Hostname: page-component-77c89778f8-fv566 Total loading time: 0 Render date: 2024-07-23T09:48:02.278Z Has data issue: false hasContentIssue false

Dietary intake of dicarbonyl compounds and changes in body weight over time in a large cohort of European adults

Published online by Cambridge University Press:  22 February 2024

Charlotte Debras
Affiliation:
Nutrition and Metabolism Branch, International Agency for Research on Cancer, World Health Organization, Lyon, France
Reynalda Cordova
Affiliation:
Department of Nutritional Sciences, University of Vienna, Vienna, Austria
Ana-Lucia Mayén
Affiliation:
Nutrition and Metabolism Branch, International Agency for Research on Cancer, World Health Organization, Lyon, France
Kim Maasen
Affiliation:
Department of Internal Medicine, CARIM School for Cardiovascular Diseases, Maastricht University Medical Centre, Maastricht, the Netherlands
Viktoria Knaze
Affiliation:
Nutrition and Metabolism Branch, International Agency for Research on Cancer, World Health Organization, Lyon, France
Simone J. P. M. Eussen
Affiliation:
Department of Epidemiology, CARIM School for Cardiovascular Diseases/CAPHRI School for Public Health and Primary Care, Maastricht University Medical Centre, Maastricht, the Netherlands
Casper G. Schalkwijk
Affiliation:
Department of Internal Medicine, CARIM School for Cardiovascular Diseases, Maastricht University Medical Centre, Maastricht, the Netherlands
Inge Huybrechts
Affiliation:
Nutrition and Metabolism Branch, International Agency for Research on Cancer, World Health Organization, Lyon, France
Anne Tjønneland
Affiliation:
Danish Cancer Society Research Center, Copenhagen, Denmark; Department of Public Health, University of Copenhagen, Copenhagen, Denmark
Jytte Halkjær
Affiliation:
Danish Cancer Society Research Center, Copenhagen, Denmark
Verena Katzke
Affiliation:
Department of Cancer Epidemiology, German Cancer research Center (DKFZ), Heidelberg, Germany
Rashmita Bajracharya
Affiliation:
Department of Cancer Epidemiology, German Cancer research Center (DKFZ), Heidelberg, Germany
Matthias B. Schulze
Affiliation:
Department of Molecular Epidemiology, German Institute of Human Nutrition Potsdam-Rehbruecke, Nuthetal, Germany; Institute of Nutritional Science, University of Potsdam, Nuthetal, Germany
Giovanna Masala
Affiliation:
Institute for Cancer Research, Prevention and Clinical Network (ISPRO), Florence, Italy
Valeria Pala
Affiliation:
Epidemiology and Prevention Unit, Department of Research, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
Fabrizio Pasanisi
Affiliation:
Department of Clinical Medicine and Surgery School of Medicine, Federico II University, Via Sergio Pansini 5, 80131, Naples, Italy
Alessandra Macciotta
Affiliation:
Department of Clinical and Biological Sciences, University of Turin, Turin, Italy
Dafina Petrova
Affiliation:
Escuela Andaluza de Salud Pública (EASP), 18011 Granada, Spain; Instituto de Investigación Biosanitaria ibs.GRANADA, 18012 Granada, Spain; Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), 28029 Madrid, Spain
Jazmin Castañeda
Affiliation:
Unit of Nutrition and Cancer, Cancer Epidemiology Research Programme, Catalan Institute of Oncology (ICO), Bellvitge Biomedical Research Institute (IDIBELL), L’Hospitalet del Llobregat, Spain
Carmen Santiuste
Affiliation:
Department of Epidemiology, Murcia Regional Health Council, IMIB-Arrixaca, Murcia, Spain; CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain
Pilar Amiano
Affiliation:
Ministry of Health of the Basque Government, Sub Directorate for Public Health and Addictions of Gipuzkoa, 2013 San Sebastian, Spain; Biodonostia Health Research Institute, Epidemiology of Chronic and Communicable Diseases Group, 20014 San Sebastián, Spain; Spanish Consortium for Research on Epidemiology and Public Health (CIBERESP), Instituto de Salud Carlos III, Madrid, Spain
Conchi Moreno-Iribas
Affiliation:
Instituto de Salud Pública y Laboral de Navarra, 31003 Pamplona, Spain; Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), 28029 Madrid, Spain; Navarra Institute for Health Research (IdiSNA), 31008 Pamplona, Spain
Yan Borné
Affiliation:
Nutrition Epidemiology, Department of Clinical Sciences Malmö, Faculty of Medicine, Lund University, Lund, Sweden
Emily Sonestedt
Affiliation:
Nutrition Epidemiology, Department of Clinical Sciences Malmö, Faculty of Medicine, Lund University, Lund, Sweden
Ingegerd Johansson
Affiliation:
Department of Odontology, Umeå University, Umeå, Sweden
Anders Esberg
Affiliation:
Department of Odontology, Umeå University, Umeå, Sweden
Elom Kouassivi Aglago
Affiliation:
Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK
Mazda Jenab*
Affiliation:
Nutrition and Metabolism Branch, International Agency for Research on Cancer, World Health Organization, Lyon, France
Heinz Freisling
Affiliation:
Nutrition and Metabolism Branch, International Agency for Research on Cancer, World Health Organization, Lyon, France
*
*Corresponding author: Mazda Jenab, email jenabm@iarc.who.int

Abstract

Dicarbonyl compounds are highly reactive precursors of advanced glycation end products (AGE), produced endogenously, present in certain foods and formed during food processing. AGE contribute to the development of adverse metabolic outcomes, but health effects of dietary dicarbonyls are largely unexplored. We investigated associations between three dietary dicarbonyl compounds, methylglyoxal (MGO), glyoxal (GO) and 3-deoxyglucosone (3-DG), and body weight changes in European adults. Dicarbonyl intakes were estimated using food composition database from 263 095 European Prospective Investigation into Cancer and Nutrition–Physical Activity, Nutrition, Alcohol, Cessation of Smoking, Eating Out of Home in Relation to Anthropometry participants with two body weight assessments (median follow-up time = 5·4 years). Associations between dicarbonyls and 5-year body-weight changes were estimated using mixed linear regression models. Stratified analyses by sex, age and baseline BMI were performed. Risk of becoming overweight/obese was assessed using multivariable-adjusted logistic regression. MGO intake was associated with 5-year body-weight gain of 0·089 kg (per 1-sd increase, 95 % CI 0·072, 0·107). 3-DG was inversely associated with body-weight change (–0·076 kg, −0·094, −0·058). No significant association was observed for GO (0·018 kg, −0·002, 0·037). In stratified analyses, GO was associated with body-weight gain among women and older participants (above median of 52·4 years). MGO was associated with higher body-weight gain among older participants. 3-DG was inversely associated with body-weight gain among younger and normal-weight participants. MGO was associated with a higher risk of becoming overweight/obese, while inverse associations were observed for 3-DG. No associations were observed for GO with overweight/obesity. Dietary dicarbonyls are inconsistently associated with body weight change among European adults. Further research is needed to clarify the role of these food components in overweight and obesity, their underlying mechanisms and potential public health implications.

Type
Research Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

These authors contributed equally to this work

References

World Health Organization. Regional Office for Europe (2022) WHO European Regional Obesity Report 2022. Copenhagen: World Health Organization. Regional Office for Europe.Google Scholar
Dai, H, Alsalhe, TA, Chalghaf, N, et al. (2020) The global burden of disease attributable to high body mass index in 195 countries and territories, 1990–2017: an analysis of the Global Burden of Disease Study. PLoS Med 17, e1003198.CrossRefGoogle ScholarPubMed
WCRF/AICR (2018) Continuous Update Project Expert Report 2018. Body Fatness and Weight Gain and the Risk of Cancer 142. https://www.wcrf.org/wp-content/uploads/2021/01/Body-fatness-and-weight-gain_0.pdf (accessed May 2023).Google Scholar
Hall, KD, Ayuketah, A, Brychta, R, et al. (2019) Ultra-processed diets cause excess calorie intake and weight gain: an inpatient randomized controlled trial of ad libitum food intake. Cell Metab 30, 6777.e3.CrossRefGoogle Scholar
Beslay, M, Srour, B, Méjean, C, et al. (2020) Ultra-processed food intake in association with BMI change and risk of overweight and obesity: a prospective analysis of the French NutriNet-Santé cohort. PLoS Med 17, e1003256.CrossRefGoogle ScholarPubMed
Cordova, R, Kliemann, N, Huybrechts, I, et al. (2021) Consumption of ultra-processed foods associated with weight gain and obesity in adults: a multi-national cohort study. Clin Nutr Edinb Scotl 40, 50795088.CrossRefGoogle ScholarPubMed
Valicente, VM, Peng, C-H, Pacheco, KN, et al. (2023) Ultra-processed foods and obesity risk: a critical review of reported mechanisms. Adv Nutr 14, 718738.CrossRefGoogle Scholar
Nigro, C, Leone, A, Fiory, F, et al. (2019) Dicarbonyl stress at the crossroads of healthy and unhealthy aging. Cells 8, 749.CrossRefGoogle ScholarPubMed
Masania, J, Malczewska-Malec, M, Razny, U, et al. (2016) Dicarbonyl stress in clinical obesity. Glycoconj J 33, 581589.CrossRefGoogle ScholarPubMed
Degen, J, Hellwig, M & Henle, T (2012) 1,2-dicarbonyl compounds in commonly consumed foods. J Agric Food Chem 60, 70717079.CrossRefGoogle ScholarPubMed
Scheijen, JLJM & Schalkwijk, CG (2014) Quantification of glyoxal, methylglyoxal and 3-deoxyglucosone in blood and plasma by ultra performance liquid chromatography tandem mass spectrometry: evaluation of blood specimen. Clin Chem Lab Med 52, 8591.CrossRefGoogle ScholarPubMed
Maasen, K, Scheijen, JLJM, Opperhuizen, A, et al. (2021) Quantification of dicarbonyl compounds in commonly consumed foods and drinks; presentation of a food composition database for dicarbonyls. Food Chem 339, 128063.CrossRefGoogle ScholarPubMed
Hellwig, M, Gensberger-Reigl, S, Henle, T, et al. (2018) Food-derived 1,2-dicarbonyl compounds and their role in diseases. Semin Cancer Biol 49, 18.CrossRefGoogle ScholarPubMed
Rabbani, N & Thornalley, PJ (2015) Dicarbonyl stress in cell and tissue dysfunction contributing to ageing and disease. Biochem Biophys Res Commun 458, 221226.CrossRefGoogle ScholarPubMed
Rabbani, N, Xue, M & Thornalley, PJ (2016) Dicarbonyls and glyoxalase in disease mechanisms and clinical therapeutics. Glycoconj J 33, 513525.CrossRefGoogle ScholarPubMed
Maessen, DEM, Stehouwer, CDA & Schalkwijk, CG (2015) The role of methylglyoxal and the glyoxalase system in diabetes and other age-related diseases. Clin Sci Lond Engl 1979 128, 839861.Google ScholarPubMed
Tikellis, C, Pickering, RJ, Tsorotes, D, et al. (2014) Dicarbonyl stress in the absence of hyperglycemia increases endothelial inflammation and atherogenesis similar to that observed in diabetes. Diabetes 63, 39153925.CrossRefGoogle ScholarPubMed
Schalkwijk, CG & Stehouwer, CDA (2020) Methylglyoxal, a highly reactive dicarbonyl compound, in diabetes, its vascular complications, and other age-related diseases. Physiol Rev 100, 407461.CrossRefGoogle ScholarPubMed
Wang, X-J, Ma, S-B, Liu, Z-F, et al. (2019) Elevated levels of α-dicarbonyl compounds in the plasma of type II diabetics and their relevance with diabetic nephropathy. J Chromatogr B Analyt Technol Biomed Life Sci 1106–1107, 1925.CrossRefGoogle ScholarPubMed
Kuhla, B, Lüth, H-J, Haferburg, D, et al. (2005) Methylglyoxal, glyoxal, and their detoxification in Alzheimer’s disease. Ann N Y Acad Sci 1043, 211216.CrossRefGoogle ScholarPubMed
Li, WY, Lee, CY, Lee, KM, et al. (2022) Advanced glycation end-product precursor methylglyoxal may lead to development of Alzheimer’s disease. Diabetes Metab Syndr Obes Targets Ther 15, 31533166.CrossRefGoogle ScholarPubMed
Thornalley, PJ, Langborg, A & Minhas, HS (1999) Formation of glyoxal, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose. Biochem J 344(Pt 1), 109116.CrossRefGoogle ScholarPubMed
Maasen, K, Eussen, SJPM, Scheijen, JLJM, et al. (2022) Higher habitual intake of dietary dicarbonyls is associated with higher corresponding plasma dicarbonyl concentrations and skin autofluorescence: the Maastricht Study. Am J Clin Nutr 115, 3444.CrossRefGoogle ScholarPubMed
Maasen, K, Eussen, SJPM, Dagnelie, PC, et al. (2022) Habitual intake of dietary methylglyoxal is associated with less low-grade inflammation: the Maastricht Study. Am J Clin Nutr 116, 17151728.CrossRefGoogle ScholarPubMed
Maasen, K, Eussen, SJPM, Dagnelie, PC, et al. (2023) Habitual intake of dietary dicarbonyls is associated with greater insulin sensitivity and lower prevalence of type 2 diabetes: the Maastricht Study. Am J Clin Nutr 118, 151161.CrossRefGoogle ScholarPubMed
Cordova, R, Knaze, V, Viallon, V, et al. (2020) Dietary intake of advanced glycation end products (AGEs) and changes in body weight in European adults. Eur J Nutr 59, 28932904.CrossRefGoogle ScholarPubMed
May, AM, Romaguera, D, Travier, N, et al. (2012) Combined impact of lifestyle factors on prospective change in body weight and waist circumference in participants of the EPIC-PANACEA study. PLOS ONE 7, e50712.CrossRefGoogle ScholarPubMed
Riboli, E, Hunt, KJ, Slimani, N, et al. (2002) European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr 5, 11131124.CrossRefGoogle Scholar
Riboli, E & Kaaks, R (1997) The EPIC Project: rationale and study design. European Prospective Investigation into Cancer and Nutrition. Int J Epidemiol 26, S6S14.Google Scholar
Vergnaud, A-C, Norat, T, Romaguera, D, et al. (2010) Meat consumption and prospective weight change in participants of the EPIC-PANACEA study. Am J Clin Nutr 92, 398407.CrossRefGoogle ScholarPubMed
Vergnaud, A-C, Norat, T, Romaguera, D, et al. (2012) 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, 184193.CrossRefGoogle ScholarPubMed
Spencer, EA, Appleby, PN, Davey, GK, et al. (2002) Validity of self-reported height and weight in 4808 EPIC–Oxford participants. Public Health Nutr 5, 561565.CrossRefGoogle ScholarPubMed
Huybrechts, I, Rauber, F, Nicolas, G, et al. (2022) Characterization of the degree of food processing in the European Prospective Investigation into Cancer and Nutrition: application of the Nova classification and validation using selected biomarkers of food processing. Front Nutr 9, 1035580.CrossRefGoogle ScholarPubMed
Slimani, N, Deharveng, G, Unwin, I, et al. (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, 10371056.CrossRefGoogle ScholarPubMed
Buckland, G, González, CA, Agudo, A, et al. (2009) Adherence to the Mediterranean diet and risk of coronary heart disease in the Spanish EPIC cohort study. Am J Epidemiol 170, 15181529.CrossRefGoogle Scholar
Goldberg, GR, Black, AE, Jebb, SA, et al. (1991) Critical evaluation of energy intake data using fundamental principles of energy physiology: 1. Derivation of cut-off limits to identify under-recording. Eur J Clin Nutr 45, 569581.Google ScholarPubMed
Mifflin, MD, St Jeor, ST, Hill, LA, et al. (1990) A new predictive equation for resting energy expenditure in healthy individuals. Am J Clin Nutr 51, 241247.CrossRefGoogle ScholarPubMed
Te Morenga, L, Mallard, S & Mann, J (2012) Dietary sugars and body weight: systematic review and meta-analyses of randomised controlled trials and cohort studies. BMJ 346, e7492e7492.CrossRefGoogle ScholarPubMed
EFSA (2021) EFSA Explains Draft Scientific Opinion on a Tolerable Upper Intake Level for Dietary Sugars. https://www.efsa.europa.eu/en/corporate-pubs/efsa-explains-draft-scientific-opinion-tolerable-upper-intake-level-dietary-sugars (accessed January 2022).Google Scholar
Mertens, E, Colizzi, C & Peñalvo, JL (2022) Ultra-processed food consumption in adults across Europe. Eur J Nutr 61, 15211539.CrossRefGoogle ScholarPubMed
Lopez-Garcia, E, van Dam, RM, Rajpathak, S, et al. (2006) Changes in caffeine intake and long-term weight change in men and women. Am J Clin Nutr 83, 674680.CrossRefGoogle ScholarPubMed
Larsen, SC, Mikkelsen, M-L, Frederiksen, P, et al. (2018) Habitual coffee consumption and changes in measures of adiposity: a comprehensive study of longitudinal associations. Int J Obes 2005 42, 880886.Google ScholarPubMed
Lee, A, Lim, W, Kim, S, et al. (2019) Coffee intake and obesity: a meta-analysis. Nutrients 11, 1274.CrossRefGoogle ScholarPubMed
Gil-Lespinard, M, Castañeda, J, Almanza-Aguilera, E, et al. (2022) Dietary Intake of 91 Individual Polyphenols and 5-Year Body Weight Change in the EPIC-PANACEA Cohort. Antioxid Basel Switz 11, 2425.CrossRefGoogle ScholarPubMed
World Cancer Research Fund/American Institute for Cancer Research (2018) Continuous Update Project. Diet, Nutrition, Physical Activity and the Prevention of Cancer. Summary of Evidence. https://www.wcrf.org/wp-content/uploads/2021/02/Summary-of-Third-Expert-Report-2018.pdf (accessed May 2023).Google Scholar
Kolb, H, Stumvoll, M, Kramer, W, et al. (2018) Insulin translates unfavourable lifestyle into obesity. BMC Med 16, 232.CrossRefGoogle ScholarPubMed
Gao, Y, Bielohuby, M, Fleming, T, et al. (2017) Dietary sugars, not lipids, drive hypothalamic inflammation. Mol Metab 6, 897908.CrossRefGoogle Scholar
Wang, F, Zhou, L, Song, X, et al. (2017) Acute reduction of incretin effect and glucose intolerance in rats by single intragastric administration of 3-deoxyglucosone. Exp Clin Endocrinol Diabetes 125, 411.Google ScholarPubMed
Ard, J, Fitch, A, Fruh, S, et al. (2021) Weight loss and maintenance related to the mechanism of action of glucagon-like peptide 1 receptor agonists. Adv Ther 38, 28212839.CrossRefGoogle Scholar
de Graaf, MCG, Scheijen, JLJM, Spooren, CEGM, et al. (2022) The intake of dicarbonyls and advanced glycation endproducts as part of the habitual diet is not associated with intestinal inflammation in inflammatory bowel disease and irritable bowel syndrome patients. Nutrients 15, 83.CrossRefGoogle Scholar
Watson, AMD, Soro-Paavonen, A, Sheehy, K, et al. (2011) Delayed intervention with AGE inhibitors attenuates the progression of diabetes-accelerated atherosclerosis in diabetic apolipoprotein E knockout mice. Diabetologia 54, 681689.CrossRefGoogle ScholarPubMed
Zemva, J, Fink, CA, Fleming, TH, et al. (2017) Hormesis enables cells to handle accumulating toxic metabolites during increased energy flux. Redox Biol 13, 674686.CrossRefGoogle ScholarPubMed
Fujioka, K & Shibamoto, T (2006) Determination of toxic carbonyl compounds in cigarette smoke. Environ Toxicol 21, 4754.CrossRefGoogle ScholarPubMed
Bao, ML, Pantani, F, Griffini, O, et al. (1998) Determination of carbonyl compounds in water by derivatization-solid-phase microextraction and gas chromatographic analysis. J Chromatogr A 809, 7587.CrossRefGoogle ScholarPubMed
Supplementary material: File

Debras et al. supplementary material

Debras et al. supplementary material
Download Debras et al. supplementary material(File)
File 1.5 MB