Exercise and cancer: a position statement from the Spanish Society of Medical Oncology

M Pollán, S Casla-Barrio, J Alfaro, C Esteban, M A Segui-Palmer, A Lucia, M Martín, M Pollán, S Casla-Barrio, J Alfaro, C Esteban, M A Segui-Palmer, A Lucia, M Martín

Abstract

Due to improvements in the number of cancer survivors and survival time, there is a growing interest in healthy behaviors, such as physical activity (PA), and their potential impact on cancer- and non-cancer-related morbidity in individuals with cancer. Commissioned by the Spanish Society of Medical Oncology (SEOM), in this review, we sought to distill the most recent evidence on this topic, focusing on the mechanisms that underpin the effects of PA on cancer, the role of PA in cancer prevention and in the prognosis of cancer and practical recommendations for clinicians regarding PA counseling. Despite the available information, the introduction of exercise programs into the global management of cancer patients remains a challenge with several areas of uncertainty. Among others, the most effective behavioral interventions to achieve long-term changes in a patient's lifestyle and the optimal intensity and duration of PA should be defined with more precision in future studies.

Keywords: Cancer; Exercise; Exercise-oncology; Oncology; Physical activity.

Conflict of interest statement

MP declares that she have no conflict of interest; SC declares that she have no conflict of interest; JA received institutional research grants from Merck Serono and Novartis; CE received speaker’s honoraria from AstraZeneca, Roche, Novartis and Pfizer; MAS-P received consulting/advisory fees from AstraZeneca, Pfizer and Amgen, and speakers’ honoraria from Amgen, Roche and Pfizer; AL declares that he have no conflict of interest; MM has received research grants from Roche and Novartis, consulting/advisory fees from AstraZeneca, Amgen, Taiho Oncology, Roche/Genentech, Novartis, PharmaMar, Eli Lilly, PUMA Taiho Oncology and Pfizer, and speakers’ honoraria from AstraZeneca, Amgen, Roche/Genentech, Novartis and Pfizer.

Figures

Fig. 1
Fig. 1
Distinguishing between patients who need specialist counseling and those who do not. Adaptation to the triage model for population-based screening of cancer survivors for weight management and physical activity interventions. Modified from National Academies of Sciences, Engineering, and Medicine 2018 [149]. Set. = setting; Tr. = training of professional; LS. = level of supervision. Specialist refers to clinicians, physical therapists, occupational therapists, dieticians, and clinical exercise physiologists
Fig. 2
Fig. 2
Specialists and activities that should be developed by each specialist to achieve an adequate exercise intervention for oncologic patients while taking into account training principles adapted to exercise-oncology

References

    1. World Health Organization . Physical activity. Geneva: WHO; 2018.
    1. National Cancer Institute. Cancer survivors and physical activity. 2018. . Accessed 5 June 2019.
    1. Figueira A, Cortinhas A, Soares J, Leitão J, Ferreira R, Duarte J. Efficacy of exercise on breast cancer outcomes: a systematic review and meta-analysis of preclinical data. Int J Sports Med. 2018;39:327–342.
    1. Betof AS, Lascola CD, Weitzel D, Landon C, Scarbrough PM, Devi GR, Palmer G, Jones LW, Dewhirst MW. Modulation of murine breast tumor vascularity, hypoxia, and chemotherapeutic response by exercise. J Natl Cancer Inst. 2015;107:djv040.
    1. Jones LW, Eves N, Courneya K, Chiu B, Baracos V, Hanson J, Johnson L, Mackey J. Effects of exercise training on antitumor efficacy of doxorubicin in MDA-MB-231 breast cancer xenografts. Clin Cancer Res. 2005;11:6695–6698.
    1. Jones LW, Fels DR, West M, Allen JD, Broadwater G, Barry WT, Wilke LG, Masko E, Douglas PS, Dash RC, Povsic TJ, Peppercorn J, Marcom PK, Blackwell KL, Kimmick G, Turkington TG, Dewhirst MW. Modulation of circulating angiogenic factors and tumor biology by aerobic training in breast cancer patients receiving neoadjuvant chemotherapy. Cancer Prev Res. 2013;6:925–937.
    1. Sturgeon K, Schadler K, Muthukumaran G, Ding D, Bajulaiye A, Thomas NJ, Ferrari V, Ryeom S, Libonati JR. Concomitant low-dose doxorubicin treatment and exercise. Am J Physiol Regul Integr Comp Physiol. 2014;307:R685–R692.
    1. Ruiz-Casado A, Martín-Ruiz A, Pérez LM, Provencio M, Fiuza-Luces C, Lucia A. Exercise and the hallmarks of cancer. Trends Cancer. 2017;3:423–441.
    1. Colbert LH, Mai V, Tooze J, Perkins S, Berrigan D, Hursting S. Negative energy balance induced by voluntary wheel running inhibits polyp development in APCMin mice. Carcinogenesis. 2006;27:2103–2107.
    1. Leung P-S, Aronson WJ, Ngo TH, Golding LA, Barnard RJ. Exercise alters the IGF axis in vivo and increases p53 protein in prostate tumor cells in vitro. J Appl Physiol. 2004;96:450–454.
    1. Ouyang P, Jiang Y, Doan HM, Xie L, Vasquez D, Welti R, Su X, Lu N, Herndon B, Yang SS, Jeannotte R, Wang W. Weight loss via exercise with controlled dietary intake may affect phospholipid profile for cancer prevention in murine skin tissues. Cancer Prev Res. 2010;3:466–477.
    1. Xie L, Jiang Y, Ouyang P, Chen J, Doan H, Herndon B, Sylvester JE, Zhang K, Molteni A, Reichle M, Zhang R, Haub MD, Baybutt RC, Wang W. Effects of dietary calorie restriction or exercise on the PI3K and ras signaling pathways in the skin of mice. J Biol Chem. 2007;282:28025–28035.
    1. Yu M, King B, Ewert E, Su X, Mardiyati N, Zhao Z, Wang W. Exercise activates p53 and negatively regulates IGF-1 pathway in epidermis within a skin cancer model. PLoS ONE. 2016;11:e0160939.
    1. Zhu Z, Jiang W, Zacher JH, Neil ES, McGinley JN, Thompson HJ. Effects of energy restriction and wheel running on mammary carcinogenesis and host systemic factors in a rat model. Cancer Prev Res. 2012;5:414–422.
    1. Kalaany NY, Sabatini DM. Tumours with PI3K activation are resistant to dietary restriction. Nature. 2009;458:725–731.
    1. Jiang W, Zhu Z, Thompson HJ. Effects of physical activity and restricted energy intake on chemically induced mammary carcinogenesis. Cancer Prev Res. 2009;2:338–344.
    1. Zhu Z, Jiang W, Sells JL, Neil ES, McGinley JN, Thompson HJ. Effect of nonmotorized wheel running on mammary carcinogenesis: circulating biomarkers, cellular processes, and molecular mechanisms in rats. Cancer Epidemiol Biomark Prev. 2008;17:1920–1929.
    1. Baltgalvis KA, Berger FG, Peña MMO, Davis JM, Carson JA. Effect of exercise on biological pathways in ApcMin/+ mouse intestinal polyps. J Appl Physiol. 2008;104:1137–1143.
    1. Ju J, Nolan B, Cheh M, Bose M, Lin Y, Wagner GC, Yang CS. Voluntary exercise inhibits intestinal tumorigenesis in Apc Min/+ mice and azoxymethane/dextran sulfate sodium-treated mice. BMC Cancer. 2008;8:316.
    1. Horak M, Zlamal F, Iliev R, Kucera J, Cacek J, Svobodova L, Hlavonova Z, Kalina T, Slaby O, Bienertova-Vasku J. Exercise-induced circulating microRNA changes in athletes in various training scenarios. PLoS ONE. 2018;13:e0191060.
    1. Khori V, Amani Shalamzari S, Isanejad A, Alizadeh Ali M, Alizadeh S, Khodayari S, Khodayari H, Shahbazi S, Zahedi A, Sohanaki H, Khaniki M, Mahdian R, Saffari M, Fayad R. Effects of exercise training together with tamoxifen in reducing mammary tumor burden in mice: possible underlying pathway of miR-21. Eur J Pharmacol. 2015;765:179–187.
    1. Dethlefsen C, Hansen LS, Lillelund C, Andersen C, Gehl J, Christensen JF, Pedersen BK, Hojman P. Exercise-induced catecholamines activate the hippo tumor suppressor pathway to reduce risks of breast cancer development. Cancer Res. 2017;77:4894–4904.
    1. Lu YP, Lou YR, Nolan B, Peng QY, Xie JG, Wagner GC, Conney AH. Stimulatory effect of voluntary exercise or fat removal (partial lipectomy) on apoptosis in the skin of UVB light-irradiated mice. Proc Natl Acad Sci USA. 2006;103:16301–16306.
    1. Higgins KA, Park D, Lee GY, Curran WJ, Deng X. Exercise-induced lung cancer regression: mechanistic findings from a mouse model. Cancer. 2014;120:3302–3310.
    1. Zheng X, Cui XX, Huang MT, Liu Y, Shih WJ, Lin Y, Lu YP, Wagner GC, Conney AH. Inhibitory effect of voluntary running wheel exercise on the growth of human pancreatic Panc-1 and prostate PC-3 xenograft tumors in immunodeficient mice. Oncol Rep. 2008;19:1583–1588.
    1. Zheng X, Cui X-X, Huang M-T, Liu Y, Wagner GC, Lin Y, Shih WJ, Lee M-J, Yang CS, Conney AH. Inhibition of progression of androgen-dependent prostate LNCaP tumors to androgen independence in SCID mice by oral caffeine and voluntary exercise. Nutr Cancer. 2012;64:1029–1037.
    1. Zhu Z, Jiang W, McGinley JN, Thompson HJ. Energetics and mammary carcinogenesis: effects of moderate-intensity running and energy intake on cellular processes and molecular mechanisms in rats. J Appl Physiol. 2009;106:911–918.
    1. Soliman S, Aronson WJ, Barnard RJ. Analyzing serum-stimulated prostate cancer cell lines after low-fat, high-fiber diet and exercise intervention. Evid Based Complement Altern Med. 2011;2011:529053.
    1. Barnard RJ, Hong Gonzalez J, Liva ME, Ngo TH. Effects of a low-fat, high-fiber diet and exercise program on breast cancer risk factors in vivo and tumor cell growth and apoptosis in vitro. Nutr Cancer. 2006;55:28–34.
    1. Hojman P, Dethlefsen C, Brandt C, Hansen J, Pedersen L, Pedersen BK. Exercise-induced muscle-derived cytokines inhibit mammary cancer cell growth. Am J Physiol Endocrinol Metabol. 2011;301:E504–E510.
    1. He C, Bassik MC, Moresi V, Sun K, Wei Y, Zou Z, An Z, Loh J, Fisher J, Sun Q, Korsmeyer S, Packer M, May HI, Hill JA, Virgin HW, Gilpin C, Xiao G, Bassel-Duby R, Scherer PE, Levine B. Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature. 2012;481:511–515.
    1. Piguet A-C, Saran U, Simillion C, Keller I, Terracciano L, Reeves HL, Dufour J-F. Regular exercise decreases liver tumors development in hepatocyte-specific PTEN-deficient mice independently of steatosis. J Hepatol. 2015;62:1296–1303.
    1. Sanchis-Gomar F. Sestrins: novel antioxidant and AMPK-modulating functions regulated by exercise? J Cell Physiol. 2013;228:1647–1650.
    1. Shannon AM, Bouchier-Hayes DJ, Condron CM, Toomey D. Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treat Rev. 2003;29:297–307.
    1. Jones LW, Viglianti BL, Tashjian JA, Kothadia SM, Keir ST, Freedland SJ, Potter MQ, Jung Moon E, Schroeder T, Herndon JE, Dewhirst MW. Effect of aerobic exercise on tumor physiology in an animal model of human breast cancer. J Appl Physiol. 2010;108:343–348.
    1. Jones LW, Antonelli J, Masko EM, Broadwater G, Lascola CD, Fels D, Dewhirst MW, Dyck JRB, Nagendran J, Flores CT, Betof AS, Nelson ER, Pollak M, Dash RC, Young ME, Freedland SJ. Exercise modulation of the host-tumor interaction in an orthotopic model of murine prostate cancer. J Appl Physiol. 2012;113:263–272.
    1. McCullough DJ, Nguyen LMD, Siemann DW, Behnke BJ. Effects of exercise training on tumor hypoxia and vascular function in the rodent preclinical orthotopic prostate cancer model. J Appl Physiol. 2013;115:1846–1854.
    1. McCullough DJ, Stabley JN, Siemann DW, Behnke BJ. Modulation of blood flow, hypoxia, and vascular function in orthotopic prostate tumors during exercise. J Natl Cancer Inst. 2014;106:dju036.
    1. Schadler KL, Thomas NJ, Galie PA, Bhang DH, Roby KC, Addai P, Till JE, Sturgeon K, Zaslavsky A, Chen CS, Ryeom S. Tumor vessel normalization after aerobic exercise enhances chemotherapeutic efficacy. Oncotarget. 2016;7:65429–65440.
    1. Zhang QB, Zhang BH, Zhang KZ, Meng XT, Jia QA, Zhang QB, Bu Y, Zhu XD, Ma DN, Ye BG, Zhang N, Ren ZG, Sun HC, Tang ZY. Moderate swimming suppressed the growth and metastasis of the transplanted liver cancer in mice model: with reference to nervous system. Oncogene. 2016;35:4122–4131.
    1. Wolff G, Davidson SJ, Wrobel JK, Toborek M. Exercise maintains blood–brain barrier integrity during early stages of brain metastasis formation. Biochem Biophys Res Commun. 2015;463:811–817.
    1. Jia W, Lu R, Martin TA, Jiang WG. The role of claudin-5 in blood-brain barrier (BBB) and brain metastases (review) Mol Med Rep. 2014;9:779–785.
    1. Hanahan D, Weinberg Robert A. Hallmarks of cancer: the next generation. Cell. 2011;144:646–674.
    1. Koelwyn GJ, Quail DF, Zhang X, White RM, Jones LW. Exercise-dependent regulation of the tumour microenvironment. Nat Rev Cancer. 2017;17:620–632.
    1. Wiggins JM, Opoku-Acheampong AB, Baumfalk DR, Siemann DW, Behnke BJ. Exercise and the tumor microenvironment. Exerc Sport Sci Rev. 2018;46:56–64.
    1. Zielinski MR, Muenchow M, Wallig MA, Horn PL, Woods JA. Exercise delays allogeneic tumor growth and reduces intratumoral inflammation and vascularization. J Appl Physiol. 2004;96:2249–2256.
    1. Almeida PWM, Gomes-Filho A, Ferreira AJ, Rodrigues CEM, Dias-Peixoto MF, Russo RC, Teixeira MM, Cassali GD, Ferreira E, Santos IC, Garcia AMC, Silami-Garcia E, Wisløff U, Pussieldi GA. Swim training suppresses tumor growth in mice. J Appl Physiol. 2009;107:261–265.
    1. Walsh NP, Gleeson M, Shephard RJ, Gleeson M, Woods JA, Bishop NC, Fleshner M, Green C, Pedersen BK, Hoffman-Goetz L, Rogers CJ, Northoff H, Abbasi A, Simon P. Position statement. Part one: immune function and exercise. Exerc Immunol Rev. 2011;17:6–63.
    1. Idorn M, Hojman P. Exercise-dependent regulation of NK cells in cancer protection. Trends Mol Med. 2016;22:565–577.
    1. Kruijsen-Jaarsma M, Revesz D, Bierings MB, Buffart LM, Takken T. Effects of exercise on immune function in patients with cancer: a systematic review. Exerc Immunol Rev. 2013;19:120–143.
    1. Pedersen L, Idorn M, Olofsson Gitte H, Lauenborg B, Nookaew I, Hansen Rasmus H, Johannesen Helle H, Becker Jürgen C, Pedersen Katrine S, Dethlefsen C, Nielsen J, Gehl J, Pedersen Bente K, Thor Straten P, Hojman P. Voluntary running suppresses tumor growth through epinephrine- and IL-6-dependent NK cell mobilization and redistribution. Cell Metabol. 2016;23:554–562.
    1. Lu Q, Ceddia MA, Price EA, Ye SM, Woods JA. Chronic exercise increases macrophage-mediated tumor cytolysis in young and old mice. Am J Physiol Regul Integr Comp Physiol. 1999;276:R482–R489.
    1. Abdalla DR, Murta EFC, Michelin MA. The influence of physical activity on the profile of immune response cells and cytokine synthesis in mice with experimental breast tumors induced by 7,12-dimethylbenzanthracene. Eur J Cancer Prev. 2013;22:251–258.
    1. Abdalla DR, Aleixo AAR, Murta EFC, Michelin MA. Innate immune response adaptation in mice subjected to administration of DMBA and physical activity. Oncol Lett. 2014;7:886–890.
    1. Kizaki T, Takemasa T, Sakurai T, Izawa T, Hanawa T, Kamiya S, Haga S, Imaizumi K, Ohno H. Adaptation of macrophages to exercise training improves innate immunity. Biochem Biophys Res Commun. 2008;372:152–156.
    1. Koelwyn GJ, Wennerberg E, Demaria S, Jones LW. Exercise in regulation of inflammation-immune axis function in cancer initiation and progression. Oncology (Williston Park) 2015;29(908–20):22.
    1. Murphy EA, Davis JM, Brown AS, Carmichael MD, Mayer EP, Ghaffar A. Effects of moderate exercise and oat β-glucan on lung tumor metastases and macrophage antitumor cytotoxicity. J Appl Physiol. 2004;97:955–959.
    1. Goh J, Tsai J, Bammler TK, Farin FM, Endicott E, Ladiges WC. Exercise training in transgenic mice is associated with attenuation of early breast cancer growth in a dose-dependent manner. PLoS ONE. 2013;8:e80123.
    1. McClellan JL, Steiner JL, Day SD, Enos RT, Davis MJ, Singh UP, Murphy EA. Exercise effects on polyp burden and immune markers in the ApcMin/+ mouse model of intestinal tumorigenesis. Int J Oncol. 2014;45:861–868.
    1. Wang J, Song H, Tang X, Yang Y, Vieira VJ, Niu Y, Ma Y. Effect of exercise training intensity on murine T-regulatory cells and vaccination response. Scand J Med Sci Sports. 2012;22:643–652.
    1. Hampras SS, Nesline M, Wallace PK, Odunsi K, Furlani N, Davis W, Moysich KB. Predictors of immunosuppressive regulatory T lymphocytes in healthy women. J Cancer Epidemiol. 2012;2012:191090.
    1. Davis JM, Kohut ML, Jackson DA, Colbert LH, Mayer EP, Ghaffar A. Exercise effects on lung tumor metastases and in vitro alveolar macrophage antitumor cytotoxicity. Am J Physiol Regul Integr Comp Physiol. 1998;274:R1454–R1459.
    1. Frellstedt L, Waldschmidt I, Gosset P, Desmet C, Pirottin D, Bureau F, Farnir F, Franck T, Dupuis-Tricaud M-C, Lekeux P, Art T. Training modifies innate immune responses in blood monocytes and in pulmonary alveolar macrophages. Am J Respir Cell Mol Biol. 2014;51:135–142.
    1. Fiuza-Luces C, Garatachea N, Berger NA, Lucia A. Exercise is the real polypill. Physiology. 2013;28:330–358.
    1. Aoi W, Naito Y, Takagi T, Tanimura Y, Takanami Y, Kawai Y, Sakuma K, Hang LP, Mizushima K, Hirai Y, Koyama R, Wada S, Higashi A, Kokura S, Ichikawa H, Yoshikawa T. A novel myokine, secreted protein acidic and rich in cysteine (SPARC), suppresses colon tumorigenesis via regular exercise. Gut. 2012;62:882–889.
    1. Benatti FB, Pedersen BK. Exercise as an anti-inflammatory therapy for rheumatic diseases—myokine regulation. Nat Rev Rheumatol. 2015;11:86–97.
    1. World Health Organization . Assessing national capacity for the prevention and control of noncommunicable diseases. Geneva: WHO; 2012.
    1. Leitzmann M, Powers H, Anderson AS, Scoccianti C, Berrino F, Boutron-Ruault M-C, Cecchini M, Espina C, Key TJ, Norat T, Wiseman M, Romieu I. European code against cancer 4th edition: physical activity and cancer. Cancer Epidemiol. 2015;39:S46–S55.
    1. World Cancer Research Fund/American Institute for Cancer Research . Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Washington, DC: AICR; 2007.
    1. World Cancer Research Fund/American Institute for Cancer Research. Food, nutrition, physical activity, and colorectal cancer. 2017. . Accessed 5 June 2019.
    1. Moore SC, Lee IM, Weiderpass E, Campbell PT, Sampson JN, Kitahara CM, Keadle SK, Arem H, Berrington de Gonzalez A, Hartge P, Adami H-O, Blair CK, Borch KB, Boyd E, Check DP, Fournier A, Freedman ND, Gunter M, Johannson M, Khaw K-T, Linet MS, Orsini N, Park Y, Riboli E, Robien K, Schairer C, Sesso H, Spriggs M, Van Dusen R, Wolk A, Matthews CE, Patel AV. Association of leisure-time physical activity with risk of 26 types of cancer in 1.44 million adults. JAMA Intern Med. 2016;176:816–825.
    1. Keum N, Bao Y, Smith-Warner SA, Orav J, Wu K, Fuchs CS, Giovannucci EL. Association of physical activity by type and intensity with digestive system cancer risk. JAMA Oncol. 2016;2:1146–1153.
    1. Kyu HH, Bachman VF, Alexander LT, Mumford JE, Afshin A, Estep K, Veerman JL, Delwiche K, Iannarone ML, Moyer ML, Cercy K, Vos T, Murray CJL, Forouzanfar MH. Physical activity and risk of breast cancer, colon cancer, diabetes, ischemic heart disease, and ischemic stroke events: systematic review and dose-response meta-analysis for the Global Burden of Disease Study 2013. BMJ. 2016;354:i3857.
    1. World Cancer Research Fund/American Institute for Cancer Research. Food, nutrition, physical activity, and the prevention of breast cancer. 2010. . Accessed 10 April 2017.
    1. Catsburg C, Kirsh VA, Soskolne CL, Kreiger N, Bruce E, Ho T, Leatherdale ST, Rohan TE. Associations between anthropometric characteristics, physical activity, and breast cancer risk in a Canadian cohort. Breast Cancer Res Treat. 2014;145:545–552.
    1. Lope V, Martín M, Castelló A, Casla S, Ruiz A, Baena-Cañada JM, Casas AM, Calvo L, Bermejo B, Muñoz M, Ramos M, de Juan-Ferré A, Jara C, Antón A, Jimeno MÁ, Lluch A, Antolín S, García-Sáenz JÁ, Estévez P, Arriola-Arellano E, Gavilá J, Pérez-Gómez B, Carrasco E, Pollán M. Physical activity and breast cancer risk by pathological subtype. Gynecol Oncol. 2017;144:577–585.
    1. World Cancer Research Fund/American Institute for Cancer Research. Food, nutrition, physical activity, and the prevention of endometrial cancer. 2013. . Accessed 5 June 2019.
    1. Schmid D, Behrens G, Keimling M, Jochem C, Ricci C, Leitzmann M. A systematic review and meta-analysis of physical activity and endometrial cancer risk. Eur J Epidemiol. 2015;30:397–412.
    1. Brenner DR, Yannitsos DH, Farris MS, Johansson M, Friedenreich CM. Leisure-time physical activity and lung cancer risk: a systematic review and meta-analysis. Lung Cancer. 2016;95:17–27.
    1. World Cancer Research Fund International/American Institute for Cancer Research. Continuous update project report: diet, nutrition, physical activity and liver cancer. 2015. . Accessed 5 June 2019.
    1. World Cancer Research Fund/American Institute for Cancer Research. Diet, nutrition, physical activity and oesophageal cancer. 2016. . Accessed 5 June 2019.
    1. Behrens G, Jochem C, Keimling M, Ricci C, Schmid D, Leitzmann MF. The association between physical activity and gastroesophageal cancer: systematic review and meta-analysis. Eur J Epidemiol. 2014;29:151–170.
    1. World Cancer Research Fund/American Institute for Cancer Research. Diet, nutrition, physical activity and stomach cancer. 2016. . Accessed 5 June 2019.
    1. World Cancer Research Fund/American Institute for Cancer Research. Diet, nutrition, physical activity, and prostate cancer. 2014. . Accessed 5 June 2019.
    1. Shephard RJ. Physical activity and prostate cancer: an updated review. Sports Med. 2017;47:1055–1073.
    1. World Cancer Research Fund/American Institute for Cancer Research. Food, nutrition, physical activity, and the prevention of ovarian cancer. 2014. . Accessed 5 June 2019.
    1. Cannioto RA, Moysich KB. Epithelial ovarian cancer and recreational physical activity: a review of the epidemiological literature and implications for exercise prescription. Gynecol Oncol. 2015;137:559–573.
    1. Huang T, Eliassen AH, Hankinson SE, Okereke OI, Kubzansky LD, Wang M, Poole EM, Chavarro JE, Tworoger SS. A prospective study of leisure-time physical activity and risk of incident epithelial ovarian cancer: impact by menopausal status. Int J Cancer. 2016;138:843–852.
    1. World Cancer Research Fund/American Institute for Cancer Research. Continous Update Project Expert Report 2018. Food, nutrition, physical activity, and the prevention of pancreatic cancer. Available at . Accesed 4 June 2019.
    1. Farris MS, Mosli MH, McFadden AA, Friedenreich CM, Brenner DR. The association between leisure time physical activity and pancreatic cancer risk in adults: a systematic review and meta-analysis. Cancer Epidemiol Biomark Prev. 2015;24:1462–1473.
    1. Noor NM, Banim PJR, Luben RN, Khaw K-T, Hart AR. Investigating physical activity in the etiology of pancreatic cancer. Pancreas. 2016;45:388–393.
    1. World Cancer Research Fund/American Institute for Cancer Research. Diet, nutrition, physical activity and kidney cancer. 2015. . Accessed 5 June 2019.
    1. Behrens G, Leitzmann MF. The association between physical activity and renal cancer: systematic review and meta-analysis. Br J Cancer. 2013;108:798–811.
    1. World Cancer Research Fund/American Institute for Cancer Research. Diet, nutrition, physical activity and bladder cancer. 2015. . Accessed 5 June 2019.
    1. Keimling M, Behrens G, Schmid D, Jochem C, Leitzmann MF. The association between physical activity and bladder cancer: systematic review and meta-analysis. Br J Cancer. 2014;110:1862–1870.
    1. Jochem C, Leitzmann MF, Keimling M, Schmid D, Behrens G. Physical activity in relation to risk of hematologic cancers: a systematic review and meta-analysis. Cancer Epidemiol Biomark Prev. 2014;23:833–846.
    1. Lahart IM, Metsios GS, Nevill AM, Carmichael AR. Physical activity, risk of death and recurrence in breast cancer survivors: a systematic review and meta-analysis of epidemiological studies. Acta Oncol. 2015;54:635–654.
    1. Lahart IM, Metsios GS, Nevill AM, Carmichael AR. Physical activity for women with breast cancer after adjuvant therapy. Cochrane Database Syst Rev. 2018;1:CD011292.
    1. Holmes MD, Chen WY, Feskanich D, Kroenke CH, Colditz GA. Physical activity and survival after breast cancer diagnosis. JAMA. 2005;293:2479–2486.
    1. Irwin ML, Smith AW, McTiernan A, Ballard-Barbash R, Cronin K, Gilliland FD, Baumgartner RN, Baumgartner KB, Bernstein L. Influence of pre- and postdiagnosis physical activity on mortality in breast cancer survivors: the health, eating, activity, and lifestyle study. J Clin Oncol. 2008;26:3958–3964.
    1. Bao P-P, Zhao G-M, Shu X-O, Peng P, Cai H, Lu W, Zheng Y. Modifiable lifestyle factors and triple-negative breast cancer survival. Epidemiology. 2015;26:909–916.
    1. Schmidt ME, Chang-Claude J, Vrieling A, Seibold P, Heinz J, Obi N, Flesch-Janys D, Steindorf K. Association of pre-diagnosis physical activity with recurrence and mortality among women with breast cancer. Int J Cancer. 2013;133:1431–1440.
    1. Holick CN, Newcomb PA, Trentham-Dietz A, Titus-Ernstoff L, Bersch AJ, Stampfer MJ, Baron JA, Egan KM, Willett WC. Physical activity and survival after diagnosis of invasive breast cancer. Cancer Epidemiol Biomark Prev. 2008;17:379–386.
    1. Ammitzbøll G, Søgaard K, Karlsen RV, Tjønneland A, Johansen C, Frederiksen K, Bidstrup P. Physical activity and survival in breast cancer. Eur J Cancer. 2016;66:67–74.
    1. Friedenreich CM, Gregory J, Kopciuk KA, Mackey JR, Courneya KS. Prospective cohort study of lifetime physical activity and breast cancer survival. Int J Cancer. 2009;124:1954–1962.
    1. Sternfeld B, Weltzien E, Quesenberry CP, Castillo AL, Kwan M, Slattery ML, Caan BJ. Physical activity and risk of recurrence and mortality in breast cancer survivors: findings from the LACE study. Cancer Epidemiol Biomark Prev. 2009;18:87–95.
    1. Irwin ML, McTiernan A, Manson JE, Thomson CA, Sternfeld B, Stefanick ML, Wactawski-Wende J, Craft L, Lane D, Martin LW, Chlebowski R. Physical activity and survival in postmenopausal women with breast cancer: results from the women’s health initiative. Cancer Prev Res. 2011;4:522–529.
    1. Bertram LAC, Stefanick ML, Saquib N, Natarajan L, Patterson RE, Bardwell W, Flatt SW, Newman VA, Rock CL, Thomson CA, Pierce JP. Physical activity, additional breast cancer events, and mortality among early-stage breast cancer survivors: findings from the WHEL Study. Cancer Causes Control. 2011;22:427–435.
    1. Bradshaw PT, Ibrahim JG, Khankari N, Cleveland RJ, Abrahamson PE, Stevens J, Satia JA, Teitelbaum SL, Neugut AI, Gammon MD. Post-diagnosis physical activity and survival after breast cancer diagnosis: the Long Island Breast Cancer Study. Breast Cancer Res Treat. 2014;145:735–742.
    1. Walter V, Jansen L, Knebel P, Chang-Claude J, Hoffmeister M, Brenner H. Physical activity and survival of colorectal cancer patients: population-based study from Germany. Int J Cancer. 2017;140:1985–1997.
    1. Arem H, Pfeiffer RM, Engels EA, Alfano CM, Hollenbeck A, Park Y, Matthews CE. Pre- and postdiagnosis physical activity, television viewing, and mortality among patients with colorectal cancer in the National Institutes of Health—AARP diet and health study. J Clin Oncol. 2015;33:180–188.
    1. Meyerhardt JA, Giovannucci EL, Holmes MD, Chan AT, Chan JA, Colditz GA, Fuchs CS. Physical activity and survival after colorectal cancer diagnosis. J Clin Oncol. 2006;24:3527–3534.
    1. van Blarigan EL, Fuchs CS, Niedzwiecki D, Zhang S, Saltz LB, Mayer RJ, Mowat RB, Whittom R, Hantel A, Benson A, Atienza D, Messino M, Kindler H, Venook A, Ogino S, Giovannucci EL, Ng K, Meyerhardt JA. Association of survival with adherence to the american cancer society nutrition and physical activity guidelines for cancer survivors after colon cancer diagnosis. JAMA Oncol. 2018;4:783–790.
    1. Campbell PT, Patel AV, Newton CC, Jacobs EJ, Gapstur SM. Associations of recreational physical activity and leisure time spent sitting with colorectal cancer survival. J Clin Oncol. 2013;31:876–885.
    1. Richman EL, Kenfield SA, Stampfer MJ, Paciorek A, Carroll PR, Chan JM. Physical activity after diagnosis and risk of prostate cancer progression: data from the cancer of the prostate strategic urologic research endeavor. Cancer Res. 2011;71:3889–3895.
    1. Friedenreich CM, Wang Q, Neilson HK, Kopciuk KA, McGregor SE, Courneya KS. Physical activity and survival after prostate cancer. Eur Urol. 2016;70:576–585.
    1. Kenfield SA, Stampfer MJ, Giovannucci E, Chan JM. Physical activity and survival after prostate cancer diagnosis in the health professionals follow-up study. J Clin Oncol. 2011;29:726–732.
    1. Liss M, Natarajan L, Hasan A, Noguchi JL, White M, Parsons JK. Physical activity decreases kidney cancer mortality. Curr Urol. 2017;10:193–198.
    1. Sloan JA, Cheville AL, Liu H, Novotny PJ, Wampfler JA, Garces YI, Clark MM, Yang P. Impact of self-reported physical activity and health promotion behaviors on lung cancer survivorship. Health Qual Outcomes. 2016;14:66.
    1. Wang L, Wang C, Wang J, Huang X, Cheng Y. Longitudinal, observational study on associations between postoperative nutritional vitamin D supplementation and clinical outcomes in esophageal cancer patients undergoing esophagectomy. Sci Rep. 2016;6:1572–1581.
    1. Ballard-Barbash R, Friedenreich CM, Courneya KS, Siddiqi SM, McTiernan A, Alfano CM. Physical activity, biomarkers, and disease outcomes in cancer survivors: a systematic review. J Natl Cancer Inst. 2012;104:815–840.
    1. Gunnell AS, Joyce S, Tomlin S, Taaffe DR, Cormie P, Newton RU, Joseph D, Spry N, Einarsdóttir K, Galvão DA. Physical activity and survival among long-term cancer survivor and non-cancer cohorts. Front Public Health. 2017;5:19.
    1. Li T, Wei S, Shi Y, Pang S, Qin Q, Yin J, Deng Y, Chen Q, Wei S, Nie S, Liu L. The dose–response effect of physical activity on cancer mortality: findings from 71 prospective cohort studies. Br J Sports Med. 2016;50:339–345.
    1. Schmid D, Leitzmann MF. Association between physical activity and mortality among breast cancer and colorectal cancer survivors: a systematic review and meta-analysis. Ann Oncol. 2014;25:1293–1311.
    1. Scott JM, Li N, Liu Q, Yasui Y, Leisenring W, Nathan PC, Gibson T, Armenian SH, Nilsen TS, Oeffinger KC, Ness KK, Adams SC, Robison LL, Armstrong GT, Jones LW. Association of exercise with mortality in adult survivors of childhood cancer. JAMA Oncol. 2018;4:1352–1358.
    1. Beasley JM, Kwan ML, Chen WY, Weltzien EK, Kroenke CH, Lu W, Nechuta SJ, Cadmus-Bertram L, Patterson RE, Sternfeld B, Shu X-O, Pierce JP, Caan BJ. Meeting the physical activity guidelines and survival after breast cancer: findings from the after breast cancer pooling project. Breast Cancer Res Treat. 2012;131:637–643.
    1. Jeon J, Sato K, Niedzwiecki D, Ye X, Saltz LB, Mayer RJ, Mowat RB, Whittom R, Hantel A, Benson A, Wigler DS, Atienza D, Messino M, Kindler H, Venook A, Fuchs CS, Meyerhardt JA. Impact of physical activity after cancer diagnosis on survival in patients with recurrent colon cancer: findings from CALGB 89803/alliance. Clin Colorectal Cancer. 2013;12:233–238.
    1. Meyerhardt JA, Heseltine D, Niedzwiecki D, Hollis D, Saltz LB, Mayer RJ, Thomas J, Nelson H, Whittom R, Hantel A, Schilsky RL, Fuchs CS. Impact of physical activity on cancer recurrence and survival in patients with stage III colon cancer: findings from CALGB 89803. J Clin Oncol. 2006;24:3535–3541.
    1. Haykowsky MJ, Scott JM, Hudson K, Denduluri N. Lifestyle interventions to improve cardiorespiratory fitness and reduce breast cancer recurrence. Am Soc Clin Oncol Educ Book. 2017;37:57–64.
    1. Casla S, Hojman P, Márquez-Rodas I, López-Tarruella S, Jerez Y, Barakat R, Martín M. Running away from side effects: physical exercise as a complementary intervention for breast cancer patients. Clin Transl Oncol. 2015;17:180–196.
    1. Mishra SI, Scherer RW, Geigle PM, Berlanstein DR, Topaloglu O, Gotay CC, Snyder C. Exercise interventions on health-related quality of life for cancer survivors. Cochrane Database Syst Rev. 2012 doi: 10.1002/14651858.cd007566.pub2.
    1. Mishra SI, Scherer RW, Snyder C, Geigle PM, Berlanstein DR, Topaloglu O. Exercise interventions on health-related quality of life for people with cancer during active treatment. Cochrane Database Syst Rev. 2012 doi: 10.1002/14651858.cd008465.pub2.
    1. Schmitz KH, Courneya KS, Matthews C, Demark-Wahnefried W, GalvÃO DA, Pinto BM, Irwin ML, Wolin KY, Segal RJ, Lucia A, Schneider CM, Von Gruenigen VE, Schwartz AL. American college of sports medicine roundtable on exercise guidelines for cancer survivors. Med Sci Sports Exerc. 2010;42:1409–1426.
    1. Jones LW, Eves ND, Peddle CJ, Courneya KS, Haykowsky M, Kumar V, Winton TW, Reiman T. Effects of presurgical exercise training on systemic inflammatory markers among patients with malignant lung lesions. Appl Physiol Nutr Metabol. 2009;34:197–202.
    1. Ligibel JA, Irwin M, Dillon D, Barry W, Giobbie-Hurder A, Frank E, Winer EP, McTiernan A, Cornwell M, Pun M, Brown M, Jeselsohn R. Impact of pre-operative exercise on breast cancer gene expresision. In: Proceedings of the thirty-ninth annual CTRC–AACR San Antonio breast cancer symposium. San Antonio: American Association for Cancer Research; 2017. p. 77.
    1. Furmaniak AC, Menig M, Markes MH. Exercise for women receiving adjuvant therapy for breast cancer. Cochrane Database Syst Rev. 2016;9:CD005001.
    1. Loughney L, West MA, Kemp GJ, Grocott MPW, Jack S. Exercise intervention in people with cancer undergoing neoadjuvant cancer treatment and surgery: a systematic review. Eur J Surg Oncol. 2016;42:28–38.
    1. Loughney L, West MA, Kemp GJ, Grocott MPW, Jack S. Exercise intervention in people with cancer undergoing adjuvant cancer treatment following surgery: a systematic review. Eur J Surg Oncol. 2015;41:1590–1602.
    1. Beaudry RI, Liang Y, Boyton ST, Tucker WJ, Brothers RM, Daniel KM, Rao R, Haykowsky MJ. Meta-analysis of exercise training on vascular endothelial function in cancer survivors. Integr Cancer Ther. 2018;17:192–199.
    1. Nelson ME, Rejeski WJ, Blair SN, Duncan PW, Judge JO, King AC, Macera CA, Castaneda-Sceppa C. Physical activity and public health in older adults. Med Sci Sports Exerc. 2007;39:1435–1445.
    1. Turner RR, Steed L, Quirk H, Greasley RU, Saxton JM, Taylor SJC, Rosario DJ, Thaha MA, Bourke L. Interventions for promoting habitual exercise in people living with and beyond cancer. Cochrane Database Syst Rev. 2018;9:CD010192.
    1. Jones LW, Liu Q, Armstrong GT, Ness KK, Yasui Y, Devine K, Tonorezos E, Soares-Miranda L, Sklar CA, Douglas PS, Robison LL, Oeffinger KC. Exercise and risk of major cardiovascular events in adult survivors of childhood hodgkin lymphoma: a report from the childhood cancer survivor study. J Clin Oncol. 2014;32:3643–3650.
    1. Sasso JP, Eves ND, Christensen JF, Koelwyn GJ, Scott J, Jones LW. A framework for prescription in exercise-oncology research. J Cachexia Sarcopenia Muscle. 2015;6:115–124.
    1. Padilha CS, Marinello PC, Galvão DA, Newton RU, Borges FH, Frajacomo F, Deminice R. Evaluation of resistance training to improve muscular strength and body composition in cancer patients undergoing neoadjuvant and adjuvant therapy: a meta-analysis. J Cancer Surviv. 2017;11:339–349.
    1. Jones LW, Courneya KS, Vallance JKH, Ladha AB, Mant MJ, Belch AR, Stewart DA, Reiman T. Association between exercise and quality of life in multiple myeloma cancer survivors. Support Care Cancer. 2004;12:780–788.
    1. Mills RC. Breast cancer survivors, common markers of inflammation, and exercise: a narrative review. Breast Cancer Basic Clin Res. 2017;11:117822341774397.
    1. Gil-Rey E, Quevedo-Jerez K, Maldonado-Martin S, Herrero-Román F. Exercise intensity guidelines for cancer survivors: a comparison with reference values. Int J Sports Med. 2014;35:e1–e9.
    1. Toohey K, Pumpa K, McKune A, Cooke J, Semple S. High-intensity exercise interventions in cancer survivors: a systematic review exploring the impact on health outcomes. J Cancer Res Clin Oncol. 2018;144:1–12.
    1. National Academies of Sciences EM, Health and Medicine Division. Board on health care services, national cancer policy forum. Incorporating weight management and physical activity throughout the cancer care continuum. In: Proceedings of a workshop. Washington, DC: National Academies Press; 2018.
    1. Tudor-Locke C, Bassett DR. How many steps/day are enough? Sports Med. 2004;34:1–8.
    1. Chen X, Lu W, Zheng W, Gu K, Matthews CE, Chen Z, Zheng Y, Shu XO. Exercise after diagnosis of breast cancer in association with survival. Cancer Prev Res. 2011;4:1409–1418.
    1. Carayol M, Bernard P, Boiché J, Riou F, Mercier B, Cousson-Gélie F, Romain AJ, Delpierre C, Ninot G. Psychological effect of exercise in women with breast cancer receiving adjuvant therapy: what is the optimal dose needed? Ann Oncol. 2013;24:291–300.
    1. Valle C. Enhancing benefits of exercise for the survivor using emerging technology. In: ASCO Annual Meeting. Chicago; 201.
    1. Joyner MJ, Sanchis-Gomar F, Lucia A. Exercise medicine education should be expanded. Br J Sports Med. 2017;51:625–626.
    1. McDermott LA, Murphy MH, McNeilly AM, Rankin JP, Gracey JH. Biological markers as an outcome measure of exercise in cancer rehabilitation: a systematic review. J Cancer Res Ther. 2018;14:267–277.
    1. Campbell KL, Winters-Stone KM, Wiskemann J, May AM, Schwartz AL, Courneya KS, et al. Exercise guidelines for cancer survivors: consensus statement from international multidisciplinary roundtable. Med Sci Sports Exerc. 2019;51:2375–2390.
    1. Jones LW, Peddle CJ, Eves ND, Haykowsky MJ, Courneya KS, Mackey JR, et al. Effects of presurgical exercise training on cardiorespiratory fitness among patients undergoing thoracic surgery for malignant lung lesions. Cancer. 2007;110:590–598.
    1. Jones LW, Hornsby WE, Goetzinger A, Forbes LM, Sherrard EL, Quist M, et al. Prognostic significance of functional capacity and exercise behavior in patients with metastatic non-small cell lung cancer. Lung Cancer. 2012;76:248–252.
    1. Travier N, Velthuis MJ, Steins Bisschop CN, van den Buijs B, Monninkhof EM, Backx F, et al. Effects of an 18-week exercise programme started early during breast cancer treatment: a randomised controlled trial. BMC Med. 2015;13:121.

Source: PubMed

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