Top

Published in:

01-10-2020 | Obesity | Original Contribution

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

Authors: 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 Freisling

Published in: European Journal of Nutrition | Issue 7/2020

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 N^ε-(carboxymethyl)-lysine (CML), N^ε-(1-carboxyethyl)-lysine (CEL), and N^δ-(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.

Available only for authorised users

Hruby A, Hu FB (2015) The epidemiology of obesity: a big picture. Pharmacoeconomics 33(7):673–689. https://doi.org/10.1007/s40273-014-0243-xCrossRefPubMedPubMedCentral

World Health Organization-WHO (April, 2011) Global status report on noncommunicable diseases 2010. https://www.who.int/nmh/publications/ncd_report2010/en/

Douketis JD, Macie C, Thabane L, Williamson DF (2005) Systematic review of long-term weight loss studies in obese adults: clinical significance and applicability to clinical practice. Int J Obes (Lond) 29(10):1153–1167. https://doi.org/10.1038/sj.ijo.0802982CrossRef

Dombrowski SU, Knittle K, Avenell A, Araujo-Soares V, Sniehotta FF (2014) Long term maintenance of weight loss with non-surgical interventions in obese adults: systematic review and meta-analyses of randomised controlled trials. BMJ 348:g2646. https://doi.org/10.1136/bmj.g2646CrossRefPubMedPubMedCentral

Hu FB (2008) Obesity epidemiology. Oxford University Press, OxfordCrossRef

De Lorenzo A, Soldati L, Sarlo F, Calvani M, Di Lorenzo N, Di Renzo L (2016) New obesity classification criteria as a tool for bariatric surgery indication. World J Gastroenterol 22(2):681–703. https://doi.org/10.3748/wjg.v22.i2.681CrossRefPubMedPubMedCentral

Crino M, Sacks G, Vandevijvere S, Swinburn B, Neal B (2015) The influence on population weight gain and obesity of the macronutrient composition and energy density of the food supply. Curr Obes Rep 4(1):1–10. https://doi.org/10.1007/s13679-014-0134-7CrossRefPubMed

Hall KD, Ayuketah A, Brychta R, Cai H, Cassimatis T, Chen KY, Chung ST, Costa E, Courville A, Darcey V, Fletcher LA, Forde CG, Gharib AM, Guo J, Howard R, Joseph PV, McGehee S, Ouwerkerk R, Raisinger K, Rozga I, Stagliano M, Walter M, Walter PJ, Yang S, Zhou M (2019) Ultra-processed diets cause excess calorie intake and weight gain an inpatient randomized controlled trial of ad libitum food intake. Cell Metab 30(1):67–77. https://doi.org/10.1016/j.cmet.2019.05.008CrossRefPubMedPubMedCentral

Scheijen J, Clevers E, Engelen L, Dagnelie PC, Brouns F, Stehouwer CDA, Schalkwijk CG (2016) Analysis of advanced glycation endproducts in selected food items by ultra-performance liquid chromatography tandem mass spectrometry: presentation of a dietary AGE database. Food Chem 190:1145–1150. https://doi.org/10.1016/j.foodchem.2015.06.049CrossRefPubMed

10.

Goldberg T, Cai W, Peppa M, Dardaine V, Baliga BS, Uribarri J, Vlassara H (2004) Advanced glycoxidation end products in commonly consumed foods. J Am Diet Assoc 104(8):1287–1291. https://doi.org/10.1016/j.jada.2004.05.214CrossRefPubMed

11.

Poulsen MW, Hedegaard RV, Andersen JM, de Courten B, Bugel S, Nielsen J, Skibsted LH, Dragsted LO (2013) Advanced glycation endproducts in food and their effects on health. Food Chem Toxicol 60:10–37. https://doi.org/10.1016/j.fct.2013.06.052CrossRefPubMed

12.

Piperi C (2017) Dietary advanced glycation end-products: molecular mechanisms and preventive tools. Curr Nutr Rep 6(1):1–8. https://doi.org/10.1007/s13668-017-0188-8CrossRef

13.

Gaens KH, Stehouwer CD, Schalkwijk CG (2013) Advanced glycation endproducts and its receptor for advanced glycation endproducts in obesity. Curr Opin Lipidol 24(1):4–11. https://doi.org/10.1097/MOL.0b013e32835aea13CrossRefPubMed

14.

Kolb H, Stumvoll M, Kramer W, Kempf K, Martin S (2018) Insulin translates unfavourable lifestyle into obesity. BMC Med 16(1):232. https://doi.org/10.1186/s12916-018-1225-1CrossRefPubMedPubMedCentral

15.

Gao Y, Bielohuby M, Fleming T, Grabner GF, Foppen E, Wagner B, Guzmán-Ruiz M, Layritz C, Legutko B, Zinser E (2017) Dietary sugars, not lipids, drive hypothalamic inflammation. Mol Metab 6(8):897–908. https://doi.org/10.1016/j.molmet.2017.06.008CrossRefPubMedPubMedCentral

16.

Cai W, Ramdas M, Zhu L, Chen X, Striker GE, Vlassara H (2012) Oral advanced glycation endproducts (AGEs) promote insulin resistance and diabetes by depleting the antioxidant defenses AGE receptor-1 and sirtuin 1. Proc Natl Acad Sci USA 109(39):15888–15893. https://doi.org/10.1073/pnas.1205847109CrossRefPubMedPubMedCentral

17.

Sayej WN, Knight Iii PR, Guo WA, Mullan B, Ohtake PJ, Davidson BA, Khan A, Baker RD, Baker SS (2016) Advanced glycation end products induce obesity and hepatosteatosis in CD-1 wild-type mice. Biomed Res Int 2016:7867852. https://doi.org/10.1155/2016/7867852CrossRefPubMedPubMedCentral

18.

Sowndhar Rajan B, Manivasagam S, Dhanusu S, Chandrasekar N, Krishna K, Kalaiarasu LP, Babu AA, Vellaichamy E (2018) Diet with high content of advanced glycation end products induces systemic inflammation and weight gain in experimental mice: protective role of curcumin and gallic acid. Food Chem Toxicol 114:237–245. https://doi.org/10.1016/j.fct.2018.02.016CrossRefPubMed

19.

Forbes JM, Sourris KC, de Courten MP, Dougherty SL, Chand V, Lyons JG, Bertovic D, Coughlan MT, Schlaich MP, Soldatos G, Cooper ME, Straznicky NE, Kingwell BA, de Courten B (2014) Advanced glycation end products (AGEs) are cross-sectionally associated with insulin secretion in healthy subjects. Amino Acids 46(2):321–326. https://doi.org/10.1007/s00726-013-1542-9CrossRefPubMed

20.

Riboli E, Kaaks R (1997) The EPIC Project: rationale and study design. European Prospective Investigation into Cancer and Nutrition. Int J of Epidemiol 26((suppl 1)):S6–S14. https://doi.org/10.1093/ije/26.suppl_1.S6CrossRef

21.

Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, Charrondiere UR, Hemon B, Casagrande C, Vignat J, Overvad K, Tjonneland A, Clavel-Chapelon F, Thiebaut A, Wahrendorf J, Boeing H, Trichopoulos D, Trichopoulou A, Vineis P, Palli D, Bueno-de-Mesquita HB, Peeters PHM, Lund E, Engeset D, Gonzalez CA, Barricarte A, Berglund G, Hallmans G, Day NE, Key TJ, Kaaks R, Saracci R (2002) European prospective investigation into cancer and nutrition (EPIC): study populations and data collection. Public Health Nutr 5(6b):1113–1124. https://doi.org/10.1079/Phn2002394CrossRefPubMed

22.

Black AE (2000) Critical evaluation of energy intake using the Goldberg cut-off for energy intake: basal metabolic rate. A practical guide to its calculation, use and limitations. Int J Obe 24(9):1119–1130. https://doi.org/10.1038/sj.ijo.0801376CrossRef

23.

Freisling H, van Bakel MME, Biessy C, May AM, Byrnes G, Norat T, Rinaldi S, de Magistris MS, Grioni S, Bueno-de-Mesquita HB, Ocke MC, Kaaks R, Teucher B, Vergnaud AC, Romaguera D, Sacerdote C, Palli D, Crowe FL, Tumino R, Clavel-Chapelon F, Boutron-Ruault MC, Khaw KT, Wareham NJ, Trichopoulou A, Naska A, Orfanos P, Boeing H, Illner AK, Riboli E, Peeters PH, Slimani N (2012) Dietary reporting errors on 24 h recalls and dietary questionnaires are associated with BMI across six European countries as evaluated with recovery biomarkers for protein and potassium intake. Brit J Nutr 107(6):910–920. https://doi.org/10.1017/S0007114511003564CrossRefPubMed

24.

Gottschald M, Knuppel S, Boeing H, Buijsse B (2016) The influence of adjustment for energy misreporting on relations of cake and cookie intake with cardiometabolic disease risk factors. Eur J Clin Nutr 70(11):1318–1324. https://doi.org/10.1038/ejcn.2016.131CrossRefPubMed

25.

Vergnaud A, Norat T, Romaguera D, Mouw T, May A, Romieu I, Freisling H, Slimani N, Boutron-Ruault M, Clavel-Chapelon F (2011) Fruit and vegetable consumption and prospective weight change in participants of the European Prospective Investigation into Cancer and Nutrition-Physical Activity, Nutrition, Alcohol, Cessation of Smoking, Eating Out of Home, and Obesity study. Am J Clin Nutr 95(1):184–193. https://doi.org/10.3945/ajcn.111.019968CrossRefPubMed

26.

Vergnaud A, Norat T, Romaguera D, Mouw T, May A, Travier N, Luan J, Wareham N, Slimani N, Rinaldi S (2010) Meat consumption and prospective weight change in participants of the EPIC-PANACEA study. Am J Clin Nutr 92(2):398–407. https://doi.org/10.3945/ajcn.2009.28713CrossRefPubMed

27.

Spencer E, Appleby P, Davey G, Key T (2002) Validity of self-reported height and weight in 4808 EPIC–Oxford participants. Public Health Nutr 5(4):561–565. https://doi.org/10.1079/PHN2001322CrossRefPubMed

28.

Slimani N, Deharveng G, Unwin I, Southgate DA, Vignat J, Skeie G, Salvini S, Parpinel M, Moller A, Ireland J, Becker W, Farran A, Westenbrink S, Vasilopoulou E, Unwin J, Borgejordet A, Rohrmann S, Church S, Gnagnarella P, Casagrande C, van Bakel M, Niravong M, Boutron-Ruault MC, Stripp C, Tjonneland A, Trichopoulou A, Georga K, Nilsson S, Mattisson I, Ray J, Boeing H, Ocke M, Peeters PH, Jakszyn P, Amiano P, Engeset D, Lund E, de Magistris MS, Sacerdote C, Welch A, Bingham S, Subar AF, Riboli E (2007) The EPIC nutrient database project (ENDB): a first attempt to standardize nutrient databases across the 10 European countries participating in the EPIC study. Eur J Clin Nutr 61(9):1037–1056. https://doi.org/10.1038/sj.ejcn.1602679CrossRefPubMed

29.

Buckland G, Gonzalez CA, Agudo A, Vilardell M, Berenguer A, Amiano P, Ardanaz E, Arriola L, Barricarte A, Basterretxea M, Chirlaque MD, Cirera L, Dorronsoro M, Egues N, Huerta JM, Larranaga N, Marin P, Martinez C, Molina E, Navarro C, Quiros JR, Rodriguez L, Sanchez MJ, Tormo MJ, Moreno-Iribas C (2009) Adherence to the Mediterranean diet and risk of coronary heart disease in the Spanish EPIC Cohort Study. Am J Epidemiol 170(12):1518–1529. https://doi.org/10.1093/aje/kwp282CrossRefPubMed

30.

Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21(11):1539–1558. https://doi.org/10.1002/sim.1186CrossRefPubMed

31.

Romaguera D, Norat T, Vergnaud AC, Mouw T, May AM, Agudo A, Buckland G, Slimani N, Rinaldi S, Couto E, Clavel-Chapelon F, Boutron-Ruault MC, Cottet V, Rohrmann S, Teucher B, Bergmann M, Boeing H, Tjonneland A, Halkjaer J, Jakobsen MU, Dahm CC, Travier N, Rodriguez L, Sanchez MJ, Amiano P, Barricarte A, Huerta JM, Luan J, Wareham N, Key TJ, Spencer EA, Orfanos P, Naska A, Trichopoulou A, Palli D, Agnoli C, Mattiello A, Tumino R, Vineis P, Bueno-de-Mesquita HB, Buchner FL, Manjer J, Wirfalt E, Johansson I, Hellstrom V, Lund E, Braaten T, Engeset D, Odysseos A, Riboli E, Peeters PH (2010) Mediterranean dietary patterns and prospective weight change in participants of the EPIC-PANACEA project. Am J Clin Nutr 92(4):912–921. https://doi.org/10.3945/ajcn.2010.29482CrossRefPubMed

32.

Birlouez-Aragon I, Saavedra G, Tessier FJ, Galinier A, Ait-Ameur L, Lacoste F, Niamba CN, Alt N, Somoza V, Lecerf JM (2010) A diet based on high-heat-treated foods promotes risk factors for diabetes mellitus and cardiovascular diseases. Am J Clin Nutr 91(5):1220–1226. https://doi.org/10.3945/ajcn.2009.28737CrossRefPubMed

33.

de Courten B, de Courten MP, Soldatos G, Dougherty SL, Straznicky N, Schlaich M, Sourris KC, Chand V, Scheijen JL, Kingwell BA, Cooper ME, Schalkwijk CG, Walker KZ, Forbes JM (2016) Diet low in advanced glycation end products increases insulin sensitivity in healthy overweight individuals: a double-blind, randomized, crossover trial. Am J Clin Nutr 103(6):1426–1433. https://doi.org/10.3945/ajcn.115.125427CrossRefPubMed

34.

Moraru A, Wiederstein J, Pfaff D, Fleming T, Miller AK, Nawroth P, Teleman AA (2018) Elevated levels of the reactive metabolite methylglyoxal recapitulate progression of Type 2 diabetes. Cell Metab 27(4):926–934. https://doi.org/10.1016/j.cmet.2018.02.003CrossRefPubMed

35.

Wisse BE, Schwartz MW (2009) Does hypothalamic inflammation cause obesity? Cell Metab 10(4):241–242. https://doi.org/10.1016/j.cmet.2009.09.003CrossRefPubMed

36.

Naska A, Lagiou A, Lagiou P (2017) Dietary assessment methods in epidemiological research: current state of the art and future prospects. F1000Res 6:926. https://doi.org/10.12688/f1000research.10703.1CrossRefPubMedPubMedCentral

37.

Palimeri S, Palioura E, Diamanti-Kandarakis E (2015) Current perspectives on the health risks associated with the consumption of advanced glycation end products: recommendations for dietary management. Diabetes Metab Syndr Obes 8:415–426. https://doi.org/10.2147/DMSO.S63089CrossRefPubMedPubMedCentral

38.

Sharma C, Kaur A, Thind SS, Singh B, Raina S (2015) Advanced glycation End-products (AGEs): an emerging concern for processed food industries. J Food Sci Technol 52(12):7561–7576. https://doi.org/10.1007/s13197-015-1851-yCrossRefPubMedPubMedCentral

39.

Koschinsky T, He CJ, Mitsuhashi T, Bucala R, Liu C, Buenting C, Heitmann K, Vlassara H (1997) Orally absorbed reactive glycation products (glycotoxins): an environmental risk factor in diabetic nephropathy. Proc Natl Acad Sci USA 94(12):6474–6479. https://doi.org/10.1073/pnas.94.12.6474CrossRefPubMedPubMedCentral

40.

Scheijen JLJM, Hanssen NMJ, van Greevenbroek MM, van der Kallen CJ, Feskens EJM, Stehouwer CDA, Schalkwijk CG (2018) Dietary intake of advanced glycation endproducts is associated with higher levels of advanced glycation endproducts in plasma and urine: the CODAM study. Clin Nutr 37(3):919–925. https://doi.org/10.1016/j.clnu.2017.03.019CrossRefPubMed

41.

Freisling H, Noh H, Slimani N, Chajes V, May AM, Peeters PH, Weiderpass E, Cross AJ, Skeie G, Jenab M, Mancini FR, Boutron-Ruault MC, Fagherazzi G, Katzke VA, Kuhn T, Steffen A, Boeing H, Tjonneland A, Kyro C, Hansen CP, Overvad K, Duell EJ, Redondo-Sanchez D, Amiano P, Navarro C, Barricarte A, Perez-Cornago A, Tsilidis KK, Aune D, Ward H, Trichopoulou A, Naska A, Orfanos P, Masala G, Agnoli C, Berrino F, Tumino R, Sacerdote C, Mattiello A, Bueno-de-Mesquita HB, Ericson U, Sonestedt E, Winkvist A, Braaten T, Romieu I, Sabate J (2018) Nut intake and 5-year changes in body weight and obesity risk in adults: results from the EPIC-PANACEA study. Eur J Nutr 57(7):2399–2408. https://doi.org/10.1007/s00394-017-1513-0CrossRefPubMed

42.

Park JY, Mitrou PN, Keogh RH, Luben RN, Wareham NJ, Khaw KT (2012) Self-reported and measured anthropometric data and risk of colorectal cancer in the EPIC–Norfolk study. Int J Obes (Lond) 36(1):107. https://doi.org/10.1038/ijo.2011.61CrossRef

43.

Skeie G, Mode N, Henningsen M, Borch KB (2015) Validity of self-reported body mass index among middle-aged participants in the Norwegian Women and Cancer study. Clin Epidemiol 7:313–323. https://doi.org/10.2147/Clep.S83839CrossRefPubMedPubMedCentral

44.

Smith JD, Hou T, Hu FB, Rimm EB, Spiegelman D, Willett WC, Mozaffarian D (2015) A Comparison of different methods for evaluating diet, physical activity, and long-term weight gain in 3 prospective cohort studies. J Nutr 145(11):2527–2534. https://doi.org/10.3945/jn.115.214171CrossRefPubMedPubMedCentral

Title: Dietary intake of advanced glycation end products (AGEs) and changes in body weight in European adults
Authors: 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 Freisling
Publication date: 01-10-2020
Publisher: Springer Berlin Heidelberg
Keywords: Obesity
Obesity
Published in: European Journal of Nutrition / Issue 7/2020
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI: https://doi.org/10.1007/s00394-019-02129-8

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

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

Abstract

Purpose

Methods

Results

Conclusion

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 7/2020

Time trends of vitamin D concentrations in northern Sweden between 1986 and 2014: a population-based cross-sectional study

Correction to: Prebiotic effect of inulin‑type fructans on faecal microbiota and short‑chain fatty acids in type 2 diabetes: a randomised controlled trial

Associations between tea and coffee beverage consumption and the risk of lung cancer in the Singaporean Chinese population

Introduction to: The ‘Seal’ of Sir Shackleton

Bifidobacteria adolescentis regulated immune responses and gut microbial composition to alleviate DNFB-induced atopic dermatitis in mice

Associations between dietary flavonoids and retinal microvasculature in older adults

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page