Exercise effects on bone mineral density in older men: a systematic review with special emphasis on study interventions

Review

Abstract

This systematic review detected only limited positive effects of exercise on bone mineral density in older men. Further, based on the present literature, we were unable to suggest dedicated exercise prescriptions for this male cohort that might differ from recommendations based on studies with postmenopausal women. The primary aim of this systematic review was to determine the effect of exercise on bone mineral density (BMD) in healthy older men. A systematic review of the literature according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement included only randomized or non-randomized controlled trials of exercise training ≥ 6 months with study groups of ≥ eight healthy men aged 50 years or older, not using bone-relevant pharmacological therapy, that determined BMD by dual-energy X-ray absorptiometry. We searched PubMed, Scopus, Web of Science, Cochrane, Science Direct, and Eric up to November 2016. Risk of bias was assessed using the PEDro scale. We identified eight trials with 789 participants (PEDro-score, mean value 6 of 10) which satisfied our eligibility criteria. Studies vary considerably with respect to type and composition of exercise. Study interventions of six trials were considered to be appropriate for successfully addressing BMD in this cohort. Between-group differences were not or not consistently reported by three studies. Three studies reported significant exercise effects on BMD for proximal femur; one of them determined significant differences between the exercise groups. None of the exercise trials determined significant BMD effects at the lumbar spine. Based on the present studies, there is only limited evidence for a favorable effect of exercise on BMD in men. More well-designed and sophisticated studies on BMD in healthy older men have to address this topic. Further, there is a need to define intervention quality standards and implement a universal scoring system that allows this pivotal determinant to be addressed much more intensively.

Keywords

Bone mineral density Exercise Men Overview Training 

Notes

Acknowledgements

We would like to thank the Friedrich-Alexander University of Erlangen-Nürnberg for funding the study.

Compliance with ethical standards

Conflicts of interest

None.

Supplementary material

198_2018_4482_MOESM1_ESM.doc (64 kb)
ESM 1 (DOC 64 kb)

References

  1. 1.
    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 26:2491–2499CrossRefPubMedGoogle Scholar
  2. 2.
    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 24:1937–1950CrossRefPubMedGoogle Scholar
  3. 3.
    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 13:177CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Marques EA, Mota J, Carvalho J (2011) Exercise effects on bone mineral density in older adults: a meta-analysis of randomized controlled trials. Age 34:1493–1515CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Martyn-St James M, Carroll S (2011) Effects of different impact exercise modalities on bone mineral density in premenopausal women: a meta-analysis. J Bone Miner Metab 28:251–267CrossRefGoogle Scholar
  6. 6.
    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 26:1605–1618CrossRefPubMedGoogle Scholar
  7. 7.
    Cawthon PM, Shahnazari M, Orwoll ES, Lane NE (2016) Osteoporosis in men: findings from the Osteoporotic Fractures in Men Study (MrOS). Ther Adv Musculoskelet Dis 8:15–27CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Cummings SR, Browner WS, Bauer D, Stone K, Ensrud K, Jamal S, Ettinger B (1998) Endogenous hormones and the risk of hip and vertebral fractures among older women. Study of Osteoporotic Fractures Research Group. N Engl J Med 339:733–738CrossRefPubMedGoogle Scholar
  9. 9.
    Cummings SR, Cawthon PM, Ensrud KE, Cauley JA, Fink HA, Orwoll ES, Osteoporotic Fractures in Men Research G, Study of Osteoporotic Fractures Research G (2006) BMD and risk of hip and nonvertebral fractures in older men: a prospective study and comparison with older women. J Bone Miner Res 21:1550–1556CrossRefPubMedGoogle Scholar
  10. 10.
    Bolam KA, van Uffelen JG, Taaffe DR (2013) The effect of physical exercise on bone density in middle-aged and older men: a systematic review. Osteoporos Int 24:2749–2762CrossRefPubMedGoogle Scholar
  11. 11.
    Kelley GA, Kelley KS, Tran ZV (2000) Exercise and bone mineral density in men: a meta-analysis. J Appl Physiol 88:1730–1736CrossRefPubMedGoogle Scholar
  12. 12.
    Kelley GA, Kelley KS, Kohrt WM (2013) Exercise and bone mineral density in men: a meta-analysis of randomized controlled trials. Bone 53:103–111CrossRefPubMedGoogle Scholar
  13. 13.
    Nichols JF, Rauh MJ (2011) Longitudinal changes in bone mineral density in male master cyclists and nonathletes. J Strength Cond Res 25:727–734CrossRefPubMedGoogle Scholar
  14. 14.
    Kemmler W, von Stengel S (2011) Exercise and osteoporosis-related fractures: perspectives and recommendations of the sports and exercise scientist. Phys Sportmed 39:142–157CrossRefGoogle Scholar
  15. 15.
    de Morton NA (2009) The PEDro scale is a valid measure of the methodological quality of clinical trials: a demographic study. Aust J Physiother 55:129–133CrossRefPubMedGoogle Scholar
  16. 16.
    Sherrington C, Herbert RD, Maher CG, Moseley AM (2000) PEDro. A database of randomized trials and systematic reviews in physiotherapy. Man Ther 5:223–226CrossRefPubMedGoogle Scholar
  17. 17.
    Kemmler W, von Stengel S (2016) Osteoporose. In: Mooren C, Knapp G, Reimers CD (eds) Prävention und Therapie durch Sport. Urban und Fischer, MünchenGoogle Scholar
  18. 18.
    Allison SJ, Folland JP, Rennie WJ, Summers GD, Brooke-Wavell K (2013) High impact exercise increased femoral neck bone mineral density in older men: a randomised unilateral intervention. Bone 53:321–328CrossRefPubMedGoogle Scholar
  19. 19.
    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 62:22–32CrossRefPubMedGoogle Scholar
  20. 20.
    Helge EW, Andersen TR, Schmidt JF, Jorgensen NR, Hornstrup T, Krustrup P, Bangsbo J (2014) Recreational football improves bone mineral density and bone turnover marker profile in elderly men. Scand J Med Sci Sports 24(Suppl 1):98–104CrossRefPubMedGoogle Scholar
  21. 21.
    Huuskonen J, Väisänen SB, Kröger H, Jurvelin JS, Alhava A, Rauramaa R (2001) Regular physical exercise and bone mineral density: a four-year controlled randomized trial in middle-aged men. Osteoporos Int 12:249–355CrossRefGoogle Scholar
  22. 22.
    Kukuljan S, Nowson CA, Sanders KM, Nicholson GC, Seibel MJ, Salmon J, Daly RM (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 96:955–963CrossRefPubMedGoogle Scholar
  23. 23.
    McCartney N, Hicks AL, Martin J, Webber CE (1995) Long-term resistance training in the elderly: effects on dynamic strength, exercise capacity, muscle, and bone. J Gerontol 50A:B97–B104CrossRefGoogle Scholar
  24. 24.
    Whiteford J, Ackland TR, Dhaliwal SS, James AP, Woodhouse JJ, Price R, Prince RL, Kerr DA (2010) Effects of a 1-year randomized controlled trial of resistance training on lower limb bone and muscle structure and function in older men. Osteoporos Int 21:1529–1536CrossRefPubMedGoogle Scholar
  25. 25.
    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 36:262–268CrossRefPubMedGoogle Scholar
  26. 26.
    Steele J, Fisher J, Giessing J, Gentil P (2017) Clarity in reporting terminology and definitions of set end points in resistance training. Muscle Nerve 368-374:368–374CrossRefGoogle Scholar
  27. 27.
    Baron RE (1997) Anatomy and ultrastructure of bone. In: Baron RE (ed) Osteoporosis—fundamentals of clinical practice. Lippincott-Raven, New York, pp 3–10Google Scholar
  28. 28.
    Christen P, Ito K, Ellouz R, Boutroy S, Sornay-Rendu E, Chapurlat RD, van Rietbergen B (2014) Bone remodelling in humans is load-driven but not lazy. Nat Commun 5:4855CrossRefPubMedGoogle Scholar
  29. 29.
    Joober R, Schmitz N, Annable L, Boksa P (2012) Publication bias: what are the challenges and can they be overcome? J Psychiatry Neurosci 37:149–152CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Schwarzer G, Carpenter JR, Rücker G (2015) Small-study effects in meta-analysis. In: Schwarzer G (ed) Meta-analysis with R. Springer-Verlag, Heidelberg, pp 107–141Google Scholar
  31. 31.
    Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) When does it make sense to perform a meta-analysis. In: Borenstein M (ed) Introduction to meta-analysis. John Wiley & Son, ChicesterCrossRefGoogle Scholar
  32. 32.
    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 99:181–188CrossRefPubMedGoogle Scholar
  33. 33.
    Greco T, Zangrillo A, Biondi-Zoccai G, Landoni G (2013) Meta-analysis: pitfalls and hints. Heart Lung Vessel 5:219–225PubMedPubMedCentralGoogle Scholar
  34. 34.
    Kukuljan S, Nowson CA, Sanders K, Daly RM (2009) Effects of resistance exercise and fortified milk on skeletal muscle mass, muscle size, and functional performance in middle-aged and older men: an 18-mo randomized controlled trial. J Appl Physiol 107:1864–1873CrossRefPubMedGoogle Scholar
  35. 35.
    Kelley GA, Kelley KS, Vu Tran Z (2002) Exercise and lumbar spine bone mineral density in postmenopausal women: a meta-analysis of individual patient data. J Gerontol 57A:M599–M604CrossRefGoogle Scholar
  36. 36.
    Martyn-St. James M, Caroll S (2006) High intensity exercise training and postmenopausal bone loss: a meta-analysis. Osteoporos Int 17:1225–1240CrossRefPubMedGoogle Scholar
  37. 37.
    Martyn-St James M, Carroll S (2009) A meta-analysis of impact exercise on postmenopausal bone loss: the case for mixed loading exercise programmes. Br J Sports Med 43:898–908CrossRefPubMedGoogle Scholar
  38. 38.
    Wallace BA, Cumming RG (2000) Systematic review of randomized trials of the effect of exercise on bone mass in pre- and postmenopausal women. Calcif Tissue Int 67:10–18CrossRefPubMedGoogle Scholar
  39. 39.
    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 36:683–704CrossRefPubMedGoogle Scholar
  40. 40.
    Gomez-Bruton A, Gonzalez-Aguero A, Gomez-Cabello A, Casajus JA, Vicente-Rodriguez G (2013) Is bone tissue really affected by swimming? A systematic review. PLoS One 8:e70119CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Gomez-Cabello A, Ara I, Gonzalez-Aguero A, Casajus JA, Vicente-Rodriguez G (2012) Effects of training on bone mass in older adults: a systematic review. Sports Med 42:301–325CrossRefPubMedGoogle Scholar
  42. 42.
    Martyn-St James M, Carroll S (2008) Meta-analysis of walking for preservation of bone mineral density in postmenopausal women. Bone 43:521–531CrossRefPubMedGoogle Scholar
  43. 43.
    Wolff I, van Croonenborg JJ, Kemper HC, Kostense PJ, Twisk JW (1999) The effect of exercise training programs on bone mass: a meta-analysis of published controlled trials in pre- and postmenopausal women. Osteoporos Int 9:1–12CrossRefPubMedGoogle Scholar
  44. 44.
    Ernst E (1998) Exercise for female osteoporosis. A systematic review of randomised clinical trials. Sports Med 25:359–368CrossRefPubMedGoogle Scholar
  45. 45.
    Casez JP, Fischer S, Stussi E, Stalder H, Gerber A, Delmas PD, Colombo JP, Jaeger P (1995) Bone mass at lumbar spine and tibia in young males—impact of physical fitness, exercise, and anthropometric parameters: a prospective study in a cohort of military recruits. Bone 17:211–219CrossRefPubMedGoogle Scholar
  46. 46.
    Leichter I, Simkin A, Margulies JY, Bivas A, Steinberg R, Giladi M, Milgrom C (1989) Gain in mass density of bone following strenguous physical activity. J Orthop Res 7:86–90CrossRefPubMedGoogle Scholar
  47. 47.
    Sharp MA, Knapik JJ, Walker LA, Burrell L, Frykman PN, Darakjy SS, Lester ME, Marin RE (2008) Physical fitness and body composition after a 9-month deployment to Afghanistan. Med Sci Sports Exerc 40:1687–1692CrossRefPubMedGoogle Scholar
  48. 48.
    Eriksen EF (2010) Cellular mechanisms of bone remodeling. Rev Endocr Metab Disord 11:219–227CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Nikander R, Sievanen H, Heinonen A, Daly RM, Uusi-Rasi K, Kannus P (2010) Targeted exercise against osteoporosis: a systematic review and meta-analysis for optimising bone strength throughout life. BMC Med 8:47CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    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 31:215–222CrossRefPubMedGoogle Scholar
  51. 51.
    Guglielmi G, Floriani I, Torri V, Li J, van Kuijk C, Genant HK, Lang TF (2005) Effect of spinal degenerative changes on volumetric bone mineral density of the central skeleton as measured by quantitative computed tomography. Acta Radiol 46:269–275CrossRefPubMedGoogle Scholar
  52. 52.
    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):W264CrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2018

Authors and Affiliations

  • W. Kemmler
    • 1
  • M. Shojaa
    • 1
  • M. Kohl
    • 2
  • S. von Stengel
    • 1
  1. 1.Institute of Medical PhysicsFriedrich-Alexander University of Erlangen-NürnbergErlangenGermany
  2. 2.Department of Medical and Life SciencesUniversity of FurtwangenFurtwangen im SchwarzwaldGermany

Personalised recommendations