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Healthy lifestyle and the risk of pancreatic cancer in the EPIC study

  • Sabine Naudin
  • Vivian Viallon
  • Dana Hashim
  • Heinz Freisling
  • Mazda Jenab
  • Elisabete Weiderpass
  • Flavie Perrier
  • Fiona McKenzie
  • H Bas Bueno-de-Mesquita
  • Anja Olsen
  • Anne Tjønneland
  • Christina C. Dahm
  • Kim Overvad
  • Francesca R. Mancini
  • Vinciane Rebours
  • Marie-Christine Boutron-Ruault
  • Verena Katzke
  • Rudolf Kaaks
  • Manuela Bergmann
  • Heiner Boeing
  • Eleni Peppa
  • Anna Karakatsani
  • Antonia Trichopoulou
  • Valeria Pala
  • Giovana Masala
  • Salvatore Panico
  • Rosario Tumino
  • Carlotta Sacerdote
  • Anne M. May
  • Carla H. van Gils
  • Charlotta Rylander
  • Kristin Benjaminsen Borch
  • María Dolores Chirlaque López
  • Maria-Jose Sánchez
  • Eva Ardanaz
  • José Ramón Quirós
  • Pilar Amiano Exezarreta
  • Malin Sund
  • Isabel Drake
  • Sara Regnér
  • Ruth C. Travis
  • Nick Wareham
  • Dagfinn Aune
  • Elio Riboli
  • Marc J. Gunter
  • Eric J. Duell
  • Paul Brennan
  • Pietro FerrariEmail author
CANCER

Abstract

Pancreatic cancer (PC) is a highly fatal cancer with currently limited opportunities for early detection and effective treatment. Modifiable factors may offer pathways for primary prevention. In this study, the association between the Healthy Lifestyle Index (HLI) and PC risk was examined. Within the European Prospective Investigation into Cancer and Nutrition cohort, 1113 incident PC (57% women) were diagnosed from 400,577 participants followed-up for 15 years (median). HLI scores combined smoking, alcohol intake, dietary exposure, physical activity and, in turn, overall and central adiposity using BMI (HLIBMI) and waist-to-hip ratio (WHR, HLIWHR), respectively. High values of HLI indicate adherence to healthy behaviors. Cox proportional hazard models with age as primary time variable were used to estimate PC hazard ratios (HR) and 95% confidence intervals (CI). Sensitivity analyses were performed by excluding, in turn, each factor from the HLI score. Population attributable fractions (PAF) were estimated assuming participants’ shift to healthier lifestyles. The HRs for a one-standard deviation increment of HLIBMI and HLIWHR were 0.84 (95% CI: 0.79, 0.89; ptrend = 4.3e−09) and 0.77 (0.72, 0.82; ptrend = 1.7e−15), respectively. Exclusions of smoking from HLIWHR resulted in HRs of 0.88 (0.82, 0.94; ptrend = 4.9e−04). The overall PAF estimate was 19% (95% CI: 11%, 26%), and 14% (6%, 21%) when smoking was removed from the score. Adherence to a healthy lifestyle was inversely associated with PC risk, beyond the beneficial role of smoking avoidance. Public health measures targeting compliance with healthy lifestyles may have an impact on PC incidence.

Keywords

Pancreatic cancer Healthy Lifestyle Index Population attributable fraction EPIC Prospective study 

Abbreviations

BMI

Body Mass Index

CI

Confidence interval

EPIC

European Prospective Investigation into Cancer and Nutrition

HR

Hazard ratio

PC

Pancreatic cancer

PAF

Population attributable fraction

WHR

Waist-to-hip ratio

Notes

Acknowledgements

We thank Carine Biessy and Bertrand Hemon for their technical support and contribution to this work. We are also grateful to all the EPIC participants who have been part of the project and to the many other members of the study teams who have enabled this research.

Funding

This work was supported by the Direction Générale de la Santé (French Ministry of Health) (Grant GR-IARC-2003-09-12-01), by the European Commission (Directorate General for Health and Consumer Affairs) and the International Agency for Research on Cancer. The national cohorts are supported by the Danish Cancer Society (Denmark); the Ligue Contre le Cancer, the Institut Gustave Roussy, the Mutuelle Générale de l’Education Nationale and the Institut National de la Santé et de la Recherche Médicale (France); the Deutsche Krebshilfe, the Deutsches Krebsforschungszentrum, and the Federal Ministry of Education and Research (Germany); the Hellenic Health Foundation, the Stavros Niarchos Foundation and the Hellenic Ministry of Health and Social Solidarity (Greece); the Italian Association for Research on Cancer and the National Research Council (Italy); the Dutch Ministry of Public Health, Welfare and Sports, the Netherlands Cancer Registry, LK Research Funds, Dutch Prevention Funds, the Dutch Zorg Onderzoek Nederland, the World Cancer Research Fund and Statistics Netherlands (The Netherlands); the Health Research Fund, Regional Governments of Andalucýa, Asturias, Basque Country, Murcia (Project 6236) and Navarra, Instituto de Salud Carlos III, Redes de Investigacion Cooperativa (RD06/0020) (Spain); the Swedish Cancer Society, the Swedish Scientific Council and the Regional Government of Skåne (Sweden); Cancer Research UK (C864/A14136 to EPIC-Norfolk; C570/A16491 and C8221/A19170 to EPIC-Oxford), Medical Research Council (MR/N003284/1 and MC-UU_12015/1 to EPIC-Norfolk, MR/M012190/1 to EPIC-Oxford) (United Kingdom), the Stroke Association, the British Heart Foundation, the Department of Health, the Food Standards Agency, and the Wellcome Trust (UK). This work was part of Sabine Naudin’s PhD at Claude Bernard Lyon I University (France), funded by Région Auvergne Rhône-Alpes, ADR 2016 (France).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10654_2019_559_MOESM1_ESM.docx (21 kb)
Supplementary material 1 (DOCX 20 kb)

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Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Sabine Naudin
    • 1
  • Vivian Viallon
    • 1
  • Dana Hashim
    • 2
  • Heinz Freisling
    • 1
  • Mazda Jenab
    • 3
  • Elisabete Weiderpass
    • 4
  • Flavie Perrier
    • 1
  • Fiona McKenzie
    • 5
  • H Bas Bueno-de-Mesquita
    • 6
    • 7
    • 8
  • Anja Olsen
    • 9
  • Anne Tjønneland
    • 9
    • 10
  • Christina C. Dahm
    • 11
  • Kim Overvad
    • 11
    • 12
  • Francesca R. Mancini
    • 13
    • 14
  • Vinciane Rebours
    • 15
    • 16
  • Marie-Christine Boutron-Ruault
    • 13
    • 14
  • Verena Katzke
    • 17
  • Rudolf Kaaks
    • 17
  • Manuela Bergmann
    • 18
  • Heiner Boeing
    • 18
  • Eleni Peppa
    • 19
  • Anna Karakatsani
    • 19
    • 20
  • Antonia Trichopoulou
    • 19
    • 21
  • Valeria Pala
    • 22
  • Giovana Masala
    • 23
  • Salvatore Panico
    • 24
  • Rosario Tumino
    • 25
  • Carlotta Sacerdote
    • 26
  • Anne M. May
    • 27
  • Carla H. van Gils
    • 27
  • Charlotta Rylander
    • 28
  • Kristin Benjaminsen Borch
    • 28
  • María Dolores Chirlaque López
    • 29
    • 30
  • Maria-Jose Sánchez
    • 30
    • 31
  • Eva Ardanaz
    • 30
    • 32
    • 33
  • José Ramón Quirós
    • 34
  • Pilar Amiano Exezarreta
    • 30
    • 35
  • Malin Sund
    • 36
  • Isabel Drake
    • 37
  • Sara Regnér
    • 37
  • Ruth C. Travis
    • 38
  • Nick Wareham
    • 39
  • Dagfinn Aune
    • 8
    • 40
    • 41
  • Elio Riboli
    • 8
  • Marc J. Gunter
    • 3
  • Eric J. Duell
    • 42
  • Paul Brennan
    • 43
  • Pietro Ferrari
    • 1
    Email author
  1. 1.Nutritional Methodology and Biostatistics GroupInternational Agency for Research on Cancer, World Health OrganizationLyon Cedex 08France
  2. 2.Department of Hematology and Oncology, Tisch Cancer InstituteIcahn School of Medicine at Mount SinaiNew YorkUSA
  3. 3.Nutritional Epidemiology GroupInternational Agency for Research on Cancer, World Health OrganizationLyonFrance
  4. 4.Director OfficeInternational Agency for Research on Cancer, World Health OrganizationLyonFrance
  5. 5.Environment and Radiation sectionAgency for Research on Cancer, World Health OrganizationLyonFrance
  6. 6.Departement for Determinants of Chronic Diseases (Former)National Institute of Public Health and the Environment (RIVM)BilthovenThe Netherlands
  7. 7.Department of Gastroenterology and HepathologyUniversity Medical CenterUtrechtThe Netherlands
  8. 8.Department of Epidemiology and BiostatisticsSchool of Public Health, Imperial College LondonLondonUnited Kingdom
  9. 9.Danish Cancer Society Research CenterCopenhagenDenmark
  10. 10.Department of Public Health, Faculty of Health and Medical SciencesUniversity of CopenhagenCopenhagenDenmark
  11. 11.Section for Epidemiology, Department of Public HealthAarhus UniversityAarhusDenmark
  12. 12.Department of Cardiology, Aalborg University HospitalAalborgDenmark
  13. 13.CESP, Faculté de médecine (USVQ), Université Paris-Sud, INSERMUniversité Paris-SaclayVillejuifFrance
  14. 14.Inserm UMR1018Institut Gustave RoussyVillejuifFrance
  15. 15.Pancreatology DepartmentBeaujon Hospital, AP-HPClichyFrance
  16. 16.Inserm UMR1149, DHU UnitParis-Diderot UniversityParisFrance
  17. 17.Division of Cancer EpidemiologyGerman Cancer Research Center (DKFZ)HeidelbergGermany
  18. 18.German Institute of Human Nutrition, Potsdam-RehbrückeNuthetalGermany
  19. 19.Hellenic Health FoundationAthensGreece
  20. 20.Pulmonary Medicine Department, School of MedicineNational and Kapodistrian University of Athens, ATTIKON University Hospital of AthensHaidariGreece
  21. 21.School of Medicine, National and Kapodistrian University of AthensAthensGreece
  22. 22.Epidemiology and Prevention UnitFondazione IRCCS Istituto Nazionale dei TumoriMilanoItaly
  23. 23.Cancer Risk Factors and Life-Style Epidemiology UnitInstitute for Cancer Research, Prevention and Clinical Network - ISPROFlorenceItaly
  24. 24.Department of Clinical and Experimental MedecineUniversity Federico IINaplesItaly
  25. 25.Cancer Registry and Histopathology DepartmentCivic M.P.Arezzo HospitalRagusaItaly
  26. 26.Unit of Cancer Epidemiology, Città della Salute e della Scienza UniversityHospital and Center for Cancer Prevention (CPO)TurinItaly
  27. 27.Julius Center for Health Sciences and Primary Care, University Medical Center UtrechtUtrecht UniversityUtrechtThe Netherlands
  28. 28.Department of Community Medicine, Faculty of Health Sciences, University of TromsøThe Arctic University of NorwayTromsøNorway
  29. 29.Department of Epidemiology, Regional Health Council, IMIB-ArrixacaMurcia UniversityMurciaSpain
  30. 30.Spanish Consortium for Research and Public Health (CIBERESP)MadridSpain
  31. 31.Escuela Andaluza de Salud Pública, Instituto de Investigación BiosanitariaUniversidad de GranadaGranadaSpain
  32. 32.Navarra Public Health InstitutePamplonaSpain
  33. 33.IdiSNA, Navarra Institute for Health ResearchPamplonaSpain
  34. 34.Public Health DirectorateAsturiasSpain
  35. 35.Public Health Division of Gipuzkoa, BioDonostia Research InstituteSan SebastianSpain
  36. 36.Department of Surgical and Preoperative SciencesUmeå UniversityUmeåSweden
  37. 37.Department of Clinical Sciences in MalmöLund UniversityMalmöSweden
  38. 38.Cancer Epidemiology Unit, Nuffield Department of Clinical MedicineUniversity of OxfordOxfordUnited Kingdom
  39. 39.MRC Epidemiology Unit, Institute of Metabolic ScienceUniversity of CambridgeCambridgeUnited Kingdom
  40. 40.Department of NutritionBjørknes University CollegeOsloNorway
  41. 41.Department of Endocrinology, Morbid Obesity and Preventive MedicineOslo University HospitalOsloNorway
  42. 42.Unit of Nutrition and CancerCatalan Institute of Oncology (ICO-IDIBELL)BarcelonaSpain
  43. 43.Genetic Epidemiology GroupInternational Agency for Research on Cancer, World Health OrganizationLyonFrance

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