Abstract
Both ethnicity and age are important determinants of musculoskeletal health. We aimed to determine the prevalence of sarcopenia, assess the suitability of current diagnostic guidelines, and explore muscle-bone relationships in adults from India. A total of 1009 young (20–35 years) and 1755 older (> 40 years) men and women from existing studies were collated and pooled for the analysis. Dual-energy x-ray absorptiometry measured areal bone mineral density (aBMD) at the hip and spine, and fat and lean mass; hand dynamometer measured hand grip strength (HGS). Indian-specific cut-points for appendicular lean mass (ALM), ALM index (ALMI) and HGS were calculated from young Indian (-2SD mean) populations. Sarcopenia was defined using cut-points from The Foundations for the National Institutes of Health (FNIH), revised European Working Group on Sarcopenia in Older People (EWGSOP2), Asian Working Group for Sarcopenia (AWGS), and Indian-specific cut-points. Low lean mass cut-points were then compared for their predictive ability in identifying low HGS. The relationship between muscle variables (ALM, ALMI, HGS) and aBMD was explored, and sex differences were tested. Indian-specific cut-points (men-HGS:22.93 kg, ALM:15.41 kg, ALMI:6.03 kg/m2; women-HGS:10.76 kg, ALM:9.95 kg, ALMI:4.64 kg/m2) were lower than existing definitions. The Indian-specific definition had the lowest, while EWGSOP2 ALMI had the highest predictive ability in detecting low HGS (men:AUC = 0.686, women:AUC = 0.641). There were sex differences in associations between aBMD and all muscle variables, with greater positive associations in women than in men. The use of appropriate cut-points for diagnosing low lean mass and physical function is necessary in ethnic populations for accurate sarcopenia assessment. Muscle-bone relationships are more tightly coupled during ageing in Indian women than men.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Aboderin IAG, Beard JR (2015) Older people’s health in sub-Saharan Africa. Lancet 385(9968):e9–e11. https://doi.org/10.1016/S0140-6736(14)61602-0
Gregson CL, Cassim B, Micklesfield LK, Lukhele M, Ferrand RA, Ward KA, Group SCW (2019) Fragility fractures in sub-Saharan Africa: time to break the myth. Lancet Glob Health 7(1):e26–e27. https://doi.org/10.1016/S2214-109X(18)30412-1
Tollman SM, Norris SA, Berkman LF (2016) Commentary: the value of life course epidemiology in low- and middle-income countries: an ageing perspective. Int J Epidemiol 45(4):997–999. https://doi.org/10.1093/ije/dyw109
Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, Schneider SM, Sieber CC, Topinkova E, Vandewoude M, Visser M, Zamboni M, Writing Group for the European Working Group on Sarcopenia in Older P, the Extended Group for E (2019) Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 48(1):16–31. https://doi.org/10.1093/ageing/afy169
Studenski SA, Peters KW, Alley DE, Cawthon PM, McLean RR, Harris TB, Ferrucci L, Guralnik JM, Fragala MS, Kenny AM, Kiel DP, Kritchevsky SB, Shardell MD, Dam TT, Vassileva MT (2014) The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A 69(5):547–558. https://doi.org/10.1093/gerona/glu010
Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, Chou MY, Chen LY, Hsu PS, Krairit O, Lee JS, Lee WJ, Lee Y, Liang CK, Limpawattana P, Lin CS, Peng LN, Satake S, Suzuki T, Won CW, Wu CH, Wu SN, Zhang T, Zeng P, Akishita M, Arai H (2014) Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc 15(2):95–101. https://doi.org/10.1016/j.jamda.2013.11.025
Kruger HS, Micklesfield LK, Wright HH, Havemann-Nel L, Goedecke JH (2015) Ethnic-specific cut-points for sarcopenia: evidence from black South African women. Eur J Clin Nutr 69(7):843–849. https://doi.org/10.1038/ejcn.2014.279
Zengin A, Maple-Brown LJ, Brennan-Olsen S, Center JR, Eades S, Ebeling PR (2018) Musculoskeletal health of Indigenous Australians. Arch Osteoporos 13(1):77. https://doi.org/10.1007/s11657-018-0493-x
Zengin A, Prentice A, Ward KA (2015) Ethnic differences in bone health. Front Endocrinol. https://doi.org/10.3389/fendo.2015.00024
Shah AD, Kandula NR, Lin F, Allison MA, Carr J, Herrington D, Liu K, Kanaya AM (2015) Less favorable body composition and adipokines in South Asians compared with other US ethnic groups: results from the MASALA and MESA studies. Int J Obes 40:639. https://doi.org/10.1038/ijo.2015.219
Zengin A, Pye SR, Cook MJ, Adams JE, Wu FC, O’Neill TW, Ward KA (2016) Ethnic differences in bone geometry between White, Black and South Asian men in the UK. Bone 91:180–185. https://doi.org/10.1016/j.bone.2016.07.018
Forrest KY, Bunker CH, Sheu Y, Wheeler VW, Patrick AL, Zmuda JM (2012) Patterns and correlates of grip strength change with age in Afro-Caribbean men. Age Ageing 41(3):326–332. https://doi.org/10.1093/ageing/afs030
Metter EJ, Conwit R, Tobin J, Fozard JL (1997) Age-associated loss of power and strength in the upper extremities in women and men. J Gerontol A 52(5):B267-276
Yang PL, Lu Y, Khoo CM, Leow MK, Khoo EY, Teo A, Lee YS, De Das S, Chong YS, Gluckman PD, Tai ES, Venkataraman K, Ng CM (2013) Associations between ethnicity, body composition, and bone mineral density in a Southeast Asian population. J Clin Endocrinol Metab 98(11):4516–4523. https://doi.org/10.1210/jc.2013-2454
Ho-Pham LT, Nguyen UD, Nguyen TV (2014) Association between lean mass, fat mass, and bone mineral density: a meta-analysis. J Clin Endocrinol Metab 99(1):30–38. https://doi.org/10.1210/jc.2013-3190
Marwaha RK, Garg MK, Bhadra K, Mithal A, Tandon N (2014) Assessment of lean (muscle) mass and its distribution by dual energy X-ray absorptiometry in healthy Indian females. Arch Osteoporos 9:186. https://doi.org/10.1007/s11657-014-0186-z
Smith J, Majmundar M (2012) Aging in Asia: Findings from new and emerging data initiatives. In: Smith JP, Majmundar M (eds) National Research Council (US) panel on policy research and data needs to meet the challenge of aging in Asia. The National Academies Collection: reports funded by National Institutes of Health. National Academies Press (US), Washington (DC). https://doi.org/10.17226/13361
Bhargava SK, Sachdev HS, Fall CH, Osmond C, Lakshmy R, Barker DJ, Biswas SK, Ramji S, Prabhakaran D, Reddy KS (2004) Relation of serial changes in childhood body-mass index to impaired glucose tolerance in young adulthood. N Engl J Med 350(9):865–875. https://doi.org/10.1056/NEJMoa035698
Tandon N, Fall CH, Osmond C, Sachdev HP, Prabhakaran D, Ramakrishnan L, Dey Biswas SK, Ramji S, Khalil A, Gera T, Reddy KS, Barker DJ, Cooper C, Bhargava SK (2012) Growth from birth to adulthood and peak bone mass and density data from the New Delhi Birth Cohort. Osteoporos Int 23(10):2447–2459. https://doi.org/10.1007/s00198-011-1857-x
Kinra S, Radha Krishna KV, Kuper H, Rameshwar Sarma KV, Prabhakaran P, Gupta V, Walia GK, Bhogadi S, Kulkarni B, Kumar A, Aggarwal A, Gupta R, Prabhakaran D, Reddy KS, Smith GD, Ben-Shlomo Y, Ebrahim S (2014) Cohort profile: Andhra Pradesh Children and Parents Study (APCAPS). Int J Epidemiol 43(5):1417–1424. https://doi.org/10.1093/ije/dyt128
Ebrahim S, Kinra S, Bowen L, Andersen E, Ben-Shlomo Y, Lyngdoh T, Ramakrishnan L, Ahuja RC, Joshi P, Das SM, Mohan M, Davey Smith G, Prabhakaran D, Reddy KS, Indian Migration Study G (2010) The effect of rural-to-urban migration on obesity and diabetes in India: a cross-sectional study. PLoS Med 7(4):e1000268. https://doi.org/10.1371/journal.pmed.1000268
Lyngdoh T, Kinra S, Shlomo YB, Reddy S, Prabhakaran D, Smith GD, Ebrahim S, Indian Migration Study G (2006) Sib-recruitment for studying migration and its impact on obesity and diabetes. Emerg Themes Epidemiol 3:2. https://doi.org/10.1186/1742-7622-3-2
Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, Garry PJ, Lindeman RD (1998) Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147(8):755–763
Cole TJ (2000) Sympercents: symmetric percentage differences on the 100 log(e) scale simplify the presentation of log transformed data. Stat Med 19(22):3109–3125. https://doi.org/10.1002/1097-0258(20001130)19:22%3c3109::AID-SIM558%3e3.0.CO;2-F[pii]
Kim YS, Lee Y, Chung YS, Lee DJ, Joo NS, Hong D, Song G, Kim HJ, Choi YJ, Kim KM (2012) Prevalence of sarcopenia and sarcopenic obesity in the Korean population based on the Fourth Korean National Health and Nutritional Examination Surveys. J Gerontol A 67(10):1107–1113. https://doi.org/10.1093/gerona/gls071
Lau EM, Lynn HS, Woo JW, Kwok TC, Melton LJ 3rd (2005) Prevalence of and risk factors for sarcopenia in elderly Chinese men and women. J Gerontol A 60(2):213–216
Lee WJ, Liu LK, Peng LN, Lin MH, Chen LK, Group IR (2013) Comparisons of sarcopenia defined by IWGS and EWGSOP criteria among older people: results from the I-Lan longitudinal aging study. J Am Med Dir Assoc. https://doi.org/10.1016/j.jamda.2013.03.019
Zengin A, Jarjou LM, Prentice A, Cooper C, Ebeling PR, Ward KA (2018) The prevalence of sarcopenia and relationships between muscle and bone in ageing West-African Gambian men and women. J Cachexia Sarcopenia Muscle 9(5):920–928. https://doi.org/10.1002/jcsm.12341
Kim KM, Lim S, Oh TJ, Moon JH, Choi SH, Lim JY, Kim KW, Park KS, Jang HC (2017) Longitudinal changes in muscle mass and strength, and bone mass in older adults: gender-specific associations between muscle and bone losses. J Gerontol A 73(8):1062–1069. https://doi.org/10.1093/gerona/glx188
Ibrahim K, May C, Patel HP, Baxter M, Sayer AA, Roberts H (2016) A feasibility study of implementing grip strength measurement into routine hospital practice (GRImP): study protocol. Pilot Feasibility Stud 2:27. https://doi.org/10.1186/s40814-016-0067-x
Leong DP, Teo KK, Rangarajan S, Lopez-Jaramillo P, Avezum A Jr, Orlandini A, Seron P, Ahmed SH, Rosengren A, Kelishadi R, Rahman O, Swaminathan S, Iqbal R, Gupta R, Lear SA, Oguz A, Yusoff K, Zatonska K, Chifamba J, Igumbor E, Mohan V, Anjana RM, Gu H, Li W, Yusuf S, Prospective Urban Rural Epidemiology Study I (2015) Prognostic value of grip strength: findings from the Prospective Urban Rural Epidemiology (PURE) study. Lancet 386(9990):266–273. https://doi.org/10.1016/S0140-6736(14)62000-6
Perez-Sousa MA, Venegas-Sanabria LC, Chavarro-Carvajal DA, Cano-Gutierrez CA, Izquierdo M, Correa-Bautista JE, Ramirez-Velez R (2019) Gait speed as a mediator of the effect of sarcopenia on dependency in activities of daily living. J Cachexia Sarcopenia Muscle. https://doi.org/10.1002/jcsm.12444
Gunasekaran V, Banerjee J, Dwivedi SN, Upadhyay AD, Chatterjee P, Dey AB (2016) Normal gait speed, grip strength and thirty seconds chair stand test among older Indians. Arch Gerontol Geriatr 67:171–178. https://doi.org/10.1016/j.archger.2016.08.003
Kallman DA, Plato CC, Tobin JD (1990) The role of muscle loss in the age-related decline of grip strength: cross-sectional and longitudinal perspectives. J Gerontol 45(3):M82-88
Shepherd JA, Schousboe JT, Broy SB, Engelke K, Leslie WD (2015) Executive SUMMARY of the 2015 ISCD position development conference on advanced measures from DXA and QCT: fracture prediction beyond BMD. J Clin Densitom 18(3):274–286. https://doi.org/10.1016/j.jocd.2015.06.013
Funding
This work was supported by the Australian Academy of Sciences, Australia-India Early and Mid-Career Fellowships (AZ). The third survey wave of APCAPS was funded by Wellcome Trust Strategic Award (084774). IMS was funded by the Wellcome Trust project Grant (GR070797MF). NDBC was funded by the Indian Council of Medical Research, British Heart Foundation, the Wellcome Trust UK, the Medical Research Council UK, the National Institute for Health Research Nutrition and Metabolism Biomedical Research Unit, University of Southampton and the National Institute for Health Research Musculoskeletal Biomedical Research Unit, University of Oxford.
Author information
Authors and Affiliations
Contributions
AZ, BK, AVK, NK, VE, NT, SKB, HSS, SS, SK, CHDF and PRE designed and conducted the study; AZ, BK, NK, SS, DS and PRE analysed the data; AZ, BK, AVK, NK, VE, NT, SKB, HSS, SS, SK, DS, CHDF and PRE interpreted the data; AZ, BK, AVK, NK, VE, NT, SKB, HSS, SS, SK, DS, CHDF and PRE prepared the manuscript and are responsible for the final content. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Disclosure
All authors declare that they have no conflicts of interest.
Ethical Approval
All studies received ethics approval, please see Methods for further details.
Human and Animal Rights and Informed Consent
Informed consent was obtained from all individual participants included in the study. All studies were performed in line with the principles of the Declaration of Helsinki. Approval was granted by Ethics Committees for each study, further details can be found in the Study Design, containing details on each study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zengin, A., Kulkarni, B., Khadilkar, A.V. et al. Prevalence of Sarcopenia and Relationships Between Muscle and Bone in Indian Men and Women. Calcif Tissue Int 109, 423–433 (2021). https://doi.org/10.1007/s00223-021-00860-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00223-021-00860-1