Muscle cross-sectional area and structural bone strength share genetic and environmental effects in older women

Journal of Bone and Mineral Research

Volumn 24, Issue 2, 2009, Pages 338-345

  Mikkola, Tuija M ^a   Sipilä, Sarianna ^a   Rantanen, Taina ^a   Sievänen, Harri ^b   Suominen, Harri ^a   Tiainen, Kristina ^a,c   Kaprio, Jaakko ^d,e   Koskenvuo, Markku ^d   Kauppinen, Markku ^a   Heinonen, Ari ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b UKK INSTITUTE FOR HEALTH PROMOTION RESEARCH   (Finland)

^c UNIVERSITY OF TAMPERE   (Finland)

^d UNIVERSITY OF HELSINKI   (Finland)

^e NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

Aging; Bone strength; Heritability; Muscle; Osteoporosis

Indexed keywords

ADULT; AGED; ARTICLE; BONE FRAGILITY; BONE STRENGTH; COMPRESSIVE STRENGTH; COMPUTER ASSISTED TOMOGRAPHY; DIZYGOTIC TWINS; ENVIRONMENTAL FACTOR; FEMALE; HEREDITY; HUMAN; HUMAN EXPERIMENT; LEG MUSCLE; MALE; MONOZYGOTIC TWINS; MUSCLE ATROPHY; PHENOTYPIC VARIATION; QUANTITATIVE ANALYSIS; TIBIA; TIBIA SHAFT;

AGING; BONE AND BONES; ENVIRONMENT; FEMALE; HUMANS; MODELS, GENETIC; MULTIVARIATE ANALYSIS; MUSCLES; TWINS, DIZYGOTIC; TWINS, MONOZYGOTIC;

EID: 58649099368     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/jbmr.081008     Document Type: Article

References (74)

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.
2. Lindle RS, Metter EJ, Lynch NA, Fleg JL, Fozard JL, Tobin J, Roy TA, Hurley BF 1997 Age and gender comparisons of muscle strength in 654 women and men aged 20-93 yr. J Appl Physiol 83:1581-1587.
3. Doherty TJ 2003 Invited review: Aging and sarcopenia. J Appl Physiol 95:1717-1727.
4. Estrada M, Kleppinger A, Judge JO, Walsh SJ, Kuchel GA 2007 Functional impact of relative versus absolute sarcopenia in healthy older women. J Am Geriatr Soc 55:1712-1719.
5. Visser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, Simonsick EM, Harris TB 2005 Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci Med Sci 60:324-333.
6. Lord S, Sherrington C, Menz H, Close J 2007 Falls in Older People: Risk Factors and Strategies for Prevention, 2nd ed. Cambridge University Press, Cambridge, NY, USA.
7. Järvinen TL, Sievänen H, Khan KM, Heinonen A, Kannus P 2008 Shifting the focus in fracture prevention, from osteoporosis to falls. BMJ 336:124-126.
8. Russo CR, Lauretani F, Bandinelli S, Bartali B, Di Iorio A, Volpato S, Guralnik JM, Harris T, Ferrucci L 2003 Aging bone in men and women: Beyond changes in bone mineral density. Osteoporos Int 14:531-538.
9. Sigurdsson G, Aspelund T, Chang M, Jonsdottir B, Sigurdsson S, Eiriksdottir G, Gudmundsson A, Harris TB, Gudnason V, Lang TF 2006 Increasing sex difference in bone strength in old age: The Age, Gene/Environment Susceptibility-Reykjavik study (AGES-REYKJAVIK). Bone 39:644-651.
10. Johnell O, Kanis JA, Oden A, Johansson H, De Laet C, Delmas P, Eisman JA, Fujiwara S, Kroger H, Mellstrom D, Meunier PJ, Melton LJ III, O'Neill T, Pols H, Reeve J, Silman A, Tenenhouse A 2005 Predictive value of BMD for hip and other fractures. J Bone Miner Res 20:1185-1194.
11. Cummings SR, Melton LJ 2002 Epidemiology and outcomes of osteoporotic fractures. Lancet 359:1761-1767.
12. Karasik D, Kiel DP 2008 Genetics of the musculoskeletal system: A pleiotropic approach. J Bone Miner Res 23:788-802.
13. Ferretti JL, Capozza RF, Cointry GR, Garcia SL, Plotkin H, Alvarez Filgueira ML, Zanchetta JR 1998 Gender-related differences in the relationship between densitometric values of whole-body bone mineral content and lean body mass in humans between 2 and 87 years of age. Bone 22:683-690.
14. Schoenau E, Neu CM, Beck B, Manz F, Rauch F 2002 Bone mineral content per muscle cross-sectional area as an index of the functional muscle-bone unit. J Bone Miner Res 17:1095-1101.
15. Lauretani F, Bandinelli S, Russo CR, Maggio M, Di Iorio A, Cherubini A, Maggio D, Ceda GP, Valenti G, Guralnik JM, Ferrucci L 2006 Correlates of bone quality in older persons. Bone 39:915-921.
16. Rantalainen T, Heinonen A, Komi PV, Linnamo V 2008 Neuromuscular performance and bone structural characteristics in young healthy men and women. Eur J Appl Physiol 102:215-222.
17. Sievänen H, Heinonen A, Kannus P 1996 Adaptation of bone to altered loading environment: A biomechanical approach using X-ray absorptiometric data from the patella of a young woman. Bone 19:55-59.
18. Proctor DN, Melton LJ, Khosla S, Crowson CS, O'Connor MK, Riggs BL 2000 Relative influence of physical activity, muscle mass and strength on bone density. Osteoporos Int 11:944-952.
19. Sievänen H 2000 A physical model for dual-energy X-ray absorptiometry-dcrived bone mineral density. Invest Radiol 35:325-330.
20. Taaffe DR, Lang TF, Fuerst T, Cauley JA, Nevitt MC, Harris TB 2003 Sex- and race-related differences in cross-sectional geometry and bone density of the femoral mid-shaft in older adults. Ann Hum Biol 30:329-346.
21. Nikander R, Sievänen H, Uusi-Rasi K, Heinonen A, Kannus P 2006 Loading modalities and bone structures at nonweight-bearing upper extremity and weight-bearing lower extremity: A pQCT study of adult female athletes. Bone 39:886-894.
22. Rittweger J, Beller G, Ehrig J, Jung C, Koch U, Ramolla J, Schmidt F, Newitt D, Majumdar S, Schiessl H, Felsenberg D 2000 Bone-muscle strength indices for the human lower leg. Bone 27:319-326.
23. Frost HM 2003 Bone's mechanostat: A 2003 update. Anat Rec A Discov Mol Cell Evol Biol 275:1081-1101.
24. Sun X, Lei SF, Deng FY, Wu S, Papacian C, Hamilton J, Recker RR, Deng HW 2006 Genetic and environmental correlations between bone geometric parameters and body compositions. Calcif Tissue Int 79:43-49.
25. Seeman E, Hopper JL, Young NR, 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.
26. Nguyen TV, Howard GM, Kelly PJ, Eisman JA 1998 Bone mass, lean mass, and fat mass: Same genes or same environments? Am J Epidemiol 147:3-16.
27. Sievänen H, Koskue V, Rauhio A, Kannus P, Heinonen A, Vuori I 1998 Peripheral quantitative computed tomography in human long bones: Evaluation of in vitro and in vivo precision. J Bone Miner Res 13:871-882.
28. Kaprio J, Koskenvuo M 2002 Genetic and environmental factors in complex diseases: The older Finnish Twin Cohort. Twin Res 5:358-365.
29. Kaprio J, Sarna S, Koskenvuo M, Rantasalo I 1978 The Finnish Twin Registry: Formation and compilation, questionnaire study, zygosity determination procedures, and research program. Prog Clin Biol Res 24:179-184.
30. Martin RB 1991 Determinants of the mechanical properties of bones. J Biomech 24(Suppl 1):79-88.
31. Carter DR, Hayes WC 1976 Bone compressive strength: The influence of density and strain rate. Science 194:1174-1176.
32. Grimby G 1986 Physical activity and muscle training in the elderly. Acta Med Scand Suppl 711:233-237.
33. Posthuma D, Beem AL, de Geus EJ, van Baal GC, von Hjelmborg JB, Iachine I, Boomsma DI 2003 Theory and practice in quantitative genetics. Twin Res 6:361-376.
34. Rijsdijk FV, Sham PC 2002 Analytic approaches to twin data using structural equation models. Brief Bioinform 3:119-133.
35. Neale MC, Cardon LR 1992 Methodology for Genetic Studies of Twins and Families. Kluwer, Dordrecht, The Netherlands.
36. Plomin R, DeFries JC, McClearn GE, McGuffin P 2001 Behavioral Genetics, 4th ed. Worth Publishers, New York, NY, USA.
37. Neale MC, Boker SM, Xie G, Maes HH 2003 Mx: Statistical Modeling. 6th ed. Department of Psychiatry, Virginia Commonwealth University, Richmond, VA, USA.
38. Prior SJ, Roth SM, Wang X, Kammerer C, Miljkovic-Gacic I, Bunker CH, Wheeler VW, Patrick AL, Zmuda JM 2007 Genetic and environmental influences on skeletal muscle phenotypes as a function of age and sex in large, multigenerational families of African heritage. J Appl Physiol 103:1121-1127.
39. Thomis MA, Beunen GP, Van Leemputte M, Maes HH, Blimkie CJ, Claessens AL, Marchal G, Willems E, Vlietinck RF 1998 Inheritance of static and dynamic arm strength and some of its determinants. Acta Physiol Scand 163:59-71.
40. Tiainen K, Sipilä S, Alén M, Heikkinen E, Kaprio J, Koskenvuo M, Tolvanen A, Pajala S, Rantanen T 2005 Shared genetic and environmental effects on strength and power in older female twins. Med Sci Sports Exerc 37:72-78.
41. Tiainen KM, Perola M, Kovanen VM, Sipilä S, Tuononen KA, Rikalainen K, Kauppinen MA, Widen EI, Kaprio J, Rantanen T, Kujala UM 2008 Genetics of maximal walking speed and skeletal muscle characteristics in older women. Twin Res Hum Genet 11:321-334.
42. Li X, Mohan S, Gu W, Wergedal J, Baylink DJ 2001 Quantitative assessment of forearm muscle size, forelimb grip strength, forearm bone mineral density, and forearm bone size in determining humerus breaking strength in 10 inbred strains of mice. Calcif Tissue Int 68:365-369.
43. Kaye M, Kusy RP 1995 Genetic lineage, bone mass, and physical activity in mice. Bone 17:131-135.
44. Xu H, Long JR, Yang YJ, Deng FY, Deng HW 2006 Genetic determination and correlation of body weight and body mass index (BMI) and cross-sectional geometric parameters of the femoral neck. Osteoporos Int 17:1602-1607.
45. Deng FY, Lei SF, Li MX, Jiang C, Dvornyk V, Deng HW 2006 Genetic determination and correlation of body mass index and bone mineral density at the spine and hip in Chinese Han ethnicity. Osteoporos Int 17:119-124.
46. Mikkola TM, Sipilä S, Rantanen T, Sievänen H, Suominen H, Kaprio J, Koskenvuo M, Kauppinen M, Heinonen A 2008 Genetic and environmental influence on structural strength of weight-bearing and non-weight-bearing bone: A twin study. J Bone Miner Res 23:492-498.
47. Videman T, Levälahti E, Battie MC, Simonen R, Vanninen E, Kaprio J 2007 Heritability of BMD of femoral neck and lumbar spine: A multivariate twin study of Finnish men. J Bone Miner Res 22:1455-1462.
48. Heinonen A, Sievänen H, Kyröläinen H, Perttunen J, Kannus P 2001 Mineral mass, size, and estimated mechanical strength of triple jumpers' lower limb. Bone 29:279-285.
49. Falchetti A, Sferrazza C, Cepollaro C, Gozzini A, Del Monte F, Masi L, Napoli N, Di Fede G, Cannone V, Cusumano G, Pandolfo MC, Rini GB, Tanini A, Brandi ML 2007 FokI polymorphism of the vitamin D receptor gene correlates with parameters of bone mass and turnover in a female population of the Italian island of Lampedusa. Calcif Tissue Int 80:15-20.
50. Roth SM, Zmuda JM, Cauley JA, Shea PR, Ferrell RE 2004 Vitamin D receptor genotype is associated with fat-free mass and sarcopenia in elderly men. J Gerontol A Biol Sci Med Sci 59:10-15.
51. McPherron AC, Lawler AM, Lee SJ 1997 Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387:83-90.
52. Zhang ZL, He JW, Qin YJ, Hu YQ, Li M, Zhang H, Hu WW, Liu YJ, Gu JM 2008 Association between myostatin gene polymorphisms and peak BMD variation in Chinese nuclear families. Osteoporos Int 19:39-47.
53. Adamo ML, Farrar RP 2006 Resistance training, and IGF involvement in the maintenance of muscle mass during the aging process. Ageing Res Rev 5:310-331.
54. Niu T, Rosen CJ 2005 The insulin-like growth factor-I gene and osteoporosis: A critical appraisal. Gene 361:38-56.
55. Rivadeneira F, Houwing-Duistermaat JJ, Beck TJ, Janssen JA, Hofman A, Pols HA, Van Duijn CM, Uitterlinden AG 2004 The influence of an insulin-like growth factor I gene promoter polymorphism on hip bone geometry and the risk of nonvertebral fracture in the elderly: The Rotterdam Study. J Bone Miner Res 19:1280-1290.
56. Kostek MC, Delmonico MJ, Reichel JB, Roth SM, Douglass L, Ferrell RE, Hurley BF 2005 Muscle strength response to strength training is influenced by insulin-like growth factor 1 genotype in older adults. J Appl Physiol 98:2147-2154.
57. Walsh S, Zmuda JM, Cauley JA, Shea PR, Metter EJ, Hurley BF, Ferrell RE, Roth SM 2005 Androgen receptor CAG repeat polymorphism is associated with fat-free mass in men. J Appl Physiol 98:132-137.
58. Stiger F, Brändström H, Gillberg P, Melhus H, Wolk A, Michaelsson K, Kindmark A 2008 Association between repeat length of exon 1 CAG microsatellite in the androgen receptor and bone density in men is modulated by sex hormone levels. Calcif Tissue Int 82:427-435.
59. Currey JD 2002 Bones: Structure and Mechanics. Princeton University Press, Princeton, NJ, USA.
60. Borer KT, Fogleman K, Gross M, La New JM, Dengel D 2007 Walking intensity for postmenopausal bone mineral preservation and accrual. Bone 41:713-721.
61. Daly RM, Saxon L, Turner CH, Robling AG, Bass SL 2004 The relationship between muscle size and bone geometry during growth and in response to exercise. Bone 34:281-287.
62. Rittweger J, Frost HM, Schiessl H, Ohshima H, Alkner B, Tesch P, Felsenberg D 2005 Muscle atrophy and bone loss after 90 days' bed rest and the effects of flywheel resistive exercise and pamidronate: Results from the LTBR study. Bone 36:1019-1029.
63. Mikkola T, Sipilä S, Portegijs E, Kallinen M, Alén M, Kiviranta I, Pekkonen M, Heinonen A 2007 Impaired geometric properties of tibia in older women with hip fracture history. Osteoporos Int 18:1083-1090.
64. Eser P, Frotzler A, Zehnder Y, Wick L, Knecht H, Denoth J, Schiessl H 2004 Relationship between the duration of paralysis and bone structure: A pQCT study of spinal cord injured individuals. Bone 34:869-880.
65. Natri A, Sievänen H, Parkkari J, Kannus P, Vihtonen K, Koskela J, Järvinen M 1999 Spontaneous shaft fracture of the tibia in weightlifting. A case report with dual-energy X-ray absorptiometry and peripheral quantitative computed tomography measurements. Am J Sports Med 27:238-240.
66. Uusi-Rasi K, Sievänen H, Pasanen M, Oja P, Vuori I 2002 Associations of calcium intake and physical activity with bone density and size in premenopausal and postmenopausal women: A peripheral quantitative computed tomography study. J Bone Miner Res 17:544-552.
67. Natsui K, Tanaka K, Suda M, Yasoda A, Sakuma Y, Ozasa A, Ozaki S, Nakao K 2006 High-dose glucocorticoid treatment induces rapid loss of trabecular bone mineral density and lean body mass. Osteoporos Int 17:105-108.
68. Sipilä S 2003 Body composition and muscle performance during menopause and hormone replacement therapy. J Endocrinol Invest 26:893-901.
69. Wells G, Tugwell P, Shea B, Guyatt G, Peterson J, Zytaruk N, Robinson V, Henry D, O'Connell D, Cranney A Osteoporosis Methodology Group, The Osteoporosis Research Advisory Group 2002 Meta-analyses of therapies for postmenopausal osteoporosis. V. Meta-analysis of the efficacy of hormone replacement therapy in treating and preventing osteoporosis in postmenopausal women. Endocr Rev 23:529-539.
70. Khan KM, Bennell KL, Hopper JL, Flicker L, Nowson CA, Sherwin AJ, Crichton KJ, Harcourt PR, Wark JD 1998 Self-reported ballet classes undertaken at age 10-12 years and hip bone mineral density in later life. Osteoporos Int 8:165-173.
71. Kalkwarf HJ, Khoury JC, Lanphear BP 2003 Milk intake during childhood and adolescence, adult bone density, and osteoporotic fractures in US women. Am J Clin Nutr 77:257-265.
72. Opotowsky AR, Bilezikian JP 2003 Racial differences in the effect of early milk consumption on peak and postmenopausal bone mineral density. J Bone Miner Res 18:1978-1988.
73. Lanham SA, Roberts C, Perry MJ, Cooper C, Oreffo RO 2008 Intrauterine programming of bone. Part 2: Alteration of skeletal structure. Osteoporos Int 19:157-167.
74. Bolotin HH, Sievänen H, Grashuis JL 2003 Patient-specific DXA bone mineral density inaccuracies: Quantitative effects of nonuniform extraosseous fat distributions. J Bone Miner Res 18:1020-1027.