Skip to main content

The effects of exercise on the bone health of people with cancer: a systematic review and meta-analysis

Abstract

Purpose

To determine the pooled effect of exercise on the bone health of people diagnosed with cancer.

Methods

Four electronic databases were systematically searched. Controlled trials that assessed the effect of exercise on the bone mineral density (BMD) or content (BMC) measured by dual-energy x-ray absorptiometry or peripheral quantitative computed tomography in people who had been diagnosed with cancer were included in the study. Random-effect meta-analyses of effect size (ES) were conducted. Sub-group analyses were performed to explore the influence of intervention duration, prescription and participant characteristics.

Results

Of 66 full-text articles screened, 22 studies, from 21 interventions, were included (primarily breast/prostate cancer, sample range n = 36–498). When all interventions were grouped, a significant pooled ES was observed for exercise on hip (ES = 0.112, 95% CI: 0.026 to 0.198; p = 0.011) and lumbar spine BMD (ES = 0.269, 95% CI: 0.036 to 0.501; p = 0.024) compared to control. There was also an influence of sex, where females had greater improvements in hip (ES = 0.120, 95% CI: 0.017 to 0.223; p = 0.022) and spine BMD (ES = 0.415, 95% CI: 0.056 to 0.774; p = 0.23) compared to males.

Conclusion

Overall, exercise regimens of studies included in this review appear to improve bone health at the hip and spine in people diagnosed with cancer. Sub-analyses suggest some influence of sex, where females had greater improvements in BMD compared to males. It is essential that future studies evaluate the dose–response of exercise training on bone health and create exercise protocols that better align with the laws of bone modelling to enhance osteogenic potential.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Data availability

All analysed data is available as supplementary material to this manuscript submission.

References

  1. 1.

    Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71: 209- 249.

  2. 2.

    Saad F, Adachi J, Brown J, Canning L, Gelmon K, Josse R, Pritchard K (2008) Cancer treatment–induced bone loss in breast and prostate cancer. J Clin Oncol 26:5465–5476

    PubMed  Article  Google Scholar 

  3. 3.

    Higano C (2008) Androgen-deprivation-therapy-induced fractures in men with nonmetastatic prostate cancer: what do we really know? Nat Clin Pract Urol 5:24–34

    PubMed  Article  PubMed Central  Google Scholar 

  4. 4.

    Van Poznak C (2015) Bone health in adults treated with endocrine therapy for early breast or prostate cancer. Am Soc Clin Oncol Educ Book e567–574

  5. 5.

    Winters-Stone K, Schwartz A, Nail L (2010) A review of exercise interventions to improve bone health in adult cancer survivors. J Cancer Surviv 4:187–201

    PubMed  Article  PubMed Central  Google Scholar 

  6. 6.

    Oefelein M, Ricchiuti V, Conrad W, Resnick M (2002) Skeletal fractures negatively correlate with overall survival in men with prostate cancer. J Urol 168:1005–1007

    PubMed  Article  PubMed Central  Google Scholar 

  7. 7.

    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 24:2749–2762

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  8. 8.

    Guadalupe-Grau A, Fuentes T, Guerra B, Calbet J (2009) Exercise and bone mass in adults. Sports Med 39:439–468

    PubMed  Article  PubMed Central  Google Scholar 

  9. 9.

    Nikander R, Sievanen H, Heinonen A, Daly R, Uusi-Rasi K, Kannus P (2010) Targeted exercise against osteoporosis: a systematic review and meta-analysis for optimising bone strength throughout life. BMC Med 8:47

    PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    Dalla Via J, Daly RM, Fraser SF (2018) The effect of exercise on bone mineral density in adult cancer survivors: a systematic review and meta-analysis. Osteoporos Int 29:287–303

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  11. 11.

    Page MJ, McKenzie JE, Bossuyt PM et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. British Journal of Medicine 372:71

    Article  Google Scholar 

  12. 12.

    Verhagen A, De Vet H, De Bie R, Kessels A, Boers M, Bouter L, Knipschild P (1998) The Delphi list: a criteria list for quality assessment of randomized clinical trials for conducting systematic reviews developed by Delphi consensus. J Clin Epidemiol 51:1235–1241

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  13. 13.

    Egger M, Davey-Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. Bristish Medical Journal 315:629–634

    CAS  Article  Google Scholar 

  14. 14.

    Saarto T, Sievänen H, Kellokumpu-Lehtinen P et al (2012) Effect of supervised and home exercise training on bone mineral density among breast cancer patients. A 12-month randomised controlled trial. Osteoporos Int 23:1601–1612

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  15. 15.

    Schwartz A, Winters-Stone K, Gallucci B (2007) Exercise effects on bone mineral density in women with breast cancer receiving adjuvant chemotherapy. Oncol Nurs Forum 34:627–633

    PubMed  Article  PubMed Central  Google Scholar 

  16. 16.

    Borenstein M, Hedges LV, Higgins JP, Rothstein HR (2009) Introduction to meta-analysis. John Wiley & Sons, Ltd

  17. 17.

    Newton RU, Galvão DA, Spry N, Joseph D, Chambers SK, Gardiner RA, Wall BA, Bolam KA, Taaffe DR (2019) Exercise mode specificity for preserving spine and hip bone mineral density in prostate cancer patients. Med Sci Sports Exerc 51:607–614

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  18. 18.

    Cormie P, Galvão D, Spry N, Joseph D, Chee R, Taaffe D, Chambers S, Newton R (2015) Can supervised exercise prevent treatment toxicity in patients with prostate cancer initiating androgen-deprivation therapy: a randomised controlled trial. BJU Int 115:256–266

    PubMed  Article  PubMed Central  Google Scholar 

  19. 19.

    Nikander R, Sievänen H, Ojala K, Kellokumpu-Lehtinen P, Palva T, Blomqvist C, Luoto R, Saarto T (2012) Effect of exercise on bone structural traits, physical performance and body composition in breast cancer patients - A 12-month RCT. J Musculoskelet Neuronal Interact 12:127–135

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Artese A, Hunt R, Ormsbee M, Kim J-S, Arjmandi B, Panton L (2020) Effect of functional impact training on body composition, bone mineral density, and strength in breast cancer survivors. Med Sci Sports Exerc 53:90-101

  21. 21.

    Bjerre ED, Petersen TH, Jørgensen AB et al (2019) Community-based football in men with prostate cancer: 1-year follow-up on a pragmatic, multicentre randomised controlled trial. PLoS Med 16:e1002936

    PubMed  PubMed Central  Article  Google Scholar 

  22. 22.

    de Paulo TRS, Winters-Stone KM, Viezel J, Rossi FE, Simões RR, Tosello G, Freitas IFJ (2018) Effects of resistance plus aerobic training on body composition and metabolic markers in older breast cancer survivors undergoing aromatase inhibitor therapy. Exp Gerontol 111:210–217

    PubMed  Article  PubMed Central  Google Scholar 

  23. 23.

    Dieli-Conwright CM, Courneya KS, Demark-Wahnefried W et al (2018) Aerobic and resistance exercise improves physical fitness, bone health, and quality of life in overweight and obese breast cancer survivors: a randomized controlled trial. Breast Cancer Res 20:124

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  24. 24.

    Irwin M, Alvarez-Reeves M, Cadmus L, Mierzejewski E, Mayne S, Yu H, Chung G, Jones B, Knobf M, DiPietro L (2009) Exercise Improves Body Fat, Lean Mass, and Bone Mass in Breast Cancer survivors. Obesity 17:1534–1541

    PubMed  Article  PubMed Central  Google Scholar 

  25. 25.

    Kim SH, Seong DH, Yoon SM, Choi YD, Choi E, Song Y, Song H (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 41:379–388

    PubMed  Article  PubMed Central  Google Scholar 

  26. 26.

    Knobf M, Jeon S, Smith B, Harris L, Kerstetter J, Thompson A, Insogna K (2016) Effect of a randomized controlled exercise trial on bone outcomes: influence of adjuvant endocrine therapy. Breast Cancer Res Treat 155:491–500

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. 27.

    Nilsen T, Raastad T, Skovlund E, Courneya K, Langberg C, Lilleby W, Fosså S, Thorsen L (2016) Effects of strength training on body composition, physical functioning, and quality of life in prostate cancer patients during androgen deprivation therapy. Acta Oncol 54:1805–1813

    Article  CAS  Google Scholar 

  28. 28.

    Rogers L, Hopkins-Price P, Vicari S et al (2009) A randomized trial to increase physical activity in breast cancer survivors. Med Sci Sports Exerc 41:935–946

    PubMed  Article  PubMed Central  Google Scholar 

  29. 29.

    Taaffe DR, Galvão DA, Spry N, Joseph D, Chambers SK, Gardiner RA, Hayne D, Cormie P, Shum DHK, Newton RU (2019) Immediate versus delayed exercise in men initiating androgen deprivation: effects on bone density and soft tissue composition. BJU Int 123:261–269

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  30. 30.

    Tabatabai LS, Bloom J, Stewart S, Sellmeyer DE (2019) A randomized controlled trial of exercise to prevent bone loss in premenopausal women with breast cancer. J Womens Health (Larchmt) 28:87–92

    Article  Google Scholar 

  31. 31.

    Thomas G, Cartmel B, Harrigan M et al (2017) The effect of exercise on body composition and bone mineral density in breast cancer survivors taking aromatase inhibitors. Obesity 25:346–351

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Uth J, Hornstrup T, Christensen J 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 27:1507–1518

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  33. 33.

    Winters-Stone K, Dobek J, Bennett J, Maddalozzo G, Ryan C, Beer T (2014) Skeletal response to resistance and impact training in prostate cancer survivors. Med Sci Sports Exerc 46:1482–1488

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  34. 34.

    Winters-Stone K, Dobek J, Nail L, Bennett J, Leo M, Naik A, Schwartz A (2011) Strength training stops bone loss and builds muscle in postmenopausal breast cancer survivors: a randomized, controlled trial. Breast Cancer Res Treat 127:447–456

    PubMed  PubMed Central  Article  Google Scholar 

  35. 35.

    Winters-Stone K, Dobek J, Nail L, Bennett J, Leo M, Torgrimson-Ojerio B, Luoh S, Schwartz A (2013) Impact + resistance training improves bone health and body composition in prematurely menopausal breast cancer survivors: a randomized controlled trial. Osteoporos Int 24:1637–1646

    CAS  PubMed  Article  Google Scholar 

  36. 36.

    Winters-Stone K, Laudermilk M, Woo K, JC B, Schmitz K (2014) Influence of weight training on skeletal health of breast cancer survivors with or at risk for breast cancer-related lymphedema. J Canc Surviv 8:260–268

  37. 37.

    Uth J, Hornstrup T, Christensen JF et al (2016) Football training in men with prostate cancer undergoing androgen deprivation therapy: activity profile and short-term skeletal and postural balance adaptations. Eur J Appl Physiol 116:471–480

    PubMed  Article  PubMed Central  Google Scholar 

  38. 38.

    Bjerre ED, Brasso K, Jørgensen AB 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 49:145–158

    PubMed  Article  Google Scholar 

  39. 39.

    Zhang X, Brown JC, Paskett ED, Zemel BS, Cheville AL, Schmitz KH (2017) Changes in arm tissue composition with slowly progressive weight-lifting among women with breast cancer-related lymphedema. Breast Cancer Res Treat 164:79–88

    PubMed  PubMed Central  Article  Google Scholar 

  40. 40.

    Borg G (1998) Borg's Perceived Exertion and Pain Scales. Human Kinetics

  41. 41.

    Warriner AH, Patkar NM, Curtis JR, Delzell E, Gary L, Kilgore M, Saag K (2011) Which fractures are most attributable to osteoporosis? J Clin Epidemiol 64:46–53

    PubMed  PubMed Central  Article  Google Scholar 

  42. 42.

    Bonnick SL (2008) Monitoring Changes in Bone Density. Womens Health 4:89–97

    Google Scholar 

  43. 43.

    Daly RM, Bass SL (2006) Lifetime sport and leisure activity participation is associated with greater bone size, quality and strength in older men. Osteoporos Int 17:1258–1267

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  44. 44.

    Vehmanen L, Sievänen H, Kellokumpu-Lehtinen P et al (2021) Five-year follow-up results of aerobic and impact training on bone mineral density in early breast cancer patients. Osteoporos Int 32:473–482

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  45. 45.

    Vehmanen L, Elomaa I, Blomqvist C, Saarto T (2006) Tamoxifen treatment after adjuvant chemotherapy has opposite effects on bone mineral density in premenopausal patients depending on menstrual status. J Clin Oncol 24:675–680

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  46. 46.

    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 26:1605–1618

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  47. 47.

    Xu J, Lombardi G, Jiao W, Banfi G (2016) Effects of exercise on bone status in female subjects, from young girls to postmenopausal women: an overview of systematic reviews and meta-analyses. Sports Med 46:1165–1182

    PubMed  Article  PubMed Central  Google Scholar 

  48. 48.

    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 20:1216–1226

    PubMed  Article  PubMed Central  Google Scholar 

  49. 49.

    Russo C (2009) The effects of exercise on bone. Basic concepts and implications for the prevention of fractures. Clin Cases Miner Bone Metab 6:223–228

    PubMed  PubMed Central  Google Scholar 

  50. 50.

    Galvao D, Nosaka K, Taaffe D, Spry N, Kristjanson L, McGuigan M, Suzuki K, Yamaya K, Newton R (2006) Resistance training and reduction of treatment side effects in prostate cancer patients. Med Sci Sports Exerc 38:2045–2052

    PubMed  Article  PubMed Central  Google Scholar 

  51. 51.

    Carter DR (1984) Mechanical loading histories and cortical bone remodeling. Calcification Tissue International 36:S19-24

    Article  Google Scholar 

  52. 52.

    Smith C, Tacey A, Mesinovic J, Scott D, Lin X, Brennan-Speranza TC, Lewis JR, Duque G, Levinger I (2021) The effects of acute exercise on bone turnover markers in middle-aged and older adults: a systematic review. Bone 143:115766

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  53. 53.

    Frost HM (1987) Bone “mass” and the “mechanostat”: a proposal. Anat Rec 219:1–9

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  54. 54.

    Greenspan SL, Coates P, Sereika SM, Nelson JB, Trump DL, Resnick NM (2005) Bone loss after initiation of androgen deprivation therapy in patients with prostate cancer. J Clin Endocrinol Metab 90:6410–6417

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  55. 55.

    Gómez-Cabello A, Ara I, González-Agüero A, Casajús JA, Vicente-Rodríguez G (2012) Effects of training on bone mass in older adults: a systematic review. Sports Med 42:301–325

    PubMed  Article  PubMed Central  Google Scholar 

  56. 56.

    Martyn-St James M, Carroll S (2010) Effects of different impact exercise modalities on bone mineral density in premenopausal women: a meta-analysis. J Bone Miner Metab 28:251–267

    PubMed  Article  PubMed Central  Google Scholar 

  57. 57.

    Liska TM, Kolen AM (2020) The role of physical activity in cancer survivors’ quality of life. Health Qual Life Outcomes 18:197

    PubMed  PubMed Central  Article  Google Scholar 

  58. 58.

    Campbell KL, Winters-Stone KM, Wiskemann J et al (2019) Exercise Guidelines for Cancer Survivors: Consensus Statement from International Multidisciplinary Roundtable. Med Sci Sports Exerc 51:2375–2390

    PubMed  Article  PubMed Central  Google Scholar 

  59. 59.

    Thomas VJ, Seet-Lee C, Marthick M, Cheema BS, Boyer M, Edwards KM (2020) Aerobic exercise during chemotherapy infusion for cancer treatment: a novel randomised crossover safety and feasibility trial. Support Care Cancer 28:625–632

    PubMed  Article  PubMed Central  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Grace L. Rose.

Ethics declarations

Ethics approval

Ethical approval is not required for this type of study.

Consent to participate

Not applicable.

Consent for publication

Not applicable given no financial contribution from any funding body.

Conflict of interest

None.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rose, G.L., Skinner, T.L., Keating, S.E. et al. The effects of exercise on the bone health of people with cancer: a systematic review and meta-analysis. Osteoporos Int (2021). https://doi.org/10.1007/s00198-021-06131-x

Download citation

Keywords

  • Bone density [MESH]
  • Neoplasms [MESH]
  • Exercise [MESH]
  • Impact-loading
  • Meta-analysis [MESH]