Exercise and other non-pharmaceutical interventions for cancer-related fatigue in patients during or after cancer treatment: a systematic review incorporating an indirect-comparisons meta-analysis
Roger Hilfiker, Andre Meichtry, Manuela Eicher, Lina Nilsson Balfe, Ruud H Knols, Martin L Verra, Jan Taeymans, Roger Hilfiker, Andre Meichtry, Manuela Eicher, Lina Nilsson Balfe, Ruud H Knols, Martin L Verra, Jan Taeymans
Abstract
Aim: To assess the relative effects of different types of exercise and other non-pharmaceutical interventions on cancer-related fatigue (CRF) in patients during and after cancer treatment.
Design: Systematic review and indirect-comparisons meta-analysis.
Data sources: Articles were searched in PubMed, Cochrane CENTRAL and published meta-analyses.
Eligibility criteria for selecting studies: Randomised studies published up to January 2017 evaluating different types of exercise or other non-pharmaceutical interventions to reduce CRF in any cancer type during or after treatment.
Study appraisal and synthesis: Risk of bias assessment with PEDro criteria and random effects Bayesian network meta-analysis.
Results: We included 245 studies. Comparing the treatments with usual care during cancer treatment, relaxation exercise was the highest ranked intervention with a standardisedmean difference (SMD) of -0.77 (95% Credible Interval (CrI) -1.22 to -0.31), while massage (-0.78; -1.55 to -0.01), cognitive-behavioural therapy combined with physical activity (combined CBT, -0.72; -1.34 to -0.09), combined aerobic and resistance training (-0.67; -1.01 to -0.34), resistance training (-0.53; -1.02 to -0.03), aerobic (-0.53; -0.80 to -0.26) and yoga (-0.51; -1.01 to 0.00) all had moderate-to-large SMDs. After cancer treatment, yoga showed the highest effect (-0.68; -0.93 to -0.43). Combined aerobic and resistance training (-0.50; -0.66 to -0.34), combined CBT (-0.45; -0.70 to -0.21), Tai-Chi (-0.45; -0.84 to -0.06), CBT (-0.42; -0.58 to -0.25), resistance training (-0.35; -0.62 to -0.08) and aerobic (-0.33; -0.51 to -0.16) showed all small-to-moderate SMDs.
Conclusions: Patients can choose among different effective types of exercise and non-pharmaceutical interventions to reduce CRF.
Keywords: cancer related fatigue; exercise; indirect comparison meta-analysis.; network meta-analysis; non-pharmaceutical interventions.
Conflict of interest statement
Competing interests: None declared.
© Article author(s) (or their employer(s) unless otherwise stated in the text of the article) 2018. All rights reserved. No commercial use is permitted unless otherwise expressly granted.
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References
- NCCN NCCN. Cancer-Related Fatigue : Network N, NCCN clinical practice guidelines in oncology (NCCN guidelines). Version 1. 2016 ed: NCCN National Comprehensive Cancer Network, 2016:1–56.
- Lawrence DP, Kupelnick B, Miller K, et al. . Evidence report on the occurrence, assessment, and treatment of fatigue in cancer patients. J Natl Cancer Inst Monogr 2004;32:40–50. 10.1093/jncimonographs/lgh027
- Hickok JT, Roscoe JA, Morrow GR, et al. . Frequency, severity, clinical course, and correlates of fatigue in 372 patients during 5 weeks of radiotherapy for cancer. Cancer 2005;104:1772–8. 10.1002/cncr.21364
- Phillips SM, McAuley E. Physical activity and fatigue in breast cancer survivors: a panel model examining the role of self-efficacy and depression. Cancer Epidemiol Biomarkers Prev 2013;22:773–81. 10.1158/1055-9965.EPI-12-0983
- Bower JE. Cancer-related fatigue-mechanisms, risk factors, and treatments. Nat Rev Clin Oncol 2014;11:597–609. 10.1038/nrclinonc.2014.127
- Bower JE, Ganz PA, Desmond KA, et al. . Fatigue in breast cancer survivors: occurrence, correlates, and impact on quality of life. J Clin Oncol 2000;18:743–53. 10.1200/JCO.2000.18.4.743
- Cella D, Davis K, Breitbart W, et al. ; Fatigue Coalition. Cancer-related fatigue: prevalence of proposed diagnostic criteria in a United States sample of cancer survivors. J Clin Oncol 2001;19:3385–91. 10.1200/JCO.2001.19.14.3385
- Minton O, Stone P, Richardson A, et al. . Drug therapy for the management of cancer related fatigue. Cochrane Database Syst Rev 2008;1:CD006704.
- Curt GA. The impact of fatigue on patients with cancer: overview of FATIGUE 1 and 2. Oncologist 2000;5(Suppl 2):9–12. 10.1634/theoncologist.5-suppl_2-9
- Eickmeyer SM, Gamble GL, Shahpar S, et al. . The role and efficacy of exercise in persons with cancer. Pm R 2012;4:874–81. 10.1016/j.pmrj.2012.09.588
- Saligan LN, Olson K, Filler K, et al. ; Multinational Association of Supportive Care in Cancer Fatigue Study Group-Biomarker Working Group. The biology of cancer-related fatigue: a review of the literature. Support Care Cancer 2015;23:2461–78. 10.1007/s00520-015-2763-0
- Meneses-Echávez JF, González-Jiménez E, Ramírez-Vélez R. Effects of supervised multimodal exercise interventions on cancer-related fatigue: systematic review and meta-analysis of randomized controlled trials. Biomed Res Int 2015;2015:1–13. 10.1155/2015/328636
- Meneses-Echávez JF, González-Jiménez E, Ramírez-Vélez R. Supervised exercise reduces cancer-related fatigue: a systematic review. J Physiother 2015;61:3–9. 10.1016/j.jphys.2014.08.019
- Tian L, Lu HJ, Lin L, et al. . Effects of aerobic exercise on cancer-related fatigue: a meta-analysis of randomized controlled trials. Support Care Cancer 2016;24:969–83. 10.1007/s00520-015-2953-9
- Cramer H, Lauche R, Klose P, et al. . A systematic review and meta-analysis of exercise interventions for colorectal cancer patients. Eur J Cancer Care 2014;23:3–14. 10.1111/ecc.12093
- Zhang J, Yang KH, Tian JH, et al. . Effects of yoga on psychologic function and quality of life in women with breast cancer: a meta-analysis of randomized controlled trials. J Altern Complement Med 2012;18:994–1002. 10.1089/acm.2011.0514
- Fong DY, Ho JW, Hui BP, et al. . Physical activity for cancer survivors: meta-analysis of randomised controlled trials. BMJ 2012;344:e70 10.1136/bmj.e70
- Fitch MI. Systematic review and meta-analysis of the correlates of cancer-related fatigue. Evid Based Nurs 2012;15:108–9. 10.1136/ebnurs-2012-100688
- Buffart LM, van Uffelen JG, et al. , Riphagen II. Physical and psychosocial benefits of yoga in cancer patients and survivors, a systematic review and meta-analysis of randomized controlled trials. BMC Cancer 2012;12:559 10.1186/1471-2407-12-559
- Oh HS, Seo WS. Systematic review and meta-analysis of the correlates of cancer-related fatigue. Worldviews Evid Based Nurs 2011;8:191–201. 10.1111/j.1741-6787.2011.00214.x
- Velthuis MJ, Agasi-Idenburg SC, Aufdemkampe G, et al. . The effect of physical exercise on cancer-related fatigue during cancer treatment: a meta-analysis of randomised controlled trials. Clin Oncol 2010;22:208–21. 10.1016/j.clon.2009.12.005
- Jacobsen PB, Donovan KA, Vadaparampil ST, et al. . Systematic review and meta-analysis of psychological and activity-based interventions for cancer-related fatigue. Health Psychol 2007;26:660–7. 10.1037/0278-6133.26.6.660
- Du S, Hu L, Dong J, et al. . Patient education programs for cancer-related fatigue: a systematic review. Patient Educ Couns 2015;98:1308–19. 10.1016/j.pec.2015.05.003
- Hasenoehrl T, Keilani M, Sedghi Komanadj T, et al. . The effects of resistance exercise on physical performance and health-related quality of life in prostate cancer patients: a systematic review. Support Care Cancer 2015;23:2479–97. 10.1007/s00520-015-2782-x
- Bradt J, Goodill SW, Dileo C. Dance/movement therapy for improving psychological and physical outcomes in cancer patients. Cochrane Database Syst Rev 2011;10:CD007103 10.1002/14651858.CD007103.pub2
- Bradt J, Dileo C, Grocke D, et al. . Music interventions for improving psychological and physical outcomes in cancer patients. Cochrane Database Syst Rev 2011;8:CD006911 10.1002/14651858.CD006911.pub2
- Bergenthal N, Will A, Streckmann F, et al. . Aerobic physical exercise for adult patients with haematological malignancies. Cochrane Database Syst Rev 2014;11:CD009075 10.1002/14651858.CD009075.pub2
- Tomlinson D, Diorio C, Beyene J, et al. . Effect of exercise on cancer-related fatigue: a meta-analysis. Am J Phys Med Rehabil 2014;93:675–86. 10.1097/PHM.0000000000000083
- Galvão DA, Taaffe DR, Spry N, et al. . Exercise can prevent and even reverse adverse effects of androgen suppression treatment in men with prostate cancer. Prostate Cancer Prostatic Dis 2007;10:340–6. 10.1038/sj.pcan.4500975
- Baumann FT, Zopf EM, Bloch W. Clinical exercise interventions in prostate cancer patients--a systematic review of randomized controlled trials. Support Care Cancer 2012;20:221–33. 10.1007/s00520-011-1271-0
- Zou LY, Yang L, He XL, Xl H, et al. . Effects of aerobic exercise on cancer-related fatigue in breast cancer patients receiving chemotherapy: a meta-analysis. Tumour Biol 2014;35:5659–67. 10.1007/s13277-014-1749-8
- Shennan C, Payne S, Fenlon D. What is the evidence for the use of mindfulness-based interventions in cancer care? A review. Psychooncology 2011;20:681–97. 10.1002/pon.1819
- Tsai HF, Chen YR, Chung MH, et al. . Effectiveness of music intervention in ameliorating cancer patients' anxiety, depression, pain, and fatigue: a meta-analysis. Cancer Nurs 2014;37:E35–E50. 10.1097/NCC.0000000000000116
- Mishra SI, Scherer RW, Snyder C, et al. . Exercise interventions on health-related quality of life for people with cancer during active treatment. Clin Otolaryngol 2012;37:390–2. 10.1111/coa.12015
- Mishra SI, Scherer RW, Snyder C, et al. . The effectiveness of exercise interventions for improving health-related quality of life from diagnosis through active cancer treatment. Oncol Nurs Forum 2015;42:E33–E53. 10.1188/15.ONF.E33-E53
- Mishra SI, Scherer RW, Snyder C, et al. . Are exercise programs effective for improving health-related quality of life among cancer survivors? A systematic review and meta-analysis. Oncol Nurs Forum 2014;41:E326–E342. 10.1188/14.ONF.E326-E342
- Mishra SI, Scherer RW, Geigle PM, et al. . Exercise interventions on health-related quality of life for cancer survivors. Cochrane Database Syst Rev 2012;8:CD007566.
- Carayol M, Delpierre C, Bernard P, et al. . Population-, intervention- and methodology-related characteristics of clinical trials impact exercise efficacy during adjuvant therapy for breast cancer: a meta-regression analysis. Psychooncology 2015;24:737–47. 10.1002/pon.3727
- 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. 10.1093/annonc/mds342
- Pan Y, Yang K, Shi X, et al. . Tai Chi Chuan exercise for patients with breast cancer: a systematic review and meta-analysis. Evid Based Complement Alternat Med 2015;2015:1–15. 10.1155/2015/535237
- Pan YQ, Yang KH, Wang YL, et al. . Massage interventions and treatment-related side effects of breast cancer: a systematic review and meta-analysis. Int J Clin Oncol 2014;19:829–41. 10.1007/s10147-013-0635-5
- Goedendorp MM, Gielissen MF, Verhagen CA, et al. . Psychosocial interventions for reducing fatigue during cancer treatment in adults. Cochrane Database Syst Rev 2009;1:CD006953 10.1002/14651858.CD006953.pub2
- Brown JC, Huedo-Medina TB, Pescatello LS, et al. . Efficacy of exercise interventions in modulating cancer-related fatigue among adult cancer survivors: a meta-analysis. Cancer Epidemiol Biomarkers Prev 2011;20:123–33. 10.1158/1055-9965.EPI-10-0988
- Bourke L, Smith D, Steed L, et al. . Exercise for men with prostate cancer: a systematic review and Meta-analysis. Eur Urol 2016;69:693–703. 10.1016/j.eururo.2015.10.047
- Mitchell SA, Hoffman AJ, Clark JC, et al. . Putting evidence into practice: an update of evidence-based interventions for cancer-related fatigue during and following treatment. Clin J Oncol Nurs 2014;(18 Suppl):38–58. 10.1188/14.CJON.S3.38-58
- Uthman OA, van der Windt DA, Jordan JL, et al. . Exercise for lower limb osteoarthritis: systematic review incorporating trial sequential analysis and network meta-analysis. Br J Sports Med 2014;48:1579 10.1136/bjsports-2014-5555rep
- Hutton B, Salanti G, Caldwell DM, et al. . The PRISMA extension statement for reporting of systematic reviews incorporating network meta-analyses of health care interventions: checklist and explanations. Ann Intern Med 2015;162:777–84. 10.7326/M14-2385
- Higgins JPT, Green S. Cochrane handbook for systematic reviews of interventions, 2011.
- Egger M, Davey Smith G, Schneider M, et al. . Bias in meta-analysis detected by a simple, graphical test. Bmj 1997;315:629–34. 10.1136/bmj.315.7109.629
- Borenstein M, Hedges LV, Higgins JPT, et al. . Introduction to Meta-Analysis. Chichester, West Sussex: John Wiley & Sons Ltd, 2009.
- Cohen J. A power primer. Psychol Bull 1992;112:155–9. 10.1037/0033-2909.112.1.155
- R Foundation for Statistical Computing. R: a language and environment for statistical computing [program], 2015.
- gemtc. Network Meta-Analysis using bayesian methods. 2015. R-package [program]. 0.7-1 version.
- rjags. Bayesian graphical models using MCMC, 2015. R package [program]. 4-4 version.
- Salanti G, Ades AE, Ioannidis JP. Graphical methods and numerical summaries for presenting results from multiple-treatment meta-analysis: an overview and tutorial. J Clin Epidemiol 2011;64:163–71. 10.1016/j.jclinepi.2010.03.016
- van Valkenhoef G, Dias S, Ades AE, et al. . Automated generation of node-splitting models for assessment of inconsistency in network meta-analysis. Res Synth Methods 2016;7:80–93. 10.1002/jrsm.1167
- Dechartres A, Trinquart L, Boutron I, et al. . Influence of trial sample size on treatment effect estimates: meta-epidemiological study. BMJ 2013;346:f2304 10.1136/bmj.f2304
- Vargas S, Antoni MH, Carver CS, et al. . Sleep quality and fatigue after a stress management intervention for women with early-stage breast cancer in southern Florida. Int J Behav Med 2014;21:971–81. 10.1007/s12529-013-9374-2
- Meneses-Echávez JF, González-Jiménez E, Ramírez-Vélez R. Effects of supervised multimodal exercise interventions on Cancer-Related fatigue: systematic review and Meta-Analysis of randomized controlled trials. Biomed Res Int 2015;2015 10.1155/2015/328636
- NCCN NCCN. Cancer-Related Fatigue : Network N, NCCN clinical practice guidelines in oncology (NCCN guidelines: NCCN National Comprehensive Cancer Network, 2015:1–45.
- Sharma A, Madaan V, Petty FD. Exercise for mental health. Prim Care Companion J Clin Psychiatry 2006;8:106 10.4088/PCC.v08n0208a
- Li AW, Goldsmith CA. The effects of yoga on anxiety and stress. Altern Med Rev 2012;17:21–35.
- Jones LW, Courneya KS, Peddle C, et al. . Oncologists' opinions towards recommending exercise to patients with cancer: a Canadian national survey. Support Care Cancer 2005;13:929–37. 10.1007/s00520-005-0805-8
- Jones LW, Courneya KS. Exercise discussions during cancer treatment consultations. Cancer Pract 2002;10:66–74. 10.1046/j.1523-5394.2002.102004.x
- Jones LW, Courneya KS. Exercise counseling and programming preferences of cancer survivors. Cancer Pract 2002;10:208–15. 10.1046/j.1523-5394.2002.104003.x
- Courneya KS, Segal RJ, Reid RD, et al. . Three independent factors predicted adherence in a randomized controlled trial of resistance exercise training among prostate cancer survivors. J Clin Epidemiol 2004;57:571–9. 10.1016/j.jclinepi.2003.11.010
- Koelwyn GJ, Wennerberg E, Demaria S, et al. . Exercise in regulation of Inflammation-Immune Axis function in Cancer initiation and progression. Oncology 2015;29.
Source: PubMed