Skip to main content
Top
Published in: Calcified Tissue International 5/2020

Open Access 01-11-2020 | Review Article

Effects of Different Types of Exercise on Bone Mineral Density in Postmenopausal Women: A Systematic Review and Meta-analysis

Authors: Wolfgang Kemmler, Mahdieh Shojaa, Matthias Kohl, Simon von Stengel

Published in: Calcified Tissue International | Issue 5/2020

Login to get access

Abstract

In this sub-analysis of a comprehensive meta-analysis, we aimed to determine the effect of different types of exercise on (areal) bone mineral density (BMD) in postmenopausal women. A systematic review of the literature according to the PRISMA statement included (a) controlled trials, (b) with at least one exercise and one control group, (c) intervention ≥ 6 months, (d) BMD assessments at lumbar spine (LS), femoral neck (FN) or total hip (TH), (e) in postmenopausal women. Eight electronic databases were scanned without language restrictions up to March 2019. The present subgroup analysis was conducted as a mixed-effect meta-analysis with “type of exercise” as the moderator. The 84 eligible exercise groups were classified into (a) weight bearing (WB, n = 30) exercise, (b) (dynamic) resistance exercise (DRT, n = 18), (c) mixed WB&DRT interventions (n = 36). Outcome measures were standardized mean differences (SMD) for BMD-changes at LS, FN and TH. All types of exercise significantly affect BMD at LS, FN and TH. SMD for LS average 0.40 (95% CI 0.15–0.65) for DRT, SMD 0.26 (0.03–0.49) for WB and SMD 0.42 (0.23–0.61) for WB&DRT. SMD for FN were 0.27 (0.09–0.45) for DRT, 0.37 (0.12–0.62) for WB and 0.35 (0.19–0.51) for WB&DRT. Lastly, SMD for TH changes were 0.51 (0.28–0.74) for DRT, 0.40 (0.21–0.58) for WB and 0.34 (0.14–0.53) for WB&DRT. In summary, we provided further evidence for the favorable effect of exercise on BMD largely independent of the type of exercise. However, in order to generate dedicated exercise recommendations or exercise guideline, meta-analyses might be a too rough tool.
Footnotes
1
e.g., 10 reps at 30% maximum isometric back muscle strength [30] or 14–16 reps at 40% 1RM [18, 29]. The same might be true for some exercises of the protocol of Woo et al. [32].
 
2
Or two sessions of 3 min/day, 7 days/week [53].
 
3
Early: ≤ 8 years vs. late postmenopausal > 9 years postmenopausal for LS-BMD (LS-BMD: 40, total hip: 20 exercise groups).
 
4
Considering site specificity of most DRT-exercises, we would expect the opposite effect, however, differences were not significant.
 
5
…or Watson et al. [102]. This highly effective and time-efficient trial had to be excluded by protocol due to the number of participants (< 10%) on osteoporosis medication.
 
Literature
1.
go back to reference Beck BR, Daly RM, Singh MA, Taaffe DR (2016) Exercise and Sports Science Australia (ESSA) position statement on exercise prescription for the prevention and management of osteoporosis. J Sci Med Sport 20:438–445PubMed Beck BR, Daly RM, Singh MA, Taaffe DR (2016) Exercise and Sports Science Australia (ESSA) position statement on exercise prescription for the prevention and management of osteoporosis. J Sci Med Sport 20:438–445PubMed
2.
go back to reference Tarantino U, Iolascon G, Cianferotti L et al (2017) Clinical guidelines for the prevention and treatment of osteoporosis: summary statements and recommendations from the Italian Society for Orthopaedics and Traumatology. J Orthop Traumatol 18:3–36PubMedPubMedCentral Tarantino U, Iolascon G, Cianferotti L et al (2017) Clinical guidelines for the prevention and treatment of osteoporosis: summary statements and recommendations from the Italian Society for Orthopaedics and Traumatology. J Orthop Traumatol 18:3–36PubMedPubMedCentral
3.
go back to reference Shojaa N, von Stengel S, Schoene D et al (2020) Effect of exercise training on bone mineral density in postmenopausal women: a systematic review and meta-analysis of intervention studies. Front Physiol 11:1427–1444 Shojaa N, von Stengel S, Schoene D et al (2020) Effect of exercise training on bone mineral density in postmenopausal women: a systematic review and meta-analysis of intervention studies. Front Physiol 11:1427–1444
4.
go back to reference Daly RM, Dalla Via J, Duckham RL, Fraser SF, Helge EW (2019) Exercise for the prevention of osteoporosis in postmenopausal women: an evidence-based guide to the optimal prescription. Braz J Phys Ther 23:170–180PubMed Daly RM, Dalla Via J, Duckham RL, Fraser SF, Helge EW (2019) Exercise for the prevention of osteoporosis in postmenopausal women: an evidence-based guide to the optimal prescription. Braz J Phys Ther 23:170–180PubMed
5.
go back to reference Kemmler W, Stengel V (eds) (2019) The role of exercise on fracture reduction and bone strengthening. Avademic Press, London Kemmler W, Stengel V (eds) (2019) The role of exercise on fracture reduction and bone strengthening. Avademic Press, London
6.
go back to reference Rahimi GRM, Smart NA, Liang MT et al (2020) The impact of different modes of exercise training on bone mineral density in older postmenopausal women: a systematic review and meta-analysis research. Calcif Tissue Int 106(6):577–590 Rahimi GRM, Smart NA, Liang MT et al (2020) The impact of different modes of exercise training on bone mineral density in older postmenopausal women: a systematic review and meta-analysis research. Calcif Tissue Int 106(6):577–590
7.
go back to reference Shojaa M, von Stengel V, Kohl M, Schoene D, Kemmler W (2020) Effects of dynamic resistance exercise on bone mineral density in postmenopausal women—a systematic review and meta-analysis with special emphasis to exercise parameters. Osteo Int 31:1427–1444 Shojaa M, von Stengel V, Kohl M, Schoene D, Kemmler W (2020) Effects of dynamic resistance exercise on bone mineral density in postmenopausal women—a systematic review and meta-analysis with special emphasis to exercise parameters. Osteo Int 31:1427–1444
8.
go back to reference Felsenberg D, Dietzel R, Pthy M, et al. (2008) Leitlinie physiotherapie und bewegungstherapie bei osteoporose. Guideline long version: Felsenberg D, Dietzel R, Pthy M, et al. (2008) Leitlinie physiotherapie und bewegungstherapie bei osteoporose. Guideline long version:
9.
go back to reference Kohrt WM, Bloomfield SA, Little KD, Nelson ME, Yingling VR (2004) American College of Sports Medicine position stand: physical activity and bone health. Med Sci Sports Exerc 366:1985–1996 Kohrt WM, Bloomfield SA, Little KD, Nelson ME, Yingling VR (2004) American College of Sports Medicine position stand: physical activity and bone health. Med Sci Sports Exerc 366:1985–1996
10.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151(264–269):W264 Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151(264–269):W264
11.
go back to reference Sherrington C, Herbert RD, Maher CG, Moseley AM (2000) PEDro. A database of randomized trials and systematic reviews in physiotherapy. Man Ther 5:223–226PubMed Sherrington C, Herbert RD, Maher CG, Moseley AM (2000) PEDro. A database of randomized trials and systematic reviews in physiotherapy. Man Ther 5:223–226PubMed
12.
go back to reference Kato T, Terashima T, Yamashita T, Hatanaka Y, Honda A, Umemura Y (2006) Effect of low-repetition jump training on bone mineral density in young women. J Appl Physiol 100:839–843PubMed Kato T, Terashima T, Yamashita T, Hatanaka Y, Honda A, Umemura Y (2006) Effect of low-repetition jump training on bone mineral density in young women. J Appl Physiol 100:839–843PubMed
13.
go back to reference Umemura Y, Ishiko T, Tsujimoto H, Miura H, Mokushi N, Suzuki H (1995) Effects of jump training on bone hypertrophy in young and old rats. Int J Sports Med 16:364–367PubMed Umemura Y, Ishiko T, Tsujimoto H, Miura H, Mokushi N, Suzuki H (1995) Effects of jump training on bone hypertrophy in young and old rats. Int J Sports Med 16:364–367PubMed
14.
go back to reference R_Development_Core_Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria R_Development_Core_Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
15.
go back to reference Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36:1–48 Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36:1–48
16.
go back to reference Cochrane (2016) Cochrane handbook for systematic reviews of interventions. In Higgins J, Green S (eds). The Cochrane Collaboration Cochrane (2016) Cochrane handbook for systematic reviews of interventions. In Higgins J, Green S (eds). The Cochrane Collaboration
17.
go back to reference Duval SJ, Tweedie RL (2000) A nonparametric "trim and fill" method of accounting for publication bias in meta-analysis. JASA 95:89–98 Duval SJ, Tweedie RL (2000) A nonparametric "trim and fill" method of accounting for publication bias in meta-analysis. JASA 95:89–98
18.
go back to reference 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 32:1949–1957PubMed 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 32:1949–1957PubMed
19.
go back to reference 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 80:941–950PubMed 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 80:941–950PubMed
20.
go back to reference de Oliveira LC, de Oliveira RG, de Almeida Pires-Oliveira DA (2019) Effects of whole-body vibration versus pilates exercise on bone mineral density in postmenopausal women: a randomized and controlled clinical trial. J Geriatr Phys Ther 42:E23–E31PubMed de Oliveira LC, de Oliveira RG, de Almeida Pires-Oliveira DA (2019) Effects of whole-body vibration versus pilates exercise on bone mineral density in postmenopausal women: a randomized and controlled clinical trial. J Geriatr Phys Ther 42:E23–E31PubMed
21.
go back to reference Duff WR, Kontulainen SA, Candow DG et al (2016) Effects of low-dose ibuprofen supplementation and resistance training on bone and muscle in postmenopausal women: a randomized controlled trial. Bone Rep 5:96–103PubMedPubMedCentral Duff WR, Kontulainen SA, Candow DG et al (2016) Effects of low-dose ibuprofen supplementation and resistance training on bone and muscle in postmenopausal women: a randomized controlled trial. Bone Rep 5:96–103PubMedPubMedCentral
22.
go back to reference Hartard M, Haber P, Ilieva D, Preisinger E, Huber JC (1996) Systematic strength training as a model of therapeutic intervention. Arch Phys Med Rehabil 75:21–28 Hartard M, Haber P, Ilieva D, Preisinger E, Huber JC (1996) Systematic strength training as a model of therapeutic intervention. Arch Phys Med Rehabil 75:21–28
23.
go back to reference Kerr D, Morton A, Dick I, Prince R (1996) Exercise effects on bone mass in postmenopausal women are site-specific and load-dependent. J Bone Miner Res 11:218–225PubMed Kerr D, Morton A, Dick I, Prince R (1996) Exercise effects on bone mass in postmenopausal women are site-specific and load-dependent. J Bone Miner Res 11:218–225PubMed
24.
go back to reference 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 40:1244–1251PubMed 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 40:1244–1251PubMed
25.
go back to reference 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 272:1909–1914PubMed 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 272:1909–1914PubMed
26.
go back to reference Nicholson VP, McKean MR, Slater GJ, Kerr A, Burkett BJ (2015) Low-load very high-repetition resistance training attenuates bone loss at the lumbar spine in active post-menopausal women. Calcif Tissue Int 96:490–499PubMed Nicholson VP, McKean MR, Slater GJ, Kerr A, Burkett BJ (2015) Low-load very high-repetition resistance training attenuates bone loss at the lumbar spine in active post-menopausal women. Calcif Tissue Int 96:490–499PubMed
27.
go back to reference Orsatti F, Petri-Nahas E, Nahas-Neto J, Orsatti C, Teixeira A (2013) Effects of isoflavone and counter-resistance training on bone mineral density in postmenopausal women. Rev Bras Cineantropom Desempenho Hum 15:726–736 Orsatti F, Petri-Nahas E, Nahas-Neto J, Orsatti C, Teixeira A (2013) Effects of isoflavone and counter-resistance training on bone mineral density in postmenopausal women. Rev Bras Cineantropom Desempenho Hum 15:726–736
28.
go back to reference Pruitt LA, Jackson RD, Bartels RL, Lehnhard HJ (1992) Weight-training effects on bone mineral density in early postmenopausal women. J Bone Miner Res 7:179–185PubMed Pruitt LA, Jackson RD, Bartels RL, Lehnhard HJ (1992) Weight-training effects on bone mineral density in early postmenopausal women. J Bone Miner Res 7:179–185PubMed
29.
go back to reference 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 10:1788–1795PubMed 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 10:1788–1795PubMed
30.
go back to reference Sinaki M, Wahner HW, Offord KP, Hodgson SF (1989) Efficacy of nonloading exercises in prevention of vertebral bone loss in postmenopausal women: a controlled trial. Mayo Clin Proc 64:762–769PubMed Sinaki M, Wahner HW, Offord KP, Hodgson SF (1989) Efficacy of nonloading exercises in prevention of vertebral bone loss in postmenopausal women: a controlled trial. Mayo Clin Proc 64:762–769PubMed
31.
go back to reference Wang H, Yu B, Chen W, Lu Y, Yu D (2015) Simplified Tai Chi resistance training versus traditional Tai Chi in slowing bone loss in postmenopausal women. Evid Based Complement Alternat Med 2015:379451PubMedPubMedCentral Wang H, Yu B, Chen W, Lu Y, Yu D (2015) Simplified Tai Chi resistance training versus traditional Tai Chi in slowing bone loss in postmenopausal women. Evid Based Complement Alternat Med 2015:379451PubMedPubMedCentral
32.
go back to reference Woo J, Hong A, Lau E, Lynn H (2007) A randomised controlled trial of Tai Chi and resistance exercise on bone health, muscle strength and balance in community-living elderly people. Age Ageing 36:262–268PubMed Woo J, Hong A, Lau E, Lynn H (2007) A randomised controlled trial of Tai Chi and resistance exercise on bone health, muscle strength and balance in community-living elderly people. Age Ageing 36:262–268PubMed
33.
go back to reference 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 26:427–435PubMed 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 26:427–435PubMed
34.
go back to reference Bassey EJ, Ramsdale SJ (1995) Weight-bearing exercise and ground reaction forces: a 12-month randomized controlled trial of effects on bone mineral density in healthy postmenopausal women. Bone 16:469–476PubMed Bassey EJ, Ramsdale SJ (1995) Weight-bearing exercise and ground reaction forces: a 12-month randomized controlled trial of effects on bone mineral density in healthy postmenopausal women. Bone 16:469–476PubMed
35.
go back to reference Bassey EJ, Rothwell MC, Littlewood JJ, Pye DW (1998) Pre- and postmenopausal women have different bone mineral density responses to the same high-impact exercise. J Bone Miner Res 13:1805–1813PubMed Bassey EJ, Rothwell MC, Littlewood JJ, Pye DW (1998) Pre- and postmenopausal women have different bone mineral density responses to the same high-impact exercise. J Bone Miner Res 13:1805–1813PubMed
36.
go back to reference Brooke-Wavell K, Jones PR, Hardman AE (1997) Brisk walking reduces calcaneal bone loss in post-menopausal women. Clin Sci (Lond) 92:75–80 Brooke-Wavell K, Jones PR, Hardman AE (1997) Brisk walking reduces calcaneal bone loss in post-menopausal women. Clin Sci (Lond) 92:75–80
37.
go back to reference Brooke-Wavell K, Jones PR, Hardman AE, Tsuritan YY (2001) Commencing, continuing and stopping brisk walking: effects on bone mineral density, quantitative ultrasound of bone and markers of bone metabolism in postmenopausal women. Osteoporos Int 12:581–587PubMed Brooke-Wavell K, Jones PR, Hardman AE, Tsuritan YY (2001) Commencing, continuing and stopping brisk walking: effects on bone mineral density, quantitative ultrasound of bone and markers of bone metabolism in postmenopausal women. Osteoporos Int 12:581–587PubMed
38.
go back to reference Chan K, Qin L, Lau M et al (2004) A randomized, prospective study of the effects of Tai Chi Chun exercise on bone mineral density in postmenopausal women. Arch Phys Med Rehabil 85:717–722PubMed Chan K, Qin L, Lau M et al (2004) A randomized, prospective study of the effects of Tai Chi Chun exercise on bone mineral density in postmenopausal women. Arch Phys Med Rehabil 85:717–722PubMed
39.
go back to reference Ebrahim SB, Thompson PW, Baskaran V (1997) Randomized placebo controlled trial of brisk walking in the prevention of postmenopausal osteoporosis. Age Aging 26:252–260 Ebrahim SB, Thompson PW, Baskaran V (1997) Randomized placebo controlled trial of brisk walking in the prevention of postmenopausal osteoporosis. Age Aging 26:252–260
40.
go back to reference Evans EM, Racette SB, Van Pelt RE, Peterson LR, Villareal DT (2007) Effects of soy protein isolate and moderate exercise on bone turnover and bone mineral density in postmenopausal women. Menopause 14:481–488PubMedPubMedCentral Evans EM, Racette SB, Van Pelt RE, Peterson LR, Villareal DT (2007) Effects of soy protein isolate and moderate exercise on bone turnover and bone mineral density in postmenopausal women. Menopause 14:481–488PubMedPubMedCentral
41.
go back to reference Hans D, Genton L, Drezner MK et al (2002) Monitored impact loading of the hip: initial testing of a home-use device. Calcif Tissue Int 71:112–120PubMed Hans D, Genton L, Drezner MK et al (2002) Monitored impact loading of the hip: initial testing of a home-use device. Calcif Tissue Int 71:112–120PubMed
42.
go back to reference Hatori M, Hasegawa A, Adachi H et al (1993) The effects of walking at the anaerobic threshold level on vertebral bone loss in postmenopausal women. Calcif Tissue Int 52:411–414PubMed Hatori M, Hasegawa A, Adachi H et al (1993) The effects of walking at the anaerobic threshold level on vertebral bone loss in postmenopausal women. Calcif Tissue Int 52:411–414PubMed
43.
go back to reference Kohrt WM, Ehsani AA (1997) Effects of exercise involving predominantly either joint-reaction or ground-reaction forces on bone mineral density in older women. J Bone Miner Res 12:1253–1261PubMed Kohrt WM, Ehsani AA (1997) Effects of exercise involving predominantly either joint-reaction or ground-reaction forces on bone mineral density in older women. J Bone Miner Res 12:1253–1261PubMed
44.
go back to reference Kohrt WM, Snead DB, Slatopolsky E, Birge SJ Jr (1995) Additive effects of weight-bearing exercise and estrogen on bone mineral density in older women. J Bone Miner Res 10:1303–1311PubMed Kohrt WM, Snead DB, Slatopolsky E, Birge SJ Jr (1995) Additive effects of weight-bearing exercise and estrogen on bone mineral density in older women. J Bone Miner Res 10:1303–1311PubMed
45.
go back to reference Korpelainen R, Keinanen-Kiukaanniemi S, Heikkinen J, Vaananen K, Korpelainen J (2006) Effects of impact exercise on bone mineral density in elderly women with low BMD: a population based randomized controlled 30-month intervention. Osteoporos Int 17:109–118PubMed Korpelainen R, Keinanen-Kiukaanniemi S, Heikkinen J, Vaananen K, Korpelainen J (2006) Effects of impact exercise on bone mineral density in elderly women with low BMD: a population based randomized controlled 30-month intervention. Osteoporos Int 17:109–118PubMed
46.
go back to reference Lau EM, Woo J, Leung PC, Swaminathan R, Leung D (1992) The effects of calcium supplementation and exercise on bone density in elderly Chinese women. Osteoporos Int 2:168–173PubMed Lau EM, Woo J, Leung PC, Swaminathan R, Leung D (1992) The effects of calcium supplementation and exercise on bone density in elderly Chinese women. Osteoporos Int 2:168–173PubMed
47.
go back to reference Liu BX, Chen SP, Li YD et al (2015) The effect of the modified eighth section of eight-section brocade on osteoporosis in postmenopausal women: a prospective randomized trial. Medicine (Baltimore) 94:e991 Liu BX, Chen SP, Li YD et al (2015) The effect of the modified eighth section of eight-section brocade on osteoporosis in postmenopausal women: a prospective randomized trial. Medicine (Baltimore) 94:e991
48.
go back to reference Marques EA, Wanderley F, Machado L et al (2011) Effects of resistance and aerobic exercise on physical function, bone mineral density, OPG and RANKL in older women. Exp Gerontol 46:524–532PubMed Marques EA, Wanderley F, Machado L et al (2011) Effects of resistance and aerobic exercise on physical function, bone mineral density, OPG and RANKL in older women. Exp Gerontol 46:524–532PubMed
49.
go back to reference Martin D, Notelovitz M (1993) Effects of aerobic training on bone mineral density of postmenopausal women. J Bone Miner Res 8:931–936PubMed Martin D, Notelovitz M (1993) Effects of aerobic training on bone mineral density of postmenopausal women. J Bone Miner Res 8:931–936PubMed
50.
go back to reference Nelson ME, Fisher EC, Dilmanian FA, Dallal GE, Evans WJ (1991) A 1-y walking program and increased dietary calcium in postmenopausal women: effects on bone. Am J Clin Nutr 53:1304–1311PubMed Nelson ME, Fisher EC, Dilmanian FA, Dallal GE, Evans WJ (1991) A 1-y walking program and increased dietary calcium in postmenopausal women: effects on bone. Am J Clin Nutr 53:1304–1311PubMed
51.
go back to reference Prince RL, Devine A, Dick I et al (1995) The effect of calcium supplementation (milk powder or tablets) and exercise on bone density in postmenopausal women. J Bone Miner Res 10:1068–1075PubMed Prince RL, Devine A, Dick I et al (1995) The effect of calcium supplementation (milk powder or tablets) and exercise on bone density in postmenopausal women. J Bone Miner Res 10:1068–1075PubMed
52.
go back to reference Ryan AS, Nicklas BJ, Dennis KE (1998) Aerobic exercise maintains regional bone mineral density during weight loss in postmenopausal women. J Appl Physiol 84:1305–1310PubMed Ryan AS, Nicklas BJ, Dennis KE (1998) Aerobic exercise maintains regional bone mineral density during weight loss in postmenopausal women. J Appl Physiol 84:1305–1310PubMed
53.
go back to reference Sakai A, Oshige T, Zenke Y, Yamanaka Y, Nagaishi H, Nakamura T (2010) Unipedal standing exercise and hip bone mineral density in postmenopausal women: a randomized controlled trial. J Bone Miner Metab 28:42–48PubMed Sakai A, Oshige T, Zenke Y, Yamanaka Y, Nagaishi H, Nakamura T (2010) Unipedal standing exercise and hip bone mineral density in postmenopausal women: a randomized controlled trial. J Bone Miner Metab 28:42–48PubMed
54.
go back to reference Silverman NE, Nicklas BJ, Ryan AS (2009) Addition of aerobic exercise to a weight loss program increases BMD, with an associated reduction in inflammation in overweight postmenopausal women. Calcif Tissue Int 84:257–265PubMedPubMedCentral Silverman NE, Nicklas BJ, Ryan AS (2009) Addition of aerobic exercise to a weight loss program increases BMD, with an associated reduction in inflammation in overweight postmenopausal women. Calcif Tissue Int 84:257–265PubMedPubMedCentral
55.
go back to reference Sugiyama T, Yamaguchi A, Kawai S (2002) Effects of skeletal loading on bone mass and compensation mechanism in bone: a new insight into the "mechanostat" theory. J Bone Miner Metab 20:196–200PubMed Sugiyama T, Yamaguchi A, Kawai S (2002) Effects of skeletal loading on bone mass and compensation mechanism in bone: a new insight into the "mechanostat" theory. J Bone Miner Metab 20:196–200PubMed
56.
go back to reference Tartibian B, Hajizadeh Maleki B, Kanaley J, Sadeghi K (2011) Long-term aerobic exercise and omega-3 supplementation modulate osteoporosis through inflammatory mechanisms in post-menopausal women: a randomized, repeated measures study. Nutr Metab (Lond) 8:71 Tartibian B, Hajizadeh Maleki B, Kanaley J, Sadeghi K (2011) Long-term aerobic exercise and omega-3 supplementation modulate osteoporosis through inflammatory mechanisms in post-menopausal women: a randomized, repeated measures study. Nutr Metab (Lond) 8:71
57.
go back to reference Wu J, Oka J, Tabata I et al (2006) Effects of isoflavone and exercise on BMD and fat mass in postmenopausal Japanese women: a 1-year randomized placebo-controlled trial. J Bone Miner Res 21:780–789PubMed Wu J, Oka J, Tabata I et al (2006) Effects of isoflavone and exercise on BMD and fat mass in postmenopausal Japanese women: a 1-year randomized placebo-controlled trial. J Bone Miner Res 21:780–789PubMed
58.
go back to reference Adami S, Gatti D, Braga V, Bianchini D, Rossini M (1999) Site-specific effects of strength training on bone structure and geometry of ultradistal radius in postmenopausal women. J Bone Miner Res 14:120–124PubMed Adami S, Gatti D, Braga V, Bianchini D, Rossini M (1999) Site-specific effects of strength training on bone structure and geometry of ultradistal radius in postmenopausal women. J Bone Miner Res 14:120–124PubMed
59.
go back to reference Bello M, Sousa MC, Neto G, Oliveira L, Guerras I, Mendes R, Sousa N (2014) The effect of a long-term, community-based exercise program on bone mineral density in postmenopausal women with pre-diabetes and type 2 diabetes. J Hum Kinet 43:43–48PubMedPubMedCentral Bello M, Sousa MC, Neto G, Oliveira L, Guerras I, Mendes R, Sousa N (2014) The effect of a long-term, community-based exercise program on bone mineral density in postmenopausal women with pre-diabetes and type 2 diabetes. J Hum Kinet 43:43–48PubMedPubMedCentral
60.
go back to reference 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 47:650–656PubMed 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 47:650–656PubMed
61.
go back to reference Bergström I, Landgren BM, Brinck J, Freyschuss B (2008) Physical training preserves bone mineral density in postmenopausal women with forearm fractures and low bone mineral density. Osteoporos Int 19:177–183PubMed Bergström I, Landgren BM, Brinck J, Freyschuss B (2008) Physical training preserves bone mineral density in postmenopausal women with forearm fractures and low bone mineral density. Osteoporos Int 19:177–183PubMed
62.
go back to reference 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 21:519–527PubMed 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 21:519–527PubMed
63.
go back to reference Bolton KL, Egerton T, Wark J et al (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 15:102–109PubMed Bolton KL, Egerton T, Wark J et al (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 15:102–109PubMed
64.
go back to reference Caplan GA, Ward JA, Lord SR (1993) The benefits of exercise in postmenopausal women. Aust J Public Health 17:23–26PubMed Caplan GA, Ward JA, Lord SR (1993) The benefits of exercise in postmenopausal women. Aust J Public Health 17:23–26PubMed
65.
go back to reference Chilibeck PD, Vatanparast H, Pierson R et al (2013) Effect of exercise training combined with isoflavone supplementation on bone and lipids in postmenopausal women: a randomized clinical trial. J Bone Miner Res 28:780–793PubMed Chilibeck PD, Vatanparast H, Pierson R et al (2013) Effect of exercise training combined with isoflavone supplementation on bone and lipids in postmenopausal women: a randomized clinical trial. J Bone Miner Res 28:780–793PubMed
66.
go back to reference Choquette S, Riesco E, Cormier E, Dion T, Aubertin-Leheudre M, Dionne IJ (2011) Effects of soya isoflavones and exercise on body composition and clinical risk factors of cardiovascular diseases in overweight postmenopausal women: a 6-month double-blind controlled trial. Br J Nutr 105:1199–1209PubMed Choquette S, Riesco E, Cormier E, Dion T, Aubertin-Leheudre M, Dionne IJ (2011) Effects of soya isoflavones and exercise on body composition and clinical risk factors of cardiovascular diseases in overweight postmenopausal women: a 6-month double-blind controlled trial. Br J Nutr 105:1199–1209PubMed
67.
go back to reference Chuin A, Labonte M, Tessier D et al (2009) Effect of antioxidants combined to resistance training on BMD in elderly women: a pilot study. Osteoporos Int 20:1253–1258PubMed Chuin A, Labonte M, Tessier D et al (2009) Effect of antioxidants combined to resistance training on BMD in elderly women: a pilot study. Osteoporos Int 20:1253–1258PubMed
68.
go back to reference de Matos O, Lopes da Silva DJ, Martinez de Oliveira J, Castelo-Branco C (2009) Effect of specific exercise training on bone mineral density in women with postmenopausal osteopenia or osteoporosis. Gynecol Endocrinol 25:616–620PubMed de Matos O, Lopes da Silva DJ, Martinez de Oliveira J, Castelo-Branco C (2009) Effect of specific exercise training on bone mineral density in women with postmenopausal osteopenia or osteoporosis. Gynecol Endocrinol 25:616–620PubMed
69.
go back to reference Deng S (2009) Effects of exercise therapy on bone mineral density in early postmenopausal women: a controlled trial. Front Med China 3:323–329 Deng S (2009) Effects of exercise therapy on bone mineral density in early postmenopausal women: a controlled trial. Front Med China 3:323–329
70.
go back to reference Englund U, Littbrand H, Sondell A, Pettersson U, Bucht G (2005) A 1-year combined weight-bearing training program is beneficial for bone mineral density and neuromuscular function in older women. Osteoporos Int 16:1117–1123PubMed Englund U, Littbrand H, Sondell A, Pettersson U, Bucht G (2005) A 1-year combined weight-bearing training program is beneficial for bone mineral density and neuromuscular function in older women. Osteoporos Int 16:1117–1123PubMed
71.
go back to reference 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 14:637–643PubMed 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 14:637–643PubMed
72.
go back to reference Grove KA, Londeree BR (1992) Bone density in postmenopausal women: high impact vs low impact exercise. Med Sci Sports Exerc 24:1190–1194PubMed Grove KA, Londeree BR (1992) Bone density in postmenopausal women: high impact vs low impact exercise. Med Sci Sports Exerc 24:1190–1194PubMed
73.
go back to reference Iwamoto J, Takeda T, Ichimura S (2001) Effects of exercise training and detraining on bone mineral density in postmenopausal women with osteoporosis. J Orthop Sci 6:128–132PubMed Iwamoto J, Takeda T, Ichimura S (2001) Effects of exercise training and detraining on bone mineral density in postmenopausal women with osteoporosis. J Orthop Sci 6:128–132PubMed
74.
go back to reference 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 4:171–180PubMed 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 4:171–180PubMed
75.
go back to reference Karakiriou S, Douda H, Smilios I, Volaklis KA, Tokmakidis SP (2012) Effects of vibration and exercise training on bone mineral density and muscle strength in post-menopausal women. Eur J Sport Sci 12:81–88 Karakiriou S, Douda H, Smilios I, Volaklis KA, Tokmakidis SP (2012) Effects of vibration and exercise training on bone mineral density and muscle strength in post-menopausal women. Eur J Sport Sci 12:81–88
76.
go back to reference Kemmler W (1999) Einfluß unterschiedlicher Lebensabschnitte auf die belastungsabhängige Reaktion ossärer Risikofaktoren einer Osteoporose. Dtsch Z Sportmed 50:114–119 Kemmler W (1999) Einfluß unterschiedlicher Lebensabschnitte auf die belastungsabhängige Reaktion ossärer Risikofaktoren einer Osteoporose. Dtsch Z Sportmed 50:114–119
77.
go back to reference 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 164:1084–1091PubMed 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 164:1084–1091PubMed
78.
go back to reference Kemmler W, von Stengel S, Engelke K, Haberle L, Kalender WA (2010) Exercise effects on bone mineral density, falls, coronary risk factors, and health care costs in older women: the randomized controlled senior fitness and prevention (SEFIP) study. Arch Intern Med 170:179–185PubMed Kemmler W, von Stengel S, Engelke K, Haberle L, Kalender WA (2010) Exercise effects on bone mineral density, falls, coronary risk factors, and health care costs in older women: the randomized controlled senior fitness and prevention (SEFIP) study. Arch Intern Med 170:179–185PubMed
79.
go back to reference Kemmler W, Bebenek M, von Stengel S, Engelke K, Kalender WA (2013) Effect of block-periodized exercise training on bone and coronary heart disease risk factors in early post-menopausal women: a randomized controlled study. Scand J Med Sci Sports 23:121–129PubMed Kemmler W, Bebenek M, von Stengel S, Engelke K, Kalender WA (2013) Effect of block-periodized exercise training on bone and coronary heart disease risk factors in early post-menopausal women: a randomized controlled study. Scand J Med Sci Sports 23:121–129PubMed
80.
go back to reference 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 16:175–181PubMed 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 16:175–181PubMed
81.
go back to reference Kwon Y, Park SK, Kim E, Park J (2008) The effects of multi-component exercise training on VO2max, muscle mass, whole bone mineral density and fall risk in community-dwelling elderly women. Jpn J Phys Fit Sport 57:339–348 Kwon Y, Park SK, Kim E, Park J (2008) The effects of multi-component exercise training on VO2max, muscle mass, whole bone mineral density and fall risk in community-dwelling elderly women. Jpn J Phys Fit Sport 57:339–348
82.
go back to reference Lord SR, Ward JA, Williams P, Zivanovic E (1996) The effect of a community exercise program on fracture risk factors in older women. Osteoporos Int 6:361–367PubMed Lord SR, Ward JA, Williams P, Zivanovic E (1996) The effect of a community exercise program on fracture risk factors in older women. Osteoporos Int 6:361–367PubMed
83.
go back to reference Marques EA, Mota J, Machado L, Sousa F, Coelho M, Moreira P, Carvalho J (2011) Multicomponent training program with weight-bearing exercises elicits favorable bone density, muscle strength, and balance adaptations in older women. Calcif Tissue Int 88:117–129PubMed Marques EA, Mota J, Machado L, Sousa F, Coelho M, Moreira P, Carvalho J (2011) Multicomponent training program with weight-bearing exercises elicits favorable bone density, muscle strength, and balance adaptations in older women. Calcif Tissue Int 88:117–129PubMed
84.
go back to reference Milliken LA, Going SB, Houtkooper LB et al (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 72:478–484PubMed Milliken LA, Going SB, Houtkooper LB et al (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 72:478–484PubMed
85.
go back to reference Nichols JF, Nelson KP, Peterson KK, Satoris DJ (1995) Bone Mineral density responses to high-intensity strength training in older women. J Age Phys Activity 3:26–38 Nichols JF, Nelson KP, Peterson KK, Satoris DJ (1995) Bone Mineral density responses to high-intensity strength training in older women. J Age Phys Activity 3:26–38
86.
go back to reference Park H, Kim KJ, Komatsu T, Park SK, Mutoh Y (2008) Effect of combined exercise training on bone, body balance, and gait ability: a randomized controlled study in community-dwelling elderly women. J Bone Miner Metab 26:254–259PubMed Park H, Kim KJ, Komatsu T, Park SK, Mutoh Y (2008) Effect of combined exercise training on bone, body balance, and gait ability: a randomized controlled study in community-dwelling elderly women. J Bone Miner Metab 26:254–259PubMed
87.
go back to reference Tolomio S, Lalli A, Travain G, Zaccaria M (2009) Effects of a combined weight- and non weight-bearing (water) exercise program on bone mass and quality in postmenopausal women with low bone mineral density. Clin Ter 160:105–109PubMed Tolomio S, Lalli A, Travain G, Zaccaria M (2009) Effects of a combined weight- and non weight-bearing (water) exercise program on bone mass and quality in postmenopausal women with low bone mineral density. Clin Ter 160:105–109PubMed
88.
go back to reference Verschueren SM, Roelants M, Delecluse C, Swinnen S, Vanderschueren D, Boonen S (2004) Effects 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 Min Res 19:352–359 Verschueren SM, Roelants M, Delecluse C, Swinnen S, Vanderschueren D, Boonen S (2004) Effects 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 Min Res 19:352–359
89.
go back to reference Yamazaki S, Ichimura S, Iwamoto J, Takeda T, Toyama Y (2004) Effect of walking exercise on bone metabolism in postmenopausal women with osteopenia/osteoporosis. J Bone Miner Metab 22:500–508PubMed Yamazaki S, Ichimura S, Iwamoto J, Takeda T, Toyama Y (2004) Effect of walking exercise on bone metabolism in postmenopausal women with osteopenia/osteoporosis. J Bone Miner Metab 22:500–508PubMed
90.
go back to reference Hoover DL, VanWye WR, Judge LW (2016) Periodization and physical therapy: bridging the gap between training and rehabilitation. Phys Ther Sport 18:1–20PubMed Hoover DL, VanWye WR, Judge LW (2016) Periodization and physical therapy: bridging the gap between training and rehabilitation. Phys Ther Sport 18:1–20PubMed
91.
go back to reference Marques EA, Mota J, Carvalho J (2011) Exercise effects on bone mineral density in older adults: a meta-analysis of randomized controlled trials. Age 34:1493–1515PubMedPubMedCentral Marques EA, Mota J, Carvalho J (2011) Exercise effects on bone mineral density in older adults: a meta-analysis of randomized controlled trials. Age 34:1493–1515PubMedPubMedCentral
92.
go back to reference Tella SH, Gallagher JC (2014) Prevention and treatment of postmenopausal osteoporosis. J Steroid Biochem Mol Biol 142:155–170PubMed Tella SH, Gallagher JC (2014) Prevention and treatment of postmenopausal osteoporosis. J Steroid Biochem Mol Biol 142:155–170PubMed
93.
go back to reference Zaidi M, Turner CH, Canalis E et al (2009) Bone loss or lost bone: rationale and recommendations for the diagnosis and treatment of early postmenopausal bone loss. Curr Osteoporos Rep 7:118–126PubMed Zaidi M, Turner CH, Canalis E et al (2009) Bone loss or lost bone: rationale and recommendations for the diagnosis and treatment of early postmenopausal bone loss. Curr Osteoporos Rep 7:118–126PubMed
94.
go back to reference Beck BR, Snow CM (2003) Bone health across the lifespan–exercising our options. Exerc Sport Sci Rev 31:117–122PubMed Beck BR, Snow CM (2003) Bone health across the lifespan–exercising our options. Exerc Sport Sci Rev 31:117–122PubMed
95.
go back to reference Kemmler W, von Stengel S (2011) Exercise and osteoporosis-related fractures: perspectives and recommendations of the sports and exercise scientist. Phys Sportmed 39:142–157 Kemmler W, von Stengel S (2011) Exercise and osteoporosis-related fractures: perspectives and recommendations of the sports and exercise scientist. Phys Sportmed 39:142–157
96.
go back to reference Ma D, Wu L, He Z (2013) Effects of walking on the preservation of bone mineral density in perimenopausal and postmenopausal women: a systematic review and meta-analysis. Menopause 20:1216–1226PubMed Ma D, Wu L, He Z (2013) Effects of walking on the preservation of bone mineral density in perimenopausal and postmenopausal women: a systematic review and meta-analysis. Menopause 20:1216–1226PubMed
97.
go back to reference Martyn-St James M, Carroll S (2008) Meta-analysis of walking for preservation of bone mineral density in postmenopausal women. Bone 43:521–531PubMed Martyn-St James M, Carroll S (2008) Meta-analysis of walking for preservation of bone mineral density in postmenopausal women. Bone 43:521–531PubMed
98.
go back to reference Gentil P, Arruda A, Souza D, Giessing J, Paoli A, Fisher J, Steele J (2017) Is there any practical application of meta-analytical results in strength training? Front Physiol 8:1PubMedPubMedCentral Gentil P, Arruda A, Souza D, Giessing J, Paoli A, Fisher J, Steele J (2017) Is there any practical application of meta-analytical results in strength training? Front Physiol 8:1PubMedPubMedCentral
99.
go back to reference Kemmler W (2013) Meta-analysis and exercise related sports medicine [Meta-Analysen im trainingswissenschaftlichen und sportmedizinischen Spannungsfeld]. Dt Ztschr Sportmedizin 64:96–98 Kemmler W (2013) Meta-analysis and exercise related sports medicine [Meta-Analysen im trainingswissenschaftlichen und sportmedizinischen Spannungsfeld]. Dt Ztschr Sportmedizin 64:96–98
100.
go back to reference von Stengel S, Kemmler W, Lauber D, Weineck J, Kalender WA, Engelke K (2005) Power training is more effective than strength training to maintain bone mineral density in postmenopausal woman. J Appl Physiol 99:181–188PubMed von Stengel S, Kemmler W, Lauber D, Weineck J, Kalender WA, Engelke K (2005) Power training is more effective than strength training to maintain bone mineral density in postmenopausal woman. J Appl Physiol 99:181–188PubMed
101.
go back to reference Rhodes EC (1995) Effect of one year of resistance training on strength and bone density in elderly women. Med Sci Sports Exerc 27:S21 Rhodes EC (1995) Effect of one year of resistance training on strength and bone density in elderly women. Med Sci Sports Exerc 27:S21
102.
go back to reference Watson SL, Weeks BK, Weis LJ, Harding AT, Horan SA, Beck BR (2018) 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 33:211–220PubMed Watson SL, Weeks BK, Weis LJ, Harding AT, Horan SA, Beck BR (2018) 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 33:211–220PubMed
Metadata
Title
Effects of Different Types of Exercise on Bone Mineral Density in Postmenopausal Women: A Systematic Review and Meta-analysis
Authors
Wolfgang Kemmler
Mahdieh Shojaa
Matthias Kohl
Simon von Stengel
Publication date
01-11-2020
Publisher
Springer US
Published in
Calcified Tissue International / Issue 5/2020
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-020-00744-w

Other articles of this Issue 5/2020

Calcified Tissue International 5/2020 Go to the issue