Skip to main content
Top
Published in: Osteoporosis International 8/2020

Open Access 01-08-2020 | Review

Effects of dynamic resistance exercise on bone mineral density in postmenopausal women: a systematic review and meta-analysis with special emphasis on exercise parameters

Authors: M. Shojaa, S. von Stengel, M. Kohl, D. Schoene, W. Kemmler

Published in: Osteoporosis International | Issue 8/2020

Login to get access

Abstract

This systematic review and meta-analysis set out to determine the effect of dynamic resistance exercise (DRT) on areal bone mineral density (aBMD) in postmenopausal women and derive evidence-based recommendations for optimized training protocols. A systematic review of the literature according to the PRISMA statement included (a) controlled trials, (b) of isolated DRT with at least one exercise and one control group, (c) with intervention durations ≥ 6 months, (d) aBMD assessments at lumbar spine or proximal femur, (e) in cohorts of postmenopausal women. We searched eight electronic databases up to March 2019 without language restrictions. The meta-analysis was performed using a random-effects model. Standardized mean differences (SMD) for BMD changes at lumbar spine (LS), femoral neck (FN), and total hip (TH) were defined as outcome measures. Moderators of the exercise effects, i.e., “intervention length,” “type of DRT,” “training frequency,” “exercise intensity,” and “exercise volume,” were addressed by sub-group analyses. The study was registered in the international prospective register of systematic reviews (PROSPERO) under ID: CRD42018095097. Seventeen articles with 20 exercise and 18 control groups were eligible. SMD average is 0.54 (95% CI 0.22–0.87) for LS-BMD, 0.22 (0.07–0.38) for FN-BMD, and 0.48 (0.22–0.75) for TH-BMD changes (all p ≤ 0.015). While sub-group analysis for FN-BMD revealed no differences within categories of moderators, lower training frequency (< 2 sessions/week) resulted in significantly higher BMD changes at LS and TH compared to higher training frequency (≥ 2 sessions/week). Additionally, free weight training was significantly superior to DRT devices for improving TH-BMD. This work provided further evidence for significant, albeit only low–moderate, effects of DRT on LS-, FN-, and TH-BMD. Unfortunately, sub-analysis results did not allow meaningful exercise recommendations to be derived. This systematic review and meta-analysis observed a significant low–moderate effect of dynamic resistance exercise on bone mineral density changes in postmenopausal women. However, sub-group analyses focusing on exercise characteristics found no results that enable the derivation of meaningful exercise recommendations in the area of exercise and osteoporosis prevention or therapy.
Footnotes
1
We do not exclude studies with participants that were not community dwelling
 
2
One study reported CI and 8 studies utilized SE.
 
3
…considering participants attendance rate.
 
4
> 30% of bone tissue loss as determined by X-ray assessment at LS or hip.
 
5
In addition to the DRT, Kohrt et al. [26] applied 2–3 × 10 min bouts of intense rowing exercise.
 
6
This relates to the high intensity exercise groups of three studies [19, 25, 32]. Further, one study [30] prescribed sets of 20–30 reps for two exercises.
 
7
E.g. 10 reps at 30% maximum isometric back muscle strength [34] or 14–16 reps at 40% 1RM [19, 32]. The same might be true for some exercises of the protocol of Woo et al. [35].
 
8
Comparing Pedro Score categories (low < 5 vs. moderate 5–6 vs. high ≥ 7 score points; [14]) did not indicate significant BMD differences (p > 0.416) at LS-, FN-, and TH-ROI.
 
9
Of importance, femoral neck ROI is a usually 15 mm slide across the middle-distal end of the femoral neck, while total hip ROI started slightly below the trochanter minor and include intertrochanter, trochanter, ward, and femoral neck ROI.
 
10
…nor the results of higher effects on femoral neck ROI compared to total hip ROI.
 
11
At least when bearing in mind that initial conditioning phases conducted by most studies might further shorten the period of over-threshold strain application…
 
12
Apart from two studies, all the RT studies included progressively increased exercise intensity during the intervention (Table 2).
 
13
LS-BMD: 5 (low ExFr) vs. 13 (high ExFr) study groups TH: 2 vs. 9 study groups (see “Results”).
 
14
Ashe et al. [55]: 0–2 sessions/w.(s/w); Bailey et al. [56]: 0–7 s/w; Bemben et al. [57]: 2 vs. 3 s/w. However, studies did not adjust for subjects’ attendance; therefore, results should be interpreted with caution.
 
15
While exercise protocols of studies that did not detect difference for TrFr were 6, 8, and 12 months, the lengths of studies that detected significant higher BMD changes in favor of the higher TrFr were 1.5, 4, 12, and 16 years.
 
16
In detail, the subgroup analysis on this issue was inconsistent, with higher effects of low intensity for TH-BMD and moderate intensity for FN- and LS-BMD.
 
17
This might be the main difference to meta-analysis in the area of pharmaceutic agents or supplements (e.g. [75, 76], with their limited number of inherent modulators.
 
18
In contrast to other researchers (e.g. [77]), we do solely include studies that apply progression (i.e. progressive resistance training as defined as “exercise in which a load is increased in predetermined steps” [78]).
 
19
By definition “strength” started at 30% 1RM [10]; relative intensity of 10 min of rowing (at least ≥ 250 reps) is below this cutoff.
 
20
E.g., as defined according to the set endpoint approach of Steele et al. [38].
 
21
as reported in time under tension in different sections of the movement (e.g., concentric–isometric–eccentric).
 
Literature
1.
go back to reference Kemmler W, Bebenek M, Kohl M, Von Stengel S (2015) Exercise and fractures in postmenopausal women. Final results of the controlled Erlangen Fitness and Osteoporosis Prevention Study (EFOPS). Osteoporos Int 26:2491–2499PubMed Kemmler W, Bebenek M, Kohl M, Von Stengel S (2015) Exercise and fractures in postmenopausal women. Final results of the controlled Erlangen Fitness and Osteoporosis Prevention Study (EFOPS). Osteoporos Int 26:2491–2499PubMed
2.
go back to reference Kemmler W, Haberle L, von Stengel S (2013) Effects of exercise on fracture reduction in older adults: a systematic review and meta-analysis. Osteoporos Int 24:1937–1950PubMed Kemmler W, Haberle L, von Stengel S (2013) Effects of exercise on fracture reduction in older adults: a systematic review and meta-analysis. Osteoporos Int 24:1937–1950PubMed
3.
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
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 Howe TE, Shea B, Dawson LJ et al (2011) Exercise for preventing and treating osteoporosis in postmenopausal women. Cochrane Database Syst Rev:CD000333 Howe TE, Shea B, Dawson LJ et al (2011) Exercise for preventing and treating osteoporosis in postmenopausal women. Cochrane Database Syst Rev:CD000333
7.
go back to reference Kelley GA, Kelley KS, Kohrt WM (2012) Effects of ground and joint reaction force exercise on lumbar spine and femoral neck bone mineral density in postmenopausal women: a meta-analysis of randomized controlled trials. BMC Musculoskelet Disord 13:177PubMedPubMedCentral Kelley GA, Kelley KS, Kohrt WM (2012) Effects of ground and joint reaction force exercise on lumbar spine and femoral neck bone mineral density in postmenopausal women: a meta-analysis of randomized controlled trials. BMC Musculoskelet Disord 13:177PubMedPubMedCentral
8.
go back to reference Martyn-St. James M, Caroll S (2006) High intensity resistance training and postmenopausal bone loss: a meta-analysis. Osteoporos Int 17:1225–1240PubMed Martyn-St. James M, Caroll S (2006) High intensity resistance training and postmenopausal bone loss: a meta-analysis. Osteoporos Int 17:1225–1240PubMed
9.
go back to reference 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. Osteoporos Int 26:1605–1618PubMed 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. Osteoporos Int 26:1605–1618PubMed
10.
go back to reference Weineck J (2019) Optimales training. Spitta-Verlag, Erlangen Weineck J (2019) Optimales training. Spitta-Verlag, Erlangen
11.
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
12.
go back to reference de Morton NA (2009) The PEDro scale is a valid measure of the methodological quality of clinical trials: a demographic study. Aust J Physiother 55:129–133PubMed de Morton NA (2009) The PEDro scale is a valid measure of the methodological quality of clinical trials: a demographic study. Aust J Physiother 55:129–133PubMed
13.
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
14.
go back to reference Ribeiro de Avila V, Bento T, Gomes W, Leitao J, Fortuna de Sousa N (2018) Functional outcomes and quality of life after ankle fracture surgically treated: a systematic review. J Sport Rehabil 27:274–283PubMed Ribeiro de Avila V, Bento T, Gomes W, Leitao J, Fortuna de Sousa N (2018) Functional outcomes and quality of life after ankle fracture surgically treated: a systematic review. J Sport Rehabil 27:274–283PubMed
15.
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
16.
go back to reference R_Development_Core_Team (2019) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing R_Development_Core_Team (2019) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing
17.
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
18.
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
19.
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
20.
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
21.
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
22.
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
23.
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
24.
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
25.
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
26.
go back to reference Kohrt WM, Ehsani AA, Brige SJ Jr (1997) Effects of exercise involving predominantly either joint-reaction of ground-reaction forces on bone mineral density in older women. J Bone Miner Res 12:1253–1261PubMed Kohrt WM, Ehsani AA, Brige SJ Jr (1997) Effects of exercise involving predominantly either joint-reaction of ground-reaction forces on bone mineral density in older women. J Bone Miner Res 12:1253–1261PubMed
27.
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
28.
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
29.
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
30.
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
31.
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
32.
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
33.
go back to reference 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 34:18–22PubMedPubMedCentral 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 34:18–22PubMedPubMedCentral
34.
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
35.
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
36.
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
37.
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
38.
go back to reference Steele J, Fisher J, Giessing J, Gentil P (2017) Clarity in reporting terminology and definitions of set end points in resistance training. Muscle Nerve 368-374:368–374 Steele J, Fisher J, Giessing J, Gentil P (2017) Clarity in reporting terminology and definitions of set end points in resistance training. Muscle Nerve 368-374:368–374
39.
go back to reference Toigo M, Boutellier U (2006) New fundamental resistance exercise determinants of molecular and cellular muscle adaptations. Eur J Appl Physiol 97:643–663PubMed Toigo M, Boutellier U (2006) New fundamental resistance exercise determinants of molecular and cellular muscle adaptations. Eur J Appl Physiol 97:643–663PubMed
40.
go back to reference Hartard M, Haber P, Ilieva D, et al. (1994) Einfluß eines systematischen Krafttrainings auf die Knochendichte und auf das Niveau von Schmerzen und Befindlichkeit in einer Gruppe von Frauen mit Osteopenie. In Ließen H, Weiß M, Baum M (eds) Regulations- und Repairmechanismen. Köln Hartard M, Haber P, Ilieva D, et al. (1994) Einfluß eines systematischen Krafttrainings auf die Knochendichte und auf das Niveau von Schmerzen und Befindlichkeit in einer Gruppe von Frauen mit Osteopenie. In Ließen H, Weiß M, Baum M (eds) Regulations- und Repairmechanismen. Köln
41.
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
42.
go back to reference Bergmann G, Deuretzbacher G, Heller M, Graichen F, Rohlmann A, Strauss J, Duda GN (2001) Hip contact forces and gait patterns from routine activities. J Biomech 34:859–871PubMed Bergmann G, Deuretzbacher G, Heller M, Graichen F, Rohlmann A, Strauss J, Duda GN (2001) Hip contact forces and gait patterns from routine activities. J Biomech 34:859–871PubMed
43.
go back to reference Kelley GA, Kelley KS, Tran ZV (2001) Resistance training and bone mineral density in women: a meta-analysis of controlled trials. Am J Phys Med Rehabil 80:65–77PubMed Kelley GA, Kelley KS, Tran ZV (2001) Resistance training and bone mineral density in women: a meta-analysis of controlled trials. Am J Phys Med Rehabil 80:65–77PubMed
44.
go back to reference Zhao R, Zhang M, Zhang Q (2017) The effectiveness of combined exercise interventions for preventing postmenopausal bone loss: a systematic review and meta-analysis. J Orthop Sports Phys Ther 47:241–251PubMed Zhao R, Zhang M, Zhang Q (2017) The effectiveness of combined exercise interventions for preventing postmenopausal bone loss: a systematic review and meta-analysis. J Orthop Sports Phys Ther 47:241–251PubMed
46.
go back to reference Frost HM (1988) Vital biomechanics: proposed general concepts for skeletal adaptations to mechanical usage. Calcif Tissue Int 42:145–156PubMed Frost HM (1988) Vital biomechanics: proposed general concepts for skeletal adaptations to mechanical usage. Calcif Tissue Int 42:145–156PubMed
47.
go back to reference Kemmler W, Engelke K, von Stengel S, Weineck J, Lauber D, Kalender WA (2007) Long-term four-year exercise has a positive effect on menopausal risk factors: the Erlangen Fitness Osteoporosis Prevention Study. J Strength Cond Res 21:232–239PubMed Kemmler W, Engelke K, von Stengel S, Weineck J, Lauber D, Kalender WA (2007) Long-term four-year exercise has a positive effect on menopausal risk factors: the Erlangen Fitness Osteoporosis Prevention Study. J Strength Cond Res 21:232–239PubMed
48.
go back to reference Kemmler W, Engelke K, von Stengel S (2016) Long-term exercise and bone mineral density changes in postmenopausal women-are there periods of reduced effectiveness? J Bone Miner Res 31:215–222PubMed Kemmler W, Engelke K, von Stengel S (2016) Long-term exercise and bone mineral density changes in postmenopausal women-are there periods of reduced effectiveness? J Bone Miner Res 31:215–222PubMed
49.
go back to reference Haff GG (2000) Roundtable discussion: machines versus free weights. Strength Conditioning J 22:18–30 Haff GG (2000) Roundtable discussion: machines versus free weights. Strength Conditioning J 22:18–30
50.
go back to reference Schott N, Johnen B, Holfelder B (2019) Effects of free weights and machine training on muscular strength in high-functioning older adults. Exp Gerontol 122:15–24PubMed Schott N, Johnen B, Holfelder B (2019) Effects of free weights and machine training on muscular strength in high-functioning older adults. Exp Gerontol 122:15–24PubMed
51.
go back to reference Newman AB, Kupelian V, Visser M, Simonsick EM, Goodpaster BH, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB, on Behalf of the Health, Aging and Body Composition Study Investigators (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 61:72–77PubMed Newman AB, Kupelian V, Visser M, Simonsick EM, Goodpaster BH, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB, on Behalf of the Health, Aging and Body Composition Study Investigators (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 61:72–77PubMed
52.
go back to reference Roshanravan B, Patel KV, Fried LF, Robinson-Cohen C, de Boer IH, Harris T, Murphy RA, Satterfield S, Goodpaster BH, Shlipak M, Newman AB, Kestenbaum B, for the Health ABC study (2017) Association of muscle endurance, fatigability, and strength with functional limitation and mortality in the health aging and body composition study. J Gerontol A Biol Sci Med Sci 72:284–291PubMed Roshanravan B, Patel KV, Fried LF, Robinson-Cohen C, de Boer IH, Harris T, Murphy RA, Satterfield S, Goodpaster BH, Shlipak M, Newman AB, Kestenbaum B, for the Health ABC study (2017) Association of muscle endurance, fatigability, and strength with functional limitation and mortality in the health aging and body composition study. J Gerontol A Biol Sci Med Sci 72:284–291PubMed
53.
go back to reference Visser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, Simonsick EM, Harris TB, for the Health ABC Study (2005) Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci Med Sci 60:324–333PubMed Visser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, Simonsick EM, Harris TB, for the Health ABC Study (2005) Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci Med Sci 60:324–333PubMed
54.
go back to reference Wagner P (2000) Aussteigen oder Dabeibleiben? Institute of Sportsciences. Technical University Darmstadt, Darmstadt, p 298 Wagner P (2000) Aussteigen oder Dabeibleiben? Institute of Sportsciences. Technical University Darmstadt, Darmstadt, p 298
55.
go back to reference Ashe MC, Gorman E, Khan KM, Brasher PM, Cooper DM, McKay HA, Liu-Ambrose T (2013) Does frequency of resistance training affect tibial cortical bone density in older women? A randomized controlled trial. Osteoporos Int 24:623–632PubMed Ashe MC, Gorman E, Khan KM, Brasher PM, Cooper DM, McKay HA, Liu-Ambrose T (2013) Does frequency of resistance training affect tibial cortical bone density in older women? A randomized controlled trial. Osteoporos Int 24:623–632PubMed
56.
go back to reference Bailey CA, Brooke-Wavell K (2010) Optimum frequency of exercise for bone health: randomised controlled trial of a high-impact unilateral intervention. Bone 46:1043–1049PubMed Bailey CA, Brooke-Wavell K (2010) Optimum frequency of exercise for bone health: randomised controlled trial of a high-impact unilateral intervention. Bone 46:1043–1049PubMed
57.
go back to reference Bemben DA, Bemben MG (2011) Dose-response effect of 40 weeks of resistance training on bone mineral density in older adults. Osteoporos Int 22:179–186PubMed Bemben DA, Bemben MG (2011) Dose-response effect of 40 weeks of resistance training on bone mineral density in older adults. Osteoporos Int 22:179–186PubMed
58.
go back to reference Cussler EC, Going SB, Houtkooper LB, Stanford VA, Blew RM, Flint-Wagner HG, Metcalfe LL, Choi JE, Lohman TG (2005) Exercise frequency and calcium intake predict 4-year bone changes in postmenopausal women. Osteoporos Int 16:2129–2141PubMed Cussler EC, Going SB, Houtkooper LB, Stanford VA, Blew RM, Flint-Wagner HG, Metcalfe LL, Choi JE, Lohman TG (2005) Exercise frequency and calcium intake predict 4-year bone changes in postmenopausal women. Osteoporos Int 16:2129–2141PubMed
59.
go back to reference Kemmler W, von Stengel S (2013) Exercise frequency, health risk factors, and diseases of the elderly. Arch Phys Med Rehabil 94:2046–2053PubMed Kemmler W, von Stengel S (2013) Exercise frequency, health risk factors, and diseases of the elderly. Arch Phys Med Rehabil 94:2046–2053PubMed
60.
go back to reference Kemmler W, von Stengel S (2014) Dose-response effect of exercise frequency on bone mineral density in post-menopausal, osteopenic women. Scand J Med Sci Sports 24:526–534PubMed Kemmler W, von Stengel S (2014) Dose-response effect of exercise frequency on bone mineral density in post-menopausal, osteopenic women. Scand J Med Sci Sports 24:526–534PubMed
61.
go back to reference Kemmler W, von Stengel S, Kohl M (2016) Exercise frequency and bone mineral density development in exercising postmenopausal osteopenic women. Is there a critical dose of exercise for affecting bone? Results of the Erlangen Fitness and Osteoporosis Prevention Study. Bone 89:1–6PubMed Kemmler W, von Stengel S, Kohl M (2016) Exercise frequency and bone mineral density development in exercising postmenopausal osteopenic women. Is there a critical dose of exercise for affecting bone? Results of the Erlangen Fitness and Osteoporosis Prevention Study. Bone 89:1–6PubMed
62.
go back to reference Maddalozzo GF, Snow CM (2000) High intensity resistance training: effects on bone in older men and women. Calcif Tissue Int 66:399–404PubMed Maddalozzo GF, Snow CM (2000) High intensity resistance training: effects on bone in older men and women. Calcif Tissue Int 66:399–404PubMed
63.
go back to reference Taaffe DR, Pruitt L, Pyka G, Guido D, Marcus R (1996) Comparative effects of high- and low-intensity resistance training on thigh muscle strength, fiber area, and tissue composition in elderly women. Clin Physiol 16:381–392PubMed Taaffe DR, Pruitt L, Pyka G, Guido D, Marcus R (1996) Comparative effects of high- and low-intensity resistance training on thigh muscle strength, fiber area, and tissue composition in elderly women. Clin Physiol 16:381–392PubMed
64.
go back to reference Vincent KR, Braith RW (2002) Resistance exercise and bone turnover in elderly men and women. Med Sci Sports Exerc 34:17–23PubMed Vincent KR, Braith RW (2002) Resistance exercise and bone turnover in elderly men and women. Med Sci Sports Exerc 34:17–23PubMed
65.
go back to reference Hsieh YF, Turner CH (2001) Effects of loading frequency on mechanically induced bone formation. J Bone Miner Res 16:918–924PubMed Hsieh YF, Turner CH (2001) Effects of loading frequency on mechanically induced bone formation. J Bone Miner Res 16:918–924PubMed
66.
go back to reference Rubin CT, Lanyon LE (1985) Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int 37:411–417PubMed Rubin CT, Lanyon LE (1985) Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int 37:411–417PubMed
67.
go back to reference Frost HM (1987) Bone mass and the mechanostat. A proposal. Anat Rec 219:1–19PubMed Frost HM (1987) Bone mass and the mechanostat. A proposal. Anat Rec 219:1–19PubMed
68.
go back to reference Hsieh YF, Robling AG, Ambrosius WT, Burr DB, Turner CH (2001) Mechanical loading of diaphyseal bone in vivo: the strain threshold for an osteogenic response varies with location. J Bone Miner Res 16:2291–2297PubMed Hsieh YF, Robling AG, Ambrosius WT, Burr DB, Turner CH (2001) Mechanical loading of diaphyseal bone in vivo: the strain threshold for an osteogenic response varies with location. J Bone Miner Res 16:2291–2297PubMed
69.
go back to reference Mosley JR, Lanyon LE (1998) Strain rate as a controlling influence on adaptive modeling in response to dynamic loading of the ulna in growing male rats. Bone 23:313–318PubMed Mosley JR, Lanyon LE (1998) Strain rate as a controlling influence on adaptive modeling in response to dynamic loading of the ulna in growing male rats. Bone 23:313–318PubMed
70.
go back to reference Turner CH (1998) Three rules for bone adaptation to mechanical stimuli. Bone 23:399–407PubMed Turner CH (1998) Three rules for bone adaptation to mechanical stimuli. Bone 23:399–407PubMed
71.
go back to reference Rubin CT, Lanyon LE (1984) Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am 66:397–402PubMed Rubin CT, Lanyon LE (1984) Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am 66:397–402PubMed
72.
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
73.
go back to reference Cullen DM, Smith RT, Akhter MP (2001) Bone-loading response varies with strain magnitude and cycle number. J Appl Physiol 91:1971–1976PubMed Cullen DM, Smith RT, Akhter MP (2001) Bone-loading response varies with strain magnitude and cycle number. J Appl Physiol 91:1971–1976PubMed
74.
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
75.
go back to reference Wang YK, Zhang YM, Qin SQ, Wang X, Ma T, Guo JB, Zhu C, Luo ZJ (2018) Effects of alendronate for treatment of glucocorticoid-induced osteoporosis: a meta-analysis of randomized controlled trials. Medicine (Baltimore) 97:e12691 Wang YK, Zhang YM, Qin SQ, Wang X, Ma T, Guo JB, Zhu C, Luo ZJ (2018) Effects of alendronate for treatment of glucocorticoid-induced osteoporosis: a meta-analysis of randomized controlled trials. Medicine (Baltimore) 97:e12691
76.
go back to reference Tai V, Leung W, Grey A, Reid IR, Bolland MJ (2015) Calcium intake and bone mineral density: systematic review and meta-analysis. BMJ 351:h4183PubMedPubMedCentral Tai V, Leung W, Grey A, Reid IR, Bolland MJ (2015) Calcium intake and bone mineral density: systematic review and meta-analysis. BMJ 351:h4183PubMedPubMedCentral
77.
go back to reference Martyn-St James M, Carroll S (2006) Progressive high-intensity resistance training and bone mineral density changes among premenopausal women: evidence of discordant site-specific skeletal effects. Sports Med 36:683–704PubMed Martyn-St James M, Carroll S (2006) Progressive high-intensity resistance training and bone mineral density changes among premenopausal women: evidence of discordant site-specific skeletal effects. Sports Med 36:683–704PubMed
78.
go back to reference Kent M (2007) The Oxford dictionary of sports science & medicine. Oxford University Press, Oxford Kent M (2007) The Oxford dictionary of sports science & medicine. Oxford University Press, Oxford
79.
go back to reference Chubak J, Ulrich CM, Tworoger SS et al (2006) Effect of exercise on bone mineral density and lean mass in postmenopausal women. Med Sci Sports Exerc 38:1236–1244PubMed Chubak J, Ulrich CM, Tworoger SS et al (2006) Effect of exercise on bone mineral density and lean mass in postmenopausal women. Med Sci Sports Exerc 38:1236–1244PubMed
80.
go back to reference Olmedillas H, Gonzalez-Aguero A, Moreno LA, Casajus JA, Vicente-Rodriguez G (2012) Cycling and bone health: a systematic review. BMC Med 10:168PubMedPubMedCentral Olmedillas H, Gonzalez-Aguero A, Moreno LA, Casajus JA, Vicente-Rodriguez G (2012) Cycling and bone health: a systematic review. BMC Med 10:168PubMedPubMedCentral
81.
go back to reference Turner CH, Owan I, Takano Y (1995) Mechanotransduction in bone: role of strain rate. Am J Physiol Endocrinol Metab 269:E438–E442 Turner CH, Owan I, Takano Y (1995) Mechanotransduction in bone: role of strain rate. Am J Physiol Endocrinol Metab 269:E438–E442
82.
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
83.
go back to reference Mangione KK, Miller AH, Naughton IV (2010) Cochrane review: improving physical function and performance with progressive resistance strength training in older adults. Phys Ther 90:1711–1715PubMed Mangione KK, Miller AH, Naughton IV (2010) Cochrane review: improving physical function and performance with progressive resistance strength training in older adults. Phys Ther 90:1711–1715PubMed
84.
go back to reference Li G, Taljaard M, Van den Heuvel ER et al (2017) An introduction to multiplicity issues in clinical trials: the what, why, when and how. Int J Epidemiol 46:746–755PubMed Li G, Taljaard M, Van den Heuvel ER et al (2017) An introduction to multiplicity issues in clinical trials: the what, why, when and how. Int J Epidemiol 46:746–755PubMed
85.
go back to reference Sterne JA, Sutton AJ, Ioannidis JP et al (2011) Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ 343:d4002PubMed Sterne JA, Sutton AJ, Ioannidis JP et al (2011) Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ 343:d4002PubMed
Metadata
Title
Effects of dynamic resistance exercise on bone mineral density in postmenopausal women: a systematic review and meta-analysis with special emphasis on exercise parameters
Authors
M. Shojaa
S. von Stengel
M. Kohl
D. Schoene
W. Kemmler
Publication date
01-08-2020
Publisher
Springer London
Published in
Osteoporosis International / Issue 8/2020
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-020-05441-w

Other articles of this Issue 8/2020

Osteoporosis International 8/2020 Go to the issue