Skip to main content

Advertisement

SpringerLink
Log in

Pre-diagnostic polyphenol intake and breast cancer survival: the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort

  • Epidemiology
  • Published:
Breast Cancer Research and Treatment Aims and scope Submit manuscript

Abstract

The aim was to investigate the association between pre-diagnostic intakes of polyphenol classes (flavonoids, lignans, phenolic acids, stilbenes, and other polyphenols) in relation to breast cancer survival (all-cause and breast cancer-specific mortality). We used data from the European Prospective Investigation into Cancer and Nutrition cohort. Pre-diagnostic usual diet was assessed using dietary questionnaires, and polyphenol intakes were estimated using the Phenol-Explorer database. We followed 11,782 breast cancer cases from time of diagnosis until death, end of follow-up or last day of contact. During a median of 6 years, 1482 women died (753 of breast cancer). We related polyphenol intake to all-cause and breast cancer-specific mortality using Cox proportional hazard models with time since diagnosis as underlying time and strata for age and country. Among postmenopausal women, an intake of lignans in the highest versus lowest quartile was related to a 28 % lower risk of dying from breast (adjusted model: HR, quartile 4 vs. quartile 1, 0.72, 95 % CI 0.53; 0.98). In contrast, in premenopausal women, a positive association between lignan intake and all-cause mortality was found (adjusted model: HR, quartile 4 vs. quartile 1, 1.63, 95 % CI 1.03; 2.57). We found no association for other polyphenol classes. Intake of lignans before breast cancer diagnosis may be related to improved survival among postmenopausal women, but may on the contrary worsen the survival for premenopausal women. This suggests that the role of phytoestrogens in breast cancer survival is complex and may be dependent of menopausal status.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

EPIC:

The European Prospective Investigation into Cancer and Nutrition

ICD-10:

The 10th revision of the International Classification of Disease, Injuries and Causes of Death

ER:

Estrogen receptor

HR:

Hazard ratio

CI:

Confidence interval

UK:

United Kingdom

References

  1. Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, Forman D, Bray F (2013) Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer 49:1374–1403

    Article  CAS  PubMed  Google Scholar 

  2. Siegel R, DeSantis C, Virgo K, Stein K, Mariotto A, Smith T, Cooper D, Gansler T, Lerro C, Fedewa S, Lin C, Leach C, Cannady RS, Cho H, Scoppa S, Hachey M, Kirch R, Jemal A, Ward E (2012) Cancer treatment and survivorship statistics. CA Cancer J Clin 62(4):220–241. doi:10.3322/caac.21149

    Article  PubMed  Google Scholar 

  3. Demark-Wahnefried W, Aziz NM, Rowland JH, Pinto BM (2005) Riding the crest of the teachable moment: promoting long-term health after the diagnosis of cancer. J Clin Oncol 23:5814–5830. doi:10.1200/JCO.2005.01.230

    Article  PubMed Central  PubMed  Google Scholar 

  4. World Cancer Research Fund (2014) continuous update project report: diet, nutrition, physical activity, and breast cancer survivors. http://www.wcrf.org/sites/default/files/Breast-Cancer-Survivors-2014-Report.pdf. Accessed 1 Oct 2015

  5. Zamora-Ros R, Touillaud M, Rothwell JA, Romieu I, Scalbert A (2014) Measuring exposure to the polyphenol metabolome in observational epidemiologic studies: current tools and applications and their limits. Am J Clin Nutr 100:11–26. doi:10.3945/ajcn.113.077743

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Perez-Jimenez J, Neveu V, Vos F, Scalbert A (2010) Systematic analysis of the content of 502 polyphenols in 452 foods and beverages: an application of the phenol-explorer database. J Agric Food Chem 58(8):4959–4969. doi:10.1021/jf100128b

    Article  CAS  PubMed  Google Scholar 

  7. Manach C, Scalbert A, Morand C, Remesy C, Jimenez L (2004) Polyphenols: food sources and bioavailability. Am J Clin Nutr 79(5):727–747

    CAS  PubMed  Google Scholar 

  8. Ramos S (2008) Cancer chemoprevention and chemotherapy: dietary polyphenols and signalling pathways. Mol Nutr Food Res 52(5):507–526. doi:10.1002/mnfr.200700326

    Article  CAS  PubMed  Google Scholar 

  9. Rodriguez-Mateos A, Vauzour D, Krueger CG, Shanmuganayagam D, Reed J, Calani L, Mena P, Del Rio D, Crozier A (2014) Bioavailability, bioactivity and impact on health of dietary flavonoids and related compounds: an update. Arch Toxicol 88:1803–1853. doi:10.1007/s00204-014-1330-7

    Article  CAS  PubMed  Google Scholar 

  10. Nagasaka R, Chotimarkorn C, Shafiqul IM, Hori M, Ozaki H, Ushio H (2007) Anti-inflammatory effects of hydroxycinnamic acid derivatives. Biochem Biophys Res Commun 358:615–619. doi:10.1016/j.bbrc.2007.04.178

    Article  CAS  PubMed  Google Scholar 

  11. Kylli P, Nousiainen P, Sipila J, Tenkanen M, Heinonen M (2008) Antioxidant potential of hydroxycinnamic acid glycoside esters. J Agric Food Chem 56(12):4797–4805. doi:10.1021/jf800317v

    Article  CAS  PubMed  Google Scholar 

  12. Chottanapund S, Van Duursen MB, Navasumrit P, Hunsonti P, Timtavorn S, Ruchirawat M, Van den Berg M (2014) Anti-aromatase effect of resveratrol and melatonin on hormonal positive breast cancer cells co-cultured with breast adipose fibroblasts. Toxicol In Vitro 28:1215–1221. doi:10.1016/j.tiv.2014.05.015

    Article  CAS  PubMed  Google Scholar 

  13. Adlercreutz H (2007) Lignans and human health. Crit Rev Clin Lab Sci 44:483–525

    Article  CAS  PubMed  Google Scholar 

  14. Buck K, Zaineddin AK, Vrieling A, Linseisen J, Chang-Claude J (2010) Meta-analyses of lignans and enterolignans in relation to breast cancer risk. Am J Clin Nutr 92:141–153

    Article  CAS  PubMed  Google Scholar 

  15. Takemura H, Sakakibara H, Yamazaki S, Shimoi K (2013) Breast cancer and flavonoids—a role in prevention. Curr Pharm Des 19:6125–6132

    Article  CAS  PubMed  Google Scholar 

  16. Zamora-Ros R, Ferrari P, Gonzalez CA, Tjonneland A, Olsen A, Bredsdorff L, Overvad K, Touillaud M, Perquier F, Fagherazzi G, Lukanova A, Tikk K, Aleksandrova K, Boeing H, Trichopoulou A, Trichopoulos D, Dilis V, Masala G, Sieri S, Mattiello A, Tumino R, Ricceri F, Bueno-de-Mesquita HB, Peeters PH, Weiderpass E, Skeie G, Engeset D, Menendez V, Travier N, Molina-Montes E, Amiano P, Chirlaque MD, Barricarte A, Wallstrom P, Sonestedt E, Sund M, Landberg R, Khaw KT, Wareham NJ, Travis RC, Scalbert A, Ward HA, Riboli E, Romieu I (2013) Dietary flavonoid and lignan intake and breast cancer risk according to menopause and hormone receptor status in the European Prospective Investigation into Cancer and Nutrition (EPIC) Study. Breast Cancer Res Treat 139:163–176. doi:10.1007/s10549-013-2483-4

    Article  CAS  PubMed  Google Scholar 

  17. Chen J, Wang L, Thompson LU (2006) Flaxseed and its components reduce metastasis after surgical excision of solid human breast tumor in nude mice. Cancer Lett 234:168–175. doi:10.1016/j.canlet.2005.03.056

    Article  CAS  PubMed  Google Scholar 

  18. Hui C, Yujie F, Lijia Y, Long Y, Hongxia X, Yong Z, Jundong Z, Qianyong Z, Mantian M (2012) MicroRNA-34a and microRNA-21 play roles in the chemopreventive effects of 3,6-dihydroxyflavone on 1-methyl-1-nitrosourea-induced breast carcinogenesis. Breast Cancer Res 14:R80. doi:10.1186/bcr3194

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Fink BN, Steck SE, Wolff MS, Britton JA, Kabat GC, Gaudet MM, Abrahamson PE, Bell P, Schroeder JC, Teitelbaum SL, Neugut AI, Gammon MD (2007) Dietary flavonoid intake and breast cancer survival among women on Long Island. Cancer Epidemiol Biomark Prev 16(11):2285–2292

    Article  CAS  Google Scholar 

  20. Fritz H, Seely D, Flower G, Skidmore B, Fernandes R, Vadeboncoeur S, Kennedy D, Cooley K, Wong R, Sagar S, Sabri E, Fergusson D (2013) Soy, red clover, and isoflavones and breast cancer: a systematic review. Plos One 8:e81968. doi:10.1371/journal.pone.0081968

    Article  PubMed Central  PubMed  Google Scholar 

  21. Seibold P, Vrieling A, Johnson TS, Buck K, Behrens S, Kaaks R, Linseisen J, Obi N, Heinz J, Flesch-Janys D, Chang-Claude J (2014) Enterolactone concentrations and prognosis after postmenopausal breast cancer: assessment of effect modification and meta-analysis. Int J Cancer 135:923–933

    Article  CAS  PubMed  Google Scholar 

  22. Neveu V, Perez-Jimenez J, Vos F, Crespy V, du CL, Mennen L, Knox C, Eisner R, Cruz J, Wishart D, Scalbert A (2010) Phenol-Explorer: an online comprehensive database on polyphenol contents in foods. Database (Oxford). doi:10.1093/database/bap024

  23. Rothwell JA, Urpi-Sarda M, Boto-Ordonez M, Knox C, Llorach R, Eisner R, Cruz J, Neveu V, Wishart D, Manach C, Andres-Lacueva C, Scalbert A (2012) Phenol-Explorer 2.0: a major update of the Phenol-Explorer database integrating data on polyphenol metabolism and pharmacokinetics in humans and experimental animals. Database (Oxford). doi:10.1093/database/bas031

  24. Rothwell JA, Perez-Jimenez J, Neveu V, Medina-Remon A, M’hiri N, Garcia-Lobato P, Manach C, Knox C, Eisner R, Wishart DS, Scalbert A (2013) Phenol-Explorer 3.0: a major update of the Phenol-Explorer database to incorporate data on the effects of food processing on polyphenol content. Database (Oxford). doi:10.1093/database/bat070

  25. Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, Charrondiere UR, Hemon B, Casagrande C, Vignat J, Overvad K, Tjonneland A, Clavel-Chapelon F, Thiebaut A, Wahrendorf J, Boeing H, Trichopoulos D, Trichopoulou A, Vineis P, Palli D, Bueno-de-Mesquita HB, Peeters PH, Lund E, Engeset D, Gonzalez CA, Barricarte A, Berglund G, Hallmans G, Day NE, Key TJ, Kaaks R, Saracci R (2002) European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr 5:1113–1124

    Article  CAS  PubMed  Google Scholar 

  26. Dik VK, Murphy N, Siersema PD, Fedirko V, Jenab M, Kong SY, Hansen CP, Overvad K, Tjonneland A, Olsen A, Dossus L, Racine A, Bastide N, Li K, Kuhn T, Boeing H, Aleksandrova K, Trichopoulou A, Trichopoulos D, Barbitsioti A, Palli D, Contiero P, Vineis P, Tumino R, Panico S, Peeters PH, Weiderpass E, Skeie G, Hjartaker A, Amiano P, Sanchez MJ, Fonseca-Nunes A, Barricarte A, Chirlaque MD, Redondo ML, Jirstrom K, Manjer J, Nilsson LM, Wennberg M, Bradbury KE, Khaw KT, Wareham N, Cross AJ, Riboli E, Bueno-de-Mesquita HB (2014) Prediagnostic intake of dairy products and dietary calcium and colorectal cancer survival–results from the EPIC cohort study. Cancer Epidemiol Biomark Prev 23:1813–1823. doi:10.1158/1055-9965.EPI-14-0172

    Article  CAS  Google Scholar 

  27. Flowers JL, Burton GV, Cox EB, McCarty KS Sr, Dent GA, Geisinger KR, McCarty KS Jr (1986) Use of monoclonal antiestrogen receptor antibody to evaluate estrogen receptor content in fine needle aspiration breast biopsies. Ann Surg 203:250–254

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Remmele W, Stegner HE (1987) Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue. Pathologe 8:138–140

    CAS  PubMed  Google Scholar 

  29. Harvey JM, Clark GM, Osborne CK, Allred DC (1999) Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer. J Clin Oncol 17:1474–1481

    CAS  PubMed  Google Scholar 

  30. McCann J (2001) Better assays needed for hormone receptor status, experts say. J Natl Cancer Inst 93:579–580

    Article  CAS  PubMed  Google Scholar 

  31. Zamora-Ros R, Knaze V, Rothwell JA, Hemon B, Moskal A, Overvad K, Tjonneland A, Kyro C, Fagherazzi G, Boutron-Ruault MC, Touillaud M, Katzke V, Kuhn T, Boeing H, Forster J, Trichopoulou A, Valanou E, Peppa E, Palli D, Agnoli C, Ricceri F, Tumino R, de Magistris MS, Peeters PH, Bueno-de-Mesquita HB, Engeset D, Skeie G, Hjartaker A, Menendez V, Agudo A, Molina-Montes E, Huerta JM, Barricarte A, Amiano P, Sonestedt E, Nilsson LM, Landberg R, Key TJ, Khaw KT, Wareham NJ, Lu Y, Slimani N, Romieu I, Riboli E, Scalbert A (2015) Dietary polyphenol intake in Europe: the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Eur J Nutr. doi:10.1007/s00394-015-0950-x

    PubMed  Google Scholar 

  32. InterAct Consortium, Peters T, Brage S, Westgate K, Franks PW, Gradmark A, Tormo Diaz MJ, Huerta JM, Bendinelli B, Vigl M, Boeing H, Wendel-Vos W, Spijkerman A, Benjaminsen-Borch K, Valanou E, de Lauzon Guillain B, Clavel-Chapelon F, Sharp S, Kerrison N, Langenberg C, Arriola L, Barricarte A, Gonzales C, Grioni S, Kaaks R, Key T, Khaw KT, May A, Nilsson P, Norat T, Overvad K, Palli D, Panico S, Ramón Quirós J, Ricceri F, Sanchez MJ, Slimani N, Tjonneland A, Tumino R, Feskins E, Riboli E, Ekelund U, Wareham N (2012) Validity of a short questionnaire to assess physical activity in 10 European countries. Eur J Epidemiol 27:15–25

    Article  Google Scholar 

  33. Cox B, Sneyd MJ (2013) Bias in breast cancer research in the screening era. Breast 22:1041–1045. doi:10.1016/j.breast.2013.07.046

    Article  PubMed  Google Scholar 

  34. Freedman LS, Schatzkin A, Midthune D, Kipnis V (2011) Dealing with dietary measurement error in nutritional cohort studies. J Natl Cancer Inst 103:1086–1092

    Article  PubMed Central  PubMed  Google Scholar 

  35. Adlercreutz H (2002) Phyto-oestrogens and cancer. Lancet Oncol 3:364–373

    Article  PubMed  Google Scholar 

  36. Penttinen P, Jaehrling J, Damdimopoulos AE, Inzunza J, Lemmen JG, van der Saag P, Pettersson K, Gauglitz G, Makela S, Pongratz I (2007) Diet-derived polyphenol metabolite enterolactone is a tissue-specific estrogen receptor activator. Endocrinology 148:4875–4886. doi:10.1210/en.2007-0289

    Article  CAS  PubMed  Google Scholar 

  37. Wang L, Chen J, Thompson LU (2005) The inhibitory effect of flaxseed on the growth and metastasis of estrogen receptor negative human breast cancer xenografts is attributed to both its lignan and oil components. Int J Cancer 116:793–798

    Article  CAS  PubMed  Google Scholar 

  38. Kang X, Zhang Q, Wang S, Huang X, Jin S (2010) Effect of soy isoflavones on breast cancer recurrence and death for patients receiving adjuvant endocrine therapy. CMAJ 182:1857–1862. doi:10.1503/cmaj.091298

    Article  PubMed Central  PubMed  Google Scholar 

  39. de Kleijn MJ, van der Schouw YT, Wilson PW, Grobbee DE, Jacques PF (2002) Dietary intake of phytoestrogens is associated with a favorable metabolic cardiovascular risk profile in postmenopausal U.S.women: the Framingham study. J Nutr 132(2):276–282

    PubMed  Google Scholar 

  40. Jordan VC (2014) Avoiding the bad and enhancing the good of soy supplements in breast cancer. J Natl Cancer Inst 106(9). doi:10.1093/jnci/dju233

  41. Shike M, Doane AS, Russo L, Cabal R, Reis-Filho JS, Gerald W, Cody H, Khanin R, Bromberg J, Norton L (2014) The effects of soy supplementation on gene expression in breast cancer: a randomized placebo-controlled study. J Natl Cancer Inst 106(9). doi:10.1093/jnci/dju189

Download references

Acknowledgments

The authors thank Bertrand Hemon, Katja Boll, and Nick Martinussen for help with data management.

Funding

This work was funded by Innovation Fund Denmark (ELIN: 0603-00580B). The coordination of EPIC is financially supported by the European Commission (DG-SANCO) and the International Agency for Research on Cancer. The national cohorts are supported by Danish Cancer Society (Denmark); Ligue Contre le Cancer, Institut Gustave Roussy, Mutuelle Générale de l’Education Nationale, Institut National de la Santé et de la Recherche Médicale (France); German Cancer Aid, German Cancer Research Center, Federal Ministry of Education and Research (Germany); the Hellenic Health Foundation (Greece); Associazione Italiana per la Ricerca sul Cancro-AIRC-Italy, and National Research Council (Italy); Dutch Ministry of Public Health, Welfare and Sports, Netherlands Cancer Registry, LK Research Funds, Dutch Prevention Funds, Dutch Zorg Onderzoek Nederland, World Cancer Research Fund, Statistics Netherlands (The Netherlands); ERC-2009-AdG 232997, the Norwegian Research Council, Extrastiftelsen Helse og Rehabiliering med Extra-midler (Norway); Health Research Fund, Regional Governments of Andalucía, Asturias, Basque Country, Murcia (no. 6236) and Navarra, RETIC (RD06/0020/0091 and RD12/0036/0018) (Spain); Swedish Cancer Society, Swedish Scientific Council and Regional Government of Skåne and Västerbotten (Sweden); and Cancer Research UK, Medical Research Council (UK).

Author information

Authors and Affiliations

  1. Danish Cancer Society Research Center, Strandboulevarden 49, 2100, Copenhagen, Denmark

    Cecilie Kyrø, Anne Tjønneland, Christoffer Johansen, Pernille Envold Bidstrup, Jane Christensen & Anja Olsen

  2. International Agency for Research on Cancer (WHO–IARC), Lyon, France

    Cecilie Kyrø, Raul Zamora-Ros, Augustin Scalbert & Isabelle Romieu

  3. Inserm, CESP Centre for Research in Epidemiology and Population Health, Villejuif, France

    Laure Dossus, Mathilde His, Françoise Clavel-Chapelon & Laura Baglietto

  4. Université Paris-Sud, Villejuif, France

    Laure Dossus, Mathilde His, Françoise Clavel-Chapelon & Laura Baglietto

  5. 5073, Oncology Clinic, Finsen Centre, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark

    Christoffer Johansen

  6. Department of Community Medicine, Faculty of Health Sciences, University of Tromsø, The Arctic University of Norway, Tromsø, Norway

    Elisabete Weiderpass & Guri Skeie

  7. Department of Research, Cancer Registry of Norway, Institute of Population Based Cancer Research, Oslo, Norway

    Elisabete Weiderpass

  8. Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden

    Elisabete Weiderpass

  9. Genetic Epidemiology Group, Folkhälsan Research Center, Samfundet Folkhälsan, Helsinki, Finland

    Elisabete Weiderpass

  10. Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK

    Heather Ward, Dagfinn Aune, Elio Riboli, H. B(as). Bueno-de-Mesquita & Petra H. Peeters

  11. Gustave Roussy, Villejuif, France

    Mathilde His, Françoise Clavel-Chapelon & Laura Baglietto

  12. Cancer Epidemiology Centre, Cancer Council of Victoria, Melbourne, VIC, Australia

    Laura Baglietto

  13. Centre for Epidemiology and Biostatistics, School of Population and Global Health, University of Melbourne, Melbourne, VIC, Australia

    Laura Baglietto

  14. Division of Cancer Epidemiology, German Cancer Research Center, DKFZ, Heidelberg, Germany

    Verena Katzke & Tilman Kühn

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

    Heiner Boeing & Anna Floegel

  16. Section for Epidemiology, Department of Public Health, Aarhus University, Aarhus, Denmark

    Kim Overvad

  17. Department of Functional Biology, Faculty of Medicine, University of Oviedo, Asturias, Spain

    Cristina Lasheras

  18. Unit of Nutrition and Cancer, Catalan Institute of Oncology (ICO-IDIBELL), Barcelona, Spain

    Noémie Travier

  19. Escuela Andaluza de Salud Pública, Instituto de Investigación Biosanitaria ibs.GRANADA, Hospitales Universitarios de Granada/Universidad de Granada, Granada, Spain

    Maria-José Sánchez

  20. CIBER de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain

    Maria-José Sánchez, Pilar Amiano, Maria-Dolores Chirlaque & Eva Ardanaz

  21. Public Health Division of Gipuzkoa, BioDonostia Research Institute, San Sebastián, Spain

    Pilar Amiano

  22. Department of Epidemiology, Regional Health Council, IMIB-Arrixaca, Murcia, Spain

    Maria-Dolores Chirlaque

  23. Department of Health and Social Sciences, Universidad de Murcia, Murcia, Spain

    Maria-Dolores Chirlaque

  24. Navarra Public Health Institute, Pamplona, Spain

    Eva Ardanaz

  25. Navarra Institute for Health Research (IdiSNA), Pamplona, Spain

    Eva Ardanaz

  26. Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK

    Kay-Tee Khaw

  27. MRC Epidemiology Unit, University of Cambridge, Cambridge, UK

    Nick Wareham

  28. Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, UK

    Aurora Perez-Cornago

  29. Hellenic Health Foundation, Athens, Greece

    Antonia Trichopoulou, Pagona Lagiou & Effie Vasilopoulou

  30. WHO Collaborating Center for Nutrition and Health, Unit of Nutritional Epidemiology and Nutrition in Public Health, Department of Hygiene, Epidemiology and Medical Statistics, University of Athens Medical School, Athens, Greece

    Antonia Trichopoulou, Pagona Lagiou & Effie Vasilopoulou

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

    Giovanna Masala

  32. Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy

    Sara Grioni & Franco Berrino

  33. Cancer Registry and Histopathology Unit, “Civile–M.P. Arezzo” Hospital, ASP, Ragusa, Italy

    Rosario Tumino

  34. Cancer Epidemiology Unit, San Giovanni Battista Hospital, CPO Piemonte and University of Turin, Turin, Italy

    Carlotta Sacerdote

  35. Dipartimento di Medicina Clinica e Chirurgia, Federico II University, Naples, Italy

    Amalia Mattiello

  36. Department for Determinants of Chronic Diseases (DCD), National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands

    H. B(as). Bueno-de-Mesquita

  37. Department of Gastroenterology and Hepatology, University Medical Centre, Utrecht, The Netherlands

    H. B(as). Bueno-de-Mesquita

  38. Department of Social & Preventive Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia

    H. B(as). Bueno-de-Mesquita

  39. Department of Epidemiology, Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The Netherlands

    Petra H. Peeters & Carla van Gils

  40. Division of Oncology and Pathology, Department of Clinical Sciences, Lund University, Lund, Sweden

    Signe Borgquist

  41. Department of Surgery, Clinical Sciences, Skåne University Hospital, Lund University, Malmö, Sweden

    Salma Butt

  42. Department of Population Health, NYU School of Medicine, New York, NY, USA

    Anne Zeleniuch-Jacquotte

  43. Department of Surgical and Perioperative Sciences, Umeå University, Umeå, Sweden

    Malin Sund

  44. Department of Nutrition, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway

    Anette Hjartåker

Authors
  1. Cecilie Kyrø
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Raul Zamora-Ros
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Augustin Scalbert
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anne Tjønneland
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Laure Dossus
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Christoffer Johansen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pernille Envold Bidstrup
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Elisabete Weiderpass
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jane Christensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Heather Ward
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Dagfinn Aune
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Elio Riboli
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Mathilde His
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Françoise Clavel-Chapelon
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Laura Baglietto
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Verena Katzke
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Tilman Kühn
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Heiner Boeing
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Anna Floegel
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Kim Overvad
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Cristina Lasheras
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Noémie Travier
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Maria-José Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Pilar Amiano
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Maria-Dolores Chirlaque
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. Eva Ardanaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  27. Kay-Tee Khaw
    View author publications

    You can also search for this author in PubMed Google Scholar

  28. Nick Wareham
    View author publications

    You can also search for this author in PubMed Google Scholar

  29. Aurora Perez-Cornago
    View author publications

    You can also search for this author in PubMed Google Scholar

  30. Antonia Trichopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  31. Pagona Lagiou
    View author publications

    You can also search for this author in PubMed Google Scholar

  32. Effie Vasilopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  33. Giovanna Masala
    View author publications

    You can also search for this author in PubMed Google Scholar

  34. Sara Grioni
    View author publications

    You can also search for this author in PubMed Google Scholar

  35. Franco Berrino
    View author publications

    You can also search for this author in PubMed Google Scholar

  36. Rosario Tumino
    View author publications

    You can also search for this author in PubMed Google Scholar

  37. Carlotta Sacerdote
    View author publications

    You can also search for this author in PubMed Google Scholar

  38. Amalia Mattiello
    View author publications

    You can also search for this author in PubMed Google Scholar

  39. H. B(as). Bueno-de-Mesquita
    View author publications

    You can also search for this author in PubMed Google Scholar

  40. Petra H. Peeters
    View author publications

    You can also search for this author in PubMed Google Scholar

  41. Carla van Gils
    View author publications

    You can also search for this author in PubMed Google Scholar

  42. Signe Borgquist
    View author publications

    You can also search for this author in PubMed Google Scholar

  43. Salma Butt
    View author publications

    You can also search for this author in PubMed Google Scholar

  44. Anne Zeleniuch-Jacquotte
    View author publications

    You can also search for this author in PubMed Google Scholar

  45. Malin Sund
    View author publications

    You can also search for this author in PubMed Google Scholar

  46. Anette Hjartåker
    View author publications

    You can also search for this author in PubMed Google Scholar

  47. Guri Skeie
    View author publications

    You can also search for this author in PubMed Google Scholar

  48. Anja Olsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  49. Isabelle Romieu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cecilie Kyrø.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 52 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kyrø, C., Zamora-Ros, R., Scalbert, A. et al. Pre-diagnostic polyphenol intake and breast cancer survival: the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. Breast Cancer Res Treat 154, 389–401 (2015). https://doi.org/10.1007/s10549-015-3595-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10549-015-3595-9

Keywords

Search

Navigation