Skip to main content

Advertisement

Log in

Exercise, muscle, and the applied load-bone strength balance

  • Review
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

A fracture occurs when the applied load is greater than the bone can withstand. Clinical practice guidelines for the management of osteoporosis include recommendations for exercise; one of the few therapies where the proposed anti-fracture mechanisms that include effects on both bone strength and applied loads, where applied loads can come in the form of a fall, externally applied loads, body weight, or muscle forces. The aim of this review is to provide an overview of the clinical evidence pertaining to the potential efficacy of exercise for preventing fractures in older adults, including its direct effects on outcomes along the causal pathway to fractures (e.g., falls, posture, bone strength) and the indirect effects on muscle or the muscle-bone relationship. The evidence is examined as it pertains to application in clinical practice. Considerations for future research are discussed, such as the need for trials in individuals with low bone mass or students that evaluate whether changes in muscle mediate changes in bone. Future trials should also consider adequacy of calorie or protein intake, the confounding effect of exercise-induced weight loss, or the most appropriate therapeutic goal (e.g., strength, weight bearing, or hypertrophy) and outcome measures (e.g., fracture, disability, cost-effectiveness).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Papaioannou A, Morin S, Cheung AM, Atkinson S, Brown JP, Feldman S, Hanley DA, Hodsman A, Jamal SA, Kaiser SM, Kvern B, Siminoski K, Leslie WD, Scientific Advisory Council of Osteoporosis Canada (2010) 2010 clinical practice guidelines for the diagnosis and management of osteoporosis in Canada: summary. CMAJ 182:1864–1873

    Article  PubMed  PubMed Central  Google Scholar 

  2. Cheung AM, Detsky AS (2008) Osteoporosis and fractures: missing the bridge? JAMA 299:1468–1470

    Article  CAS  PubMed  Google Scholar 

  3. Cummings SR, Nevitt MC (1989) A hypothesis: the causes of hip fractures. J Gerontol 44:M107–M111

    Article  CAS  PubMed  Google Scholar 

  4. Nikander R, Gagnon C, Dunstan DW, Magliano DJ, Ebeling PR, ZX L, Zimmet PZ, Shaw JE, Daly RM (2011) 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 26:1638–1647

    Article  PubMed  Google Scholar 

  5. Rikkonen T, Salovaara K, Sirola J, Kärkkäinen M, Tuppurainen M, Jurvelin J, Honkanen R, Alhava E, Kröger H (2010) Physical activity slows femoral bone loss but promotes wrist fractures in postmenopausal women: a 15-year follow-up of the OSTPRE study. J Bone Miner Res 25:2332–2340

    Article  PubMed  Google Scholar 

  6. Gold DT, Shipp KM, Pieper CF, Duncan PW, Martinez S, Lyles KW (2004) Group treatment improves trunk strength and psychological status in older women with vertebral fractures: results of a randomized, clinical trial. J Am Geriatr Soc 52:1471–1478

    Article  PubMed  Google Scholar 

  7. Gillespie LD, Robertson MC, Gillespie WJ, Lamb SE, Gates S, Cumming RG, Rowe BH (2009) Interventions for preventing falls in older people living in the community. Cochrane Database Syst Rev 2

  8. Howe TE, Shea B, Dawson LJ, Downie F, Murray A, Ross C, Harbour RT, Caldwell LM, Creed G (2011) Exercise for preventing and treating osteoporosis in postmenopausal women. Cochrane Database Syst Rev 7:CD000333

    Google Scholar 

  9. El-Khoury F, Bernard C, Charles M, Dargent-Molina P (2015) The effect of fall prevention exercise programmes on fall induced injuries in community dwelling older adults. Br J Sports Med 49:1348

    Article  PubMed  Google Scholar 

  10. Kemmler W, Häberele L, von Stengel S (2013) Effects of exercise on fracture reduction in older adults. Osteoporosis Int 24:1937–1950

    Article  CAS  Google Scholar 

  11. Moayyeri A (2008) The association between physical activity and osteoporotic fractures: a review of the evidence and implications for future research. Ann Epidemiol 18:827–835

    Article  PubMed  Google Scholar 

  12. Armstrong ME, Cairns BJ, Banks E, Green J, Reeves GK, Beral V, Million Women Study Collaborators (2012) Different effects of age, adiposity and physical activity on the risk of ankle, wrist and hip fractures in postmenopausal women. Bone 50:1394–1400

    Article  Google Scholar 

  13. Englund U, Nordström P, Nilsson J, Bucht G, Björnstig U, Hallmans G, Svensson O, Pettersson U (2011) Physical activity in middle-aged women and hip fracture risk: the UFO study. Osteoporosis Int 22:499–505

    Article  CAS  Google Scholar 

  14. Jokinen H, Pulkkinen P, Korpelainen J, Heikkinen J, Keinänen-Kiukaanniemi S, Jämsä T, Korpelainen R (2010) Risk factors for cervical and trochanteric hip fractures in elderly women: a population-based 10-year follow-up study. Calcif Tissue Int 87:44–51

    Article  CAS  PubMed  Google Scholar 

  15. Määttä M, Terho E, Jokinen H, Pulkkinen P, Korpelainen J, Heikkinen J, Keinänen-Kiukaanniemi S, Jämsä T, Korpelainen R (2012) Lifestyle factors and site-specific risk of hip fracture in community dwelling older women—a 13-year prospective population-based cohort study. BMC Musculoskelet Disord 13

  16. Morseth B, Ahmed LA, Bjørnerem Å, Emaus N, Jacobsen BK, Joakimsen R, Størmer J, Wilsgaard T, Jørgensen L (2012) Leisure time physical activity and risk of non-vertebral fracture in men and women aged 55 years and older: the Tromsø study. Eur J Epidemiol 27:463–471

    Article  PubMed  Google Scholar 

  17. Rouzi AA, Al-Sibiani SA, Al-Senani NS, Radaddi RM, Ardawi MM (2012) Independent predictors of all osteoporosis-related fractures among healthy Saudi postmenopausal women: the CEOR study. Bone 50:713–722

    Article  PubMed  Google Scholar 

  18. Wactawski-Wende J, Larson J, Cauley J, Chen Z, LaCroix A, LaMonte M, Leboff M, Ockene J, Robbins J (2012) Physical activity and incident fracture in postmenopausal women: the Women’s Health Initiative Observational Study. J Bone Miner Res 27

  19. Gregson CL, Carson C, Amuzu A, Ebrahim S (2010) The association between graded physical activity in postmenopausal British women, and the prevalence and incidence of hip and wrist fractures. Age Ageing 39:565–574

    Article  PubMed  Google Scholar 

  20. Mackey DC, Hubbard AE, Cawthon PM, Cauley JA, Cummings SR, Tager IB, Osteoporotic Fractures in Men Research Group (2011) Usual physical activity and hip fracture in older men: an application of semiparametric methods to observational data. Am J Epidemiol 173(5):578–586

  21. Giangregorio LM, Papaioannou A, MacIntyre NJ, Ashe MC, Heinonen A, Shipp K, Wark J, McGill S, Keller H, Jain R, Laprade J, Cheung AM (2014) Too fit to fracture: exercise recommendations for individuals with osteoporosis or osteoporotic vertebral fracture. Osteoporosis Int 25:821–835

    Article  CAS  Google Scholar 

  22. Sherrington C, Tiedemann A, Fairhall N, Close JC, Lord SR (2011) Exercise to prevent falls in older adults: an updated meta-analysis and best practice recommendations. N S W Public Health Bull 22:78–83

    Article  PubMed  Google Scholar 

  23. El-Khoury F, Cassou B, Latouche A, Aegerter P, Charles MA, Dargent-Molina P (2015) Effectiveness of two year balance training programme on prevention of fall induced injuries in at risk women aged 75-85 living in community: Ossebo randomised controlled trial. BMJ 351:h3830

    Article  PubMed  PubMed Central  Google Scholar 

  24. Benichou O, Lord SR (2016) Rationale for strengthening muscle to prevent falls and fractures: a review of the evidence. Calcif Tissue Int 98:531–545

    Article  CAS  PubMed  Google Scholar 

  25. Giangregorio L, McGill S, Wark J, Laprade J, Heinonen A, Ashe M, MacIntyre N, Cheung A, Shipp K, Keller H (2015) Too fit to fracture: outcomes of a Delphi consensus process on physical activity and exercise recommendations for adults with osteoporosis with or without vertebral fractures. Osteoporosis Int 26:891–910

    Article  CAS  Google Scholar 

  26. Ishikawa Y, Miyakoshi N, Kasukawa Y, Hongo M, Shimada Y (2009) Spinal curvature and postural balance in patients with osteoporosis. Osteoporosis Int 20:2049–2053

    Article  CAS  Google Scholar 

  27. 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

    Article  PubMed  PubMed Central  Google Scholar 

  28. Diong J, Allen N, Sherrington C (2015) Structured exercise improves mobility after hip fracture: a meta-analysis with meta-regression. Br J Sports Med 50:346–355

    Article  PubMed  Google Scholar 

  29. Dufour AB, Roberts B, Broe KE, Kiel DP, Bouxsein ML, Hannan MT (2012) The factor-of-risk biomechanical approach predicts hip fracture in men and women: the Framingham study. Osteoporosis Int 23:513–520

    Article  CAS  Google Scholar 

  30. Maitland LA, Myers ER, Hipp JA, Hayes WC, Greenspan SL (1993) Read my hips: measuring trochanteric soft tissue thickness. Calcif Tissue Int 52:85–89

    Article  CAS  PubMed  Google Scholar 

  31. Bouxsein ML, Szulc P, Munoz F, Thrall E, Sornay-Rendu E, Delmas PD (2007) Contribution of trochanteric soft tissues to fall force estimates, the factor of risk, and prediction of hip fracture risk. J Bone Miner Res 22:825–831

    Article  PubMed  Google Scholar 

  32. Nielson CM, Bouxsein ML, Freitas SS, Ensrud KE, Orwoll ES (2009) Trochanteric soft tissue thickness and hip fracture in older men. J Clin Endocrinol Metab 94:491–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Malkov S, Cawthon PM, Peters KW, Cauley JA, Murphy RA, Visser M, Wilson JP, Harris T, Satterfield S, Cummings S, Shepherd JA (2015) Hi fractures risk in older men and women associated with DXA-derived measures of thigh subcutaneous fat thickness, cross-sectional muscle area, and muscle density. J Bone Miner Res 30:1414–1421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Briggs AM, Greig AM, Wark JD, Fazzalari NL, Bennell KL (2004) A review of anatomical and mechanical factors affecting vertebral body integrity. Int J Med Sci 1:170–180

    Article  PubMed  PubMed Central  Google Scholar 

  35. Greig AM, Briggs AM, Bennell KL, Hodges PW (2014) Trunk muscle activity is modified in osteoporotic vertebral fracture and thoracic kyphosis with potential consequences for vertebral health. PLoS One 9:e109515

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Katzman WB, Vittinghoff E, Kado DM, Lane NE, Ensrud KE, Shipp K (2016) Thoracic kyphosis and rate of incident vertebral fracture: the fracture intervention trial. Osteoporosis Int 27:899–903

    Article  CAS  Google Scholar 

  37. Iyer S, Christiansen BA, Roberts BJ, Valentine MJ, Manoharan RK, Bouxsein ML (2010) A biomechanical model for estimating loads on thoracic and lumbar vertebrae. Clin Biomech 25:853–858

    Article  Google Scholar 

  38. Bansal S, Katzman WB, Giangregorio LM (2014) Exercise for improving age-related hyperkyphotic posture: a systematic review. Arch Phys Med Rehabil 95:129–140

    Article  PubMed  Google Scholar 

  39. Katzman WB, Kado DM, Vittinghoff E, Lin F, Schafer A, Long RK, Wong S, Gladin A, Lane NE (2016) Targeted multi-modal spinal strengthening exercise program to reduce hyperkyphosis in older adults: preliminary results from the SHEAF study. American Society for Bone and Mineral Research meeting, abstract in press

  40. Giangregorio LM, MacIntyre NJ, Thabane L, Skidmore CJ, Papaioannou A (2013) Exercise for improving outcomes after osteoporotic vertebral fracture. Cochrane Database Syst Rev (1):CD008618. doi:10.1002/14651858.CD008618.pub2

  41. Sinaki M, Itoi E, Wahner W, Wollan P, Gelzcer R, Mullan P, Collins DA, Hodgson SF (2002) Stronger back muscles reduce the incidence of vertebral fractures: a prospective 10 year follow-up of postmenopausal women. Bone 30:836–841

    Article  CAS  PubMed  Google Scholar 

  42. Anderson DE, Quinn E, Parker E, Allaire BT, Muir JW, Rubin CT, Magaziner J, Hannan MT, Bouxsein ML, Kiel DP (2015) Associations of computed tomography-based trunk muscle size and density with balance and falls in older adults. J Gerontol A Biol Sci Med Sci

  43. Granacher U, Gollhofer A, Hortobágyi T, Kressig RW, Muehlbauer T (2013) The importance of trunk muscle strength for balance, functional performance, and fall prevention in seniors: a systematic review. Sports Med 43:627–641

    Article  PubMed  Google Scholar 

  44. Katzman WB, Harrison SL, Fink HA, Marshall LM, Orwoll E, Barrett-Connor E, Cawthon PM, Kado DM (2015) Physical function in older men with hyperkyphosis. J Gerontol A Biol Sci Med Sci 70:635–640

    Article  PubMed  Google Scholar 

  45. Katzman WB, Vittinghoff E, Kado DM (2011) Age-related hyperkyphosis, independent of spinal osteoporosis, is associated with impaired mobility in older community-dwelling women. Osteoporosis Int 22:85–90

    Article  CAS  Google Scholar 

  46. Kado DM, Miller-Martinez D, Lui LY, Cawthon P, Katzman WB, Hillier TA, Fink HA, Ensrud KE (2014) Hyperkyphosis, kyphosis progression, and risk of non-spine fractures in older community dwelling women: the study of osteoporotic fractures (SOF). J Bone Miner Res 29:2210–2216

    Article  PubMed  PubMed Central  Google Scholar 

  47. Kado DM, Lui LY, Ensrud KE, Fink HA, Karlamangla AS, Cummings SR (2009) Hyperkyphosis predicts mortality independent of vertebral osteoporosis in older women. Ann Intern Med 150:681–687

    Article  PubMed  PubMed Central  Google Scholar 

  48. Polidoulis I, Beyene J, Cheung A (2012) 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. Osteoporosis Int 23:39–51

    Article  CAS  Google Scholar 

  49. Ashe M, Gorman E, Khan K, Brasher P, Cooper D, McKay H, Liu-Ambrose T (2013) Does frequency of resistance training affect tibial cortical bone density in older women? A randomized controlled trial. Osteoporosis Int 24:623–632

    Article  CAS  Google Scholar 

  50. Zhao R, Zhao M, Xu Z (2015) The effects of differing resistance training modes on the preservation of bone mineral density in postmenopausal women: a meta-analysis. Osteoporosis Int 26:1605–1618

    Article  CAS  Google Scholar 

  51. Cussler EC, Timothy GL, Going SB, Houtkooper LB, Metcalfe LL, Flint-Wagner HG, Harris RB, Teixeira PJ (2003) Weight lifted in strength training predicts bone change in postmenopausal women. Med Sci Sports Exerc 35:10–17

    Article  PubMed  Google Scholar 

  52. Martyn-St James M, Carroll S (2010) Effects of different impact exercise modalities on bone mineral density in premenopausal women: a meta-analysis. J Bone Miner Metab 28:251–267

    Article  PubMed  Google Scholar 

  53. Kelley GA, Kelley KS, Kohrt WM (2013) Exercise and bone mineral density in men: a meta-analysis of randomized controlled trials. Bone 53:103–111

    Article  CAS  PubMed  Google Scholar 

  54. Bolam KA, Van Uffelen JG, Taaffe DR (2013) The effect of physical exercise on bone density in middle-aged and older men: a systematic review. Osteoporosis Int 24:2749–2762

    Article  CAS  Google Scholar 

  55. Ashe MC, McAllister MM, Barnes R, Sale J, Giangregorio LM, McKay H. 2000 Physical activity for preventing or managing osteoporosis in men (protocol). Cochrane Database of Syst Rev Issue 1. Art. No.:CD001982. doi:10.1002/14651858.CD001982

  56. Allison SJ, Folland JP, Rennie WJ, Summers GD, Brooke-Wavell K (2013) High impact exercise increased femoral neck bone mineral density in older men: a randomised unilateral intervention. Bone 53:321–328

    Article  PubMed  Google Scholar 

  57. Gianoudis J, Bailey CA, Ebeling PR, Nowson CA, Sanders KM, Hill K, Daly RM (2014) 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 29:182–191

    Article  PubMed  Google Scholar 

  58. Shah K, Armamento-Villareal R, Parimi N, Chode S, Sinacore DR, Hilton TN, Napoli N, Qualls C, Villareal DT (2011) Exercise training in obese older adults prevents increase in bone turnover and attenuates decrease in hip bone mineral density induced by weight loss despite decline in bone-active hormones. J Bone Miner Res 26:2851–2859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Siris ES, Brenneman SK, Miller PD, Connor-Barrett E, Chen Y, Sherwood LM, Abbott TA (2004) Predictive value of low BMD for 1-year fracture outcomes is similar for postmenopausal women ages 50-64 and 65 and older: results from the National Osteoporosis Risk Assessment (NORA). J Bone Miner Res 19:1215–1220

    Article  PubMed  Google Scholar 

  60. Bolton KL, Egerton T, Wark J, Wee E, Matthews B, Kelly A, Craven R, Kantor S, Bennell KL (2012) Effects of exercise on bone density and falls risk factors in post-menopausal women with osteopenia: a randomised controlled trial. J Sci Med Sport 15:102–109

    Article  PubMed  Google Scholar 

  61. Kemmler W, Bebenek M, Kohl M, Stengel v (2015) Exercise and fractures in postmenopausal women. Final results of the controlled Erlangen Fitness and Osteoporosis Prevention Study (EFOPS). Osteoporosis Int 26:2491–2499

    Article  CAS  Google Scholar 

  62. Papaioannou A, Adachi J, Winegard K, Ferko N, Parkinson W, Cook R, Webber C, McCartney N (2003) Efficacy of home-based exercise for improving quality of life among elderly women with symptomatic osteoporosis-related vertebral fractures. Osteoporosis Int 14:677–682

    Article  CAS  Google Scholar 

  63. Evstigneeva L, Lesnyak O, Bultink I, Lems W, Kozhemyakina E, Negodaeva E, Guselnikova G, Belkin A (2016) Effect of twelve-month physical exercise program on patients with osteoporotic vertebral fractures: a randomized, controlled trial. Osteoporosis Int 1–10

  64. Watson S, Weeks B, Weis L, Horan S, Beck B (2015) Heavy resistance training is safe and improves bone, function, and stature in postmenopausal women with low to very low bone mass: novel early findings from the LIFTMOR trial. Osteoporosis Int 26:2889–2894

    Article  CAS  Google Scholar 

  65. Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, Waite LM, Seibel MJ, Sambrook PN (2010) Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: the Concord Health and Ageing in Men Project. J Am Geriatr Soc 58:2055–2062

    Article  PubMed  Google Scholar 

  66. Janssen I, Heymsfield SB, Ross R (2002) Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 50:889–896

    Article  PubMed  Google Scholar 

  67. Van Roie E, Delecluse C, Coudyzer W, Boonen S, Bautmans I (2013) Strength training at high versus low external resistance in older adults: effects on muscle volume, muscle strength, and force–velocity characteristics. Exp Gerontol 48:1351–1361

    Article  PubMed  Google Scholar 

  68. Frost HM (1997) On our age-related bone loss: insights from a new paradigm. J Bone Miner Res 12:1539–1546

    Article  CAS  PubMed  Google Scholar 

  69. Burr DB (1997) Muscle strength, bone mass, and age-related bone loss. J Bone Miner Res 12:1547–1551

    Article  CAS  PubMed  Google Scholar 

  70. Binkley N, Buehring B (2009) Beyond FRAX®: It’s time to consider “sarco-osteopenia. J Clin Densitom 12:413–416

    Article  PubMed  Google Scholar 

  71. Goodman CA, Hornberger TA, Robling AG (2015) Bone and skeletal muscle: key players in mechanotransduction and potential overlapping mechanisms. Bone 80:24–36

    Article  PubMed  PubMed Central  Google Scholar 

  72. Brotto M, Bonewald L (2015) Bone and muscle: interactions beyond mechanical. Bone 80:109–114

    Article  PubMed  PubMed Central  Google Scholar 

  73. Blain H, Jaussent A, Thomas E, Micallef J, Dupuy A, Bernard PL, Mariano-Goulart D, Cristol J, Sultan C, Rossi M (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 

  74. 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 

  75. Miyakoshi N, Hongo M, Mizutani Y, Shimada Y (2013) Prevalence of sarcopenia in Japanese women with osteopenia and osteoporosis. J Bone Miner Metab 31:556–561

    Article  PubMed  Google Scholar 

  76. Verschueren S, Gielen E, O’Neill T, Pye S, Adams J, Ward K, Wu F, Szulc P, Laurent M, Claessens F (2013) Sarcopenia and its relationship with bone mineral density in middle-aged and elderly European men. Osteoporosis Int 24:87–98

    Article  CAS  Google Scholar 

  77. Kim JY, Chae SU, Kim GD, Cha MS (2013) Changes of paraspinal muscles in postmenopausal osteoporotic spinal compression fractures: magnetic resonance imaging study. J Bone Metab 20:75–81

    Article  PubMed  PubMed Central  Google Scholar 

  78. Menant JC, Weber F, Lo J, Sturnieks DL, Close JC, Sachdev PS, Brodaty H, Lord SR (2016) Strength measures are better than muscle mass measures in predicting health-related outcomes in older people: time to abandon the term sarcopenia? Osteoporosis Int. doi:10.1007/s00198-016-3691-7

  79. Al Snih S, Markides KS, Ottenbacher KJ, Raji MA (2004) Hand grip strength and incident ADL disability in elderly Mexican Americans over a seven-year period. Aging Clin Exp Res 16:481–486

    Article  PubMed  Google Scholar 

  80. Cawthon PM, Fox KM, Gandra SR, Delmonico MJ, Chiou C, Anthony MS, Sewall A, Goodpaster B, Satterfield S, Cummings SR (2009) Do muscle mass, muscle density, strength, and physical function similarly influence risk of hospitalization in older adults? J Am Geriatr Soc 57:1411–1419

    Article  PubMed  PubMed Central  Google Scholar 

  81. Taekema DG, Gussekloo J, Maier AB, Westendorp RG, de Craen AJ (2010) Handgrip strength as a predictor of functional, psychological and social health. A prospective population-based study among the oldest old. Age Ageing 39:331–337

    Article  PubMed  Google Scholar 

  82. Ling CH, Taekema D, de Craen AJ, Gussekloo J, Westendorp RG, Maier AB (2010) Handgrip strength and mortality in the oldest old population: the Leiden 85-plus study. CMAJ 182:429–435

    Article  PubMed  PubMed Central  Google Scholar 

  83. Newman AB, Kupelian V, Visser M, Simonsick EM, Goodpaster BH, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB (2006) Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort. J Gerontol A Biol Sci Med Sci 61:72–77

    Article  PubMed  Google Scholar 

  84. Cheung CL, Tan KC, Bow CH, Soong CS, Loong CH, Kung AW (2012) Low handgrip strength is a predictors of osteoporotic fractures: cross-sectional and prospective evidence from the Hong Kong osteoporosis study. Age (Dordr) 34:1239–1248

    Article  Google Scholar 

  85. Cawthon PM, Blackwell TL, Cauley J, Kado DM, Barrett-Connor E, Lee CG, Hoffman AR, Nevitt M, Stefanick ML, Lane NE, Ensurd KR, Cummings SR, Orwoll ES (2015) An evaluation of the usefulness of consensus definitions of sarcopenia in older men: results from the observational fractures in men (MrOS) cohort study. J Am Geriatr Soc 63:2247–2259

    Article  PubMed  PubMed Central  Google Scholar 

  86. Yu R, Leung J, Woo J (2014) Incremental predictive value of sarcopenia for incident fracture in an elderly Chinese cohort: results from the osteoporotic fractures in men (MrOs) study. J Am Med Dir Assoc 15:551–558

    Article  PubMed  Google Scholar 

  87. Yu R, Leung J, Woo J (2014) Sarcopenia combined with FRAX probabilities improves fracture risk prediction in older Chinese men. J Am Dir Assoc 15:918–923

    Article  Google Scholar 

  88. Schipilow J, Macdonald H, Liphardt A, Kan M, Boyd S (2013) Bone micro-architecture, estimated bone strength, and the muscle-bone interaction in elite athletes: an HR-pQCT study. Bone 56:281–289

    Article  CAS  PubMed  Google Scholar 

  89. Liphardt A, Schipilow J, Macdonald H, Kan M, Zieger A, Boyd S (2015) Bone micro-architecture of elite alpine skiers is not reflected by bone mineral density. Osteoporosis Int 26:2309–2317

    Article  Google Scholar 

  90. Rantalainen T, Nikander R, Kukuljan S, Daly R (2013) Mid-femoral and mid-tibial muscle cross-sectional area as predictors of tibial bone strength in middle-aged and older men. J Musculoskelet Neuronal Interact 13:273–282

    CAS  PubMed  Google Scholar 

  91. Castro MJ, Apple DF Jr, Hillegass EA, Dudley GA (1999) Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury. Eur J Appl Phyisol 80:373–378

    Article  CAS  Google Scholar 

  92. Garland DE, Adkins RH, Stewart CA (2005) The natural history of bone loss in the lower extremity of complete spinal cord injured males. Top Spinal Cord Inj Rehabil 11:48–60

    Article  Google Scholar 

  93. Singh R, Rohilla RK, Saini G, Kaur K (2014) Longitudinal study of body composition in spinal cord injury patients. Indian J Orthop 48:168–177

    Article  PubMed  PubMed Central  Google Scholar 

  94. Gibbs JC, Craven BC, Moore C, Thabane L, Adachi JD, Giangregorio LM (2015) Muscle density and bone quality of the distal lower extremity among individuals with chronic spinal cord injury. Top Spinal Cord Inj Rehabil 21:282–293

    Article  PubMed  PubMed Central  Google Scholar 

  95. Modlesky CM, Slade JM, Bickel CS, Meyer RA, Dudley GA (2005) Deteriorated geometric structure and strength of the midfemur in men with complete spinal cord injury. Bone 36:331–339

    Article  PubMed  Google Scholar 

  96. Totosy de Zepetnek JO, Craven BC, Giangregorio LM (2012) An evaluation of the muscle-bone unit theory among individuals with chronic spinal cord injury. Spinal Cord 50:147–152

    Article  CAS  PubMed  Google Scholar 

  97. Craven BC, Robertson LA, McGillivray CF, Adachi JD (2009) Detection and treatment of sublesional osteoporosis among patients with chronic spinal cord injury: proposed paradigms. Top Spinal Cord Inj Rehabil 14:1–22

    Article  Google Scholar 

  98. Chalhoub D, Cawthon PM, Ensrud KE, Stefanick ML, Kado DM, Boudreau R, Greenspan S, Newman AB, Zmuda J, Orwoll ES (2015) Risk of nonspine fractures in older adults with sarcopenia, low bone mass, or both. J Am Geriatr Soc 63:1733–1740

    Article  PubMed  PubMed Central  Google Scholar 

  99. Leslie WD, Orwoll ES, Nielson CM, Morin SN, Majumdar SR, Johansson H, Odén A, McCloskey EV, Kanis JA (2014) Estimated lean mass and fat mass differentially affect femoral bone density and strength index but are not FRAX independent risk factors for fracture. J Bone Miner Res 29:2511–2519

    Article  PubMed  Google Scholar 

  100. Lang T, Cauley JA, Tylavsky F, Bauer D, Cummings S, Harris TB (2010) Computed tomographic measurements of thigh muscle cross-sectional area and attenuation coefficient predict hip fracture: the health, aging and body composition study. J Bone Mineral Res 25:513–519

    Article  Google Scholar 

  101. Daly RM, Rosengren BE, Alwis G, Ahlborg HG, Sernbo I, Karlsson MK (2013) Gender specific age-related changes in bone density, muscle strength and functional performance in the elderly: A-10 year prospective population-based study. BMC Geriatr 13:71–80

    Article  PubMed  PubMed Central  Google Scholar 

  102. Pham HM, Nguyen ND, Center JR, Eisman JA, Nguyen TV (2016) Contribution of quadriceps weakness to fragility fracture: a prospective study. J Bone Mineral Res 31:208–214

    Article  Google Scholar 

  103. Reginster J, Cooper C, Rizzoli R, Kanis JA, Appelboom G, Bautmans I, Bischoff-Ferrari HA, Boers M, Brandi ML, Bruyère O (2015) Recommendations for the conduct of clinical trials for drugs to treat or prevent sarcopenia. Aging Clin Exp Res: 1–12

  104. Becker C, Lord SR, Studenski SA, Warden SJ, Fielding RA, Recknor CP, Hochberg MC, Ferrari SL, Blain H, Binder EF (2015) Myostatin antibody (LY2495655) in older weak fallers: a proof-of-concept, randomised, phase 2 trial. Lancet Diabetes Endocrinol 3:948–957

    Article  CAS  PubMed  Google Scholar 

  105. 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

    Article  PubMed  PubMed Central  Google Scholar 

  106. Borde R, Hortobágyi T, Granacher U (2015) Dose–response relationships of resistance training in healthy old adults: a systematic review and meta-analysis. Sports Med 45:1693–1720

    Article  PubMed  PubMed Central  Google Scholar 

  107. Watanabe Y, Madarame H, Ogasawara R, Nakazato K, Ishii N (2014) Effect of very low-intensity resistance training with slow movement on muscle size and strength in healthy older adults. Clin Physiol Funct Imaging 34:463–470

    Article  PubMed  Google Scholar 

  108. Liu C, Latham NK (2009) Progressive resistance strength training for improving physical function in older adults. Cochrane Database Syst Rev 3

  109. Straight CR, Lindheimer JB, Brady AO, Dishman RK, Evans EM (2016) Effects of resistance training on lower-extremity muscle power in middle-aged and older adults: a systematic review and meta-analysis of randomized controlled trails. Sports Med 46:353–364

    Article  PubMed  Google Scholar 

  110. Fielding RA, LeBrasseur NK, Cuoco A, Bean J, Mizer K, Fiatarone Singh MA (2002) High-velocity resistance training increases skeletal muscle peak power in older women. J Am Geriatr Soc 50:655–662

    Article  PubMed  Google Scholar 

  111. Reid KF, Martin KI, Doros G, Clark DJ, Hau C, Patten C, Phillips EM, Frontera WR, Fielding RA (2015) Comparative effects of light or heavy resistance power training for improving lower extremity power and physical performance in mobility-limited older adults. J Gerontol A Biol Sci Med Sci 70:374–380

    Article  PubMed  Google Scholar 

  112. Daly R, Saxon L, Turner C, Robling A, Bass S (2004) The relationship between muscle size and bone geometry during growth and in response to exercise. Bone 34:281–287

    Article  CAS  PubMed  Google Scholar 

  113. Armamento-Villareal R, Aguirre L, Napoli N, Shah K, Hilton T, Sinacore D, Qualls C, Villareal D (2014) Changes in thigh muscle volume predict bone mineral density response to lifestyle therapy in frail, obese older adults. Osteoporosis Int 25:551–558

    Article  CAS  Google Scholar 

  114. Sievänen H, Heinonen A, Kannus P (1996) Adaptation of bone to altered loading environment: a biochemical approach using X-ray absorptiometric data from the patella of a young woman. Bone 19:55–59

    Article  PubMed  Google Scholar 

  115. Pahor M, Guralnik JM, Ambrosius WT, Blair S, Bonds DE, Church TS, Espeland MA, Fielding RA, Gill TM, Groessl EJ (2014) Effect of structured physical activity on prevention of major mobility disability in older adults: the LIFE study randomized clinical trial. JAMA 311:2387–2396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Patil R, Kolu P, Raitanen J, Valvanne J, Kannus P, Karinkanta S, Sievänen H, Uusi-Rasi K (2016) Cost-effectiveness of vitamin D supplementation and exercise in preventing injurious falls among older home-dwelling women: findings from an RCT. Osteoporosis Int 27:193–201

    Article  CAS  Google Scholar 

  117. Devries MC, Breen L, Von Allmen M, MacDonald MJ, Moore DR, Offord EA, Horcajada MN, Breuille D, Phillips SM (2015) Low-load resistance training during step-reduction attenuates declines in muscle mass and strength and enhances anabolic sensitivity in older men. Physiol Rep 3(8):1–13

  118. Bauer J, Biolo G, Cederholm T, Cesari M, Cruz-Jentoft AJ, Morley JE, Phillips S, Sieber C, Stehle P, Teta D (2013) Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE Study Group. J Am Med Dir Assoc 14:542–559

    Article  PubMed  Google Scholar 

  119. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinkova E, Vandewoude M, Zamboni M, European Working Group on Sarcopenia in Older People (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  PubMed Central  Google Scholar 

Download references

Acknowledgments

The work was assisted with funding from the Ontario Ministry of Health and Long Term Care. L. Giangregorio is the recipient of the Bloomberg Manulife Prize for the Promotion of Active Health, a Canadian Institutes of Health Research New Investigator Award, and an Early Researcher Award from the Ontario Ministry of Research and Innovation.

Conflicts of interest

Dr. Giangregorio has received funding as a co-investigator from Amgen and has consulted for ICON on behalf of Eli Lilly on unrelated projects. Rasha El-Kotob declares that she has no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. Giangregorio.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Giangregorio, L., El-Kotob, R. Exercise, muscle, and the applied load-bone strength balance. Osteoporos Int 28, 21–33 (2017). https://doi.org/10.1007/s00198-016-3780-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-016-3780-7

Keywords

Navigation