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Dietary intake of advanced glycation end products (AGEs) and changes in body weight in European adults

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Advanced glycation end products (AGEs) can be formed in foods by the reaction of reducing sugars with proteins, and have been shown to induce insulin resistance and obesity in experimental studies. We examined the association between dietary AGEs intake and changes in body weight in adults over an average of 5 years of follow-up.

Methods

A total of 255,170 participants aged 25–70 years were recruited in ten European countries (1992–2000) in the PANACEA study (Physical Activity, Nutrition, Alcohol, Cessation of smoking, Eating out of home in relation to Anthropometry), a sub-cohort of the EPIC (European Prospective Investigation into Cancer and Nutrition). Body weight was measured at recruitment and self-reported between 2 and 11 years later depending on the study center. A reference database for AGEs was used containing UPLC–MS/MS-measured Nε-(carboxymethyl)-lysine (CML), Nε-(1-carboxyethyl)-lysine (CEL), and Nδ-(5-hydro-5-methyl-4-imidazolon-2-yl)-ornithine (MG-H1) in 200 common European foods. This reference database was matched to foods and decomposed recipes obtained from country-specific validated dietary questionnaires in EPIC and intake levels of CEL, CML, and MG-H1 were estimated. Associations between dietary AGEs intake and body weight change were estimated separately for each of the three AGEs using multilevel mixed linear regression models with center as random effect and dietary AGEs intake and relevant confounders as fixed effects.

Results

A one-SD increment in CEL intake was associated with 0.111 kg (95% CI 0.087–0.135) additional weight gain over 5 years. The corresponding additional weight gain for CML and MG-H1 was 0.065 kg (0.041–0.089) and 0.034 kg (0.012, 0.057), respectively. The top six food groups contributing to AGEs intake, with varying proportions across the AGEs, were cereals/cereal products, meat/processed meat, cakes/biscuits, dairy, sugar and confectionary, and fish/shellfish.

Conclusion

In this study of European adults, higher intakes of AGEs were associated with marginally greater weight gain over an average of 5 years of follow-up.

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Data availability

Data described in the manuscript, code book, and analytic code will be made available upon request pending application and approval. 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.

Abbreviations

AGEs:

Advanced glycation end products

CEL:

Nε -1- Carboxyethyl-lysine

CML:

Nε-Carboxymethyl-lysine

DQ:

Dietary questionnaires

DXA:

Dual-energy X-ray absorptiometry

EPIC:

European Prospective Investigation into Cancer and nutrition

MG-H1:

Nδ-(5-Hydro-5-methyl-4-imidazolon-2-yl) ornithines

mrMDS:

Modified relative Mediterranean Diet Score

PANACEA:

Physical Activity, Nutrition, Alcohol, Cessation of smoking, Eating out of home in relation to Anthropometry

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Acknowledgements

We thank Petra H. Peeters and Anne M. May from the Julius Centre for Health Sciences and Primary Care, University Medical Centre Utrecht, The Netherlands, for coordinating the EPIC-Panacea study, and all EPIC participants and staff for their contribution to the study.

Funding

This work was partially financially supported by the World Cancer Research Fund International (WCRF, Grant No. 2015/1391, MJ, VK, and HF) and the Fondation de France (FDF, Grant No. 00081166, HF, and FDF Grant No. 00089811, ALMC). 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 the following funders: 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), Federal Ministry of Education and Research (BMBF) (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); Health Research Fund (FIS-ISCIII), the Regional Governments of Andalucía, Asturias, Basque Country, Murcia, Navarra, and the Catalan Institute of Oncology (Barcelona), Spain); Cancer Research UK (14136 to EPIC-Norfolk; C570/A16491 and C8221/A19170 to EPIC-Oxford), Medical Research Council (1000143 to EPIC-Norfolk, MR/M012190/1 to EPIC-Oxford) (UK).

Author information

Authors and Affiliations

  1. Department of Nutritional Sciences, University of Vienna, Vienna, Austria

    R. Cordova, P. Rust & K-H. Wagner

  2. Section of Early Detection and Prevention, International Agency for Research on Cancer (IARC-WHO), Lyon, France

    V. Knaze

  3. Section of Nutrition and Metabolism, International Agency for Research on Cancer (IARC-WHO), Lyon, France

    V. Viallon, A-L. Mayen-Chacon, E. K. Aglago, M. J. Gunter & M. Jenab

  4. Department of Internal Medicine, Laboratory of Metabolism and Vascular Medicine, Maastricht University Medical Center, Maastricht, The Netherlands

    C. G. Schalkwijk

  5. Department of Community Medicine, Faculty of Health Sciences, UiT-The Arctic University of Norway, Tromsø, Norway

    G. Skeie, C. Rylander & K. B. Borch

  6. International Agency for Research on Cancer (IARC-WHO), Lyon, France

    E. Weiderpass

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

    C. C. Dahm & K. Overvad

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

    K. Overvad

  9. Danish Cancer Society Research Center Copenhagen, Copenhagen, Denmark

    A. Tjønneland & J. Halkjær

  10. Department of Public Health, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark

    A. Tjønneland

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

    F. R. Mancini, M-C. Boutron-Ruault & G. Fagherazzi

  12. Institut Gustave Roussy, Villejuif, France

    F. R. Mancini, M-C. Boutron-Ruault & G. Fagherazzi

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

    V. Katzke & T. Kühn

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

    M. B. Schulze

  15. Institute of Nutrition Science, University of Potsdam, Nuthetal, Germany

    M. B. Schulze

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

    H. Boeing

  17. Hellenic Health Foundation, Athens, Greece

    A. Trichopoulou, A. Karakatsani & P. Thriskos

  18. 2nd Pulmonary Medicine Department, School of Medicine, National and Kapodistrian University of Athens, ATTIKON University Hospital, Haidari, Greece

    A. Karakatsani

  19. Cancer Risk Factors and Lifestyle Epidemiology Unit, Institute for Cancer Research, Prevention and Clinical Network-ISPRO, Florence, Italy

    G. Masala

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

    V. Krogh

  21. Dipartimento di Medicina Clinica E Chirurgia, Federico II University, Naples, Italy

    S. Panico

  22. Cancer Registry and Histopathology Unit, Azienda Sanitaria Provinciale (ASP) Ragusa, Ragusa, Italy

    R. Tumino

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

    F. Ricceri

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

    F. Ricceri

  25. National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands

    A. Spijkerman & J. Boer

  26. Public Health Directorate, Asturias, Spain

    J. R. Quirós

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

    A. Agudo

  28. Andalusian School of Public Health. Biomedical Research Institute ibs.GRANADA, University of Granada, Granada, Spain

    D. Redondo-Sánchez

  29. CIBER of Epidemiology and Public Health, Madrid, Spain

    D. Redondo-Sánchez, P. Amiano & A. Barricarte

  30. Public Health Division of Gipuzkoa, BioDonostia Research Institute, San Sebastian, Spain

    P. Amiano

  31. Department of Epidemiology and Murcia Regional Health Council, Universidad de Murcia, Murcia, Spain

    J-H. Gómez-Gómez

  32. Navarra Public Health Institute, Pamplona, Spain

    A. Barricarte

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

    A. Barricarte

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

    S. Ramne & E. Sonestedt

  35. Department of Odontology, Umeå University, Umeå, Sweden

    I. Johansson & A. Esberg

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

    T. Tong

  37. Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK

    D. Aune & K. K. Tsilidis

  38. Department of Hygiene and Epidemiology, University of Ioannina School of Medicine University Campus Ioannina, Ioannina, Greece

    K. K. Tsilidis

  39. International Agency for Research on Cancer (IARC-WHO), 150 cours Albert Thomas, CEDEX 08, 69372, Lyon, France

    Heinz Freisling

Authors
  1. R. Cordova
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  2. V. Knaze
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  3. V. Viallon
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  4. P. Rust
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  5. C. G. Schalkwijk
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  43. A. Esberg
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  44. T. Tong
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  45. D. Aune
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  46. K. K. Tsilidis
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  48. M. Jenab
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  49. Heinz Freisling
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Contributions

Heinz Freisling and Mazda Jenab developed the overall research plan; Viktoria Knaze and Reynalda Cordova performed the data matching; Casper G. Schalkwijk provided the AGEs database; Reynalda Cordova conducted the statistical analyses. Vivian Viallon contributed to the statistical analyses; Reynalda Cordova and Heinz Freisling wrote the manuscript; Heinz Freisling supervised the data analysis, reviewed/edited the manuscript, and had primary responsibility for final content; and all authors: contributed substantially to data collection, the interpretation of data, and the drafting or critical revision of the manuscript for important intellectual content. 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.

Corresponding author

Correspondence to Heinz Freisling.

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Conflict of interest

None of the authors declared a conflict of interest.

Ethics approval

The present study was approved by the ethics committees of the IARC and the individual study centers.

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Cordova, R., Knaze, V., Viallon, V. et al. Dietary intake of advanced glycation end products (AGEs) and changes in body weight in European adults. Eur J Nutr 59, 2893–2904 (2020). https://doi.org/10.1007/s00394-019-02129-8

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  • DOI: https://doi.org/10.1007/s00394-019-02129-8

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