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Citrus intake and risk of skin cancer in the European Prospective Investigation into Cancer and Nutrition cohort (EPIC)

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Abstract

Citrus intake has been suggested to increase the risk of skin cancer. Although this relation is highly plausible biologically, epidemiologic evidence is lacking. We aimed to examine the potential association between citrus intake and skin cancer risk. EPIC is an ongoing multi-center prospective cohort initiated in 1992 and involving ~ 520,000 participants who have been followed-up in 23 centers from 10 European countries. Dietary data were collected at baseline using validated country-specific dietary questionnaires. We used Cox proportional hazards regression models to compute hazard ratios (HR) and 95% confidence intervals (CI). During a mean follow-up of 13.7 years, 8448 skin cancer cases were identified among 270,112 participants. We observed a positive linear dose–response relationship between total citrus intake and skin cancer risk (HR = 1.10, 95% CI 1.03–1.18 in the highest vs. lowest quartile; Ptrend = 0.001), particularly with basal cell carcinoma (BCC) (HR = 1.11, 95% CI 1.02–1.20, Ptrend = 0.007) and squamous cell carcinoma (SCC) (HR = 1.23, 95% CI 1.04–1.47, Ptrend = 0.01). Citrus fruit intake was positively associated with skin cancer risk (HR = 1.08, 95% CI 1.01–1.16, Ptrend = 0.01), particularly with melanoma (HR = 1.23, 95% CI 1.02–1.48; Ptrend = 0.01), although with no heterogeneity across skin cancer types (Phomogeneity = 0.21). Citrus juice was positively associated with skin cancer risk (Ptrend = 0.004), particularly with BCC (Ptrend = 0.008) and SCC (Ptrend = 0.004), but not with melanoma (Phomogeneity = 0.02). Our study suggests moderate positive linear dose–response relationships between citrus intake and skin cancer risk. Studies with available biomarker data and the ability to examine sun exposure behaviors are warranted to clarify these associations and examine the phototoxicity mechanisms of furocoumarin-rich foods.

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Abbreviations

BCCs:

Basal-cell carcinomas

BMI:

Body mass index

CIs:

Confidence intervals

E3N:

Etude Epidemiologique auprès de femmes de l’Education Nationale

EPIC:

European Prospective Investigation into Cancer and Nutrition

HPFS:

Health professionals follow-up study

HR:

Hazard ratio

IARC:

International Agency for Research on Cancer

KCs:

Keratinocyte cancers

METs:

Metabolic equivalents of task

NHS:

Nurses’ health study

PUVA:

Psoralen and ultraviolet radiation A radiation

SCCs:

Squamous-cell carcinomas

SD:

Standard deviation

UV:

Ultraviolet radiation

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Acknowledgements

We thank all study participants for their cooperation and all interviewers who participated in the fieldwork studies in each EPIC center. We also thank Bertrand Hemon at IARC for his valuable work and technical support with the EPIC database. IARC disclaimer: Where authors are identified as personnel of the International Agency for Research on Cancer/World Health Organization, the authors alone are responsible for the views expressed in this article and they do not necessarily represent the decisions, policy or views of the International Agency for Research on Cancer/World Health Organization.

Funding

Yahya Mahamat-Saleh was supported by a research scholarship from the Paris Ile-de-France region. 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); the French National Institute of Health and Medical Research (Inserm), the Mutuelle Générale de l’Education Nationale, the Gustave Roussy Institute, and the French League against Cancer (France); Deutsche Krebshilfe, Deutsches Krebsforschungszentrum (DKFZ); and Federal Ministry of Education and Research (Germany); Stavros Niarchos Foundation; the Hellenic Health Foundation; and Ministry of Health and Social Solidarity (Greece); Italian Association for Research on Cancer (AIRC); National Research Council; and AIRE-ONLUS Ragusa, AVIS Ragusa, Sicilian Government (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); the National Institute for Public Health and the Environment (RIVM) and Statistics Netherlands (the Netherlands); European Research Council (ERC) (Grant Number ERC-2009-AdG 232997) and Nordforsk; and 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; and ISCIII RETIC (RD06/0020) and the Catalan Institute of Oncology (Spain); Swedish Cancer Society; Swedish Scientific Council; and Regional Government of Skåne and Västerbotten (Sweden); Cancer Research UK (14136 to EPIC-Norfolk; C570/A16491 and C8221/A19170 for EPIC-Oxford); Medical Research Council (1000143 to EPIC-Norfolk, MR/M012190/1 to EPIC-Oxford); Stroke Association; British Heart Foundation; Department of Health; Food Standards Agency; and Wellcome Trust (UK). Reza Ghiasvand was supported by a grant (Project 6823329) from the Norwegian Cancer Society.

Author information

Authors and Affiliations

  1. CESP, Fac. de médecine - Univ. Paris-Sud, Fac. de médecine - UVSQ, INSERM, Université Paris Saclay, 94 805, Villejuif, France

    Yahya Mahamat-Saleh, Iris Cervenka, Marie Al-Rahmoun, Francesca R. Mancini, Gianluca Severi, Marie-Christine Boutron-Ruault & Marina Kvaskoff

  2. Inserm UMR1018, Gustave Roussy, 114 Rue Edouard Vaillant, F-94805, Villejuif, France

    Yahya Mahamat-Saleh, Iris Cervenka, Marie Al-Rahmoun, Francesca R. Mancini, Gianluca Severi, Marie-Christine Boutron-Ruault & Marina Kvaskoff

  3. Oslo Centre for Biostatistics and Epidemiology, Department of Biostatistics, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway

    Reza Ghiasvand & Marit B. Veierod

  4. Cancer Risk Factors and Lifestyle Epidemiology Unit, Cancer Research, Prevention and Clinical Network Institute (ISPRO), Florence, Italy

    Saverio Caini & Domenico Palli

  5. Department of Bowel Cancer Screening, Cancer Registry of Norway, Oslo University Hospital, Oslo, Norway

    Edoardo Botteri

  6. Norwegian National Advisory Unit for Women’s Health, Women’s Clinic, Oslo University Hospital, Oslo, Norway

    Edoardo Botteri

  7. Piedmont Reference Centre for Epidemiology and Cancer Prevention (CPO Piemonte), Turin, 10126, Italy

    Carlotta Sacerdote

  8. Epidemiology Unit, ASL TO3, Piedmont Region, Grugliasco, 10095, Italy

    Fulvio Ricceri

  9. Hellenic Health Foundation, Athens, Greece

    Antonia Trichopoulou, Eleni Peppa & Carlo La Vecchia

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

    Carlo La Vecchia

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

    Kim Overvad & Christina C. Dahm

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

    Kim Overvad

  13. Danish Cancer Society Research Center, Copenhagen, Denmark

    Anja Olsen & Anne Tjønneland

  14. Department of Public Health, University of Copenhagen, Copenhagen, Denmark

    Anne Tjønneland

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

    Aurora Perez-Cornago

  16. Unit of Nutrition and Cancer, Cancer Epidemiology Research Programme, Catalan Institute of Oncology, ĹHospitallet de Llobregat, Barcelona, Spain

    Paula Jakszyn

  17. Facultat de Ciències de la Salut Blanquerna, Universitat Ramón Llull, Barcelona, Spain

    Paula Jakszyn

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

    Sara Grioni

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

    Matthias B. Schulze

  20. Institute of Nutritional Sciences, University of Potsdam, Nuthetal, Germany

    Matthias B. Schulze

  21. Department of Community Medicine, University of Tromsø, The Arctic University of Norway, Tromsø, Norway

    Guri Skeie

  22. Department of Functional Biology, University of Oviedo, Asturias, Spain

    Cristina Lasheras

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

    Sandra Colorado-Yohar

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

    Sandra Colorado-Yohar, Miguel Rodríguez-Barranco & Pilar Amiano

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

    Sandra Colorado-Yohar

  26. Andalusian School of Public Health (EASP), Granada, Spain

    Miguel Rodríguez-Barranco

  27. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Universidad de Granada, Granada, Spain

    Miguel Rodríguez-Barranco

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

    Tilman Kühn & Verena A. Katzke

  29. Public Health Division of Gipuzkoa, BioDonostia Research Institue, Donostia-San Sebastian, Spain

    Pilar Amiano

  30. Cancer Registry and Histopathology Department, Civic-M. P. Arezzo Hospital, ASP Ragusa, Ragusa, Italy

    Rosario Tumino

  31. Dipartimento di Medicina Clinica e Sperimentale, Federico II University, Naples, Italy

    Salvatore Panico

  32. Clínica Universidad de Navarra, Pamplona, Spain

    Ana Ezponda

  33. Nutritional Epidemiology, Department of Clinical Sciences Malmö, Lund University, Malmö, Sweden

    Emily Sonestedt

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

    Augustin Scalbert

  35. International Agency for Research on Cancer, World Health Organization, Lyon, France

    Elisabete Weiderpass

Authors
  1. Yahya Mahamat-Saleh
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  2. Iris Cervenka
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  3. Marie Al-Rahmoun
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  4. Francesca R. Mancini
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  8. Saverio Caini
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  37. Marie-Christine Boutron-Ruault
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  38. Marina Kvaskoff
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Correspondence to Marina Kvaskoff.

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Mahamat-Saleh, Y., Cervenka, I., Al-Rahmoun, M. et al. Citrus intake and risk of skin cancer in the European Prospective Investigation into Cancer and Nutrition cohort (EPIC). Eur J Epidemiol 35, 1057–1067 (2020). https://doi.org/10.1007/s10654-020-00666-9

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