Abstract
The aim of this systematic review and meta-analysis was to provide an updated analysis, including the use of more robust methods, on the effects of exercise on bone mineral density in men. Randomised Control Trials of > 24 weeks and published in English up to 01/05/20 were retrieved from 3 electronic databases, cross-referencing, and expert review. The primary outcome measures were changes in FN, LS, and lower limb BMD Standardised effect sizes were calculated from each study and pooled using the inverse heterogeneity model. A statistically significant benefit of exercise was observed on FN BMD [g = 0.21 (0.03, 0.40), Z = 2.23 p = 0.03], with no observed statistically significant benefit of exercise on LS BMD [g = 0.10 (− 0.07, 0.26), Z = 1.15 p = 0.25]. This analysis provided additional evidence to recommend ground- and/or joint-reaction force exercises for improving or maintaining FN, but not LS BMD. Additional well-designed RCTs are unlikely to alter this evidence, although interventions that include activities that directly load the lumbar spine are needed to ensure this is not a potential method of improving LS BMD.
Similar content being viewed by others
Data Availability
An Open Science Framework project entitled the effects of exercise on bone mineral density in men: a systematic review and meta-analysis of randomised controlled trials with all materials can be found here https://doi.org/10.17605/OSF.IO/E6W3V [42]
Abbreviations
- BMD :
-
Bone mineral density
- DPA:
-
Dual-energy photon absorptiometry
- DXA:
-
Dual-energy X-ray absorptiometry
- ES:
-
Effect size
- FN:
-
Femoral neck
- g:
-
Hedges standardised mean difference effect size
- GRADE:
-
Grading of Recommendations assessment, development and evaluation
- IVhet:
-
Inverse heterogeneity
- LFK:
-
Luis furuya-kanamori
- LS:
-
Lumbar spine
- NNS:
-
Number-needed-to-screen
- PRISMA:
-
Preferred reporting items for systematic reviews and meta-analyses
- pQCT:
-
Peripheral quantified computer tomography
- RCT:
-
Randomised controlled trial
- SD:
-
Standard deviation
References
Unluhizarci K (2019) Osteoporosis: unawareness or Ignorance? Erciyes Med J 41(1):1–3
Sözen T, Özışık L, Başaran NÇ (2017) An overview and management of osteoporosis. Eur J Rheumatolo 4(1):46
Center JR, Nguyen TV, Schneider D, Sambrook PN, Eisman JA (1999) Mortality after all major types of osteoporotic fracture in men and women: an observational study. Lancet 353(9156):878–882
Feldstein A, Elmer PJ, Orwoll E, Herson M, Hillier T (2003) Bone mineral density measurement and treatment for osteoporosis in older individuals with fractures: a gap in evidence-based practice guideline implementation. Arch Intern Med 163(18):2165–2172
Reginster JY, Burlet N (2006) Osteoporosis: a still increasing prevalence. Bone 38(2):4–9
Forsen L, Søgaard A, Meyer H, Edna TH, Kopjar B (1999) Survival after hip fracture: short-and long-term excess mortality according to age and gender. Osteoporos Int 10(1):73–78
Haentjens P, Magaziner J, Colón-Emeric CS, Vanderschueren D, Milisen K, Velkeniers B et al (2010) Meta-analysis: excess mortality after hip fracture among older women and men. Ann Intern Med 152(6):380–390
Holt G, Smith R, Duncan K, Hutchison J, Gregori A (2008) Gender differences in epidemiology and outcome after hip fracture: evidence from the Scottish hip fracture audit. J Bone Jt Surg Br Vol 90(4):480–483
Sterling RS (2011) Gender and race/ethnicity differences in hip fracture incidence, morbidity, mortality, and function. Clin Orthop Rel Res 469(7):1913–1918
Kelley GA, Kelley KS, Kohrt WM (2013) Exercise and bone mineral density in men: a meta-analysis of randomized controlled trials. Bone 53(1):103–111
Khan K, McKay H, Kannus P, Wark J, Bailey D, Bennell K (2001) Physical activity and bone health: human kinetics, pp 275, HB
Barry DW, Kohrt WM (2008) BMD decreases over the course of a year in competitive male cyclists. J Bone Miner Res 23(4):484–491
Fredericson M, Ngo J, Cobb K (2005) Effects of ball sports on future risk of stress fracture in runners. Clin J Sport Med 15(3):136–141
Fredericson M, Chew K, Ngo J, Cleek T, Kiratli J, Cobb K (2007) Regional bone mineral density in male athletes: a comparison of soccer players, runners and controls. Br J Sports Med 41(10):664–668
Nagle KB, Brooks MA (2011) A systematic review of bone health in cyclists. Sports health 3(3):235–243
Kujala UM, Kaprio J, Kannus P, Sarna S, Koskenvuo M (2000) Physical activity and osteoporotic hip fracture risk in men. Arch Intern Med 160(5):705–708
Stagi S, Cavalli L, Cavalli T, de Martino M, Brandi ML (2016) Peripheral quantitative computed tomography (pQCT) for the assessment of bone strength in most of bone affecting conditions in developmental age: a review. Ital J Pediatr 42(1):1–20
Colt E, Akram M, Sunyer FP (2017) Comparison of high-resolution peripheral quantitative computerized tomography with dual-energy X-ray absorptiometry for measuring bone mineral density. Eur J Clin Nutr 71(6):778–781
Bolam KA, Skinner TL, Jenkins DG, Galvao DA, Taaffe DR (2015) The osteogenic effect of impact-loading and resistance exercise on bone mineral density in middle-aged and older men: a pilot study. Gerontology 62(1):22–32
Allison SJ, Folland JP, Rennie WJ, Summers GD, Brooke-Wavell K (2013) High impact exercise increased femoral neck bone mineral density in older men: a randomised unilateral intervention. Bone 53(2):321–328
Doi SA, Barendregt JJ, Khan S, Thalib L, Williams GM (2015) Advances in the meta-analysis of heterogeneous clinical trials I: the inverse variance heterogeneity model. Contemp Clin Trials 45:130–138
Furuya-Kanamori L, Thalib L, Barendregt JJ (2017) Meta-analysis in evidence-based healthcare: a paradigm shift away from random effects is overdue. Int J Evid Based Healthc 15(4):152–160
VanderWeele TJ, Ding P (2017) Sensitivity analysis in observational research: introducing the E-value. Ann Intern Med 167(4):268–274
Furuya-Kanamori L, Barendregt JJ, Doi SA (2018) A new improved graphical and quantitative method for detecting bias in meta-analysis. Int J Evid Based Healthc 16(4):195–203
Garner P, Hopewell S, Chandler J, MacLehose H, Akl EA, Beyene J et al (2016) When and how to update systematic reviews: consensus and checklist. BMJ 354:i3507
Sacks H, Chalmers TC, Smith H (1982) Randomized versus historical controls for clinical trials. Am J Med 72(2):233–240
Schulz KF, Chalmers I, Hayes RJ, Altman DG (1995) Empirical evidence of bias: dimensions of methodological quality associated with estimates of treatment effects in controlled trials. JAMA 273(5):408–412
Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS med 6(7):e1000097
Hamilton BR, Staines KA, Kelley GA, Kelley KS, Kohrt WM, Pitsiladis Y et al (2020) The effects of exercise on Bone Mineral Density in Men: a protocol for a systematic review and meta-analysis of randomised controlled trials. SportRxiv. https://doi.org/10.31236/osf.io/y8nue
Hamilton BR, Staines K, Kelley GA, Kelley KS, Kohrt WM, Pitsiladis YP et al (2020) The effects of exercise on bone mineral density in men: a systematic review and meta-analysis of randomised controlled trials. Available from: https://www.crd.york.ac.uk/prospero/display_record.php?ID=CRD42020180441. Accessed 31 May 2020
Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560
Cohen J (1968) Weighted kappa: nominal scale agreement with provision for scaled disagreement or partial credit. Psychol Bull 70:213–220
Lee E, Dobbins M, DeCorby K, McRae L, Tirilis D, Husson H (2012) An optimal search filter for retrieving systematic reviews and meta-analyses. BMC Med Res Methodol 12(1):51
Sterne JA, Savović J, Page MJ, Elbers RG, Blencowe NS, Boutron I et al (2019) RoB 2: a revised tool for assessing risk of bias in randomised trials. BMJ. https://doi.org/10.1136/bmj.l4898
Maher CG, Sherrington C, Herbert RD, Moseley AM, Elkins M (2003) Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther 83(8):713–721
Smart NA, Waldron M, Ismail H, Giallauria F, Vigorito C, Cornelissen V et al (2015) Validation of a new tool for the assessment of study quality and reporting in exercise training studies: TESTEX. Int J Evid Based Healthc 13(1):9–18
Ahn S, Becker BJ (2011) Incorporating quality scores in meta-analysis. J Educ Behav Stat 36(5):555–585
Hedges LV, Olkin I (2014) Statistical methods for meta-analysis. Academic Press, pp 191, HB
Follmann D, Elliott P, Suh I, Cutler J (1992) Variance imputation for overviews of clinical trials with continuous response. J Clin Epidemiol 45(7):769–773
Furuya-Kanamori L, Xu C, Lin L, Doan T, Chu H, Thalib L et al (2020) P value–driven methods were underpowered to detect publication bias: analysis of Cochrane review meta-analyses. J Clin Epidemiol 118:86–92
Schünemann H, Brożek J, Guyatt G, Oxman A. 2013 GRADE handbook for grading quality of evidence and strength of recommendations. Updated October 2013. The GRADE Working Group, 2013. Available from guidelinedevelopment org/handbook
Hamilton BR, Staines K, Kelley GA, Kelley KS, Kohrt WM, Pitsiladis YP et al (2021) The effects of exercise on bone mineral density in men: a systematic review and meta-analysis of randomised controlled trials. [Cited 6 Mar 2021]; Available from: https://osf.io/e6w3v/. Accessed 6 Mar 2021
Hong WL (2004) Tai Chi and resistance training exercise: would these really improve the health of the elderly?: The Chinese University of Hong Kong (Hong Kong). ProQuest Dissertations Publishing. 3150510
Kukuljan S, Nowson CA, Sanders KM, Nicholson GC, Seibel MJ, Salmon J et al (2011) Independent and combined effects of calcium-vitamin D3 and exercise on bone structure and strength in older men: an 18-month factorial design randomized controlled trial. J Clin Endocrinol Metab 96(4):955–963
Helge EW, Andersen TR, Schmidt JF, Jorgensen NR, Hornstrup T, Krustrup P et al (2014) Recreational football improves bone mineral density and bone turnover marker profile in elderly men. Scand J Med Sci Sports 24(Suppl 1):98–104
Harding AT, Weeks BK, Lambert C, Watson SL, Weis LJ, Beck BR (2020) Effects of supervised high-intensity resistance and impact training or machine-based isometric training on regional bone geometry and strength in middle-aged and older men with low bone mass: The LIFTMOR-M semi-randomised controlled trial. Bone 136:115362
Newton RU, Galvao DA, Spry N, Joseph D, Chambers SK, Gardiner RA et al (2019) Exercise mode specificity for preserving spine and hip bone mineral density in prostate cancer patients. Med Sci Sports Exerc 51(4):607–614
Zeilman CJ III (2007) Inflammatory bowel disease, osteoporosis, exercise, and bone mineral density. University of Florida, Gainesville, p 56
Uth J, Hornstrup T, Christensen JF, Christensen KB, Jorgensen NR, Schmidt JF et al (2016) Efficacy of recreational football on bone health, body composition, and physical functioning in men with prostate cancer undergoing androgen deprivation therapy: 32-week follow-up of the FC prostate randomised controlled trial. Osteoporos Int 27(4):1507–1518
Bjerre ED, Jørgensen AB, Petersen TH, Eriksen AR, Midtgaard J, Krustrup P et al (2019) Football compared with usual care in men with prostate cancer (FC prostate community trial): a pragmatic multicentre randomized controlled trial. Sports Med 49(1):145–158
Kemmler W, Kohl M, Frohlich M, Jakob F, Engelke K, von Stengel S et al (2020) Effects of high-intensity resistance training on osteopenia and sarcopenia parameters in older men with osteosarcopenia-one-year results of the randomized controlled Franconian osteopenia and sarcopenia trial (FrOST). J Bone Miner Res 35(9):1634–1644
Kim SH, Seong DH, Yoon SM, Choi YD, Choi E, Song Y et al (2018) The effect on bone outcomes of home-based exercise intervention for prostate cancer survivors receiving androgen deprivation therapy: a pilot randomized controlled trial. Cancer Nurs 41(5):379–388
Ashe MC, Santos IKd, Edward NY, Burnett LA, Barnes R, Fleig L et al (2021) Physical activity and bone health in men: a systematic review and meta-analysis. J Bone Metab 28(1):27–39
Booth A, Clarke M, Dooley G, Ghersi D, Moher D, Petticrew M et al (2012) The nuts and bolts of PROSPERO: an international prospective register of systematic reviews. Syst Rev 1(1):1–9
Rücker G, Schumacher M (2008) Simpson’s paradox visualized: the example of the rosiglitazone meta-analysis. BMC Med Res Methodol 8(1):1–8
Bloomfield SA, Little K, Nelson M, Yingling V (2004) American college of sports medicine position stand: physical activity and bone health. Med Sci Sports Exerc 195(9131/04):3611
Watts NB, Adler RA, Bilezikian JP, Drake MT, Eastell R, Orwoll ES et al (2012) Osteoporosis in men: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 97(6):1802–1822
Bull FC, Al-Ansari SS, Biddle S, Borodulin K, Buman MP, Cardon G et al (2020) World Health Organization 2020 guidelines on physical activity and sedentary behaviour. Br J Sports Med 54(24):1451–1462
Funding
This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.
Author information
Authors and Affiliations
Contributions
Conceptualization, FMG and KS; methodology, BRH, FMG and GK; writing–original draft preparation, BRH and FMG; writing–review and editing, ALL.
Corresponding author
Ethics declarations
Conflict of interest
There are no competing interests for any author.
Ethical Approval
No ethical approval was required for this study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hamilton, B.R., Staines, K.A., Kelley, G.A. et al. The Effects of Exercise on Bone Mineral Density in Men: A Systematic Review and Meta-Analysis of Randomised Controlled Trials. Calcif Tissue Int 110, 41–56 (2022). https://doi.org/10.1007/s00223-021-00893-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00223-021-00893-6