Journal of Cancer Survivorship

, Volume 8, Issue 2, pp 260–268 | Cite as

Influence of weight training on skeletal health of breast cancer survivors with or at risk for breast cancer-related lymphedema

  • Kerri M. Winters-StoneEmail author
  • Monica Laudermilk
  • Kaitlin Woo
  • Justin C. Brown
  • Kathryn H. Schmitz



This study aimed to determine whether the Physical Activity and Lymphedema (PAL) trial weight training program for breast cancer survivors at risk of or with breast cancer-related lymphedema provided skeletal benefits.


Of the 295 participants in the randomized controlled PAL trial, 258 (weight training; N = 128; control, N = 130) had complete measures of bone mineral density (BMD (in grams per square centimeter)) of the proximal femur and lumbar spine and were also categorized by T scores. Women in the weight training group performed slowly progressive weight training 2 days/week for 12 months compared to women in the control group who maintained their usual physical activities.


There were no significant differences in the rate of BMD change at any skeletal site between weight training and control groups, regardless of menopausal status. Distribution of bone health categories was not significantly different between groups at baseline, but became different at 12 months (p < 0.03) among postmenopausal women due to an increase in the percentage of controls who became osteopenic (35 to 44 %) compared to stable bone health in weight lifters.


The PAL weight training program that increased muscle strength without exacerbating or causing lymphedema among breast cancer survivors was not as efficacious at improving skeletal health. The skeletal loads produced from the PAL program may be insufficient to notably shift BMD, but may have a subtle osteogenic effect.

Implications for cancer survivors

The safety and efficacy of rigorous weight training programs for improving skeletal health in women at risk for or with breast cancer-related lymphedema remain to be determined.


Resistance exercise Osteoporosis Fractures Neoplasms Survivorship 



The work was supported by grants from the National Cancer Institute (R01-CA106851, to Dr. Schmitz) and the National Center for Research Resources (UL1RR024134, to the University of Pennsylvania). BSN Medical provided custom-fitted compression garments, and the fitness centers where the weight training sessions took place (YMCA of Philadelphia and Vicinity, Sisters in Shape, and the Family YMCA of Burlington County, NJ) provided discounted membership fees for study participants.

Conflict of interest

The authors have no disclosures to report.


  1. 1.
    Chen Z, Maricic M, Aragaki AK, Mouton C, Arendell L, Lopez AM, et al. Fracture risk increases after diagnosis of breast or other cancers in postmenopausal women: results from the Women’s Health Initiative. Osteoporos Int. 2009;20(4):527–36.PubMedCentralCrossRefPubMedGoogle Scholar
  2. 2.
    Sweeney C, Schmitz KH, Lazovich D, Virnig BA, Wallace RB, Folsom AR. Functional limitations in elderly female cancer survivors. J Natl Cancer Inst. 2006;98(8):521–9.CrossRefPubMedGoogle Scholar
  3. 3.
    Vance V, Mourtzakis M, McCargar L, Hanning R. Weight gain in breast cancer survivors: prevalence, pattern and health consequences. Obes Rev. 2011;12(4):282–94.CrossRefPubMedGoogle Scholar
  4. 4.
    Santen RJ. Effect of endocrine therapies on bone in breast cancer patients. J Clin Endocrinol Metab. 2011;96(2):308–19.CrossRefPubMedGoogle Scholar
  5. 5.
    Cameron D, Douglas S, Brown J, Anderson R. 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. 2010;23(3):805–14.CrossRefGoogle Scholar
  6. 6.
    Armstrong MEG, Spencer EA, Cairns BJ, Banks E, Pirie K, Green J, et al. Body mass index and physical activity in relation to the incidence of hip fracture in postmenopausal women. J Bone Miner Res. 2011;26(6):1330–8.CrossRefPubMedGoogle Scholar
  7. 7.
    Irwin ML, Crumley D, McTiernan A, Bernstein L, Baumgartner R, Gilliland FD, et al. Physical activity levels before and after a diagnosis of breast carcinoma: the Health, Eating, Activity, and Lifestyle (HEAL) study. Cancer. 2003;97(7):1746–57.PubMedCentralCrossRefPubMedGoogle Scholar
  8. 8.
    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(33):5465–76.CrossRefPubMedGoogle Scholar
  9. 9.
    Kelley G, Kelley K, Kohrt W. 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. 2012;13(1):177.PubMedCentralCrossRefPubMedGoogle Scholar
  10. 10.
    Demark-Wahnefried W, Peterson BL, Winer EP, Marks L, Aziz N, Marcom PK, et al. Changes in weight, body composition, and factors influencing energy balance among premenopausal breast cancer patients receiving adjuvant chemotherapy. J Clin Oncol. 2001;19(9):2381–9.PubMedGoogle Scholar
  11. 11.
    Freedman RJ, Aziz N, Albanes D, Hartman T, Danforth D, Hill S, et al. Weight and body composition changes during and after adjuvant chemotherapy in women with breast cancer. J Clin Endocrinol Metab. 2004;89(5):2248–53.CrossRefPubMedGoogle Scholar
  12. 12.
    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(18):2373–8.CrossRefPubMedGoogle Scholar
  13. 13.
    Saarto T, Blomqvist C, Valimaki M, Makela P, Sarna S, Elomaa I. Clodronate improves bone mineral density in post-menopausal breast cancer patients treated with adjuvant antioestrogens. Br J Cancer. 1997;75(4):602–5.PubMedCentralCrossRefPubMedGoogle Scholar
  14. 14.
    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(14):3306–11.PubMedGoogle Scholar
  15. 15.
    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(5):1601–12.CrossRefPubMedGoogle Scholar
  16. 16.
    Winters-Stone K, Dobek J, Nail L, Bennett JA, Naik A, Schwartz A. Strength training stops bone loss and builds muscle in postmenopausal breast cancer survivors: a randomized controlled trial. Breast Cancer Res Treat. 2011;27(2):447–56.CrossRefGoogle Scholar
  17. 17.
    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(5):1637–46.CrossRefPubMedGoogle Scholar
  18. 18.
    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(3):187–201.CrossRefPubMedGoogle Scholar
  19. 19.
    Saarto T, Penttinen HM, Sievanen H, Kellokumpu-Lehtinen PL, Hakamies-Blomqvist L, Nikander R, et al. Effectiveness of a 12-month exercise program on physical performance and quality of life of breast cancer survivors. Anticancer Res. 2012;32(9):3875–84.PubMedGoogle Scholar
  20. 20.
    Winters-Stone KM, Dobek J, Bennett JA, Nail LM, Leo MC, Schwartz A. The effect of resistance training on muscle strength and physical function in older, postmenopausal breast cancer survivors: a randomized controlled trial. J Cancer Surviv. 2012;6(2):189–99.PubMedCentralCrossRefPubMedGoogle Scholar
  21. 21.
    Schmitz KH, Ahmed RL, Troxel AB, Cheville A, Lewis-Grant L, Smith R, et al. Weight lifting for women at risk for breast cancer-related lymphedema. JAMA. 2010;304(24):2699–705.CrossRefPubMedGoogle Scholar
  22. 22.
    Schmitz KH, Ahmed RL, Troxel A, Cheville A, Smith R, Lewis-Grant L, et al. Weight lifting in women with breast-cancer-related lymphedema. New Engl J Med. 2009;361(7):664–73.CrossRefPubMedGoogle Scholar
  23. 23.
    Speck RM, Gross CR, Hormes JM, Ahmed RL, Lytle LA, Hwang WT, et al. Changes in the body image and relationship scale following a one-year strength training trial for breast cancer survivors with or at risk for lymphedema. Breast Cancer Res Treat. 2010;121(2):421–30.CrossRefPubMedGoogle Scholar
  24. 24.
    Schmitz KH, Troxel AB, Cheville A, Grant LL, Bryan CJ, Gross CR, et al. Physical Activity and Lymphedema (the PAL trial): assessing the safety of progressive strength training in breast cancer survivors. Contemp Clin Trials. 2009;30(3):233–45.PubMedCentralCrossRefPubMedGoogle Scholar
  25. 25.
    Baim S, Binkley N, Bilezikian JP, Kendler DL, Hans DB, Lewiecki EM, et al. Official positions of the International Society for Clinical Densitometry and executive summary of the 2007 ISCD Position Development Conference. J Clin Densitom. 2008;11(1):75–91.CrossRefPubMedGoogle Scholar
  26. 26.
    Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, Ainsworth BE, et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003;35(8):1381–95.CrossRefPubMedGoogle Scholar
  27. 27.
    Subar AF, Thompson FE, Kipnis V, Midthune D, Hurwitz P, McNutt S, et al. Comparative validation of the Block, Willett, and National Cancer Institute food frequency questionnaires: the Eating at America’s Table Study. Am J Epidemiol. 2001;154(12):1089–99.CrossRefPubMedGoogle Scholar
  28. 28.
    National Lymphedema Network Medical Advisory Committee. (2011) Position statement of the National Lymphedema Network. Available at, Accessed 12 Oct 2012.
  29. 29.
    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(3):627–33.CrossRefPubMedGoogle Scholar
  30. 30.
    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(8):1361–9.CrossRefPubMedGoogle Scholar
  31. 31.
    Kelley G. Aerobic exercise and lumbar spine bone mineral density in postmenopausal women: a meta-analysis. J Am Geriatr Soc. 1998;46(2):143–52.CrossRefPubMedGoogle Scholar
  32. 32.
    Kelley GA. Aerobic exercise and bone density at the hip in postmenopausal women: a meta-analysis. Prev Med. 1998;27(6):798–807.CrossRefPubMedGoogle Scholar
  33. 33.
    Kelley GA, Kelley KS. Efficacy of resistance exercise on lumbar spine and femoral neck bone mineral density in premenopausal women: a meta-analysis of individual patient data. J Women’s Health. 2004;13(3):293–300.CrossRefGoogle Scholar
  34. 34.
    Kelley GA, Kelley KS. Exercise and bone mineral density at the femoral neck in postmenopausal women: a meta-analysis of controlled clinical trials with individual patient data. Am J Obstet Gynecol. 2006;194(3):760–7.CrossRefPubMedGoogle Scholar
  35. 35.
    Kelley GA, Kelley KS, Tran ZV. Exercise and bone mineral density in men: a meta-analysis. J Appl Physiol. 2000;88(5):1730–6.PubMedGoogle Scholar
  36. 36.
    Kelley GADA, Kelley KSM, Tran ZVP. Resistance training and bone mineral density in women: a meta-analysis of controlled trials. Am J Phys Med Rehabil. 2001;80(1):65–77.CrossRefPubMedGoogle Scholar
  37. 37.
    Martyn-St James M, Carroll S. High-intensity resistance training and postmenopausal bone loss: a meta-analysis. Osteoporos Int. 2006;17(8):1225–40.CrossRefPubMedGoogle Scholar
  38. 38.
    Martyn-St James M, Carroll S. Meta-analysis of walking for preservation of bone mineral density in postmenopausal women. Bone. 2008;43(3):521–31.CrossRefPubMedGoogle Scholar
  39. 39.
    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(12):898–908.CrossRefPubMedGoogle Scholar
  40. 40.
    Wolff I, van Croonenborg J, Kemper H, Kostense P, Twisk J. The effect of exercise training programs on bone mass: a meta-analysis of published controlled trials in pre- and postmenopausal women. Osteoporos Int. 1999;9(1):1–12.CrossRefPubMedGoogle Scholar
  41. 41.
    Berard A, Bravo G, Gauthier P. Meta-analysis of the effectiveness of physical activity for the prevention of bone loss in postmenopausal women. Osteoporos Int. 1997;7(4):331–7.CrossRefPubMedGoogle Scholar
  42. 42.
    Kohrt WM, Bloomfield SA, Little KD, Nelson ME, Yingling VR. American College of Sports Medicine Position Stand: physical activity and bone health. Med Sci Sports Exerc. 2004;36(11):1985–96.CrossRefPubMedGoogle Scholar
  43. 43.
    No authors listed. Management of osteoporosis in postmenopausal women: 2010 position statement of The North American Menopause Society. Menopause. 2010;17(1):25–54.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Kerri M. Winters-Stone
    • 1
    Email author
  • Monica Laudermilk
    • 2
  • Kaitlin Woo
    • 3
  • Justin C. Brown
    • 3
  • Kathryn H. Schmitz
    • 3
  1. 1.School of NursingOregon Health & Sciences UniversityPortlandUSA
  2. 2.Core PerformancePhoenixUSA
  3. 3.Department of Biostatistics and Epidemiology, Perelman School of MedicineUniversity of PennsylvaniaPhiladelphiaUSA

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