The metabolic syndrome, oxidative stress, environment, and cardiovascular disease: the great exploration

Rebecca Hutcheson, Petra Rocic, Rebecca Hutcheson, Petra Rocic

Abstract

The metabolic syndrome affects 30% of the US population with increasing prevalence. In this paper, we explore the relationship between the metabolic syndrome and the incidence and severity of cardiovascular disease in general and coronary artery disease (CAD) in particular. Furthermore, we look at the impact of metabolic syndrome on outcomes of coronary revascularization therapies including CABG, PTCA, and coronary collateral development. We also examine the association between the metabolic syndrome and its individual component pathologies and oxidative stress. Related, we explore the interaction between the main external sources of oxidative stress, cigarette smoke and air pollution, and metabolic syndrome and the effect of this interaction on CAD. We discuss the apparent lack of positive effect of antioxidants on cardiovascular outcomes in large clinical trials with emphasis on some of the limitations of these trials. Finally, we present evidence for successful use of antioxidant properties of pharmacological agents, including metformin, statins, angiotensin II type I receptor blockers (ARBs), and angiotensin II converting enzyme (ACE) inhibitors, for prevention and treatment of the cardiovascular complications of the metabolic syndrome.

References

    1. Grundy SM. Metabolic syndrome pandemic. Arteriosclerosis, Thrombosis, and Vascular Biology. 2008;28(4):629–636.
    1. Wilson PWF, Kannel WB, Silbershatz H, D’Agostino RB. Clustering of metabolic factors and coronary heart disease. Archives of Internal Medicine. 1999;159(10):1104–1109.
    1. Suzuki T, Hirata K, Elkind MSV, et al. Metabolic syndrome, endothelial dysfunction, and risk of cardiovascular events: the Northern Manhattan study (NOMAS) American Heart Journal. 2008;156(2):405–410.
    1. Ford ES, Giles WH, Mokdad AH. Increasing prevalence of the metabolic syndrome among U.S. adults. Diabetes Care. 2004;27(10):2444–2449.
    1. Sookoian S, Pirola CJ. Genetics of the cardiometabolic syndrome: new insights and therapeutic implications. Therapeutic Advances in Cardiovascular Disease. 2007;1(1):37–47.
    1. Alberti KGMM, Zimmet P, Shaw J. Metabolic syndrome—a new world-wide definition. A consensus statement from the International Diabetes Federation. Diabetic Medicine. 2006;23(5):469–480.
    1. Ärnlöv J, Ingelsson E, Sundström J, Lind L. Impact of body mass index and the metabolic syndrome on the risk of cardiovascular disease and death in middle-aged men. Circulation. 2010;121(2):230–236.
    1. Noda H, Iso H, Saito I, Konishi M, Inoue M, Tsugane S. The impact of the metabolic syndrome and its components on the incidence of ischemic heart disease and stroke: the Japan public health center-based study. Hypertension Research. 2009;32(4):289–298.
    1. Lassègue B, Griendling KK. NADPH oxidases: functions and pathologies in the vasculature. Arteriosclerosis, Thrombosis, and Vascular Biology. 2010;30(4):653–661.
    1. Cavalca V, Veglia F, Squellerio I, et al. Glutathione, vitamin E and oxidative stress in coronary artery disease: relevance of age and gender. European Journal of Clinical Investigation. 2009;39(4):267–272.
    1. Azumi H, Inoue N, Ohashi Y, et al. Superoxide generation in directional coronary atherectomy specimens of patients with angina pectoris: important role of NAD(P)H oxidase. Arteriosclerosis, Thrombosis, and Vascular Biology. 2002;22(11):1838–1844.
    1. Folli F, Corradi D, Fanti P, et al. The role of oxidative stress in the pathogenesis of type 2 diabetes mellitus micro-and macrovascular complications: avenues for a mechanistic-based therapeutic approach. Current Diabetes Reviews. 2011;7(5):313–324.
    1. Fortuño A, San José G, Moreno MU, Beloqui O, Díez J, Zalba G. Phagocytic NADPH oxidase overactivity underlies oxidative stress in metabolic syndrome. Diabetes. 2006;55(1):209–215.
    1. Hansel B, Giral P, Nobecourt E, et al. Metabolic syndrome is associated with elevated oxidative stress and dysfunctional dense high-density lipoprotein particles displaying impaired antioxidative activity. Journal of Clinical Endocrinology and Metabolism. 2004;89(10):4963–4971.
    1. Roberts CK, Barnard RJ, Sindhu RK, Jurczak M, Ehdaie A, Vaziri ND. Oxidative stress and dysregulation of NAD(P)H oxidase and antioxidant enzymes in diet-induced metabolic syndrome. Metabolism. 2006;55(7):928–934.
    1. Ford ES, Mokdad AH, Giles WH, Brown DW. The metabolic syndrome and antioxidant concentrations: findings from the Third National Health and Nutrition Examination Survey. Diabetes. 2003;52(9):2346–2352.
    1. Perticone F, Ceravolo R, Candigliota M, et al. Obesity and body fat distribution induce endothelial dysfunction by oxidative stress: protective effect of vitamin C. Diabetes. 2001;50(1):159–165.
    1. Montero D, Walther G, Perez-Martin A, Roche E, Vinet A. Endothelial dysfunction, inflammation, and oxidative stress in obese children and adolescents: markers and effect of lifestyle intervention. Obesity Reviews. 2012;13(5):441–455.
    1. Rector RS, Warner SO, Liu Y, et al. Exercise and diet induced weight loss improves measures of oxidative stress and insulin sensitivity in adults with characteristics of the metabolic syndrome. American Journal of Physiology. 2007;293(2):E500–E506.
    1. Roberts CK, Won D, Pruthi S, et al. Effect of a short-term diet and exercise intervention on oxidative stress, inflammation, MMP-9, and monocyte chemotactic activity in men with metabolic syndrome factors. Journal of Applied Physiology. 2006;100(5):1657–1665.
    1. Furukawa S, Fujita T, Shimabukuro M, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. Journal of Clinical Investigation. 2004;114(12):1752–1761.
    1. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature. 2006;440(7086):944–948.
    1. de Mattia G, Bravi MC, Laurenti O, et al. Endothelial dysfunction and oxidative stress in type 1 and type 2 diabetic patients without clinical macrovascular complications. Diabetes Research and Clinical Practice. 2008;79(2):337–342.
    1. de Oliveira J, Hort MA, Moreira ELG, et al. Positive correlation between elevated plasma cholesterol levels and cognitive impairments in LDL receptor knockout mice: relevance of cortico-cerebral mitochondrial dysfunction and oxidative stress. Neuroscience. 2011;197:99–106.
    1. Marques de Mattos A, Marino LV, Ovidio PP, Jordão AA, Almeida CC, Chiarello PG. Protein oxidative stress and dyslipidemia in dialysis patients. Therapeutic Apheresis and Dialysis. 2012;16(1):68–74.
    1. Zelzer S, Fuchs N, Almer G, et al. High density lipoprotein cholesterol level is a robust predictor of lipid peroxidation irrespective of gender, age, obesity, and inflammatory or metabolic biomarkers. Clinica Chimica Acta. 2011;412(15-16):1345–1349.
    1. Andreadou I, Farmakis D, Prokovas E, et al. Short-term statin administration in hypercholesterolaemic rabbits resistant to postconditioning: effects on infarct size, endothelial nitric oxide synthase, and nitro-oxidative stress. Cardiovascular Research. 2012;94(3):501–509.
    1. Ansari JA, Bhandari U, Pillai KK, Haque SE. Effect of rosuvastatin on obesity-induced cardiac oxidative stress in wistar rats—a preliminary study. Indian Journal of Experimental Biology. 2012;50(3):216–222.
    1. Ward NC, Hodgson JM, Puddey IB, Mori TA, Beilin LJ, Croft KD. Oxidative stress in human hypertension: association with antihypertensive treatment, gender, nutrition, and lifestyle. Free Radical Biology and Medicine. 2004;36(2):226–232.
    1. Redón J, Oliva MR, Tormos C, et al. Antioxidant activities and oxidative stress byproducts in human hypertension. Hypertension. 2003;41(5):1096–1101.
    1. Wang D, Strandgaard S, Iversen J, Wilcox CS. Asymmetric dimethylarginine, oxidative stress, and vascular nitric oxide synthase in essential hypertension. American Journal of Physiology. 2009;296(2):R195–R200.
    1. Abdilla N, Tormo MC, Fabia MJ, Chaves FJ, Saez G, Redon J. Impact of the components of metabolic syndrome on oxidative stress and enzymatic antioxidant activity in essential hypertension. Journal of Human Hypertension. 2007;21(1):68–75.
    1. Chen HJ, Pan WH. Probable blind spot in the international diabetes federation definition of metabolic syndrome. Obesity. 2007;15(5):1096–1100.
    1. Monami M, Marchionni N, Masotti G, Mannucci E. IDF and ATP-III definitions of metabolic syndrome in the prediction of all-cause mortality in type 2 diabetic patients. Diabetes, Obesity and Metabolism. 2007;9(3):350–353.
    1. Sanchez R, Fischer P, Cuniberti L, Masnatta LD, Ramírez AJ. Vascular oxidative stress is associated with insulin resistance in hyper-reninemic nonmodulating essential hypertension. Journal of Hypertension. 2007;25(12):2434–2440.
    1. Cottone S, Mulè G, Nardi E, et al. C-reactive protein and intercellular adhesion molecule-1 are stronger predictors of oxidant stress than blood pressure in established hypertension. Journal of Hypertension. 2007;25(2):423–428.
    1. Somers MJ, Mavromatis K, Galis ZS, Harrison DG. Vascular superoxide production and vasomotor function in hypertension induced by deoxycorticosterone acetate-salt. Circulation. 2000;101(14):1722–1728.
    1. Landmesser U, Cai H, Dikalov S, et al. Role of p47phox in vascular oxidative stress and hypertension caused by angiotensin II. Hypertension. 2002;40(4):511–515.
    1. Heitzer T, Wenzel U, Hink U, et al. Increased NAD(P)H oxidase-mediated superoxide production in renovascular hypertension: evidence for an involvement of protein kinase C. Kidney International. 1999;55(1):252–260.
    1. Rajagopalan S, Kurz S, Münzel T, et al. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation: contribution to alterations of vasomotor tone. Journal of Clinical Investigation. 1996;97(8):1916–1923.
    1. Freedman DS, Dietz WH, Srinivasan SR, Berenson GS. The relation of overweight to cardiovascular risk factors among children and adolescents: the Bogalusa Heart study. Pediatrics. 1999;103(6 I):1175–1182.
    1. Berenson GS, Srinivasan SR, Bao W, Newman WP, Tracy RE, Wattigney WA. Association between multiple cardiovascular risk factors and atherosclerosis in children and young adults. The New England Journal of Medicine. 1998;338(23):1650–1656.
    1. Galili O, Versari D, Sattler KJ, et al. Early experimental obesity is associated with coronary endothelial dysfunction and oxidative stress. American Journal of Physiology. 2007;292(2):H904–H911.
    1. Kelly AS, Steinberger J, Kaiser DR, Olson TP, Bank AJ, Dengel DR. Oxidative stress and adverse adipokine profile characterize the metabolic syndrome in children. Journal of the Cardiometabolic syndrome. 2006;1(4):248–252.
    1. Ghio AJ, Carraway MS, Madden MC. Composition of air pollution particles and oxidative stress in cells, tissues, and living systems. Journal of Toxicology and Environmental Health Part B. 2012;15(1):1–21.
    1. Chuang KJ, Chan CC, Su TC, Lee CT, Tang CS. The effect of urban air pollution on inflammation, oxidative stress, coagulation, and autonomic dysfunction in young adults. American Journal of Respiratory and Critical Care Medicine. 2007;176(4):370–376.
    1. Mills NL, Donaldson K, Hadoke PW, et al. Adverse cardiovascular effects of air pollution. Nature Clinical Practice Cardiovascular Medicine. 2009;6(1):36–44.
    1. Zanobetti A, Franklin M, Koutrakis P, Schwartz J. Fine particulate air pollution and its components in association with cause-specific emergency admissions. Environmental Health. 2009;8(1, article 58)
    1. Tonstad S, Svendsen M. Premature coronary heart disease, cigarette smoking, and the metabolic syndrome. The American Journal of Cardiology. 2005;96(12):1681–1685.
    1. Chen CC, Li TC, Chang PC, et al. Association among cigarette smoking, metabolic syndrome, and its individual components: the metabolic syndrome study in Taiwan. Metabolism. 2008;57(4):544–548.
    1. Nakatani D, Sakata Y, Sato H, et al. Clinical impact of metabolic syndrome and its additive effect with smoking on subsequent cardiac events after acute myocardial infarction. The American Journal of Cardiology. 2007;99(7):885–889.
    1. Zhang J, Jiang S, Watson RR. Antioxidant supplementation prevents oxidation and inflammatory responses induced by sidestream cigarette smoke in old mice. Environmental Health Perspectives. 2001;109(10):1007–1009.
    1. Chen H, Goldberg MS, Viileneuve PJ. A systematic review of the relation between long-term exposure to ambient air pollution and chronic diseases. Reviews on Environmental Health. 2008;23(4):243–297.
    1. Henrotin JB, Zeller M, Lorgis L, Cottin Y, Giroud M, Béjot Y. Evidence of the role of short-term exposure to ozone on ischaemic cerebral and cardiac events: the Dijon Vascular project (DIVA) Heart. 2010;96(24):1990–1996.
    1. Mustafić H, Jabre P, Caussin C, et al. Main air pollutants and myocardial infarction: a systematic review and meta-analysis. The Journal of the American Medical Association. 2012;307(7):713–721.
    1. Brook RD, Rajagopalan S, Pope CA, et al. Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the american heart association. Circulation. 2010;121(21):2331–2378.
    1. Pereira Filho MA, Pereira LAA, Arbex FF, et al. Effect of air pollution on diabetes and cardiovascular diseases in São Paulo, Brazil. Brazilian Journal of Medical and Biological Research. 2008;41(6):526–532.
    1. Bateson TF, Schwartz J. Who is sensitive to the effects of particulate air pollution on mortality? A case-crossover analysis of effect modifiers. Epidemiology. 2004;15(2):143–149.
    1. Park SK, Auchincloss AH, O’Neill MS, et al. Particulate air pollution, metabolic syndrome, and heart rate variability: the multi-ethnic study of atherosclerosis (MESA) Environmental Health Perspectives. 2010;118(10):1406–1411.
    1. Cotrim HP, Carvalho F, Siqueira AC, Lordelo M, Rocha R, de Freitas LAR. Nonalcoholic fatty liver and insulin resistance among petrochemical workers. The Journal of the American Medical Association. 2005;294(13):1618–1620.
    1. Sirit Y, Acero C, Bellorin M, Portillo R. Metabolic syndrome and other factors cardiovascular risk in workers of a plant of vinyl polychloride. Revista de Salud Publica. 2008;10(2):239–249.
    1. Mohan V, Deepa M, Farooq S, Prabhakaran D, Reddy KS. Surveillance for risk factors of cardiovascular disease among an industrial population in Southern India. National Medical Journal of India. 2008;21(1):8–13.
    1. Lang IA, Galloway TS, Scarlett A, et al. Association of Urinary Bisphenol A concentration with medical disorders and laboratory abnormalities in adults. The Journal of the American Medical Association. 2008;300(11):1303–1310.
    1. Sakurai K, Kawazuma M, Adachi T, et al. Bisphenol A affects glucose transport in mouse 3T3-F442A adipocytes. British Journal of Pharmacology. 2004;141(2):209–214.
    1. Prozialeck WC, Edwards JR, Nebert DW, Woods JM, Barchowsky A, Atchison WD. The vascular system as a target of metal toxicity. Toxicological Sciences. 2008;102(2):207–218.
    1. Wang SL, Chiou JM, Chen CJ, et al. Prevalence of non-insulin-dependent diabetes mellitus and related vascular diseases in Southwestern arseniasis-endemic and nonendemic areas in Taiwan. Environmental Health Perspectives. 2003;111(2):155–159.
    1. Rahman M, Tondel M, Ahmad SA, Axelson O. Diabetes mellitus associated with arsenic exposure in Bangladesh. American Journal of Epidemiology. 1998;148(2):198–203.
    1. Afridi HI, Kazi TG, Kazi N, et al. Evaluation of status of toxic metals in biological samples of diabetes mellitus patients. Diabetes Research and Clinical Practice. 2008;80(2):280–288.
    1. Navas-Acien A, Silbergeld EK, Pastor-Barriuso R, Guallar E. Arsenic exposure and prevalence of type 2 diabetes in US adults. The Journal of the American Medical Association. 2008;300(7):814–822.
    1. Paul DS, Harmon AW, Devesa V, Thomas DJ, Stýblo M. Molecular mechanisms of the diabetogenic effects of arsenic inhibition of insulin signaling by arsenite and methylarsonous acid. Environmental Health Perspectives. 2007;115(5):734–742.
    1. Sun Q, Yue P, Deiuliis JA, et al. Ambient air pollution exaggerates adipose inflammation and insulin resistance in a mouse model of diet-induced obesity. Circulation. 2009;119(4):538–546.
    1. Esposito K, Marfella R, Ciotola M, et al. Effect of a Mediterranean-style diet on endothelial dysfunction and markers of vascular inflammation in the metabolic syndrome: a randomized trial. The Journal of the American Medical Association. 2004;292(12):1440–1446.
    1. Cottone S, Mulè G, Nardi E, et al. Relation of C-reactive protein to oxidative stress and to endothelial activation in essential hypertension. American Journal of Hypertension. 2006;19(3):313–318.
    1. Abramson JL, Hooper WC, Jones DP, et al. Association between novel oxidative stress markers and C-reactive protein among adults without clinical coronary heart disease. Atherosclerosis. 2005;178(1):115–121.
    1. Fitó M, Cladellas M, de la Torre R, et al. Antioxidant effect of virgin olive oil in patients with stable coronary heart disease: a randomized, crossover, controlled, clinical trial. Atherosclerosis. 2005;181(1):149–158.
    1. John JH, Ziebland S, Yudkin P, Roe LS, Neil HAW. Effects of fruit and vegetable consumption on plasma antioxidant concentrations and blood pressure: a randomised controlled trial. The Lancet. 2002;359(9322):1969–1974.
    1. Basu A, Sanchez K, Leyva MJ, et al. Green tea supplementation affects body weight, lipids, and lipid peroxidation in obese subjects with metabolic syndrome. Journal of the American College of Nutrition. 2010;29(1):31–40.
    1. Stancliffe RA, Thorpe T, Zemel MB. Dairy attentuates oxidative and inflammatory stress in metabolic syndrome. The American Journal of Clinical Nutrition. 2011;94(2):422–430.
    1. Antonini-Canterin F, la Carrubba S, Gullace G, et al. Association between carotid atherosclerosis and metabolic syndrome: results from the ISMIR study. Angiology. 2010;61(5):443–448.
    1. Kawamoto R, Tomita H, Ohtsuka N, Inoue A, Kamitani A. Metabolic syndrome, diabetes and subclinical atherosclerosis as assessed by carotid intima-media thickness. Journal of Atherosclerosis and Thrombosis. 2007;14(2):78–85.
    1. Iglseder B, Cip P, Malaimare L, Ladurner G, Paulweber B. The metabolic syndrome is a stronger risk factor for early carotid atherosclerosis in women than in men. Stroke. 2005;36(6):1212–1217.
    1. Kip KE, Marroquin OC, Kelley DE, et al. Clinical importance of obesity versus the metabolic syndrome in cardiovascular risk in women: a report from the women’s ischemia syndrome evaluation (WISE) study. Circulation. 2004;109(6):706–713.
    1. Roger VL, Go AS, Lloyd-Jones DM, et al. Heart disease and stroke statistics—2011 update: a report from the American Heart Association. Circulation. 2011;123:e18–e209.
    1. Kim JY, Mun HS, Lee BK, et al. Impact of metabolic syndrome and its individual components on the presence and severity of angiographic coronary artery disease. Yonsei Medical Journal. 2010;51(5):676–682.
    1. Schernthaner G. Cardiovascular mortality and morbidity in type-2 diabetes mellitus. Diabetes Research and Clinical Practice. 1996;31:S3–S13.
    1. Lakka HM, Laaksonen DE, Lakka TA, et al. The metabolic syndrome and total and cardiovascular disease mortality in middle-aged men. The Journal of the American Medical Association. 2002;288(21):2709–2716.
    1. Kotur-Stevuljevic J, Memon L, Stefanovic A, et al. Correlation of oxidative stress parameters and inflammatory markers in coronary artery disease patients. Clinical Biochemistry. 2007;40(3-4):181–187.
    1. Meisinger C, Baumert J, Khuseyinova N, Loewel H, Koenig W. Plasma oxidized low-density lipoprotein, a strong predictor for acute coronary heart disease events in apparently healthy, middle-aged men from the general population. Circulation. 2005;112(5):651–657.
    1. Kajimoto K, Kasai T, Miyauchi K, et al. Metabolic syndrome predicts 10-year mortality in non-diabetic patients following coronary artery bypass surgery. Circulation Journal. 2008;72(9):1481–1486.
    1. Brackbill ML, Sytsma CS, Sykes K. Perioperative outcomes of coronary artery bypass grafting: effects of metabolic syndrome and patient’s sex. American Journal of Critical Care. 2009;18(5):468–473.
    1. Hoffmann R, Stellbrink E, Schröder J, et al. Impact of the metabolic syndrome on angiographic and clinical events after coronary intervention using bare-metal or sirolimus-eluting stents. The American Journal of Cardiology. 2007;100(9):1347–1352.
    1. Yaginuma K, Kasai T, Miyauchi K, Kajimoto K, Amano A, Daida H. Propensity score analysis of 10-year long-term outcome after bypass surgery or plain old balloon angioplasty in patients with metabolic syndrome. International Heart Journal. 2011;52(6):372–376.
    1. Marso SP, Murphy JW, House JA, Safley DM, Harris WS. Metabolic syndrome-mediated inflammation following elective percutaneous coronary intervention. Diabetes and Vascular Disease Research. 2005;2(1):31–36.
    1. Almalla M, Schröder J, Deserno V, et al. Long-term clinical outcome of sirolimus-eluting stent implantation in metabolic syndrome and diabetes. Journal of Invasive Cardiology. 2010;22(7):317–321.
    1. Hu R, Ma CS, Nie SP, et al. Effect of metabolic syndrome on prognosis and clinical characteristics of revascularization in patients with coronary artery disease. Chinese Medical Journal. 2006;119(22):1871–1876.
    1. Onishi T, Shimada K, Sunayama S, et al. Effects of cardiac rehabilitation in patients with metabolic syndrome after coronary artery bypass grafting. Journal of Cardiology. 2009;53(3):381–387.
    1. Sung SH, Wu TC, Huang CH, Lin SJ, Chen JW. Prognostic impact of body mass index in patients undergoing coronary artery bypass surgery. Heart. 2011;97(8):648–654.
    1. Foody JAM, Ferdinand FD, Pearce GL, Lytle BW, Cosgrove DM, Sprecher DL. HDL cholesterol level predicts survival in men after coronary artery bypass graft surgery: 20-year experience from the Cleveland Clinic Foundation. Circulation. 2000;102(19):III-90–III-94.
    1. Yun J, Rocic P, Pung YF, et al. Redox-dependent mechanisms in coronary collateral growth: the “redox window” hypothesis. Antioxidants and Redox Signaling. 2009;11(8):1961–1974.
    1. Yilmaz MB, Caldir V, Guray Y, et al. Relation of coronary collateral vessel development in patients with a totally occluded right coronary artery to the metabolic syndrome. The American Journal of Cardiology. 2006;97(5):636–639.
    1. Sasmaz H, Yilmaz MB. Coronary collaterals in obese patients: impact of metabolic syndrome. Angiology. 2009;60(2):164–168.
    1. Mouquet F, Cuilleret F, Susen S, et al. Metabolic syndrome and collateral vessel formation in patients with documented occluded coronary arteries: association with hyperglycaemia, insulin-resistance, adiponectin and plasminogen activator inhibitor-1. European Heart Journal. 2009;30(7):840–849.
    1. Reed R, Kolz C, Potter B, Rocic P. The mechanistic basis for the disparate effects of angiotensin II on coronary collateral growth. Arteriosclerosis, Thrombosis, and Vascular Biology. 2008;28(1):61–67.
    1. Hattan N, Chilian WM, Park F, Rocic P. Restoration of coronary collateral growth in the zucker obese rat: impact of VEGF and ecSOD. Basic Research in Cardiology. 2007;102(3):217–223.
    1. Weihrauch D, Lohr NL, Mraovic B, et al. Chronic hyperglycemia attenuates coronary collateral development and impairs proliferative properties of myocardial interstitial fluid by production of angiostatin. Circulation. 2004;109(19):2343–2348.
    1. Lassaletta AD, Chu LM, Robich MP, et al. Overfed Ossabaw swine with early stage metabolic syndrome have normal coronary collateral development in response to chronic ischemia. Basic Research in Cardiology. 2012;107(2, article 243)
    1. Mohri M, Tomoike H, Noma M, Inoue T, Hisano K, Nakamura M. Duration of ischemia is vital for collateral development: repeated brief coronary artery occlusion in conscious dogs. Circulation Research. 1989;64(2):287–296.
    1. Yamanishi K, Fujita M, Ohno A, Sasayama S. Importance of myocardial ischemia for recruitment of coronary collateral circulation in dogs. Cardiovascular Research. 1990;24(4):271–277.
    1. Rocic P, Kolz C, Reed R, Potter B, Chilian WM. Optimal reactive oxygen species concentration and p38 MAP kinase are required for coronary collateral growth. American Journal of Physiology. 2007;292(6):H2729–H2736.
    1. Pung YF, Rocic P, Murphy MP, et al. Resolution of mitochondrial oxidative stress rescues coronary collateral growth in zucker obese fatty rats. Arteriosclerosis, Thrombosis, and Vascular Biology. 2012;32(2):325–334.
    1. Reed R, Potter B, Smith E, et al. Redox-sensitive Akt and Src regulate coronary collateral growth in metabolic syndrome. American Journal of Physiology. 2009;296(6):H1811–H1821.
    1. Miller SJ, Coppinger BJ, Zhou X, Unthank JL. Antioxidants reverse age-related collateral growth impairment. Journal of Vascular Research. 2010;47(2):108–114.
    1. Lonn E, Bosch J, Yusuf S, et al. Effects of long-term vitamin E supplementation on cardiovascular events and cancer: a randomized controlled trial. The Journal of the American Medical Association. 2005;293(11):1338–1347.
    1. Knekt P, Ritz J, Pereira MA, et al. Antioxidant vitamins and coronary heart disease risk: a pooled analysis of 9 cohorts. The American Journal of Clinical Nutrition. 2004;80(6):1508–1520.
    1. Halliwell B. The antioxidant paradox. The Lancet. 2000;355(9210):1179–1180.
    1. Meagher EA, Barry OP, Lawson JA, Rokach J, FitzGerald GA. Effects of vitamin E on lipid peroxidation in healthy persons. The Journal of the American Medical Association. 2001;285(9):1178–1182.
    1. Czernichow S, Vergnaud AC, Galan P, et al. Effects of long-term antioxidant supplementation and association of serum antioxidant concentrations with risk of metabolic syndrome in adults. The American Journal of Clinical Nutrition. 2009;90(2):329–335.
    1. Demircan N, Gürel A, Armutcu F, Ünalacak M, Aktunç E, Atmaca H. The evaluation of serum cystatin C, malondialdehyde, and total antioxidant status in patients with metabolic syndrome. Medical Science Monitor. 2008;14(2):CR97–CR101.
    1. Beydoun MA, Shroff MR, Chen X, Beydoun HA, Wang Y, Zonderman AB. Serum antioxidant status is associated with metabolic syndrome among U.S. adults in recent national surveys. Journal of Nutrition. 2011;141(5):903–913.
    1. Cangemi R, Angelico F, Loffredo L, et al. Oxidative stress-mediated arterial dysfunction in patients with metabolic syndrome: effect of ascorbic acid. Free Radical Biology and Medicine. 2007;43(5):853–859.
    1. Basu A, Betts NM, Ortiz J, Simmons B, Wu M, Lyons TJ. Low-energy cranberry juice decreases lipid oxidation and increases plasma antioxidant capacity in women with metabolic syndrome. Nutrition Research. 2011;31(3):190–196.
    1. Upston JM, Terentis AC, Morris K, Keaney JF, Jr., Stocker R. Oxidized lipid accumulates in the presence of α-tocopherol in atherosclerosis. Biochemical Journal. 2002;363(3):753–760.
    1. Seon Hwa Lee, Oe T, Blair IA. Vitamin C-induced decomposition of lipid hydroperoxides to endogenous genotoxins. Science. 2001;292(5524):2083–2086.
    1. Boaz M, Smetana S, Weinstein T, et al. Secondary prevention with antioxidants of cardiovascular disease in endstage renal disease (SPACE): randomised placebo-controlled trial. The Lancet. 2000;356(9237):1213–1218.
    1. Heinecke JW. Oxidized amino acids: culprits in human atherosclerosis and indicators of oxidative stress. Free Radical Biology and Medicine. 2002;32(11):1090–1101.
    1. Hou X, Song J, Li XN, et al. Metformin reduces intracellular reactive oxygen species levels by upregulating expression of the antioxidant thioredoxin via the AMPK-FOXO3 pathway. Biochemical and Biophysical Research Communications. 2010;396(2):199–205.
    1. Bellin C, de Wiza DH, Wiernsperger NF, Rösen P. Generation of reactive oxygen species by endothelial and smooth muscle cells: influence of hyperglycemia and metformin. Hormone and Metabolic Research. 2006;38(11):732–739.
    1. Alhaider AA, Korashy HM, Sayed-Ahmed MM, Mobark M, Kfoury H, Mansour MA. Metformin attenuates streptozotocin-induced diabetic nephropathy in rats through modulation of oxidative stress genes expression. Chemico-Biological Interactions. 2011;192(3):233–242.
    1. Meaney E, Vela A, Samaniego V, et al. Metformin, arterial function, intima-media thickness and nitroxidation in metabolic syndrome: the mefisto study. Clinical and Experimental Pharmacology and Physiology. 2008;35(8):895–903.
    1. Yusuf S. Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The New England Journal of Medicine. 2000;342(3):145–153.
    1. Kovesdy C, Bangalore S, Imai E, Esquivel E. Telmisartan, Ramipril, or both in patients at high risk for vascular events. Commentary from F1000. The New England Journal of Medicine. 2008;358:1547–1559.
    1. Harrison DG, Cai H, Landmesser U, Griendling KK. The Pickering Lecture British Hypertension Society, 10th September 2002: interactions of angiotensin II with NAD(P)H oxidase, oxidant stress and cardiovascular disease. Journal of the Renin-Angiotensin-Aldosterone System. 2003;4(2):51–61.
    1. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circulation Research. 1994;74(6):1141–1148.
    1. Cingolani OH, Pérez NG, Ennis IL, et al. In vivo key role of reactive oxygen species and NHE-1 activation in determining excessive cardiac hypertrophy. Pflügers Archiv European Journal of Physiology. 2011;462(5):733–743.
    1. Khan BV, Sola S, Lauten WB, et al. Quinapril, an ACE inhibitor, reduces markers of oxidative stress in the metabolic syndrome. Diabetes Care. 2004;27(7):1712–1715.
    1. Yoshida J, Yamamoto K, Mano T, et al. AT1 receptor blocker added to ACE inhibitor provides benefits at advanced stage of hypertensive diastolic heart failure. Hypertension. 2004;43(3):686–691.
    1. Henriksen EJ. Improvement of insulin sensitivity by antagonism of the renin-angiotensin system. American Journal of Physiology. 2007;293(3):R974–R980.
    1. Henriksen EJ, Jacob S, Kinnick TR, Teachey MK, Krekler M. Selective angiotensin II receptor antagonism reduces insulin resistance in obese zucker rats. Hypertension. 2001;38(4):884–890.
    1. Oltman CL, Kleinschmidt TL, Davidson EP, Coppey LJ, Lund DD, Yorek MA. Treatment of cardiovascular dysfunction associated with the metabolic syndrome and type 2 diabetes. Vascular Pharmacology. 2008;48(1):47–53.
    1. Al-Thanoon ZA, Mahmood IH. Effects of losartan vs. enalapril on the markers of metabolic syndrome. Oman Medical Journal. 2012;27(1):27–30.
    1. Csibi A, Communi D, Müller N, Bottari SP. Angiotensin II inhibits insulin-stimulated GLUT4 translocation and Akt activation through tyrosine nitration-dependent mechanisms. PLoS ONE. 2010;5(4)e10070
    1. Wei Y, Sowers JR, Nistala R, et al. Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. The Journal of Biological Chemistry. 2006;281(46):35137–35146.

Source: PubMed

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