Body composition, energy expenditure and physical activity

The association between low lean mass and osteoporosis increases the risk of weakness, poor physical performance and frailty in Brazilian older adults: data from SARCOS study



To characterize the phenotypes of older adults with low lean mass and osteoporosis, concomitantly or isolated, in regards to poor physical performance and frailty status.


Cross-sectional analysis of the SARCopenia and OSteoporosis in Older Adults with Cardiovascular Diseases Study (SARCOS).


Outpatient geriatric cardiology clinic.

Participants and method

385 older adults underwent DXA analysis. Low lean mass was diagnosed according to FNIH and low BMD by a T-score ≤ −2.5 SD. Subjects were grouped into: I—Low lean mass and Osteoporosis (LLMO); II—Low lean mass (LLM); III—Osteoporosis (OP), and IV—Controls. Poor physical performance was diagnosed by weakness or slow walking speed or impaired mobility. Frailty was diagnosed by CHS criteria.


The mean age was 78.22 ± 7.16 years. The prevalence of LLMO, LLM, and OP were 14.8%, 39.5%, and 19.2%, respectively. LLMO subjects were older, predominantly women, with a high percentage of body fat (HTBF). LLM was represented by obese men, while individuals with OP were preferably women, older and leaner. In a regression analyses, LLMO presented an OR: 6.42 (2.63‒15.65; p < 0.001) for weakness, OR: 2.55 (1.09‒5.95; p = 0.030) for impaired mobility, and OR: 14.75 (2.72‒79.94; p = 0.002) for frailty. After adjusting for HTBF, the OR for frailty, decreased to 7.25 (1.11–47.21; p = 0.038). LLM and OP were associated only with weakness with an OR: 3.06 (1.36–6.84; p = 0.006) and OR: 3.14 (1.29–7.62; p = 0.011), respectively.


In Brazilian older community-dwelling outpatient adults, the phenotype characterized by low lean mass and osteoporosis presents a higher association with impaired mobility, weakness and frailty status compared to the others phenotyeps and controls. A high percentage of body fat presents a synergistic effect with low lean mass and osteoporosis phenotype in regards to frailty.

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Fig. 1: The flowchart of selection of musculoskeletal phenotypes.


  1. 1.

    Shephard RJ. Age and physical work capacity. Exp Aging Res. 1999;25:331–43.

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Beaudart C, Rizzoli R, Bruyere O, Reginster JY, Biver E. Sarcopenia: burden and challenges for public health. Arch Public Health. 2014;72:45

    Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Dempster DW. Osteoporosis and the burden of osteoporosis-related fractures. Am J Managed Care. 2011;17:S164–169.

    Google Scholar 

  4. 4.

    Roux C, Wyman A, Hooven FH, Gehlbach SH, Adachi JD, Chapurlat RD, et al. Burden of non-hip, non-vertebral fractures on quality of life in postmenopausal women: the Global Longitudinal study of Osteoporosis in Women (GLOW). Osteoporos Int. 2012;23:2863–71.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Rikkonen T, Sirola J, Salovaara K, Tuppurainen M, Jurvelin JS, Honkanen R, et al. Muscle strength and body composition are clinical indicators of osteoporosis. Calcif Tissue Int. 2012;91:131–8.

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Laurent MR, Dubois V, Claessens F, Verschueren SM, Vanderschueren D, Gielen E, et al. Muscle-bone interactions: from experimental models to the clinic? A critical update. Mol Cell Endocrinol. 2016;432:14–36.

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Tagliaferri C, Wittrant Y, Davicco MJ, Walrand S, Coxam V. Muscle and bone, two interconnected tissues. Ageing Res Rev. 2015;21:55–70.

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Brotto M, Johnson ML. Endocrine crosstalk between muscle and bone. Curr Osteoporos Rep. 2014;12:135–41.

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Edwards MH, Gregson CL, Patel HP, Jameson KA, Harvey NC, Sayer AA, et al. Muscle size, strength, and physical performance and their associations with bone structure in the Hertfordshire Cohort Study. J Bone Min Res. 2013;28:2295–304.

    Article  Google Scholar 

  10. 10.

    Lauretani F, Russo CR, Bandinelli S, Bartali B, Cavazzini C, Di Iorio A, et al. Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol. 2003;95:1851–60.

    Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Hughes VA, Frontera WR, Roubenoff R, Evans WJ, Singh MA. Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am J Clin Nutr. 2002;76:473–81.

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Binkley N, Buehring B. Beyond FRAX: it’s time to consider “sarco-osteopenia”. J Clin Densitom. 2009;12:413–6.

    Article  PubMed  Google Scholar 

  13. 13.

    Huo YR, Suriyaarachchi P, Gomez F, Curcio CL, Boersma D, Muir SW, et al. Phenotype of osteosarcopenia in older individuals with a history of falling. J Am Med Dir Assoc. 2015;16:290–5.

    Article  PubMed  Google Scholar 

  14. 14.

    Crepaldi G, Maggi S. Sarcopenia and osteoporosis: a hazardous duet. J Endocrinol Invest. 2005;28:66–68.

    CAS  Article  Google Scholar 

  15. 15.

    Frisoli A Jr., Chaves PH, Ingham SJ, Fried LP. 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. 2011;48:952–7.

    Article  PubMed  Google Scholar 

  16. 16.

    Wang YJ, Wang Y, Zhan JK, Tang ZY, He JY, Tan P, et al. Sarco-osteoporosis: prevalence and association with frailty in Chinese community-dwelling older adults. Int J Endocrinol. 2015;2015:482940

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Yoo JI, Kim H, Ha YC, Kwon HB, Koo KH. Osteosarcopenia in patients with hip fracture is related with high mortality. J Korean Med Sci. 2018;33:e27

    Article  PubMed  Google Scholar 

  18. 18.

    Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48:16–31.

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Studenski SA, Peters KW, Alley DE, Cawthon PM, McLean RR, Harris TB, et al. The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci. 2014;69:547–58.

    Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, et al. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc. 2014;15:95–101.

    Article  Google Scholar 

  21. 21.

    WHO. Obesity: preventing and managing the global epidemic. Report of a WHO consultation. WHO Technical Report Series. WHO; 2000.894:i-xii–1-253.

  22. 22.

    World Health Organization. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report of a WHO Study Group. WHO Technical Report Series; 843. World Health Organization; 1994. p. 1–129.

  23. 23.

    Sjoblom S, Suuronen J, Rikkonen T, Honkanen R, Kroger H, Sirola J. Relationship between postmenopausal osteoporosis and the components of clinical sarcopenia. Maturitas. 2013;75:175–80.

    Article  PubMed  Google Scholar 

  24. 24.

    Gonzalez-Montalvo JI, Alarcon T, Gotor P, Queipo R, Velasco R, Hoyos R, et al. Prevalence of sarcopenia in acute hip fracture patients and its influence on short-term clinical outcome. Geriatrics Gerontol Int. 2016;16:1021–7.

    Article  Google Scholar 

  25. 25.

    Yoshimura N, Muraki S, Oka H, Iidaka T, Kodama R, Kawaguchi H, et al. Is osteoporosis a predictor for future sarcopenia or vice versa? Four-year observations between the second and third ROAD study surveys. Osteoporos Int. 2017;28:189–99.

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Lamb SE, Keene DJ. Measuring physical capacity and performance in older people. Best Pract Res Clin Rheumatol. 2017;31:243–54.

    Article  PubMed  Google Scholar 

  27. 27.

    Guralnik JM, Simonsick EM, Ferrucci L, Glynn RJ, Berkman LF, Blazer DG, et al. A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol. 1994;49:M85–94.

    CAS  Article  Google Scholar 

  28. 28.

    Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56:M146–156.

    CAS  Article  Google Scholar 

  29. 29.

    Stenholm S, Sallinen J, Koster A, Rantanen T, Sainio P, Heliovaara M, et al. Association between obesity history and hand grip strength in older adults–exploring the roles of inflammation and insulin resistance as mediating factors. J Gerontol A Biol Sci Med Sci. 2011;66:341–8. e-pub ahead of print 2011/02/12; glq226 [pii]

  30. 30.

    Hulens M, Vansant G, Lysens R, Claessens AL, Muls E, Brumagne S. Study of differences in peripheral muscle strength of lean versus obese women: an allometric approach. Int J Obes Relat Metab Disord. 2001;25:676–81.

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Cooper R, Hardy R, Bann D, Aihie Sayer A, Ward KA, Adams JE, et al. Body mass index from age 15 years onwards and muscle mass, strength, and quality in early old age: findings from the MRC National Survey of Health and Development. J Gerontol A Biol Sci Med Sci. 2014;69:1253–9.

    Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Marcus RL, Addison O, Kidde JP, Dibble LE, Lastayo PC. Skeletal muscle fat infiltration: impact of age, inactivity, and exercise. J Nutr Health Aging. 2010;14:362–6.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Weinbrenner T, Schroder H, Escurriol V, Fito M, Elosua R, Vila J, et al. Circulating oxidized LDL is associated with increased waist circumference independent of body mass index in men and women. Am J Clin Nutr. 2006;83:30–35.

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    Kanapuru B, Ershler WB. Inflammation, coagulation, and the pathway to frailty. Am J Med. 2009;122:605–13.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Howard C, Ferrucci L, Sun K, Fried LP, Walston J, Varadhan R, et al. Oxidative protein damage is associated with poor grip strength among older women living in the community. J Appl Physiol. 2007;103:17–20.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Nishimura S, Manabe I, Nagasaki M, Eto K, Yamashita H, Ohsugi M, et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med. 2009;15:914–20.

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Mantovani G, Maccio A, Lai P, Massa E, Ghiani M, Santona MC. Cytokine involvement in cancer anorexia/cachexia: role of megestrol acetate and medroxyprogesterone acetate on cytokine downregulation and improvement of clinical symptoms. Crit Rev Oncog. 1998;9:99–106.

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Beyer I, Njemini R, Bautmans I, Demanet C, Bergmann P, Mets T. Inflammation-related muscle weakness and fatigue in geriatric patients. Exp Gerontol. 2012;47:52–59.

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Stenholm S, Strandberg TE, Pitkala KH, Sainio P, Heliovaara M, Koskinen S. Midlife obesity and risk of frailty in old age during a 22-year follow-up in men and women: the Mini-Finland Follow-up Survey. J Gerontol A Biol Sci Med Sci. 2014;69:73–78.

    Article  PubMed  Google Scholar 

  40. 40.

    Garcia-Esquinas E, Jose Garcia-Garcia F, Leon-Munoz LM, Carnicero JA, Guallar-Castillon P, Gonzalez-Colaco Harmand M, et al. Obesity, fat distribution, and risk of frailty in two population-based cohorts of older adults in Spain. Obes (Silver Spring). 2015;23:847–55.

    Article  Google Scholar 

  41. 41.

    Cawthon PM, Travison TG, Manini TM, Patel S, Pencina KM, Fielding RA, et al. Establishing the link between lean mass and grip strength cut-points with mobility disability and other health outcomes: proceedings of the sarcopenia definition and outcomes consortium conference. J Gerontol A Biol Sci Med Sci. 2019.

    Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Pietschmann P, Mechtcheriakova D, Meshcheryakova A, Foger-Samwald U, Ellinger I. Immunology of osteoporosis: a mini-review. Gerontology. 2016;62:128–37.

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Tieland M, Trouwborst I, Clark BC. Skeletal muscle performance and ageing. J cachexia, sarcopenia muscle. 2018;9:3–19.

    Article  Google Scholar 

  44. 44.

    Mo C, Romero-Suarez S, Bonewald L, Johnson M, Brotto M. Prostaglandin E2: from clinical applications to its potential role in bone- muscle crosstalk and myogenic differentiation. Recent Pat Biotechnol. 2012;6:223–9.

    CAS  Article  Google Scholar 

  45. 45.

    Gorski J, Huffman NT, Brotto L, Dallas M , Breggia A, Chittur SV, Huang J, Mo C, Liu Y, Seidah NG, Rosen C, Brotto M, Bonewald L. Potential role of leptin and BMP2 in osteocyte regulation of muscle mass and function in the adult skeleton and with age. in: ASBMR 2013 Annual Meeting; October 4-7, 2013; Baltimore Convention Center. Baltimore, MD: American Society for Bone and Mineral Research; 2013.

  46. 46.

    Schrager MA, Metter EJ, Simonsick E, Ble A, Bandinelli S, Lauretani F, et al. Sarcopenic obesity and inflammation in the InCHIANTI study. J Appl Physiol. 2007;102:919–25.

    Article  PubMed  Google Scholar 

  47. 47.

    Mohiti-Ardekani J, Soleymani-Salehabadi H, Owlia MB, Mohiti A. Relationships between serum adipocyte hormones (adiponectin, leptin, resistin), bone mineral density and bone metabolic markers in osteoporosis patients. J bone Miner Metab. 2014;32:400–4.

    CAS  Article  PubMed  Google Scholar 

  48. 48.

    Ducy P. The role of osteocalcin in the endocrine cross-talk between bone remodelling and energy metabolism. Diabetologia. 2011;54:1291–7.

    CAS  Article  PubMed  Google Scholar 

  49. 49.

    Drey M, Sieber CC, Bertsch T, Bauer JM, Schmidmaier R. Fi ATig. Osteosarcopenia is more than sarcopenia and osteopenia alone. Aging Clin Exp Res. 2016;28:895–9.

    Article  PubMed  Google Scholar 

  50. 50.

    Frisoli A Jr, Martin FC, Ingham SJ, Carvalho AC, Chaves P. The association of osteosarcopenia, sarcopenia and osteoporosis with weakness and mobility in older adults with cardiovascular disease: Data from Sarcos. Osteoporos Int. 2017;28:79

    Article  Google Scholar 

  51. 51.

    Greeves JP, Cable NT, Reilly T, Kingsland C. Changes in muscle strength in women following the menopause: a longitudinal assessment of the efficacy of hormone replacement therapy. Clin Sci. 1999;97:79–84.

    CAS  Article  Google Scholar 

  52. 52.

    Phillips SK, Rook KM, Siddle NC, Bruce SA, Woledge RC. Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy. Clin Sci. 1993;84:95–98.

    CAS  Article  Google Scholar 

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The authors would like to thank Tania Brunini Berna and Neusa Maria for help with the administrative aspects and organization of our study.

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Correspondence to Alberto Frisoli Jr.

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Frisoli Jr, A., Paes, A.T., Borges, J. et al. The association between low lean mass and osteoporosis increases the risk of weakness, poor physical performance and frailty in Brazilian older adults: data from SARCOS study. Eur J Clin Nutr (2020).

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