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

Breast Cancer Research and Treatment

Volumn 148, Issue 2, 2014, Pages 249-268

  Cheema, Birinder S ^a,b   Kilbreath, Sharon L ^c   Fahey, Paul P ^a   Delaney, Geoffrey P ^d,e,f   Atlantis, Evan ^a,g  

^a UNIVERSITY OF WESTERN SYDNEY   (Australia)

^b WESTERN SYDNEY UNIVERSITY   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

^d INGHAM INSTITUTE FOR APPLIED MEDICAL RESEARCH   (Australia)

^e UNIVERSITY OF NEW SOUTH WALES   (Australia)

^f LIVERPOOL HOSPITAL   (Australia)

^g UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

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

Indexed keywords

AEROBIC EXERCISE; BACKACHE; BREAST CANCER; CLINICAL EFFECTIVENESS; COMPARATIVE EFFECTIVENESS; DISEASE EXACERBATION; DISEASE SEVERITY; EXERCISE INTENSITY; FEMALE; HUMAN; KNEE PAIN; LYMPHEDEMA; MAJOR CLINICAL STUDY; META ANALYSIS; MUSCLE STRENGTH; MUSCULOSKELETAL INJURY; MYALGIA; OUTCOME ASSESSMENT; PATIENT SAFETY; PHYSICAL CAPACITY; PHYSIOTHERAPY; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIAL (TOPIC); RESISTANCE TRAINING; REVIEW; RISK REDUCTION; SYSTEMATIC REVIEW; VITAMIN SUPPLEMENTATION; BREAST NEOPLASMS; KINESIOTHERAPY; SAFETY;

BREAST NEOPLASMS; EXERCISE THERAPY; FEMALE; HUMANS; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RESISTANCE TRAINING; SAFETY;

EID: 84911471247     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-014-3162-9     Document Type: Review

References (70)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90
2. GLOBOCAN: estimated cancer incidence, mortality and prevalence worldwide in 2012. http://globocan.iarc.fr/Pages/fact_sheets_cancer.aspx
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):127–138
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):1133–1145
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):60–62
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):1687–1717
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):1402–1411
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):115–123
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):513–520
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):405–414
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):282–294
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):398–406
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):552–558
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):3437–3444
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):5383–5391
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):2433–2439
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):206–210
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):679–690
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):21–31
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):665–673
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):386–405
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):20–31
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):406–412
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 109:9–26
25. Demark-Wahnefried W (2009) A weighty matter—lifting after breast cancer. N Engl J Med 361(7):710–711
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):2765–2772
27. Ohira T, Schmitz K, Ahmed R, Yee D (2006) Effects of weight training on quality of life in recent breast cancer survivors. Cancer 106:2076–2083
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):4396–4404
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):627–633
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):20–27
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 361:664–673
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):2699–2705
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):421–430
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):1844–1848
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):189–199
36. Musanti R (2012) A study of exercise modality and physical self-esteem in breast cancer survivors. Med Sci Sports Exerc 44(2):352–361
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):667–676
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):1637–1646
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):413–424
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):1821–1832
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–vi24
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):159–160
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):122–192
44. Foldi E, Foldi M, Clodius L (1989) The lymphedema chaos: a lancet. Ann Plast Surg 22:505–515
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):2756–2768
46. Schulz KF, Altman DG, Moher D (2010) CONSORT 2010 statement: updated guidelines for reporting parallel group randomised trials. Trials 11:32
47. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188
48. Higgins J, Green S (2011) Cochrane handbook for systematic reviews of interventions, version 5.1.0
49. Haldane JB (1956) The estimation and significance of the logarithm of a ratio of frequencies. Ann Hum Genet 20(4):309–311
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):1351–1375
51. Higgins J, Thompson S, Deeks J, Altman D (2003) Measuring inconsistency in meta-analysis. Br Med J 327(7414):557–560
52. Higgins J, Thompson S (2002) Quantifying heterogeneity in meta-analysis. Stat Med 21(11):1539–1558
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):629–634
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):1192–1205
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):1672–1680
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):1120–1128
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):3536–3542
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):2237–2249
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):1253–1257
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):981–991
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):875–881
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):57–64
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):1059–1064
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):72–77
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):257–264
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):101–108
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):125–134
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):116–128
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):2198–2204
70. Merchant CR, Chapman T, Kilbreath SL, Refshauge KM, Krupa K (2008) Decreased muscle strength following management of breast cancer. Disabil Rehabil 30(15):1098–1105