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European Journal of Nutrition
Published in: European Journal of Nutrition 2/2014

01-03-2014 | Original Contribution

Effect of dietary advanced glycation end products on postprandial appetite, inflammation, and endothelial activation in healthy overweight individuals

Authors: Malene W. Poulsen, Monika J. Bak, Jeanette M. Andersen, Rastislav Monošík, Anne C. Giraudi-Futin, Jens J. Holst, John Nielsen, Lotte Lauritzen, Lesli H. Larsen, Susanne Bügel, Lars O. Dragsted

Published in: European Journal of Nutrition | Issue 2/2014

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Abstract

Purpose

Advanced glycation end products (AGEs) formed in food during high-heat cooking may induce overeating and inflammation. We investigated whether AGE contents in a single meal affect postprandial appetite and markers of inflammation, endothelial activation, and oxidative stress.

Methods

In total, 19 healthy overweight individuals completed a crossover meal test with two meals of identical ingredients prepared by roasting (H-AGE) or steaming (L-AGE), respectively. Postprandial blood samples were analysed for Nε-carboxymethyl-lysine (CML), appetite-regulating gut hormones, glucose, insulin, triacylglycerol, and markers of inflammation and endothelial activation. Subjective appetite ratings and subsequent food intake were also assessed, and urine was analysed for CML, methylglyoxal-derived hydroimidazolone (MG-H1), and F2-isoprostanes.

Results

CML content of the H- and L-AGE meals was 5.0 and 2.8 mg, respectively. Plasma CML and urinary CML and MG-H1 tended to be higher after the H-AGE meal. There was no change in subsequent food intake, appetite sensations, or appetite hormone responses between meals, except for the overall ghrelin response, which was higher after the H-AGE meal compared with the L-AGE meal (p = 0.016). There was an increased glycaemic response to the H-AGE meal (p = 0.027) compared with the L-AGE meal. Inflammatory and endothelial activation markers did not differ between meals, but there was an overall effect on endothelial activation (p = 0.021) and on the oxidative marker, F2-isoprostanes, in urine (p = 0.013).

Conclusion

The present study did not show any pronounced effects of AGEs on appetite and markers of inflammation, but did indicate that AGEs may affect postprandial ghrelin, oxidative stress, and glucose responses.
Literature
1.
Hossain P, Kawar B, El NM (2007) Obesity and diabetes in the developing world—a growing challenge. N Engl J Med 356:213–215CrossRef
2.
Uribarri J, Woodruff S, Goodman S, Cai W, Chen X, Pyzik R, Yong A, Striker GE, Vlassara H (2010) Advanced glycation end products in foods and a practical guide to their reduction in the diet. J Am Diet Assoc 110:911–916CrossRef
3.
van Boekel MA (2006) Formation of flavour compounds in the Maillard reaction. Biotechnol Adv 24:230–233CrossRef
4.
Perez-Locas C, Yaylayan VA (2010) The Maillard reaction and food quality deterioration. In: Skibsted LH, Risbo J, Andersen ML (eds) Chemical deterioration and physical instability of food and beverages. Woodhead Publishing, Cambridge, pp 70–94CrossRef
5.
Vlassara H, Striker GE (2011) AGE restriction in diabetes mellitus: a paradigm shift. Nat Rev Endocrinol 7:526–539CrossRef
6.
Cai W, Gao QD, Zhu L, Peppa M, He C, Vlassara H (2002) Oxidative stress-inducing carbonyl compounds from common foods: novel mediators of cellular dysfunction. Mol Med 8:337–346
7.
Kilhovd BK, Berg TJ, Birkeland KI, Thorsby P, Hanssen KF (1999) Serum levels of advanced glycation end products are increased in patients with type 2 diabetes and coronary heart disease. Diabetes Care 22:1543–1548CrossRef
8.
Tan KC, Chow WS, Ai VH, Metz C, Bucala R, Lam KS (2002) Advanced glycation end products and endothelial dysfunction in type 2 diabetes. Diabetes Care 25:1055–1059CrossRef
9.
Tan KC, Chow WS, Tam S, Bucala R, Betteridge J (2004) Association between acute-phase reactants and advanced glycation end products in type 2 diabetes. Diabetes Care 27:223–228CrossRef
10.
Negrean M, Stirban A, Stratmann B, Gawlowski T, Horstmann T, Gotting C, Kleesiek K, Mueller-Roesel M, Koschinsky T, Uribarri J, Vlassara H, Tschoepe D (2007) Effects of low- and high-advanced glycation endproduct meals on macro- and microvascular endothelial function and oxidative stress in patients with type 2 diabetes mellitus. Am J Clin Nutr 85:1236–1243
11.
Flint A, Raben A, Blundell JE, Astrup A (2000) Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. Int J Obes Relat Metab Disord 24:38–48CrossRef
12.
Bingham S, Cummings JH (1983) The use of 4-aminobenzoic acid as a marker to validate the completeness of 24 h urine collections in man. Clin Sci 64:629–635
13.
Orskov C, Jeppesen J, Madsbad S, Holst JJ (1991) Proglucagon products in plasma of noninsulin-dependent diabetics and nondiabetic controls in the fasting state and after oral glucose and intravenous arginine. J Clin Invest 87:415–423CrossRef
14.
Zhang H, Il’yasova D, Sztaray J, Young SP, Wang F, Millington DS (2010) Quantification of the oxidative damage biomarker 2,3-dinor-8-isoprostaglandin-F(2alpha) in human urine using liquid chromatography-tandem mass spectrometry. Anal Biochem 399:302–304CrossRef
15.
Ames JM (2008) Determination of N epsilon-(carboxymethyl)lysine in foods and related systems. Ann N Y Acad Sci 1126:20–24CrossRef
16.
Thornalley PJ, Battah S, Ahmed N, Karachalias N, Agalou S, Babaei-Jadidi R, Dawnay A (2003) Quantitative screening of advanced glycation endproducts in cellular and extracellular proteins by tandem mass spectrometry. Biochem J 375:581–592CrossRef
17.
Jongberg S, Rasmussen M, Skibsted LH, Olsen K (2012) Detection of advanced glycation end-products (AGEs) during dry-state storage of beta-lactoglobulin/lactose. Aust J Chem 65:1620–1624CrossRef
18.
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 91:1220–1226CrossRef
19.
Delgado-Andrade C, Tessier FJ, Niquet-Leridon C, Seiquer I, Pilar NM (2012) Study of the urinary and faecal excretion of Nepsilon-carboxymethyllysine in young human volunteers. Amino Acids 43:595–602CrossRef
20.
Schiekofer S, Franke S, Andrassy M, Chen J, Rudofsky G, Schneider JG, von EM, Wendt T, Morcos M, Kientsch-Engel R, Stein G, Schleicher E, Nawroth PP, Bierhaus A (2006) Postprandial mononuclear NF-kappaB activation is independent of the AGE-content of a single meal. Exp Clin Endocrinol Diabetes 114:160–167
21.
Janssen P, Van den Berghe P, Verschueren S, Lehmann A, Depoortere I, Tack J (2011) Review article: the role of gastric motility in the control of food intake. Aliment Pharmacol Ther 33:880–894CrossRef
22.
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 94:6474–6479CrossRef
23.
Henle T (2007) Dietary advanced glycation end products—a risk to human health? A call for an interdisciplinary debate. Mol Nutr Food Res 51:1075–1078CrossRef
24.
Henle T (2008) Maillard reaction of proteins and advanced glycation end products (AGEs) in food. In: Stadler RH, Lineback DR (eds) Process-induced food toxicants. Wiley, Hoboken, pp 215–242CrossRef
25.
Assar SH, Moloney C, Lima M, Magee R, Ames JM (2009) Determination of Nepsilon-(carboxymethyl)lysine in food systems by ultra performance liquid chromatography-mass spectrometry. Amino Acids 36:317–326CrossRef
26.
Sebekova K, Klenovics KS, Boor P, Celec P, Behuliak M, Schieberle P, Heidland A, Palkovits M, Somoza V (2012) Behaviour and hormonal status in healthy rats on a diet rich in Maillard reaction products with or without solvent extractable aroma compounds. Physiol Behav 105:693–701CrossRef
27.
Ruijschop RM, Boelrijk AE, de Ru JA, de Graaf C, Westerterp-Plantenga MS (2008) Effects of retro-nasal aroma release on satiation. Br J Nutr 99:1140–1148CrossRef
28.
Ruijschop RM, Boelrijk AE, Burgering MJ, de Graaf C, Westerterp-Plantenga MS (2010) Acute effects of complexity in aroma composition on satiation and food intake. Chem Senses 35:91–100CrossRef
29.
Gil-Campos M, Aguilera CM, Canete R, Gil A (2006) Ghrelin: a hormone regulating food intake and energy homeostasis. Br J Nutr 96:201–226CrossRef
30.
Stirban A, Negrean M, Gotting C, Stratmann B, Gawlowski T, Mueller-Roesel M, Kleesiek K, Koschinsky T, Tschoepe D (2008) Leptin decreases postprandially in people with type 2 diabetes, an effect reduced by the cooking method. Horm Metab Res 40:896–900CrossRef
31.
Rosen LA, Ostman EM, Bjorck IM (2011) Effects of cereal breakfasts on postprandial glucose, appetite regulation and voluntary energy intake at a subsequent standardized lunch; focusing on rye products. Nutr J 10:7CrossRef
32.
Miele C, Riboulet A, Maitan MA, Oriente F, Romano C, Formisano P, Giudicelli J, Beguinot F, Van OE (2003) Human glycated albumin affects glucose metabolism in L6 skeletal muscle cells by impairing insulin-induced insulin receptor substrate (IRS) signaling through a protein kinase C alpha-mediated mechanism. J Biol Chem 278:47376–47387CrossRef
33.
Unoki H, Bujo H, Yamagishi S, Takeuchi M, Imaizumi T, Saito Y (2007) Advanced glycation end products attenuate cellular insulin sensitivity by increasing the generation of intracellular reactive oxygen species in adipocytes. Diabetes Res Clin Pract 76:236–244CrossRef
34.
Cassese A, Esposito I, Fiory F, Barbagallo AP, Paturzo F, Mirra P, Ulianich L, Giacco F, Iadicicco C, Lombardi A, Oriente F, Van OE, Beguinot F, Formisano P, Miele C (2008) In skeletal muscle advanced glycation end products (AGEs) inhibit insulin action and induce the formation of multimolecular complexes including the receptor for AGEs. J Biol Chem 283:36088–36099CrossRef
35.
Puddu A, Storace D, Odetti P, Viviani GL (2010) Advanced glycation end-products affect transcription factors regulating insulin gene expression. Biochem Biophys Res Commun 395:122–125CrossRef
36.
Uribarri J, Cai W, Ramdas M, Goodman S, Pyzik R, Chen X, Zhu L, Striker GE, Vlassara H (2011) Restriction of advanced glycation end products improves insulin resistance in human type 2 diabetes: potential role of AGER1 and SIRT1. Diabetes Care 34:1610–1616CrossRef
37.
Uribarri J, Stirban A, Sander D, Cai W, Negrean M, Buenting CE, Koschinsky T, Vlassara H (2007) Single oral challenge by advanced glycation end products acutely impairs endothelial function in diabetic and nondiabetic subjects. Diabetes Care 30:2579–2582CrossRef
38.
Aljada A, Mohanty P, Ghanim H, Abdo T, Tripathy D, Chaudhuri A, Dandona P (2004) Increase in intranuclear nuclear factor kappaB and decrease in inhibitor kappaB in mononuclear cells after a mixed meal: evidence for a proinflammatory effect. Am J Clin Nutr 79:682–690
39.
Vlassara H, Cai W, Crandall J, Goldberg T, Oberstein R, Dardaine V, Peppa M, Rayfield EJ (2002) Inflammatory mediators are induced by dietary glycotoxins, a major risk factor for diabetic angiopathy. Proc Natl Acad Sci USA 99:15596–15601CrossRef
40.
Peppa M, Uribarri J, Cai W, Lu M, Vlassara H (2004) Glycoxidation and inflammation in renal failure patients. Am J Kidney Dis 43:690–695CrossRef
41.
Vlassara H, Cai WJ, Goodman S, Pyzik R, Yong A, Chen X, Zhu L, Neade T, Beeri M, Silverman JM, Ferrucci L, Tansman L, Striker GE, Uribarri J (2009) Protection against loss of innate defenses in adulthood by low advanced glycation end products (AGE) intake: role of the antiinflammatory AGE receptor-1. J Clin Endocrinol Metab 94:4483–4491CrossRef
42.
Vlassara H, Fuh H, Donnelly T, Cybulsky M (1995) Advanced glycation endproducts promote adhesion molecule (VCAM-1, ICAM-1) expression and atheroma formation in normal rabbits. Mol Med 1:447–456
43.
Schmidt AM, Hori O, Chen JX, Li JF, Crandall J, Zhang J, Cao R, Yan SD, Brett J, Stern D (1995) Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice. A potential mechanism for the accelerated vasculopathy of diabetes. J Clin Invest 96:1395–1403CrossRef
44.
Basta G, Lazzerini G, Massaro M, Simoncini T, Tanganelli P, Fu C, Kislinger T, Stern DM, Schmidt AM, De CR (2002) Advanced glycation end products activate endothelium through signal-transduction receptor RAGE: a mechanism for amplification of inflammatory responses. Circulation 105:816–822CrossRef
45.
Basta G, Lazzerini G, Del TS, Ratto GM, Schmidt AM, De CR (2005) At least 2 distinct pathways generating reactive oxygen species mediate vascular cell adhesion molecule-1 induction by advanced glycation end products. Arterioscler Thromb Vasc Biol 25:1401–1407CrossRef
46.
Ramasamy R, Yan SF, Herold K, Clynes R, Schmidt AM (2008) Receptor for advanced glycation end products: fundamental roles in the inflammatory response: winding the way to the pathogenesis of endothelial dysfunction and atherosclerosis. Ann N Y Acad Sci 1126:7–13CrossRef
47.
Ramasamy R, Yan SF, Schmidt AM (2011) Receptor for AGE (RAGE): signaling mechanisms in the pathogenesis of diabetes and its complications. Ann N Y Acad Sci 1243:88–102CrossRef
48.
Coelho RC, Hermsdorff HH, Bressan J (2013) Anti-inflammatory properties of orange juice: possible favorable molecular and metabolic effects. Plant Foods Hum Nutr 68:1–10CrossRef
49.
Brouns F, Bjorck I, Frayn KN, Gibbs AL, Lang V, Slama G, Wolever TM (2005) Glycaemic index methodology. Nutr Res Rev 18:145–171CrossRef
Metadata
Title
Effect of dietary advanced glycation end products on postprandial appetite, inflammation, and endothelial activation in healthy overweight individuals
Authors
Malene W. Poulsen
Monika J. Bak
Jeanette M. Andersen
Rastislav Monošík
Anne C. Giraudi-Futin
Jens J. Holst
John Nielsen
Lotte Lauritzen
Lesli H. Larsen
Susanne Bügel
Lars O. Dragsted
Publication date
01-03-2014
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 2/2014
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-013-0574-y

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