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A Systematic Review and Meta-Analysis of the Safety, Feasibility, and Effect of Exercise in Women With Stage II+ Breast Cancer

  • Ben Singh
    Correspondence
    Corresponding author Ben Singh, MSc, School of Public Health and Social Work, Queensland University of Technology, Victoria Park Road, Kelvin Grove, Queensland, Australia 4059.
    Affiliations
    School of Public Health and Social Work, Queensland University of Technology, Victoria Park Road, Brisbane, Queensland, Australia

    Institute of Health and Biomedical Innovation, Queensland University of Technology, Musk Avenue, Kelvin Grove, Queensland, Australia
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  • Rosalind R. Spence
    Affiliations
    School of Public Health and Social Work, Queensland University of Technology, Victoria Park Road, Brisbane, Queensland, Australia

    Institute of Health and Biomedical Innovation, Queensland University of Technology, Musk Avenue, Kelvin Grove, Queensland, Australia
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  • Megan L. Steele
    Affiliations
    School of Public Health and Social Work, Queensland University of Technology, Victoria Park Road, Brisbane, Queensland, Australia

    Institute of Health and Biomedical Innovation, Queensland University of Technology, Musk Avenue, Kelvin Grove, Queensland, Australia
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  • Carolina X. Sandler
    Affiliations
    School of Public Health and Social Work, Queensland University of Technology, Victoria Park Road, Brisbane, Queensland, Australia

    Institute of Health and Biomedical Innovation, Queensland University of Technology, Musk Avenue, Kelvin Grove, Queensland, Australia

    Cancer Prevention Research Centre, School of Public Health, Faculty of Medicine, The University of Queensland, Herston, Queensland, Australia
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  • Jonathan M. Peake
    Affiliations
    Institute of Health and Biomedical Innovation, Queensland University of Technology, Musk Avenue, Kelvin Grove, Queensland, Australia

    School of Biomedical Sciences, Queensland University of Technology, Victoria Park Road, Kelvin Grove, Queensland, Australia
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  • Sandra C. Hayes
    Affiliations
    School of Public Health and Social Work, Queensland University of Technology, Victoria Park Road, Brisbane, Queensland, Australia

    Institute of Health and Biomedical Innovation, Queensland University of Technology, Musk Avenue, Kelvin Grove, Queensland, Australia
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      Abstract

      Objective

      To systematically evaluate the safety, feasibility, and effect of exercise among women with stage II+ breast cancer.

      Data Sources

      CINAHL, Cochrane, Ebscohost, MEDLINE, Pubmed, ProQuest Health and Medical Complete, ProQuest Nursing and Allied Health Source, Science Direct and SPORTDiscus were searched for articles published before March 1, 2017.

      Study Selection

      Randomized, controlled, exercise trials involving at least 50% of women diagnosed with stage II+ breast cancer were included.

      Data Extraction

      Risk of bias was assessed and adverse event severity was classified using the Common Terminology Criteria. Feasibility was evaluated by computing median (range) recruitment, withdrawal, and adherence rates. Meta-analyses were performed to evaluate exercise safety and effects on health outcomes only. The influence of intervention characteristics (mode, supervision, duration and timing) on exercise outcomes were also explored.

      Data Synthesis

      There were no differences in adverse events between exercise and usual care (risk difference: <0.01 ([95% CI: -0.01, 0.01], P=0.38). Median recruitment rate was 56% (1%-96%), withdrawal rate was 10% (0%-41%) and adherence rate was 82% (44%-99%). Safety and feasibility outcomes were similar, irrespective of exercise mode, supervision, duration, or timing. Effects of exercise for quality of life, fitness, fatigue, strength, anxiety, depression, body mass index and waist circumference compared with usual care were significant (standardized mean difference range: 0.17-0.77, P<0.05).

      Conclusion

      The findings support the safety, feasibility, and effects of exercise for those with stage II+ breast cancer, suggesting that national and international exercise guidelines appear generalizable to women with local, regional, and distant breast cancer.

      Keywords

      List of Abbreviations:

      1RM (one repetition maximum), CI (confidence interval), PEDro (physiotherapy evidence database), QOL (quality of life), RCT (randomized control trial), RD (risk difference), SMD (standardized mean difference)
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      References

        • Hayes S.C.
        • Spence R.R.
        • Galvão D.A.
        • Newton R.U.
        Australian Association for Exercise and Sport Science position stand: optimizing cancer outcomes through exercise.
        J Sci Med Sport. 2009; 12: 428-434
        • Cheema B.
        • Gaul C.A.
        • Lane K.
        • Fiatarone Singh M.A.
        Progressive resistance training in breast cancer: a systematic review of clinical trials.
        Breast Cancer Res Treat. 2008; 109: 9-26
        • Speck R.M.
        • Courneya K.S.
        • Mâsse L.C.
        • Duval S.
        • Schmitz K.H.
        An update of controlled physical activity trials in cancer survivors: a systematic review and meta-analysis.
        J Cancer Surviv. 2010; 4: 87-100
        • Tian L.
        • Lu H.J.
        • Lin L.
        • Hu Y.
        Effects of aerobic exercise on cancer-related fatigue: a meta-analysis of randomized controlled trials.
        Support Care Cancer. 2016; 24: 969-983
        • Spence R.R.
        • Heesch K.C.
        • Brown W.J.
        Exercise and cancer rehabilitation: a systematic review.
        Cancer Treat Rev. 2010; 36: 185-194
        • Schmitz K.H.
        • Holtzman J.
        • Courneya K.S.
        • Mâsse L.C.
        • Duval S.
        • Kane R.
        Controlled physical activity trials in cancer survivors: a systematic review and meta-analysis.
        Cancer Epidemiol Biomarkers Prev. 2005; 14: 1588-1595
        • Cormie P.
        • Zopf E.M.
        • Zhang X.
        • Schmitz K.H.
        The impact of exercise on cancer mortality, recurrence, and treatment-related adverse effects.
        Epidemiol Rev. 2017; 39: 1-22
        • Baumann F.T.
        Physical exercise programs following cancer treatment.
        Eur Rev Aging Phys Act. 2013; 10: 57-59
        • Hayes S.C.
        • Rye S.
        • Disipio T.
        • et al.
        Exercise for health: a randomized, controlled trial evaluating the impact of a pragmatic, translational exercise intervention on the quality of life, function and treatment-related side effects following breast cancer.
        Breast Cancer Res Treat. 2013; 137: 175-186
        • Courneya K.S.
        Physical activity and cancer survivorship: a simple framework for a complex field.
        Exerc Sport Sci Rev. 2014; 42: 102-109
        • Irwin M.L.
        Physical activity interventions for cancer survivors.
        Br J Sports Med. 2009; 43: 32-38
        • Ibrahim E.M.
        • Al-Homaidh A.
        Physical activity and survival after breast cancer diagnosis: meta-analysis of published studies.
        Med Oncol. 2011; 28: 753-765
        • Spence R.R.
        • Di Sipio T.
        • Schmitz K.
        • Hayes S.C.
        Is unsupervised exercise following breast cancer safe for all women?.
        Int J Phys Med Rehabil. 2014; 2: 1-8
        • Maddocks M.
        • Mockett S.
        • Wilcock A.
        Is exercise an acceptable and practical therapy for people with or cured of cancer? A systematic review.
        Cancer Treat Rev. 2009; 35: 383-390
        • Australian Institute of Health and Welfare and National Breast and Ovarian Cancer Centre
        Breast cancer in Australia: an overview.
        Australian Institute of Health and Welfare, Canberra2009
        • American Cancer Society
        Cancer Treatment and Survivorship Facts andFigures 2014-2015.
        American Cancer Society, Atlanta2014
        • Oldervoll L.M.
        • Loge J.H.
        • Paltiel H.
        • et al.
        Are palliative cancer patients willing and able to participate in a physical exercise program?.
        Palliat Support Care. 2005; 3: 281-287
        • Dixon J.M.
        ABC of breast diseases.
        4th edition. Blackwell, Chichester, West Sussex2012
        • Brown P.
        • Clark M.M.
        • Atherton P.
        • et al.
        Will improvement in quality of life (QOL) impact fatigue in patients receiving radiation therapy for advanced cancer?.
        Am J Clin Oncol. 2006; 29: 52-58
        • Cheville A.L.
        • Troxel A.B.
        • Basford J.R.
        • Kornblith A.B.
        Prevalence and treatment patterns of physical impairments in patients with metastatic breast cancer.
        J Clin Oncol. 2008; 26: 2621-2629
        • Cancer Australia
        Report to the nation—breast cancer 2012.
        Australian Government, Surry Hills, NSW2012
        • American Cancer Society
        Breast Cancer Survival Rates.
        American Cancer Society, Atlanta2014
        • Schardt C.
        • Adams M.B.
        • Owens T.
        • Keitz S.
        • Fontelo P.
        Utilization of the PICO framework to improve searching PubMed for clinical questions.
        BMC Med Inform Decis Mak. 2007; 7: 16
        • Howley E.T.
        Type of activity: resistance, aerobic and leisure versus occupational physical activity.
        Med Sci Sports Exerc. 2001; 33: S364-S369
        • McNeely M.L.
        • Campbell K.L.
        • Rowe B.H.
        • Klassen T.P.
        • Mackey J.R.
        • Courneya K.S.
        Effects of exercise on breast cancer patients and survivors: a systematic review and meta-analysis.
        CMAJ. 2006; 175: 34-41
        • National Cancer Institute
        Common terminology criteria for adverse events (CTCAE) version 4.0.
        National Institutes of Health, Bethesda: Maryland2009
        • Australian Government Department of Health and Ageing
        The Australian clinical trial handbook: a simple, practical guide to the conduct of clinical trials to international standards of good clinical practice (GCP) in the Australian context.
        Commonwealth of Australia, Canberra2006
        • Wayne P.M.
        • Berkowitz D.L.
        • Litrownik D.E.
        • Buring J.E.
        • Yeh G.Y.
        What do we really know about the safety of tai chi? A systematic review of adverse event reports in randomized trials.
        Arch Phys Med Rehabil. 2014; 95: 2470-2483
        • Maher C.G.
        • Sherrington C.
        • Herbert R.D.
        • Moseley A.M.
        • Elkins M.
        Reliability of the PEDro Scale for Rating Quality of Randomized Controlled Trials.
        Phys Ther. 2003; 83: 713-721
        • Sherrington C.
        • Herbert R.D.
        • Maher C.G.
        • Moseley A.M.
        PEDro. A database of randomized trials and systematic reviews in physiotherapy.
        Man Ther. 2000; 5: 223-226
        • Armijo-Olivo S.
        • da Costa B.R.
        • Cummings G.G.
        • et al.
        PEDro or Cochrane to assess the quality of clinical trials? A meta-epidemiological study.
        PLOS ONE. 2015; 10e0132634
        • Harrison R.W.
        • Hasselblad V.
        • Mehta R.H.
        • Levin R.
        • Harrington R.A.
        • Alexander J.H.
        Effect of levosimendan on survival and adverse events after cardiac surgery: a meta-analysis.
        J Cardiothorac Vasc Anesth. 2013; 27: 1224-1232
        • Hasselblad V.
        • Mosteller F.
        • Littenberg B.
        • et al.
        A survey of current problems in meta-analysis. Discussion from the Agency for Health Care Policy and Research inter-PORT Work Group on Literature Review/Meta-Analysis.
        Med Care. 1995; 33: 202-220
        • Lewis P.B.
        • Ruby D.
        • Bush-Joseph C.A.
        Muscle soreness and delayed-onset muscle soreness.
        Clin Sports Med. 2012; 31: 255-262
        • Riebe D.
        • Ehrman J.K.
        • Liguori G.
        • Meir M.
        ACSM's guidelines for exercise testing and prescription.
        10th edition. Wolters Kluwer Health, Philadelphia, PA2018
        • De Jesus S.
        • Fitzgeorge L.
        • Unsworth K.
        • et al.
        Feasibility of an exercise intervention for fatigued breast cancer patients at a community-based cardiac rehabilitation program.
        Cancer Manag Res. 2017; 9: 29-39
        • Newton M.J.
        • Hayes S.C.
        • Janda M.
        • et al.
        Safety, feasibility and effects of an individualised walking intervention for women undergoing chemotherapy for ovarian cancer: a pilot study.
        BMC Cancer. 2011; 11: 389
        • Valkenet K.
        • Trappenburg J.C.
        • Schippers C.C.
        • et al.
        Feasibility of exercise training in cancer patients scheduled for elective gastrointestinal surgery.
        Dig Surg. 2016; 33: 439-447
        • Coats V.
        • Maltais F.
        • Simard S.
        • et al.
        Feasibility and effectiveness of a home-based exercise training program before lung resection surgery.
        Can Respir J. 2013; 20: e10-e16
        • Higgins J.P.
        • Deeks J.J.
        • Altman D.G.
        Special topics in statistics.
        in: Higgins J.P.T. Green S. Cochrane Handbook for Systematic Reviews of Interventions. John Wiley and Sons, Ltd, 2008: 481-529
        • Egger M.
        • Davey Smith G.
        • Schneider M.
        • Minder C.
        Bias in meta-analysis detected by a simple, graphical test.
        BMJ. 1997; 315: 629-634
        • Thompson G.
        • Higgins J.P.
        How should meta-regression analyses be undertaken and interpreted?.
        Stat Med. 2002; 21: 1559-1573
        • Deeks J.J.
        • Higgins J.P.T.
        • Altman D.G.
        Analysing data and undertaking meta-analyses, in Cochrane handbook for systematic reviews of interventions.
        John Wiley and Sons, Ltd. 2008; : 243-296
        • Cohen J.
        Statistical power analysis for the behavioral sciences.
        2nd edition. Lawrence Erlbaum Associates, Hillsdale, New Jersey1988
        • Guinan E.M.
        • Connolly E.M.
        • Hussey J.
        Exercise training in breast cancer survivors: a review of trials examining anthropometric and obesity-related biomarkers of breast cancer risk.
        Phys Ther Rev. 2013; 18: 79-89
        • Cormie P.
        • Pumpa K.
        • Galvão D.A.
        • et al.
        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 Surviv. 2013; 7: 413-424
        • Dolan L.B.
        • Campbell K.
        • Gelmon K.
        • Neil-Sztramko S.
        • Holmes D.
        • McKenzie D.C.
        Interval versus continuous aerobic exercise training in breast cancer survivors—a pilot RCT.
        Support Care Cancer. 2016; 24: 119-127
        • Kim C.J.
        • Kang D.H.
        • Smith B.A.
        • Landers K.A.
        Cardiopulmonary responses and adherence to exercise in women newly diagnosed with breast cancer undergoing adjuvant therapy.
        Cancer Nurs. 2006; 29: 156-165
        • Winters-Stone K.M.
        • Dobek J.
        • Nail L.
        • et al.
        Strength training stops bone loss and builds muscle in postmenopausal breast cancer survivors: a randomized, controlled trial.
        Breast Cancer Res Treat. 2011; 127: 447-456
        • Gokal K.
        • Wallis D.
        • Ahmed S.
        • Boiangiu I.
        • Kancherla K.
        • Munir F.
        Effects of a self-managed home-based walking intervention on psychosocial health outcomes for breast cancer patients receiving chemotherapy: a randomised controlled trial.
        Support Care Cancer. 2016; 24: 1139-1166
        • Headley J.A.
        • Ownby K.K.
        • John L.D.
        The effect of seated exercise on fatigue and quality of life in women with advanced breast cancer.
        Oncol Nurs Forum. 2004; 31: 977-983
        • Hornsby W.E.
        • Douglas P.S.
        • West M.J.
        • et al.
        Safety and efficacy of aerobic training in operable breast cancer patients receiving neoadjuvant chemotherapy: a phase II randomized trial.
        Acta Oncol. 2014; 53: 65-74
        • Ligibel J.A.
        • Giobbie-Hurder A.
        • Shockro L.
        • et al.
        Randomized trial of a physical activity intervention in women with metastatic breast cancer.
        Cancer. 2016; 122: 1169-1177
        • Macvicar M.G.
        • Winningham M.L.
        • Nickel J.L.
        Effects of aerobic interval training on cancer patients' functional capacity.
        Nurs Res. 1989; 38: 348-353
        • Portela A.L.M.
        • Santaella C.L.
        • Gómez C.C.
        • Burch A.
        Feasibility of an exercise program for Puerto Rican women who are breast cancer survivors.
        Rehabil Oncol. 2008; 26: 20-31
        • Raghavendra R.M.
        • Nagarathna R.
        • Nagendra H.R.
        • et al.
        Effects of an integrated yoga programme on chemotherapy-induced nausea and emesis in breast cancer patients.
        Eur J Cancer Care. 2007; 16: 462-474
        • Rao R.
        • Cruz V.
        • Peng Y.
        • et al.
        Bootcamp during neoadjuvant chemotherapy for breast cancer: a randomized pilot trial.
        Breast Cancer. 2012; 6: 39-46
        • Rao R.M.
        • Raghuram N.
        • Nagendra H.R.
        • et al.
        Effects of an integrated yoga program on self-reported depression scores in breast cancer patients undergoing conventional treatment: a randomized controlled trial.
        Indian J Palliat Care. 2015; 21: 174-181
        • Campbell K.L.
        • Kam J.W.
        • Neil-Sztramko S.E.
        • et al.
        Effect of aerobic exercise on cancer-associated cognitive impairment: a proof-of-concept RCT.
        Psychooncology. 2018; 27: 53-60
        • Courneya K.S.
        • Mackey J.R.
        • Bell G.J.
        • Jones L.W.
        • Field C.J.
        • Fairey A.S.
        Randomized controlled trial of exercise training in postmenopausal breast cancer survivors: cardiopulmonary and quality of life outcomes.
        J Clin Oncol. 2003; 21: 1660-1668
        • Drouin J.S.
        • Young T.J.
        • Beeler J.
        • et al.
        Effects of aerobic exercise training on peak aerobic capacity, fatigue, and psychological factors during radiation for breast cancer.
        Rehabil Oncol. 2005; 23: 11-17
        • Murtezani A.
        • Ibraimi Z.
        • Bakalli A.
        • Krasniqi S.
        • Disha E.D.
        • Kurtishi I.
        The effect of aerobic exercise on quality of life among breast cancer survivors: a randomized controlled trial.
        J Cancer Res Ther. 2014; 10: 658-664
        • Naraphong W.
        Exercise intervention for fatigue-related symptoms in Thai women with breast cancer: a pilot study.
        Nurs Health Sci. 2014; 17: 33-41
        • Pinto B.M.
        • Papandonatos G.D.
        • Goldstein M.G.
        A randomized trial to promote physical activity among breast cancer patients.
        Health Psychol. 2013; 32: 616-626
        • Pinto B.M.
        • Stein K.
        • Dunsiger S.
        Peers Promoting Physical activity among breast cancer survivors: a randomized controlled trial.
        Health Psychol. 2015; 34: 463-472
        • Rogers L.Q.
        • Hopkins-Price P.
        • Vicari S.
        • et al.
        A randomized trial to increase physical activity in breast cancer survivors.
        Med Sci Sports Exerc. 2009; 41: 935-946
        • Vallance J.K.
        • Courneya K.S.
        • Plotnikoff R.C.
        • Yasui Y.
        • Mackey J.R.
        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. 2007; 25: 2352-2359
        • Wang Y.J.
        • Boehmke M.
        • Wu Y.W.
        • Dickerson S.S.
        • Fisher N.
        Effects of a 6-week walking program on Taiwanese women newly diagnosed with early-stage breast cancer.
        Cancer Nurs. 2011; 34: e1-e13
        • Yang C.Y.
        • Tsai J.C.
        • Huang Y.C.
        • Lin C.C.
        Effects of a home-based walking program on perceived symptom and mood statusin postoperative breast cancer women receiving adjuvant chemotherapy.
        J Adv Nurs. 2011; 67: 158-168
        • Pinto B.M.
        • Frierson G.M.
        • Rabin C.
        • Trunzo J.J.
        • Marcus B.H.
        Home-based physical activity intervention for breast cancer patients.
        J Clin Oncol. 2005; 23: 3577-3587
        • Vallance J.K.
        • Friedenreich C.M.
        • Lavallee C.M.
        • et al.
        Exploring the feasibility of a broad-reach physical activity behavior change intervention for women receiving chemotherapy for breast cancer: a randomized trial.
        Cancer Epidemiol Biomarkers Prev. 2016; 25: 391-398
        • Eakin E.G.
        • Lawler S.P.
        • Winkler E.A.
        • Hayes S.C.
        A randomized trial of a telephone-delivered exercise intervention for non-urban dwelling women newly diagnosed with breast cancer: exercise for health.
        Ann Behav Med. 2012; 43: 229-238
        • Anderson R.T.
        • Kimmick G.G.
        • McCoy T.P.
        • et al.
        A randomized trial of exercise on well-being and function following breast cancer surgery: the RESTORE trial.
        J Cancer Surviv. 2012; 6: 172-181
        • Cantarero-Villanueva I.
        • Fernández-Lao C.
        • Del Moral-Avila R.
        • Fernández-de-Las-Peñas C.
        • Feriche-Fernández-Castanys M.B.
        • Arroyo-Morales M.
        Effectiveness of core stability exercises and recovery myofascial release massage on fatigue in breast cancer survivors: a randomized controlled clinical trial.
        Evid Based Complement Alternat Med. 2012; : 620619
        • Cornette T.
        • Vincent F.
        • Mandigout S.
        • et al.
        Effects of home-based exercise training on Vo2 in breast cancer patients under adjuvant or neoadjuvant chemotherapy (SAPA): a randomized controlled trial.
        Eur J Phys Rehabil Med. 2016; 52: 223-232
        • De Luca V.
        • Minganti C.
        • Borrione P.
        • et al.
        Effects of concurrent aerobic and strength training on breast cancer survivors: a pilot study.
        Public Health. 2016; 136: 126-132
        • Dethlefsen C.
        • Lillelund C.
        • Midtgaard J.
        • et al.
        Exercise regulates breast cancer cell viability: systemic training adaptations versus acute exercise responses.
        Breast Cancer Res Treat. 2016; 159: 469-479
        • Fernández-Lao C.
        • Cantarero-Villanueva I.
        • Ariza-Garcia A.
        • et al.
        Water versus land-based multimodal exercise program effects on body composition in breast cancer survivors: a controlled clinical trial.
        Support Care Cancer. 2013; 21: 521-530
        • Hatchett A.
        • Hallam J.S.
        • Ford M.A.
        Evaluation of a social cognitive theory-based email intervention designed to influence the physical activity of survivors of breast cancer.
        Psychooncology. 2013; 22: 829-836
        • Herrero F.
        • San Juan A.F.
        • Fleck S.J.
        • et al.
        Combined aerobic and resistance training in breast cancer survivors: A randomized, controlled pilot trial.
        Int J Sports Med. 2006; 27: 573-580
        • Husebø A.M.L.
        • Dyrstad S.M.
        • Mjaaland I.
        • Søreide J.A.
        • Bru E.
        Effects of scheduled exercise on cancer-related fatigue in women with early breast cancer.
        Sci World J. 2014; 9: 271828
        • Hutnick N.A.
        • Williams N.I.
        • Kraemer W.J.
        • et al.
        Exercise and lymphocyte activation following chemotherapy for breast cancer.
        Med Sci Sports Exerc. 2005; 37: 1827-1835
        • Ligibel J.A.
        • Campbell N.
        • Partridge A.
        • et al.
        Impact of a mixed strength and endurance exercise intervention on insulin levels in breast cancer survivors.
        J Clin Oncol. 2008; 26: 907-912
        • Maryam A.
        • Fazlollah A.
        • Eesa M.
        • Ebrahim H.
        • Abbas V.F.
        The effect of designed exercise programme on quality of life in women with breast cancer receiving chemotherapy.
        Scand J Caring Sci. 2010; 24: 251-258
        • Milne H.M.
        • Wallman K.E.
        • Gordon S.
        • Courneya K.S.
        Effects of a combined aerobic and resistance exercise program in breast cancer survivors: a randomized controlled trial.
        Breast Cancer Res Treat. 2008; 108: 279-288
        • Naumann F.
        • Munro A.
        • Martin E.
        • et al.
        An individual-based versus group-based exercise and counselling intervention for improving quality of life in breast cancer survivors: a feasibility and efficacy study.
        Psychooncology. 2012; 21: 1136-1139
        • van Waart H.
        • Stuiver M.M.
        • van Harten W.H.
        • et al.
        Effect of low-intensity physical activity and moderate-to high-intensity physical exercise during adjuvant chemotherapy on physical fitness, fatigue, and chemotherapy completion rates: results of the PACES randomized clinical trial.
        J Clin Oncol. 2015; 33: 1918-1927
        • Galiano-Castillo N.
        • Cantarero-Villanueva I.
        • Fernández-Lao C.
        • et al.
        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. 2016; 122: 3166-3174
        • Short C.E.
        • James E.L.
        • Girgis A.
        • D'Souza M.I.
        • Plotnikoff R.C.
        Main outcomes of the move more for life trial: a randomised controlled trial examining the effects of tailored-print and targeted-print materials for promoting physical activity among post-treatment breast cancer survivors.
        Psychooncology. 2015; 24: 771-778
        • Ahmed R.L.
        • Thomas W.
        • Yee D.
        • Schmitz K.H.
        Randomized controlled trial of weight training and lymphedema in breast cancer survivors.
        J Clin Oncol. 2006; 24: 2765-2772
        • Kilbreath S.L.
        • Refshauge K.M.
        • Beith J.M.
        • et al.
        Upper limb progressive resistance training and stretching exercises following surgery for early breast cancer: a randomized controlled trial.
        Breast Cancer Res Treat. 2012; 133: 667-676
        • Schmidt M.E.
        • Wiskemann J.
        • Armbrust P.
        • et al.
        Effects of resistance exercise on fatigue and quality of life in breast cancer patients undergoing adjuvant chemotherapy: a randomized controlled trial.
        Int J Cancer. 2015; 137: 471-480
        • Winters-Stone K.M.
        • Dobek J.
        • Nail L.M.
        • 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: 1637-1646
        • Banerjee B.
        • Vadiraj H.S.
        • Ram A.
        • et al.
        Effects of an integrated yoga program in modulating psychological stress and radiation-induced genotoxic stress in breast cancer patients undergoing radiotherapy.
        Integr Cancer Ther. 2007; 6: 242-250
        • Cantarero-Villanueva I.
        • Fernández-Lao C.
        • Caro-Morán E.
        • et al.
        Aquatic exercise in a chest-high pool for hormone therapy-induced arthralgia in breast cancer survivors: a pragmatic controlled trial.
        Clin Rehabil. 2013; 27: 123-132
        • Cantarero-Villanueva I.
        • Fernández-Lao C.
        • Cuesta-Vargas A.I.
        • et al.
        The effectiveness of a deep water aquatic exercise program in cancer-related fatigue in breast cancer survivors: a randomized controlled trial.
        Arch Phys Med Rehabil. 2013; 94: 221-230
        • Cantarero-Villanueva I.
        • Fernández-Lao C.
        • Fernández-de-Las-Peñas C.
        • et al.
        Effectiveness of water physical therapy on pain, pressure pain sensitivity, and myofascial trigger points in breast cancer survivors: a randomized, controlled clinical trial.
        Pain Med. 2012; 13: 1509-1519
        • Chandwani K.D.
        • Perkins G.
        • Nagendra H.R.
        • et al.
        Randomized, controlled trial of yoga in women with breast cancer undergoing radiotherapy.
        J Clin Oncol. 2014; 32: 1058-1065
        • Danhauer S.C.
        • Mihalko S.L.
        • Russell G.B.
        • et al.
        Restorative yoga for women with breast cancer: findings from a randomized pilot study.
        Psychooncology. 2009; 18: 360-368
        • Loudon A.
        • Barnett T.
        • Piller N.
        • Immink M.A.
        • Williams A.D.
        Yoga management of breast cancer-related lymphoedema: a randomised controlled pilot-trial.
        BMC Complement Altern Med. 2013; 14: 214
        • Moadel A.B.
        • Shah C.
        • Wylie-Rosett J.
        • et al.
        Randomized controlled trial of yoga among a multiethnic sample of breast cancer patients: effects on quality of life.
        J Clin Oncol. 2007; 25: 4387-4395
        • Courneya K.S.
        • Segal R.J.
        • Mackey J.R.
        • et al.
        Effects of aerobic and resistance exercise in breast cancer patients receiving adjuvant chemotherapy: a multicenter randomized controlled trial.
        J Clin Oncol. 2007; 25: 4396-4404
        • Musanti R.
        A study of exercise modality and physical self-esteem in breast cancer survivors.
        Med Sci Sports Exerc. 2012; 44: 352-361
        • Schwartz A.L.
        • Winters-Stone K.
        • Gallucci B.
        Exercise effects on bone mineral density in women with breast cancer receiving adjuvant chemotherapy.
        Oncol Nurs Forum. 2007; 34: 627-633
        • Zeng Y.
        • Huang M.
        • Cheng A.S.
        • Zhou Y.
        • So W.K.
        Meta-analysis of the effects of exercise intervention on quality of life in breast cancer survivors.
        Breast Cancer. 2014; 21: 262-274
        • Duijts S.F.
        • Faber M.M.
        • Oldenburg H.S.
        • van Beurden M.
        • Aaronson N.K.
        Effectiveness of behavioral techniques and physical exercise on psychosocial functioning and health-related quality of life in breast cancer patients and survivors—a meta-analysis.
        Psychooncology. 2011; 20: 115-126
        • Lipsett A.
        • Barrett S.
        • Haruna F.
        • Mustian K.
        • O'Donovan A.
        The impact of exercise during adjuvant radiotherapy for breast cancer on fatigue and quality of life: a systematic review and meta-analysis.
        Breast. 2017; 32: 144-155
        • Carayol M.
        • Bernard P.
        • Boiché J.
        • et al.
        Psychological effect of exercise in women with breast cancer receiving adjuvant therapy: what is the optimal dose needed?.
        Ann Oncol. 2013; 24: 291-300
        • Juvet L.K.
        • Thune I.
        • Elvsaas I.K.Ø.
        • et al.
        The effect of exercise on fatigue and physical functioning in breast cancer patients during and after treatment and at 6 months follow-up: a meta-analysis.
        Breast. 2017; 33: 166-177
        • van Vulpen J.K.
        • Peeters P.H.
        • Velthuis M.J.
        • van der Wall E.
        • May A.M.
        Effects of physical exercise during adjuvant breast cancer treatment on physical and psychosocial dimensions of cancer-related fatigue: a meta-analysis.
        Maturitas. 2016; 85: 104-111
        • Kim C.
        • Kang D.
        • Park J.
        A meta-analysis of aerobic exercise interventions for women with breast cancer.
        West J Nurs Res. 2009; 31: 437-461
        • Massie M.J.
        Prevalence of depression in patients with cancer.
        J Natl Cancer Inst Monogr. 2004; 32: 57-71
        • Mishra S.I.
        • Scherer R.W.
        • Snyder C.
        • et al.
        Exercise interventions on health-related quality of life for people with cancer during active treatment.
        Cochrane Database Syst Rev. 2012; 8Cd008465
        • McCaskill-Stevens W.
        • Abrams J.S.
        Comorbidities in the aging breast cancer population: are current assessments leading to improved outcomes?.
        J Natl Cancer Inst. 2011; 103: 1072-1073
        • Schmitz K.H.
        • Speck R.M.
        • Rye S.A.
        • DiSipio T.
        • Hayes S.C.
        Prevalence of breast cancer treatment sequelae over 6 years of follow-up: the pulling through study.
        Cancer. 2012; 118: 2217-2225
        • Branstrom R.
        • Petersson L.M.
        • Saboonchi F.
        • et al.
        Physical activity following a breast cancer diagnosis: Implications for self-rated health and cancer-related symptoms.
        Eur J Oncol Nurs. 2015; 19: 680-685
        • Schmitz K.H.
        • Courneya K.S.
        • Matthews C.
        • et al.
        American College of Sports Medicine roundtable on exercise guidelines for cancer survivors.
        Med Sci Sports Exerc. 2010; 42: 1409-1426