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Epidemiology

Dietary intake of total, heme and non-heme iron and the risk of colorectal cancer in a European prospective cohort study

British Journal of Cancer volume 128, pages 1529–1540 (2023)Cite this article

Subjects

Abstract

Background

Iron is an essential micronutrient with differing intake patterns and metabolism between men and women. Epidemiologic evidence on the association of dietary iron and its heme and non-heme components with colorectal cancer (CRC) development is inconclusive.

Methods

We examined baseline dietary questionnaire-assessed intakes of total, heme, and non-heme iron and CRC risk in the EPIC cohort. Sex-specific multivariable-adjusted hazard ratios (HRs) and 95% confidence intervals (CIs) were computed using Cox regression. We modelled substitution of a 1 mg/day of heme iron intake with non-heme iron using the leave one-out method.

Results

Of 450,105 participants (318,680 women) followed for 14.2 ± 4.0 years, 6162 (3511 women) developed CRC. In men, total iron intake was not associated with CRC risk (highest vs. lowest quintile, HRQ5vs.Q1:0.88; 95%CI:0.73, 1.06). An inverse association was observed for non-heme iron (HRQ5vs.Q1:0.80, 95%CI:0.67, 0.96) whereas heme iron showed a non-significant association (HRQ5vs.Q1:1.10; 95%CI:0.96, 1.27). In women, CRC risk was not associated with intakes of total (HRQ5vs.Q1:1.11, 95%CI:0.94, 1.31), heme (HRQ5vs.Q1:0.95; 95%CI:0.84, 1.07) or non-heme iron (HRQ5vs.Q1:1.03, 95%CI:0.88, 1.20). Substitution of heme with non-heme iron demonstrated lower CRC risk in men (HR:0.94; 95%CI: 0.89, 0.99).

Conclusions

Our findings suggest potential sex-specific CRC risk associations for higher iron consumption that may differ by dietary sources.

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Fig. 1: Splines of the associations between dietary iron intake and colorectal risk in men and women.

Data availability

For information on how to submit an application for gaining access to EPIC data and/or biospecimens, please follow the instructions at http://epic.iarc.fr/access/index.php.

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Acknowledgements

The authors would like to thank the EPIC study participants and staff for their valuable contribution to this research. The coordination of EPIC is financially supported by International Agency for Research on Cancer (IARC) and also by the Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London which has additional infrastructure support provided by the NIHR Imperial Biomedical Research Centre (BRC). 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 Center (DKFZ), German Institute of Human Nutrition PotsdamRehbruecke (DIfE), Federal Ministry of Education and Research (BMBF) (Germany); Associazione Italiana per la Ricerca sul Cancro-AIRC-Italy, Compagnia di SanPaolo 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); Health Research Fund (FIS), Instituto de Salud Carlos III (ISCIII), Regional Governments of Andalucía, Asturias, Basque Country, Murcia and Navarra, and the Catalan Institute of Oncology, ICO (Spain); Swedish Cancer Society, Swedish Research Council, Region Skåne and Region Västerbotten (Sweden); Cancer Research UK (14136 to EPIC-Norfolk; C8221/A29017 to EPIC-Oxford), Medical Research Council (1000143 to EPIC-Norfolk; MR/M012190/1 to EPIC-Oxford). (United Kingdom). VF is supported by the Cancer Prevention and Research Institute of Texas (CPRIT) Rising Stars Award (Grant ID RR200056). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the paper.

Funding

Internal funds of the IARC were used to support these analyses.

Author information

Authors and Affiliations

  1. Nutrition and Metabolism Branch, International Agency for Research on Cancer, Lyon, France

    Elom K. Aglago, Heinz Freisling, Marc J. Gunter, Corinne Casagrande, Inge Huybrechts & Mazda Jenab

  2. Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom

    Elom K. Aglago, Amanda J. Cross, Elio Riboli, Alicia K. Heath & Konstantinos K. Tsilidis

  3. Department of Epidemiology, University of Texas M. D. Anderson Cancer Center, Houston, TX, USA

    Veronika Fedirko

  4. Department of Epidemiology, Rollins School of Public Health, Emory University, Atlanta, GA, USA

    Veronika Fedirko

  5. Cancer Biology and Therapeutics Group (CBT), Conway Institute, School of Biomolecular and Biomedical Science (SBBS), University College Dublin, Dublin, Ireland

    David J. Hughes

  6. Centre de Recherche en Epidémiologie et Santé des Populations, Université Paris-Sud, UVSQ, INSERM, Université Paris-Saclay, Villejuif, France

    Agnes Fournier, Marie-Christine Boutron-Ruault, Joseph A. Rothwell & Gianluca Severi

  7. Institut Gustave Roussy, Villejuif, France

    Agnes Fournier, Marie-Christine Boutron-Ruault, Joseph A. Rothwell & Gianluca Severi

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

    Paula Jakszyn

  9. Blanquerna School of Health Sciences, Ramon Llull University, Barcelona, Spain

    Paula Jakszyn

  10. Department of Public Health, Aarhus University, Aarhus, Denmark

    Christina C. Dahm & Kim Overvad

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

    Kim Overvad

  12. Danish Cancer Society Research Center, Copenhagen, Denmark

    Anne Tjønneland & Cecilie Kyrø

  13. Department of Public Health, Section of Environmental Health, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark

    Anne Tjønneland

  14. Department of Statistics, Computer Science, Applications “G. Parenti”, University of Florence, Florence, Italy

    Gianluca Severi

  15. Division of Cancer Epidemiology, German Cancer research Center (DKFZ), Heidelberg, Germany

    Verena Katzke & Bernard Srour

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

    Matthias B. Schulze & Clemens Wittenbecher

  17. Institute of Nutritional Science, University of Potsdam, Potsdam, Germany

    Matthias B. Schulze

  18. Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA, USA

    Clemens Wittenbecher

  19. German Center for Diabetes Research (DZD), Neuherberg, Germany

    Clemens Wittenbecher

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

    Domenico Palli

  21. Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Via Venezian, 120133, Milano, Italy

    Sabina Sieri

  22. Internal Medicine and Clinical Nutrition Unit, Department of Clinical Medicine and Surgery, Federico II University Hospital, Naples, Italy

    Fabrizio Pasanisi

  23. Hyblean Association for Epidemiological Research, AIRE-ONLUS, 97100, Ragusa, Italy

    Rosario Tumino

  24. Department of Clinical and Biological Sciences, University of Turin, Turin, Italy

    Fulvio Ricceri

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

    Fulvio Ricceri

  26. Former senior scientist, Department for Determinants of Chronic Diseases (DCD), National Institute for Public Health and the Environment (RIVM), PO Box 1, 3720 BA, Bilthoven, The Netherlands

    Bas Bueno-de-Mesquita

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

    Jeroen W. G. Derksen

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

    Guri Skeie, Torill Enget Jensen & Marko Lukic

  29. Escuela Andaluza de Salud Pública (EASP), Granada, Spain

    Maria-Jose Sánchez

  30. Instituto de Investigación Biosanitaria ibs.GRANADA, Granada, Spain

    Maria-Jose Sánchez

  31. Department of Preventive Medicine and Public Health, University of Granada, Granada, Spain

    Maria-Jose Sánchez

  32. Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), Madrid, Spain

    Maria-Jose Sánchez, Pilar Amiano, Sandra Colorado-Yohar & Aurelio Barricarte

  33. Ministry of Health of the Basque Government, Sub-Directorate for Public Health and Addictions of Gipuzkoa, San Sebastián, Spain

    Pilar Amiano

  34. Biodonostia Health Research Institute, Epidemiology and Public Health Area, San Sebastián, Spain

    Pilar Amiano

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

    Sandra Colorado-Yohar

  36. Research Group on Demography and Health, National Faculty of Public Health, University of Antioquia, Medellín, Colombia

    Sandra Colorado-Yohar

  37. Navarra Public Health Institute, Pamplona, Spain

    Aurelio Barricarte

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

    Aurelio Barricarte

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

    Ulrika Ericson

  40. Department of Radiation Sciences, Wallenberg Centre for Molecular Medicine, Umeå University, Umeå, Sweden

    Bethany van Guelpen

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

    Keren Papier & Anika Knuppel

Authors
  1. Elom K. Aglago
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  2. Amanda J. Cross
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  3. Elio Riboli
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  4. Veronika Fedirko
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  5. David J. Hughes
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  6. Agnes Fournier
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  7. Paula Jakszyn
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  8. Heinz Freisling
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  9. Marc J. Gunter
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  10. Christina C. Dahm
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  11. Kim Overvad
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  12. Anne Tjønneland
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  13. Cecilie Kyrø
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  14. Marie-Christine Boutron-Ruault
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  15. Joseph A. Rothwell
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  16. Gianluca Severi
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  17. Verena Katzke
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  18. Bernard Srour
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  19. Matthias B. Schulze
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  20. Clemens Wittenbecher
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  21. Domenico Palli
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  22. Sabina Sieri
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  23. Fabrizio Pasanisi
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  24. Rosario Tumino
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  25. Fulvio Ricceri
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  26. Bas Bueno-de-Mesquita
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  27. Jeroen W. G. Derksen
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  28. Guri Skeie
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  29. Torill Enget Jensen
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  30. Marko Lukic
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  31. Maria-Jose Sánchez
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  32. Pilar Amiano
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  33. Sandra Colorado-Yohar
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  34. Aurelio Barricarte
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  35. Ulrika Ericson
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  36. Bethany van Guelpen
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  37. Keren Papier
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  38. Anika Knuppel
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  39. Corinne Casagrande
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  40. Inge Huybrechts
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  41. Alicia K. Heath
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  42. Konstantinos K. Tsilidis
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  43. Mazda Jenab
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Contributions

Conception and design: MJ, EKA, Acquisition and interpretation of data: all authors; Performed analyses: EKA, MJ, Drafted the paper: EKA, AJC, ER, VF, PJ, HF, DJH; Critically revised paper: all authors; Approved of final submission: all authors.

Corresponding author

Correspondence to Mazda Jenab.

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Aglago, E.K., Cross, A.J., Riboli, E. et al. Dietary intake of total, heme and non-heme iron and the risk of colorectal cancer in a European prospective cohort study. Br J Cancer 128, 1529–1540 (2023). https://doi.org/10.1038/s41416-023-02164-7

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