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Exp Clin Endocrinol Diabetes 2022; 130(08): 546-553
DOI: 10.1055/a-1785-3729
Article

Hyperuricemia Associated with Low Skeletal Muscle in the Middle-Aged and Elderly Population in China

Lingyan Chen
1   Department of Geriatrics, Zhongshan Hospital, Fudan University, Fenglin Road, Shanghai, China
,
Li Wu
2   Fudan Institute for Metabolic Diseases, Fenglin Road, Shanghai, China
,
Qian Li
2   Fudan Institute for Metabolic Diseases, Fenglin Road, Shanghai, China
,
Yu Hu
1   Department of Geriatrics, Zhongshan Hospital, Fudan University, Fenglin Road, Shanghai, China
,
Hui Ma
1   Department of Geriatrics, Zhongshan Hospital, Fudan University, Fenglin Road, Shanghai, China
,
Huandong Lin
2   Fudan Institute for Metabolic Diseases, Fenglin Road, Shanghai, China
3   Department of Endocrinology and Metabolism, Zhongshan Hospital, Fudan University, Fenglin Road, Shanghai, China
,
Xin Gao
2   Fudan Institute for Metabolic Diseases, Fenglin Road, Shanghai, China
3   Department of Endocrinology and Metabolism, Zhongshan Hospital, Fudan University, Fenglin Road, Shanghai, China
› Author Affiliations Funding The research was supported by the National Key Basic Research Program of China (Grant No. 2012CB524906 to Gao X and Grant No. 2011CB504004 to Gao X), the Shanghai Municipal Health Bureau Foundation (Grant No.12GWZX0103 to Gao X), the Shanghai Municipal Science and Technology Major Project (2017SHZDZX01 to Gao X), the key basic research grants from Science and Technology Commission of Shanghai Municipality (grant number 16JC1400500 and 16411954800to Gao X).
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Abstract

Background Previous studies have presented inconsistent results on the relationship between serum uric acid and skeletal muscle mass (SMM). We aimed to explore whether a higher serum uric acid level was associated with low SMM in the Chinese population.

Methods We performed a cross-sectional analysis of 6595 subjects aged 45 years or older. They were tested for fasting blood glucose, total cholesterol, triglycerides, high-density lipoprotein-cholesterol, low-density lipoprotein-cholesterol, uric acid, blood urea nitrogen, creatinine, and estimated glomerular filtration rate. SMM was accessed by dual-energy x-ray absorptiometry using two approaches: weight-adjusted appendicular skeletal muscle mass (ASM)% and ASM/BMI (body mass index (kg/m2)). Low SMM was defined as a cut-off point of ASM/BMI<0.789 for men and<0.512 for women.

Results Compared with their normal group, patients with hyperuricemia had lower ASM% (29.33±2.33 vs 30.03±2.34 for males and 24.71±1.99 vs 25.19±2.07 for females, P<0.01) and ASM/BMI (0.83±0.10 vs 0.85±0.10 for male and 0.60±0.07 vs 0.62±0.07 for female), with a higher prevalence of the associated low SMM in both sexes (35.2 vs 26.5% for male and 10.5 vs 5.9% for female, P<0.01). Pearson analysis showed that ASM% and ASM/BMI were negatively correlated with SUA (male: ASM/BMI, r=−0.097, ASM%, r=−0.146; female: ASM/BMI, r=−0.151, ASM%, r=−0.157; all P<0.001). Logistic regression analysis showed a positive association of hyperuricemia with adjusted risk of low SMM association.

Conclusions In a middle-aged and elderly Chinese population, hyperuricemia is independently and positively associated with low SMM and can vary by age and gender.

Key words

uric acid - skeletal muscle mass - middle-aged and elderly community people - sarcopenia


Publication History

Received: 16 September 2021
Received: 06 January 2022

Accepted: 11 February 2022

Article published online:
24 May 2022

© 2022. Thieme. All rights reserved.

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  • References

  • 1 Baumgartner RN, Koehler KM, Gallagher D. et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 1988; 147: 755-763
    CrossrefPubMedGoogle Scholar
  • 2 Landi F, Cruz-Jentoft AJ, Liperoti R. et al. Sarcopenia and mortality risk in frail older persons aged 80 years and older: Results from iISIRENTE study. Age Aging 2013; 42: 203-209
    CrossrefPubMedGoogle Scholar
  • 3 Kim H, Hirano H, Edahiro A. et al. Sarcopenia: pPevalence and associated factors based on different suggested definitions in community-dwelling older adults. Geriatr Gerontol Int 2016; 16: 110-122
    CrossrefPubMedGoogle Scholar
  • 4 Yalcin A, Aras S, Atmis V. et al. Sarcopenia and mortality in older people living in a nursing home in Turkey. Geriatr Gerontol Int 2017; 17: 1118-1124
    CrossrefPubMedGoogle Scholar
  • 5 Beaudart C, Zaaria M, Pasleau F. et al. Health outcomes of Sarcopenia: A systematic review and meta-analysis. PLoS One 2017; 12: e0169548
    CrossrefPubMedGoogle Scholar
  • 6 Rygiel KA, Picard M, Turnbull DM. The ageing neuromuscular system and sarcopenia: A mitochondrial perspective. J Physiol 2016; 594: 4499-4512
    CrossrefPubMedGoogle Scholar
  • 7 Ames BN, Cathcart R, Schwiers E. et al. Uric acid provides an antioxidant defence in humans against oxidant-and radical-caused aging and cancer: A hypothesis. Proc Natl Acad Sci USA 1981; 78: 6858-6862
    CrossrefPubMedGoogle Scholar
  • 8 Sevanian A, Davies KJA, Hochstein P. Serum urate as an antioxidant for ascorbic acid. Am J Clin Nutr 1991; 54: 1129S-1134S
    CrossrefPubMedGoogle Scholar
  • 9 Yoo TW, Sung KC, Shin HS. et al. Relationship between serum uric acid concentration and insulin resistance and metabolic syndrome. Circ J 2005; 69: 928-933
    CrossrefPubMedGoogle Scholar
  • 10 Alcaino H, Greig D, Chiong M. et al. Serum uric acid correlates with extracellular superoxide dismutase activity in patients with chronic heart failure. Eur J Heart Fail 2008; 10: 646-651
    CrossrefPubMedGoogle Scholar
  • 11 Grayson PC, Kim SY, LaValley M. et al. Hyperuricemia and incident hypertension: A systematic review and meta-analysis. Arthritis Care Res (Hoboken) 2011; 63: 102-110
    CrossrefPubMedGoogle Scholar
  • 12 Lippi G, Montagnana M, Franchini M. et al. The paradoxical relationship between serum uric acid and cardiovascular disease. Clinica Chimica Acta 2008; 392: 1-7
    CrossrefPubMedGoogle Scholar
  • 13 Molino-Lova R, Sofi F, Pasquini G. et al. Higher uric acid serum levels are associated with better muscle function in the oldest old: Results from the Mugello Study. Eur J Intern Med 2017; 41: 39-43
    CrossrefPubMedGoogle Scholar
  • 14 Macchi C, Molino-Lova R, Polcaro P. et al. Higher circulating levels of uric acid are prospectively associated with better muscle function in older persons. Mech Ageing Dev 2008; 129: 522-527
    PubMedGoogle Scholar
  • 15 Kawamoto R, Ninomiya D, Kasai Y. et al. Serum uric acid is positively associated with hand grip strength among Japanese community-dwelling elderly women. PLoS One 2016; 11: e0151044
    CrossrefPubMedGoogle Scholar
  • 16 Dong XW, Tian HY, He J. et al. Elevated serum uric acid is associated with greater bone mineral density and skeletal muscle mass in middle-aged and older adults. PLoS One 2016; 11: e0154692
    CrossrefPubMedGoogle Scholar
  • 17 Garcia-Esquinas E, Guallar-Castallon P, Carnicero JA. et al. Serum uric acid concentrations and risk of frailty in older adults. Exp Gerontol 2016; 82: 160-165
    CrossrefPubMedGoogle Scholar
  • 18 Huang C, Niu K, Kobayashi Y. et al. An inverted J-shaped association of serum uric acid with muscle strength among Japanese adult men: A cross-sectional study. BMC Musculoskelet Disord 2013; 14: 258
    CrossrefPubMedGoogle Scholar
  • 19 Kim YS, Lee Y, Chung YS. et al. Prevalence of sarcopenia and sarcopenic obesity in the Korean population based on the Fourth Korean National Health and Nutritional Examination Surveys. J Gerontol Biol Sci Med Sci 2012; 67: 1107-1113
    CrossrefPubMedGoogle Scholar
  • 20 Tang TC, Hwang AC, Liu LK. et al. FNIH-defined sarcopenia predicts adverse outcomes among community-dwelling older people in Taiwan: Results from I-Lan longitudinal aging study. J Gerontol Biol Sci Med Sci 2018; 73: 828-834
    CrossrefPubMedGoogle Scholar
  • 21 Cawthon PM, Peters KW, Shardell MD. 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
    CrossrefPubMedGoogle Scholar
  • 22 Gallagher D, Visser M, De Meersman RE. et al. Appendicular skeletal muscle mass: Effects of age, gender, and ethnicity. J Appl Physiol (1985) 1997; 83: 229-239
    CrossrefPubMedGoogle Scholar
  • 23 Alley DE, Shardell M, Peters KW. et al. Grip strength cutpoints for the identification of clinically relevant weakness. J Gerontol A Biol Sci Med Sci 2014; 5: 559-566
    CrossrefPubMedGoogle Scholar
  • 24 Gao X, Hofman A, Hu Y. et al. The Shanghai Changfeng Study: A community-based prospective cohort study of chronic diseases among middle-aged and elderly: Objectives and design. Eur J Epidemiol 2010; 25: 885-893
    CrossrefPubMedGoogle Scholar
  • 25 Lin H, Li Q, Hu Y. et al. The prevalence of multiple non-communicable diseases among middle-aged and elderly people: The Shanghai Changfeng Study. Eur J Epidemiol 2017; 32: 159-163
    CrossrefPubMedGoogle Scholar
  • 26 Levey AS, Bosch JP, Lewis JB. et al. A more accurate method to estimate glomerular filtration rate from serum creatinine: A new prediction equation. Modification of Diet in Renal Disease Study Group. Ann Intern Med 1999; 130: 461-470
    CrossrefPubMedGoogle Scholar
  • 27 Wu YF, Ma GS, Hu YH. et al. The current prevalence status of body overweight and obesity in China data from the China National Nutrition and Health Survey. Zhonghua Yu Fang Yi Xue Za Zhi 2005; 39: 316-320
    PubMedGoogle Scholar
  • 28 World Health Organization. Department of Noncommunicable Disease Surveillance. Definition, Diagnosis and Classification of Diabetes Mellitus and Its Complications: Report of a WHO Consultation. Geneva: World Health Org; 1999
    Google Scholar
  • 29 Chobanian AV, Bakris GL, Black HR. et al. Seventh report of the Joint National Committee on prevention, detection, evaluation, and treatment of high blood pressure. Hypertension 2003; 42: 1206-1252
    CrossrefPubMedGoogle Scholar
  • 30 Studenski SA, Peters KW, Alley DE. et al. The FNIH Sarcopenia Project: Rationale, study description, conference recommendations, and final estimates. J Gerontol Biol Sci Med Sci 2014; 69: 547-558
    CrossrefPubMedGoogle Scholar
  • 31 Bouchard DR, Heroux M, Janssen I. Association between muscle mass, leg strength, and fat mass with physical function in older adults: influence of age and sex. J Aging Health 2011; 23: 313-328
    CrossrefPubMedGoogle Scholar
  • 32 Tanimoto Y, Watanabe M, Sun W. et al. Sarcopenia and falls in community-dwelling elderly subjects in Japan: Defining sarcopenia according to criteria of the European Working Group on Sarcopenia in Older People. Arch Gerontol Geriatr 2014; 59: 295-299
    CrossrefPubMedGoogle Scholar
  • 33 Moon JH, Choo SR, Kim JS. Relationship between low muscle mass and metabolic syndrome in elderly people with normal body mass index. J Bone Metab 2015; 22: 99-106
    CrossrefPubMedGoogle Scholar
  • 34 Moon SJ, Kim TH, Yoon SY. et al. Relationship between stage of chronic kidney disease and sarcopenia in Korean aged 40 years and older using the Korea National Health and Nutrition Examination Surveys (KNHANES IV-2, 3, and V-1, 2), 2008–2011. PLoS One 2015; 10: 1-11
    CrossrefPubMedGoogle Scholar
  • 35 He H, Liu Y, Tian Q. et al. Relationship of sarcopenia and body composition with osteoporosis. Osteoporos Int 2016; 27: 473-482
    CrossrefPubMedGoogle Scholar
  • 36 Lee YH, Kim SU, Song K. et al. Sarcopenia is associated with significant liver fibrosis independently of obesity and insulin resistance in nonalcoholic fatty liver disease: Nationwide surveys (KNHANES 2008–2011). Hepatology 2016; 63: 776-786
    CrossrefPubMedGoogle Scholar
  • 37 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
    CrossrefPubMedGoogle Scholar
  • 38 Lo YC, Wahlqvist ML, Huang YC. et al. Medical costs of a low SMM are modulated by dietary diversity and physical activity in community-dwelling older Taiwanese: A longitudinal study. Int J Behav Nutr Phys Act 2017; 14: 31
    CrossrefPubMedGoogle Scholar
  • 39 Beavers KM, Beavers DP, Serra MC. et al. Low relative skeletal muscle mass indicative of sarcopenia is associated with elevations in serum uric acid levels: Findings from NHANES III. J Nutr Health Aging 2009; 13: 177-182
    CrossrefPubMedGoogle Scholar
  • 40 Beberashvili I, Sinuani I, Azar A. et al. Serum uric acid as a clinically useful nutritional marker and predictor of outcome in maintenance hemodialysis patients. Nutrition 2015; 31: 138-147
    CrossrefPubMedGoogle Scholar
  • 41 Tanaka KI, Kanazawa I, Notsu M. et al. Higher serum uric acid was a risk factor of reduced muscle mass in men with type 2 DM. Exp Clin Endocrinol Diabetes 2021; 129: 50-55
    Article in Thieme ConnectPubMedGoogle Scholar
  • 42 Macchia C, Molino-Lovaa R, Polcaroa P. et al. Higher circulating levels of uric acid are prospectively associated with better muscle function in older persons. Mech Ageing Dev 2008; 129: 522-527
    CrossrefPubMedGoogle Scholar
  • 43 Liu DM, Jiang LD, Gan L. et al. Association between serum uric acid level and body mass index in sex- and age-sepcific groups in southwestern China. Endocr Pract 2019; 25: 438-445
    CrossrefPubMedGoogle Scholar
  • 44 Nascimento DDC, Oliveira SDC, Vieira DCL. et al. The impact of sarcopenic obesity on inflammation, lean body mass, and muscle strength in elderly women. Int J Gen Med 2018; 11: 443-449
    CrossrefPubMedGoogle Scholar
  • 45 Hamdy O, Porramatikul S, Al-Ozairi E. Metabolic obesity: The paradox between visceral and subcutaneous fat. Curr Diabetes Rev 2006; 2: 367-373
    CrossrefPubMedGoogle Scholar
  • 46 Rao M, Jaber BL, Balakrishnan VS. Chronic kidney disease and acquired mitochondrial myopathy. Curr Opin Nephrol Hypertens 2018; 27: 113-120
    CrossrefPubMedGoogle Scholar
  • 47 Zhou X, Matavelli L, Frohlich ED. Uric acid: Its relationship to renal hemodynamics and the renal renin-angiotensin system. Curr Hypertens Rep 2006; 8: 120-124
    CrossrefPubMedGoogle Scholar
  • 48 Storhaug HM, Norvik JV, Toft I. et al. Uric acid is a risk factor for ischemic stroke and all-cause mortality in the general population: a gender specific analysis from The Tromsø Study. BMC Cardiovasc Disord 2013; 13: 115
    CrossrefPubMedGoogle Scholar
  • 49 Chen JH, Yeh WT, Chuang SY. et al. Gender-specific risk factors for incident gout: A prospective cohort study. Clin Rheumatol 2012; 31: 239-245
    CrossrefPubMedGoogle Scholar