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Inflammatory potential of diet and risk of lymphoma in the European Prospective Investigation into Cancer and Nutrition

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Abstract

Introduction

Chronic inflammation plays a critical role in lymphomagenesis and several dietary factors seem to be involved its regulation. The aim of the current study was to assess the association between the inflammatory potential of the diet and the risk of lymphoma and its subtypes in the European Investigation into Cancer and Nutrition (EPIC) study.

Methods

The analysis included 476,160 subjects with an average follow-up of 13.9 years, during which 3,136 lymphomas (135 Hodgkin lymphoma (HL), 2606 non-Hodgkin lymphoma (NHL) and 395 NOS) were identified. The dietary inflammatory potential was assessed by means of an inflammatory score of the diet (ISD), calculated using 28 dietary components and their corresponding inflammatory weights. The association between the ISD and lymphoma risk was estimated by hazard ratios (HR) and 95% confidence intervals (CI) calculated by multivariable Cox regression models adjusted for potential confounders.

Results

The ISD was not associated with overall lymphoma risk. Among lymphoma subtypes, a positive association between the ISD and mature B-cell NHL (HR for a 1-SD increase: 1.07 (95% CI 1.01; 1.14), p trend = 0.03) was observed. No statistically significant association was found among other subtypes. However, albeit with smaller number of cases, a suggestive association was observed for HL (HR for a 1-SD increase = 1.22 (95% CI 0.94; 1.57), p trend 0.13).

Conclusions

Our findings suggested that a high ISD score, reflecting a pro-inflammatory diet, was modestly positively associated with the risk of B-cell lymphoma subtypes. Further large prospective studies on low-grade inflammation induced by diet are warranted to confirm these findings.

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Acknowledgements

We thank all participants of the EPIC study. We thank Catalina Bonet for data management support and Bertrand Hémon at IARC for his valuable work and technical support with the EPIC database.

Funding

European Commission (DG-SANCO), International Agency for Research on Cancer, Danish Cancer Society (Denmark), Ligue Contre le Cancer, Institut Gustave Roussy, Mutuelle Generale de l’Education Nationale, Institut National de la Sante et de la Recherche Medicale (INSERM) (France), German Cancer Aid, German Cancer Research Center (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); German Federal Ministry of Education and Research (BMBF 01EO1303); Grant sponsor: Spanish Ministry of Economy and Competitiveness-Carlos III Institute of Health cofunded by FEDER funds/European Regional Development Fund (ERDF)—a way to build Europe, Grant numbers: [PI13/00061 (to Granada), PI13/01162 (to EPIC-Murcia, Regional Governments of Andalucıa, Asturias, Basque Country, Murcia and Navarra), PI17/01280 and PI14/01219 (to Barcelona), Centro de Investigación Biomédica en Red: Epidemiología y Salud Pública (CIBERESP, Spain)]; Grant sponsor: Agència de Gestió d’Ajuts Universitaris i de Recerca (AGAUR), CERCA Programme / Generalitat de Catalunya for institutional support; Grant number (2017SGR1085); Grant sponsors: Swedish Cancer Society, Swedish Research Council and County Councils of Skåne and Vasterbotten (Sweden) and Cancer Research UK; Grant numbers: 14136 (to EPIC-Norfolk), C570/A16491 and C8221/A19170 (to EPIC-Oxford); Grant sponsor: Medical Research Council; Grant numbers: 1000143 (to EPIC-Norfolk), MR/M012190/1 (to EPIC-Oxford, UK).

Author information

Authors and Affiliations

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

    Marta Solans, Yolanda Benavente, Marc Saez, Maria-Jose Sánchez, Pilar Amiano, María Dolores Chirlaque, Eva Ardanaz, Silvia de Sanjose & Delphine Casabonne

  2. Research Group on Statistics, Econometrics and Health (GRECS), University of Girona, Girona, Spain

    Marta Solans & Marc Saez

  3. Epidemiology Unit and Girona Cancer Registry, Catalan Institute of Oncology, Girona, Spain

    Marta Solans

  4. Unit of Molecular and Genetic Epidemiology in Infections and Cancer, Cancer Epidemiology Research Programme, IDIBELL, Catalan Institute of Oncology (ICO-IDIBELL), Av. Gran Via de l’Hospitalet 199-203, L’Hospitalet de Llobregat, 08908, Barcelona, Spain

    Yolanda Benavente, Silvia de Sanjose & Delphine Casabonne

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

    Antonio Agudo & Paula Jakszyn

  6. Nutritional Methodology and Biostatistics Group, International Agency for Research on Cancer (IARC-WHO), Lyon, France

    Sabine Naudin & Pietro Ferrari

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

    Fatemeh Saberi Hosnijeh & Roel Vermeulen

  8. Immunology Department, Erasmus University Medical Center, Rotterdam, The Netherlands

    Fatemeh Saberi Hosnijeh

  9. Nutritional Epidemiology Group (NEP), International Agency for Research on Cancer (IARC-WHO), Lyon, France

    Marc Gunter & Inge Huybrechts

  10. Department of Hematology and Oncology, Hospital of Versailles, Le Chesnay, France

    Caroline Besson

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

    Caroline Besson, Yahya Mahamat-Saleh & Marie-Christine Boutron-Ruault

  12. Gustave Roussy, Villejuif, France

    Caroline Besson, Yahya Mahamat-Saleh & Marie-Christine Boutron-Ruault

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

    Tilman Kühn & Rudolf Kaaks

  14. Department of Epidemiology, German Institute of Human Nutrition (DIfE) Postdam-Rehbrücke, Nuthetal, Germany

    Heiner Boeing

  15. Department of Functional Biology, Oviedo University, Oviedo, Spain

    Cristina Lasheras

  16. Escuela Andaluza de Salud Pública, Instituto de Investigación Biosanitaria ibs. GRANADA, Granada, Spain

    Maria-Jose Sánchez

  17. Public Health Division of Gipuzkoa, Regional Government of the Basque Country, Donostia, Spain

    Pilar Amiano

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

    María Dolores Chirlaque

  19. Navarra Public Health Institute, Pamplona, Spain

    Eva Ardanaz

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

    Eva Ardanaz

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

    Julie A. Schmidt

  22. Department of Epidemiology and Biostatistics, MRC-HPA Centre for Environment and Health, School of Public Health, Imperial College London, London, UK

    Paolo Vineis

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

    Elio Riboli

  24. Hellenic Health Foundation, Athens, Greece

    Antonia Trichopoulou, Anna Karakatsani & Elisavet Valanou

  25. Pulmonary Medicine Department, School of Medicine, National and Kapodistrian University of Athens, “ATTIKON” University Hospital, Haidari, Greece

    Anna Karakatsani

  26. Cancer Risk Factors and Life-Style Epidemiology Unit, Institute for Cancer Research, Prevention and Clinical Network-ISPRO, 50141, Florence, Italy

    Giovanna Masala

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

    Claudia Agnoli

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

    Rosario Tumino

  29. Unit of Cancer Epidemiology, Città della Salute e della Scienza University-Hospital and Center for Cancer Prevention (CPO), Turin, Italy

    Carlotta Sacerdote

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

    Amalia Mattiello

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

    Guri Skeie & Elisabete Weiderpass

  32. Department of Research, Cancer Registry of Norway-Institute of Population-Based Cancer Research, Oslo, Norway

    Elisabete Weiderpass

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

    Elisabete Weiderpass

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

    Elisabete Weiderpass

  35. Department of Oncology, Skåne University Hospital, Lund, Sweden

    Mats Jerkeman

  36. Department of Clinical Sciences, Research Group in Nutritional Epidemiology, Lund University, Malmö, Sweden

    Joana Alves Dias

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

    Florentin Späth

  38. Public Health and Clinical Medicine, Nutritional Research and Arctic Research Centre, Umeå University, Umeå, Sweden

    Lena Maria Nilsson

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

    Christina C. Dahm & Kim Overvad

  40. Unit of Diet, Genes and Environment, Danish Cancer Society Research Center, Copenhagen, Denmark

    Kristina Elin Nielsen Petersen & Anne Tjønneland

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

    Anne Tjønneland

  42. PATH, Reproductive Health, Seattle, USA

    Silvia de Sanjose

  43. Center for Chronic Immunodeficiency (CCI), Faculty of Medicine, Medical Center-University of Freiburg, University of Freiburg, Freiburg, Germany

    Alexandra Nieters

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  1. Marta Solans
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  13. Marie-Christine Boutron-Ruault
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  21. Eva Ardanaz
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  22. Julie A. Schmidt
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  28. Giovanna Masala
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  29. Claudia Agnoli
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  30. Rosario Tumino
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  31. Carlotta Sacerdote
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  32. Amalia Mattiello
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  33. Guri Skeie
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  34. Elisabete Weiderpass
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  35. Mats Jerkeman
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  46. Delphine Casabonne
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DC designed and conducted the research, contributed to the data analysis and manuscript writing, and had primary responsibility for the final content of the manuscript. MSo designed and conducted the research, performed the statistical analysis, wrote the manuscript, and had primary responsibility for the final content of the manuscript. YB, AA, PJ contributed to the data analysis and YB contributed to manuscript writing. MSa contributed to the statistical analysis. ER is the overall coordinator of the EPIC study. All authors contributed to recruitment, data collection and acquisition, biological sample collection, and follow-up and/or management of the EPIC cohort and to the interpretation of the present findings and approval of the final version of the manuscript for publication.

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Correspondence to Delphine Casabonne.

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Solans, M., Benavente, Y., Saez, M. et al. Inflammatory potential of diet and risk of lymphoma in the European Prospective Investigation into Cancer and Nutrition. Eur J Nutr 59, 813–823 (2020). https://doi.org/10.1007/s00394-019-01947-0

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  • DOI: https://doi.org/10.1007/s00394-019-01947-0

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