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Osteoporosis International

, Volume 24, Issue 5, pp 1637–1646 | Cite as

Impact + resistance training improves bone health and body composition in prematurely menopausal breast cancer survivors: a randomized controlled trial

  • K. M. Winters-Stone
  • J. Dobek
  • L. M. Nail
  • J. A. Bennett
  • M. C. Leo
  • B. Torgrimson-Ojerio
  • S.-W. Luoh
  • A. Schwartz
Original Article

Abstract

Summary

Our randomized controlled trial in prematurely menopausal breast cancer survivors showed that impact + resistance training prevented increases in percentage of body fat compared with controls and also improved BMD at the hip and prevented BMD loss at the spine among exercise-trained women who were menopausal for >1 year.

Introduction

Cancer treatment-related menopause worsens bone health and body composition in breast cancer survivors (BCS). We investigated whether impact + resistance training could improve bone mineral density (BMD), reduce bone turnover, build muscle, and decrease fat mass in BCS with premature menopause.

Methods

We conducted a randomized controlled trial in 71 BCS (mean age, 46.5 years) within 5 years of treatment-related menopause. Women were randomly assigned to one of two groups: (1) impact + resistance training (prevent osteoporosis with impact + resistance (POWIR)) or (2) exercise placebo (FLEX) 3×/week for 1 year. Outcomes were hip and spine BMD (in grams per square centimeter) and body composition (percent body fat (%BF) and lean and fat mass (in kilograms)) by DXA and bone turnover markers (serum osteocalcin (in nanograms per milliliter) and urinary deoxypryrodinoline (in nanomoles per milliliter).

Results

There were no significant group × time interactions for bone outcomes when using an intent-to-treat approach on the full sample. In analyses restricted to BCS who were menopausal for ≥1 year, POWIR increased BMD at the hip and slowed BMD loss at the spine compared with FLEX (femoral neck—POWIR, 0.004 ± 0.093 g/cm2 vs. FLEX, −0.010 ± 0.089 g/cm2; p < 0.01; spine—POWIR, −0.003 ± 0.114 g/cm2 vs. FLEX, −0.020 ± 0.110 g/cm2; p = 0.03). POWIR prevented increases in %BF (POWIR, 0.01 % vs. FLEX, 1.3 %; p < 0.04). Women with attendance to POWIR at ≥64 % had better improvements in %BF than women attending less often (p < 0.03).

Conclusion

Impact + resistance training may effectively combat bone loss and worsening body composition from premature menopause in BCS.

Keywords

Chemotherapy Neoplasm Obesity Osteoporosis Physical activity 

Notes

Acknowledgments

Funding was provided by an American Cancer Society Research Scholar Grant (RSGPB-06-092-01-CPPB). We thank the Oregon State Cancer Registry for their assistance with recruitment; Thera-band, Inc. for providing elastic exercise bands; and our research assistants, exercise trainers, and participants.

Conflicts of interest

None

References

  1. 1.
    Vance V, Mourtzakis M, McCargar L, Hanning R (2011) Weight gain in breast cancer survivors: prevalence, pattern and health consequences. Obesity Rev 12(4):282–294CrossRefGoogle Scholar
  2. 2.
    Santen RJ (2011) Effect of endocrine therapies on bone in breast cancer patients. J Clin Endocrinol Metab 96(2):308–319PubMedCrossRefGoogle Scholar
  3. 3.
    Cameron D, Douglas S, Brown J, Anderson R (2010) Bone mineral density loss during adjuvant chemotherapy in pre-menopausal women with early breast cancer: is it dependent on oestrogen deficiency? Breast Cancer Res Treat 23(3):805–814CrossRefGoogle Scholar
  4. 4.
    Vehmanen L, Saarto T, Elomaa I, Makela P, Valimaki M, Blomqvist C (2001) 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 37(18):2373–2378PubMedCrossRefGoogle Scholar
  5. 5.
    Demark-Wahnefried W, Peterson BL, Winer EP, Marks L, Aziz N, Marcom PK, Blackwell K, Rimer BK (2001) Changes in weight, body composition, and factors influencing energy balance among premenopausal breast cancer patients receiving adjuvant chemotherapy. J Clin Oncol 19(9):2381–2389PubMedGoogle Scholar
  6. 6.
    Bruning P, Pit M, Md J-B, Avd E, Hart A, Av E (1990) Bone mineral density after adjuvant chemotherapy for premenopausal breast cancer. Br J Cancer 61(2):308–310PubMedCrossRefGoogle Scholar
  7. 7.
    Goodwin PJ, Ennis M, Pritchard KI, McCready D, Koo J, Sidlofsky S, Trudeau M, Hood N, Redwood S (1999) Adjuvant treatment and onset of menopause predict weight gain after breast cancer diagnosis. J Clin Oncol 17(1):120–129PubMedGoogle Scholar
  8. 8.
    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 26(33):5465–5476PubMedCrossRefGoogle Scholar
  9. 9.
    Freedman RJ, Aziz N, Albanes D, Hartman T, Danforth D, Hill S, Sebring N, Reynolds JC, Yanovski JA (2004) Weight and body composition changes during and after adjuvant chemotherapy in women with breast cancer. J Clin Endocrinol Metab 89(5):2248–2253PubMedCrossRefGoogle Scholar
  10. 10.
    Shapiro CL, Manola J, Leboff M (2001) Ovarian failure after adjuvant chemotherapy is associated with rapid bone loss in women with early-stage breast cancer. J Clin Oncol 19(14):3306–3311PubMedGoogle Scholar
  11. 11.
    van Londen G, Perera S, Vujevich K, Rastogi P, Lembersky B, Brufsky A, Vogel V, Greenspan S (2011) The impact of an aromatase inhibitor on body composition and gonadal hormone levels in women with breast cancer. Breast Cancer Res Treat 125(2):441–446PubMedCrossRefGoogle Scholar
  12. 12.
    Hurley BF, Hanson ED, Sheaff AK (2011) Strength training as a countermeasure to aging muscle and chronic disease. Sports Med 41(4):289–306PubMedCrossRefGoogle Scholar
  13. 13.
    Kohrt WM, Bloomfield SA, Little KD, Nelson ME, Yingling VR (2004) American college of sports medicine position stand: physical activity and bone health. Med Sci Sports Exerc 36(11):1985–1996PubMedCrossRefGoogle Scholar
  14. 14.
    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(12):898–908PubMedCrossRefGoogle Scholar
  15. 15.
    Winters-Stone K, Dobek J, Nail L, Bennett JA, 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 27(2):447–456CrossRefGoogle Scholar
  16. 16.
    Winters KM, Snow CM (2000) Detraining reverses positive effects of exercise on the musculoskeletal system in premenopausal women. J Bone Miner Res 15:2495–2503PubMedCrossRefGoogle Scholar
  17. 17.
    Winters-Stone K, Snow C (2006) Site-specific response of bone to exercise in premenopausal women. Bone 39(6):1203–1209PubMedCrossRefGoogle Scholar
  18. 18.
    Garnero P (2008) Biomarkers for osteoporosis management: utility in diagnosis, fracture risk prediction and therapy monitoring. Molec Diagnos Ther 12(3):157–170CrossRefGoogle Scholar
  19. 19.
    Khosla S, Melton LJ 3rd, Atkinson EJ, O’Fallon WM, Klee GG, Riggs BL (1998) Relationship of serum sex steroid levels and bone turnover markers with bone mineral density in men and women: a key role for bioavailable estrogen. J Clin Endocrinol Metab 83(7):2266–2274PubMedCrossRefGoogle Scholar
  20. 20.
    Hadji P, Asmar L, van Nes J, Menschik T, Hasenburg A, Kuck J, Nortier J, van de Velde C, Jones S, Ziller M (2011) 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 137(6):1015–1025PubMedCrossRefGoogle Scholar
  21. 21.
    Snow CM, Shaw JM, Winters KM, Witzke KA (2000) Long-term exercise using weighted vests prevents hip bone loss in postmenopausal women. J Gerontol A Biol Sci Med Sci 55(9):M489–M491PubMedCrossRefGoogle Scholar
  22. 22.
    Schmitz KH, Courneya KS, Matthews C, Demark-Wahnefried W, Galvao DA, Pinto BM, Irwin ML, Wolin KY, Segal RJ, Lucia A, Schneider CM, Vong VE, Schwartz AL (2010) American college of sports medicine roundtable on exercise guidelines for cancer survivors. Med Sci Sports Exerc 42(7):1409–1426PubMedCrossRefGoogle Scholar
  23. 23.
    Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40(5):373–383PubMedCrossRefGoogle Scholar
  24. 24.
    Stewart A, Mills K, King A, Haskell W, Gillis D, Ritter P (2001) CHAMPS physical activity questionnaire for older adults: outcomes for interventions. Med Sci Sports Exerc 33(7):1126–1141PubMedGoogle Scholar
  25. 25.
    Binkley N, Bilezikian JP, Kendler DL, Leib ES, Lewiecki EM, Petak SM (2007) Summary of the International Society for Clinical Densitometry 2005 Position Development Conference. J Bone Miner Res 22(5):643–645PubMedCrossRefGoogle Scholar
  26. 26.
    Bicego D, Brown K, Ruddick M, Storey D, Wong C, Harris SR (2006) Exercise for women with or at risk for breast cancer–related lymphedema. Phys Ther 86(10):1398–1405PubMedCrossRefGoogle Scholar
  27. 27.
    Dalsky GP (1990) Effect of exercise on bone: permissive influence of estrogen and calcium. Med Sci Sports Exerc 22(3):281–285PubMedGoogle Scholar
  28. 28.
    Frost HM (1992) The role of changes in mechanical usage set points in the pathogenesis of osteoporosis. J Bone Miner Res 7(3):253–261PubMedCrossRefGoogle Scholar
  29. 29.
    Winters KM, Snow CM (2000) Body composition predicts bone mineral density and balance in premenopausal women. J Womens Health Gend Based Med 9(8):865–872PubMedCrossRefGoogle Scholar
  30. 30.
    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):1805–1813PubMedCrossRefGoogle Scholar
  31. 31.
    Kohrt WM (2001) Aging and the osteogenic response to mechanical loading. Int J Sport Nutr Exerc Metab 11(Suppl):S137–S142PubMedGoogle Scholar
  32. 32.
    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(8):683–704PubMedCrossRefGoogle Scholar
  33. 33.
    Martyn-St James M, Carroll S (2006) High-intensity resistance training and postmenopausal bone loss: a meta-analysis. Osteoporos Int 17(8):1225–1240PubMedCrossRefGoogle Scholar
  34. 34.
    Saarto T, Sievänen H, Kellokumpu-Lehtinen P, Nikander R, Vehmanen L, Huovinen R, Kautiainen H, Järvenpää S, Penttinen H, Utriainen M, Jääskeläinen A, 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 23:1601–1612PubMedCrossRefGoogle Scholar
  35. 35.
    Lanyon LE (1996) Using functional loading to influence bone mass and architecture: objectives, mechanisms, and relationship with estrogen of the mechanically adaptive process in bone. Bone 18(1 Suppl):37S–43SPubMedCrossRefGoogle Scholar
  36. 36.
    Hadji P, Ziller M, Maskow C, Albert U, Kalder M (2009) The influence of chemotherapy on bone mineral density, quantitative ultrasonometry and bone turnover in pre-menopausal women with breast cancer. Eur J Cancer 45(18):3205–3212PubMedCrossRefGoogle Scholar
  37. 37.
    Schwartz AL, Winters-Stone K (2009) Effects of a 12-month randomized controlled trial of aerobic or resistance exercise during and following cancer treatment in women. Phys Sportsmed 37(3):62–67PubMedCrossRefGoogle Scholar
  38. 38.
    Schmitz KH, Ahmed RL, Hannan PJ, Yee D (2005) Safety and efficacy of weight training in recent breast cancer survivors to alter body composition, insulin, and insulin-like growth factor axis proteins. Cancer Epidemiol Biomarkers Prev 14(7):1672–1680PubMedCrossRefGoogle Scholar
  39. 39.
    Schmitz KH, Ahmed RL, Troxel AB, Cheville A, Lewis-Grant L, Smith R, Bryan CJ, Williams-Smith CT, Chittams J (2010) Weight lifting for women at risk for breast cancer-related lymphedema. JAMA 304(24):2699–2705PubMedCrossRefGoogle Scholar
  40. 40.
    Slentz CA, Houmard JA, Kraus WE (2009) Exercise, abdominal obesity, skeletal muscle, and metabolic risk: evidence for a dose response. Obesity 17(3):S27–S33PubMedCrossRefGoogle Scholar
  41. 41.
    Winters-Stone KM, Nail L, Bennett JA, Schwartz A (2009) Bone health and falls: fracture risk in breast cancer survivors with chemotherapy-induced amenorrhea. Oncol Nurs Forum 36(3):315–325PubMedCrossRefGoogle Scholar
  42. 42.
    Gordon AM, Hurwitz S, Shapiro CL, Leboff MS (2011) Premature ovarian failure and body composition changes with adjuvant chemotherapy for breast cancer. Menopause 18(11):1244–1248PubMedCrossRefGoogle Scholar
  43. 43.
    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):1361–1369PubMedCrossRefGoogle Scholar
  44. 44.
    Schmitz KH, Ahmed RL, Troxel A, Cheville A, Smith R, Lewis-Grant L, Bryan CJ, Williams-Smith CT, Greene QP (2009) Weight lifting in women with breast-cancer-related lymphedema. New Engl J Med 361(7):664–673PubMedCrossRefGoogle Scholar
  45. 45.
    Ganz PA, Land SR, Geyer CE, Cecchini RS, Costantino JP, Pajon ER, Fehrenbacher L, Atkins JN, Polikoff JA, Vogel VG, Erban JK, Livingston RB, Perez EA, Mamounas EP, Wolmark N, Swain SM (2011) Menstrual history and quality-of-life outcomes in women with node-positive breast cancer treated with adjuvant therapy on the NSABP B-30 trial. J Clin Oncol 29(9):1110–1116PubMedCrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2012

Authors and Affiliations

  • K. M. Winters-Stone
    • 1
    • 3
    • 7
  • J. Dobek
    • 1
    • 2
  • L. M. Nail
    • 1
    • 3
  • J. A. Bennett
    • 1
    • 3
  • M. C. Leo
    • 5
  • B. Torgrimson-Ojerio
    • 1
  • S.-W. Luoh
    • 4
  • A. Schwartz
    • 6
  1. 1.School of NursingOregon Health & Science UniversityPortlandUSA
  2. 2.School of MedicineOregon Health & Science UniversityPortlandUSA
  3. 3.Knight Cancer CenterOregon Health & Science UniversityPortlandUSA
  4. 4.Portland VA Medical CenterPortlandUSA
  5. 5.Kaiser Permanente Center for Health ResearchPortlandUSA
  6. 6.Idaho State UniversityPocatelloUSA
  7. 7.Oregon Health & Science UniversityPortlandUSA

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