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

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).

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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.

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Correspondence to Heinz Freisling.

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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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Keywords

  • Dietary advanced glycation end products
  • Weight change
  • Obesity
  • Adults
  • Europe