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Physical Activity and Breast Cancer Survival–Epidemiologic Evidence and Potential Biologic Mechanisms

  • Cancer (MF Leitzmann and T Kuhn, Section Editor)
  • Published:
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Abstract

Purpose of Review

To review the biologic mechanisms that may be operative between physical activity and survival after breast cancer.

Recent Findings

Physical activity decreases risk of mortality from breast cancer by up to 40%. Several biologic mechanisms have been hypothesized to explain this association. Previous cohort studies and randomized trials have examined the primary mechanisms that appear to be operative, which involve a decrease in sex hormone levels, insulin resistance, and inflammation. The evidence is still inconsistent and several limitations in the existing literature exist.

Summary

Understanding the biologic mechanisms involved in the association of physical activity and breast cancer survival will provide more precision to physical activity guidelines for cancer survival. To achieve this objective, future research should include direct measurements of physical activity, sedentary behaviour, and health-related fitness to provide a more comprehensive assessment of these factors and their association with biomarkers and survival after breast cancer.

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References

Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–49. https://doi.org/10.3322/caac.21660.

    Article  Google Scholar 

  2. McCormack V, McKenzie F, Foerster M, Zietsman A, Galukande M, Adisa C, et al. Breast cancer survival and survival gap apportionment in sub-Saharan Africa (ABC-DO): a prospective cohort study. Lancet Glob Health. 2020;8(9):e1203–12. https://doi.org/10.1016/s2214-109x(20)30261-8.

    Article  Google Scholar 

  3. Holmes MD, Chen WY, Feskanich D, Kroenke CH, Colditz GA. Physical activity and survival after breast cancer diagnosis. JAMA. 2005;293(20):2479–86.

    Article  CAS  Google Scholar 

  4. Friedenreich CM, Stone CR, Cheung WY, Hayes SC. Physical activity and mortality in cancer survivors: a systematic review and meta-analysis. JNCI Cancer Spectr. 2020;4(1):pkz080. https://doi.org/10.1093/jncics/pkz080.

    Article  Google Scholar 

  5. Allin KH, Bojesen SE, Nordestgaard BG. Baseline C-reactive protein is associated with incident cancer and survival in patients with cancer. J Clin Oncol. 2009;27(13):2217–24. https://doi.org/10.1200/jco.2008.19.8440.

    Article  CAS  Google Scholar 

  6. Al Murri AM, Bartlett JM, Canney PA, Doughty JC, Wilson C, McMillan DC. Evaluation of an inflammation-based prognostic score (GPS) in patients with metastatic breast cancer. Br J Cancer. 2006;94(2):227–30. https://doi.org/10.1038/sj.bjc.6602922.

    Article  CAS  Google Scholar 

  7. Albuquerque K, Price M, Badley R, Jonrup I, Pearson D, Blamey R, et al. Pre-treatment serum levels of tumour markers in metastatic breast cancer: a prospective assessment of their role in predicting response to therapy and survival. Eur J Surg. 1995;21(5):504–9. https://doi.org/10.1016/s0748-7983(95)96935-7.

    Article  CAS  Google Scholar 

  8. Salgado R, Junius S, Benoy I, Van Dam P, Vermeulen P, Van Marck E, et al. Circulating interleukin-6 predicts survival in patients with metastatic breast cancer. Int J Cancer. 2003;103(5):642–6. https://doi.org/10.1002/ijc.10833.

    Article  CAS  Google Scholar 

  9. Berrino F, Pasanisi P, Bellati C, Venturelli E, Krogh V, Mastroianni A, et al. Serum testosterone levels and breast cancer recurrence. Int J Cancer. 2005;113(3):499–502. https://doi.org/10.1002/ijc.20582.

    Article  CAS  Google Scholar 

  10. Pasanisi P, Venturelli E, Morelli D, Fontana L, Secreto G, Berrino F. Serum insulin-like growth factor-I and platelet-derived growth factor as biomarkers of breast cancer prognosis. Cancer Epidemiol Biomarkers Prev. 2008;17(7):1719–22. https://doi.org/10.1158/1055-9965.EPI-07-0654.

    Article  CAS  Google Scholar 

  11. Ligibel JA, Dillon D, Giobbie-Hurder A, McTiernan A, Frank E, Cornwell M, et al. Impact of a pre-operative exercise intervention on breast cancer proliferation and gene expression: results from the pre-operative health and body (PreHAB) study. Clin Cancer Res. 2019;25(17):5398–406. https://doi.org/10.1158/1078-0432.CCR-18-3143.

    Article  CAS  Google Scholar 

  12. Tjoe JA, Piacentine LB, Papanek PE, Raff H, Richards J, Harkins AL, et al. Team triathlon effects on physiological, psychological, and immunological measures in women breast cancer survivors. Support Care Cancer. 2020;28(12):6095–104. https://doi.org/10.1007/s00520-020-05457-2.

    Article  Google Scholar 

  13. Schulz SVW, Schumann U, Otto S, Kirsten J, Treff G, Janni W, et al. Two-year follow-up after a six-week high-intensity training intervention study with breast cancer patients: physiological, psychological and immunological differences. Disabil Rehabil. 2021. https://doi.org/10.1080/09638288.2021.1921861.

    Article  Google Scholar 

  14. Gomez AM, Martinez C, Fiuza-Luces C, Herrero F, Perez M, Madero L, et al. Exercise training and cytokines in breast cancer survivors. Int J Sports Med. 2011;32(6):461–7. https://doi.org/10.1055/s-0031-1271697.

    Article  CAS  Google Scholar 

  15. Shimura T, Shibata M, Gonda K, Murakami Y, Noda M, Tachibana K, et al. Prognostic impact of interleukin-6 and C-reactive protein on patients with breast cancer. Oncol Lett. 2019;17(6):5139–46. https://doi.org/10.3892/ol.2019.10183.

    Article  CAS  Google Scholar 

  16. de Jesus Leite MAF, Mariano IM, Dechichi JGC, Giolo JS, Goncalves AC, Puga GM. Exercise training and detraining effects on body composition, muscle strength and lipid, inflammatory and oxidative markers in breast cancer survivors under tamoxifen treatment. Life Sci. 2021;284: 119924. https://doi.org/10.1016/j.lfs.2021.119924.

    Article  CAS  Google Scholar 

  17. Ravishankaran P, Karunanithi R. Clinical significance of preoperative serum interleukin-6 and C-reactive protein level in breast cancer patients. World J Surg Oncol. 2011;9:18. https://doi.org/10.1186/1477-7819-9-18.

    Article  Google Scholar 

  18. Slavin RE. Best-evidence synthesis: an alternative to meta-analytic and traditional reviews. Educ Res. 1986;15(9):5–11.

    Article  Google Scholar 

  19. Slavin RE. Best evidence synthesis: an intelligent alternative to meta-analysis. J Clin Epidemiol. 1995;48(1):9–18.

    Article  CAS  Google Scholar 

  20. Sterne JA, Savović J, Page MJ, Elbers RG, Blencowe NS, Boutron I, et al. RoB 2: a revised tool for assessing risk of bias in randomised trials. bmj. 2019;366:l4898.

    Article  Google Scholar 

  21. Akdeniz N, Kaplan MA, Küçüköner M, Urakçı Z, Laçin Ş, Ceylan EH, et al. The effect of exercise on disease-free survival and overall survival in patients with breast cancer. Ir J Med Sci. 2021. https://doi.org/10.1007/s11845-021-02785-y.

    Article  Google Scholar 

  22. Irwin ML, Smith AW, McTiernan A, Ballard-Barbash R, Cronin K, Gilliland FD, et al. 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(24):3958–64. https://doi.org/10.1200/JCO.2007.15.9822.

    Article  Google Scholar 

  23. Williams PT. Significantly greater reduction in breast cancer mortality from post-diagnosis running than walking. Int J Cancer. 2014;135(5):1195–202. https://doi.org/10.1002/ijc.28740.

    Article  CAS  Google Scholar 

  24. Tarasenko YN, Linder DF, Miller EA. Muscle-strengthening and aerobic activities and mortality among 3+ year cancer survivors in the US. Cancer Causes Control. 2018;29(4–5):475–84. https://doi.org/10.1007/s10552-018-1017-0.

    Article  Google Scholar 

  25. Palesh O, Kamen C, Sharp S, Golden A, Neri E, Spiegel D, et al. Physical activity and survival in women with advanced breast cancer. Cancer Nurs. 2018;41(4):E31–8. https://doi.org/10.1097/ncc.0000000000000525.

    Article  Google Scholar 

  26. Nelson SH, Marinac CR, Patterson RE, Nechuta SJ, Flatt SW, Caan BJ, et al. Impact of very low physical activity, BMI, and comorbidities on mortality among breast cancer survivors. Breast Cancer Res Treat. 2016;155(3):551–7. https://doi.org/10.1007/s10549-016-3694-2.

    Article  Google Scholar 

  27. Ligibel JA, Huebner L, Rugo HS, Burstein HJ, Toppmeyer DL, Anders CK, et al. Physical activity, weight, and outcomes in patients receiving chemotherapy for metastatic breast cancer (C40502/Alliance). JNCI Cancer Spectr. 2021;5(3):pkab025. https://doi.org/10.1093/jncics/pkab025.

    Article  Google Scholar 

  28. Maliniak ML, Patel AV, McCullough ML, Campbell PT, Leach CR, Gapstur SM, et al. Obesity, physical activity, and breast cancer survival among older breast cancer survivors in the Cancer Prevention Study-II Nutrition Cohort. Breast Cancer Res Treat. 2018;167(1):133–45. https://doi.org/10.1007/s10549-017-4470-7.

    Article  Google Scholar 

  29. Jung AY, Behrens S, Schmidt M, Thoene K, Obi N, Hüsing A, et al. Pre- to postdiagnosis leisure-time physical activity and prognosis in postmenopausal breast cancer survivors. Breast Cancer Res. 2019;21(1):117. https://doi.org/10.1186/s13058-019-1206-0.

    Article  CAS  Google Scholar 

  30. Johnsson A, Broberg P, Krüger U, Johnsson A, Tornberg ÅB, Olsson H. Physical activity and survival following breast cancer. Eur J Cancer Care (Engl). 2019;28(4): e13037. https://doi.org/10.1111/ecc.13037.

    Article  Google Scholar 

  31. Irwin ML, McTiernan A, Manson JE, Thomson CA, Sternfeld B, Stefanick ML, et al. Physical activity and survival in postmenopausal women with breast cancer: results from the women’s health initiative. Cancer Prev Res (Phila). 2011;4(4):522–9. https://doi.org/10.1158/1940-6207.Capr-10-0295.

    Article  Google Scholar 

  32. Holick CN, Newcomb PA, Trentham-Dietz A, Titus-Ernstoff L, Bersch AJ, Stampfer MJ, et al. Physical activity and survival after diagnosis of invasive breast cancer. Cancer Epidemiol Biomarkers Prev. 2008;17(2):379–86. https://doi.org/10.1158/1055-9965.Epi-07-0771.

    Article  Google Scholar 

  33. Hayes SC, Steele ML, Spence RR, Gordon L, Battistutta D, Bashford J, et al. Exercise following breast cancer: exploratory survival analyses of two randomised, controlled trials. Breast Cancer Res Treat. 2018;167(2):505–14. https://doi.org/10.1007/s10549-017-4541-9.

    Article  CAS  Google Scholar 

  34. de Glas NA, Fontein DB, Bastiaannet E, Pijpe A, De Craen AJ, Liefers GJ, et al. Physical activity and survival of postmenopausal, hormone receptor-positive breast cancer patients: results of the Tamoxifen Exemestane Adjuvant Multicenter Lifestyle study. Cancer. 2014;120(18):2847–54. https://doi.org/10.1002/cncr.28783.

    Article  CAS  Google Scholar 

  35. Courneya KS, Segal RJ, McKenzie DC, Dong H, Gelmon K, Friedenreich CM, et al. Effects of exercise during adjuvant chemotherapy on breast cancer outcomes. Med Sci Sports Exerc. 2014;46(9):1744–51. https://doi.org/10.1249/mss.0000000000000297.

    Article  CAS  Google Scholar 

  36. Cao Y, Baumgartner KB, Visvanathan K, Boone SD, Baumgartner RN, Connor AE. Ethnic and biological differences in the association between physical activity and survival after breast cancer. NPJ Breast Cancer. 2020;6:51. https://doi.org/10.1038/s41523-020-00194-5.

    Article  CAS  Google Scholar 

  37. Bradshaw PT, Ibrahim JG, Khankari N, Cleveland RJ, Abrahamson PE, Stevens J, et al. Post-diagnosis physical activity and survival after breast cancer diagnosis: the Long Island Breast Cancer Study. Breast Cancer Res Treat. 2014;145(3):735–42. https://doi.org/10.1007/s10549-014-2966-y.

    Article  Google Scholar 

  38. Borch KB, Braaten T, Lund E, Weiderpass E. Physical activity before and after breast cancer diagnosis and survival - the Norwegian women and cancer cohort study. BMC Cancer. 2015;15:967. https://doi.org/10.1186/s12885-015-1971-9.

    Article  Google Scholar 

  39. Ammitzbøll G, Søgaard K, Karlsen RV, Tjønneland A, Johansen C, Frederiksen K, et al. Physical activity and survival in breast cancer. Eur J Cancer. 2016;66:67–74. https://doi.org/10.1016/j.ejca.2016.07.010.

    Article  Google Scholar 

  40. Beasley JM, Kwan ML, Chen WY, Weltzien EK, Kroenke CH, Lu W, et al. Meeting the physical activity guidelines and survival after breast cancer: findings from the after breast cancer pooling project. Breast Cancer Res Treat. 2012;131(2):637–43. https://doi.org/10.1007/s10549-011-1770-1.

    Article  Google Scholar 

  41. Nechuta S, Chen WY, Cai H, Poole EM, Kwan ML, Flatt SW, et al. A pooled analysis of post-diagnosis lifestyle factors in association with late estrogen-receptor-positive breast cancer prognosis. Int J Cancer. 2016;138(9):2088–97. https://doi.org/10.1002/ijc.29940.

    Article  CAS  Google Scholar 

  42. Bull FC, Al-Ansari SS, Biddle S, Borodulin K, Buman MP, Cardon G, et al. World Health Organization 2020 guidelines on physical activity and sedentary behaviour. Br J Sports Med. 2020;54(24):1451–62. https://doi.org/10.1136/bjsports-2020-102955.

    Article  Google Scholar 

  43. •• Brown JC, Gilmore LA. Physical activity reduces the risk of recurrence and mortality in cancer patients. Exerc Sport Sci Rev. 2020;48(2):67–73. https://doi.org/10.1249/JES.0000000000000214. This review provides a comprehensive summary of the indirect and direct effects of physical activity in cancer recurrence and mortality.

  44. •• Hong BS, Lee KP. A systematic review of the biological mechanisms linking physical activity and breast cancer. Phys Act Nutr. 2020;24(3):25–31. https://doi.org/10.20463/pan.2020.0018. This systematic review and meta-analysis summarize the biologic and molecular mechanisms involved in the initiation, progression, and survival of breast cancer.

  45. McTiernan A. Mechanisms linking physical activity with cancer. Nat Rev Cancer. 2008;8(3):205–11. https://doi.org/10.1038/nrc2325.

    Article  CAS  Google Scholar 

  46. Ennour-Idrissi K, Maunsell E, Diorio C. Effect of physical activity on sex hormones in women: a systematic review and meta-analysis of randomized controlled trials. Breast Cancer Res. 2015;17(1):139. https://doi.org/10.1186/s13058-015-0647-3.

    Article  CAS  Google Scholar 

  47. Dieli-Conwright CM, Parmentier JH, Sami N, Lee K, Spicer D, Mack WJ, et al. Adipose tissue inflammation in breast cancer survivors: effects of a 16-week combined aerobic and resistance exercise training intervention. Breast Cancer Res Treat. 2018;168(1):147–57. https://doi.org/10.1007/s10549-017-4576-y.

    Article  Google Scholar 

  48. Full KM, Johnson E, Takemoto M, Hartman SJ, Kerr J, Natarajan L, et al. Using isotemporal analyses to examine the relationships between daytime activities and cancer recurrence biomarkers in breast cancer survivors. J Phys Act Health. 2020;17(2):217–24. https://doi.org/10.1123/jpah.2019-0037.

    Article  Google Scholar 

  49. Fairey AS, Courneya KS, Field CJ, Bell GJ, Jones LW, Mackey JR. Effects of exercise training on fasting insulin, insulin resistance, insulin-like growth factors, and insulin-like growth factor binding proteins in postmenopausal breast cancer survivors: a randomized controlled trial. Cancer Epidemiol Biomarkers Prev. 2003;12(8):721–7.

    CAS  Google Scholar 

  50. Fairey AS, Courneya KS, Field CJ, Bell GJ, Jones LW, Martin BS, et al. Effect of exercise training on C-reactive protein in postmenopausal breast cancer survivors: a randomized controlled trial. Brain Behav Immun. 2005;19(5):381–8. https://doi.org/10.1016/j.bbi.2005.04.001.

    Article  CAS  Google Scholar 

  51. Irwin ML, McTiernan A, Bernstein L, Gilliland FD, Baumgartner R, Baumgartner K, et al. Relationship of obesity and physical activity with C-peptide, leptin, and insulin-like growth factors in breast cancer survivors. Cancer Epidemiol Biomarkers Prev. 2005;14(12):2881–8. https://doi.org/10.1158/1055-9965.Epi-05-0185.

    Article  CAS  Google Scholar 

  52. Dieli-Conwright CM, Courneya KS, Demark-Wahnefried W, Sami N, Lee K, Buchanan TA, et al. Effects of aerobic and resistance exercise on metabolic syndrome, sarcopenic obesity, and circulating biomarkers in overweight or obese survivors of breast cancer: a randomized controlled trial. J Clin Oncol. 2018;36(9):875–83. https://doi.org/10.1200/jco.2017.75.7526.

    Article  CAS  Google Scholar 

  53. Irwin ML, Varma K, Alvarez-Reeves M, Cadmus L, Wiley A, Chung GG, et al. Randomized controlled trial of aerobic exercise on insulin and insulin-like growth factors in breast cancer survivors: the Yale Exercise and Survivorship study. Cancer Epidemiol Biomarkers Prev. 2009;18(1):306–13. https://doi.org/10.1158/1055-9965.Epi-08-0531.

    Article  CAS  Google Scholar 

  54. Jones SB, Thomas GA, Hesselsweet SD, Alvarez-Reeves M, Yu H, Irwin ML. Effect of exercise on markers of inflammation in breast cancer survivors: the Yale exercise and survivorship study. Cancer Prev Res (Phila). 2013;6(2):109–18. https://doi.org/10.1158/1940-6207.CAPR-12-0278.

    Article  CAS  Google Scholar 

  55. Schmitz KH, Ahmed RL, Hannan PJ, Yee D. Safety and efficacy of weight training in recent breast cancer survivors to alter body composition, insulin, and insulin-like growth factor axis proteins. Cancer Epidemiol Biomarkers Prev. 2005;14(7):1672–80. https://doi.org/10.1158/1055-9965.Epi-04-0736.

    Article  CAS  Google Scholar 

  56. Janelsins MC, Davis PG, Wideman L, Katula JA, Sprod LK, Peppone LJ, et al. Effects of Tai Chi Chuan on insulin and cytokine levels in a randomized controlled pilot study on breast cancer survivors. Clin Breast Cancer. 2011;11(3):161–70. https://doi.org/10.1016/j.clbc.2011.03.013.

    Article  CAS  Google Scholar 

  57. Winters-Stone KM, Wood LJ, Stoyles S, Dieckmann NF. The effects of resistance exercise on biomarkers of breast cancer prognosis: a pooled analysis of three randomized trials. Cancer Epidemiol Biomarkers Prev. 2018;27(2):146–53. https://doi.org/10.1158/1055-9965.Epi-17-0766.

    Article  CAS  Google Scholar 

  58. Guinan E, Hussey J, Broderick JM, Lithander FE, O’Donnell D, Kennedy MJ, et al. The effect of aerobic exercise on metabolic and inflammatory markers in breast cancer survivors–a pilot study. Support Care Cancer. 2013;21(7):1983–92. https://doi.org/10.1007/s00520-013-1743-5.

    Article  CAS  Google Scholar 

  59. Sprod LK, Janelsins MC, Palesh OG, Carroll JK, Heckler CE, Peppone LJ, et al. Health-related quality of life and biomarkers in breast cancer survivors participating in tai chi chuan. J Cancer Surviv. 2012;6(2):146–54. https://doi.org/10.1007/s11764-011-0205-7.

    Article  Google Scholar 

  60. Nuri R, Kordi M, Moghaddasi M, Rahnama N, Damirchi A, Rahmani-Nia F, et al. Effect of combination exercise training on metabolic syndrome parameters in postmenopausal women with breast cancer. J Cancer Res Ther. 2012;8(2):238–42. https://doi.org/10.4103/0973-1482.98977.

    Article  Google Scholar 

  61. Ligibel JA, Campbell N, Partridge A, Chen WY, Salinardi T, Chen H, et al. Impact of a mixed strength and endurance exercise intervention on insulin levels in breast cancer survivors. J Clin Oncol. 2008;26(6):907–12. https://doi.org/10.1200/JCO.2007.12.7357.

    Article  CAS  Google Scholar 

  62. Karimi N, Dabidi Roshan V, Fathi Bayatiyani Z. Individually and combined water-based exercise with ginger supplement, on systemic inflammation and metabolic syndrome indices, among the obese women with breast neoplasms. Iran J Cancer Prev. 2015;8(6):e3856. https://doi.org/10.17795/ijcp-3856.

    Article  Google Scholar 

  63. Kim TH, Chang JS, Park KS, Park J, Kim N, Lee JI, et al. Effects of exercise training on circulating levels of Dickkpof-1 and secreted frizzled-related protein-1 in breast cancer survivors: a pilot single-blind randomized controlled trial. PLoS ONE. 2017;12(2): e0171771. https://doi.org/10.1371/journal.pone.0171771.

    Article  CAS  Google Scholar 

  64. D’Alonzo NJ, Qiu L, Sears DD, Chinchilli V, Brown JC, Sarwer DB, et al. WISER survivor trial: combined effect of exercise and weight loss interventions on insulin and insulin resistance in breast cancer survivors. Nutrients. 2021;13(9):3108. https://doi.org/10.3390/nu13093108.

    Article  CAS  Google Scholar 

  65. Hagstrom AD, Marshall PW, Lonsdale C, Papalia S, Cheema BS, Toben C, et al. The effect of resistance training on markers of immune function and inflammation in previously sedentary women recovering from breast cancer: a randomized controlled trial. Breast Cancer Res Treat. 2016;155(3):471–82. https://doi.org/10.1007/s10549-016-3688-0.

    Article  CAS  Google Scholar 

  66. Bower JE, Greendale G, Crosswell AD, Garet D, Sternlieb B, Ganz PA, et al. Yoga reduces inflammatory signaling in fatigued breast cancer survivors: a randomized controlled trial. Psychoneuroendocrinology. 2014;43:20–9. https://doi.org/10.1016/j.psyneuen.2014.01.019.

    Article  CAS  Google Scholar 

  67. de Paulo TRS, Winters-Stone KM, Viezel J, Rossi FE, Simoes RR, Tosello G, et al. Effects of resistance plus aerobic training on body composition and metabolic markers in older breast cancer survivors undergoing aromatase inhibitor therapy. Exp Gerontol. 2018;111:210–7. https://doi.org/10.1016/j.exger.2018.07.022.

    Article  Google Scholar 

  68. Pierce BL, Neuhouser ML, Wener MH, Bernstein L, Baumgartner RN, Ballard-Barbash R, et al. Correlates of circulating C-reactive protein and serum amyloid A concentrations in breast cancer survivors. Breast Cancer Res Treat. 2009;114(1):155–67. https://doi.org/10.1007/s10549-008-9985-5.

    Article  CAS  Google Scholar 

  69. Kiecolt-Glaser JK, Bennett JM, Andridge R, Peng J, Shapiro CL, Malarkey WB, et al. Yoga’s impact on inflammation, mood, and fatigue in breast cancer survivors: a randomized controlled trial. J Clin Oncol. 2014;32(10):1040–9. https://doi.org/10.1200/JCO.2013.51.8860.

    Article  Google Scholar 

  70. Hooshmand Moghadam B, Golestani F, Bagheri R, Cheraghloo N, Eskandari M, Wong A, et al. The effects of high-intensity interval training vs. moderate-intensity continuous training on inflammatory markers, body composition, and physical fitness in overweight/obese survivors of breast cancer: a randomized controlled clinical trial. Cancers (Basel). 2021;13(17):4386. https://doi.org/10.3390/cancers13174386.

    Article  CAS  Google Scholar 

  71. Alizadeh AM, Isanejad A, Sadighi S, Mardani M, Kalaghchi B, Hassan ZM. High-intensity interval training can modulate the systemic inflammation and HSP70 in the breast cancer: a randomized control trial. J Cancer Res Clin Oncol. 2019;145(10):2583–93. https://doi.org/10.1007/s00432-019-02996-y.

    Article  CAS  Google Scholar 

  72. Ergun M, Eyigor S, Karaca B, Kisim A, Uslu R. Effects of exercise on angiogenesis and apoptosis-related molecules, quality of life, fatigue and depression in breast cancer patients. Eur J Cancer Care (Engl). 2013;22(5):626–37. https://doi.org/10.1111/ecc.12068.

    Article  CAS  Google Scholar 

  73. Rogers LQ, Fogleman A, Trammell R, Hopkins-Price P, Vicari S, Rao K, et al. Effects of a physical activity behavior change intervention on inflammation and related health outcomes in breast cancer survivors: pilot randomized trial. Integr Cancer Ther. 2013;12(4):323–35. https://doi.org/10.1177/1534735412449687.

    Article  CAS  Google Scholar 

  74. Karimi N, Roshan VD. Change in adiponectin and oxidative stress after modifiable lifestyle interventions in breast cancer cases. Asian Pac J Cancer Prev. 2013;14(5):2845–50. https://doi.org/10.7314/apjcp.2013.14.5.2845.

    Article  Google Scholar 

  75. Ligibel JA, Giobbie-Hurder A, Olenczuk D, Campbell N, Salinardi T, Winer EP, et al. Impact of a mixed strength and endurance exercise intervention on levels of adiponectin, high molecular weight adiponectin and leptin in breast cancer survivors. Cancer Causes Control. 2009;20(8):1523–8. https://doi.org/10.1007/s10552-009-9358-3.

    Article  Google Scholar 

  76. Kensler KH, Eliassen AH, Rosner BA, Hankinson SE, Brown M, Tamimi RM. Pre-diagnostic sex hormone levels and survival among breast cancer patients. Breast Cancer Res Treat. 2019;174(3):749–58. https://doi.org/10.1007/s10549-018-05121-8.

    Article  CAS  Google Scholar 

  77. Goodwin PJ, Ennis M, Pritchard KI, Trudeau ME, Koo J, Madarnas Y, et al. Fasting insulin and outcome in early-stage breast cancer: results of a prospective cohort study. J Clin Oncol. 2002;20(1):42–51. https://doi.org/10.1200/jco.2002.20.1.42.

    Article  CAS  Google Scholar 

  78. Borugian MJ, Sheps SB, Kim-Sing C, Van Patten C, Potter JD, Dunn B, et al. Insulin, macronutrient intake, and physical activity: are potential indicators of insulin resistance associated with mortality from breast cancer? Cancer Epidemiol Biomarkers Prev. 2004;13(7):1163–72.

    Article  CAS  Google Scholar 

  79. Ferroni P, Riondino S, Laudisi A, Portarena I, Formica V, Alessandroni J, et al. Pretreatment insulin levels as a prognostic factor for breast cancer progression. Oncologist. 2016;21(9):1041–9. https://doi.org/10.1634/theoncologist.2015-0462.

    Article  CAS  Google Scholar 

  80. Goodwin PJ, Ennis M, Pritchard KI, Trudeau ME, Koo J, Hartwick W, et al. Insulin-like growth factor binding proteins 1 and 3 and breast cancer outcomes. Breast Cancer Res Treat. 2002;74(1):65–76. https://doi.org/10.1023/a:1016075709022.

    Article  CAS  Google Scholar 

  81. Pierce BL, Ballard-Barbash R, Bernstein L, Baumgartner RN, Neuhouser ML, Wener MH, et al. Elevated biomarkers of inflammation are associated with reduced survival among breast cancer patients. J Clin Oncol. 2009;27(21):3437–44. https://doi.org/10.1200/jco.2008.18.9068.

    Article  CAS  Google Scholar 

  82. Allin KH, Nordestgaard BG, Flyger H, Bojesen SE. Elevated pre-treatment levels of plasma C-reactive protein are associated with poor prognosis after breast cancer: a cohort study. Breast Cancer Res. 2011;13(3):R55. https://doi.org/10.1186/bcr2891.

    Article  CAS  Google Scholar 

  83. McMillan DC, Elahi MM, Sattar N, Angerson WJ, Johnstone J, McArdle CS. Measurement of the systemic inflammatory response predicts cancer-specific and non-cancer survival in patients with cancer. Nutr Cancer. 2001;41(1–2):64–9. https://doi.org/10.1080/01635581.2001.9680613.

    Article  CAS  Google Scholar 

  84. Al Murri AM, Wilson C, Lannigan A, Doughty JC, Angerson WJ, McArdle CS, et al. Evaluation of the relationship between the systemic inflammatory response and cancer-specific survival in patients with primary operable breast cancer. Br J Cancer. 2007;96(6):891–5. https://doi.org/10.1038/sj.bjc.6603682.

    Article  CAS  Google Scholar 

  85. Villasenor A, Flatt SW, Marinac C, Natarajan L, Pierce JP, Patterson RE. Postdiagnosis c-reactive protein and breast cancer survivorship: findings from the WHEL study. Cancer Epidemiol Biomarkers Prev. 2014;23(1):189–99. https://doi.org/10.1158/1055-9965.EPI-13-0852.

    Article  CAS  Google Scholar 

  86. Goodwin P, Ennis M, Fantus I, Pritchard K, Trudeau M, Koo J, et al. Is leptin a mediator of adverse prognostic effects of obesity in breast cancer? J Clin Oncol. 2005;23(25):6037–42. https://doi.org/10.1200/JCO.2005.02.048.

    Article  CAS  Google Scholar 

  87. Lee SA, Sung H, Han W, Noh DY, Ahn SH, Kang D. Serum adiponectin but not leptin at diagnosis as a predictor of breast cancer survival. Asian Pac J Cancer Prev. 2014;15(15):6137–43. https://doi.org/10.7314/apjcp.2014.15.15.6137.

    Article  Google Scholar 

  88. Domaszewska K, Janiak A, Podgórski T, Demuth A, Kryściak J, Perkowski P, et al. A pilot study of influence of endurance training on the prooxidative and antioxidant status of women after breast cancer. Int J Environ Res Public Health. 2021;18(6):2822. https://doi.org/10.3390/ijerph18062822.

    Article  CAS  Google Scholar 

  89. Delrieu L, Touillaud M, Pérol O, Morelle M, Martin A, Friedenreich CM, et al. Impact of physical activity on oxidative stress markers in patients with metastatic breast cancer. Oxid Med Cell Longev. 2021;2021:6694594. https://doi.org/10.1155/2021/6694594.

    Article  CAS  Google Scholar 

  90. Tomasello B, Malfa GA, Strazzanti A, Gangi S, Di Giacomo C, Basile F, et al. Effects of physical activity on systemic oxidative/DNA status in breast cancer survivors. Oncol Lett. 2017;13(1):441–8. https://doi.org/10.3892/ol.2016.5449.

    Article  CAS  Google Scholar 

  91. Lee JD, Cai Q, Shu XO, Nechuta SJ. The role of biomarkers of oxidative stress in breast cancer risk and prognosis: a systematic review of the epidemiologic literature. J Womens Health (Larchmt). 2017;26(5):467–82. https://doi.org/10.1089/jwh.2016.5973.

    Article  Google Scholar 

  92. Ennour-Idrissi K, Maunsell E, Diorio C. Telomere length and breast cancer prognosis: a systematic review. Cancer Epidemiol Biomarkers Prev. 2017;26(1):3–10. https://doi.org/10.1158/1055-9965.Epi-16-0343.

    Article  CAS  Google Scholar 

  93. Garland SN, Johnson B, Palmer C, Speck RM, Donelson M, Xie SX, et al. Physical activity and telomere length in early stage breast cancer survivors. Breast Cancer Res. 2014;16(4):413. https://doi.org/10.1186/s13058-014-0413-y.

    Article  Google Scholar 

  94. Duggan C, Risques R, Alfano C, Prunkard D, Imayama I, Holte S, et al. Change in peripheral blood leukocyte telomere length and mortality in breast cancer survivors. J Natl Cancer Inst. 2014;106(4):dju035. https://doi.org/10.1093/jnci/dju035.

    Article  Google Scholar 

  95. Zhang C, Chen X, Li L, Zhou Y, Wang C, Hou S. The association between telomere length and cancer prognosis: evidence from a meta-analysis. PLoS ONE. 2015;10(7): e0133174. https://doi.org/10.1371/journal.pone.0133174.

    Article  CAS  Google Scholar 

  96. Sumsuzzman DM, Jin Y, Choi J, Yu JH, Lee TH, Hong Y. Pathophysiological role of endogenous irisin against tumorigenesis and metastasis: is it a potential biomarker and therapeutic? Tumour Biol. 2019;41(12):1010428319892790. https://doi.org/10.1177/1010428319892790.

    Article  CAS  Google Scholar 

  97. Tsiani E, Tsakiridis N, Kouvelioti R, Jaglanian A, Klentrou P. Current evidence of the role of the myokine irisin in cancer. Cancers (Basel). 2021;13(11):2628. https://doi.org/10.3390/cancers13112628.

    Article  CAS  Google Scholar 

  98. Fox J, Rioux BV, Goulet EDB, Johanssen NM, Swift DL, Bouchard DR, et al. Effect of an acute exercise bout on immediate post-exercise irisin concentration in adults: a meta-analysis. Scand J Med Sci Sports. 2018;28(1):16–28. https://doi.org/10.1111/sms.12904.

    Article  CAS  Google Scholar 

  99. Qiu S, Cai X, Sun Z, Schumann U, Zügel M, Steinacker JM. Chronic exercise training and circulating irisin in adults: a meta-analysis. Sports Med. 2015;45(11):1577–88. https://doi.org/10.1007/s40279-014-0293-4.

    Article  Google Scholar 

  100. Gannon NP, Vaughan RA, Garcia-Smith R, Bisoffi M, Trujillo KA. Effects of the exercise-inducible myokine irisin on malignant and non-malignant breast epithelial cell behavior in vitro. Int J Cancer. 2015;136(4):E197-202. https://doi.org/10.1002/ijc.29142.

    Article  CAS  Google Scholar 

  101. Zhang ZP, Zhang XF, Li H, Liu TJ, Zhao QP, Huang LH, et al. Serum irisin associates with breast cancer to spinal metastasis. Medicine (Baltimore). 2018;97(17): e0524. https://doi.org/10.1097/md.0000000000010524.

    Article  CAS  Google Scholar 

  102. Friedenreich CM, Vallance JK, McNeely ML, Culos-Reed SN, Matthews CE, Bell GJ, et al. The Alberta moving beyond breast cancer (AMBER) cohort study: baseline description of the full cohort. Cancer Causes Control. 2022;33(3):441–53. https://doi.org/10.1007/s10552-021-01539-6.

    Article  Google Scholar 

  103. Cao C, Friedenreich CM, Yang L. Association of daily sitting time and leisure-time physical activity with survival among US cancer survivors. JAMA Oncol. 2022;8(3):395–403. https://doi.org/10.1001/jamaoncol.2021.6590.

    Article  Google Scholar 

  104. Courneya K, Booth C, Gill S, O’Brien P, Vardy J, Friedenreich C, et al. The Colon Health and Life-Long Exercise Change trial: a randomized trial of the National Cancer Institute of Canada Clinical Trial Group. Curr Oncol. 2008;15(6):279–85. https://doi.org/10.3747/co.v15i6.378.

    Article  CAS  Google Scholar 

  105. Courneya KS, Vardy JL, O’Callaghan CJ, Friedenreich CM, Campbell KL, Prapavessis H, et al. Effects of a structured exercise program on physical activity and fitness in colon cancer survivors: one year feasibility results from the CHALLENGE trial. Cancer Epidemiol Biomarkers Prev. 2016;25(6):969–77. https://doi.org/10.1158/1055-9965.EPI-15-1267.

    Article  Google Scholar 

  106. Newton RU, Kenfield SA, Hart NH, Chan JM, Courneya KS, Catto J, et al. Intense Exercise for Survival among Men with Metastatic Castrate-Resistant Prostate Cancer (INTERVAL-GAP4): a multicentre, randomised, controlled phase III study protocol. BMJ Open. 2018;8(5): e022899. https://doi.org/10.1136/bmjopen-2018-022899.

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Cancer Epidemiology and Prevention Research, Cancer Care Alberta, Alberta Health Services, Holy Cross Centre, 2210-2nd St SW, Calgary, AB, T2S 3C3, Canada

    Christine M. Friedenreich, Andria R. Morielli, Irizelle Lategan, Charlotte Ryder-Burbidge & Lin Yang

  2. Department of Oncology, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada

    Christine M. Friedenreich & Lin Yang

  3. Department of Community Health Sciences, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada

    Christine M. Friedenreich & Lin Yang

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Friedenreich, C.M., Morielli, A.R., Lategan, I. et al. Physical Activity and Breast Cancer Survival–Epidemiologic Evidence and Potential Biologic Mechanisms. Curr Nutr Rep 11, 717–741 (2022). https://doi.org/10.1007/s13668-022-00431-2

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