Epidemiology

Physical activity and risk of breast cancer overall and by hormone receptor status: The European prospective investigation into cancer and nutrition

  1. Karen Steindorf1,†,*,
  2. Rebecca Ritte2,
  3. Piia-Piret Eomois2,
  4. Annekatrin Lukanova2,
  5. Anne Tjonneland3,
  6. Nina Føns Johnsen3,
  7. Kim Overvad4,
  8. Jane Nautrup Østergaard4,
  9. Françoise Clavel-Chapelon5,6,
  10. Agnès Fournier5,6,
  11. Laure Dossus5,6,
  12. Birgit Teucher2,
  13. Sabine Rohrmann7,
  14. Heiner Boeing8,
  15. Angelika Wientzek8,
  16. Antonia Trichopoulou9,10,
  17. Tina Karapetyan10,
  18. Dimitrios Trichopoulos9,10,
  19. Giovanna Masala11,
  20. Franco Berrino12,
  21. Amalia Mattiello13,
  22. Rosario Tumino14,
  23. Fulvio Ricceri15,
  24. J.Ramón Quirós16,
  25. Noémie Travier17,
  26. María-José Sánchez18,
  27. Carmen Navarro19,20,
  28. Eva Ardanaz20,21,
  29. Pilar Amiano19,22,
  30. H.B(as). Bueno-de-Mesquita23,24,
  31. Franzel van Duijnhoven23,25,
  32. Evelyn Monninkhof26,
  33. Anne M. May26,
  34. Kay-Tee Khaw27,
  35. Nick Wareham28,
  36. Tim J. Key29,
  37. Ruth C. Travis29,
  38. Kristin Benjaminsen Borch30,
  39. Malin Sund31,
  40. Anne Andersson32,33,
  41. Veronika Fedirko34,
  42. Sabina Rinaldi35,
  43. Isabelle Romieu36,
  44. Jürgen Wahrendorf37,
  45. Elio Riboli38,
  46. Rudolf Kaaks2

Article first published online: 14 SEP 2012

DOI: 10.1002/ijc.27778

Issue

International Journal of Cancer

International Journal of Cancer

Volume 132, Issue 7, pages 1667–1678, 1 April 2013

Additional Information

How to Cite

Steindorf, K., Ritte, R., Eomois, P.-P., Lukanova, A., Tjonneland, A., Johnsen, N. F., Overvad, K., Østergaard, J. N., Clavel-Chapelon, F., Fournier, A., Dossus, L., Teucher, B., Rohrmann, S., Boeing, H., Wientzek, A., Trichopoulou, A., Karapetyan, T., Trichopoulos, D., Masala, G., Berrino, F., Mattiello, A., Tumino, R., Ricceri, F., Quirós, J.Ramón., Travier, N., Sánchez, M.-J., Navarro, C., Ardanaz, E., Amiano, P., Bueno-de-Mesquita, H.B(as)., van Duijnhoven, F., Monninkhof, E., May, A. M., Khaw, K.-T., Wareham, N., Key, T. J., Travis, R. C., Borch, K. B., Sund, M., Andersson, A., Fedirko, V., Rinaldi, S., Romieu, I., Wahrendorf, J., Riboli, E. and Kaaks, R. (2013), Physical activity and risk of breast cancer overall and by hormone receptor status: The European prospective investigation into cancer and nutrition. Int. J. Cancer, 132: 1667–1678. doi: 10.1002/ijc.27778

Author Information

  1. 1

    Unit of Physical activity and Cancer, Divisions of Environmental Epidemiology and Preventive Oncology, German Cancer Research Center (DKFZ), Heidelberg, Germany

  2. 2

    Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany

  3. 3

    Institute of Cancer Epidemiology, Danish Cancer Society Research Center, Copenhagen, Denmark

  4. 4

    Department of Epidemiology, School of Public Health, Aarhus University, Aarhus, Denmark

  5. 5

    Inserm, Centre for Research in Epidemiology and Population Health, Institut Gustave Roussy, Villejuif, France

  6. 6

    Paris South University, Villejuif, France

  7. 7

    Division of Cancer Epidemiology and Prevention, Institute of Social and Preventive Medicine, University of Zurich, Zurich, Switzerland

  8. 8

    Department of Epidemiology, German Institute of Human, Nutrition Potsdam-Rehbruecke, Nuthetal, Germany

  9. 9

    Department of Hygiene, Epidemiology and Medical Statistics, WHO Collaborating Center for Food and Nutrition Policies University of Athens, Epidemiology and Medical Statistics, Athens, Greece

  10. 10

    Hellenic Health Foundation, Athens, Greece

  11. 11

    Molecular and Nutritional Epidemiology Unit, Cancer Research and Prevention Institute – ISPO, Florence, Italy

  12. 12

    Department of Preventive and Predictive Medicine Epidemiology Unit, Fondazione IRCCS Istituto Nazionale Tumori, Milano, Italy

  13. 13

    Department of Clinical and Experimental Medicine, Federico II University, Naples, Italy

  14. 14

    Cancer Registry and Histopathology Unit, "Civile - M.P. Arezzo" Hospital, ASP Ragusa, Italy

  15. 15

    Human Genetic Foundation (HuGeF), Torino, Italy

  16. 16

    Public Health and Participation Directorate, Health and Health Care Services Council, Asturias, Spain

  17. 17

    Unit of Nutrition, Environment and Cancer, Cancer Epidemiology Research Programme, Catalan Institute of Oncology (ICO-IDIBELL), Barcelona, Spain

  18. 18

    Andalusian School of Public Health, Granada, Spain and CIBER Epidemiología y Salud Pública CIBERESP, Spain

  19. 19

    Department of Epidemiology, Murcia Regional Health Authority, Murcia, Spain

  20. 20

    CIBER in Epidemiology and Public Health (CIBERESP), Barcelona, Spain

  21. 21

    Navarra Public Health Institute, Pamplona, Spain

  22. 22

    Public Health Division of Gipuzkoa, Instituto Investigación BioDonostia, Basque Government; CIBER Epidemiología y Salud Pública, CIBERESP, Spain

  23. 23

    National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands

  24. 24

    Department of Gastroenterology and Hepatology, University Medical Center, Utrecht, The Netherlands

  25. 25

    Division of Human Nutrition, Wageningen University, Wageningen, The Netherlands

  26. 26

    Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The Netherlands

  27. 27

    University of Cambridge, United Kingdom

  28. 28

    MRC-Epidemiology Unit, Cambridge, United Kingdom

  29. 29

    Cancer Epidemiology Unit, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, United Kingdom

  30. 30

    Department of Community Medicine, University of Tromsø, Tromsø, Norway

  31. 31

    Department of Surgery, Umeå University, Umeå, Sweden

  32. 32

    Department of Radiation Sciences, Umeå, Sweden

  33. 33

    Department of Oncology, Umeå University, Sweden

  34. 34

    Nutrition and Metabolism Section, International Agency for Research on Cancer, Lyon, France

  35. 35

    Biomarkers Group, International Agency for Research on Cancer, Lyon, France

  36. 36

    Nutritional Epidemiology Group, International Agency for Research on Cancer, Lyon, France

  37. 37

    Unit of Environmental Epidemiology, German Cancer Research Center, Heidelberg, Germany

  38. 38

    Imperial College School of Public Health, London, United Kingdom

  1. †

    Tel: +49-(0)6221-42-2351, Fax: +49-(0)6221-42-2229

*Unit of Physical Activity and Cancer; Divisions of Environmental Epidemiology and Preventive Oncology, German Cancer Research Center (DKFZ); Im Neuenheimer Feld 280; D- 69120 Heidelberg; Germany

  1. †

    Tel: +49-(0)6221-42-2351, Fax: +49-(0)6221-42-2229

Publication History

  1. Issue published online: 28 JAN 2013
  2. Article first published online: 14 SEP 2012
  3. Accepted manuscript online: 18 AUG 2012 12:48AM EST
  4. Manuscript Accepted: 21 JUN 2012
  5. Manuscript Received: 30 MAR 2012

Funded by

  • European Commission (DG-SANCO), International Agency for Research on Cancer, Danish Cancer Society (Denmark)
  • Ligue contre le Cancer, Mutuelle Générale de l'Education Nationale, Institut National de la Santé et de la Recherche Médicale (France)
  • Deutsche Krebshilfe, Deutsches Krebsforschungszentrum and Federal Ministry of Education and Research (Germany)
  • the Hellenic Health Foundation, and the Stavros Niarchos Foundation (Greece)
  • Italian Association for Research on Cancer (AIRC) and National Research Council (Italy)
  • Dutch Ministry of Public Health, Welfare and Sports (VWS), Netherlands Cancer Registry (NKR), LK Research Funds, Dutch Prevention Funds, Dutch ZON (Zorg Onderzoek Nederland), World Cancer Research Fund (WCRF), Statistics Netherlands (The Netherlands)
  • ERC-2009-AdG 232997 and Nordforsk, Nordic Center of Excellence programme on Food, Nutrition and Health. (Norway)
  • Health Research Fund (FIS), Regional Governments of Andalucía, Asturias, Basque Country, Murcia (no. 6236) and Navarra, ISCIII RTICC ‘Red Temática de Investigación Cooperativa en Cáncer (R06/0020) (Spain)’
  • Swedish Cancer Society, Swedish Scientific Council and Regional Government of Skåne and Västerbotten (Sweden)
  • Cancer Research UK, Medical Research Council (United Kingdom)

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Keywords:

  • physical activity;
  • breast cancer;
  • etiology;
  • estrogen receptor;
  • progesterone receptor;
  • cohort study

Abstract

Physical activity is associated with reduced risks of invasive breast cancer. However, whether this holds true for breast cancer subtypes defined by the estrogen receptor (ER) and the progesterone receptor (PR) status is controversial. The study included 257,805 women from the multinational EPIC-cohort study with detailed information on occupational, recreational and household physical activity and important cofactors assessed at baseline. During 11.6 years of median follow-up, 8,034 incident invasive breast cancer cases were identified. Data on ER, PR and combined ER/PR expression were available for 6,007 (67.6%), 4,814 (54.2%) and 4,798 (53.9%) cases, respectively. Adjusted hazard ratios (HR) were estimated by proportional hazards models. Breast cancer risk was inversely associated with moderate and high levels of total physical activity (HR = 0.92, 95% confidence interval (CI): 0.86–0.99, HR = 0.87, 95%-CI: 0.79–0.97, respectively; p-trend = 0.002), compared to the lowest quartile. Among women diagnosed with breast cancer after age 50, the largest risk reduction was found with highest activity (HR = 0.86, 95%-CI: 0.77–0.97), whereas for cancers diagnosed before age 50 strongest associations were found for moderate total physical activity (HR = 0.78, 95%-CI: 0.64–0.94). Analyses by hormone receptor status suggested differential associations for total physical activity (p-heterogeneity = 0.04), with a somewhat stronger inverse relationship for ER+/PR+ breast tumors, primarily driven by PR+ tumors (p-heterogeneity < 0.01). Household physical activity was inversely associated with ER–/PR– tumors. The results of this largest prospective study on the protective effects of physical activity indicate that moderate and high physical activity are associated with modest decreased breast cancer risk. Heterogeneities by receptor status indicate hormone-related mechanisms.

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