Advertisement

Breast Cancer Research and Treatment

, Volume 148, Issue 2, pp 249–268 | Cite as

Safety and efficacy of progressive resistance training in breast cancer: a systematic review and meta-analysis

  • Birinder S. CheemaEmail author
  • Sharon L. Kilbreath
  • Paul P. Fahey
  • Geoffrey P. Delaney
  • Evan Atlantis
Review

Abstract

The purpose of this study was to assess the safety and efficacy of progressive resistance training (PRT) in breast cancer. Randomized controlled trials (RCTs) published to November 2013 that reported on the effects of PRT (>6 weeks) on breast cancer-related lymphedema (BCRL) (incidence/exacerbation, arm volume, and symptom severity), physical functioning (upper and lower body muscular strength), and health-related quality of life (HRQoL) in breast cancer patients were included. Of 446 citations retrieved, 15 RCTs in 1,652 patients were included and yielded five studies on BCRL incidence/exacerbation (N = 647), four studies on arm volume (N = 384) and BCRL symptom severity (N = 479), 11 studies on upper body muscular strength (N = 1,252), nine studies on lower body muscular strength (N = 1,079), and seven studies on HRQoL (N = 823). PRT reduced the risk of BCRL versus control conditions [OR = 0.53 (95 % CI 0.31–0.90); I 2 = 0 %] and did not worsen arm volume or symptom severity (both SMD = −0.07). PRT significantly improved upper [SMD = 0.57 (95 % CI 0.37–0.76); I 2 = 58.4 %] and lower body muscular strength [SMD = 0.48 (95 % CI 0.30–0.67); I 2 = 46.7 %] but not HRQoL [SMD = 0.17 (95 % CI −0.03 to 0.38); I 2  = 47.0 %]. The effect of PRT on HRQoL became significant in our sensitivity analysis when two studies conducted during adjuvant chemotherapy [SMD = 0.30 (95 % CI 0.04–0.55), I 2 = 37.0 %] were excluded. These data indicate that PRT improves physical functioning and reduces the risk of BCRL. Clinical practice guidelines should be updated to inform clinicians on the benefits of PRT in this cohort.

Keywords

Strength Physical functioning Quality of life Rehabilitation Exercise Health Lymphedema Survival Fitness 

Notes

Acknowledgments

We sincerely thank Ms Katrina Chaudhary for her work in developing the database searches.

Funding

All authors have completed the ICMJE uniform disclosure form at http://www.icmje.org/coi_disclosure.pdf and declare: no support from any organization for the submitted work.

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

10549_2014_3162_MOESM1_ESM.docx (68 kb)
Supplementary material 1 (DOCX 68 kb)

References

  1. 1.
    Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90PubMedCrossRefGoogle Scholar
  2. 2.
    GLOBOCAN: estimated cancer incidence, mortality and prevalence worldwide in 2012. http://globocan.iarc.fr/Pages/fact_sheets_cancer.aspx
  3. 3.
    Coleman MP, Forman D, Bryant H, Butler J, Rachet B, Maringe C, Nur U, Tracey E, Coory M, Hatcher J et al (2011) Cancer survival in Australia, Canada, Denmark, Norway, Sweden, and the UK, 1995–2007 (the International Cancer Benchmarking Partnership): an analysis of population-based cancer registry data. Lancet 377(9760):127–138PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Bray F, Ren J-S, Masuyer E, Ferlay J (2013) Global estimates of cancer prevalence for 27 sites in the adult population in 2008. Int J Cancer 132(5):1133–1145PubMedCrossRefGoogle Scholar
  5. 5.
    Howell A, Cuzick J, Baum M, Buzdar A, Dowsett M, Forbes JF, Hoctin-Boes G, Houghton J, Locker GY, Tobias JS (2005) Results of the ATAC (Arimidex, Tamoxifen, Alone or in Combination) trial after completion of 5 years’ adjuvant treatment for breast cancer. Lancet 365(9453):60–62PubMedCrossRefGoogle Scholar
  6. 6.
    Early Breast Cancer Trialists’ Collaborative Group (EBCTCG) (2005) Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 365(9472):1687–1717Google Scholar
  7. 7.
    Hwang ES, Lichtensztajn DY, Gomez SL, Fowble B, Clarke CA (2013) Survival after lumpectomy and mastectomy for early stage invasive breast cancer: the effect of age and hormone receptor status. Cancer 119(7):1402–1411PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Dominick SA, Madlensky L, Natarajan L, Pierce JP (2013) Risk factors associated with breast cancer-related lymphedema in the WHEL Study. J Cancer Surv 7(1):115–123CrossRefGoogle Scholar
  9. 9.
    Harrington S, Padua D, Battaglini C, Michener LA (2013) Upper extremity strength and range of motion and their relationship to function in breast cancer survivors. Physiother Theory Pract 29(7):513–520PubMedCrossRefGoogle Scholar
  10. 10.
    Reinertsen KV, Cvancarova M, Loge JH, Edvardsen H, Wist E, Fossa SD (2010) Predictors and course of chronic fatigue in long-term breast cancer survivors. J Cancer Surv 4(4):405–414CrossRefGoogle Scholar
  11. 11.
    Vance V, Mourtzakis M, McCargar L, Hanning R (2011) Weight gain in breast cancer survivors: prevalence, pattern and health consequences. Obes Rev 12(4):282–294PubMedCrossRefGoogle Scholar
  12. 12.
    Villasenor A, Ballard-Barbash R, Baumgartner K, Baumgartner R, Bernstein L, McTiernan A, Neuhouser ML (2012) Prevalence and prognostic effect of sarcopenia in breast cancer survivors: the HEAL Study. J Cancer Surv 6(4):398–406CrossRefGoogle Scholar
  13. 13.
    Chen Z, Maricic M, Bassford TL et al (2005) Fracture risk among breast cancer survivors: results from the women’s health initiative observational study. Arch Intern Med 165(5):552–558PubMedCrossRefGoogle Scholar
  14. 14.
    Pierce BL, Ballard-Barbash R, Bernstein L, Baumgartner RN, Neuhouser ML, Wener MH, Baumgartner KB, Gilliland FD, Sorensen BE, McTiernan A et al (2009) Elevated biomarkers of inflammation are associated with reduced survival among breast cancer patients. J Clin Oncol 27(21):3437–3444PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Ray-Coquard I, Cropet C, Van Glabbeke M, Sebban C, Le Cesne A, Judson I, Tredan O, Verweij J, Biron P, Labidi I et al (2009) Lymphopenia as a prognostic factor for overall survival in advanced carcinomas, sarcomas, and lymphomas. Cancer Res 69(13):5383–5391PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Speck RM, DeMichele A, Farrar JT, Hennessy S, Mao JJ, Stineman MG, Barg FK (2012) Scope of symptoms and self-management strategies for chemotherapy-induced peripheral neuropathy in breast cancer patients. Support Care Cancer 20(10):2433–2439PubMedCrossRefGoogle Scholar
  17. 17.
    Galiano-Castillo N, Ariza-Garcia A, Cantarero-Villanueva I, Fernandez-Lao C, Diaz-Rodriguez L, Arroyo-Morales M (2013) Depressed mood in breast cancer survivors: associations with physical activity, cancer-related fatigue, quality of life, and fitness level. Eur J Oncol Nurs 18(2):206–210PubMedCrossRefGoogle Scholar
  18. 18.
    Kwan ML, Sternfeld B, Ergas IJ, Timperi AW, Roh JM, Hong CC, Quesenberry CP, Kushi LH (2012) Change in physical activity during active treatment in a prospective study of breast cancer survivors. Breast Cancer Res Treat 131(2):679–690PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Smoot B, Johnson M, Duda JJ, Krasnoff J, Dodd M (2012) Cardiorespiratory fitness in women with and without lymphedema following breast cancer treatment. Cancer Clin Oncol 1(1):21–31PubMedCentralPubMedGoogle Scholar
  20. 20.
    Pinto M, Gimigliano F, Tatangelo F, Megna M, Izzo F, Gimigliano R, Iolascon G (2013) Upper limb function and quality of life in breast cancer related lymphedema: a cross-sectional study. Eur J Phys Rehabil Med 49(5):665–673PubMedGoogle Scholar
  21. 21.
    Howard-Anderson J, Ganz PA, Bower JE, Stanton AL (2012) Quality of life, fertility concerns, and behavioral health outcomes in younger breast cancer survivors: a systematic review. J Natl Cancer Inst 104(5):386–405PubMedCrossRefGoogle Scholar
  22. 22.
    Sehl M, Lu X, Silliman R, Ganz PA (2013) Decline in physical functioning in first 2 years after breast cancer diagnosis predicts 10-year survival in older women. J Cancer Surv 7(1):20–31CrossRefGoogle Scholar
  23. 23.
    Epplein M, Zheng Y, Zheng W, Chen Z, Gu K, Penson D, Lu W, Shu XO (2011) Quality of life after breast cancer diagnosis and survival. J Clin Oncol 29(4):406–412PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Cheema B, Gaul C, Lane K, Fiatarone Singh MA (2008) Progressive resistance training in breast cancer: a systematic review of clinical trials. Breast Cancer Res Treat 109:9–26PubMedCrossRefGoogle Scholar
  25. 25.
    Demark-Wahnefried W (2009) A weighty matter—lifting after breast cancer. N Engl J Med 361(7):710–711PubMedCrossRefGoogle Scholar
  26. 26.
    Ahmed R, Thomas W, Yee D, Schmitz K (2006) Randomized controlled trial of weight training and lymphedema in breast cancer survivors. J Clin Oncol 24(18):2765–2772PubMedCrossRefGoogle Scholar
  27. 27.
    Ohira T, Schmitz K, Ahmed R, Yee D (2006) Effects of weight training on quality of life in recent breast cancer survivors. Cancer 106:2076–2083PubMedCrossRefGoogle Scholar
  28. 28.
    Courneya K, Segal R, Mackey J, Gelmon K, Reid R, Friedenreich C, Ladha A, Proulx C, Vallance J, Lane K et al (2007) Effects of aerobic and resistance exercise in breast cancer patients receiving adjuvant chemotherapy: a multicenter randomized controlled trial. J Clin Oncol 25(28):4396–4404PubMedCrossRefGoogle Scholar
  29. 29.
    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):627–633PubMedCrossRefGoogle Scholar
  30. 30.
    Twiss JJ, Waltman NL, Berg K, Ott CD, Gross GJ, Lindsey AM (2009) An exercise intervention for breast cancer survivors with bone loss. J Nurs Scholarsh 41(1):20–27PubMedCrossRefGoogle Scholar
  31. 31.
    Schmitz K, Ahmed R, Troxel A, Cheville A, Smith R, Lewis-Grant L, Bryan C, Williams-Smith C, Greene Q (2009) Weight lifting in women with breast-cancer-related lymphedema. N Engl J Med 361:664–673PubMedCrossRefGoogle Scholar
  32. 32.
    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: a randomized trial. JAMA 304(24):2699–2705PubMedCrossRefGoogle Scholar
  33. 33.
    Speck RM, Gross CR, Hormes JM, Ahmed RL, Lytle LA, Hwang WT, Schmitz KH (2010) 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 121(2):421–430PubMedCrossRefGoogle Scholar
  34. 34.
    Kim do S, Sim YJ, Jeong HJ, Kim GC (2010) Effect of active resistive exercise on breast cancer-related lymphedema: a randomized controlled trial. Arch Phys Med Rehabil 91(12):1844–1848PubMedCrossRefGoogle Scholar
  35. 35.
    Winters-Stone KM, Dobek J, Bennett JA, Nail LM, Leo MC, Schwartz A (2012) The effect of resistance training on muscle strength and physical function in older, postmenopausal breast cancer survivors: a randomized controlled trial. J Cancer Surv 6(2):189–199CrossRefGoogle Scholar
  36. 36.
    Musanti R (2012) A study of exercise modality and physical self-esteem in breast cancer survivors. Med Sci Sports Exerc 44(2):352–361PubMedCrossRefGoogle Scholar
  37. 37.
    Kilbreath SL, Refshauge KM, Beith JM, Ward LC, Lee M, Simpson JM, Hansen R (2012) Upper limb progressive resistance training and stretching exercises following surgery for early breast cancer: a randomized controlled trial. Breast Cancer Res Treat 133(2):667–676PubMedCrossRefGoogle Scholar
  38. 38.
    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):1637–1646PubMedCrossRefGoogle Scholar
  39. 39.
    Cormie P, Pumpa K, Galvao DA, Turner E, Spry N, Saunders C, Zissiadis Y, Newton RU (2013) Is it safe and efficacious for women with lymphedema secondary to breast cancer to lift heavy weights during exercise: a randomised controlled trial. J Cancer Surv 7(3):413–424CrossRefGoogle Scholar
  40. 40.
    Courneya KS, McKenzie DC, Mackey JR, Gelmon K, Friedenreich CM, Yasui Y, Reid RD, Cook D, Jespersen D, Proulx C et al (2013) Effects of exercise dose and type during breast cancer chemotherapy: multicenter randomized trial. J Natl Cancer Inst 105(23):1821–1832PubMedCrossRefGoogle Scholar
  41. 41.
    Aebi S, Davidson T, Gruber G, Cardoso F (2011) Primary breast cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 22(Suppl 6):vi12–vi24Google Scholar
  42. 42.
    Yarnold J (2009) Early and locally advanced breast cancer: diagnosis and treatment National Institute for Health and Clinical Excellence guideline 2009. Clin Oncol 21(3):159–160CrossRefGoogle Scholar
  43. 43.
    Carlson RW, Allred DC, Anderson BO, Burstein HJ, Carter WB, Edge SB, Erban JK, Farrar WB, Goldstein LJ, Gradishar WJ (2009) Breast cancer. J Natl Compr Canc Netw 7(2):122–192PubMedGoogle Scholar
  44. 44.
    Foldi E, Foldi M, Clodius L (1989) The lymphedema chaos: a lancet. Ann Plast Surg 22:505–515PubMedCrossRefGoogle Scholar
  45. 45.
    Sprangers MA, Groenvold M, Arraras JI, Franklin J, te Velde A, Muller M, Franzini L, Williams A, de Haes HC, Hopwood P et al (1996) The European Organization for Research and Treatment of Cancer breast cancer-specific quality-of-life questionnaire module: first results from a three-country field study. J Clin Oncol 14(10):2756–2768PubMedGoogle Scholar
  46. 46.
    Schulz KF, Altman DG, Moher D (2010) CONSORT 2010 statement: updated guidelines for reporting parallel group randomised trials. Trials 11:32PubMedCentralPubMedCrossRefGoogle Scholar
  47. 47.
    DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188PubMedCrossRefGoogle Scholar
  48. 48.
    Higgins J, Green S (2011) Cochrane handbook for systematic reviews of interventions, version 5.1.0Google Scholar
  49. 49.
    Haldane JB (1956) The estimation and significance of the logarithm of a ratio of frequencies. Ann Hum Genet 20(4):309–311PubMedCrossRefGoogle Scholar
  50. 50.
    Sweeting MJ, Sutton AJ, Lambert PC (2004) What to add to nothing? Use and avoidance of continuity corrections in meta-analysis of sparse data. Stat Med 23(9):1351–1375PubMedCrossRefGoogle Scholar
  51. 51.
    Higgins J, Thompson S, Deeks J, Altman D (2003) Measuring inconsistency in meta-analysis. Br Med J 327(7414):557–560CrossRefGoogle Scholar
  52. 52.
    Higgins J, Thompson S (2002) Quantifying heterogeneity in meta-analysis. Stat Med 21(11):1539–1558PubMedCrossRefGoogle Scholar
  53. 53.
    Eggers M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. Br Med J 315(7109):629–634CrossRefGoogle Scholar
  54. 54.
    Norman SA, Miller LT, Erikson HB, Norman MF, McCorkle R (2001) Development and validation of a telephone questionnaire to characterize lymphedema in women treated for breast cancer. Phys Ther 81(6):1192–1205PubMedGoogle Scholar
  55. 55.
    Schmitz K, Ahmed R, Hannan P, 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 Biomark Prev 14(7):1672–1680CrossRefGoogle Scholar
  56. 56.
    Brown JC, Troxel AB, Schmitz KH (2012) Safety of weightlifting among women with or at risk for breast cancer-related lymphedema: musculoskeletal injuries and health care use in a weightlifting rehabilitation trial. Oncologist 17(8):1120–1128PubMedCentralPubMedCrossRefGoogle Scholar
  57. 57.
    Hayes SC, Janda M, Cornish B, Battistutta D, Newman B (2008) Lymphedema after breast cancer: incidence, risk factors, and effect on upper body function. J Clin Oncol 26(21):3536–3542PubMedCrossRefGoogle Scholar
  58. 58.
    Hayes SC, Johansson K, Stout NL, Prosnitz R, Armer JM, Gabram S, Schmitz KH (2012) Upper-body morbidity after breast cancer. Cancer 118(S8):2237–2249PubMedCrossRefGoogle Scholar
  59. 59.
    Beaulac S, McNair L, Scott T, LaMorte W, Kavanah M (2002) Lymphedema and quality of life in survivors of early-stage breast cancer. Arch Surg 137(11):1253–1257PubMedCrossRefGoogle Scholar
  60. 60.
    Ahmed RL, Schmitz KH, Prizment AE, Folsom AR (2011) Risk factors for lymphedema in breast cancer survivors, the Iowa Women’s Health Study. Breast Cancer Res Treat 130(3):981–991PubMedCentralPubMedCrossRefGoogle Scholar
  61. 61.
    Sagen A, Kaaresen R, Sandvik L, Thune I, Risberg MA (2014) Upper limb physical function and adverse effects after breast cancer surgery: a prospective 2.5-year follow-up study and preoperative measures. Arch Phys Med Rehabil 95(5):875–881PubMedCrossRefGoogle Scholar
  62. 62.
    Simonavice E, Liu P-Y, Ilich JZ, Kim J-S, Panton LB (2011) Body composition, muscular strength, and physical function in breast cancer survivors. Int J Body Compos Res 9(2):57–64Google Scholar
  63. 63.
    Goodpaster B, Park S, Harris T, Kritchevsky S, Nevitt M, Schwartz A, Simonsick E, Tylavsky F, Visser M, Newman A (2006) The loss of skeletal muscle strength, mass, and quality in older adults: the Health, Aging and Body Composition Study. J Gerontol 61A(10):1059–1064CrossRefGoogle Scholar
  64. 64.
    Newman AB, Kupelian V, Visser M, Simonsick EM, Goodpaster BH, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB (2006) Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort. J Gerontol Ser A 61(1):72–77CrossRefGoogle Scholar
  65. 65.
    Takata Y, Shimada M, Ansai T, Yoshitake Y, Nishimuta M, Nakagawa N, Ohashi M, Yoshihara A, Miyazaki H (2012) Physical performance and 10-year mortality in a 70-year-old community-dwelling population. Aging Clin Exp Res 24(3):257–264PubMedGoogle Scholar
  66. 66.
    Lee ES, Lee MK, Kim SH, Ro JS, Kang HS, Kim SW, Lee KS, Yun YH (2011) Health-related quality of life in survivors with breast cancer 1 year after diagnosis compared with the general population: a prospective cohort study. Ann Surg 253(1):101–108PubMedCrossRefGoogle Scholar
  67. 67.
    Klein D, Mercier M, Abeilard E, Puyraveau M, Danzon A, Dalstein V, Pozet A, Guizard A-V, Henry-Amar M, Velten M (2011) Long-term quality of life after breast cancer: a French registry-based controlled study. Breast Cancer Res Treat 129(1):125–134PubMedCrossRefGoogle Scholar
  68. 68.
    Alfano CM, Smith AW, Irwin ML, Bowen DJ, Sorensen B, Reeve BB, Meeske KA, Bernstein L, Baumgartner KB, Ballard-Barbash R et al (2007) Physical activity, long-term symptoms, and physical health-related quality of life among breast cancer survivors: a prospective analysis. J Cancer Surv 1(2):116–128CrossRefGoogle Scholar
  69. 69.
    Blanchard CM, Courneya KS, Stein K (2008) Cancer survivors’ adherence to lifestyle behavior recommendations and associations with health-related quality of life: results from the American Cancer Society’s SCS-II. J Clin Oncol 26(13):2198–2204PubMedCrossRefGoogle Scholar
  70. 70.
    Merchant CR, Chapman T, Kilbreath SL, Refshauge KM, Krupa K (2008) Decreased muscle strength following management of breast cancer. Disabil Rehabil 30(15):1098–1105PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Birinder S. Cheema
    • 1
    • 2
    Email author
  • Sharon L. Kilbreath
    • 3
  • Paul P. Fahey
    • 1
  • Geoffrey P. Delaney
    • 4
    • 5
    • 6
  • Evan Atlantis
    • 7
    • 8
  1. 1.School of Science and HealthUniversity of Western SydneyPenrithAustralia
  2. 2.The National Institute of Complementary MedicinePenrithAustralia
  3. 3.Faculty of Health SciencesUniversity of SydneyLidcombeAustralia
  4. 4.Ingham Institute for Applied Medical ResearchLiverpoolAustralia
  5. 5.South Western Sydney Clinical SchoolUniversity of New South WalesSydneyAustralia
  6. 6.Liverpool HospitalLiverpoolAustralia
  7. 7.School of Nursing and MidwiferyUniversity of Western SydneyPenrithAustralia
  8. 8.School of MedicineUniversity of AdelaideAdelaideAustralia

Personalised recommendations