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The relationship between sarcopenia and fragility fracture—a systematic review

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Summary

Sarcopenia is a common geriatric syndrome characterized by progressive decrease of muscle mass and function leading to an increased risk of physical disability, poor quality of life, and mortality. Increasing evidence shows that sarcopenia is related with fragility fractures. This systematic review aimed to summarize the following: (1) the prevalence of sarcopenia in patients with fragility fracture and (2) the associated risk factors for fragility fracture in patients with sarcopenia. Literature search was conducted in PubMed and Cochrane databases. Studies with the prevalence of sarcopenia in elderly patients with fragility fracture and associated risk factors in patients with sarcopenia were included. A total of 15 papers were included, with 10 reporting sarcopenia prevalence, and 5 on fracture risk in patients with sarcopenia. The prevalence of sarcopenia after fracture ranged from 12.4 to 95% in males and 18.3 to 64% in females. The prevalence of sarcopenia in elderly patients with fragility fracture was high, especially in men. Two studies showed that sarcopenia was a risk factor for fragility fracture when associated with low bone mineral density (BMD) but only in men. Caution should be taken for male patients with sarcopenia and low BMD, which is related to significantly increased risk of fractures. There is a pressing need for further research on sarcopenia and its risk on fragility fracture to better understand the relationship, pathophysiology, and mechanisms, which may shed light on potential interventions to improve clinical outcomes.

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References

  1. 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 89:81–88

    Article  CAS  PubMed  Google Scholar 

  2. 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 39:412–423

    Article  PubMed  PubMed Central  Google Scholar 

  3. 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 43:748–759

    Article  PubMed  PubMed Central  Google Scholar 

  4. Frisoli A, Chaves PH, Ingham SJM, Fried LP (2011) Severe osteopenia and osteoporosis, sarcopenia, and frailty status in community-dwelling older women: results from the Women’s Health and Aging Study (WHAS) II. Bone 48:952–957

    Article  PubMed  Google Scholar 

  5. 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 12:249–256

    Article  PubMed  Google Scholar 

  6. Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, Chou MY, Chen LY, Hsu PS, Krairit O, Lee JSW, 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 15:95–101

    Article  PubMed  Google Scholar 

  7. Studenski SA, Peters KW, Alley DE et al (2014) The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. Journals of Gerontology Series a-Biological Sciences and Medical Sciences 69:547–558

    Article  PubMed  PubMed Central  Google Scholar 

  8. Woo J, Leung J, Morley JE (2015) Defining sarcopenia in terms of incident adverse outcomes. J Am Med Dir Assoc 16:247–252

    Article  PubMed  Google Scholar 

  9. Blain H, Jaussent A, Thomas E, Micallef JP, Dupuy AM, Bernard PL, Mariano-Goulart D, Cristol JP, Sultan C, Rossi M (2010) Appendicular skeletal muscle mass is the strongest independent factor associated with femoral neck bone mineral density in adult and older men. Exp Gerontol 45:679–684

    Article  PubMed  Google Scholar 

  10. Verschueren S, Gielen E, O’Neill TW et al (2013) Sarcopenia and its relationship with bone mineral density in middle-aged and elderly European men. Osteoporos Int 24:87–98

    Article  CAS  PubMed  Google Scholar 

  11. Orsatti FL, Nahas EAP, Nahas-Neto J, Orsatti CL, Marocolo M, Barbosa-Neto O, da Mota GR (2011) Low appendicular muscle mass is correlated with femoral neck bone mineral density loss in postmenopausal women. BMC Musculoskelet Disord 12

  12. Szulc P, Beck TJ, Marchand F, Delmas PD (2005) Low skeletal muscle mass is associated with poor structural parameters of bone and impaired balance in elderly men - the MINOS study. J Bone Miner Res 20:721–729

    Article  PubMed  Google Scholar 

  13. Landi F, Liperoti R, Russo A, Giovannini S, Tosato M, Capoluongo E, Bernabei R, Onder G (2012) Sarcopenia as a risk factor for falls in elderly individuals: results from the ilSIRENTE study. Clin Nutr 31:652–658

    Article  PubMed  Google Scholar 

  14. Cheung CL, Tan KCB, Bow CH, Soong CSS, Loong CHN, Kung AWC (2012) Low handgrip strength is a predictor of osteoporotic fractures: cross-sectional and prospective evidence from the Hong Kong Osteoporosis Study. Age 34:1239–1248

    Article  PubMed  Google Scholar 

  15. Hong W, Cheng Q, Zhu XY, 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

  16. Lang T, Cauley JA, Tylavsky F, Bauer D, Cummings S, Harris TB, Study HA (2010) Computed tomographic measurements of thigh muscle cross-sectional area and attenuation coefficient predict hip fracture: the health, aging, and Body Composition Study. J Bone Miner Res 25:513–519

    Article  PubMed  Google Scholar 

  17. Landi F, Calvani R, Ortolani E, Salini S, Martone AM, Santoro L, Santoliquido A, Sisto A, Picca A, Marzetti E (2017) The association between sarcopenia and functional outcomes among older patients with hip fracture undergoing in-hospital rehabilitation. Osteoporos Int 28:1569–1576

    Article  CAS  PubMed  Google Scholar 

  18. Roh YH, Do Koh Y, Noh JH, Gong HS, Baek GH (2017) Evaluation of sarcopenia in patients with distal radius fractures. Arch Osteoporos 12

  19. Steihaug OM, Gjesdal CG, Bogen B, Kristoffersen MH, Lien G, Ranhoff AH (2017) Sarcopenia in patients with hip fracture: a multicenter cross-sectional study. PLoS One 12

  20. Gonzalez-Montalvo JI, Alarcon T, Gotor P, Queipo R, Velasco R, Hoyos R, Pardo A, Otero A (2016) Prevalence of sarcopenia in acute hip fracture patients and its influence on short-term clinical outcome. Geriatr Gerontol Int 16:1021–1027

    Article  PubMed  Google Scholar 

  21. 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 25:3424–3431

    Article  PubMed  Google Scholar 

  22. Ho AWH, Lee MML, Chan EWC, Ng HMY, Lee CW, Ng WS, Wong SH (2016) Prevalence of pre-sarcopenia and sarcopenia in Hong Kong Chinese geriatric patients with hip fracture and its correlation with different factors. Hong Kong Med J 22:23–29

    PubMed  Google Scholar 

  23. Yoo JI, Ha YC, Kwon HB, Lee YK, Koo KH, Yoo MJ (2016) High prevalence of sarcopenia in Korean patients after hip fracture: a case-control study. J Korean Med Sci 31:1479–1484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hida T, Ishiguro N, Shimokata H, Sakai Y, Matsui Y, Takemura M, Terabe Y, Harada A (2013) High prevalence of sarcopenia and reduced leg muscle mass in Japanese patients immediately after a hip fracture. Geriatr Gerontol Int 13:413–420

    Article  PubMed  Google Scholar 

  25. Di Monaco M, Castiglioni C, Vallero F, Di Monaco R, Tappero R (2012) Sarcopenia is more prevalent in men than in women after hip fracture: a cross-sectional study of 591 inpatients. Arch Gerontol Geriatr 55:E48–E52

    Article  PubMed  Google Scholar 

  26. Singh MAF, Singh NA, Hansen RD et al (2009) Methodology and baseline characteristics for the sarcopenia and hip fracture study: a 5-year prospective study. Journals of Gerontology Series a-biological Sciences and Medical Sciences 64:568–574

    Article  PubMed  Google Scholar 

  27. Harris R, Chang Y, Beavers K, Laddu-Patel D, Bea J, Johnson K, LeBoff M, Womack C, Wallace R, Li W (2017) Risk of fracture in women with sarcopenia, low bone mass, or both. J Am Geriatr Soc 65:2673–2678

    Article  PubMed  PubMed Central  Google Scholar 

  28. 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 Ser A:glx245

  29. 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 31:2048–2056

    Article  CAS  PubMed  Google Scholar 

  30. Chalhoub D, Cawthon PM, Ensrud KE, Stefanick ML, Kado DM, Boudreau R, Greenspan S, Newman AB, Zmuda J, Orwoll ES (2015) Risk of nonspine fractures in older adults with sarcopenia, low bone mass, or both. J Am Geriatr Soc 63:1733–1740

    Article  PubMed  PubMed Central  Google Scholar 

  31. 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 15:551–558

    Article  PubMed  Google Scholar 

  32. 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 25:603–605

    Article  PubMed  Google Scholar 

  33. Carter ND, Khan KM, Mallinson A, Janssen PA, Heinonen A, Petit MA, McKay HA, Grp F-FBR (2002) Knee extension strength is a significant determinant of static and dynamic balance as well as quality of life in older community-dwelling women with osteoporosis. Gerontology 48:360–368

    Article  PubMed  Google Scholar 

  34. Yoshimura N, Muraki S, Oka H, Iidaka T, Kodama R, Horii C, Kawaguchi H, Nakamura K, Akune T, Tanaka S (2018) Do sarcopenia and/or osteoporosis increase the risk of frailty? A 4-year observation of the second and third ROAD study surveys. Osteoporos Int 29:2181–2190

    Article  CAS  PubMed  Google Scholar 

  35. Moreland JD, Richardson JA, Goldsmith CH, Clase CM (2004) Muscle weakness and falls in older adults: a systematic review and meta-analysis. J Am Geriatr Soc 52:1121–1129

    Article  PubMed  Google Scholar 

  36. Churilov I, Churilov L, MacIsaac RJ, Ekinci EI (2018) Systematic review and meta-analysis of prevalence of sarcopenia in post acute inpatient rehabilitation. Osteoporos Int 29:805–812

    Article  CAS  PubMed  Google Scholar 

  37. 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 87:589–598

    Article  CAS  PubMed  Google Scholar 

  38. 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 96:3855–3863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Urban RJ, Bodenburg YH, Gilkison C, Foxworth J, Coggan AR, Wolfe RR, Ferrando A (1995) Testosterone administration to elderly men increases skeletal-muscle strength and protein-synthesis. Am J Physiol Endocrinol Metab 269:E820–E826

    Article  CAS  Google Scholar 

  40. van Geel TA, Geusens PP, Winkens B, Sels J-PJ, Dinant G-J (2009) Measures of bioavailable serum testosterone and estradiol and their relationships with muscle mass, muscle strength and bone mineral density in postmenopausal women: a cross-sectional study. Eur J Endocrinol 160:681–687

    Article  CAS  PubMed  Google Scholar 

  41. Messier V, Rabasa-Lhoret R, Barbat-Artigas S, Elisha B, Karelis AD, Aubertin-Leheudre M (2011) Menopause and sarcopenia: a potential role for sex hormones. Maturitas 68:331–336

    Article  CAS  PubMed  Google Scholar 

  42. 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 61:1059–1064

    Article  PubMed  Google Scholar 

  43. Yoon BH, Lee JK, Choi DS, Han SH (2018) Prevalence and associated risk factors of sarcopenia in female patients with osteoporotic fracture. J Bone Metab 25:59–62

    Article  PubMed  PubMed Central  Google Scholar 

  44. Westbury LD, Dodds RM, Syddall HE, Baczynska AM, Shaw SC, Dennison EM, Roberts HC, Sayer AA, Cooper C, Patel HP (2018) Associations between objectively measured physical activity, body composition and sarcopenia: findings from the Hertfordshire Sarcopenia Study (HSS). Calcif Tissue Int 103:237–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. D’Adamo CR, Hawkes WG, Miller RR, Jones M, Hochberg M, Yu-Yahiro J, Hebel JR, Magaziner J (2014) Short-term changes in body composition after surgical repair of hip fracture. Age Ageing 43:275–280

    Article  PubMed  Google Scholar 

  46. Girgis CM (2015) Integrated therapies for osteoporosis and sarcopenia: from signaling pathways to clinical trials. Calcif Tissue Int 96:243–255

    Article  CAS  PubMed  Google Scholar 

  47. Karsenty G, Mera P (2017) Molecular bases of the crosstalk between bone and muscle. Bone

  48. Edwards MH, Ward KA, Ntani G, Parsons C, Thompson J, Sayer AA, Dennison EM, Cooper C (2015) Lean mass and fat mass have differing associations with bone microarchitecture assessed by high resolution peripheral quantitative computed tomography in men and women from the Hertfordshire Cohort Study. Bone 81:145–151

    Article  PubMed  PubMed Central  Google Scholar 

  49. LeBrasseur NK, Achenbach SJ, Melton LJ, Amin S, Khosla S (2012) Skeletal muscle mass is associated with bone geometry and microstructure and serum insulin-like growth factor binding protein-2 levels in adult women and men. J Bone Miner Res 27:2159–2169

    Article  CAS  PubMed  Google Scholar 

  50. Szulc P, Blaizot S, Boutroy S, Vilayphiou N, Boonen S, Chapurlat R (2013) Impaired bone microarchitecture at the distal radius in older men with low muscle mass and grip strength: the STRAMBO Study. J Bone Miner Res 28:169–178

    Article  PubMed  Google Scholar 

  51. Carbonare LD, Giannini S (2004) Bone microarchitecture as an important determinant of bone strength. J Endocrinol Investig 27:99–105

    Article  Google Scholar 

  52. Binkley N, Buehring B (2009) Beyond FRAX: it’s time to consider “sarco-osteopenia”. J Clin Densitom 12:413–416

    Article  PubMed  Google Scholar 

  53. Wang YJ, Wang Y, Zhan JK, Tang ZY, He JY, Tan P, Deng HQ, Huang W, Liu YS (2015) Sarco-osteoporosis: prevalence and association with frailty in Chinese community-dwelling older adults. Int J Endocrinol 2015:482940

  54. Patel HP, Dawson A, Westbury LD, Hasnaoui G, Syddall HE, Shaw S, Sayer AA, Cooper C, Dennison EM (2018) Muscle mass, muscle morphology and bone health among community-dwelling older men: findings from the Hertfordshire sarcopenia Study (HSS). Calcif Tissue Int 103:35–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This study was partially supported by General Research Fund (Reference: 14113018).

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Authors and Affiliations

  1. Department of Orthopaedics and Traumatology, 5/F, Clinical Sciences Building, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, SAR, China

    R. M. Y. Wong, H. Wong, N. Zhang, S. K. H. Chow, W. W. Chau, J. Wang, Y. N. Chim, K. S. Leung & W. H. Cheung

  2. The CUHK-ACC Space Medicine Centre on Health Maintenance of Musculoskeletal System, The Chinese University of Hong Kong Shenzhen Research Institute, Shenzhen, People’s Republic of China

    S. K. H. Chow & W. H. Cheung

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  1. R. M. Y. Wong
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  2. H. Wong
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  6. J. Wang
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Correspondence to W. H. Cheung.

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Wong, R.M.Y., Wong, H., Zhang, N. et al. The relationship between sarcopenia and fragility fracture—a systematic review. Osteoporos Int 30, 541–553 (2019). https://doi.org/10.1007/s00198-018-04828-0

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