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Epidemiology

Haem iron intake and risk of lung cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort

European Journal of Clinical Nutrition volume 73, pages 1122–1132 (2019)Cite this article

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Abstract

Background

Epidemiological studies suggest that haem iron, which is found predominantly in red meat and increases endogenous formation of carcinogenic N-nitroso compounds, may be positively associated with lung cancer. The objective was to examine the relationship between haem iron intake and lung cancer risk using detailed smoking history data and serum cotinine to control for potential confounding.

Methods

In the European Prospective Investigation into Cancer and Nutrition (EPIC), 416,746 individuals from 10 countries completed demographic and dietary questionnaires at recruitment. Cox proportional hazards models were used to estimate hazard ratios (HRs) and 95% confidence intervals (CIs) for incident lung cancer (n = 3731) risk relative to haem iron, non-haem iron, and total dietary iron intake. A corresponding analysis was conducted among a nested subset of 800 lung cancer cases and 1489 matched controls for whom serum cotinine was available.

Results

Haem iron was associated with lung cancer risk, including after adjustment for details of smoking history (time since quitting, number of cigarettes per day): as a continuous variable (HR per 0.3 mg/1000 kcal 1.03, 95% CI 1.00–1.07), and in the highest versus lowest quintile (HR 1.16, 95% CI 1.02–1.32; trend across quintiles: P = 0.035). In contrast, non-haem iron intake was related inversely with lung cancer risk; however, this association attenuated after adjustment for smoking history. Additional adjustment for serum cotinine did not considerably alter the associations detected in the nested case–control subset.

Conclusions

Greater haem iron intake may be modestly associated with lung cancer risk.

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Acknowledgements

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 (INSERM) (France); German Cancer Aid, German Cancer Research Centre (DKFZ), Federal Ministry of Education and Research (BMBF), Deutsche Krebshilfe, Deutsches Krebsforschungszentrum and 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 (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 Centre of Excellence programme on Food, Nutrition and Health (Norway); Health Research Fund (FIS), PI13/00061 to Granada, PI13/01162 to EPIC-Murcia, Regional Governments of Andalucía, Asturias, Basque Country, Murcia ((no. 6236) and Navarra, ISCIII RETIC (RD06/0020) (Spain); Swedish Cancer Society, Swedish Research Council and County Councils of Skåne and Västerbotten (Sweden); Cancer Research UK (14136 to K.T. Khaw, N.J. Wareham; C570/A16491 to RCT and C8221/A19170 to T. Key (EPIC-Oxford), Medical Research Council (1000143 to K.T. Khaw, N.J. Wareham, MR/M012190/1 to T. Key (EPIC-Oxford)) (United Kingdom).

Author Contributions

AJC originated the idea. AJC was responsible for the study design and data management. HW was responsible for the statistical analysis. AJC, HW and JW drafted the first version of the manuscript, contributed to interpretation of results and revised the manuscript critically for important intellectual content. All listed EPIC co-authors contributed data and reviewed the final manuscript.

Author information

Authors and Affiliations

  1. School of Public Health, Imperial College London, London, UK

    Heather A. Ward, Julia Whitman, David C. Muller, H. Bas Bueno-de-Mesquita, Petra H. Peeters, Melissa A. Merritt, Elio Riboli & Amanda J. Cross

  2. International Agency for Research on Cancer, Lyon, France

    Mattias Johansson, Anouar Fanidi, Heinz Freisling & Magdalena Stepien

  3. Unit of Nutrition, Environment and Cancer, Catalan Institute of Oncology, Barcelona, Spain

    Paula Jakszyn

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

    Elisabete Weiderpass, Therese Haugdahl Nøst & Torkjel M. Sandanger

  5. Department of Research, Cancer Registry of Norway, Institute of Population-based Cancer Research, Oslo, Norway

    Elisabete Weiderpass

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

    Elisabete Weiderpass

  7. Genetic Epidemiology Group, Folkhälsan Research Center and Faculty of Medicine, University of Helsinki, Helsinki, Finland

    Elisabete Weiderpass

  8. Cancer Risk Factors and Life-Style Epidemiology Unit, Institute for Cancer Research, Prevention and Clinical Network, Florence, Italy

    Domenico Palli

  9. Division of Environmental Epidemiology, Institute for Risk Assessment Sciences, Utrecht University, Utrecht, The Netherlands

    Roel Vermeulen

  10. Danish Cancer Society Research Centre, Copenhagen, Denmark

    Anne Tjønneland & Louise Hansen

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

    Christina C. Dahm & Kim Overvad

  12. Department of Cardiology, Aalborg University Hospital, Aalborg, Denmark

    Kim Overvad

  13. Human Genetics Foundation, Torino, Italy

    Gianluca Severi

  14. CESP Inserm, Facultés de Medicine Université Paris-Sud, UVSQ, Université Paris-Saclay, Gustave Roussy, Villejuif, France

    Gianluca Severi, Marie-Christine Boutron-Ruault & Aurélie Affret

  15. Division of Cancer Epidemiology, German Cancer Research Centre, Heidelberg, Germany

    Rudolf Kaaks & Renee Fortner

  16. Department of Epidemiology, German Institute of Human Nutrition, Potsdam-Rehbrücke, Germany

    Heiner Boeing

  17. Hellenic Health Foundation, Athens, Greece

    Antonia Trichopoulou, Carlo La Vecchia & Anastasia Kotanidou

  18. WHO Collaborating Centre for Nutrition and Health, Unit of Nutritional Epidemiology and Nutrition in Public Health, Department of Hygiene, Epidemiology and Medical Statistics, School of Medicine, National and Kapodistrian University of Athens, Athens, Greece

    Antonia Trichopoulou

  19. Department of Clinical Sciences and Community Health, Università degli Studi di Milano, Milan, Italy

    Carlo La Vecchia

  20. 1st Department of Critical Care Medicine & Pulmonary Services, University of Athens Medical School, Evangelismos Hospital, Athens, Greece

    Anastasia Kotanidou

  21. Fondazione IRCCS National Cancer Institute, Milan, Italy

    Franco Berrino & Vittorio Krogh

  22. Cancer Registry and Histopathology Unit, “Civic - M.P.Arezzo” Hospital, ASP Ragusa, Italy

    Rosario Tumino

  23. Department of Clinical and Biological Sciences, University of Turin, Orbassano, Italy

    Fulvio Ricceri

  24. Unit of Epidemiology, Regional Health Service, ASL TO3, Grugliasco, Italy

    Fulvio Ricceri

  25. Department of Clinical Medicine and Surgery, Federico II University, Naples, Italy

    Salvatore Panico

  26. Department for Determinants of Chronic Diseases, National Institute for Public Health and the Environment, Bilthoven, The Netherlands

    H. Bas Bueno-de-Mesquita

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

    Petra H. Peeters

  28. Public Health Directorate, Asturias, Spain

    Jose Ramón Quirós

  29. Unit of Nutrition and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology-IDIBELL. L’Hospitalet de Llobregat, Barcelona, Spain

    Antonio Agudo

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

    Miguel Rodríguez-Barranco

  31. CIBER Epidemiology and Public Health CIBERESP, Madrid, Spain

    Miguel Rodríguez-Barranco, Nerea Larrañaga, Jose Maria Huerta & Eva Ardanaz

  32. Public Health Division and BioDonostia Research Institute, San Sebastian, Spain

    Nerea Larrañaga & Eva Ardanaz

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

    Jose Maria Huerta & Eva Ardanaz

  34. Public Health Institute, Pamplona, Spain

    Eva Ardanaz & Eva Ardanaz

  35. IdiSNA, Navarra Institute for Health Research, Pamplona, Spain

    Eva Ardanaz

  36. Department of Clinical Sciences in Malmö, Lund University, Malmö, Sweden

    Isabel Drake

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

    Hans Brunnström

  38. Laboratory Medicine, Department of Pathology, Lund University, Malmö, Sweden

    Hans Brunnström

  39. Department of Radiation Sciences, Oncology, Umeå University, Umeå, Sweden

    Mikael Johansson

  40. Department of Medical Biosciences, Clinical Chemistry, Umeå University, Umeå, Sweden

    Kjell Grankvist

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

    Ruth C. Travis

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  1. Heather A. Ward
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Correspondence to Heather A. Ward.

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Ward, H.A., Whitman, J., Muller, D.C. et al. Haem iron intake and risk of lung cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. Eur J Clin Nutr 73, 1122–1132 (2019). https://doi.org/10.1038/s41430-018-0271-2

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