Endocrinology and Metabolism

  • 제33권4호
  • /
  • Pages.435-444
  • /
  • 2018
  • /
  • 2093-596X(pISSN)
  • /
  • 2093-5978(eISSN)
대한내분비학회 (The Korean Endocrine Society)
권호 표지
DOI QR코드

DOI QR Code

Effects of Resistance Exercise on Bone Health

  • Hong, A Ram (Department of Internal Medicine, Chonnam National University Medical School) ;
  • Kim, Sang Wan (Department of Internal Medicine, Seoul National University College of Medicine and Seoul Metropolitan Government Seoul National University Boramae Medical Center)
  • 투고 : 2018.10.26
  • 심사 : 2018.11.02
  • 발행 : 2018.12.31
⟨ 이전 논문 다음 논문 ⟩

초록

The prevalence of chronic diseases including osteoporosis and sarcopenia increases as the population ages. Osteoporosis and sarcopenia are commonly associated with genetics, mechanical factors, and hormonal factors and primarily associated with aging. Many older populations, particularly those with frailty, are likely to have concurrent osteoporosis and sarcopenia, further increasing their risk of disease-related complications. Because bones and muscles are closely interconnected by anatomy, metabolic profile, and chemical components, a diagnosis should be considered for both sarcopenia and osteoporosis, which may be treated with optimal therapeutic interventions eliciting pleiotropic effects on both bones and muscles. Exercise training has been recommended as a promising therapeutic strategy to encounter the loss of bone and muscle mass due to osteosarcopenia. To stimulate the osteogenic effects for bone mass accretion, bone tissues must be exposed to mechanical load exceeding those experienced during daily living activities. Of the several exercise training programs, resistance exercise (RE) is known to be highly beneficial for the preservation of bone and muscle mass. This review summarizes the mechanisms of RE for the preservation of bone and muscle mass and supports the clinical evidences for the use of RE as a therapeutic option in osteosarcopenia.

키워드

과제정보

연구 과제 주관 기관 : National Research Foundation of Korea

참고문헌

  1. Reginster JY, Burlet N. Osteoporosis: a still increasing prevalence. Bone 2006;38(2 Suppl 1):S4-9.
  2. Consensus development conference: diagnosis, prophylaxis, and treatment of osteoporosis. Am J Med 1993;94:646-50. https://doi.org/10.1016/0002-9343(93)90218-E
  3. Kanis JA, Gluer CC. An update on the diagnosis and assessment of osteoporosis with densitometry. Committee of Scientific Advisors, International Osteoporosis Foundation. Osteoporos Int 2000;11:192-202. https://doi.org/10.1007/s001980050281
  4. Walston JD. Sarcopenia in older adults. Curr Opin Rheumatol 2012;24:623-7. https://doi.org/10.1097/BOR.0b013e328358d59b
  5. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing 2010;39:412-23. https://doi.org/10.1093/ageing/afq034
  6. Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, et al. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc 2011;12:249-56. https://doi.org/10.1016/j.jamda.2011.01.003
  7. Abimanyi-Ochom J, Watts JJ, Borgstrom F, Nicholson GC, Shore-Lorenti C, Stuart AL, et al. Changes in quality of life associated with fragility fractures: Australian arm of the International Cost and Utility Related to Osteoporotic Fractures Study (AusICUROS). Osteoporos Int 2015;26:1781-90. https://doi.org/10.1007/s00198-015-3088-z
  8. Peterson SJ, Braunschweig CA. Prevalence of sarcopenia and associated outcomes in the clinical setting. Nutr Clin Pract 2016;31:40-8. https://doi.org/10.1177/0884533615622537
  9. Curtis E, Litwic A, Cooper C, Dennison E. Determinants of muscle and bone aging. J Cell Physiol 2015;230:2618-25. https://doi.org/10.1002/jcp.25001
  10. 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. https://doi.org/10.1016/j.jamda.2014.10.018
  11. Beck BR, Daly RM, Singh MA, Taaffe DR. Exercise and Sports Science Australia (ESSA) position statement on exercise prescription for the prevention and management of osteoporosis. J Sci Med Sport 2017;20:438-45. https://doi.org/10.1016/j.jsams.2016.10.001
  12. Fleg JL. Aerobic exercise in the elderly: a key to successful aging. Discov Med 2012;13:223-8.
  13. Palombaro KM, Black JD, Buchbinder R, Jette DU. Effectiveness of exercise for managing osteoporosis in women postmenopause. Phys Ther 2013;93:1021-5. https://doi.org/10.2522/ptj.20110476
  14. Frost HM. Vital biomechanics: proposed general concepts for skeletal adaptations to mechanical usage. Calcif Tissue Int 1988;42:145-56. https://doi.org/10.1007/BF02556327
  15. Zehnacker CH, Bemis-Dougherty A. Effect of weighted exercises on bone mineral density in post menopausal women: a systematic review. J Geriatr Phys Ther 2007;30:79-88. https://doi.org/10.1519/00139143-200708000-00007
  16. Turner CH, Robling AG. Mechanisms by which exercise improves bone strength. J Bone Miner Metab 2005;23 Suppl:16-22. https://doi.org/10.1007/BF03026318
  17. Howe TE, Shea B, Dawson LJ, Downie F, Murray A, Ross C, et al. Exercise for preventing and treating osteoporosis in postmenopausal women. Cochrane Database Syst Rev 2011;7:CD000333.
  18. Martyn-St James M, Carroll S. Meta-analysis of walking for preservation of bone mineral density in postmenopausal women. Bone 2008;43:521-31. https://doi.org/10.1016/j.bone.2008.05.012
  19. Taaffe DR, Snow-Harter C, Connolly DA, Robinson TL, Brown MD, Marcus R. Differential effects of swimming versus weight-bearing activity on bone mineral status of eumenorrheic athletes. J Bone Miner Res 1995;10:586-93.
  20. Rector RS, Rogers R, Ruebel M, Hinton PS. Participation in road cycling vs running is associated with lower bone mineral density in men. Metabolism 2008;57:226-32. https://doi.org/10.1016/j.metabol.2007.09.005
  21. Floras JS, Notarius CF, Harvey PJ. Exercise training: not a class effect. Blood pressure more buoyant after swimming than walking. J Hypertens 2006;24:269-72. https://doi.org/10.1097/01.hjh.0000202814.79964.84
  22. Guadalupe-Grau A, Fuentes T, Guerra B, Calbet JA. Exercise and bone mass in adults. Sports Med 2009;39:439-68. https://doi.org/10.2165/00007256-200939060-00002
  23. Ma D, Wu L, He Z. Effects of walking on the preservation of bone mineral density in perimenopausal and postmenopausal women: a systematic review and meta-analysis. Menopause 2013;20:1216-26. https://doi.org/10.1097/GME.0000000000000100
  24. Ebrahim S, Thompson PW, Baskaran V, Evans K. Randomized placebo-controlled trial of brisk walking in the prevention of postmenopausal osteoporosis. Age Ageing 1997;26:253-60. https://doi.org/10.1093/ageing/26.4.253
  25. Nikander R, Gagnon C, Dunstan DW, Magliano DJ, Ebeling PR, Lu ZX, et al. Frequent walking, but not total physical activity, is associated with increased fracture incidence: a 5-year follow-up of an Australian population-based prospective study (AusDiab). J Bone Miner Res 2011;26:1638-47. https://doi.org/10.1002/jbmr.363
  26. Sherrington C, Tiedemann A, Fairhall N, Close JC, Lord SR. Exercise to prevent falls in older adults: an updated meta-analysis and best practice recommendations. N S W Public Health Bull 2011;22:78-83. https://doi.org/10.1071/NB10056
  27. Allison SJ, Poole KE, Treece GM, Gee AH, Tonkin C, Rennie WJ, et al. The influence of high-impact exercise on cortical and trabecular bone mineral content and 3d distribution across the proximal femur in older men: a randomized controlled unilateral intervention. J Bone Miner Res 2015;30:1709-16. https://doi.org/10.1002/jbmr.2499
  28. Bailey CA, Brooke-Wavell K. Optimum frequency of exercise for bone health: randomised controlled trial of a highimpact unilateral intervention. Bone 2010;46:1043-9. https://doi.org/10.1016/j.bone.2009.12.001
  29. Marques EA, Mota J, Carvalho J. Exercise effects on bone mineral density in older adults: a meta-analysis of randomized controlled trials. Age (Dordr) 2012;34:1493-515. https://doi.org/10.1007/s11357-011-9311-8
  30. Frost HM. Bone "mass" and the "mechanostat": a proposal. Anat Rec 1987;219:1-9. https://doi.org/10.1002/ar.1092190104
  31. Borde R, Hortobagyi T, Granacher U. Dose-response relationships of resistance training in healthy old adults: a systematic review and meta-analysis. Sports Med 2015;45:1693-720. https://doi.org/10.1007/s40279-015-0385-9
  32. Stewart VH, Saunders DH, Greig CA. Responsiveness of muscle size and strength to physical training in very elderly people: a systematic review. Scand J Med Sci Sports 2014;24:e1-10. https://doi.org/10.1111/sms.12123
  33. World Health Organization. Global recommendations on physical activity for health. Geneva: World Health Organization; 2010.
  34. Kerr D, Morton A, Dick I, Prince R. Exercise effects on bone mass in postmenopausal women are site-specific and load-dependent. J Bone Miner Res 1996;11:218-25.
  35. Zhao R, Zhao M, Xu Z. The effects of differing resistance training modes on the preservation of bone mineral density in postmenopausal women: a meta-analysis. Osteoporos Int 2015;26:1605-18. https://doi.org/10.1007/s00198-015-3034-0
  36. Marcus R, Feldman D, Dempster DW, Luckey M, Cauley JA. Osteoporosis. 4th ed. Amsterdam: Elsevier; 2013. Chapter 29, Physical activity and exercise in the maintenance of the adult skeleton and the prevention of osteoporotic fractures; p. 683-719.
  37. Martyn-St James M, Carroll S. Progressive high-intensity resistance training and bone mineral density changes among premenopausal women: evidence of discordant site-specific skeletal effects. Sports Med 2006;36:683-704. https://doi.org/10.2165/00007256-200636080-00005
  38. Steib S, Schoene D, Pfeifer K. Dose-response relationship of resistance training in older adults: a meta-analysis. Med Sci Sports Exerc 2010;42:902-14. https://doi.org/10.1249/MSS.0b013e3181c34465
  39. von Stengel S, Kemmler W, Kalender WA, Engelke K, Lauber D. Differential effects of strength versus power training on bone mineral density in postmenopausal women: a 2-year longitudinal study. Br J Sports Med 2007;41:649-55. https://doi.org/10.1136/bjsm.2006.033480
  40. Stengel SV, Kemmler W, Pintag R, Beeskow C, Weineck J, Lauber D, et al. Power training is more effective than strength training for maintaining bone mineral density in postmenopausal women. J Appl Physiol (1985) 2005;99:181-8. https://doi.org/10.1152/japplphysiol.01260.2004
  41. Izquierdo M, Cadore EL. Muscle power training in the institutionalized frail: a new approach to counteracting functional declines and very late-life disability. Curr Med Res Opin 2014;30:1385-90. https://doi.org/10.1185/03007995.2014.908175
  42. Giangregorio LM, Papaioannou A, Macintyre NJ, Ashe MC, Heinonen A, Shipp K, et al. Too fit to fracture: exercise recommendations for individuals with osteoporosis or osteoporotic vertebral fracture. Osteoporos Int 2014;25:821-35. https://doi.org/10.1007/s00198-013-2523-2
  43. Clark BC. In vivo alterations in skeletal muscle form and function after disuse atrophy. Med Sci Sports Exerc 2009;41:1869-75. https://doi.org/10.1249/MSS.0b013e3181a645a6
  44. Atherton PJ, Smith K. Muscle protein synthesis in response to nutrition and exercise. J Physiol 2012;590:1049-57. https://doi.org/10.1113/jphysiol.2011.225003
  45. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2012;149:274-93. https://doi.org/10.1016/j.cell.2012.03.017
  46. Yan Z, Biggs RB, Booth FW. Insulin-like growth factor immunoreactivity increases in muscle after acute eccentric contractions. J Appl Physiol (1985) 1993;74:410-4. https://doi.org/10.1152/jappl.1993.74.1.410
  47. Coleman ME, DeMayo F, Yin KC, Lee HM, Geske R, Montgomery C, et al. Myogenic vector expression of insulin-like growth factor I stimulates muscle cell differentiation and myofiber hypertrophy in transgenic mice. J Biol Chem 1995;270:12109-16. https://doi.org/10.1074/jbc.270.20.12109
  48. Goldspink DF, Cox VM, Smith SK, Eaves LA, Osbaldeston NJ, Lee DM, et al. Muscle growth in response to mechanical stimuli. Am J Physiol 1995;268(2 Pt 1):E288-97.
  49. Adams GR, Haddad F. The relationships among IGF-1, DNA content, and protein accumulation during skeletal muscle hypertrophy. J Appl Physiol (1985) 1996;81:2509-16. https://doi.org/10.1152/jappl.1996.81.6.2509
  50. Musaro A, McCullagh K, Paul A, Houghton L, Dobrowolny G, Molinaro M, et al. Localized IGF-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 2001;27:195-200. https://doi.org/10.1038/84839
  51. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, et al. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 2001;3:1009-13. https://doi.org/10.1038/ncb1101-1009
  52. Hornberger TA, Stuppard R, Conley KE, Fedele MJ, Fiorotto ML, Chin ER, et al. Mechanical stimuli regulate rapamycin-sensitive signalling by a phosphoinositide 3-kinase-, protein kinase B- and growth factor-independent mechanism. Biochem J 2004;380(Pt 3):795-804. https://doi.org/10.1042/bj20040274
  53. O'Neil TK, Duffy LR, Frey JW, Hornberger TA. The role of phosphoinositide 3-kinase and phosphatidic acid in the regulation of mammalian target of rapamycin following eccentric contractions. J Physiol 2009;587(Pt 14):3691-701. https://doi.org/10.1113/jphysiol.2009.173609
  54. Spangenburg EE, Le Roith D, Ward CW, Bodine SC. A functional insulin-like growth factor receptor is not necessary for load-induced skeletal muscle hypertrophy. J Physiol 2008;586:283-91. https://doi.org/10.1113/jphysiol.2007.141507
  55. West DW, Kujbida GW, Moore DR, Atherton P, Burd NA, Padzik JP, et al. Resistance exercise-induced increases in putative anabolic hormones do not enhance muscle protein synthesis or intracellular signalling in young men. J Physiol 2009;587(Pt 21):5239-47. https://doi.org/10.1113/jphysiol.2009.177220
  56. Fang Y, Vilella-Bach M, Bachmann R, Flanigan A, Chen J. Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 2001;294:1942-5. https://doi.org/10.1126/science.1066015
  57. You JS, Lincoln HC, Kim CR, Frey JW, Goodman CA, Zhong XP, et al. The role of diacylglycerol kinase ${\zeta}$ and phosphatidic acid in the mechanical activation of mammalian target of rapamycin (mTOR) signaling and skeletal muscle hypertrophy. J Biol Chem 2014;289:1551-63. https://doi.org/10.1074/jbc.M113.531392
  58. Jacobs BL, You JS, Frey JW, Goodman CA, Gundermann DM, Hornberger TA. Eccentric contractions increase the phosphorylation of tuberous sclerosis complex-2 (TSC2) and alter the targeting of TSC2 and the mechanistic target of rapamycin to the lysosome. J Physiol 2013;591:4611-20. https://doi.org/10.1113/jphysiol.2013.256339
  59. Koopman R, van Loon LJ. Aging, exercise, and muscle protein metabolism. J Appl Physiol (1985) 2009;106:2040-8. https://doi.org/10.1152/japplphysiol.91551.2008
  60. Burd NA, Tang JE, Moore DR, Phillips SM. Exercise training and protein metabolism: influences of contraction, protein intake, and sex-based differences. J Appl Physiol (1985) 2009;106:1692-701. https://doi.org/10.1152/japplphysiol.91351.2008
  61. Smith SM, Heer MA, Shackelford LC, Sibonga JD, Ploutz-Snyder L, Zwart SR. Benefits for bone from resistance exercise and nutrition in long-duration spaceflight: evidence from biochemistry and densitometry. J Bone Miner Res 2012;27:1896-906. https://doi.org/10.1002/jbmr.1647
  62. Evans WJ. Effects of exercise on body composition and functional capacity of the elderly. J Gerontol A Biol Sci Med Sci 1995;50 Spec No:147-50.
  63. Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA, Evans WJ. High-intensity strength training in nonagenarians: effects on skeletal muscle. JAMA 1990;263:3029-34. https://doi.org/10.1001/jama.1990.03440220053029
  64. Fiatarone MA, O'Neill EF, Ryan ND, Clements KM, Solares GR, Nelson ME, et al. Exercise training and nutritional supplementation for physical frailty in very elderly people. N Engl J Med 1994;330:1769-75. https://doi.org/10.1056/NEJM199406233302501
  65. Greig CA, Gray C, Rankin D, Young A, Mann V, Noble B, et al. Blunting of adaptive responses to resistance exercise training in women over 75y. Exp Gerontol 2011;46:884-90. https://doi.org/10.1016/j.exger.2011.07.010
  66. Hakkinen K, Kallinen M, Izquierdo M, Jokelainen K, Lassila H, Malkia E, et al. Changes in agonist-antagonist EMG, muscle CSA, and force during strength training in middleaged and older people. J Appl Physiol (1985) 1998;84:1341-9. https://doi.org/10.1152/jappl.1998.84.4.1341
  67. Raue U, Slivka D, Minchev K, Trappe S. Improvements in whole muscle and myocellular function are limited with high-intensity resistance training in octogenarian women. J Appl Physiol (1985) 2009;106:1611-7. https://doi.org/10.1152/japplphysiol.91587.2008
  68. Welle S, Totterman S, Thornton C. Effect of age on muscle hypertrophy induced by resistance training. J Gerontol A Biol Sci Med Sci 1996;51:M270-5.
  69. Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, et al. Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol 2009;587:211-7. https://doi.org/10.1113/jphysiol.2008.164483
  70. Hameed M, Orrell RW, Cobbold M, Goldspink G, Harridge SD. Expression of IGF-I splice variants in young and old human skeletal muscle after high resistance exercise. J Physiol 2003;547(Pt 1):247-54. https://doi.org/10.1113/jphysiol.2002.032136
  71. Gianoudis J, Bailey CA, Ebeling PR, Nowson CA, Sanders KM, Hill K, et al. Effects of a targeted multimodal exercise program incorporating high-speed power training on falls and fracture risk factors in older adults: a community-based randomized controlled trial. J Bone Miner Res 2014;29:182-91. https://doi.org/10.1002/jbmr.2014
  72. Guirguis-Blake JM, Michael YL, Perdue LA, Coppola EL, Beil TL. Interventions to prevent falls in older adults: updated evidence report and systematic review for the US preventive services task force. JAMA 2018;319:1705-16. https://doi.org/10.1001/jama.2017.21962
  73. Frost HM. Bone's mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol 2003;275:1081-101.
  74. Klein-Nulend J, Bakker AD, Bacabac RG, Vatsa A, Weinbaum S. Mechanosensation and transduction in osteocytes. Bone 2013;54:182-90. https://doi.org/10.1016/j.bone.2012.10.013
  75. Galea GL, Lanyon LE, Price JS. Sclerostin's role in bone's adaptive response to mechanical loading. Bone 2017;96:38-44. https://doi.org/10.1016/j.bone.2016.10.008
  76. Martyn-St James M, Carroll S. A meta-analysis of impact exercise on postmenopausal bone loss: the case for mixed loading exercise programmes. Br J Sports Med 2009;43:898-908. https://doi.org/10.1136/bjsm.2008.052704
  77. Bolam KA, van Uffelen JG, Taaffe DR. The effect of physical exercise on bone density in middle-aged and older men: a systematic review. Osteoporos Int 2013;24:2749-62. https://doi.org/10.1007/s00198-013-2346-1
  78. Kukuljan S, Nowson CA, Sanders KM, Nicholson GC, Seibel MJ, Salmon J, et al. Independent and combined effects of calcium-vitamin D3 and exercise on bone structure and strength in older men: an 18-month factorial design randomized controlled trial. J Clin Endocrinol Metab 2011;96:955-63. https://doi.org/10.1210/jc.2010-2284
  79. Liu-Ambrose TY, Khan KM, Eng JJ, Heinonen A, McKay HA. Both resistance and agility training increase cortical bone density in 75- to 85-year-old women with low bone mass: a 6-month randomized controlled trial. J Clin Densitom 2004;7:390-8. https://doi.org/10.1385/JCD:7:4:390
  80. Faulkner KG, Wacker WK, Barden HS, Simonelli C, Burke PK, Ragi S, et al. Femur strength index predicts hip fracture independent of bone density and hip axis length. Osteoporos Int 2006;17:593-9. https://doi.org/10.1007/s00198-005-0019-4
  81. Leslie WD, Pahlavan PS, Tsang JF, Lix LM; Manitoba Bone Density Program. Prediction of hip and other osteoporotic fractures from hip geometry in a large clinical cohort. Osteoporos Int 2009;20:1767-74. https://doi.org/10.1007/s00198-009-0874-5
  82. LaCroix AZ, Beck TJ, Cauley JA, Lewis CE, Bassford T, Jackson R, et al. Hip structural geometry and incidence of hip fracture in postmenopausal women: what does it add to conventional bone mineral density? Osteoporos Int 2010;21:919-29. https://doi.org/10.1007/s00198-009-1056-1
  83. Lanyon LE, Rubin CT. Static vs dynamic loads as an influence on bone remodelling. J Biomech 1984;17:897-905. https://doi.org/10.1016/0021-9290(84)90003-4
  84. O'Connor JA, Lanyon LE, MacFie H. The influence of strain rate on adaptive bone remodelling. J Biomech 1982;15:767-81. https://doi.org/10.1016/0021-9290(82)90092-6
  85. Hsieh YF, Turner CH. Effects of loading frequency on mechanically induced bone formation. J Bone Miner Res 2001;16:918-24. https://doi.org/10.1359/jbmr.2001.16.5.918
  86. Rubin CT, Lanyon LE. Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int 1985;37:411-7. https://doi.org/10.1007/BF02553711
  87. Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am 1984;66:397-402. https://doi.org/10.2106/00004623-198466030-00012
  88. Robling AG, Burr DB, Turner CH. Recovery periods restore mechanosensitivity to dynamically loaded bone. J Exp Biol 2001;204(Pt 19):3389-99.
  89. Lanyon LE. Using functional loading to influence bone mass and architecture: objectives, mechanisms, and relationship with estrogen of the mechanically adaptive process in bone. Bone 1996;18(1 Suppl):37S-43S. https://doi.org/10.1016/8756-3282(95)00378-9
  90. Warden SJ, Mantila Roosa SM, Kersh ME, Hurd AL, Fleisig GS, Pandy MG, et al. Physical activity when young provides lifelong benefits to cortical bone size and strength in men. Proc Natl Acad Sci U S A 2014;111:5337-42. https://doi.org/10.1073/pnas.1321605111
  91. Kontulainen S, Sievanen H, Kannus P, Pasanen M, Vuori I. Effect of long-term impact-loading on mass, size, and estimated strength of humerus and radius of female racquetsports players: a peripheral quantitative computed tomography study between young and old starters and controls. J Bone Miner Res 2003;18:352-9. https://doi.org/10.1359/jbmr.2003.18.2.352
  92. Kelley GA, Kelley KS, Tran ZV. Resistance training and bone mineral density in women: a meta-analysis of controlled trials. Am J Phys Med Rehabil 2001;80:65-77. https://doi.org/10.1097/00002060-200101000-00017
  93. Martyn-St James M, Carroll S. High-intensity resistance training and postmenopausal bone loss: a meta-analysis. Osteoporos Int 2006;17:1225-40. https://doi.org/10.1007/s00198-006-0083-4
  94. Engelke K, Kemmler W, Lauber D, Beeskow C, Pintag R, Kalender WA. Exercise maintains bone density at spine and hip EFOPS: a 3-year longitudinal study in early postmenopausal women. Osteoporos Int 2006;17:133-42. https://doi.org/10.1007/s00198-005-1938-9
  95. Kukuljan S, Nowson CA, Bass SL, Sanders K, Nicholson GC, Seibel MJ, et al. Effects of a multi-component exercise program and calcium-vitamin-D3-fortified milk on bone mineral density in older men: a randomised controlled trial. Osteoporos Int 2009;20:1241-51. https://doi.org/10.1007/s00198-008-0776-y
  96. Gomez-Cabello A, Ara I, Gonzalez-Aguero A, Casajus JA, Vicente-Rodriguez G. Effects of training on bone mass in older adults: a systematic review. Sports Med 2012;42:301-25. https://doi.org/10.2165/11597670-000000000-00000
  97. Warden SJ, Fuchs RK, Castillo AB, Nelson IR, Turner CH. Exercise when young provides lifelong benefits to bone structure and strength. J Bone Miner Res 2007;22:251-9.
  98. Cheung AM, Detsky AS. Osteoporosis and fractures: missing the bridge? JAMA 2008;299:1468-70. https://doi.org/10.1001/jama.299.12.1468
  99. Jarvinen TL, Kannus P, Sievanen H. Have the DXA-based exercise studies seriously underestimated the effects of mechanical loading on bone? J Bone Miner Res 1999;14:1634-5. https://doi.org/10.1359/jbmr.1999.14.9.1634
  100. Bolotin HH, Sievanen H. Inaccuracies inherent in dual-energy X-ray absorptiometry in vivo bone mineral density can seriously mislead diagnostic/prognostic interpretations of patient-specific bone fragility. J Bone Miner Res 2001;16:799-805. https://doi.org/10.1359/jbmr.2001.16.5.799
  101. Beck TJ. Extending DXA beyond bone mineral density: understanding hip structure analysis. Curr Osteoporos Rep 2007;5:49-55. https://doi.org/10.1007/s11914-007-0002-4
  102. Watson SL, Weeks BK, Weis LJ, Harding AT, Horan SA, Beck BR. High-intensity resistance and impact training improves bone mineral density and physical function in postmenopausal women with osteopenia and osteoporosis: the LIFTMOR randomized controlled trial. J Bone Miner Res 2018;33:211-20. https://doi.org/10.1002/jbmr.3284
  103. Silva BC, Leslie WD, Resch H, Lamy O, Lesnyak O, Binkley N, et al. Trabecular bone score: a noninvasive analytical method based upon the DXA image. J Bone Miner Res 2014;29:518-30. https://doi.org/10.1002/jbmr.2176
  104. Polidoulis I, Beyene J, Cheung AM. The effect of exercise on pQCT parameters of bone structure and strength in postmenopausal women: a systematic review and meta-analysis of randomized controlled trials. Osteoporos Int 2012;23:39-51. https://doi.org/10.1007/s00198-011-1734-7
  105. Karinkanta S, Heinonen A, Sievanen H, Uusi-Rasi K, Pasanen M, Ojala K, et al. A multi-component exercise regimen to prevent functional decline and bone fragility in home-dwelling elderly women: randomized, controlled trial. Osteoporos Int 2007;18:453-62. https://doi.org/10.1007/s00198-006-0256-1