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Plasma cytokine response during the postprandial period: a potential causal process in vascular disease?

Published online by Cambridge University Press:  08 March 2007

Graham C. Burdge  and
Philip C. Calder
Graham C. Burdge*
Affiliation:
Institute of Human Nutrition, Developmental Origins of Adult Health and Disease Division, Biomedical Sciences Building (62), University of Southampton, Bassett Crescent East, Southampton, SO16 7PX, UK
Philip C. Calder
Affiliation:
Institute of Human Nutrition, Developmental Origins of Adult Health and Disease Division, Biomedical Sciences Building (62), University of Southampton, Bassett Crescent East, Southampton, SO16 7PX, UK
*
*Corresponding author: Dr G. C. Burdge, fax +44 2380 594379, email [email protected]
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Abstract

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Chronic inflammation of the vascular endothelium produces endothelial dysfunction and ultimately atherogenesis. Postprandial hyperlipidaemia is an independent risk factor for cardiovascular disease. Recent studies show that the magnitude of postprandial lipaemia following a single fatty meal is negatively related to vascular function. This is associated with a transient increase in the concentrations of pro-inflammatory cytokines and soluble adhesion molecules and in pro-oxidant activity. One possible interpretation is that repeated exposure of the blood vessel wall to the activities of pro-inflammatory cytokines and pro-oxidants may damage the vascular endothelium and promote atherogenesis. Based on these results, we propose a model of a causal mechanism to explain how consumption of a fatty meal may impair vascular dysfunction.

Keywords

Vascular dysfunctioncytokinespostprandialcardiovascular disease
Type
Horizons in nutritional science
Information
British Journal of Nutrition , Volume 93 , Issue 1 , January 2005 , pp. 3 - 9
Copyright
Copyright © The Nutrition Society 2005

References

Bae, JH, Bassenge, E, Kim, KB, Kim, YN, Kim, KS, Lee, HJ, Moon, KC, Lee, MS, Park, KY & Schwemmer, M (2001) Postprandial hypertriglyceridemia impairs endothelial function by enhanced oxidant stress. Atherosclerosis 155, 517–523.CrossRefGoogle ScholarPubMed
Bae, JH, Schwemmer, M, Lee, IK, Lee, HJ, Park, KR, Kim, KY & Bassenge, E (2003) Postprandial hypertriglyceridemia-induced endothelial dysfunction in healthy subjects is independent of lipid oxidation. Int J Cardiol 87, 259–267.CrossRefGoogle ScholarPubMed
Burdge, GC, Jones, AE, Frye, SM, Goodson, L & Wootton, SA (2003) Effect of meal sequence on postprandial lipid, glucose and insulin responses in young men. Eur J Clin Nutr 57, 1536–1544.CrossRefGoogle ScholarPubMed
Carmena, R, Duriez, P & Fruchart, JC (2004) Atherogenic lipoprotein particles in atherosclerosis. Circulation 109, Suppl. III III-2–III-7.CrossRefGoogle ScholarPubMed
Ceriello, A, Quagliaro, L, Piconi, L, Assaloni, R, Da Ros, R, Maier, A, Esposito, K & Giugliano, D (2004) Effect of postprandial hypertriglyceridemia and hyperglycemia on circulating adhesion molecules and oxidative stress generation and the possible role of simvastatin treatment. Diabetes 53, 701–710.CrossRefGoogle ScholarPubMed
Chowienczyk, PJ, Watts, GF, Wierzbicki, AS, Cockcroft, JR, Brett, SE & Ritter, JM (1997) Preserved endothelial function in patients with severe hypertriglyceridemia and low functional lipoprotein lipase activity. J Am Coll Cardiol 29, 964–968.CrossRefGoogle ScholarPubMed
Cosentino, F, Hishikawa, K, Katusic, ZS & Luscher, TF (1997) High glucose increases nitric oxide synthase expression and superoxide anion generation in human aortic endothelial cells. Circulation 96, 25–28.CrossRefGoogle ScholarPubMed
Cox, DA, Vita, JA, Treasure, CB, Fish, RD, Alexander, RW, Ganz, P & Selwyn, AP (1989) Atherosclerosis impairs flow-mediated dilation of coronary arteries in humans. Circulation 80, 458–465.CrossRefGoogle ScholarPubMed
de Kreutzenberg, SV, Puato, M, Kiwanuka, E, Del Prato, S, Pauletto, P, Pasini, L, Tiengo, A & Avogaro, A (2003) Elevated non-esterified fatty acids impair nitric oxide independent vasodilation, in humans: evidence for a role of inwardly rectifying potassium channels. Atherosclerosis 169, 147–153.CrossRefGoogle ScholarPubMed
Djousse, L, Ellison, RC, McLennan, CE, Cupples, LA, Lipinska, I, Tofler, GH, Gokce, N & Vita, JA (1999) Acute effects of a high-fat meal with and without red wine on endothelial function in healthy subjects. Am J Cardiol 84, 660–664.CrossRefGoogle ScholarPubMed
Ebenbichler, CF, Kirchmair, R, Egger, C & Patsch, JR (1995) Postprandial state and atherosclerosis. Curr Opin Lipidol 6, 286–290.CrossRefGoogle ScholarPubMed
Esposito, K, Nappo, F, Marfella, R, Giugliano, G, Giugliano, F, Ciotola, M, Quagliaro, L, Ceriello, A & Giugliano, D (2002a) Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: role of oxidative stress. Circulation 106, 2067–2072.CrossRefGoogle ScholarPubMed
Esposito, K, Pontillo, A, Ciotola, M, Di Palo, C, Grella, E, Nicoletti, G & Giugliano, D (2002b) Weight loss reduces interleukin-18 levels in obese women. J Clin Endocrinol Metab 87, 3864–3866.CrossRefGoogle ScholarPubMed
Esposito, K, Nappo, F, Giugliano, F, Giugliano, G, Marfella, R & Giugliano, D (2003a) Effect of dietary antioxidants on postprandial endothelial dysfunction induced by a high-fat meal in healthy subjects. Am J Clin Nutr 77, 139–143.CrossRefGoogle ScholarPubMed
Esposito, K, Nappo, F, Giugliano, F, Di Palo, C, Ciotola, M, Barbieri, M, Paolisso, G & Giugliano, D (2003b) Meal modulation of circulating interleukin 18 and adiponectin concentrations in healthy subjects and in patients with type 2 diabetes mellitus. Am J Clin Nutr 78, 1135–1140.CrossRefGoogle ScholarPubMed
Evans, K, Burdge, GC, Wootton, SA, Clark, ML & Frayn, KN (2002) Regulation of dietary fatty acid entrapment in subcutaneous adipose tissue and skeletal muscle. Diabetes 51, 2684–2690.CrossRefGoogle ScholarPubMed
Fain, JN, Bahouth, SW & Madan, AK (2004) TNFalpha release by the nonfat cells of human adipose tissue. Int J Obes Relat Metab Disord 28, 616–622.CrossRefGoogle ScholarPubMed
Fichtlscherer, S, Kaszkin, M, Breuer, S, Dimmeler, S & Zeiher, AM (2004) Elevated secretory non-pancreatic type II phospholipase A2 serum activity is associated with impaired endothelial vasodilator function in patients with coronary artery disease. Clin Sci 106, 511–517.CrossRefGoogle ScholarPubMed
Frankel, EN, Kanner, J, German, JB, Parks, E & Kinsella, JE (1993) Inhibition of oxidation of human low-density lipoprotein by phenolic substances in red wine. Lancet 341, 454–457.CrossRefGoogle ScholarPubMed
Giugliano, G, Nicoletti, G, Grella, E, Giugliano, F, Esposito, K, Scuderi, N & D'Andrea, F (2004) Effect of liposuction on insulin resistance and vascular inflammatory markers in obese women. Br J Plast Surg 57, 190–194.CrossRefGoogle ScholarPubMed
Glass, CK & Witztum, JL (2001) Atherosclerosis: the road ahead. Cell 104, 503–516.CrossRefGoogle ScholarPubMed
Groot, PH, van Stiphout, WA, Krauss, XH, Jansen, H, van Tol, A, van Ramshorst, E, Chin-On, S, Hofman, A, Cresswell, SR & Havekes, L (1991) Postprandial lipoprotein metabolism in normolipidemic men with and without coronary artery disease. Arterioscler Thromb 11, 653–662.CrossRefGoogle ScholarPubMed
Guha, M, Bai, W, Nadler, JL & Natarajan, R (2000) Molecular mechanisms of tumor necrosis factor alpha gene expression in monocytic cells via hyperglycemia-induced oxidant stress-dependent and -independent pathways. J Biol Chem 275, 17728–17739.CrossRefGoogle ScholarPubMed
Hasdai, D, Gibbons, RJ, Holmes DR, Jr, Higano, ST & Lerman, A (1997) Coronary endothelial dysfunction in humans is associated with myocardial perfusion defects. Circulation 96, 3390–3395.CrossRefGoogle ScholarPubMed
Hurt-Camejo, E, Andersen, S, Standal, R, Rosengren, B, Sartipy, P, Stadberg, E & Johansen, B (1997) Localization of nonpancreatic secretory phospholipase A2 in normal and atherosclerotic arteries. Activity of the isolated enzyme on low-density lipoproteins. Arterioscler Thromb Vasc Biol 17, 300–309.CrossRefGoogle ScholarPubMed
Hwang, SJ, Ballantyne, CM, Sharrett, AR, Smith, LC, Davis, CE, Gotto AM, Jr & Boerwinkle, E (1997) Circulating adhesion molecules VCAM-1, ICAM-1, and E-selectin in carotid atherosclerosis and incident coronary heart disease cases: the Atherosclerosis Risk In Communities (ARIC) study. Circulation 16, 4219–4225.CrossRefGoogle Scholar
Hyson, DA, Paglieroni, TG, Wun, T & Rutledge, JC (2002) Postprandial lipemia is associated with platelet and monocyte activation and increased monocyte cytokine expression in normolipemic men. Clin Appl Thromb Hemost 8, 147–155.CrossRefGoogle ScholarPubMed
Ido, Y, Kilo, C & Williamson, JR (1997) Cytosolic NADH/NAD +, free radicals, and vascular dysfunction in early diabetes mellitus. Diabetologia 40, Suppl. 2S115–S117.CrossRefGoogle ScholarPubMed
Joannides, R, Haefeli, WE, Linder, L, Richard, V, Bakkali, EH, Thuillez, C & Luscher, TF (1995) Nitric oxide is responsible for flow-dependent dilatation of human peripheral conduit arteries in vivo. Circulation 91, 1314–1319.CrossRefGoogle ScholarPubMed
Karpe, F (1997) Postprandial lipid metabolism in relation to coronary heart disease. Proc Nutr Soc 56, 671–678.CrossRefGoogle ScholarPubMed
Katan, MB, Zock, PL & Mensink, RP (1995) Dietary oils, lipoproteins and coronary heart disease. Am J Clin Nutr 61, 1368S – 1373S.CrossRefGoogle ScholarPubMed
Kirwan, JP, Krishnan, RK, Weaver, JA, Del Aguila, LF & Evans, WJ (2001) Human aging is associated with altered TNF-alpha production during hyperglycemia and hyperinsulinemia. Am J Physiol Endocrinol Metab 281, E1137–E1143.CrossRefGoogle Scholar
Lundman, P, Eriksson, M, Schenck-Gustafsson, K, Karpe, F & Tornvall, P (1997) Transient triglyceridemia decreases vascular reactivity in young, healthy men without risk factors for coronary heart disease. Circulation 96, 3266–3268.CrossRefGoogle ScholarPubMed
Lundman, P, Eriksson, MJ, Stuhlinger, M, Cooke, JP, Hamsten, A & Tornvall, P (2001) Mild-to-moderate hypertriglyceridemia in young men is associated with endothelial dysfunction and increased plasma concentrations of asymmetric dimethylarginine. J Am Coll Cardiol 38, 111–116.CrossRefGoogle ScholarPubMed
Maggi, FM, Raselli, S, Grigore, L, Redaelli, L, Fantappie, S & Catapano, AL (2004) Lipoprotein remnants and endothelial dysfunction in the postprandial phase. J Clin Endocrinol Metab 89, 2946–2950.CrossRefGoogle ScholarPubMed
Marchesi, S, Lupattelli, G, Schillaci, G, Pirro, M, Siepi, D, Roscini, AR, Pasqualini, L & Mannarino, E (2000) Impaired flow-mediated vasoactivity during post-prandial phase in young healthy men. Atherosclerosis 153, 397–402.CrossRefGoogle ScholarPubMed
Marfella, R, Esposito, K, Giunta, R, Coppola, G, De Angelis, L, Farzati, B, Paolisso, G & Giugliano, D (2000) Circulating adhesion molecules in humans: role of hyperglycemia and hyperinsulinemia. Circulation 101, 2247–2251.CrossRefGoogle Scholar
Menschikowski, M, Rosner-Schiering, A, Eckey, R, Mueller, E, Koch, R & Jaross, W (2000) Expression of secretory group IIA phospholipase A(2) in relation to the presence of microbial agents, macrophage infiltrates, and transcripts of proinflammatory cytokines in human aortic tissues. Arterioscler Thromb Vasc Biol 20, 751–762.CrossRefGoogle Scholar
Morisaki, N, Saito, I, Tamura, K, Tashiro, J, Masuda, M, Kanzaki, T, Watanabe, S, Masuda, Y & Saito, Y (1997) New indices of ischemic heart disease and aging: studies on the serum levels of soluble intercellular adhesion molecule-1 (ICAM-1) and soluble vascular cell adhesion molecule-1 (VCAM-1) in patients with hypercholesterolemia and ischemic heart disease. Atherosclerosis 131, 43–48.CrossRefGoogle ScholarPubMed
Nappo, F, Esposito, K, Cioffi, M, Giugliano, G, Molinari, AM, Paolisso, G, Marfella, R & Giugliano, D (2002) Postprandial endothelial activation in healthy subjects and in type 2 diabetic patients: role of fat and carbohydrate meals. J Am Coll Cardiol 39, 1145–1150.CrossRefGoogle ScholarPubMed
Neunteufl, T, Katzenschlager, R, Hassan, A, Klaar, U, Schwarzacher, S, Glogar, D, Bauer, P & Weidinger, F (1997) Systemic endothelial dysfunction is related to the extent and severity of coronary artery disease. Atherosclerosis 28, 111–118.CrossRefGoogle Scholar
Ohara, Y, Peterson, TE & Harrison, DG (1993) Hypercholesterolemia increases endothelial superoxide anion production. J Clin Invest 91, 2546–2551.CrossRefGoogle ScholarPubMed
Patsch, JR, Miesenbock, G, Hoferwieser, T, Muhlberger, V, Knapp, E, Dunn, JK, Gotto, AM & Patsch, W (1992) Relation of triglyceride metabolism and coronary artery disease. Atheroscler Thromb 12, 1336–1345.Google ScholarPubMed
Perticone, F, Ceravolo, R & Pujia, A, et al. (2001) Prognostic significance of endothelial dysfunction in hypertensive patients. Circulation 104, 191–196.CrossRefGoogle ScholarPubMed
Plotnick, GD, Corretti, MC & Vogel, RA (1997) Effect of antioxidant vitamins on the transient impairment of endothelium-dependent brachial artery vasoactivity following a single high-fat meal. J Am Med Assoc 278, 1682–1686.CrossRefGoogle ScholarPubMed
Plutzky, J (1999) Atherosclerotic plaque rupture: emerging insights and opportunities. Am J Cardiol 84, 15J – 20J.CrossRefGoogle Scholar
Pontiroli, AE, Pizzocri, P, Koprivec, D, Vedani, P, Marchi, M, Arcelloni, C, Paroni, R, Esposito, K & Giugliano, D (2004) Body weight and glucose metabolism have a different effect on circulating levels of ICAM-1, E-selectin, and endothelin-1 in humans. Eur J Endocrinol 150, 195–200.CrossRefGoogle ScholarPubMed
Raitakari, OT, Lai, N, Griffiths, K, McCredie, R, Sullivan, D & Celermajer, DS (2000) Enhanced peripheral vasodilation in humans after a fatty meal. J Am Coll Cardiol 36, 417–422.CrossRefGoogle ScholarPubMed
Ridker, PM, Hennekens, CH, Roitman-Johnson, B, Stampfer, MJ & Allen, J (1998) Plasma concentration of soluble intercellular adhesion molecule 1 and risks of future myocardial infarction in apparently healthy men. Lancet 351, 88–92.CrossRefGoogle ScholarPubMed
Rohde, LE, Lee, RT, Rivero, J, Jamacochian, M, Arroyo, LH, Briggs, W, Rifai, N, Libby, P, Creager, MA & Ridker, PM (1998) Circulating cell adhesion molecules are correlated with ultrasound-based assessment of carotid atherosclerosis. Arterioscler Thromb Vasc Biol 18, 1765–1770.CrossRefGoogle ScholarPubMed
Ross, R (1999) Atherosclerosis – an inflammatory disease. N Engl J Med 340, 115–126.CrossRefGoogle ScholarPubMed
Schachinger, V, Britten, MB & Zeiher, AM (2000) Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation 101, 1899–1906.CrossRefGoogle ScholarPubMed
Stampfer, MJ, Krauss, RM, Ma, J, Blanche, PJ, Holl, LG, Sacks, FM & Hennekens, CH (1996) A prospective study of triglyceride level, low-density lipoprotein particle diameter, and risk of myocardial infarction. J Am Med Assoc 176, 882–888.CrossRefGoogle Scholar
Suwaidi, JA, Hamasaki, S, Higano, ST, Nishimura, RA, Holmes, DR & Lerman, A (2000) Long-term follow-up of patients with mild coronary artery disease and endothelial dysfunction. Circulation 101, 948–954.CrossRefGoogle ScholarPubMed
Thannickal, VJ & Fanburg, BL (2000) Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279, L1005–L1028.CrossRefGoogle ScholarPubMed
Twickler, TB, Cramer, MJ, Dallinga-Thie, GM, Chapman, MJ, Erkelens, DW & Koppeschaar, HP (2003) Adult-onset growth hormone deficiency: relation of postprandial dyslipidemia to premature atherosclerosis. J Clin Endocrinol Metab 88, 2479–2488.CrossRefGoogle ScholarPubMed
Ushio-Fukai, M, Zafari, AM, Fukui, T, Ishizaka, N & Griendling, KK (1996) p22phox is a critical component of the superoxide-generating NADH/NADPH oxidase system and regulates angiotensin II-induced hypertrophy in vascular smooth muscle cells. J Biol Chem 271, 23317–23321.CrossRefGoogle ScholarPubMed
Verhaar, MC, Wever, RM, Kastelein, JJ, van Dam, T, Koomans, HA & Rabelink, TJ (1998) 5-Methyltetrrahydrofolate, the active form of folic acid, restores endothelial function in familial hypercholesterolemia. Circulation 97, 237–241.CrossRefGoogle ScholarPubMed
Vita, JA, Treasure, CB, Nabel, EG, McLenachan, JM, Fish, RD, Yeung, AC, Vekshtein, VI, Selwyn, AP & Ganz, P (1990) Coronary vasomotor response to acetylcholine relates to risk factors for coronary artery disease. Circulation 81, 491–497.CrossRefGoogle ScholarPubMed
Vogel, RA, Corretti, MC & Plotnick, GD (1997) Effect of a single high-fat meal on endothelial function in healthy subjects. Am J Cardiol 79, 350–354.CrossRefGoogle ScholarPubMed
Vogel, RA, Corretti, MC & Plotnick, GD (2000) The postprandial effect of components of the Mediterranean diet on endothelial function. J Am Coll Cardiol 36, 1455–1460.CrossRefGoogle ScholarPubMed
Weisberg, SP, McCann, D, Desai, M, Rosenbaum, M, Leibel, RL & Ferrante, AW (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112, 1796–1808.CrossRefGoogle ScholarPubMed
Wellen, KE & Hotamisligil, GS (2003) Obesity-induced inflammatory changes in adipose tissue. J Clin Invest 112, 1785–1788.CrossRefGoogle ScholarPubMed
Wever, RM, van Dam, T, van Rijn, HJ, de Groot, F & Rabelink, TJ (1997) Tetrahydrobiopterin regulates superoxide and nitric oxide generation by recombinant endothelial nitric oxide synthase. Biochem Biophys Res Commun 237, 340–344.CrossRefGoogle ScholarPubMed
Williams, MJ, Sutherland, WH, McCormick, MP, de Jong, SA, Walker, RJ & Wilkins, GT (1999) Impaired endothelial function following a meal rich in used cooking fat. J Am Coll Cardiol 33, 1050–1055.CrossRefGoogle Scholar
Wilmink, HW, Stroes, ES, Erkelens, WD, Gerritsen, WB, Wever, R, Banga, JD & Rabelink, TJ (2000) Influence of folic acid on postprandial endothelial dysfunction. Arterioscler Thromb Vasc Biol 20, 185–188.CrossRefGoogle ScholarPubMed
Wilmink, HW, Twickler, MB, Banga, JD, Dallinga-Thie, GM, Eeltink, H, Erkelens, DW, Rabelink, TJ & Stroes, ES (2001) Effect of statin versus fibrate on postprandial endothelial dysfunction: role of remnant-like particles. Cardiovasc Res 50, 577–582.CrossRefGoogle ScholarPubMed
Yaqoob, P, Newsholme, EA & Calder, PC (1999) Production of tumour necrosis factor-α by blood mononuclear cells increases with age and with BMI in healthy women. Proc Nutr Soc 58, 129A.Google Scholar
Zeiher, AM, Krause, T, Schachinger, V, Minners, J & Moser, E (1995) Impaired endothelium-dependent vasodilation of coronary resistance vessels is associated with exercise-induced myocardial ischemia. Circulation 91, 2345–2352.CrossRefGoogle ScholarPubMed
Ziccardi, P, Nappo, F, Giugliano, G, Esposito, K, Marfella, R, Cioffi, M, D'Andrea, F, Molinari, AM & Giugliano, D (2002) Reduction of inflammatory cytokine concentrations and improvement of endothelial functions in obese women after weight loss over one year. Circulation 105, 804–809.CrossRefGoogle ScholarPubMed