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Sarcopenia and its relationship with bone mineral density in middle-aged and elderly European men

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Abstract

Summary

The aim of this study was to determine the relationship between reduced muscle mass (sarcopenia) and areal bone mineral density (BMDa) in middle-aged and elderly community-dwelling European men. Men with sarcopenia had significantly lower BMDa and were more likely to have osteoporosis compared with men without sarcopenia.

Introduction

In men, the relationship between reduced muscle mass (sarcopenia) and BMDa is unclear. This study aimed to determine this relationship in middle-aged and elderly community-dwelling men.

Methods

Men aged 40–79 years from the Manchester (UK) and Leuven (Belgium) cohorts of the European Male Ageing Study were invited to attend for assessment including dual-energy X-ray absorptiometry, from which appendicular lean mass (aLM), fat mass (FM) and whole-body, spine and hip BMDa were determined. Relative appendicular skeletal muscle mass (RASM) was calculated as aLM/height². Muscle strength was assessed in subjects from Leuven. Sarcopenia was defined by RASM at <7.26 kg/m² and by the recent definition of the European Working Group on Sarcopenia in Older People (RASM at <7.26 kg/m2 plus low muscle function). Linear regression was used to determine the associations between aLM, FM, muscle strength and BMDa and logistic regression to determine the association between sarcopenia and osteoporosis.

Results

Six hundred seventy-nine men with a mean age of 59.6 (SD = 10.7), contributed data to the analysis; 11.9 % were sarcopenic by the conventional definition. After adjustment for age and centre, aLM, RASM and FM were positively associated with BMDa. Men with RASM at <7.26 kg/m² had significantly lower BMDa compared with those with RASM at ≥7.26 kg/m2. In a multivariable model, aLM was most consistently associated with BMDa. Men with sarcopenia were more likely to have osteoporosis compared with those with normal RASM (odds ratio = 3.0; 95 % CI = 1.6–5.8).

Conclusions

Sarcopenia is associated with low BMDa and osteoporosis in middle-aged and elderly men. Further studies are necessary to assess whether maintaining muscle mass contributes to prevent osteoporosis.

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References

  1. Seeman E, Young N, Formica C, Goss P, Tsalamandris C (1996) Do genetic factors explain associations between muscle strength, lean mass, and bone density? A twin study. Am J Physiol 270:E320–E327

    PubMed  CAS  Google Scholar 

  2. Blain H, Jaussent A, Thomas E, Micallef JP, Dupuy AM, Bernard PL, Mariano-Goulart D, Cristol JP, Sultan C, Rossi M et al (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 

  3. Coin A, Perissinotto E, Enzi G, Zamboni M, Inelmen EM, Frigo AC, Manzato E, Busetto L, Buja A, Sergi G (2008) Predictors of low bone mineral density in the elderly: the role of dietary intake, nutritional status and sarcopenia. Eur J Clin Nutr 62:802–809

    Article  PubMed  CAS  Google Scholar 

  4. Zofkova I (2008) Hormonal aspects of the muscle-bone unit. Physiol Res 57(Suppl 1):S159–S169

    PubMed  CAS  Google Scholar 

  5. Frost HM (2003) Bone’s mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol 275:1081–1101

    Article  PubMed  Google Scholar 

  6. Forwood MR, Turner CH (1995) Skeletal adaptations to mechanical usage: results from tibial loading studies in rats. Bone 17:197S–205S

    PubMed  CAS  Google Scholar 

  7. Pluijm SM, Visser M, Smit JH, Popp-Snijders C, Roos JC, Lips P (2001) Determinants of bone mineral density in older men and women: body composition as mediator. J Bone Miner Res 16:2142–2151

    Article  PubMed  CAS  Google Scholar 

  8. Genaro PS, Pereira GA, Pinheiro MM, Szejnfeld VL, Martini LA (2010) Influence of body composition on bone mass in postmenopausal osteoporotic women. Arch Gerontol Geriatr 51:295–298

    Article  PubMed  Google Scholar 

  9. Taaffe DR, Cauley JA, Danielson M, Nevitt MC, Lang TF, Bauer DC, Harris TB (2001) Race and sex effects on the association between muscle strength, soft tissue, and bone mineral density in healthy elders: the Health, Aging, and Body Composition Study. J Bone Miner Res 16:1343–1352

    Article  PubMed  CAS  Google Scholar 

  10. Blain H, Vuillemin A, Teissier A, Hanesse B, Guillemin F, Jeandel C (2001) Influence of muscle strength and body weight and composition on regional bone mineral density in healthy women aged 60 years and over. Gerontology 47:207–212

    Article  PubMed  CAS  Google Scholar 

  11. Sherk VD, Palmer IJ, Bemben MG, Bemben DA (2009) Relationships between body composition, muscular strength, and bone mineral density in estrogen-deficient postmenopausal women. J Clin Densitom 12:292–298

    Article  PubMed  Google Scholar 

  12. Wu F, Ames R, Clearwater J, Evans MC, Gamble G, Reid IR (2002) Prospective 10-year study of the determinants of bone density and bone loss in normal postmenopausal women, including the effect of hormone replacement therapy. Clin Endocrinol (Oxf) 56:703–711

    Article  CAS  Google Scholar 

  13. Aloia JF, Vaswani A, Ma R, Flaster E (1995) To what extent is bone mass determined by fat-free or fat mass? Am J Clin Nutr 61:1110–1114

    PubMed  CAS  Google Scholar 

  14. Khosla S, Atkinson EJ, Riggs BL, Melton LJ 3rd (1996) Relationship between body composition and bone mass in women. J Bone Miner Res 11:857–863

    Article  PubMed  CAS  Google Scholar 

  15. Madsen OR, Schaadt O, Bliddal H, Egsmose C, Sylvest J (1993) Relationship between quadriceps strength and bone mineral density of the proximal tibia and distal forearm in women. J Bone Miner Res 8:1439–1444

    Article  PubMed  CAS  Google Scholar 

  16. Nguyen TV, Center JR, Eisman JA (2000) Osteoporosis in elderly men and women: effects of dietary calcium, physical activity, and body mass index. J Bone Miner Res 15:322–331

    Article  PubMed  CAS  Google Scholar 

  17. Lima RM, Bezerra LM, Rabelo HT, Silva MA, Silva AJ, Bottaro M, de Oliveira RJ (2009) Fat-free mass, strength, and sarcopenia are related to bone mineral density in older women. J Clin Densitom 12:35–41

    Article  PubMed  Google Scholar 

  18. 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 147:755–763

    Article  PubMed  CAS  Google Scholar 

  19. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM et al (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  Google Scholar 

  20. 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 

  21. Taes YE, Lapauw B, Vanbillemont G, Bogaert V, De Bacquer D, Zmierczak H, Goemaere S, Kaufman JM (2009) Fat mass is negatively associated with cortical bone size in young healthy male siblings. J Clin Endocrinol Metab 94:2325–2331

    Article  PubMed  CAS  Google Scholar 

  22. Van Langendonck L, Claessens A, Lefevre J, Thomis M, Phillipaerts R, Delvaux K, Lysens R, Vandeneynde B, Beunen G (2002) Association between bone mineral density (DXA), body structure, and body composition in middle-aged men. Am J Hum Biol 14:735–742

    Article  PubMed  Google Scholar 

  23. Reid IR, Plank LD, Evans MC (1992) Fat mass is an important determinant of whole body bone density in premenopausal women but not in men. J Clin Endocrinol Metab 75:779–782

    Article  PubMed  CAS  Google Scholar 

  24. Glynn NW, Meilahn EN, Charron M, Anderson SJ, Kuller LH, Cauley JA (1995) Determinants of bone mineral density in older men. J Bone Miner Res 10:1769–1777

    Article  PubMed  CAS  Google Scholar 

  25. Lee DM, O’Neill TW, Pye SR, Silman AJ, Finn JD, Pendleton N, Tajar A, Bartfai G, Casanueva F, Forti G et al (2009) The European Male Ageing Study (EMAS): design, methods and recruitment. Int J Androl 32:11–24

    Article  PubMed  Google Scholar 

  26. Washburn RA, Smith KW, Jette AM, Janney CA (1993) The Physical Activity Scale for the Elderly (PASE): development and evaluation. J Clin Epidemiol 46:153–162

    Article  PubMed  CAS  Google Scholar 

  27. Reuben DB, Siu AL (1990) An objective measure of physical function of elderly outpatients. The Physical Performance Test. J Am Geriatr Soc 38:1105–1112

    PubMed  CAS  Google Scholar 

  28. Tinetti ME, Williams TF, Mayewski R (1986) Fall risk index for elderly patients based on number of chronic disabilities. Am J Med 80:429–434

    Article  PubMed  CAS  Google Scholar 

  29. Roberts HC, Denison HJ, Martin HJ, Patel HP, Syddall H, Cooper C, Sayer AA (2011) A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardised approach. Age Ageing 40:423–429

    Article  PubMed  Google Scholar 

  30. Boonen S, Lesaffre E, Dequeker J, Aerssens J, Nijs J, Pelemans W, Bouillon R (1996) Relationship between baseline insulin-like growth factor-I (IGF-I) and femoral bone density in women aged over 70 years: potential implications for the prevention of age-related bone loss. J Am Geriatr Soc 44:1301–1306

    PubMed  CAS  Google Scholar 

  31. Kanis JA, McCloskey EV, Johansson H, Oden A, Melton LJ 3rd, Khaltaev N (2008) A reference standard for the description of osteoporosis. Bone 42:467–475

    Article  PubMed  CAS  Google Scholar 

  32. Wang W, Wang Z, Faith MS, Kotler D, Shih R, Heymsfield SB (1999) Regional skeletal muscle measurement: evaluation of new dual-energy X-ray absorptiometry model. J Appl Physiol 87:1163–1171

    PubMed  CAS  Google Scholar 

  33. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G et al (2001) Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci 56:M146–M156

    Article  PubMed  CAS  Google Scholar 

  34. Cesari M, Kritchevsky SB, Penninx BW, Nicklas BJ, Simonsick EM, Newman AB, Tylavsky FA, Brach JS, Satterfield S, Bauer DC et al (2005) Prognostic value of usual gait speed in well-functioning older people—results from the Health, Aging and Body Composition Study. J Am Geriatr Soc 53:1675–1680

    Article  PubMed  Google Scholar 

  35. Walsh MC, Hunter GR, Livingstone MB (2006) Sarcopenia in premenopausal and postmenopausal women with osteopenia, osteoporosis and normal bone mineral density. Osteoporos Int 17:61–67

    Article  PubMed  Google Scholar 

  36. Baumgartner RN, Stauber PM, Koehler KM, Romero L, Garry PJ (1996) Associations of fat and muscle masses with bone mineral in elderly men and women. Am J Clin Nutr 63:365–372

    PubMed  CAS  Google Scholar 

  37. Orwoll ES, Oviatt SK, Mann T (1990) The impact of osteophytic and vascular calcifications on vertebral mineral density measurements in men. J Clin Endocrinol Metab 70:1202–1207

    Article  PubMed  CAS  Google Scholar 

  38. Szulc P, Varennes A, Delmas PD, Goudable J, Chapurlat R (2010) Men with metabolic syndrome have lower bone mineral density but lower fracture risk—the MINOS study. J Bone Mineral Res: Off J Am Soc Bone Mineral Res 25:1446–1454

    Article  Google Scholar 

  39. Halade GV, El Jamali A, Williams PJ, Fajardo RJ, Fernandes G (2011) Obesity-mediated inflammatory microenvironment stimulates osteoclastogenesis and bone loss in mice. Exp Gerontol 46:43–52

    Article  PubMed  CAS  Google Scholar 

  40. Thomas T, Burguera B (2002) Is leptin the link between fat and bone mass? J Bone Miner Res 17:1563–1569

    Article  PubMed  CAS  Google Scholar 

  41. Cornish J, Reid IR (2001) Effects of amylin and adrenomedullin on the skeleton. J Musculoskelet Neuronal Interact 2:15–24

    PubMed  CAS  Google Scholar 

  42. van den Beld AW, de Jong FH, Grobbee DE, Pols HA, Lamberts SW (2000) Measures of bioavailable serum testosterone and estradiol and their relationships with muscle strength, bone density, and body composition in elderly men. J Clin Endocrinol Metab 85:3276–3282

    Article  PubMed  Google Scholar 

  43. Lang T, Streeper T, Cawthon P, Baldwin K, Taaffe DR, Harris TB (2010) Sarcopenia: etiology, clinical consequences, intervention, and assessment. Osteoporos Int 21:543–559

    Article  PubMed  CAS  Google Scholar 

  44. Kyle UG, Genton L, Hans D, Karsegard VL, Michel JP, Slosman DO, Pichard C (2001) Total body mass, fat mass, fat-free mass, and skeletal muscle in older people: cross-sectional differences in 60-year-old persons. J Am Geriatr Soc 49:1633–1640

    Article  PubMed  CAS  Google Scholar 

  45. Hedayati KK, Dittmar M (2010) Prevalence of sarcopenia among older community-dwelling people with normal health and nutritonal state. Ecol Food Nutr 49:9

    Article  Google Scholar 

  46. Di Monaco M, Vallero F, Di Monaco R, Tappero R (2011) Prevalence of sarcopenia and its association with osteoporosis in 313 older women following a hip fracture. Arch Gerontol Geriatr 52:71–74

    Article  PubMed  Google Scholar 

  47. Liu CJ and Latham NK (2009) Progressive resistance strength training for improving physical function in older adults. Cochrane Database Syst Rev:CD002759

  48. Peterson MD, Rhea MR, Sen A, Gordon PM (2010) Resistance exercise for muscular strength in older adults: a meta-analysis. Ageing Res Rev 9:226–237

    Article  PubMed  Google Scholar 

  49. Peterson MD, Sen A, Gordon PM (2011) Influence of resistance exercise on lean body mass in aging adults: a meta-analysis. Med Sci Sports Exerc 43:249–258

    PubMed  Google Scholar 

  50. Fiatarone MA, O’Neill EF, Ryan ND, Clements KM, Solares GR, Nelson ME, Roberts SB, Kehayias JJ, Lipsitz LA, Evans WJ (1994) Exercise training and nutritional supplementation for physical frailty in very elderly people. N Engl J Med 330:1769–1775

    Article  PubMed  CAS  Google Scholar 

  51. Roelants M, Delecluse C, Verschueren SM (2004) Whole-body-vibration training increases knee-extension strength and speed of movement in older women. J Am Geriatr Soc 52:901–908

    Article  PubMed  Google Scholar 

  52. Bogaerts A, Delecluse C, Claessens AL, Coudyzer W, Boonen S, Verschueren SM (2007) Impact of whole-body vibration training versus fitness training on muscle strength and muscle mass in older men: a 1-year randomized controlled trial. J Gerontol A Biol Sci Med Sci 62:630–635

    Article  PubMed  Google Scholar 

  53. Howe TE, Shea B, Dawson LJ, Downie F, Murray A, Ross C, Harbour RT, Caldwell LM and Creed G (2011) Exercise for preventing and treating osteoporosis in postmenopausal women. Cochrane database of systematic reviews:CD000333

  54. Gomez-Cabello A, Ara I, Gonzalez-Aguero A, Casajus JA, Vicente-Rodriguez G (2012) Effects of training on bone mass in older adults: a systematic review. Sports Med 42:301–325

    Article  PubMed  CAS  Google Scholar 

  55. Borer KT (2005) Physical activity in the prevention and amelioration of osteoporosis in women: interaction of mechanical, hormonal and dietary factors. Sports Med 35:779–830

    Article  PubMed  Google Scholar 

  56. Whiteford J, Ackland T, Dhaliwal S, James A, Woodhouse J, Price R (2010) Effects of a 1-year randomized controlled trial of resistance training on lower limb bone and muscle structure and function in older men. Osteoporos Int 21:8

    Article  Google Scholar 

  57. Wysocki A, Butler M, Shamliyan T, Kane RL (2011) Whole-body vibration therapy for osteoporosis: state of the science. Ann Intern Med 155(680–686):W206–W613

    Google Scholar 

Download references

Acknowledgements

The European Male Ageing Study (EMAS) was funded by the Commission of the European Communities Fifth Framework Programme “Quality of Life and Management of Living Resources” Grant QLK6-CT-2001-00258. S. Boonen is senior clinical investigator of the Fund for Scientific Research (FWO-Vlaanderen) and holder of the Leuven University Chair in Gerontology and Geriatrics. This work was supported also by grant G.0488.08 from the Fund for Scientific Research (FWO-Vlaanderen) to S. Boonen, research grants OT-05-53 and OT-09-035 from the KU Leuven to D. Vanderschueren, and research funding from Arthritis Research UK. D. Vanderschueren is a senior clinical investigator of the Leuven University Hospital Clinical Research Fund. K. Ward is a senior research scientist working within the Nutrition and Bone Health Core Program at MRC Human Nutrition Research, funded by the UK Medical Research Council (grant code U105960371). S. Verschueren and E. Gielen provided an equal contribution to this manuscript.

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Authors and Affiliations

  1. Research Group for Musculoskeletal Rehabilitation, Department of Rehabilitation Sciences, KU Leuven, Leuven, Belgium

    S. Verschueren

  2. Gerontology and Geriatrics, Department of Clinical and Experimental Medicine, KU Leuven, Leuven, Belgium

    E. Gielen, M. Laurent & S. Boonen

  3. Arthritis Research UK Epidemiology Unit, Manchester Academic Health Science Centre (MAHSC), University of Manchester, Manchester, UK

    T. W. O’Neill & S. R. Pye

  4. Manchester Academic Health Science Centre (MAHSC) and Radiology at Manchester Royal Infirmary, Manchester, UK

    J. E. Adams & K. A. Ward

  5. Nutrition and Bone Health, MRC Human Nutrition Research, Cambridge, UK

    K. A. Ward

  6. Andrology Research Unit, Manchester Academic Health Science Centre (MAHSC), University of Manchester, Manchester, UK

    F. C. Wu

  7. INSERM UMR 1033, University of Lyon, Lyon, France

    P. Szulc

  8. Laboratory of Molecular Endocrinology, Department of Cellular and Molecular Medicine, KU Leuven, Leuven, Belgium

    M. Laurent & F. Claessens

  9. Clinical and Experimental Endocrinology, Department of Clinical and Experimental Medicine, KU Leuven, Leuven, Belgium

    D. Vanderschueren

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  1. S. Verschueren
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  2. E. Gielen
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  3. T. W. O’Neill
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  7. F. C. Wu
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  8. P. Szulc
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  9. M. Laurent
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  10. F. Claessens
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  11. D. Vanderschueren
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  12. S. Boonen
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Correspondence to S. Boonen.

Additional information

S. Verschueren and E. Gielen contributed equally to the manuscript.

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Verschueren, S., Gielen, E., O’Neill, T.W. et al. Sarcopenia and its relationship with bone mineral density in middle-aged and elderly European men. Osteoporos Int 24, 87–98 (2013). https://doi.org/10.1007/s00198-012-2057-z

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