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).
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References
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
Cheung AM, Detsky AS (2008) Osteoporosis and fractures: missing the bridge? JAMA 299:1468–1470
Cummings SR, Nevitt MC (1989) A hypothesis: the causes of hip fractures. J Gerontol 44:M107–M111
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
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
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
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
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
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
Kemmler W, Häberele L, von Stengel S (2013) Effects of exercise on fracture reduction in older adults. Osteoporosis Int 24:1937–1950
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Bansal S, Katzman WB, Giangregorio LM (2014) Exercise for improving age-related hyperkyphotic posture: a systematic review. Arch Phys Med Rehabil 95:129–140
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Frost HM (1997) On our age-related bone loss: insights from a new paradigm. J Bone Miner Res 12:1539–1546
Burr DB (1997) Muscle strength, bone mass, and age-related bone loss. J Bone Miner Res 12:1547–1551
Binkley N, Buehring B (2009) Beyond FRAX®: It’s time to consider “sarco-osteopenia. J Clin Densitom 12:413–416
Goodman CA, Hornberger TA, Robling AG (2015) Bone and skeletal muscle: key players in mechanotransduction and potential overlapping mechanisms. Bone 80:24–36
Brotto M, Bonewald L (2015) Bone and muscle: interactions beyond mechanical. Bone 80:109–114
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Liu C, Latham NK (2009) Progressive resistance strength training for improving physical function in older adults. Cochrane Database Syst Rev 3
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
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
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
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
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
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
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
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
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
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
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
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.
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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
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DOI: https://doi.org/10.1007/s00198-016-3780-7