Abstract
Objectives
The primary purpose of this systematic review is to structure the available evidence concerning physical exercise programs and their effects on (1) physical performance outcomes, (2) experienced fatigue, and (3) quality of life (QoL) in patients during the initial treatment for breast cancer.
Data sources
A systematic literature search, based upon the PRISMA guideline, up to January 1, 2018, was performed using four databases (Web of Science, Cochrane Library for Clinical Trials, PubMed, and Medline).
Study selection
Inclusion criteria were as follows: (1) adults > 18 years; (2) patients with breast cancer undergoing initial treatment; (3) interventions with the aim to influence the patient’s physical activity, QoL, or fatigue; (4) randomized controlled trials (RCTs) of all ages. The selected studies were scored for methodological quality, and data concerning physical performance, QoL, and fatigue were extracted. Twenty-eight RCTs were included.
Data extraction
Different treatment modalities during initial treatment were identified (radiation therapy, chemotherapy, and combination therapy), as well as different types of physical training interventions (cardiovascular endurance exercise, strengthening programs, or a combination of both). Therefore, the results were clustered with regard to the above-mentioned grouping; extracting every relevant outcome related to physical performance (6 MWT or VO2peak; grip/muscle strength), QoL (questionnaires), and fatigue (questionnaires).
Data synthesis
Different training programs (endurance, resistance, or a combination of both) were found. These programs were applied during different phases of initial treatment. Some programs were supervised while others were home based. Overall, most training interventions provided an improvement in physical performance and a decrease in perceived fatigue. QoL was the outcome variable least susceptible to improvement.
Conclusion
Different types of exercise programs are available for rehabilitation purposes of breast cancer patients during adjuvant therapy. Overall resistance training or resistance training in combination with CV endurance training provides the best results, especially on physical performance and perceived fatigue.
Similar content being viewed by others
Abbreviations
- QoL:
-
quality of life
- 6 MWT:
-
6-min walking test
- 12 MWT:
-
12-min walking test
- CT:
-
chemotherapy
- RT:
-
radiation therapy
- ADL:
-
activities of daily living
- VO2peak :
-
peak oxygen uptake
- 1 RM:
-
one repetition maximum
- CV:
-
cardiovascular
References
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359–E386
Kootstra JJ, Hoekstra-Weebers JE, Rietman JS, de Vries J, Baas PC, Geertzen JH et al (2010) A longitudinal comparison of arm morbidity in stage I-II breast cancer patients treated with sentinel lymph node biopsy, sentinel lymph node biopsy followed by completion lymph node dissection, or axillary lymph node dissection. Ann Surg Oncol 17:2384–2394
Juvet LK, Thune I, Elvsaas IKO, Fors EA, Lundgren S, Bertheussen G, Leivseth G, Oldervoll LM (2017) 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 33:166–177
Christiansen P, Carstensen SL, Ejlertsen B, Kroman N, Offersen B, Bodilsen A, Jensen MB (2018) Breast conserving surgery versus mastectomy: overall and relative survival-a population based study by the Danish Breast Cancer Cooperative Group (DBCG). Acta Oncol 57:19–25
Eggemann H, Altmann U, Costa SD, Ignatov A (2018) Survival benefit of tamoxifen and aromatase inhibitor in male and female breast cancer. J Cancer Res Clin Oncol 144:337–341
Kast K, Schoffer O, Link T, Forberger A, Petzold A, Niedostatek A, Werner C, Klug SJ, Werner A, Gatzweiler A, Richter B, Baretton G, Wimberger P (2017) Trastuzumab and survival of patients with metastatic breast cancer. Arch Gynecol Obstet 296:303–312
Roberts MC, Miller DP, Shak S, Petkov VI (2017) Breast cancer-specific survival in patients with lymph node-positive hormone receptor-positive invasive breast cancer and Oncotype DX Recurrence Score results in the SEER database. Breast Cancer Res Treat 163:303–310
Yoon TI, Hwang UK, Kim ET, Lee S, Sohn G, Ko BS, Lee JW, Son BH, Kim S, Ahn SH, Kim HJ (2017) Survival improvement in hormone-responsive young breast cancer patients with endocrine therapy. Breast Cancer Res Treat 165:311–320
Allemani C, Weir HK, Carreira H, Harewood R, Spika D, Wang XS, Bannon F, Ahn JV, Johnson CJ, Bonaventure A, Marcos-Gragera R, Stiller C, Azevedo e Silva G, Chen WQ, Ogunbiyi OJ, Rachet B, Soeberg MJ, You H, Matsuda T, Bielska-Lasota M, Storm H, Tucker TC, Coleman MP, CONCORD Working Group (2015) Global surveillance of cancer survival 1995-2009: analysis of individual data for 25,676,887 patients from 279 population-based registries in 67 countries (CONCORD-2). Lancet 385:977–1010
De Angelis R, Sant M, Coleman MP, Francisci S, Baili P, Pierannunzio D et al (2014) Cancer survival in Europe 1999-2007 by country and age: results of EUROCARE--5-a population-based study. Lancet Oncol 15:23–34
Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H et al (2013) Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer 49:1374–1403
Dean A (2008) Primary breast cancer: risk factors, diagnosis and management. Nurs Stand 22:9
Van de Wiel M, Dockx Y, Van den Wyngaert T, Stroobants S, Tjalma WAA, Huizing MT (2017) Neoadjuvant systemic therapy in breast cancer: challenges and uncertainties. Eur J Obstet Gynecol Reprod Biol 210:144–156
Diaby V, Tawk R, Sanogo V, Xiao H, Montero AJ (2015) A review of systematic reviews of the cost-effectiveness of hormone therapy, chemotherapy, and targeted therapy for breast cancer. Breast Cancer Res Treat 151:27–40
Bengala C, Zamagni C, Pedrazzoli P, Matteucci P, Ballestrero A, Da Prada G et al (2006) Cardiac toxicity of trastuzumab in metastatic breast cancer patients previously treated with high-dose chemotherapy: a retrospective study. Br J Cancer 94:1016–1020
DiSipio T, Rye S, Newman B, Hayes S (2013) Incidence of unilateral arm lymphoedema after breast cancer: a systematic review and meta-analysis. Lancet Oncol 14:500–515
Adamsen L, Quist M, Andersen C, Møller T, Herrstedt J, Kronborg D et al (2009) Effect of a multimodal high intensity exercise intervention in cancer patients undergoing chemotherapy: randomised controlled trial. BMJ 339:b3410
Kim CJ, Kang DH, Smith BA, Landers KA (2006) Cardiopulmonary responses and adherence to exercise in women newly diagnosed with breast cancer undergoing adjuvant therapy. Cancer Nurs 29:156–165
Ligibel JA, Giobbie-Hurder A, Shockro L, Campbell N, Partridge AH, Tolaney SM, Lin NU, Winer EP (2016) Randomized trial of a physical activity intervention in women with metastatic breast cancer. Cancer 122:1169–1177
Henneghan A (2016) Modifiable factors and cognitive dysfunction in breast cancer survivors: a mixed-method systematic review. Support Care Cancer 24:481–497
Morean DF, O’Dwyer L, Cherney LR (2015) Therapies for cognitive deficits associated with chemotherapy for breast cancer: a systematic review of objective outcomes. Arch Phys Med Rehabil 96:1880–1897
Heim ME, v d Malsburg ML, Niklas A (2007) Randomized controlled trial of a structured training program in breast cancer patients with tumor-related chronic fatigue. Onkologie 30:429–434
Headley JA, Ownby KK, John LD (2004) The effect of seated exercise on fatigue and quality of life in women with advanced breast cancer. Oncol Nurs Forum 31:977–983
Hwang JH, Chang HJ, Shim YH, Park WH, Park W, Huh SJ, Yang JH (2008) Effects of supervised exercise therapy in patients receiving radiotherapy for breast cancer. Yonsei Med J 49:443–450
Husebo AM, Dyrstad SM, Mjaaland I, Soreide JA, Bru E (2014) Effects of scheduled exercise on cancer-related fatigue in women with early breast cancer. ScientificWorldJournal 2014:271828
Lipsett A, Barrett S, Haruna F, Mustian K, O’Donovan A (2017) The impact of exercise during adjuvant radiotherapy for breast cancer on fatigue and quality of life: a systematic review and meta-analysis. Breast 32:144–155
Mock V, Frangakis C, Davidson NE, Ropka ME, Pickett M, Poniatowski B, Stewart KJ, Cameron L, Zawacki K, Podewils LJ, Cohen G, McCorkle R (2005) Exercise manages fatigue during breast cancer treatment: a randomized controlled trial. Psycho-Oncology 14:464–477
Mock V, Burke M, Sheehan P, Creaton E, Winningham M, McKenney-Tedder S et al (1994) A nursing rehabilitation program for women with breast cancer receiving adjuvant chemotherapy. Oncol Nurs Forum 21:899–907 discussion 8
Zeng Y, Huang M, Cheng AS, Zhou Y, So WK (2014) Meta-analysis of the effects of exercise intervention on quality of life in breast cancer survivors. Breast Cancer 21:262–274
Lahart IM, Metsios GS, Nevill AM, Carmichael AR (2018) Physical activity for women with breast cancer after adjuvant therapy. Cochrane Database Syst Rev 1:CD011292
Battaglini C, Mihalik J, Bottaro M, Dennehy C, Petschauer M, Hairston L et al (2008) Effect of exercise on the caloric intake of breast cancer patients undergoing treatment. Braz J Med Biol Res 41:709–715
Mutrie N, Campbell AM, Whyte F, McConnachie A, Emslie C, Lee L, Kearney N, Walker A, Ritchie D (2007) Benefits of supervised group exercise programme for women being treated for early stage breast cancer: pragmatic randomised controlled trial. Bmj 334:517
Haines TP, Sinnamon P, Wetzig NG, Lehman M, Walpole E, Pratt T, Smith A (2010) Multimodal exercise improves quality of life of women being treated for breast cancer, but at what cost? Randomized trial with economic evaluation. Breast Cancer Res Treat 124:163–175
Courneya KS, Segal RJ, Gelmon K, Reid RD, Mackey JR, Friedenreich CM, Proulx C, Lane K, Ladha AB, Vallance JK, Liu Q, Yasui Y, McKenzie DC (2007) Six-month follow-up of patient-rated outcomes in a randomized controlled trial of exercise training during breast cancer chemotherapy. Cancer Epidemiol Biomark Prev 16:2572–2578
Backman M, Wengstrom Y, Johansson B, Skoldengen I, Borjesson S, Tarnbro S et al (2014) A randomized pilot study with daily walking during adjuvant chemotherapy for patients with breast and colorectal cancer. Acta Oncol 53:510–520
Campbell A, Mutrie N, White F, McGuire F, Kearney N (2005) A pilot study of a supervised group exercise programme as a rehabilitation treatment for women with breast cancer receiving adjuvant treatment. Eur J Oncol Nurs 9:56–63
Furmaniak AC, Menig M, Markes MH (2016) Exercise for women receiving adjuvant therapy for breast cancer. Cochrane Database Syst Rev 9:CD005001
Eakin EG, Lawler SP, Winkler EA, Hayes SC (2012) 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 43:229–238
Hayes SC, Rye S, Disipio T, Yates P, Bashford J, Pyke C et al (2013) 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 137:175–186
Travier N, Velthuis MJ, Bisschop CNS, van den Buijs B, Monninkhof EM, Backx F et al (2015) Effects of an 18-week exercise programme started early during breast cancer treatment: a randomised controlled trial. BMC Med 13:121
Chaoul A, Milbury K, Spelman A, Basen-Engquist K, Hall MH, Wei Q et al (2018) Randomized trial of Tibetan yoga in patients with breast cancer undergoing chemotherapy. Cancer 124:36–45
Cornette T, Vincent F, Mandigout S, Antonini MT, Leobon S, Labrunie A, Venat L, Lavau-Denes S, Tubiana-Mathieu N (2016) 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 Rehab Med 52:223–232
Dolan LB, Gelmon K, Courneya KS, Mackey JR, Segal RJ, Lane K, Reid RD, McKenzie DC (2010) Hemoglobin and aerobic fitness changes with supervised exercise training in breast cancer patients receiving chemotherapy. Cancer Epidemiol Biomark Prev 19:2826–2832
Gokal K, Wallis D, Ahmed S, Boiangiu I, Kancherla K, Munir F (2017) 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 24:1139–1166
Hornsby WE, Douglas PS, West MJ, Kenjale AA, Lane AR, Schwitzer ER, Ray KA, Herndon JE II, Coan A, Gutierrez A, Hornsby KP, Hamilton E, Wilke LG, Kimmick GG, Peppercorn JM, Jones LW (2014) Safety and efficacy of aerobic training in operable breast cancer patients receiving neoadjuvant chemotherapy: a phase II randomized trial. Acta Oncol 53:65–74
Schmidt T, Weisser B, Durkop J, Jonat W, Van Mackelenbergh M, Rocken C et al (2015) Comparing endurance and resistance training with standard care during chemotherapy for patients with primary breast cancer. Anticancer Res 35:5623–5629
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 34:627–633
Vallance J, Friedenreich C, Lavallee C, Culos-Reed N, Mackey J, Walley B et al (2017) Exploring the feasibility of a broad-reach physical activity behavior change intervention for women receiving chemotherapy for breast cancer: a randomized trial. Cancer Epidemiol Biomark Prev 25:391–398
Yang CY, Tsai JC, Huang YC, Lin CC (2011) Effects of a home-based walking program on perceived symptom and mood status in postoperative breast cancer women receiving adjuvant chemotherapy. J Adv Nurs 67:158–168
Drouin J, Armstrong H, Krause S, Orr J, Birk T, Hryniuk W. (2005) Effects of aerobic exercise training on peak aerobic capacity, fatigue, and psychological factors during radiation for breast cancer. Rehab Oncol 11–7
Milecki P, Hojan K, Ozga-Majchrzak O, Molińska-Glura M (2013) Exercise tolerance in breast cancer patients during radiotherapy after aerobic training. Contemp Oncol (Pozn) 17:205–209
Reis D, Walsh ME, Young-McCaughan S, Jones T (2013) Effects of Nia exercise in women receiving radiation therapy for breast cancer. Oncol Nurs Forum 40:E374–E381
Wiskemann J, Schmidt ME, Klassen O, Debus J, Ulrich CM, Potthoff K, Steindorf K (2017) Effects of 12-week resistance training during radiotherapy in breast cancer patients. Scand J Med Sci Sports 27:1500–1510
Funding
Funding was provided by University of Antwerp; no additional funding was requested. Prof. Gebruers received funding from IWT-TBM, grant IWT.150178. No further conflicts of interest to be declared by any of the authors.
The current review was registered on PROSPERO (www.crd.york.ac.uk/PROSPERO); registration CRD42017071940 and used the PRISMA statement for reporting the results.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors did not receive any funding for any of the steps taken to write this systematic review.
None of the authors have any conflict of interest to declare.
The data table created for this systematic review is under the control of Prof. Dr. Nick Gebruers and is available on request.
Additional information
This material was not presented anywhere thus far.
Electronic supplementary material
ESM 1
(DOC 64 kb)
Rights and permissions
About this article
Cite this article
Gebruers, N., Camberlin, M., Theunissen, F. et al. The effect of training interventions on physical performance, quality of life, and fatigue in patients receiving breast cancer treatment: a systematic review. Support Care Cancer 27, 109–122 (2019). https://doi.org/10.1007/s00520-018-4490-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00520-018-4490-9