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Breast Cancer Research and Treatment

, Volume 170, Issue 3, pp 455–476 | Cite as

Effects of physical exercise after treatment of early breast cancer: systematic review and meta-analysis

  • Frederico Soares Falcetta
  • Henrique de Araújo Vianna Träsel
  • Fernando Kude de Almeida
  • Mariana Rangel Ribeiro Falcetta
  • Maicon Falavigna
  • Daniela Dornelles Rosa
Review

Abstract

Purpose

Randomized clinical trials are inconclusive regarding the role of physical exercise in anthropometric measurements, quality of life, and survival in breast cancer patients. Our aim was to conduct a systematic review and meta-analysis to assess the effects of physical exercise on these outcomes in women who went through curative treatment of early-stage breast cancer.

Methods

Pubmed, Embase, Cochrane Library were searched for randomized clinical trial comparing physical exercise (counseling or structured programs with supervised/individualized exercise sessions) with usual care in women that went through for breast cancer treatment. Primary outcomes were overall survival and disease-free survival, while secondary outcomes were weight loss, body mass index, waist–hip ratio, percentage of body fat, and quality of life.

Results

We found 60 randomized clinical trials, only one of them showed mortality data; the HR for mortality was 0.45 (95% CI 0.21–0.97) for the intervention group when compared to the control group. Physical exercise was associated with weight reduction (− 1.36 kg, 95% CI − 2.51 to − 0.21, p = 0.02), lower body mass index (− 0.89 kg/m2, 95% CI − 1.50 to − 0.28, p < 0.01), and lower percentage of body fat (− 1.60 percentage points, 95% CI − 2.31 to − 0.88, p < 0.01). There was an increase in the quality of life (standardized mean difference of 0.45, 95% CI 0.20–0.69, p < 0.01).

Conclusions

The articles found had heterogeneous types of intervention, but they showed significant effects on anthropometric measures and quality of life. Among them, only one study had mortality as outcome and it showed physical exercise as a protective intervention. Despite these findings, publication bias and poor methodological quality were presented. Physical exercise should be advised for breast cancer survivors since it has no adverse effects and can improve anthropometrics measures and quality of life. PROSPERO registry: CRD42014008743.

Keywords

Breast cancer Meta-analysis Physical exercise Quality of life 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest to carry out this work.

Supplementary material

10549_2018_4786_MOESM1_ESM.docx (975 kb)
Supplementary material 1 (DOCX 975 kb)

References

  1. 1.
    Runowicz CD, Leach CR, Henry NL et al (2016) American Cancer Society/American Society of Clinical Oncology Breast Cancer Survivorship Care Guideline. J Clin Oncol 34:611–635CrossRefPubMedGoogle Scholar
  2. 2.
    Cowens-Alvarado R, Sharpe K, Pratt-Chapman M et al (2013) Advancing survivorship care through the National Cancer Survivorship Resource Center: developing American Cancer Society guidelines for primary care providers. CA Cancer J Clin 63:147–150CrossRefPubMedGoogle Scholar
  3. 3.
    Schapira DV, Kumar NB, Lyman GH et al (1991) Obesity and body fat distribution and breast cancer prognosis. Cancer 67:523–528CrossRefPubMedGoogle Scholar
  4. 4.
    Goodwin PJ, Boyd NF (1990) Body size and breast cancer prognosis: a critical review of the evidence. Breast Cancer Res Treat 16:205–214CrossRefPubMedGoogle Scholar
  5. 5.
    Holmes MD, Kroenke CH (2004) Beyond treatment: lifestyle choices after breast cancer to enhance quality of life and survival. Womens Health Issues 14:11–13CrossRefPubMedGoogle Scholar
  6. 6.
    Moradi T, Adami HO, Bergstrom R et al (1999) Occupational physical activity and risk for breast cancer in a nationwide cohort study in Sweden. Cancer Causes Control 10:423–430CrossRefPubMedGoogle Scholar
  7. 7.
    Rockhill B, Willett WC, Hunter DJ et al (1999) A prospective study of recreational physical activity and breast cancer risk. Arch Intern Med 159:2290–2296CrossRefPubMedGoogle Scholar
  8. 8.
    Holmes MD, Chen WY, Feskanich D et al (2005) Physical activity and survival after breast cancer diagnosis. JAMA 293:2479–2486CrossRefPubMedGoogle Scholar
  9. 9.
    Bluethmann SM, Vernon SW, Gabriel KP et al (2015) Taking the next step: a systematic review and meta-analysis of physical activity and behavior change interventions in recent post-treatment breast cancer survivors. Breast Cancer Res Treat 149:331–342CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Falavigna M, Lima KM, Giacomazzi J et al (2014) Effects of lifestyle modification after breast cancer treatment: a systematic review protocol. Syst Rev 3:72CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Higgins J, Green S (2011) Cochrane handbook for systematic reviews of interventions. Version 5.1.0, In: The Cochrane CollaborationGoogle Scholar
  12. 12.
    Liberati A, Altman DG, Tetzlaff J et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339:b2700CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Harrigan M, Cartmel B, Loftfield E et al (2016) Randomized trial comparing telephone versus in-person weight loss counseling on body composition and circulating biomarkers in women treated for breast cancer: the lifestyle, exercise, and nutrition (LEAN) study. J Clin Oncol 34:669–676CrossRefPubMedGoogle Scholar
  14. 14.
    Demark-Wahnefried W, Jones LW, Snyder DC et al (2014) Daughters and Mothers Against Breast Cancer (DAMES): main outcomes of a randomized controlled trial of weight loss in overweight mothers with breast cancer and their overweight daughters. Cancer 120:2522–2534CrossRefPubMedGoogle Scholar
  15. 15.
    Vallance JKH, Courneya KS, Plotnikoff RC et al (2007) Randomized controlled trial of the effects of print materials and step pedometers on physical activity and quality of life in breast cancer survivors. J Clin Oncol 25:2352–2359CrossRefPubMedGoogle Scholar
  16. 16.
    Herrero F, San JA, Fleck S et al (2006) Combined aerobic and resistance training in breast cancer survivors: a randomized, controlled pilot trial. Int J Sports Med 27:573–580CrossRefPubMedGoogle Scholar
  17. 17.
    Lee MK, Yun YH, Park H-A et al (2014) A Web-based self-management exercise and diet intervention for breast cancer survivors: pilot randomized controlled trial. Int J Nurs Stud 51:1557–1567CrossRefPubMedGoogle Scholar
  18. 18.
    Heim M, von der Malsburg M, Niklas A (2007) Randomized controlled trial of a structured training program in breast cancer patients with tumor-related chronic fatigue. Onkologie 30:429–434PubMedGoogle Scholar
  19. 19.
    Rogers LQ, Hopkins-Price P, Vicari S et al (2009) Physical activity and health outcomes three months after completing a physical activity behavior change intervention: persistent and delayed effects. Cancer Epidemiol Biomark Prev 18:1410–1418CrossRefGoogle Scholar
  20. 20.
    Baruth M, Wilcox S, Der Ananian C et al (2015) Effects of home-based walking on quality of life and fatigue outcomes in early stage breast cancer survivors: a 12-week pilot study. J Phys Act Health 12(Suppl 1):S110–S118CrossRefPubMedGoogle Scholar
  21. 21.
    Fields J, Richardson A, Hopkinson J et al (2016) Nordic walking as an exercise intervention to reduce pain in women with aromatase inhibitor-associated arthralgia: a feasibility study. J Pain Symptom Manag 52:548–559CrossRefGoogle Scholar
  22. 22.
    Balshem H, Helfand M, Schunemann HJ et al (2011) GRADE guidelines: 3. Rating the quality of evidence. J Clin Epidemiol 64:401–406CrossRefPubMedGoogle Scholar
  23. 23.
    Hayes SC, Steele M, Spence R et al (2017) Can exercise influence survival following breast cancer: Results from a randomised, controlled trial. J Clin Oncol 35(Suppl 15):10067Google Scholar
  24. 24.
    Welch HG, Prorok PC, O’Malley AJ et al (2016) Breast-cancer tumor size, overdiagnosis, and mammography screening effectiveness. N Engl J Med 375:1438–1447CrossRefPubMedGoogle Scholar
  25. 25.
    Pan H, Gray R, Braybrooke J et al (2017) 20-Year risks of breast-cancer recurrence after stopping endocrine therapy at 5 years. N Engl J Med 377:1836–1846CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Nyrop KA, Callahan LF, Cleveland RJ et al (2017) Randomized controlled trial of a home-based walking program to reduce moderate to severe aromatase inhibitor-associated arthralgia in breast cancer survivors. Oncologist 22(10):1238–1249CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Anderson DJ, Seib C, McCarthy AL et al (2015) Facilitating lifestyle changes to manage menopausal symptoms in women with breast cancer: a randomized controlled pilot trial of The Pink Women’s Wellness Program. Menopause (New York, NY) 22:937–945CrossRefGoogle Scholar
  28. 28.
    Cadmus LA, Salovey P, Yu H et al (2009) Exercise and quality of life during and after treatment for breast cancer: results of two randomized controlled trials. Psycho-Oncology 18:343–352CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Campbell KL, Kam JW, Neil-Sztramko SE et al (2017) Effect of aerobic exercise on cancer-associated cognitive impairment: a proof-of-concept RCT. Psychooncology 27(1):53–60CrossRefPubMedGoogle Scholar
  30. 30.
    Casla S, López-Tarruella S, Jerez Y et al (2015) Supervised physical exercise improves VO2max, quality of life, and health in early stage breast cancer patients: a randomized controlled trial. Breast Cancer Res Treat 153:371–382CrossRefPubMedGoogle Scholar
  31. 31.
    Courneya K, Mackey JR, Bell G et al (2003) Randomized controlled trial of exercise training in postmenopausal breast cancer survivors: cardiopulmonary and quality of life outcomes. J Clin Oncol 21:1660–1668CrossRefPubMedGoogle Scholar
  32. 32.
    Daley A, Crank H, Saxton J et al (2007) Randomized trial of exercise therapy in women treated for breast cancer. J Clin Oncol 25:1713–1721CrossRefPubMedGoogle Scholar
  33. 33.
    De Luca V, Minganti C, Borrione P et al (2016) Effects of concurrent aerobic and strength training on breast cancer survivors: A pilot study. Public Health 136:126–132CrossRefPubMedGoogle Scholar
  34. 34.
    Demark-Wahnefried W, Colditz GA, Rock CL et al (2015) Quality of life outcomes from the Exercise and Nutrition Enhance Recovery and Good Health for You (ENERGY)-randomized weight loss trial among breast cancer survivors. Breast Cancer Res Treat 154:329–337CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Do J, Cho Y, Jeon J (2015) Effects of a 4-week multimodal rehabilitation program on quality of life, cardiopulmonary function, and fatigue in breast cancer patients. J Breast Cancer 18:87–96CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Duijts S, Beurden M, Oldenburg H et al (2012) Efficacy of cognitive behavioral therapy and physical exercise in alleviating treatment-induced menopausal symptoms in patients with breast cancer: results of a randomized, controlled, multicenter trial. J Clin Oncol 30:4124–4133CrossRefPubMedGoogle Scholar
  37. 37.
    Fairey AS, Courneya KS, Field CJ et al (2003) Effects of exercise training on fasting insulin, insulin resistance, insulin-like growth factors, and insulin-like growth factor binding proteins in postmenopausal breast cancer survivors: a randomized controlled trial. Cancer Epidemiol Biomark Prev 12:721–727Google Scholar
  38. 38.
    Fillion L, Gagnon P, Leblond F et al (2008) A brief intervention for fatigue management in breast cancer survivors. Cancer Nurs 31:145–159CrossRefPubMedGoogle Scholar
  39. 39.
    Galiano-Castillo N, Cantarero-Villanueva I, Fernández-Lao C et al (2016) Telehealth system: a randomized controlled trial evaluating the impact of an internet-based exercise intervention on quality of life, pain, muscle strength, and fatigue in breast cancer survivors. Cancer 122:3166–3174CrossRefPubMedGoogle Scholar
  40. 40.
    Ghavami H, Akyolcu N (2017) The impact of lifestyle interventions in breast cancer women after completion of primary therapy: a randomized study. J Breast Health (Meme Sagligi Dergisi) 13:94–99CrossRefGoogle Scholar
  41. 41.
    Giallauria F, Maresca L, Vitelli A et al (2015) Exercise training improves heart rate recovery in women with breast cancer. SpringerPlus 4:388CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Goodwin P, Segal R, Vallis M et al (2014) Randomized trial of a telephone-based weight loss intervention in postmenopausal women with breast cancer receiving letrozole: the LISA trial. J Clin Oncol 32:2231–2239CrossRefPubMedGoogle Scholar
  43. 43.
    Greenlee H, Awad D, Crew K et al (2013) Influence of a clinic-based survivorship intervention on dietary change and lifestyle recommendations among Hispanic and non-Hispanic women following adjuvant therapy for breast cancer. Cancer research.  https://doi.org/10.1158/0008-5472.SABCS13-P3-08-12 Google Scholar
  44. 44.
    Guinan E, Hussey J, Broderick J et al (2013) The effect of aerobic exercise on metabolic and inflammatory markers in breast cancer survivors—a pilot study. Support Care Cancer 21:1983–1992CrossRefPubMedGoogle Scholar
  45. 45.
    Hagstrom A, Marshall P, Lonsdale C et al (2016) The effect of resistance training on markers of immune function and inflammation in previously sedentary women recovering from breast cancer: a randomized controlled trial. Breast Cancer Res Treat 155:471–482CrossRefPubMedGoogle Scholar
  46. 46.
    Irwin M, Alvarez-Reeves M, Cadmus L et al (2009) Exercise improves body fat, lean mass, and bone mass in breast cancer survivors. Obesity (Silver Spring, Md.) 17:1534–1541CrossRefGoogle Scholar
  47. 47.
    Irwin ML, Cartmel B, Gross C et al (2013) Randomized trial of exercise vs. usual care on aromatase inhibitor-associated arthralgias in women with breast cancer: the hormones and physical exercise (HOPE) study. Cancer Res.  https://doi.org/10.1158/0008-5472.SABCS13-S3-03 PubMedGoogle Scholar
  48. 48.
    Karimi N, Roshan VD (2013) Change in adiponectin and oxidative stress after modifiable lifestyle interventions in breast cancer cases. Asian Pac J Cancer Prev 14:2845–2850CrossRefPubMedGoogle Scholar
  49. 49.
    Kim SH, Shin MS, Lee HS et al (2011) Randomized pilot test of a simultaneous stage-matched exercise and diet intervention for breast cancer survivors. Oncol Nurs Forum 38:E97–E106CrossRefPubMedGoogle Scholar
  50. 50.
    Kim TH, Chang JS, Park KS et al (2017) Effects of exercise training on circulating levels of Dickkpof-1 and secreted frizzled-related protein-1 in breast cancer survivors: a pilot single-blind randomized controlled trial. PLoS ONE 12:e0171771CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Kwiatkowski F, Mouret-Reynier M, Duclos M et al (2013) Long term improved quality of life by a 2-week group physical and educational intervention shortly after breast cancer chemotherapy completion. Results of the ‘Programme of Accompanying women after breast Cancer treatment completion in Thermal resorts’ (PACThe) randomised clinical trial of 251 patients. Eur J Cancer (Oxford, England: 1990) 49:1530–1538CrossRefGoogle Scholar
  52. 52.
    Lahart I, Metsios G, Nevill A et al (2016) Randomised controlled trial of a home-based physical activity intervention in breast cancer survivors. BMC Cancer 16:234CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Ligibel J, Campbell N, Partridge A et al (2008) Impact of a mixed strength and endurance exercise intervention on insulin levels in breast cancer survivors. J Clin Oncol 26:907–912CrossRefPubMedGoogle Scholar
  54. 54.
    Matthews C, Wilcox S, Hanby C et al (2007) Evaluation of a 12-week home-based walking intervention for breast cancer survivors. Support Care Cancer 15:203–211CrossRefPubMedGoogle Scholar
  55. 55.
    Mefferd K, Nichols J, Pakiz B et al (2007) A cognitive behavioral therapy intervention to promote weight loss improves body composition and blood lipid profiles among overweight breast cancer survivors. Breast Cancer Res Treat 104:145–152CrossRefPubMedGoogle Scholar
  56. 56.
    Milne HM, Wallman KE, Gordon S et al (2008) Effects of a combined aerobic and resistance exercise program in breast cancer survivors: a randomized controlled trial. Breast Cancer Res Treat 108:279–288CrossRefPubMedGoogle Scholar
  57. 57.
    Nuri R, Kordi MR, Moghaddasi M et al (2012) Effect of combination exercise training on metabolic syndrome parameters in postmenopausal women with breast cancer. J Cancer Res Ther 8:238–242CrossRefPubMedGoogle Scholar
  58. 58.
    Ohira T, Schmitz K, Ahmed R et al (2006) Effects of weight training on quality of life in recent breast cancer survivors: the Weight Training for Breast Cancer Survivors (WTBS) study. Cancer 106:2076–2083CrossRefPubMedGoogle Scholar
  59. 59.
    Pakiz B, Flatt S, Bardwell W et al (2011) Effects of a weight loss intervention on body mass, fitness, and inflammatory biomarkers in overweight or obese breast cancer survivors. Int J Behav Med 18:333–341CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Pinto B, Frierson G, Rabin C et al (2005) Home-based physical activity intervention for breast cancer patients. J Clin Oncol 23:3577–3587CrossRefPubMedGoogle Scholar
  61. 61.
    Rahnama N, Nouri R, Rahmaninia F et al (2010) The effects of exercise training on maximum aerobic capacity, resting heart rate, blood pressure and anthropometric variables of postmenopausal women with breast cancer. J Res Med Sci 15:78–83PubMedPubMedCentralGoogle Scholar
  62. 62.
    Reeves M, Winkler E, McCarthy N et al (2017) The Living Well after Breast Cancer Pilot Trial: a weight loss intervention for women following treatment for breast cancer. Asia Pac J Clin Oncol 13:125–136CrossRefPubMedGoogle Scholar
  63. 63.
    Rock CL, Flatt SW, Byers TE et al (2015) Results of the Exercise and Nutrition to Enhance Recovery and Good Health for You (ENERGY) trial: a behavioral weight loss intervention in overweight or obese breast cancer survivors. J Clin Oncol 33:3169–3176CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Roveda E, Vitale JA, Bruno E et al (2017) Protective effect of aerobic physical activity on sleep behavior in breast cancer survivors. Integr Cancer Ther 16:21–31CrossRefPubMedGoogle Scholar
  65. 65.
    Saarto T, Penttinen H, Sievänen H et al (2012) Effectiveness of a 12-month exercise program on physical performance and quality of life of breast cancer survivors. Anticancer Res 32:3875–3884PubMedGoogle Scholar
  66. 66.
    Schmitz KH, Ahmed RL, Hannan PJ et al (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 14:1672–1680CrossRefGoogle Scholar
  67. 67.
    Scott E, Daley AJ, Doll H et al (2013) Effects of an exercise and hypocaloric healthy eating program on biomarkers associated with long-term prognosis after early-stage breast cancer: a randomized controlled trial. Cancer Causes Control 24:181–191CrossRefPubMedGoogle Scholar
  68. 68.
    Sheppard VB, Hicks J, Makambi K et al (2016) The feasibility and acceptability of a diet and exercise trial in overweight and obese black breast cancer survivors: the Stepping STONE study. Contempor Clin Trials 46:106–113CrossRefGoogle Scholar
  69. 69.
    Shobeiri F, Masoumi SZ, Nikravesh A et al (2016) The impact of aerobic exercise on quality of life in women with breast cancer: a randomized controlled trial. J Res Health Sci 16:127–132PubMedGoogle Scholar
  70. 70.
    Speck R, Gross C, Hormes J et al (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 121:421–430CrossRefPubMedGoogle Scholar
  71. 71.
    Sturgeon KM, Dean LT, Heroux M et al (2016) Commercially available lifestyle modification program: randomized controlled trial addressing heart and bone health in BRCA1/2+ breast cancer survivors after risk-reducing salpingo-oophorectomy. J Cancer Surviv 11:246–255CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Swisher AK, Abraham J, Bonner D et al (2015) Exercise and dietary advice intervention for survivors of triple-negative breast cancer: effects on body fat, physical function, quality of life, and adipokine profile. Support Care Cancer 23:2995–3003CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Thomas GA, Cartmel B, Harrigan M et al (2017) The effect of exercise on body composition and bone mineral density in breast cancer survivors taking aromatase inhibitors. Obesity 25:346–351CrossRefPubMedGoogle Scholar
  74. 74.
    Tirado-Gomez M, Palacios C, Ortiz A, et al (2015) Serum adipokines and inflammatory markers in Hispanic breast cancer survivors. Cancer Epidemiology Biomarkers and Prevention. In: Conference: 7th AACR Conference on the Science of Health Disparities in Racial/Ethnic Minorities and the Medically Underserved San Antonio, TX United States. Conference Start: 20141109 Conference End: 20141112. Conference Publication: (var.pagings), vol 24, 2015Google Scholar
  75. 75.
    Winters-Stone KM, Dobek J, Nail LM et al (2013) Impact + resistance training improves bone health and body composition in prematurely menopausal breast cancer survivors: a randomized controlled trial. Osteoporos Int 24:1637–1646CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Frederico Soares Falcetta
    • 1
  • Henrique de Araújo Vianna Träsel
    • 1
  • Fernando Kude de Almeida
    • 1
  • Mariana Rangel Ribeiro Falcetta
    • 2
  • Maicon Falavigna
    • 2
  • Daniela Dornelles Rosa
    • 1
    • 3
  1. 1.Pathology Post-Graduate Program - Universidade Federal de Ciências da Saúde de Porto AlegrePorto AlegreBrazil
  2. 2.Hospital de Clínicas de Porto AlegrePorto AlegreBrazil
  3. 3.Hospital Moinhos de VentoPorto AlegreBrazil

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