthoff ML, Janz KF, Nielsen DH. The Relationship between Lower Extremity Strength and Power to Everyday Walking Be-haviors in Older Adults with Functional Limitations. Journal of Geriatric Physical Therapy. 2008; 31: 24–31.

[9] Jurca R, Lamonte MJ, Barlow CE, Kampert JB, Church TS, et al. Association of Muscular Strength with Incidence of Metabolic Syndrome in Men. Medicine and Science in Sports and Exercise. 2005; 37: 1849–1855.

[10] Marette A, Liu Y, Sweeney G. Skeletal muscle glucose metabolism and inflammation in the development of the metabolic syndrome. Reviews in Endocrine and Metabolic Dis-orders. 2014; 15: 299–305.

[11] Kim H, Kim YH, Kim W. Association of low muscle mass and isokinetic strength with metabolic syndrome. Journal of Men’s Health. 2020; 16: e50–e58.

[12] Power GA, Allen MD, Booth WJ, Thompson RT, Marsh GD, Rice CL. The influence on sarcopenia of muscle quality and quantity derived from magnetic resonance imaging and neuro-muscular properties. Age. 2014; 36: 9642.

[13] Korshøj M, Lidegaard M, Skotte JH, Krustrup P, Krause N, Sø-gaard K, et al. Does aerobic exercise improve or impair car-diorespiratory fitness and health among cleaners? A cluster ran-domized controlled trial. Scandinavian Journal of Work, Envi-ronment and Health. 2015; 41: 140–152.

[14] Alberga AS, Prud’homme D, Sigal RJ, Goldfield GS, Hadjiyan-nakis S, Phillips P, et al. Effects of aerobic training, resistance training, or both on cardiorespiratory and musculoskeletal fit-ness in adolescents with obesity: the HEARTY trial. Applied Physiology, Nutrition, and Metabolism. 2016; 41: 255–265.

[15] Schumann M, Yli-Peltola K, Abbiss CR, Häkkinen K. Cardiorespiratory adaptations during concurrent aerobic and strength training in men and women. PLoS ONE. 2015; 10: e0139279–e0139293.

[16] Mosca L, Barrett-Connor E, Kass Wenger N. Sex/Gender Differ-ences in Cardiovascular Disease Prevention. Circulation. 2011; 124: 2145–2154.

[17] Aguilar M, Bhuket T, Torres S, Liu B, Wong RJ. Prevalence of the Metabolic Syndrome in the United States, 2003–2012. JAMA. 2015; 313: 1973.

[18] Li Y, Zhao L, Yu D, Wang Z, Ding G. Metabolic syndrome prevalence and its risk factors among adults in China: A na-tionally representative cross-sectional study. PLoS ONE. 2018; 13: e0199293–e0199308.

[19] National High Blood Pressure Education Program. The seventh report of the Joint National Committee on prevention, detection, evaluation, and treatment of high blood pressure (Report No.: 04- 5230). Department of health and human service, D.C.: Washington. 2004.

[20] Lima-Oliveira G, Lippi G, Salvagno GL, Picheth G, Guidi GC. Laboratory diagnostics and quality of blood collection. Journal of Medical Biochemistry. 2015; 34: 288–294.

[21] Ostchega Y, Seu R, Isfahani NS, Zhang G, Hughes JP, et al. Waist Circumference Measurement Methodology Study: Na-tional Health and Nutrition Examination Survey, 2016. Vital and Health Statistics. Series 2, Data Evaluation and Methods Re-search. 2019; 1–20.

[22] Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults. Executive Summary of the third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) JAMA: the Journal of the American Medical Association. 2001; 285: 2486–2497.

[23] Inoue S, Zimmet P, Caterson I, Chunming C, Ikeda Y, et al. The Asia-Pacific perspective: redefining obesity and its treatment. World Health Organization Sydney: Sydney. 2000.

[24] CSMi. Humac Norm Users Guide; Computer Sports Medicine, Inc.: Stoughton, MA. 2019.

[25] ACSM. ACSM’s guidelines for exercise testing and prescrip-tion. 10th edn. Lippincott Williams and Wilkins: Philadelphia, PA. 2017.

[26] Kim B, Ku M, Kiyoji T, Isobe T, Sakae T, Oh S. Cardiorespi-ratory fitness is strongly linked to metabolic syndrome among physical fitness components: a retrospective cross-sectional study. Journal of Physiological Anthropology. 2020; 39: 30.

[27] Stabelini Neto A, Sasaki JE, Mascarenhas LP, Boguszewski MC, Bozza R, Ulbrich AZ, et al. Physical activity, cardiorespi-ratory fitness, and metabolic syndrome in adolescents: a cross-sectional study. BMC Public Health. 2011; 11: 674.

[28] Kodama S. Cardiorespiratory Fitness as a Quantitative Predic-tor of all-Cause Mortality and Cardiovascular Events in Healthy Men and Women. JAMA. 2009; 301: 2024.

[29] Bergman BC, Horning MA, Casazza GA, Wolfel EE, Butter-field GE, Brooks GA. Endurance training increases gluconeo-genesis during rest and exercise in men. American Journal of Physiology-Endocrinology and Metabolism. 2000; 278: E244–E251.

[30] Zhang W, Zhao Z, Sun X, Tian X. Prevalence of Metabolic Syndrome According to Absolute and Relative Values of Mus-cle Strength in Middle-Aged and Elderly Women. International Journal of Environmental Research and Public Health. 2021; 18: 9073–9095.

[31] Steins Bisschop CN, Peeters PHM, Monninkhof EM, van der Schouw YT, May AM. Associations of visceral fat, physical ac-tivity and muscle strength with the metabolic syndrome. Matu-ritas. 2013; 76: 139–145.

[32] Mesinovic J, McMillan LB, Shore-Lorenti C, De Courten B, Ebeling PR, et al. Metabolic syndrome and its associations with components of sarcopenia in overweight and obese older adults. Journal of Clinical Medicine. 2019; 8: 145–158.

[33] Jurca R, Lamonte MJ, Church TS, Earnest CP, Fitzgerald SJ, et al. Associations of Muscle Strength and Fitness with Metabolic Syndrome in Men. Medicine and science in sports and exercise. 2004; 36: 1301–1307.

[34] Merchant RA, Chan YH, Lim JY, Morley JE. Prevalence of Metabolic Syndrome and Association with Grip Strength in Older Adults: Findings from the Hope Study. Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy. 2020; 13: 2677–2686.

[35] Newman AB, Kupelian V, Visser M, Simonsick EM, Good-paster BH, Kritchevsky SB, et al. Strength, but not Muscle Mass, is Associated with Mortality in the Health, Aging and Body Composition Study Cohort. The Journals of Gerontology Series a: Biological Sciences and Medical Sciences. 2006; 61: 72–77.

[36] Song P, Han P, Zhao Y, Zhang Y, Wang L, Tao Z, et al. Muscle mass rather than muscle strength or physical performance is as-sociated with metabolic syndrome in community-dwelling older Chinese adults. BMC Geriatrics. 2021; 21: 191.

[37] Atlantis E, Martin SA, Haren MT, Taylor AW, Wittert GA. Inverse associations between muscle mass, strength, and the metabolic syndrome. Metabolism. 2009; 58: 1013–1022.

[38] Jorge ML, de Oliveira VN, Resende NM, Paraiso LF, Calixto A, Diniz AL, et al. The effects of aerobic, resistance, and combined exercise on metabolic control, inflammatory markers, adipocy-tokines, and muscle insulin signaling in patients with type 2 di-abetes mellitus. Metabolism: Clinical and Experimental. 2011; 60: 1244–1252.

[39] Marini E, Mariani PG, Ministrini S, Pippi R, Aiello C, Regi-nato E, et al. Combined aerobic and resistance training improves microcirculation in metabolic syndrome. The Journal of Sports Medicine and Physical Fitness. 2019; 59: 1571–1576.

[40] Wewege MA, Thom JM, Rye K, Parmenter BJ. Aerobic, re-sistance or combined training: a systematic review and meta-analysis of exercise to reduce cardiovascular risk in adults with metabolic syndrome. Atherosclerosis. 2018; 274: 162–171.

[41] Garcia M, Mulvagh SL, Bairey Merz CN, Buring JE, Manson JE. Cardiovascular Disease in Women. Circulation Research. 2016; 118: 1273–1293.

[42] Yi Y, An J. Sex Differences in Risk Factors for Metabolic Syn-drome in the Korean Population. International Journal of Envi-ronmental Research and Public Health. 2020; 17: 9513–9526.

[43] Shin D, Kongpakpaisarn K, Bohra C. Trends in the prevalence of metabolic syndrome and its components in the United States 2007–2014. International Journal of Cardiology. 2018; 259: 216–219.

[44] Xi B, He D, Hu Y, Zhou D. Prevalence of metabolic syndrome and its influencing factors among the Chinese adults: the China Health and Nutrition Survey in 2009. Preventive Medicine. 2013; 57: 867–871.

[45] Ko DH, Lee KH, Kim YH. Longitudinal study on the relative risk of type 2 diabetes mellitus according to obesity and physical activity. Journal of Men’s Health. 2020; 16: 1–10.

[46] Min HJ, Jung WJ, Kim YH. Changes in obesity and physical activity according to gender in South Korean adults, 2002–2013. Journal of Men’s Health. 2019; 15: e28–e36.

[47] Humphries KH, Izadnegahdar M, Sedlak T, Saw J, Johnston N, Schenck-Gustafsson K, et al. Sex differences in cardiovascular disease – Impact on care and outcomes. Frontiers in Neuroen-docrinology. 2017; 46: 46–70.

[48] Chooi YC, Ding C, Magkos F. The epidemiology of obesity. Metabolism. 2019; 92: 6–10.

[49] Pradhan AD. Sex Differences in the Metabolic Syndrome: Im-plications for Cardiovascular Health in Women. Clinical Chem-istry. 2014; 60: 44–52.

[50] Bleich SN, Jarlenski MP, Bell CN, LaVeist TA. Health Inequal-ities: Trends, Progress, and Policy. Annual Review of Public Health. 2012; 33: 7–40.

[51] Moore JX, Chaudhary N, Akinyemiju T. Peer reviewed: Metabolic syndrome prevalence by race/ethnicity and sex in the United States, National Health and Nutrition Examination Sur-vey, 1988–2012. Preventing Chronic Disease. 2017; 14: 287–302.

[52] Lucado A, Fraher L, Patel H, Munck G. Comparison of portable handheld versus fixed isokinetic dynamometers in measuring strength of the wrist and forearm. Physiotherapy Theory and Practice. 2019; 35: 677–685.

[53] Wong P, Chan E, Ng D, Kwok K, Yip A, Leung S. Corre-lation between 6-min walk test and cardiopulmonary exercise test in Chinese patients. Pediatric Respirology and Critical Care Medicine. 2018; 2: 32.

[54] Stark T, Walker B, Phillips JK, Fejer R, Beck R. Hand-held Dy-namometry Correlation with the Gold Standard Isokinetic Dy-namometry: a Systematic Review. PM&R Journal. 2011; 3: 472–479.

[55] Paley CA, Johnson MI. Abdominal obesity and metabolic syn-drome: exercise as medicine? BMC Sports Science, Medicine and Rehabilitation. 2018; 10: 7.

[56] Lee S, Shin Y, Kim Y. Risk of metabolic syndrome among middle-aged Koreans from rural and urban areas. Nutrients. 2018; 10: 859–873.

[57] Park JH, Cho KK, Kim YH. Low 6-minute walk distance and muscle mass predict drop out in cardiac rehabilitation. Health-care. 2020; 8: 430–439.