Skip to main content

Advertisement

Log in

The effect of exercise on bone mineral density in adult cancer survivors: a systematic review and meta-analysis

  • Review
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Purpose

Certain cancer treatments are associated with bone loss and increased fracture risk. Weight-bearing impact exercise, resistance training or the combination, are recommended to preserve or improve bone mineral density (BMD) inhealthy older adults, but their efficacy in cancer survivors is less well understood. The aim of this systematic review with meta-analysis of randomised control trials (RCT) was to review the evidence regarding the role of exercise to counteract cancer treatment-induced bone loss.

Methods

Four databases were searched systematically with 12 RCTs of at least 6-month duration investigating the effects of exercise on BMD compared to a control group in adult cancer survivors identified.

Results

Meta-analysis was completed using available data from six studies enrolling 814 participants, with lumbar spine, femoral neck and/or total hip BMD as the primary outcome measures. Overall, there was no significant benefit of exercise compared to controls on BMD at the lumbar spine (0.0071 g/cm , 95% CI −0.0002 to 0.0145, p = 0.057), femoral neck (0.0044 g/cm , 95% CI −0.0005 to 0.0093, p = 0.077), or total hip (0.0024 g/cm , 95% CI −0.0038 to 0.0086, p = 0.443). Subgroup analysis revealed a positive effect on lumbar spine BMD in three studies implementing a combined resistance and impact exercise intervention (0.015 g/cm , 95% CI 0.003 to 0.028, p = 0.019).

Conclusions

From the evidence available, exercise may not be sufficient to improve bone health in cancer survivors, but given the heterogeneity in the participant characteristics and several exercise programs which may not have been designed to specifically optimise bone health, these findings should be interpreted with caution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Reid DM, Doughty J, Eastell R, Heys SD, Howell A, McCloskey EV, Powles T, Selby P, Coleman RE (2008) Guidance for the management of breast cancer treatment-induced bone loss: a consensus position statement from a UK Expert Group. Cancer Treat Rev 34:S3–S18

    Article  CAS  Google Scholar 

  2. Saad F, Adachi JD, Brown JP, Canning LA, Gelmon KA, Josse RG, Pritchard KI (2008) Cancer treatment-induced bone loss in breast and prostate cancer. J Clin Oncol Off J Am Soc Clin Oncol 26(33):5465–5476

    Article  Google Scholar 

  3. Grossmann M, Hamilton EJ, Gilfillan C, Bolton D, Joon DL, Zajac JD (2011) Bone and metabolic health in patients with non-metastatic prostate cancer who are receiving androgen deprivation therapy. Med J Aust 194(6):301–306

    PubMed  Google Scholar 

  4. Gardner JR, Livingston PM, Fraser SF (2014) Effects of exercise on treatment-related adverse effects for patients with prostate cancer receiving androgen-deprivation therapy: a systematic review. J Clin Oncol Off J Am Soc Clin Oncol 32(4):335–346. https://doi.org/10.1200/JCO.2013.49.5523

    Article  Google Scholar 

  5. Østergren PB, Kistorp C, Bennedbæk FN, Faber J, Sønksen J, Fode M (2016) The use of exercise interventions to overcome adverse effects of androgen deprivation therapy. Nat Rev Urol 13(6):353–364

    Article  Google Scholar 

  6. Loprinzi PD, Cardinal BJ (2012) Effects of physical activity on common side effects of breast cancer treatment. Breast Cancer 19(1):4–10

    Article  Google Scholar 

  7. Casla S, Hojman P, Márquez-Rodas I, López-Tarruella S, Jerez Y, Barakat R, Martín M (2015) Running away from side effects: physical exercise as a complementary intervention for breast cancer patients. Clin Transl Oncol 17(3):180–196

    Article  CAS  Google Scholar 

  8. 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(1):177

    Article  Google Scholar 

  9. Marques E, Mota J, Carvalho J (2012) Exercise effects on bone mineral density in older adults: a meta-analysis of randomized controlled trials. Age (Dordr) 34(6):1493–1515. https://doi.org/10.1007/s11357-011-9311-8

    Article  Google Scholar 

  10. Kelley GA, Kelley KS, Kohrt WM (2013) Exercise and bone mineral density in premenopausal women: a meta-analysis of randomized controlled trials. Int J Endocrinol 2013:741639

    PubMed  PubMed Central  Google Scholar 

  11. 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(5):1605–1618. https://doi.org/10.1007/s00198-015-3034-0

    Article  CAS  PubMed  Google Scholar 

  12. Winters-Stone KM, Schwartz A, Nail LM (2010) A review of exercise interventions to improve bone health in adult cancer survivors. J Cancer Surviv 4(3):187–201. https://doi.org/10.1007/s11764-010-0122-1

    Article  PubMed  Google Scholar 

  13. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6(7):e1000097

  14. Higgins JPT, Green S (editors) The Cochrane Collaboration (2011) Cochrane handbook for systematic reviews of interventions. Version 5.1.0 [updated March 2011]. Available from www.cochrane-handbook.org.

  15. Higgin J, Thompson S, Deeks J, Altman D (2003) Measuring inconsistency in meta-analysis. BMJ 327:557–560

    Article  Google Scholar 

  16. Schwartz AL, Winters-Stone K, Gallucci B (2007) Exercise effects on bone mineral density in women with breast cancer receiving adjuvant chemotherapy. Oncol Nurs Forum 34(3):627–633. https://doi.org/10.1188/07.onf.627-633

    Article  PubMed  Google Scholar 

  17. Irwin ML, Alvarez-Reeves M, Cadmus L, Mierzejewski E, Mayne ST, Yu H, Chung GG, Jones B, Knobf MT, DiPietro L (2009) Exercise improves body fat, lean mass, and bone mass in breast cancer survivors. Obesity (Silver Spring, Md) 17(8):1534–1541. https://doi.org/10.1038/oby.2009.18

    Article  Google Scholar 

  18. Waltman NL, Twiss JJ, Ott CD, Gross GJ, Lindsey AM, Moore TE, Berg K, Kupzyk K (2010) The effect of weight training on bone mineral density and bone turnover in postmenopausal breast cancer survivors with bone loss: a 24-month randomized controlled trial. Osteoporos Int 21(8):1361–1369. https://doi.org/10.1007/s00198-009-1083-y

    Article  CAS  PubMed  Google Scholar 

  19. Winters-Stone KM, Dobek J, Nail L, Bennett JA, Leo MC, 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(2):447–456. https://doi.org/10.1007/s10549-011-1444-z

    Article  PubMed  PubMed Central  Google Scholar 

  20. Saarto T, Sievänen H, Kellokumpu-Lehtinen P, Nikander R, Vehmanen L, Huovinen R, Kautiainen H, Järvenpää S, Penttinen HM, Utriainen M, Jääskeläinen AS, Elme A, Ruohola J, Palva T, Vertio H, Rautalahti M, Fogelholm M, Luoto R, Blomqvist C (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(5):1601–1612

    Article  CAS  Google Scholar 

  21. Winters-Stone KM, Dobek J, Nail LM, Bennett JA, Leo MC, Torgrimson-Ojerio B, Luoh SW, 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(5):1637–1646. https://doi.org/10.1007/s00198-012-2143-2

    Article  CAS  PubMed  Google Scholar 

  22. Winters-Stone KM, Dobek JC, Bennett JA, Maddalozzo GF, Ryan CW, Beer TM (2014) Skeletal response to resistance and impact training in prostate cancer survivors. Med Sci Sports Exerc 46(8):1482–1488. https://doi.org/10.1249/MSS.0000000000000265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Winters-Stone KM, Laudermilk M, Woo K, Brown JC, Schmitz KH (2014) Influence of weight training on skeletal health of breast cancer survivors with or at risk for breast cancer-related lymphedema. J Cancer Surviv 8(2):260–268. https://doi.org/10.1007/s11764-013-0337-z

    Article  PubMed  PubMed Central  Google Scholar 

  24. Kim SH, Cho YU, Kim SJ, Hong S, Han MS, Choi E (2016) The effect on bone outcomes of adding exercise to supplements for osteopenic breast cancer survivors: a pilot randomized controlled trial. Cancer Nurs 39(2):144–152. https://doi.org/10.1097/ncc.0000000000000245

    Article  PubMed  Google Scholar 

  25. Knobf MT, Jeon S, Smith B, Harris L, Kerstetter J, Thompson AS, Insogna K (2016) Effect of a randomized controlled exercise trial on bone outcomes: influence of adjuvant endocrine therapy. Breast Cancer Res Treat 155(3):491–500. https://doi.org/10.1007/s10549-016-3693-3

    Article  CAS  PubMed  Google Scholar 

  26. Uth J, Hornstrup T, Christensen JF, Christensen KB, Jørgensen NR, Schmidt JF, Brasso K, Jakobsen MD, Sundstrup E, Andersen LL, Rørth M, Midtgaard J, Krustrup P, Helge EW (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

    Article  CAS  Google Scholar 

  27. Thomas GA, Cartmel B, Harrigan M, Fiellin M, Capozza S, Zhou Y, Ercolano E, Gross CP, Hershman D, Ligibel J, Schmitz K, Li F-Y, Sanft T, Irwin ML (2017) The effect of exercise on body composition and bone mineral density in breast cancer survivors taking aromatase inhibitors. Obesity 25(2):346–351. https://doi.org/10.1002/oby.21729

    Article  CAS  PubMed  Google Scholar 

  28. Bassey E, Rothwell M, Littlewood J, Pye D (1998) Pre-and postmenopausal women have different bone mineral density responses to the same high-impact exercise. J Bone Miner Res 13(12):1805–1813

    Article  CAS  Google Scholar 

  29. 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(4):196–200

    Article  Google Scholar 

  30. Beck BR, Snow CM (2003) Bone health across the lifespan—exercising our options. Exerc Sport Sci Rev 31(3):117–122

    Article  Google Scholar 

  31. Winters-Stone KM, Snow CM (2003) Musculoskeletal response to exercise is greatest in women with low initial values. Med Sci Sports Exerc 35(10):1691–1696

    Article  Google Scholar 

  32. Kohrt WM, Bloomfield SA, Little KD, Nelson ME, Yingling VR (2004) ACSM position stand: physical activity and bone health. Med Sci Sports Exerc 36(11):1985–1996

    Article  Google Scholar 

  33. Martyn-St James M, Carroll S (2008) Meta-analysis of walking for preservation of bone mineral density in postmenopausal women. Bone 43(3):521–531

    Article  Google Scholar 

  34. 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(11):1216–1226

    Article  Google Scholar 

  35. Beck BR, Daly RM, Singh MAF, Taaffe DR (2017) Exercise and Sports Science Australia (ESSA) position statement on exercise prescription for the prevention and management of osteoporosis. J Sci Med Sport 20(5):438–445. https://doi.org/10.1016/j.jsams.2016.10.001

    Article  PubMed  Google Scholar 

  36. Turner C (1998) Three rules for bone adaptation to mechanical stimuli. Bone 23(5):399–407

    Article  CAS  Google Scholar 

  37. Winters-Stone KM, Snow CM (2006) Site-specific response of bone to exercise in premenopausal women. Bone 39(6):1203–1209

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Dalla Via.

Ethics declarations

Conflicts of interest

None.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dalla Via, J., Daly, R.M. & Fraser, S.F. The effect of exercise on bone mineral density in adult cancer survivors: a systematic review and meta-analysis. Osteoporos Int 29, 287–303 (2018). https://doi.org/10.1007/s00198-017-4237-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-017-4237-3

Keywords

Navigation