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

Osteoporosis International

Volumn 24, Issue 1, 2013, Pages 87-98

  Verschueren, S ^a   Gielen, E ^b   O'Neill, T W ^c   Pye, S R ^c   Adams, J E ^d   Ward, K A ^d,e   Wu, F C ^c   Szulc, P ^f   Laurent, M ^b   Claessens, F ^b   Vanderschueren, D ^b   Boonen, S ^b  

^a KU LEUVEN DEPARTMENT OF REHABILITATION SCIENCES   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e MRC HUMAN NUTRITION RESEARCH   (United Kingdom)

^f UNIVERSITÉ DE LYON   (France)

Author keywords

Areal bone mineral density (BMDa); Lean mass; Muscle strength; Osteoporosis; Relative appendicular skeletal muscle mass (RASM), sarcopenia

Indexed keywords

ADULT; AGED; ARTICLE; BONE DENSITY; COMMUNITY LIVING; DISEASE ASSOCIATION; DUAL ENERGY X RAY ABSORPTIOMETRY; EUROPE; FAT MASS; HUMAN; LEAN BODY WEIGHT; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MUSCLE ATROPHY; MUSCLE MASS; MUSCLE STRENGTH; OSTEOPOROSIS; PRIORITY JOURNAL;

ABSORPTIOMETRY, PHOTON; ADULT; AGED; AGING; ANTHROPOMETRY; BELGIUM; BONE DENSITY; CROSS-SECTIONAL STUDIES; ENGLAND; HUMANS; MALE; MIDDLE AGED; MOTOR ACTIVITY; MUSCLE STRENGTH; OSTEOPOROSIS; SARCOPENIA;

EID: 84872351743     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-012-2057-z     Document Type: Article

References (57)

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
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
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
4. Zofkova I (2008) Hormonal aspects of the muscle-bone unit. Physiol Res 57(Suppl 1):S159-S169
5. Frost HM (2003) Bone's mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol 275:1081-1101
6. Forwood MR, Turner CH (1995) Skeletal adaptations to mechanical usage: results from tibial loading studies in rats. Bone 17:197S-205S
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
40. Thomas T, Burguera B (2002) Is leptin the link between fat and bone mass? J Bone Miner Res 17:1563-1569
41. Cornish J, Reid IR (2001) Effects of amylin and adrenomedullin on the skeleton. J Musculoskelet Neuronal Interact 2:15-24
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
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
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
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
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
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
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
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
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
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
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
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
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
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