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Inflammatory potential of the diet and association with risk of differentiated thyroid cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort

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European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Chronic inflammation is thought to initiate or promote differentiated thyroid cancer (DTC) and previous studies have shown that diet can modulate this inflammatory process. We aimed to evaluate the association of several dietary scores reflecting the inflammatory potential of the diet with DTC risk.

Methods

Within the EPIC cohort, 450,063 participants were followed during a mean period of 14 years, and 712 newly incident DTC cases were identified. Associations between four dietary inflammatory scores [the dietary inflammatory index (DII®) and two energy-adjusted derivatives (the E-DIIr and the E-DIId), and the Inflammatory Score of the Diet (ISD)] and DTC risk were evaluated in the EPIC cohort using multivariable Cox regression models.

Results

Positive associations were observed between DTC risk and the DIIs (HR for 1 SD increase in DII: 1.11, 95%CI: 1.01, 1.23, similar results for its derivatives), but not with the ISD (HR for 1 SD increase: 1.04, 95% CI 0.93, 1.16).

Conclusion

Diet-associated inflammation, as estimated by the DII and its derivatives, was weakly positively associated with DTC risk in a European adult population. These results suggesting that diet-associated inflammation acts in the etiology of DTC need to be validated in independent studies.

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Data availability

EPIC data and biospecimens are available for investigators who seek to answer important questions on health and disease in the context of research projects that are consistent with the legal and ethical standard practices of IARC/WHO and the EPIC Centers. The primary responsibility for accessing the data obtained in the frame of the present publication belongs to the EPIC centers that provided them. The use of a random sample of anonymized data from the EPIC study can be requested by contacting epic@iarc.fr. The request will then be passed on to members of the EPIC Steering Committee for deliberation.

Abbreviations

BMI:

Body mass index

CI:

Confidence interval

CRP:

C-reactive protein

DII:

Dietary inflammatory index

DTC:

Differentiated thyroid cancer

E-DIId :

Dietary inflammatory index adjusted on energy intakes using the density method

E-DIIr :

Dietary inflammatory index adjusted on energy intakes using the residual method

EPIC:

European Prospective Investigation into Cancer and Nutrition

FFQ:

Food frequency questionnaire

HR:

Hazard ratio

IARC:

International Agency for Research on Cancer

IL:

Interleukin

ISD:

Inflammatory score of the diet

SD:

Standard deviation

TNF:

Tumor necrosis factor

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Acknowledgements

The authors thank all participants in the EPIC cohort for their invaluable contribution to the study. The authors also thank Bertrand Hémon (IARC) for his precious help with the EPIC database. We thank the National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands, for their contribution to, and ongoing support of, the EPIC Study. We acknowledge the use of data and biological samples from the EPIC-Oxford cohort, PI Tim Key, from the EPIC-Utrecht cohort, PI Roel Vermeulen, and from the EPIC-Asturias cohort, PI Ramón Quirós. We thank CERCA Program/Generalitat de Catalunya for the institutional support to IDIBELL. RZ-R and we would like to thank the “Miguel Servet” program (CPII20/00009) from the Institute of Health Carlos III (Spain) and the European Social Fund (ESF).

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

This work was supported by the Association pour la Recherche sur le Cancer (ARC) (Grant RF20180207126). The funders had no role in the design, analysis, or writing of this article. The coordination of EPIC is financially supported by the 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 Center (BRC). The national cohorts are supported by the following: 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), Agence Nationale pour la Recherche (ANR-10-COHO-0006) within the Investissement d’Avenir program, Ministère de l’enseignement supérieur, de la recherche et de l’innovation (MESRI, grant number 2103 586016) (France); German Cancer Aid, German Cancer Research Center (DKFZ), German Institute of Human Nutrition Potsdam Rehbruecke (DIfE), Federal Ministry of Education and Research (BMBF) (Germany); Associazione Italiana per la Ricerca sul Cancro-AIRC-Italy, Compagnia di San Paolo 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 (Spain); Swedish Cancer Society, Swedish Research Council and County Councils of Skåne and 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), (UK). The EPIC-Norfolk study (https://doi.org/10.22025/2019.10.105.00004) has received funding from the Medical Research Council (MR/N003284/1, MC-UU_12015/1 and MC_UU_00006/1) and Cancer Research UK (C864/A14136). We are grateful to all the participants who have been part of the project and to the many members of the study teams at the University of Cambridge who have enabled this research.

Author information

Author notes

  1. Marie-Christine Boutron-Ruault and Thérèse Truong contributed equally as last authors.

Authors and Affiliations

  1. Paris-Saclay University, UVSQ, Gustave Roussy, Inserm, CESP, Team “Exposome and Heredity”, 94807, Villejuif, France

    Lucie Lécuyer, Nasser Laouali, Marie-Christine Boutron-Ruault & Thérèse Truong

  2. Department of Biostatistics and Epidemiology, School of Public Health and Health Sciences, University of Massachusetts, Amherst, MA, USA

    Nasser Laouali

  3. Section of Nutrition and Metabolism, International Agency for Research On Cancer, 150, Cours Albert Thomas, 69008, Lyon, France

    Laure Dossus, Inge Huybrechts & Sabina Rinaldi

  4. Cancer Prevention and Control Program, University of South Carolina, Columbia, SC, USA

    Nitin Shivappa & James R. Hébert

  5. Department of Epidemiology and Biostatistics, Arnold School of Public Health, University of South Carolina, Columbia, SC, USA

    Nitin Shivappa & James R. Hébert

  6. Unit of Nutrition and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology (ICO), Bellvitge Biomedical Research Institute (IDIBELL), Barcelona, Spain

    Antonio Agudo & Raul Zamora-Ros

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

    Anne Tjonneland

  8. Danish Cancer Society Research Center, Institute of Cancer Epidemiology, Copenhagen, Denmark

    Anne Tjonneland & Jytte Halkjaer

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

    Kim Overvad

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

    Verena A. Katzke & Charlotte Le Cornet

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

    Matthias B. Schulze & Franziska Jannasch

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

    Matthias B. Schulze & Franziska Jannasch

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

    Domenico Palli

  14. Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale Dei Tumori, Milan, Italy

    Claudia Agnoli

  15. Hyblean Association for Epidemiological Research, A.I.R.E.-O.N.L.U.S., Ragusa, Italy

    Rosario Tumino

  16. Unit of Cancer Epidemiology, Città della Salute e della Scienza University-Hospital, 10126, Turin, Italy

    Luca Dragna

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

    Gabriella Iannuzzo

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

    Torill Enget Jensen, Magritt Brustad & Guri Skeie

  19. The Public Dental Service Competence Centre of Northern Norway (TkNN), Tromsø, Norway

    Magritt Brustad

  20. Escuela Andaluza de Salud Pública (EASP), 18011, Granada, Spain

    Miguel Rodriguez-Barranco

  21. Instituto de Investigación Biosanitaria Ibs.GRANADA, 18012, Granada, Spain

    Miguel Rodriguez-Barranco

  22. Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), 28029, Madrid, Spain

    Miguel Rodriguez-Barranco & Eva Ardanaz

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

    Pilar Amiano

  24. Epidemiology of Chronic and Communicable Diseases Group, Biodonostia Health Research Institute, San Sebastián, Spain

    Pilar Amiano

  25. Spanish Consortium for Research on Epidemiology and Public Health (CIBERESP), Instituto de Salud Carlos III, Madrid, Spain

    Pilar Amiano

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

    María-Dolores Chirlaque

  27. CIBER in Epidemiology and Public Health (CIBERESP), Madrid, Spain

    María-Dolores Chirlaque

  28. Navarra Public Health Institute, Pamplona, Spain

    Eva Ardanaz

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

    Eva Ardanaz

  30. Department of Clinical Sciences Lund, Skåne University Hospital, Lund University, Lund, Sweden

    Martin Almquist

  31. Department of Surgery Section of Endocrine and Sarcoma Lund, Skåne University Hospital, Lund University, Lund, Sweden

    Martin Almquist

  32. Department of Clinical Sciences Malmö, Lund University, Malmö, Sweden

    Emily Sonestedt

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

    Maria Sandström

  34. Department of Epidemiology and Global Health, Umeå University, Umeå, Sweden

    Lena Maria Nilsson

  35. International Agency for Research On Cancer, Lyon, France

    Elisabete Weiderpass

  36. Team Exposome and Heredity, Inserm U1018, CESP, 114 rue Edouard Vaillant, 94805, Villejuif Cedex, France

    Thérèse Truong

Authors
  1. Lucie Lécuyer
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  2. Nasser Laouali
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  3. Laure Dossus
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  4. Nitin Shivappa
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  5. James R. Hébert
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  6. Antonio Agudo
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  7. Anne Tjonneland
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  8. Jytte Halkjaer
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  9. Kim Overvad
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  10. Verena A. Katzke
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  11. Charlotte Le Cornet
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  12. Matthias B. Schulze
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  13. Franziska Jannasch
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  14. Domenico Palli
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  15. Claudia Agnoli
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  16. Rosario Tumino
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  17. Luca Dragna
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  18. Gabriella Iannuzzo
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  19. Torill Enget Jensen
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  20. Magritt Brustad
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  21. Guri Skeie
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  22. Raul Zamora-Ros
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  23. Miguel Rodriguez-Barranco
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  24. Pilar Amiano
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  25. María-Dolores Chirlaque
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  26. Eva Ardanaz
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  27. Martin Almquist
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  28. Emily Sonestedt
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  29. Maria Sandström
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  30. Lena Maria Nilsson
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  31. Elisabete Weiderpass
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  32. Inge Huybrechts
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  33. Sabina Rinaldi
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  34. Marie-Christine Boutron-Ruault
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  35. Thérèse Truong
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Contributions

The author’s contribution were as follows: MCBR and TT coordinated the project. LL, NL, LD, SR, MCBR and TT designed and conducted the research; NS and JRH designed the DII; AA designed the ISD; LL performed the statistical analyses; NL, MCBR and TT supervised the statistical analyses; LL, NS, MCBR and TT interpreted the results and drafted the manuscript. All authors reviewed the manuscript and approved the final version of the paper.

Corresponding author

Correspondence to Thérèse Truong.

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Conflict of interest

Dr. Marie-Christine Boutron-Ruault declares the following two sponsored conferences outside the present work as: MAYOLI-SPINDLER: 03/07/2020–30/07/2020 Symposium: Pancreatology in practice in 2020 e-JFHOD 2020 Conference « Why do I see more and more pancreatic cancers?» GILEAD 04/12/2020–04/12/2020- e-conference Weight gain and HIV infection in 2020. Dr. James R. Hébert owns controlling interest in Connecting Health Innovations LLC (CHI), a company that has licensed the right to his invention of the dietary inflammatory index (DII®) from the University of South Carolina in order to develop computer and smart phone applications for patient counseling and dietary intervention in clinical settings. Dr. Nitin Shivappa is an employee of CHI. The subject matter of this paper will not have any direct bearing on that work, nor has that activity exerted any influence on this project.

Ethics approval

The study was conducted according to the guidelines of the Declaration of Helsinki. Approval for the EPIC study was obtained from the ethical review boards of the International Agency for Research on Cancer (IARC) and all national recruitment institutions. Informed consent was obtained from all EPIC participants.

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Lécuyer, L., Laouali, N., Dossus, L. et al. Inflammatory potential of the diet and association with risk of differentiated thyroid cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. Eur J Nutr 61, 3625–3635 (2022). https://doi.org/10.1007/s00394-022-02897-w

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  • DOI: https://doi.org/10.1007/s00394-022-02897-w

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