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

  • R. Cordova
  • V. Knaze
  • V. Viallon
  • P. Rust
  • C. G. Schalkwijk
  • E. Weiderpass
  • K-H. Wagner
  • A-L. Mayen-Chacon
  • E. K. Aglago
  • C. C. Dahm
  • K. Overvad
  • A. Tjønneland
  • J. Halkjær
  • F. R. Mancini
  • M-C. Boutron-Ruault
  • G. Fagherazzi
  • V. Katzke
  • T. Kühn
  • M. B. Schulze
  • H. Boeing
  • A. Trichopoulou
  • A. Karakatsani
  • P. Thriskos
  • G. Masala
  • V. Krogh
  • S. Panico
  • R. Tumino
  • F. Ricceri
  • A. Spijkerman
  • J. Boer
  • G. Skeie
  • C. Rylander
  • K. B. Borch
  • J. R. Quirós
  • A. Agudo
  • D. Redondo-Sánchez
  • P. Amiano
  • J-H. Gómez-Gómez
  • A. Barricarte
  • S. Ramne
  • E. Sonestedt
  • I. Johansson
  • A. Esberg
  • T. Tong
  • D. Aune
  • K. K. Tsilidis
  • M. J. Gunter
  • M. Jenab
  • Heinz FreislingEmail author
Original Contribution

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.

Keywords

Dietary advanced glycation end products Weight change Obesity Adults Europe 

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

Notes

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.

Author 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.

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).

Compliance with ethical standards

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.

Supplementary material

394_2019_2129_MOESM1_ESM.pdf (726 kb)
Supplementary material 1 (PDF 725 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • R. Cordova
    • 1
  • V. Knaze
    • 2
  • V. Viallon
    • 3
  • P. Rust
    • 1
  • C. G. Schalkwijk
    • 4
  • E. Weiderpass
    • 6
  • K-H. Wagner
    • 1
  • A-L. Mayen-Chacon
    • 3
  • E. K. Aglago
    • 3
  • C. C. Dahm
    • 7
  • K. Overvad
    • 7
    • 8
  • A. Tjønneland
    • 9
    • 10
  • J. Halkjær
    • 9
  • F. R. Mancini
    • 11
    • 12
  • M-C. Boutron-Ruault
    • 11
    • 12
  • G. Fagherazzi
    • 11
    • 12
  • V. Katzke
    • 13
  • T. Kühn
    • 13
  • M. B. Schulze
    • 14
    • 15
  • H. Boeing
    • 16
  • A. Trichopoulou
    • 17
  • A. Karakatsani
    • 17
    • 18
  • P. Thriskos
    • 17
  • G. Masala
    • 19
  • V. Krogh
    • 20
  • S. Panico
    • 21
  • R. Tumino
    • 22
  • F. Ricceri
    • 23
    • 24
  • A. Spijkerman
    • 25
  • J. Boer
    • 25
  • G. Skeie
    • 5
  • C. Rylander
    • 5
  • K. B. Borch
    • 5
  • J. R. Quirós
    • 26
  • A. Agudo
    • 27
  • D. Redondo-Sánchez
    • 28
    • 29
  • P. Amiano
    • 29
    • 30
  • J-H. Gómez-Gómez
    • 31
  • A. Barricarte
    • 29
    • 32
    • 33
  • S. Ramne
    • 34
  • E. Sonestedt
    • 34
  • I. Johansson
    • 35
  • A. Esberg
    • 35
  • T. Tong
    • 36
  • D. Aune
    • 37
  • K. K. Tsilidis
    • 37
    • 38
  • M. J. Gunter
    • 3
  • M. Jenab
    • 3
  • Heinz Freisling
    • 39
    Email author
  1. 1.Department of Nutritional SciencesUniversity of ViennaViennaAustria
  2. 2.Section of Early Detection and PreventionInternational Agency for Research on Cancer (IARC-WHO)LyonFrance
  3. 3.Section of Nutrition and MetabolismInternational Agency for Research on Cancer (IARC-WHO)LyonFrance
  4. 4.Department of Internal Medicine, Laboratory of Metabolism and Vascular MedicineMaastricht University Medical CenterMaastrichtThe Netherlands
  5. 5.Department of Community Medicine, Faculty of Health SciencesUiT-The Arctic University of NorwayTromsøNorway
  6. 6.International Agency for Research on Cancer (IARC-WHO)LyonFrance
  7. 7.Department of Public HealthAarhus UniversityAarhusDenmark
  8. 8.Department of CardiologyAalborg University HospitalAalborgDenmark
  9. 9.Danish Cancer Society Research Center CopenhagenCopenhagenDenmark
  10. 10.Department of Public Health, Faculty of Health and Medical SciencesUniversity of CopenhagenCopenhagenDenmark
  11. 11.CESP, Fac. de médecineUniv. Paris-Sud, Fac. de médecine-UVSQ-INSERM, Université Paris-SaclayVillejuifFrance
  12. 12.Institut Gustave RoussyVillejuifFrance
  13. 13.Division of Cancer EpidemiologyGerman Cancer Research Center (DKFZ)HeidelbergGermany
  14. 14.Department of Molecular EpidemiologyGerman Institute of Human Nutrition Potsdam-RehbrueckeNuthetalGermany
  15. 15.Institute of Nutrition ScienceUniversity of PotsdamNuthetalGermany
  16. 16.Department of EpidemiologyGerman Institute of Human Nutrition Potsdam-RehbrueckeNuthetalGermany
  17. 17.Hellenic Health FoundationAthensGreece
  18. 18.2nd Pulmonary Medicine Department, School of MedicineNational and Kapodistrian University of Athens, ATTIKON University HospitalHaidariGreece
  19. 19.Cancer Risk Factors and Lifestyle Epidemiology UnitInstitute for Cancer Research, Prevention and Clinical Network-ISPROFlorenceItaly
  20. 20.Epidemiology and Prevention UnitFondazione IRCCS Istituto Nazionale dei TumoriMilanItaly
  21. 21.Dipartimento di Medicina Clinica E ChirurgiaFederico II UniversityNaplesItaly
  22. 22.Cancer Registry and Histopathology UnitAzienda Sanitaria Provinciale (ASP) RagusaRagusaItaly
  23. 23.Department of Clinical and Biological SciencesUniversity of TurinTurinItaly
  24. 24.Unit of EpidemiologyRegional Health Service ASL TO3TurinItaly
  25. 25.National Institute for Public Health and the Environment (RIVM)BilthovenThe Netherlands
  26. 26.Public Health DirectorateAsturiasSpain
  27. 27.Unit of Nutrition and Cancer, Cancer Epidemiology Research ProgramCatalan Institute of Oncology-IDIBELL, L’Hospitalet de LlobregatBarcelonaSpain
  28. 28.Andalusian School of Public Health. Biomedical Research Institute ibs.GRANADAUniversity of GranadaGranadaSpain
  29. 29.CIBER of Epidemiology and Public HealthMadridSpain
  30. 30.Public Health Division of GipuzkoaBioDonostia Research InstituteSan SebastianSpain
  31. 31.Department of Epidemiology and Murcia Regional Health CouncilUniversidad de MurciaMurciaSpain
  32. 32.Navarra Public Health InstitutePamplonaSpain
  33. 33.Navarra Institute for Health Research (IdiSNA)PamplonaSpain
  34. 34.Nutritional Epidemiology, Department of Clinical Sciences MalmöLund UniversityMalmöSweden
  35. 35.Department of OdontologyUmeå UniversityUmeåSweden
  36. 36.Cancer Epidemiology Unit, Nuffield Department of Population HealthUniversity of OxfordOxfordUK
  37. 37.Department of Epidemiology and BiostatisticsSchool of Public Health, Imperial College LondonLondonUK
  38. 38.Department of Hygiene and EpidemiologyUniversity of Ioannina School of Medicine University Campus IoanninaIoanninaGreece
  39. 39.International Agency for Research on Cancer (IARC-WHO)LyonFrance

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