Abstract
Summary
This meta-analysis synthesized current evidence from 24 clinical trials to evaluate the impact of different resistance training modes on postmenopausal bone loss. Exercise interventions were categorized into two training modes, namely resistance-alone versus combined resistance training protocols. The combined resistance training protocols were defined as the combination of resistance training and high-impact or weight-bearing exercise. The results suggested that the combined resistance training protocols were effective in improving bone mineral density (BMD) at the femoral neck and lumbar spine.
Introduction
The current meta-analysis aimed to examine the effects of combined resistance and resistance-alone training protocols on the preservation of femoral neck and lumbar spine BMD in postmenopausal women.
Methods
An electronic database search was conducted in PubMed, EMBASE, SPORTDiscus, Web of Science, and ProQuest up to March 1, 2014 for the influence of resistance exercise on BMD in postmenopausal women. The study quality was evaluated. The effect sizes were estimated in terms of the standardized mean difference (SMD). A subgroup analysis was conducted by exercise categories.
Results
Twenty-four studies were included in the overall analysis of skeletal response to resistance exercise. The between-study heterogeneity was evident for the hip (I 2 = 46.5 %) and spine (I 2 = 62.3 %). The overall analysis suggested that resistance training significantly increased femoral neck BMD (SMD = 0.303, 95 % confidence interval (95 % CI) = 0.127–0.479, p = 0.001) and lumbar spine BMD (SMD = 0.311, 95 % CI = 0.115–0.507, p = 0.002) in postmenopausal women. However, subgroup analysis indicated that combined resistance training programs significantly affected both the hip BMD (SMD = 0.411, 95 % CI = 0.176–0.645, p = 0.001) and spine BMD (SMD = 0.431, 95 % CI = 0.159–0.702, p = 0.002), whereas resistance-alone protocols only produced nonsignificant positive effects both on the femoral neck and lumbar spine BMD.
Conclusions
Combined resistance exercise protocols appear effective in preserving femoral neck and lumbar spine BMD in postmenopausal women, whereas resistance-alone protocols only produced a nonsignificant positive effect.
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References
National Osteoporosis Foundation (2002) America’s bone health: the state of osteoporosis and low bone mass in our nation. National Osteoprosis Foundation, Washington
Zhao D, Wu H, Liu Z (2006) Epidemiology of osteoporosis. In: Liu Z (ed) Bone mineral and clinic practice. Science and Technology Press, Beijing, pp 5–6
Johnell O, Kanis JA (2006) An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int 17:1726–1733
Moreira LD, Fronza FC, Dos Santos RN, Zach PL, Kunii IS, Hayashi LF, Teixeira LR, Kruel LF, Castro ML (2013) The benefits of a high-intensity aquatic exercise program (HydrOS) for bone metabolism and bone mass of postmenopausal women. J Bone Miner Metab. doi:10.1007/s00774-00013-00509-y
Basat H, Esmaeilzadeh S, Eskiyurt N (2013) The effects of strengthening and high-impact exercises on bone metabolism and quality of life in postmenopausal women: a randomized controlled trial. J back Musculoskelet Rehabil 26:427–435
Frost HM (1987) Bone “mass” and the “mechanostat”: a proposal. Anat Rec 219:1–9
Ryan AS, Ivey FM, Hurlbut DE, Martel GF, Lemmer JT, Sorkin JD, Metter EJ, Fleg JL, Hurley BF (2004) Regional bone mineral density after resistive training in young and older men and women. Scand J Med Sci Sports 14:16–23
Bemben DA, Fetters NL, Bemben MG, Nabavi N, Koh ET (2000) Musculoskeletal responses to high- and low-intensity resistance training in early postmenopausal women. Med Sci Sports Exerc 32:1949–1957
Bemben DA, Palmer IJ, Bemben MG, Knehans AW (2010) Effects of combined whole-body vibration and resistance training on muscular strength and bone metabolism in postmenopausal women. Bone 47:650–656
Bocalini DS, Serra AJ, dos Santos L, Murad N, Levy RF (2009) Strength training preserves the bone mineral density of postmenopausal women without hormone replacement therapy. J Aging Health 21:519–527
Chilibeck PD, Davison KS, Whiting SJ, Suzuki Y, Janzen CL, Peloso P (2002) The effect of strength training combined with bisphosphonate (etidronate) therapy on bone mineral, lean tissue, and fat mass in postmenopausal women. Can J Physiol Pharmacol 80:941–950
Chuin A, Labonte M, Tessier D, Khalil A, Bobeuf F, Doyon CY, Rieth N, Dionne IJ (2009) Effect of antioxidants combined to resistance training on BMD in elderly women: a pilot study. Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found U S A 20:1253–1258
Kerr D, Ackland T, Maslen B, Morton A, Prince R (2001) Resistance training over 2 years increases bone mass in calcium-replete postmenopausal women. J Bone Miner Res Off J Am Soc Bone Miner Res 16:175–181
Maddalozzo GF, Widrick JJ, Cardinal BJ, Winters-Stone KM, Hoffman MA, Snow CM (2007) The effects of hormone replacement therapy and resistance training on spine bone mineral density in early postmenopausal women. Bone 40:1244–1251
Marques EA, Wanderley F, Machado L, Sousa F, Viana JL, Moreira-Goncalves D, Moreira P, Mota J, Carvalho J (2011) Effects of resistance and aerobic exercise on physical function, bone mineral density, OPG and RANKL in older women. Exp Gerontol 46:524–532
Nelson ME, Fiatarone MA, Morganti CM, Trice I, Greenberg RA, Evans WJ (1994) Effects of high-intensity strength training on multiple risk factors for osteoporotic fractures. A randomized controlled trial. JAMA J Am Med Assoc 272:1909–1914
Pruitt LA, Jackson RD, Bartels RL, Lehnhard HJ (1992) Weight-training effects on bone mineral density in early postmenopausal women. J Bone Miner Res Off J Am Soc Bone Miner Res 7:179–185
Pruitt LA, Taaffe DR, Marcus R (1995) Effects of a one-year high-intensity versus low-intensity resistance training program on bone mineral density in older women. J Bone Miner Res Off J Am Soc Bone Miner Res 10:1788–1795
Rhodes EC, Martin AD, Taunton JE, Donnelly M, Warren J, Elliot J (2000) Effects of one year of resistance training on the relation between muscular strength and bone density in elderly women. Br J Sports Med 34:18–22
Smidt GL, Lin SY, O’Dwyer KD, Blanpied PR (1992) The effect of high-intensity trunk exercise on bone mineral density of postmenopausal women. Spine 17:280–285
Verschueren SM, Roelants M, Delecluse C, Swinnen S, Vanderschueren D, Boonen S (2004) Effect of 6-month whole body vibration training on hip density, muscle strength, and postural control in postmenopausal women: a randomized controlled pilot study. J Bone Miner Res Off J Am Soc Bone Miner Res 19:352–359
Notomi T, Okazaki Y, Okimoto N, Saitoh S, Nakamura T, Suzuki M (2000) A comparison of resistance and aerobic training for mass, strength and turnover of bone in growing rats. Eur J Appl Physiol 83:469–474
Martyn-St James M, Carroll S (2006) High-intensity resistance training and postmenopausal bone loss: a meta-analysis. Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found U S A 17:1225–1240
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
Chilibeck PD, Vatanparast H, Pierson R, Case A, Olatunbosun O, Whiting SJ, Beck TJ, Pahwa P, Biem HJ (2013) Effect of exercise training combined with isoflavone supplementation on bone and lipids in postmenopausal women: a randomized clinical trial. J Bone Miner Res Off J Am Soc Bone Miner Res 28:780–793
Engelke K, Kemmler W, Lauber D, Beeskow C, Pintag R, Kalender WA (2006) Exercise maintains bone density at spine and hip EFOPS: a 3-year longitudinal study in early postmenopausal women. Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found U S A 17:133–142
Going S, Lohman T, Houtkooper L et al (2003) Effects of exercise on bone mineral density in calcium-replete postmenopausal women with and without hormone replacement therapy. Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found U S A 14:637–643
Jessup JV, Horne C, Vishen RK, Wheeler D (2003) Effects of exercise on bone density, balance, and self-efficacy in older women. Biol Res Nurs 4:171–180
Kemmler W, Engelke K, Weineck J, Hensen J, Kalender WA (2003) The Erlangen Fitness Osteoporosis Prevention Study: a controlled exercise trial in early postmenopausal women with low bone density-first-year results. Arch Phys Med Rehabil 84:673–682
Kemmler W, Lauber D, Weineck J, Hensen J, Kalender W, Engelke K (2004) Benefits of 2 years of intense exercise on bone density, physical fitness, and blood lipids in early postmenopausal osteopenic women: results of the Erlangen Fitness Osteoporosis Prevention Study (EFOPS). Arch Intern Med 164:1084–1091
Kemmler W, von Stengel S, Bebenek M, Engelke K, Hentschke C, Kalender WA (2012) Exercise and fractures in postmenopausal women: 12-year results of the Erlangen Fitness and Osteoporosis Prevention Study (EFOPS). Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found U S A 23:1267–1276
Milliken LA, Going SB, Houtkooper LB, Flint-Wagner HG, Figueroa A, Metcalfe LL, Blew RM, Sharp SC, Lohman TG (2003) Effects of exercise training on bone remodeling, insulin-like growth factors, and bone mineral density in postmenopausal women with and without hormone replacement therapy. Calcif Tissue Int 72:478–484
Villareal DT, Binder EF, Yarasheski KE, Williams DB, Brown M, Sinacore DR, Kohrt WM (2003) Effects of exercise training added to ongoing hormone replacement therapy on bone mineral density in frail elderly women. J Am Geriatr Soc 51:985–990
von Stengel S, Kemmler W, Engelke K, Kalender WA (2011) Effects of whole body vibration on bone mineral density and falls: results of the randomized controlled ELVIS study with postmenopausal women. Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found U S A 22:317–325
Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151(264–269):W264
Higgins J, Green S (2008) Cochrane reviewers’ handbook 5.0.1 (updated September 2008). The Cochrane Library. Wiley, Chichester
Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJ, Gavaghan DJ, McQuay HJ (1996) Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 17:1–12
Milliken LA, Wilhelmy J, Martin CJ, Finkenthal N, Cussler E, Metcalfe L, Guido TA, Going SB, Lohman TG (2006) Depressive symptoms and changes in body weight exert independent and site-specific effects on bone in postmenopausal women exercising for 1 year. J Gerontol A: Biol Med Sci 61:488–494
Liu-Ambrose TY, Khan KM, Eng JJ, Heinonen A, McKay HA (2004) 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 Off J Int Soc Clin Densitom 7:390–398
Tobias JH (2003) At the crossroads of skeletal responses to estrogen and exercise. Trends Endocrinol Metab TEM 14:441–443
Zhang J, Gao R, Cao P, Yuan W (2014) Additive effects of antiresorptive agents and exercise on lumbar spine bone mineral density in adults with low bone mass: a meta-analysis. Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found U S A 25:1585–1594
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. The Cochrane database of systematic reviews CD000333
Martyn-St James M, Carroll S (2009) A meta-analysis of impact exercise on postmenopausal bone loss: the case for mixed loading exercise programmes. Br J Sports Med 43:898–908
Shaw JM, Snow CM (1998) Weighted vest exercise improves indices of fall risk in older women. J Gerontol A: Biol Med Sci 53:M53–M58
Snow CM, Shaw JM, Winters KM, Witzke KA (2000) Long-term exercise using weighted vests prevents hip bone loss in postmenopausal women. J Gerontol A: Biol Med Sci 55:M489–M491
El-Khoury F, Cassou B, Charles MA, Dargent-Molina P (2013) The effect of fall prevention exercise programmes on fall induced injuries in community dwelling older adults: systematic review and meta-analysis of randomised controlled trials. BMJ 347:f6234
Karinkanta S, Piirtola M, Sievanen H, Uusi-Rasi K, Kannus P (2010) Physical therapy approaches to reduce fall and fracture risk among older adults. Nat Rev Endocrinol 6:396–407
Cummings SR, Black DM, Nevitt MC, Browner W, Cauley J, Ensrud K, Genant HK, Palermo L, Scott J, Vogt TM (1993) Bone density at various sites for prediction of hip fractures. The Study of Osteoporotic Fractures Research Group. Lancet 341:72–75
Lanyon LE (1987) Functional strain in bone tissue as an objective, and controlling stimulus for adaptive bone remodelling. J Biomech 20:1083–1093
Borer KT (2005) Physical activity in the prevention and amelioration of osteoporosis in women: interaction of mechanical, hormonal and dietary factors. Sports Med 35:779–830
Rubin CT, McLeod KJ (1994) Promotion of bony ingrowth by frequency-specific, low-amplitude mechanical strain. Clin Orthop Relat Res 298:165–174
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
Rachner TD, Khosla S, Hofbauer LC (2011) Osteoporosis: now and the future. Lancet 377:1276–1287
Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol 62:e1–e34
Harris ST, Watts NB, Genant HK et al (1999) Effects of risedronate treatment on vertebral and nonvertebral fractures in women with postmenopausal osteoporosis: a randomized controlled trial. Vertebral Efficacy With Risedronate Therapy (VERT) Study Group. JAMA J Am Med Assoc 282:1344–1352
Rabenda V, Mertens R, Fabri V, Vanoverloop J, Sumkay F, Vannecke C, Deswaef A, Verpooten GA, Reginster JY (2008) Adherence to bisphosphonates therapy and hip fracture risk in osteoporotic women. Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found U S A 19:811–818
Cramer JA, Gold DT, Silverman SL, Lewiecki EM (2007) A systematic review of persistence and compliance with bisphosphonates for osteoporosis. Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found U S A 18:1023–1031
Reid IR (2013) Osteoporosis treatment: focus on safety. Eur J Intern Med 24:691–697
Miller PD, Derman RJ (2010) What is the best balance of benefits and risks among anti-resorptive therapies for postmenopausal osteoporosis? Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found U S A 21:1793–1802
Rossouw JE, Anderson GL, Prentice RL et al (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women’s Health Initiative randomized controlled trial. JAMA J Am Med Assoc 288:321–333
Kennel KA, Drake MT (2009) Adverse effects of bisphosphonates: implications for osteoporosis management. Mayo Clin Proc 84:632–637, quiz 638
Pildal J, Hrobjartsson A, Jorgensen KJ, Hilden J, Altman DG, Gotzsche PC (2007) Impact of allocation concealment on conclusions drawn from meta-analyses of randomized trials. Int J Epidemiol 36:847–857
Wood L, Egger M, Gluud LL, Schulz KF, Juni P, Altman DG, Gluud C, Martin RM, Wood AJ, Sterne JA (2008) Empirical evidence of bias in treatment effect estimates in controlled trials with different interventions and outcomes: meta-epidemiological study. BMJ 336:601–605
Wang Q, Nicholson PH, Suuriniemi M, Lyytikainen A, Helkala E, Alen M, Suominen H, Cheng S (2004) Relationship of sex hormones to bone geometric properties and mineral density in early pubertal girls. J Clin Endocrinol Metab 89:1698–1703
Karinkanta S, Heinonen A, Sievanen H, Uusi-Rasi K, Pasanen M, Ojala K, Fogelholm M, Kannus P (2007) A multi-component exercise regimen to prevent functional decline and bone fragility in home-dwelling elderly women: randomized, controlled trial. Osteoporos Int J Established Result Coop Eur Found Osteoporos Natl Osteoporos Found U S A 18:453–462
Ammann P, Rizzoli R (2003) Bone strength and its determinants. Osteoporos Int 14:S13–S18
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This material was based upon the work funded by Zhejiang Provincial Natural Science Foundation of China under Grant No. LY14H070001.
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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 26, 1605–1618 (2015). https://doi.org/10.1007/s00198-015-3034-0
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DOI: https://doi.org/10.1007/s00198-015-3034-0