Abstract
To our knowledge, no comprehensive meta-analysis has examined the association between sarcopenia and the risk of fractures. This systematic review and meta-analysis of prospective cohort studies aims to summarize whether sarcopenia is a risk factor for fractures among community-dwelling older adults. We searched four electronic literature databases (Ovid MEDLINE, EMBASE, Cochrane Central Register of Controlled Trials, PubMed) for relevant publications from inception to December 2017, using relevant keywords. We conducted a pooled analysis of the association between sarcopenia and the risk of fractures by employing a random-effects model. Subgroup analyses were conducted based on definitions of sarcopenia and gender. In total, nine studies were included in our systematic review and meta-analysis. The prevalence of sarcopenia ranged from 4.3 to 33.1%. The pooled RR of fractures for the sarcopenic versus the nonsarcopenic was 1.34 (95% CI = 1.13–1.58, P = 0.001, I2 = 5.5%, P-heterogeneity = 0.391). Subgroup analyses showed that associations between sarcopenia and fractures were significant when using the AWGS definition (combined effect size = 1.78, 95% CI = 1.25–2.54, P = 0.001), and studies in males (combined effect size = 1.39, 95% CI = 1.13–1.71, P = 0.002). In conclusion, we found that compared to nonsarcopenic, the association between sarcopenia and fractures among community-dwelling older people was significant when using the AWGS definition, and only for males. Future studies are needed to establish a possible association between sarcopenia definitions and risk of fractures of different sites.
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Rivas A, Romero A, Mariscal-Arcas M, Monteagudo C, Feriche B, Lorenzo ML, Olea F (2013) Mediterranean diet and bone mineral density in two age groups of women. Int J Food Sci Nutr 64(2):155–161. https://doi.org/10.3109/09637486.2012.718743
Siris ES, Brenneman SK, Barrett-Connor E, Miller PD, Sajjan S, Berger ML, Chen YT (2006) The effect of age and bone mineral density on the absolute, excess, and relative risk of fracture in postmenopausal women aged 50-99: results from the National Osteoporosis Risk Assessment (NORA). Osteoporos Int 17(4):565–574. https://doi.org/10.1007/s00198-005-0027-4
Anker SD, Coats AJ, Morley JE, Rosano G, Bernabei R, von Haehling S, Kalantar-Zadeh K (2014) Muscle wasting disease: a proposal for a new disease classification. J Cachexia Sarcopenia Muscle 5(1):1–3. https://doi.org/10.1007/s13539-014-0135-0
Cao L, Morley JE (2016) Sarcopenia is recognized as an independent condition by an International Classification of Disease, Tenth Revision, Clinical Modification (ICD-10-CM) code. J Am Med Dir Assoc 17(8):675–677. https://doi.org/10.1016/j.jamda.2016.06.001
Newman AB, Kupelian V, Visser M, Simonsick E, Goodpaster B, Nevitt M, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB (2003) Sarcopenia: alternative definitions and associations with lower extremity function. J Am Geriatr Soc 51(11):1602–1609. https://doi.org/10.1046/j.1532-5415.2003.51534.x
Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinkova E, Vandewoude M, Zamboni M (2010) Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing 39(4):412–423. https://doi.org/10.1093/ageing/afq034
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
Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, Abellan van Kan G, Andrieu S, Bauer J, Breuille D, Cederholm T, Chandler J, De Meynard C, Donini L, Harris T, Kannt A, Keime Guibert F, Onder G, Papanicolaou D, Rolland Y, Rooks D, Sieber C, Souhami E, Verlaan S, Zamboni M (2011) Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc 12(4):249–256. https://doi.org/10.1016/j.jamda.2011.01.003
Dam TT, Peters KW, Fragala M, Cawthon PM, Harris TB, McLean R, Shardell M, Alley DE, Kenny A, Ferrucci L, Guralnik J, Kiel DP, Kritchevsky S, Vassileva MT, Studenski S (2014) An evidence-based comparison of operational criteria for the presence of sarcopenia. J Gerontol A Biol Sci Med Sci 69(5):584–590. https://doi.org/10.1093/gerona/glu013
Woo J, Arai H, Ng TP, Sayer AA, Wong M, Syddall H, Yamada M, Zeng P, Wu S, Zhang TM (2014) Ethnic and geographic variations in muscle mass, muscle strength and physical performance measures. Eur Geriatr Med 5(3):155–164. https://doi.org/10.1016/j.eurger.2014.04.003
Beaudart C, Reginster JY, Petermans J, Gillain S, Quabron A, Locquet M, Slomian J, Buckinx F, Bruyere O (2015) Quality of life and physical components linked to sarcopenia: the SarcoPhAge study. Exp Gerontol 69:103–110. https://doi.org/10.1016/j.exger.2015.05.003
Manrique-Espinoza B, Salinas-Rodriguez A, Rosas-Carrasco O, Gutierrez-Robledo LM, Avila-Funes JA (2017) Sarcopenia is associated with physical and mental components of health-related quality of life in older adults. J Am Medl Dir Assoc 18(7):636.e631–636.e635. https://doi.org/10.1016/j.jamda.2017.04.005
Kelley GA, Kelley KS (2017) Is sarcopenia associated with an increased risk of all-cause mortality and functional disability? Exp Gerontol 96:100–103. https://doi.org/10.1016/j.exger.2017.06.008
Eguchi Y, Suzuki M, Yamanaka H, Tamai H, Kobayashi T, Orita S, Yamauchi K, Suzuki M, Inage K, Fujimoto K, Kanamoto H, Abe K, Aoki Y, Toyone T, Ozawa T, Takahashi K, Ohtori S (2017) Associations between sarcopenia and degenerative lumbar scoliosis in older women. Scoliosis Spinal Disord 12:9. https://doi.org/10.1186/s13013-017-0116-0
Bianchi L, Ferrucci L, Cherubini A, Maggio M, Bandinelli S, Savino E, Brombo G, Zuliani G, Guralnik JM, Landi F, Volpato S (2016) The predictive value of the EWGSOP definition of sarcopenia: results from the InCHIANTI study. J Gerontol A Biol Sci Med Sci 71(2):259–264. https://doi.org/10.1093/gerona/glv129
Liu P, Hao Q, Hai S, Wang H, Cao L, Dong B (2017) Sarcopenia as a predictor of all-cause mortality among community-dwelling older people: a systematic review and meta-analysis. Maturitas 103:16–22. https://doi.org/10.1016/j.maturitas.2017.04.007
Yu R, Leung J, Woo J (2014) Incremental predictive value of sarcopenia for incident fracture in an elderly Chinese cohort: results from the Osteoporotic Fractures in Men (MrOs) Study. J Am Med Dir Assoc 15(8):551–558. https://doi.org/10.1016/j.jamda.2014.02.005
Hars M, Biver E, Chevalley T, Herrmann F, Rizzoli R, Ferrari S, Trombetti A (2016) Low lean mass predicts incident fractures independently from FRAX: a prospective cohort study of recent retirees. J Bone Miner Res 31(11):2048–2056. https://doi.org/10.1002/jbmr.2878
Hong W, Cheng Q, Zhu X, Zhu H, Li H, Zhang X, Zheng S, Du Y, Tang W, Xue S, Ye Z (2015) Prevalence of sarcopenia and its relationship with sites of fragility fractures in elderly Chinese men and women. PLoS One 10(9):e0138102. https://doi.org/10.1371/journal.pone.0138102
Hida T, Shimokata H, Sakai Y, Ito S, Matsui Y, Takemura M, Kasai T, Ishiguro N, Harada A (2016) Sarcopenia and sarcopenic leg as potential risk factors for acute osteoporotic vertebral fracture among older women. Eur Spine J 25(11):3424–3431. https://doi.org/10.1007/s00586-015-3805-5
Clynes MA, Edwards MH, Buehring B, Dennison EM, Binkley N, Cooper C (2015) Definitions of sarcopenia: associations with previous falls and fracture in a population sample. Calcif Tissue Int 97(5):445–452. https://doi.org/10.1007/s00223-015-0044-z
Cawthon PM, Blackwell TL, Cauley J, Kado DM, Barrett-Connor E, Lee CG, Hoffman AR, Nevitt M, Stefanick ML, Lane NE, Ensrud KE, Cummings SR, Orwoll ES (2015) Evaluation of the usefulness of consensus definitions of sarcopenia in older men: results from the Observational Osteoporotic Fractures in Men Cohort Study. J Am Geriatr Soc 63(11):2247–2259. https://doi.org/10.1111/jgs.13788
Chalhoub D, Cawthon PM, Ensrud KE, Stefanick ML, Kado DM, Boudreau R, Greenspan S, Newman AB, Zmuda J, Orwoll ES, Cauley JA (2015) Risk of nonspine fractures in older adults with sarcopenia, low bone mass, or both. J Am Geriatr Soc 63(9):1733–1740. https://doi.org/10.1111/jgs.13605
Yu R, Leung J, Woo J (2014) Sarcopenia combined with FRAX probabilities improves fracture risk prediction in older Chinese men. J Am Med Dir Assoc 15(12):918–923. https://doi.org/10.1016/j.jamda.2014.07.011
Oliveira A, Vaz C (2015) The role of sarcopenia in the risk of osteoporotic hip fracture. Clin Rheumatol 34(10):1673–1680. https://doi.org/10.1007/s10067-015-2943-9
Beaudart C, Zaaria M, Pasleau F, Reginster JY, Bruyere O (2017) Health outcomes of sarcopenia: a systematic review and meta-analysis. PLoS One 12(1):e0169548. https://doi.org/10.1371/journal.pone.0169548
Moher D, Liberati A, Tetzlaff J, Altman DG (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg (London, England) 8(5):336–341. https://doi.org/10.1016/j.ijsu.2010.02.007
Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25(9):603–605. https://doi.org/10.1007/s10654-010-9491-z
Sadeghi O, Saneei P, Nasiri M, Larijani B, Esmaillzadeh A (2017) Abdominal obesity and risk of hip fracture: a systematic review and meta-analysis of prospective studies. Adv Nutr (Bethesda, Md) 8(5):728–738. https://doi.org/10.3945/an.117.015545
Zhang J, Yu KF (1998) What's the relative risk? A method of correcting the odds ratio in cohort studies of common outcomes. JAMA 280(19):1690–1691. https://doi.org/10.1001/jama.280.19.1690
Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. Bmj 327(7414):557–560. https://doi.org/10.1136/bmj.327.7414.557
Chang KV, Hsu TH, Wu WT, Huang KC, Han DS (2017) Is sarcopenia associated with depression? A systematic review and meta-analysis of observational studies. Age Ageing 46(5):738–746. https://doi.org/10.1093/ageing/afx094
Balogun S, Winzenberg T, Wills K, Scott D, Jones G, Aitken D, Callisaya ML (2017) Prospective associations of low muscle mass and function with 10-year falls risk, incident fracture and mortality in community-dwelling older adults. J Nutr Health Aging 21(7):843–848. https://doi.org/10.1007/s12603-016-0843-6
Harris R, Chang Y, Beavers K, Laddu-Patel D (2017) Risk of fracture in women with sarcopenia, low bone mass, or both. https://doi.org/10.1111/jgs.15050
Scott D, Seibel M, Cumming R, Naganathan V, Blyth F, Le Couteur DG, Handelsman DJ, Waite LM, Hirani V (2017) Sarcopenic obesity and its temporal associations with changes in bone mineral density, incident falls, and fractures in older men: the Concord Health and Ageing in Men Project. J Bone Miner Res 32(3):575–583. https://doi.org/10.1002/jbmr.3016
Schaap LA, van Schoor NM, Lips P, Visser M (2017) Associations of sarcopenia definitions, and their components, with the incidence of recurrent falling and fractures; the Longitudinal Aging Study Amsterdam. J Gerontol A Biol Sci Med Sci. https://doi.org/10.1093/gerona/glx245
Scott D, Chandrasekara SD, Laslett LL, Cicuttini F, Ebeling PR, Jones G (2016) Associations of sarcopenic obesity and dynapenic obesity with bone mineral density and incident fractures over 5-10 years in community-dwelling older adults. Calcif Tissue Int 99(1):30–42. https://doi.org/10.1007/s00223-016-0123-9
Kawao N, Kaji H (2015) Interactions between muscle tissues and bone metabolism. J Cell Biochem 116(5):687–695. https://doi.org/10.1002/jcb.25040
Ormsbee MJ, Prado CM, Ilich JZ, Purcell S, Siervo M, Folsom A, Panton L (2014) Osteosarcopenic obesity: the role of bone, muscle, and fat on health. J Cachexia Sarcopenia Muscle 5(3):183–192. https://doi.org/10.1007/s13539-014-0146-x
Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, Simonsick EM, Tylavsky FA, Visser M, Newman AB (2006) 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 61(10):1059–1064. https://doi.org/10.1093/gerona/61.10.1059
Janssen I, Heymsfield SB, Wang ZM, Ross R (2000) Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol (Bethesda, Md : 1985) 89(1):81–88. https://doi.org/10.1152/jappl.2000.89.1.81
LeBlanc ES, Wang PY, Lee CG, Barrett-Connor E, Cauley JA, Hoffman AR, Laughlin GA, Marshall LM, Orwoll ES (2011) Higher testosterone levels are associated with less loss of lean body mass in older men. J Clin Endocrinol Metab 96(12):3855–3863. https://doi.org/10.1210/jc.2011-0312
Mouser JG, Loprinzi PD, Loenneke JP (2016) The association between physiologic testosterone levels, lean mass, and fat mass in a nationally representative sample of men in the United States. Steroids 115:62–66. https://doi.org/10.1016/j.steroids.2016.08.009
Feldman HA, Longcope C, Derby CA, Johannes CB, Araujo AB, Coviello AD, Bremner WJ, McKinlay JB (2002) Age trends in the level of serum testosterone and other hormones in middle-aged men: longitudinal results from the Massachusetts male aging study. J Clin Endocrinol Metab 87(2):589–598. https://doi.org/10.1210/jcem.87.2.8201
Cruz-Jentoft AJ, Landi F, Schneider SM, Zuniga C, Arai H, Boirie Y, Chen LK, Fielding RA, Martin FC, Michel JP, Sieber C, Stout JR, Studenski SA, Vellas B, Woo J, Zamboni M, Cederholm T (2014) Prevalence of and interventions for sarcopenia in ageing adults: a systematic review. Report of the international sarcopenia initiative (EWGSOP and IWGS). Age Ageing 43(6):748–759. https://doi.org/10.1093/ageing/afu115
Acknowledgements
The authors thank the staff of the Department of Geriatrics Medicine, West China Hospital, for their guidance and support. We also thank Professor Xiangfa Zeng, from Chengdu Medical College, for helping with language editing.
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Zhang, Y., Hao, Q., Ge, M. et al. Association of sarcopenia and fractures in community-dwelling older adults: a systematic review and meta-analysis of cohort studies. Osteoporos Int 29, 1253–1262 (2018). https://doi.org/10.1007/s00198-018-4429-5
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DOI: https://doi.org/10.1007/s00198-018-4429-5