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Association between pre-diagnosis recreational physical activity and risk of breast cancer recurrence: the California Teachers Study

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Abstract

Purpose

Studies have reported inverse associations of pre-diagnosis recreational physical activity (RPA) level with all-cause and breast cancer (BCa)-specific mortality among BCa patients. However, the association between pre-diagnosis RPA level and BCa recurrence is unclear. We investigated the association between pre-diagnosis RPA level and risk of BCa recurrence in the California Teachers Study (CTS).

Methods

Stage I–IIIb BCa survivors (n = 6,479) were followed with median of 7.4 years, and 474 BCa recurrence cases were identified. Long-term (from high school to age at baseline questionnaire, or, age 55 years, whichever was younger) and baseline (past 3 years reported at baseline questionnaire) pre-diagnosis RPA levels were converted to metabolic equivalent of task-hours per week (MET-hrs/wk). Multivariable Cox proportional hazards models estimated hazard ratios (HRs) and 95% confidence intervals (CIs) for risk of BCa recurrence overall and by estrogen receptor (ER)/progesterone receptor (PR) status.

Results

Long-term RPA was not associated with BCa recurrence risk (ptrend = 0.99). The inverse association between baseline pre-diagnosis RPA level and BCa recurrence risk was marginally significant (≥26.0 vs. <3.4 MET-hrs/wk: HR = 0.79, 95% CI = 0.60–1.03; ptrend = 0.07). However, the association became non-significant after adjusting for post-diagnosis RPA (ptrend = 0.65). An inverse association between baseline pre-diagnosis RPA level and BCa recurrence risk was observed in ER−PR− cases (≥26.0 vs. <3.4 MET-hrs/wk: HR = 0.31, 95% CI = 0.13–0.72; ptrend = 0.04), but not in ER+ or PR+ cases (ptrend = 0.97).

Conclusions

Our data indicates that the benefit of baseline RPA on BCa recurrence may differ by tumor characteristics. This information may be particularly important for populations at higher risk of ER−PR− BCa.

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Data availability

The collection of cancer incidence data used in the California Teachers Study was supported by the California Department of Public Health pursuant to California Health and Safety Code Section 103885; Centers for Disease Control and Prevention’s National Program of Cancer Registries, under cooperative agreement 5NU58DP006344; the National Cancer Institute’s Surveillance, Epidemiology and End Results Program under contract HHSN261201800032I awarded to the University of California, San Francisco, contract HHSN261201800015I awarded to the University of Southern California, and contract HHSN261201800009I awarded to the Public Health Institute. The opinions, findings, and conclusions expressed herein are those of the author(s) and do not necessarily reflect the official views of the State of California, Department of Public Health, the National Cancer Institute, the National Institutes of Health, the Centers for Disease Control and Prevention or their Contractors and Subcontractors, or the Regents of the University of California, or any of its programs. All of the data associated with this publication and in the California Teachers Study are available for research use. The California Teachers Study welcomes all such inquiries and encourages individuals to visit https://www.calteachersstudy.org/for-researchers.

References

  1. American Cancer Society (2023) Key statistics for breast cancer. American Cancer Society

    Google Scholar 

  2. American Cancer Society (2022) Cancer treatment & survivorship facts & figures 2022–2024. American Cancer Society

    Google Scholar 

  3. Pedersen RN, Esen BÖ, Mellemkjær L et al (2021) The incidence of breast cancer recurrence 10–32 years after primary diagnosis. J Natl Cancer Inst 114:391–399. https://doi.org/10.1093/jnci/djab202

    Article  CAS  PubMed Central  Google Scholar 

  4. Colleoni M, Sun Z, Price KN et al (2016) Annual hazard rates of recurrence for breast cancer during 24 years of follow-up: results from the International Breast Cancer Study Group Trials I to V. J Clin Oncol 34:927–935. https://doi.org/10.1200/jco.2015.62.3504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Come SE (2023) Overview of long-term complications of therapy in breast cancer survivors and patterns of relapse. In: Ganz PA, Pierce LJ, Whitman GJ (eds) UpToDate. UpToDate, Waltham, MA

    Google Scholar 

  6. Lahart IM, Metsios GS, Nevill AM, Carmichael AR (2015) Physical activity, risk of death and recurrence in breast cancer survivors: a systematic review and meta-analysis of epidemiological studies. Acta Oncol 54:635–654. https://doi.org/10.3109/0284186x.2014.998275

    Article  PubMed  Google Scholar 

  7. Tao MH, Hainaut P, Marian C et al (2013) Association of prediagnostic physical activity with survival following breast cancer diagnosis: influence of TP53 mutation status. Cancer Causes Control 24:2177–2186. https://doi.org/10.1007/s10552-013-0294-x

    Article  PubMed  Google Scholar 

  8. Friedenreich CM, Gregory J, Kopciuk KA, Mackey JR, Courneya KS (2009) Prospective cohort study of lifetime physical activity and breast cancer survival. Int J Cancer 124:1954–1962. https://doi.org/10.1002/ijc.24155

    Article  CAS  PubMed  Google Scholar 

  9. West-Wright CN, Henderson KD, Sullivan-Halley J et al (2009) Long-term and recent recreational physical activity and survival after breast cancer: the California Teachers Study. Cancer Epidemiol Biomarkers Prev 18:2851–2859. https://doi.org/10.1158/1055-9965.Epi-09-0538

    Article  PubMed  PubMed Central  Google Scholar 

  10. Schmidt ME, Chang-Claude J, Vrieling A et al (2013) Association of pre-diagnosis physical activity with recurrence and mortality among women with breast cancer. Int J Cancer 133:1431–1440. https://doi.org/10.1002/ijc.28130

    Article  CAS  PubMed  Google Scholar 

  11. Cannioto RA, Hutson A, Dighe S et al (2021) Physical activity before, during, and after chemotherapy for high-risk breast cancer: relationships with survival. J Natl Cancer Inst 113:54–63. https://doi.org/10.1093/jnci/djaa046

    Article  CAS  PubMed  Google Scholar 

  12. Ackerman D, Simon MC (2014) Hypoxia, lipids, and cancer: surviving the harsh tumor microenvironment. Trends Cell Biol 24:472–478. https://doi.org/10.1016/j.tcb.2014.06.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hughes VS, Wiggins JM, Siemann DW (2019) Tumor oxygenation and cancer therapy-then and now. Br J Radiol 92:20170955. https://doi.org/10.1259/bjr.20170955

    Article  PubMed  Google Scholar 

  14. Dhani N, Fyles A, Hedley D, Milosevic M (2015) The clinical significance of hypoxia in human cancers. Semin Nucl Med 45:110–121. https://doi.org/10.1053/j.semnuclmed.2014.11.002

    Article  PubMed  Google Scholar 

  15. Milani M, Venturini S, Bonardi S et al (2017) Hypoxia-related biological markers as predictors of epirubicin-based treatment responsiveness and resistance in locally advanced breast cancer. Oncotarget 8:78870–78881. https://doi.org/10.18632/oncotarget.20239

    Article  PubMed  PubMed Central  Google Scholar 

  16. Generali D, Berruti A, Brizzi MP et al (2006) Hypoxia-inducible factor-1alpha expression predicts a poor response to primary chemoendocrine therapy and disease-free survival in primary human breast cancer. Clin Cancer Res 12:4562–4568. https://doi.org/10.1158/1078-0432.Ccr-05-2690

    Article  CAS  PubMed  Google Scholar 

  17. Esteves M, Monteiro MP, Duarte JA (2021) The effects of physical exercise on tumor vasculature: systematic review and meta-analysis. Int J Sports Med 42:1237–1249. https://doi.org/10.1055/a-1533-1876

    Article  PubMed  Google Scholar 

  18. California Teachers Study. California Teachers Study. https://www.calteachersstudy.org/about-us. Accessed 11 April 2024

  19. Bernstein L, Allen M, Anton-Culver H et al (2002) High breast cancer incidence rates among California teachers: results from the California Teachers Study (United States). Cancer Causes Control 13:625–635. https://doi.org/10.1023/a:1019552126105

    Article  PubMed  Google Scholar 

  20. Ainsworth BE, Haskell WL, Herrmann SD et al (2011) 2011 Compendium of Physical Activities: a second update of codes and MET values. Med Sci Sports Exerc 43:1575–1581. https://doi.org/10.1249/MSS.0b013e31821ece12

    Article  PubMed  Google Scholar 

  21. California Cancer Registry (2018) About California Cancer Registry

  22. Bauer KR, Brown M, Cress RD, Parise CA, Caggiano V (2007) Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California Cancer Registry. Cancer 109:1721–1728. https://doi.org/10.1002/cncr.22618

    Article  PubMed  Google Scholar 

  23. Chubak J, Yu O, Pocobelli G et al (2012) Administrative data algorithms to identify second breast cancer events following early-stage invasive breast cancer. J Natl Cancer Inst 104:931–940. https://doi.org/10.1093/jnci/djs233

    Article  PubMed  PubMed Central  Google Scholar 

  24. Ibrahim EM, Al-Homaidh A (2011) Physical activity and survival after breast cancer diagnosis: meta-analysis of published studies. Med Oncol 28:753–765. https://doi.org/10.1007/s12032-010-9536-x

    Article  PubMed  Google Scholar 

  25. Lacey JV Jr, Chung NT, Hughes P et al (2020) Insights from adopting a data commons approach for large-scale observational cohort studies: the California Teachers Study. Cancer Epidemiol Biomarkers Prev 29:777–786. https://doi.org/10.1158/1055-9965.Epi-19-0842

    Article  PubMed  PubMed Central  Google Scholar 

  26. Lafourcade A, His M, Baglietto L, Boutron-Ruault M-C, Dossus L, Rondeau V (2018) Factors associated with breast cancer recurrences or mortality and dynamic prediction of death using history of cancer recurrences: the French E3N cohort. BMC Cancer 18:171. https://doi.org/10.1186/s12885-018-4076-4

    Article  PubMed  PubMed Central  Google Scholar 

  27. Anderson SJ, Wapnir I, Dignam JJ et al (2009) Prognosis after ipsilateral breast tumor recurrence and locoregional recurrences in patients treated by breast-conserving therapy in five National Surgical Adjuvant Breast and Bowel Project protocols of node-negative breast cancer. J Clin Oncol 27:2466–2473. https://doi.org/10.1200/jco.2008.19.8424

    Article  PubMed  PubMed Central  Google Scholar 

  28. Friedenreich CM, Stone CR, Cheung WY, Hayes SC (2019) Physical activity and mortality in cancer survivors: a systematic review and meta-analysis. JNCI Cancer Spectrum 4:pkz080. https://doi.org/10.1093/jncics/pkz080

    Article  PubMed  PubMed Central  Google Scholar 

  29. Romero SAD, Jones L, Bauml JM, Li QS, Cohen RB, Mao JJ (2018) The association between fatigue and pain symptoms and decreased physical activity after cancer. Support Care Cancer 26:3423–3430. https://doi.org/10.1007/s00520-018-4203-4

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Lin D, Liu Y, Tobias DK, Sturgeon K (2022) Physical activity from menarche-to-first pregnancy and risk of breast cancer: the California Teachers Study. Cancer Causes Control 33:1343–1353. https://doi.org/10.1007/s10552-022-01617-3

    Article  PubMed  PubMed Central  Google Scholar 

  32. Weikart D, Lin D, Dhingra R, Al-Shaar L, Sturgeon K (2022) Pre-diagnosis diet and physical activity and risk of cardiovascular disease mortality among female cancer survivors. Cancers (Basel) 14:3096

    Article  PubMed  Google Scholar 

  33. Ma H, Xu X, Clague J et al (2016) Recreational physical activity and risk of triple negative breast cancer in the California Teachers Study. Breast Cancer Res 18:62. https://doi.org/10.1186/s13058-016-0723-3

    Article  PubMed  PubMed Central  Google Scholar 

  34. Haine D, Dohoo I, Dufour S (2018) Selection and misclassification biases in longitudinal studies. Front Vet Sci 5:99. https://doi.org/10.3389/fvets.2018.00099

    Article  PubMed  PubMed Central  Google Scholar 

  35. Howlader N, Cronin KA, Kurian AW, Andridge R (2018) Differences in breast cancer survival by molecular subtypes in the United States. Cancer Epidemiol Biomarkers Prev 27:619–626. https://doi.org/10.1158/1055-9965.Epi-17-0627

    Article  CAS  PubMed  Google Scholar 

  36. Jones LW, Kwan ML, Weltzien E et al (2016) Exercise and prognosis on the basis of clinicopathologic and molecular features in early-stage breast cancer: the LACE and pathways studies. Cancer Res 76:5415–5422. https://doi.org/10.1158/0008-5472.Can-15-3307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors would like to thank the California Teachers Study Steering Committee that is responsible for the formation and maintenance of the Study within which this research was conducted. A full list of California Teachers Study team members is available at https://www.calteachersstudy.org/team. The authors also express their appreciation to Dr. James V. Lacey, Jr for his contribution and effort related to this research.

Funding

The California Teachers Study and the research reported in this publication were supported by the National Cancer Institute of the National Institutes of Health under award number U01-CA199277; P30-CA033572; P30-CA023100; UM1-CA164917; and R01-CA077398. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Cancer Institute or the National Institutes of Health.

Author information

Authors and Affiliations

  1. Department of Public Health Sciences, Pennsylvania State University College of Medicine, Penn State Cancer Institute, CH69, 500 University Drive, Hershey, PA, 17033, USA

    Dan Lin, Cheryl L. Thompson, Rebecca Derbes, Laila Al-Shaar & Kathleen M. Sturgeon

  2. Pennsylvania State University College of Medicine, Hershey, PA, 17033, USA

    Alaina Demalis

  3. Department of Computational and Quantitative Medicine, City of Hope, Duarte, CA, 91010, USA

    Emma S. Spielfogel

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  1. Dan Lin
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Contributions

DL: Investigation, study design, data curation, formal analysis, writing—original draft, and writing—review and editing; CLT, AD, RD, LAS: Investigation, study design, and writing—review and editing; KMS: Conceptualization, investigation, study design, writing—review and editing, project administration and supervision.

Corresponding author

Correspondence to Kathleen M. Sturgeon.

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This study was approved by the Penn State University Institutional Review Board.

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All study participants provided written informed consent to participate in the study.

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Lin, D., Thompson, C.L., Demalis, A. et al. Association between pre-diagnosis recreational physical activity and risk of breast cancer recurrence: the California Teachers Study. Cancer Causes Control (2024). https://doi.org/10.1007/s10552-024-01870-8

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