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Exercise for improving bone health in women treated for stages I–III breast cancer: a systematic review and meta-analyses

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Abstract

Purpose

The purpose of this study was to evaluate the efficacy of exercise, either alone or in combination with other interventions, compared to a control, for the preservation of bone mineral density (BMD) in early breast cancer (BC) patients.

Methods

A systematic search was conducted to identify randomized or quasi-randomized trials which met inclusion criteria including prescribed exercise for ≥12 months. Ten publications from seven randomized controlled trials (RCTs), involving 1199 participants, were identified. Data on primary and secondary outcome measures related to BMD at the lumbar spine, total hip, femoral neck and greater trochanter were analysed. Meta-analyses were limited to subgroups by menopausal status as other data could not be pooled.

Results

Based on mean differences or mean percentage differences between groups at 1 year, exercise did not preserve BMD or bone mineral content at any site in post-menopausal women. In contrast, evidence from one RCT (n = 498) found that exercise reduced bone loss in pre-menopausal women at the femoral neck [% MD = 1.20 (95% CI 0.22–2.18); P = 0.02] but not at the lumbar spine.

Conclusions

Although this review indicated that exercise may result in a clinically important preservation of bone health among pre-menopausal but not post-menopausal women, further studies are needed to confirm whether or not exercise is important in preservation of bone health in women diagnosed with early BC.

Implications for cancer survivors

Exercise alone may not be sufficient to prevent bone loss in post-menopausal women at high risk of osteoporosis. Further evidence is required to determine if it provides any benefit to pharmacological therapy.

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Notes

  1. SD = (upper 95% CI − lower 95% CI) × √N/(1.96 × 2) [32].

References

  1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66:7–30.

    Article  PubMed  Google Scholar 

  2. Chen Z, Maricic M, Bassford TL, Pettinger M, Ritenbaugh C, Lopez AM, et al. Fracture risk among breast cancer survivors: results from the Women’s Health Initiative Observational Study. Arch Intern Med. 2005;165:552–8.

    Article  PubMed  Google Scholar 

  3. Kanis JA, McCloskey EV, Powles T, Paterson AH, Ashley S, Spector T. A high incidence of vertebral fracture in women with breast cancer. Br J Cancer. 1999;79:1179–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Hadji P. Aromatase inhibitor-associated bone loss in breast cancer patients is distinct from postmenopausal osteoporosis. Crit Rev Oncol Hematol. 2009;69:73–82.

    Article  PubMed  Google Scholar 

  5. Santen RJ. Clinical review: effect of endocrine therapies on bone in breast cancer patients. J Clin Endocrinol Metab. 2011;96:308–19.

    Article  CAS  PubMed  Google Scholar 

  6. Hadji P, Asmar L, van Nes JG, Menschik T, Hasenburg A, Kuck J, et al. The effect of exemestane and tamoxifen on bone health within the Tamoxifen Exemestane Adjuvant Multinational (TEAM) trial: a meta-analysis of the US, German, Netherlands, and Belgium sub-studies. J Cancer Res Clin Oncol. 2011;137:1015–25.

    Article  CAS  PubMed  Google Scholar 

  7. Vehmanen L, Saarto T, Elomaa I, Makela P, Valimaki M, Blomqvist C. Long-term impact of chemotherapy-induced ovarian failure on bone mineral density (BMD) in premenopausal breast cancer patients. The effect of adjuvant clodronate treatment. Eur J Cancer. 2001;37:2373–8.

    Article  CAS  PubMed  Google Scholar 

  8. Shapiro CL, Manola J, Leboff M. Ovarian failure after adjuvant chemotherapy is associated with rapid bone loss in women with early-stage breast cancer. J Clin Oncol. 2001;19:3306–11.

    Article  CAS  PubMed  Google Scholar 

  9. Tonezzer T, Pereira CM, Filho UP, Marx A. Hormone therapy/adjuvant chemotherapy induced deleterious effects on the bone mass of breast cancer patients and the intervention of physiotherapy: a literature review. Eur J Gynaecol Oncol. 2010;31:262–7.

    CAS  PubMed  Google Scholar 

  10. Bruning PF, Pit MJ, de Jong-Bakker M, van den Ende A, Hart A, van Enk A. Bone mineral density after adjuvant chemotherapy for premenopausal breast cancer. Br J Cancer. 1990;61:308–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Goodwin PJ, Ennis M, Pritchard KI, McCready D, Koo J, Sidlofsky S, et al. Adjuvant treatment and onset of menopause predict weight gain after breast cancer diagnosis. J Clin Oncol. 1999;17:120–9.

    Article  CAS  PubMed  Google Scholar 

  12. Saad F, Adachi JD, Brown JP, Canning LA, Gelmon KA, Josse RG, et al. Cancer treatment-induced bone loss in breast and prostate cancer. J Clin Oncol. 2008;26:5465–76.

    Article  PubMed  Google Scholar 

  13. Riggs BL. The mechanisms of estrogen regulation of bone resorption. J Clin Invest. 2000;106:1203–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Freedman OC, Fletcher GG, Gandhi S, Mates M, Dent SF, Trudeau ME, et al. Adjuvant endocrine therapy for early breast cancer: a systematic review of the evidence for the 2014 Cancer Care Ontario systemic therapy guideline. Curr Oncol. 2015;22:S95–S113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Early Breast Cancer Trialists’ Collaborative G. Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet. 2005;365:1687–717.

    Article  Google Scholar 

  16. Smith IE, Dowsett M. Aromatase inhibitors in breast cancer. N Engl J Med. 2003;348:2431–42.

    Article  CAS  PubMed  Google Scholar 

  17. Winters-Stone KM, Laudermilk M, Woo K, Brown JC, Schmitz KH. Influence of weight training on skeletal health of breast cancer survivors with or at risk for breast cancer-related lymphedema. J Cancer Surviv. 2014;8:260–8.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Winters-Stone KM, Dobek J, Nail LM, Bennett JA, Leo MC, Torgrimson-Ojerio B, et al. Impact + resistance training improves bone health and body composition in prematurely menopausal breast cancer survivors: a randomized controlled trial. Osteoporos Int. 2013;24:1637–46.

    Article  CAS  PubMed  Google Scholar 

  19. Saarto T, Sievanen H, Kellokumpu-Lehtinen P, Nikander R, Vehmanen L, Huovinen R, et al. Effect of supervised and home exercise training on bone mineral density among breast cancer patients. A 12-month randomised controlled trial. Osteoporos Int. 2012;23:1601–12.

    Article  CAS  PubMed  Google Scholar 

  20. Winters-Stone KM, Dobek J, Nail L, Bennett JA, Leo MC, Naik A, et al. Strength training stops bone loss and builds muscle in postmenopausal breast cancer survivors: a randomized, controlled trial. [Erratum appears in Breast Cancer Res Treat. 2011 Jun;127(2):457]. Breast Cancer Res Treat. 2011;127:447–56.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Waltman NL, Twiss JJ, Ott CD, Gross GJ, Lindsey AM, Moore TE, et al. 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. 2010;21:1361–9.

    Article  CAS  PubMed  Google Scholar 

  22. Swenson KK, Nissen MJ, Anderson E, Shapiro A, Schousboe J, Leach J. Effects of exercise vs bisphosphonates on bone mineral density in breast cancer patients receiving chemotherapy. J Support Oncol. 2009;7:101–7.

    CAS  PubMed  Google Scholar 

  23. Knobf MT, Jeon S, Smith B, Harris L, Kerstetter J, Thompson AS, et al. Effect of a randomized controlled exercise trial on bone outcomes: influence of adjuvant endocrine therapy. Breast Cancer Res Treat. 2016;155:491–500.

    Article  CAS  PubMed  Google Scholar 

  24. Peppone LJ, Mustian KM, Janelsins MC, Palesh OG, Rosier RN, Piazza KM, et al. Effects of a structured weight-bearing exercise program on bone metabolism among breast cancer survivors: a feasibility trial. Clin Breast Cancer. 2010;10:224–9.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Irwin ML, Alvarez-Reeves M, Cadmus L, Mierzejewski E, Mayne ST, Yu H, et al. Exercise improves body fat, lean mass, and bone mass in breast cancer survivors. Obesity. 2009;17:1534–41.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Schwartz AL, Winters-Stone K, Gallucci B. Exercise effects on bone mineral density in women with breast cancer receiving adjuvant chemotherapy. Oncol Nurs Forum. 2007;34:627–33.

    Article  PubMed  Google Scholar 

  27. Sellmeyer D, Stewart S, Bloom J. A randomized controlled trial of exercise to prevent bone loss and adverse cardiovascular changes in premenopausal women with breast cancer. J Bone Miner Res. 2013;28(S1):FR0428.

  28. Simonavice E, Liu PY, Ilich JZ, Kim JS, Arjmandi B, Panton LB. The effects of a 6-month resistance training and dried plum consumption intervention on strength, body composition, blood markers of bone turnover, and inflammation in breast cancer survivors. Appl Physiol Nutr Metab. 2014;39:730–9.

    Article  CAS  PubMed  Google Scholar 

  29. Howe TE, Shea B, Dawson LJ, Downie F, Murray A, Ross C, et al. Exercise for preventing and treating osteoporosis in postmenopausal women. Cochrane Database Syst Rev. 2011;7:CD000333.

    Google Scholar 

  30. Cramer H, Lauche R, Klose P, Lange S, Langhorst J, Dobos GJ. Yoga for women diagnosed with breast cancer. Cochrane Database Syst Rev. 2013;(​10):CD010802. doi:10.1002/14651858.CD010802.

  31. Winters-Stone KM, Schwartz A, Nail LM. A review of exercise interventions to improve bone health in adult cancer survivors. J Cancer Surviv. 2010;4:187–201.

    Article  PubMed  Google Scholar 

  32. Higgins JPT, Green S (editors). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0. The Cochrane Collaboration. 2011. Available from www.handbook.cochrane.org.

  33. Schulz KF, Altman DG, Moher D, Group C. CONSORT 2010 statement: updated guidelines for reporting parallel group randomised trials. Trials. 2010;11:32.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Nikander R, Sievanen H, Ojala K, Kellokumpu-Lehtinen PL, Palva T, Blomqvist C, et al. Effect of exercise on bone structural traits, physical performance and body composition in breast cancer patients—a 12-month RCT. J Musculoskelet Neuronal Interact. 2012;12:127–35.

    CAS  PubMed  Google Scholar 

  35. Winters-Stone KM, Leo MC, Schwartz A. Exercise effects on hip bone mineral density in older, post-menopausal breast cancer survivors are age dependent. Arch Osteoporos. 2012;7:301–6.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Dobek J, Winters-Stone KM, Bennett JA, Nail L. Musculoskeletal changes after 1 year of exercise in older breast cancer survivors. J Cancer Surviv. 2014;8:304–11.

    Article  PubMed  Google Scholar 

  37. Winters-Stone KM, Dobek J, Nail L, Bennett JA, Leo MC, Naik A, et al. Erratum to: Strength training stops bone loss and builds muscle in postmenopausal breast cancer survivors: a randomized, controlled trial. Breast Cancer Res Treat. 2011;127:457.

    Article  Google Scholar 

  38. Twiss JJ, Waltman NL, Berg K, Ott CD, Gross GJ, Lindsey AM. An exercise intervention for breast cancer survivors with bone loss. J Nurs Scholarsh. 2009;41:20–7.

    Article  PubMed  Google Scholar 

  39. Knobf M, Winters-Stone K. Exercise and cancer. Annu Rev Nurs Res. 2013;31:327–65.

    Article  PubMed  Google Scholar 

  40. Pacifici R. Estrogen, cytokines, and pathogenesis of postmenopausal osteoporosis. J Bone Miner Res. 1996;11:1043–51.

    Article  CAS  PubMed  Google Scholar 

  41. Cenci S, Weitzmann MN, Roggia C, Namba N, Novack D, Woodring J, et al. Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Invest. 2000;106:1229–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Perez EA, Weilbaecher K. Aromatase inhibitors and bone loss. Oncology (Williston Park). 2006;20:1029–39.

  43. Maximov PY, Lee TM, Jordan VC. The discovery and development of selective estrogen receptor modulators (SERMs) for clinical practice. Curr Clin Pharmacol. 2013;8:135–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Kohrt WM. Aging and the osteogenic response to mechanical loading. Int J Sport Nutr Exerc Metab. 2001;11(Suppl):S137–42.

    Article  PubMed  Google Scholar 

  45. Maccormick RE. Possible acceleration of aging by adjuvant chemotherapy: a cause of early onset frailty? Med Hypotheses. 2006;67:212–5.

    Article  CAS  PubMed  Google Scholar 

  46. Arnold P, Bautmans I. The influence of strength training on muscle activation in elderly persons: a systematic review and meta-analysis. Exp Gerontol. 2014;58:58–68.

    Article  PubMed  Google Scholar 

  47. Martyn-St James M, Carroll S. A meta-analysis of impact exercise on postmenopausal bone loss: the case for mixed loading exercise programmes. Br J Sports Med. 2009;43:898–908.

    Article  CAS  PubMed  Google Scholar 

  48. Martyn-St James M, Carroll S. Meta-analysis of walking for preservation of bone mineral density in postmenopausal women. Bone. 2008;43:521–31.

    Article  PubMed  Google Scholar 

  49. Swenson KK, Nissen MJ, Henly SJ. Physical activity in women receiving chemotherapy for breast cancer: adherence to a walking intervention. Oncol Nurs Forum. 2010;37:321–30.

    Article  PubMed  Google Scholar 

  50. Runowicz CD, Leach CR, Henry NL, Henry KS, Mackey HT, Cowens-Alvarado RL, et al. American Cancer Society/American Society of Clinical Oncology Breast Cancer Survivorship Care Guideline. J Clin Oncol. 2016;34:611–35.

    Article  CAS  PubMed  Google Scholar 

  51. Hadji P, Aapro MS, Body JJ, Bundred NJ, Brufsky A, Coleman RE, et al. Management of aromatase inhibitor-associated bone loss in postmenopausal women with breast cancer: practical guidance for prevention and treatment. Ann Oncol. 2011;22:2546–55.

    Article  CAS  PubMed  Google Scholar 

  52. Ott CD, Twiss JJ, Waltman NL, Gross GJ, Lindsey AM. Challenges of recruitment of breast cancer survivors to a randomized clinical trial for osteoporosis prevention. Cancer Nurs. 2006;29:21–31.

  53. Fernandez Ortega A, Jolis Lopez L, Vinas Villaro G, Villanueva Vazquez R, Garcia Arias A, Gonzalez Farre X, et al. Individualization of treatment strategies. Adv Ther. 2011;28(Suppl 6):19–38.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Sharon L. Kilbreath.

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Fornusek, C.P., Kilbreath, S.L. Exercise for improving bone health in women treated for stages I–III breast cancer: a systematic review and meta-analyses. J Cancer Surviv 11, 525–541 (2017). https://doi.org/10.1007/s11764-017-0622-3

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