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Int J Angiol 2014; 23(04): 217-226
DOI: 10.1055/s-0034-1387169
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Oxidative Stress as a Mechanism of Added Sugar-Induced Cardiovascular Disease

Kailash Prasad
1   Department of Physiology, College of Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada
,
Indu Dhar
2   Department of Pharmacology, College of Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada
› Author Affiliations
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Publication History

Publication Date:
19 August 2014 (online)

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Abstract

Added sugars comprising of table sugar, brown sugar, corn syrup, maple syrup, honey, molasses, and other sweeteners in the prepared processed foods and beverages have been implicated in the pathophysiology of cardiovascular diseases. This article deals with the reactive oxygen species (ROS) as a mechanism of sugar-induced cardiovascular diseases. There is an association between the consumption of high levels of serum glucose with cardiovascular diseases. Various sources of sugar-induced generation of ROS, including mitochondria, nicotinamide adenine dinucleotide phosphate-oxidase, advanced glycation end products, insulin, and uric acid have been discussed. The mechanism by which ROS induce the development of atherosclerosis, hypertension, peripheral vascular disease, coronary artery disease, cardiomyopathy, heart failure, and cardiac arrhythmias have been discussed in detail. In conclusion, the data suggest that added sugars induce atherosclerosis, hypertension, peripheral vascular disease, coronary artery disease, cardiomyopathy, heart failure, and cardiac arrhythmias and that these effects of added sugars are mediated through ROS.

Keywords

added sugars - reactive oxygen species - atherosclerosis - hypertension - coronary artery disease - peripheral vascular disease
 

  • References

  • 1 Johnson RK, Appel LJ, Brands M , et al; American Heart Association Nutrition Committee of the Council on Nutrition, Physical Activity, and Metabolism and the Council on Epidemiology and Prevention. Dietary sugars intake and cardiovascular health: a scientific statement from the American Heart Association. Circulation 2009; 120 (11) 1011-1020
    CrossrefPubMedGoogle Scholar
  • 2 Malik VS, Popkin BM, Bray GA, Després JP, Hu FB. Sugar-sweetened beverages, obesity, type 2 diabetes mellitus, and cardiovascular disease risk. Circulation 2010; 121 (11) 1356-1364
    CrossrefPubMedGoogle Scholar
  • 3 de Koning L, Malik VS, Kellogg MD, Rimm EB, Willett WC, Hu FB. Sweetened beverage consumption, incident coronary heart disease, and biomarkers of risk in men. Circulation 2012; 125 (14) 1735-1741 , S1
    CrossrefPubMedGoogle Scholar
  • 4 Benn M, Tyberg-Hensen A, McCarthy MI, Jensen GB, Grande P, Nordestgaard BG. Nonfasting glucose, ischemic heart disease, and myocardial infarction: a Mendelian randomization study. J Am Coll Cardiol 2012; 59 (25) 2356-2365
    CrossrefPubMedGoogle Scholar
  • 5 Sherman WM. Metabolism of sugars and physical performance. Am J Clin Nutr 1995; 62 (1) 228S-241S
    PubMedGoogle Scholar
  • 6 Brown IJ, Stamler J, Van Horn L , et al; International Study of Macro/Micronutrients and Blood Pressure Research Group. Sugar-sweetened beverage, sugar intake of individuals, and their blood pressure: international study of macro/micronutrients and blood pressure. Hypertension 2011; 57 (4) 695-701
    CrossrefPubMedGoogle Scholar
  • 7 Yang Q, Zhang Z, Gregg EW, Flanders WD, Merritt R, Hu FB. Added sugar intake and cardiovascular diseases mortality among US adults. JAMA Intern Med 2014; 174 (4) 516-524
    CrossrefPubMedGoogle Scholar
  • 8 Prasad K. Oxygen free radicals and peripheral vascular disease. In: Chang JB, Olsen ER, Prasad K, Sumpio BE, , eds. Textbook of Angiology. New York, NY: Springer Verlag; 2000: 427-438
    CrossrefGoogle Scholar
  • 9 Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol 2003; 552 (Pt 2) 335-344
    CrossrefPubMedGoogle Scholar
  • 10 Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 2005; 54 (6) 1615-1625
    CrossrefPubMedGoogle Scholar
  • 11 Yu T, Sheu S-S, Robotham JL, Yoon Y. Mitochondrial fission mediates high glucose-induced cell death through elevated production of reactive oxygen species. Cardiovasc Res 2008; 79 (2) 341-351
    CrossrefPubMedGoogle Scholar
  • 12 Shah A, Xia L, Goldberg H, Lee KW, Quaggin SE, Fantus IG. Thioredoxin-interacting protein mediates high glucose-induced reactive oxygen species generation by mitochondria and the NADPH oxidase, Nox4, in mesangial cells. J Biol Chem 2013; 288 (10) 6835-6848
    CrossrefPubMedGoogle Scholar
  • 13 Bonnefont-Rousselot D. Glucose and reactive oxygen species. Curr Opin Clin Nutr Metab Care 2002; 5 (5) 561-568
    CrossrefPubMedGoogle Scholar
  • 14 Balteau M, Tajeddine N, de Meester C , et al. NADPH oxidase activation by hyperglycaemia in cardiomyocytes is independent of glucose metabolism but requires SGLT1. Cardiovasc Res 2011; 92 (2) 237-246
    CrossrefPubMedGoogle Scholar
  • 15 Gupte RS, Floyd BC, Kozicky M , et al. Synergistic activation of glucose-6-phosphate dehydrogenase and NAD(P)H oxidase by Src kinase elevates superoxide in type 2 diabetic, Zucker fa/fa, rat liver. Free Radic Biol Med 2009; 47 (3) 219-228
    CrossrefPubMedGoogle Scholar
  • 16 Zuurbier CJ, Eerbeek O, Goedhart PT , et al. Inhibition of the pentose phosphate pathway decreases ischemia-reperfusion-induced creatine kinase release in the heart. Cardiovasc Res 2004; 62 (1) 145-153
    CrossrefPubMedGoogle Scholar
  • 17 Quagliaro L, Piconi L, Assaloni R, Martinelli L, Motz E, Ceriello A. Intermittent high glucose enhances apoptosis related to oxidative stress in human umbilical vein endothelial cells: the role of protein kinase C and NAD(P)H-oxidase activation. Diabetes 2003; 52 (11) 2795-2804
    CrossrefPubMedGoogle Scholar
  • 18 Inoguchi T, Li P, Umeda F , et al. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C—dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes 2000; 49 (11) 1939-1945
    CrossrefPubMedGoogle Scholar
  • 19 Benerjee Banerjee D, Sharma P. Dual effects of glucose on macrophage NADPH-oxidase activity: a possible link between diabetes and tuberculosis. Oxid Antioxid Med Sci 2012; 1: 91-96
    CrossrefPubMedGoogle Scholar
  • 20 Jansen F, Yang X, Franklin BS , et al. High glucose condition increases NADPH oxidase activity in endothelial microparticles that promote vascular inflammation. Cardiovasc Res 2013; 98 (1) 94-106
    CrossrefPubMedGoogle Scholar
  • 21 Thorpe SR, Baynes JW. Maillard reaction products in tissue proteins: new products and new perspectives. Amino Acids 2003; 25 (3-4) 275-281
    CrossrefPubMedGoogle Scholar
  • 22 Prasad K. Soluble receptor for advanced glycation end products (sRAGE) and cardiovascular disease. Int J Angiol 2006; 15: 57-68
    PubMedGoogle Scholar
  • 23 Bucala R, Cerami A. Advanced glycosylation: chemistry, biology, and implications for diabetes and aging. Adv Pharmacol 1992; 23: 1-34
    PubMedGoogle Scholar
  • 24 Uribarri J, Tuttle KR. Advanced glycation end products and nephrotoxicity of high-protein diets. Clin J Am Soc Nephrol 2006; 1 (6) 1293-1299
    CrossrefPubMedGoogle Scholar
  • 25 Thornalley PJ. Pharmacology of methylglyoxal: formation, modification of proteins and nucleic acids, and enzymatic detoxification—a role in pathogenesis and antiproliferative chemotherapy. Gen Pharmacol 1996; 27 (4) 565-573
    CrossrefPubMedGoogle Scholar
  • 26 Vlassara H, Bucala R, Striker L. Pathogenic effects of advanced glycosylation: biochemical, biologic, and clinical implications for diabetes and aging. Lab Invest 1994; 70 (2) 138-151
    PubMedGoogle Scholar
  • 27 Jana CK, Das N, Sohal RS. Specificity of age-related carbonylation of plasma proteins in the mouse and rat. Arch Biochem Biophys 2002; 397 (2) 433-439
    CrossrefPubMedGoogle Scholar
  • 28 Lorenzi M. The polyol pathway as a mechanism for diabetic retinopathy: attractive, elusive, and resilient. Exp Diabetes Res 2007; 2007: 61038
    PubMedGoogle Scholar
  • 29 Hofmann MA, Drury S, Fu C , et al. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 1999; 97 (7) 889-901
    CrossrefPubMedGoogle Scholar
  • 30 Yan SD, Schmidt AM, Anderson GM , et al. Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem 1994; 269 (13) 9889-9897
    PubMedGoogle Scholar
  • 31 Wautier MP, Chappey O, Corda S, Stern DM, Schmidt AM, Wautier JL. Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab 2001; 280 (5) E685-E694
    PubMedGoogle Scholar
  • 32 Reznikov LL, Waksman J, Azam T , et al. Effect of advanced glycation end products on endotoxin-induced TNF-alpha, IL-1beta and IL-8 in human peripheral blood mononuclear cells. Clin Nephrol 2004; 61 (5) 324-336
    CrossrefPubMedGoogle Scholar
  • 33 Mohammed AM, Syeda K, Hadden T, Kowluru A. Upregulation of phagocyte-like NADPH oxidase by cytokines in pancreatic beta-cells: attenuation of oxidative and nitrosative stress by 2-bromopalmitate. Biochem Pharmacol 2013; 85 (1) 109-114
    CrossrefPubMedGoogle Scholar
  • 34 Braquet P, Hosford D, Braquet M, Bourgain R, Bussolino F. Role of cytokines and platelet-activating factor in microvascular immune injury. Int Arch Allergy Appl Immunol 1989; 88 (1-2) 88-100
    CrossrefPubMedGoogle Scholar
  • 35 Paubert-Braquet M, Lonchampt MO, Koltz P, Guilbaud J. Tumor necrosis factor (TNF) primes human neutrophil neutrophil (PMN) platelet-activating factor (PAF)-induced superoxide generation. Consequences in promoting PMN-mediated endothelial cells (EC) damages. Prostaglandins 1988; 35: 803
    PubMedGoogle Scholar
  • 36 Uribarri J, Cai W, Peppa M, Goodman S, Ferrucci L, Striker G, Vlassara H , et al. Circulating glycotoxins and dietary advanced glycation endproducts: two links to inflammatory response, oxidative stress, and aging. J Gerontol A Biol Sci Med Sci 2007; 62 (4) 427-433
    CrossrefPubMedGoogle Scholar
  • 37 Prasad K. C-reactive protein increases oxygen radical generation by neutrophils. J Cardiovasc Pharmacol Ther 2004; 9 (3) 203-209
    CrossrefPubMedGoogle Scholar
  • 38 Kraegen EW, Chisholm DJ, Young JD, Lazarus L. The gastrointestinal stimulus to insulin release. II. A dual action of secretin. J Clin Invest 1970; 49 (3) 524-529
    CrossrefPubMedGoogle Scholar
  • 39 Elrick H, Stimmler L, Hlad Jr CJ, Arai Y. Plasma insulin response to oral and intravenous glucose administration. J Clin Endocrinol Metab 1964; 24: 1076-1082
    CrossrefPubMedGoogle Scholar
  • 40 Krieger-Brauer HI, Kather H. Human fat cells possess a plasma membrane-bound H2O2-generating system that is activated by insulin via a mechanism bypassing the receptor kinase. J Clin Invest 1992; 89 (3) 1006-1013
    CrossrefPubMedGoogle Scholar
  • 41 Mukherjee SP, Lane RH, Lynn WS. Endogenous hydrogen peroxide and peroxidative metabolism in adipocytes in response to insulin and sulfhydryl reagents. Biochem Pharmacol 1978; 27 (22) 2589-2594
    CrossrefPubMedGoogle Scholar
  • 42 May JM, de Haën C. Insulin-stimulated intracellular hydrogen peroxide production in rat epididymal fat cells. J Biol Chem 1979; 254 (7) 2214-2220
    PubMedGoogle Scholar
  • 43 Goldstein BJ, Mahadev K, Wu X, Zhu L, Motoshima H. Role of insulin-induced reactive oxygen species in the insulin signaling pathway. Antioxid Redox Signal 2005; 7 (7-8) 1021-1031
    CrossrefPubMedGoogle Scholar
  • 44 Espinosa A, Campos C, Díaz-Vegas A , et al. Insulin-dependent H2O2 production is higher in muscle fibers of mice fed with a high-fat diet. Int J Mol Sci 2013; 14 (8) 15740-15754
    CrossrefPubMedGoogle Scholar
  • 45 Stirpe F, Della Corte E, Bonetti E, Abbondanza A, Abbati A, De Stefano F. Fructose-induced hyperuricaemia. Lancet 1970; 2 (7686) 1310-1311
    PubMedGoogle Scholar
  • 46 Stavric B, Johnson WJ, Clayman S, Gadd RE, Chartrand A. Effect of fructose administration on serum urate levels in the uricase inhibited rat. Experientia 1976; 32 (3) 373-374
    CrossrefPubMedGoogle Scholar
  • 47 Muraoka S, Miura T. Inhibition by uric acid of free radicals that damage biological molecules. Pharmacol Toxicol 2003; 93 (6) 284-289
    CrossrefPubMedGoogle Scholar
  • 48 Maples KR, Mason RP. Free radical metabolite of uric acid. J Biol Chem 1988; 263 (4) 1709-1712
    PubMedGoogle Scholar
  • 49 Vásquez-Vivar J, Santos AM, Junqueira VB, Augusto O. Peroxynitrite-mediated formation of free radicals in human plasma: EPR detection of ascorbyl, albumin-thiyl and uric acid-derived free radicals. Biochem J 1996; 314 (Pt 3) 869-876
    CrossrefPubMedGoogle Scholar
  • 50 Bagnati M, Perugini C, Cau C, Bordone R, Albano E, Bellomo G. When and why a water-soluble antioxidant becomes pro-oxidant during copper-induced low-density lipoprotein oxidation: a study using uric acid. Biochem J 1999; 340 (Pt 1) 143-152
    CrossrefPubMedGoogle Scholar
  • 51 Prasad K, Kalra J. Oxygen free radicals and hypercholesterolemic atherosclerosis: effect of vitamin E. Am Heart J 1993; 125 (4) 958-973
    CrossrefPubMedGoogle Scholar
  • 52 Prasad K. Reduction of serum cholesterol and hypercholesterolemic atherosclerosis in rabbits by secoisolariciresinol diglucoside isolated from flaxseed. Circulation 1999; 99 (10) 1355-1362
    CrossrefPubMedGoogle Scholar
  • 53 Prasad K, Kalra J, Lee P. Oxygen free radicals as a mechanism of hypercholesterolemic atherosclerosis: effect of probucol. Int J Angiol 1994; 3: 100-112
    Article in Thieme ConnectPubMedGoogle Scholar
  • 54 Steinberg D. Antioxidants and atherosclerosis. A current assessment. Circulation 1991; 84 (3) 1420-1425
    CrossrefPubMedGoogle Scholar
  • 55 Steinberg D. Antioxidant in the prevention of human atherosclerosis. Summary of the proceedings of a National Heart, Lung, and Blood Institute Workshop:. September 5-6, 1991, Bethesda, Maryland. Circulation 1992; 85 (6) 2337-2344
    CrossrefPubMedGoogle Scholar
  • 56 Prasad K. Pathophysiology of atherosclerosis. In: Chang JB, Olsen ER, Prasad K, Sumpio BE, , eds. Textbook of Angiology. New York, NY: Springer Verlag; 2000: 8-105
    CrossrefGoogle Scholar
  • 57 Martin A, Foxall T, Blumberg JB, Meydani M. Vitamin E inhibits low-density lipoprotein-induced adhesion of monocytes to human aortic endothelial cells in vitro. Arterioscler Thromb Vasc Biol 1997; 17 (3) 429-436
    CrossrefPubMedGoogle Scholar
  • 58 Faruqi R, de la Motte C, DiCorleto PE. Alpha-tocopherol inhibits agonist-induced monocytic cell adhesion to cultured human endothelial cells. J Clin Invest 1994; 94 (2) 592-600
    CrossrefPubMedGoogle Scholar
  • 59 Devaraj S, Li D, Jialal I. The effects of alpha tocopherol supplementation on monocyte function. Decreased lipid oxidation, interleukin 1 β secretion, and monocyte adhesion to endothelium. J Clin Invest 1996; 98 (3) 756-763
    CrossrefPubMedGoogle Scholar
  • 60 Buñag RD, Tomita T, Sasaki S. Chronic sucrose ingestion induces mild hypertension and tachycardia in rats. Hypertension 1983; 5 (2) 218-225
    CrossrefPubMedGoogle Scholar
  • 61 Martinez FJ, Rizza RA, Romero JC. High-fructose feeding elicits insulin resistance, hyperinsulinism, and hypertension in normal mongrel dogs. Hypertension 1994; 23 (4) 456-463
    CrossrefPubMedGoogle Scholar
  • 62 Tran LT, Yuen VG, McNeill JH. The fructose-fed rat: a review on the mechanisms of fructose-induced insulin resistance and hypertension. Mol Cell Biochem 2009; 332 (1-2) 145-159
    CrossrefPubMedGoogle Scholar
  • 63 Dhar I, Dhar A, Wu L, Desai KM. Increased methylglyoxal formation with upregulation of renin angiotensin system in fructose fed Sprague Dawley rats. PLoS ONE 2013; 8 (9) e74212
    CrossrefPubMedGoogle Scholar
  • 64 Preuss HG, Knapka JJ. Sugar-induced hypertension in Fischer 344 and F1-hybrid rats (F344BN) at different ages. Geriatr Nephrol Urol 1994; 4 (1) 15-21
    CrossrefPubMedGoogle Scholar
  • 65 Brown CM, Dulloo AG, Yepuri G, Montani J-P. Fructose ingestion acutely elevates blood pressure in healthy young humans. Am J Physiol Regul Integr Comp Physiol 2008; 294 (3) R730-R737
    CrossrefPubMedGoogle Scholar
  • 66 Kitiyakara C, Wilcox CS. Antioxidants for hypertension. Curr Opin Nephrol Hypertens 1998; 7 (5) 531-538
    CrossrefPubMedGoogle Scholar
  • 67 Touyz RM, Schiffrin EL. Reactive oxygen species in vascular biology: implications in hypertension. Histochem Cell Biol 2004; 122 (4) 339-352
    CrossrefPubMedGoogle Scholar
  • 68 Welch WJ. Intrarenal oxygen and hypertension. Clin Exp Pharmacol Physiol 2006; 33 (10) 1002-1005
    CrossrefPubMedGoogle Scholar
  • 69 Redón J, Oliva MR, Tormos C , et al. Antioxidant activities and oxidative stress byproducts in human hypertension. Hypertension 2003; 41 (5) 1096-1101
    CrossrefPubMedGoogle Scholar
  • 70 Zalba G, Beaumont FJ, San José G , et al. Vascular NADH/NADPH oxidase is involved in enhanced superoxide production in spontaneously hypertensive rats. Hypertension 2000; 35 (5) 1055-1061
    CrossrefPubMedGoogle Scholar
  • 71 Elmarakby AA, Loomis ED, Pollock JS, Pollock DM. NADPH oxidase inhibition attenuates oxidative stress but not hypertension produced by chronic ET-1. Hypertension 2005; 45 (2) 283-287
    CrossrefPubMedGoogle Scholar
  • 72 Houston MC. Nutraceuticals, vitamins, antioxidants, and minerals in the prevention and treatment of hypertension. Prog Cardiovasc Dis 2005; 47 (6) 396-449
    CrossrefPubMedGoogle Scholar
  • 73 Hong HJ, Hsiao G, Cheng TH, Yen MH. Supplemention with tetrahydrobiopterin suppresses the development of hypertension in spontaneously hypertensive rats. Hypertension 2001; 38 (5) 1044-1048
    CrossrefPubMedGoogle Scholar
  • 74 Lacy F, Kailasam MT, O'Connor DT, Schmid-Schönbein GW, Parmer RJ. Plasma hydrogen peroxide production in human essential hypertension: role of heredity, gender, and ethnicity. Hypertension 2000; 36 (5) 878-884
    CrossrefPubMedGoogle Scholar
  • 75 Sagar S, Kallo IJ, Kaul N, Ganguly NK, Sharma BK. Oxygen free radicals in essential hypertension. Mol Cell Biochem 1992; 111 (1-2) 103-108
    PubMedGoogle Scholar
  • 76 Yasunari K, Maeda K, Nakamura M, Yoshikawa J. Oxidative stress in leukocytes is a possible link between blood pressure, blood glucose, and C-reacting protein. Hypertension 2002; 39 (3) 777-780
    CrossrefPubMedGoogle Scholar
  • 77 Fortuño A, Oliván S, Beloqui O , et al. Association of increased phagocytic NADPH oxidase-dependent superoxide production with diminished nitric oxide generation in essential hypertension. J Hypertens 2004; 22 (11) 2169-2175
    CrossrefPubMedGoogle Scholar
  • 78 Higashi Y, Sasaki S, Nakagawa K, Matsuura H, Oshima T, Chayama K. Endothelial function and oxidative stress in renovascular hypertension. N Engl J Med 2002; 346 (25) 1954-1962
    CrossrefPubMedGoogle Scholar
  • 79 Lip GY, Edmunds E, Nuttall SL, Landray MJ, Blann AD, Beevers DG. Oxidative stress in malignant and non-malignant phase hypertension. J Hum Hypertens 2002; 16 (5) 333-336
    CrossrefPubMedGoogle Scholar
  • 80 Harrison DG, Gongora MC. Oxidative stress and hypertension. Med Clin North Am 2009; 93 (3) 621-635
    CrossrefPubMedGoogle Scholar
  • 81 Vaziri ND. Roles of oxidative stress and antioxidant therapy in chronic kidney disease and hypertension. Curr Opin Nephrol Hypertens 2004; 13 (1) 93-99
    CrossrefPubMedGoogle Scholar
  • 82 Addabbo F, Montagnani M, Goligorsky MS. Mitochondria and reactive oxygen species. Hypertension 2009; 53 (6) 885-892
    CrossrefPubMedGoogle Scholar
  • 83 Bharadwaj LA, Prasad K. Mechanism of superoxide anion-induced modulation of vascular tone. Int J Angiol 2002; 11: 23-29
    Article in Thieme ConnectPubMedGoogle Scholar
  • 84 Bharadwaj LA, Prasad K. Mediation of H2O2-induced vascular relaxation by endothelium-derived relaxing factor. Mol Cell Biochem 1995; 149-150: 267-270
    CrossrefPubMedGoogle Scholar
  • 85 Prasad K, Kalra J, Chan WP, Chaudhary AK. Effect of oxygen free radicals on cardiovascular function at organ and cellular levels. Am Heart J 1989; 117 (6) 1196-1202
    CrossrefPubMedGoogle Scholar
  • 86 Prasad K, Kalra J, Chaudhary AK, Debnath D. Effect of polymorphonuclear leukocyte-derived oxygen free radicals and hypochlorous acid on cardiac function and some biochemical parameters. Am Heart J 1990; 119 (3 Pt 1) 538-550
    CrossrefPubMedGoogle Scholar
  • 87 Hughes AK, Stricklett PK, Padilla E, Kohan DE. Effect of reactive oxygen species on endothelin-1 production by human mesangial cells. Kidney Int 1996; 49 (1) 181-189
    CrossrefPubMedGoogle Scholar
  • 88 Masumoto N, Tasaka K, Miyake A, Tanizawa O. Superoxide anion increases intracellular free calcium in human myometrial cells. J Biol Chem 1990; 265 (36) 22533-22536
    PubMedGoogle Scholar
  • 89 Dreher D, Junod AF. Differential effects of superoxide, hydrogen peroxide, and hydroxyl radical on intracellular calcium in human endothelial cells. J Cell Physiol 1995; 162 (1) 147-153
    CrossrefPubMedGoogle Scholar
  • 90 Sun L, Yau H-Y, Lau O-C, Huang Y, Yao X. Effect of hydrogen peroxide and superoxide anions on cytosolic Ca2+: comparison of endothelail cells from large-sized and small-sized arteries. PLoS ONE 2011; 6 (9) e25432
    CrossrefPubMedGoogle Scholar
  • 91 Volk T, Hensel M, Kox WJ. Transient Ca2+ changes in endothelial cells induced by low doses of reactive oxygen species: role of hydrogen peroxide. Mol Cell Biochem 1997; 171 (1-2) 11-21
    CrossrefPubMedGoogle Scholar
  • 92 Az-ma T, Saeki N, Yuge O. Cytosolic Ca2+ movements of endothelial cells exposed to reactive oxygen intermediates: role of hydroxyl radical-mediated redox alteration of cell-membrane Ca2+ channels. Br J Pharmacol 1999; 126 (6) 1462-1470
    CrossrefPubMedGoogle Scholar
  • 93 Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci U S A 1987; 84 (24) 9265-9269
    CrossrefPubMedGoogle Scholar
  • 94 Kooy NW, Royall JA. Agonist-induced peroxynitrite production from endothelial cells. Arch Biochem Biophys 1994; 310 (2) 352-359
    CrossrefPubMedGoogle Scholar
  • 95 Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A 1990; 87 (4) 1620-1624
    CrossrefPubMedGoogle Scholar
  • 96 Lee DS, McCallum EA, Olson DM. Effects of reactive oxygen species on prostacyclin production in perinatal rat lung cells. J Appl Physiol (1985) 1989; 66 (3) 1321-1327
    PubMedGoogle Scholar
  • 97 Young JB, Landsberg L. Stimulation of the sympathetic nervous system during sucrose feeding. Nature 1977; 269 (5629) 615-617
    CrossrefPubMedGoogle Scholar
  • 98 Kopp W. Chronically increased activity of the sympathetic nervous system: our diet-related “evolutionary” inheritance. J Nutr Health Aging 2009; 13 (1) 27-29
    CrossrefPubMedGoogle Scholar
  • 99 Sarwar N, Gao P, Seshasai SR , et al; Emerging Risk Factors Collaboration. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet 2010; 375 (9733) 2215-2222
    CrossrefPubMedGoogle Scholar
  • 100 Coutinho M, Gerstein HC, Wang Y, Yusuf S. The relationship between glucose and incident cardiovascular events. A metaregression analysis of published data from 20 studies of 95,783 individuals followed for 12.4 years. Diabetes Care 1999; 22 (2) 233-240
    CrossrefPubMedGoogle Scholar
  • 101 Ray KK, Seshasai SR, Wijesuriya S , et al. Effect of intensive control of glucose on cardiovascular outcomes and death in patients with diabetes mellitus: a meta-analysis of randomised controlled trials. Lancet 2009; 373 (9677) 1765-1772
    CrossrefPubMedGoogle Scholar
  • 102 Selvin E, Coresh J, Golden SH, Brancati FL, Folsom AR, Steffes MW. Glycemic control and coronary heart disease risk in persons with and without diabetes: the atherosclerosis risk in communities study. Arch Intern Med 2005; 165 (16) 1910-1916
    CrossrefPubMedGoogle Scholar
  • 103 Liu S, Willett WC, Stampfer MJ , et al. A prospective study of dietary glycemic load, carbohydrate intake, and risk of coronary heart disease in US women. Am J Clin Nutr 2000; 71 (6) 1455-1461
    PubMedGoogle Scholar
  • 104 Yudkin J. Sugar and ischaemic heart disease. Practitioner 1967; 198 (187) 680-683
    PubMedGoogle Scholar
  • 105 Lê KA, Tappy L. Metabolic effects of fructose. Curr Opin Clin Nutr Metab Care 2006; 9 (4) 469-475
    CrossrefPubMedGoogle Scholar
  • 106 Fried SK, Rao SP. Sugars, hypertriglyceridemia, and cardiovascular disease. Am J Clin Nutr 2003; 78 (4) 873S-880S
    PubMedGoogle Scholar
  • 107 Ernst N, Fisher M, Smith W , et al. The association of plasma high-density lipoprotein cholesterol with dietary intake and alcohol consumption. The Lipid Research Clinics Prevalence Study. Circulation 1980; 62 (4 Pt 2) IV41-IV52
    PubMedGoogle Scholar
  • 108 Liu S, Manson JE, Buring JE, Stampfer MJ, Willett WC, Ridker PM. Relation between a diet with a high glycemic load and plasma concentrations of high-sensitivity C-reactive protein in middle-aged women. Am J Clin Nutr 2002; 75 (3) 492-498
    Google Scholar
  • 109 Shanmugam N, Reddy MA, Guha M, Natarajan R. High glucose-induced expression of proinflammatory cytokine and chemokine genes in monocytic cells. Diabetes 2003; 52 (5) 1256-1264
    CrossrefPubMedGoogle Scholar
  • 110 Castelli WP. Cholesterol and lipids in the risk of coronary artery disease—the Framingham Heart Study. Can J Cardiol 1988; 4 (Suppl A ): 5A-10A
    PubMedGoogle Scholar
  • 111 Fuller JH, Shipley MJ, Rose G, Jarrett RJ, Keen H. Mortality from coronary heart disease and stroke in relation to degree of glycaemia: the Whitehall study. Br Med J (Clin Res Ed) 1983; 287 (6396) 867-870
    CrossrefPubMedGoogle Scholar
  • 112 Vogel RA. Coronary risk factors, endothelial function, and atherosclerosis: a review. Clin Cardiol 1997; 20 (5) 426-432
    CrossrefPubMedGoogle Scholar
  • 113 Fielding JE. Smoking: health effects and control (1). N Engl J Med 1985; 313 (8) 491-498
    CrossrefPubMedGoogle Scholar
  • 114 Kannel WB. Role of blood pressure in cardiovascular disease: the Framingham Study. Angiology 1975; 26 (1 Pt. 1) 1-14
    CrossrefPubMedGoogle Scholar
  • 115 Warnholtz A, Nickenig G, Schulz E , et al. Increased NADH-oxidase-mediated superoxide production in the early stages of atherosclerosis: evidence for involvement of the renin-angiotensin system. Circulation 1999; 99 (15) 2027-2033
    CrossrefPubMedGoogle Scholar
  • 116 Stokes KY, Clanton EC, Russell JM, Ross CR, Granger DN. NAD(P)H oxidase-derived superoxide mediates hypercholesterolemia-induced leukocyte-endothelial cell adhesion. Circ Res 2001; 88 (5) 499-505
    CrossrefPubMedGoogle Scholar
  • 117 Liu H-R, Tao L, Gao E , et al. Rosiglitazone inhibits hypercholesterolaemia-induced myeloperoxidase upregulation—a novel mechanism for the cardioprotective effects of PPAR agonists. Cardiovasc Res 2009; 81 (2) 344-352
    PubMedGoogle Scholar
  • 118 Prasad K. Hypocholesterolemic and antiatherosclerotic effect of flax lignan complex isolated from flaxseed. Atherosclerosis 2005; 179 (2) 269-275
    CrossrefPubMedGoogle Scholar
  • 119 Prasad K, Mantha SV, Kalra J, Lee P. Prevention of hypercholesterolemic atherosclerosis by garlic, an antioxidant. J Cardiovasc Pharmacol Ther 1997; 2 (4) 309-320
    CrossrefPubMedGoogle Scholar
  • 120 Khan MA, Baseer A. Increased malondialdehyde levels in coronary heart disease. J Pak Med Assoc 2000; 50 (8) 261-264
    PubMedGoogle Scholar
  • 121 Dubois-Randé JL, Artigou JY, Darmon JY , et al. Oxidative stress in patients with unstable angina. Eur Heart J 1994; 15 (2) 179-183
    CrossrefPubMedGoogle Scholar
  • 122 Kaur K, Bedi G, Kaur M, Vij A, Kaur I. Lipid peroxidation and the levels of antioxidant enzymes in coronary artery disease. Indian J Clin Biochem 2008; 23 (1) 33-37
    CrossrefPubMedGoogle Scholar
  • 123 Vasanji Z, Cantor EJ, Juric D, Moyen M, Netticadan T. Alterations in cardiac contractile performance and sarcoplasmic reticulum function in sucrose-fed rats is associated with insulin resistance. Am J Physiol Cell Physiol 2006; 291 (4) C772-C780
    CrossrefPubMedGoogle Scholar
  • 124 Chang KC, Liang JT, Tseng CD , et al. Aminoguanidine prevents fructose-induced deterioration in left ventricular-arterial coupling in Wistar rats. Br J Pharmacol 2007; 151 (3) 341-346
    PubMedGoogle Scholar
  • 125 Davidoff AJ, Mason MM, Davidson MB , et al. Sucrose-induced cardiomyocyte dysfunction is both preventable and reversible with clinically relevant treatments. Am J Physiol Endocrinol Metab 2004; 286 (5) E718-E724
    CrossrefPubMedGoogle Scholar
  • 126 Dutta K, Podolin DA, Davidson MB, Davidoff AJ. Cardiomyocyte dysfunction in sucrose-fed rats is associated with insulin resistance. Diabetes 2001; 50 (5) 1186-1192
    CrossrefPubMedGoogle Scholar
  • 127 Semeniuk LM, Kryski AJ, Severson DL. Echocardiographic assessment of cardiac function in diabetic db/db and transgenic db/db-hGLUT4 mice. Am J Physiol Heart Circ Physiol 2002; 283 (3) H976-H982
    CrossrefPubMedGoogle Scholar
  • 128 Van den Bergh A, Flameng W, Herijgers P. Type II diabetic mice exhibit contractile dysfunction but maintain cardiac output by favourable loading conditions. Eur J Heart Fail 2006; 8 (8) 777-783
    CrossrefPubMedGoogle Scholar
  • 129 Fonarow GC, Srikanthan P. Diabetic cardiomyopathy. Endocrinol Metab Clin North Am 2006; 35 (3) 575-599 , ix
    CrossrefPubMedGoogle Scholar
  • 130 Ruddy TD, Shumak SL, Liu PP , et al. The relationship of cardiac diastolic dysfunction to concurrent hormonal and metabolic status in type I diabetes mellitus. J Clin Endocrinol Metab 1988; 66 (1) 113-118
    CrossrefPubMedGoogle Scholar
  • 131 Severson DL. Diabetic cardiomyopathy: recent evidence from mouse models of type 1 and type 2 diabetes. Can J Physiol Pharmacol 2004; 82 (10) 813-823
    CrossrefPubMedGoogle Scholar
  • 132 Fein FS, Strobeck JE, Malhotra A, Scheuer J, Sonnenblick EH. Reversibility of diabetic cardiomyopathy with insulin in rats. Circ Res 1981; 49 (6) 1251-1261
    CrossrefPubMedGoogle Scholar
  • 133 Paolisso G, Giugliano D. Oxidative stress and insulin action: is there a relationship?. Diabetologia 1996; 39 (3) 357-363
    CrossrefPubMedGoogle Scholar
  • 134 Armstrong AM, Chestnutt JE, Gormley MJ, Young IS. The effect of dietary treatment on lipid peroxidation and antioxidant status in newly diagnosed noninsulin dependent diabetes. Free Radic Biol Med 1996; 21 (5) 719-726
    CrossrefPubMedGoogle Scholar
  • 135 Sundaram RK, Bhaskar A, Vijayalingam S, Viswanathan M, Mohan R, Shanmugasundaram KR. Antioxidant status and lipid peroxidation in type II diabetes mellitus with and without complications. Clin Sci (Lond) 1996; 90 (4) 255-260
    PubMedGoogle Scholar
  • 136 Ceriello A, Giugliano D, Quatraro A, Dello Russo P, Lefèbvre PJ. Metabolic control may influence the increased superoxide generation in diabetic serum. Diabet Med 1991; 8 (6) 540-542
    CrossrefPubMedGoogle Scholar
  • 137 Prasad K, Mantha SV, Muir AD, Westcott ND. Protective effect of secoisolariciresinol diglucoside against streptozotocin-induced diabetes and its mechanism. Mol Cell Biochem 2000; 206 (1-2) 141-149
    CrossrefPubMedGoogle Scholar
  • 138 Prasad K. Oxidative stress as a mechanism of diabetes in diabetic BB prone rats: effect of secoisolariciresinol diglucoside (SDG). Mol Cell Biochem 2000; 209 (1-2) 89-96
    CrossrefPubMedGoogle Scholar
  • 139 Prasad K. Secoisolariciresinol diglucoside from flaxseed delays the development of type 2 diabetes in Zucker rat. J Lab Clin Med 2001; 138 (1) 32-39
    CrossrefPubMedGoogle Scholar
  • 140 Prasad K, Kalra J, Bharadwaj L. Cardiac depressant effects of oxygen free radicals. Angiology 1993; 44 (4) 257-270
    CrossrefPubMedGoogle Scholar
  • 141 Nichols GA, Reinier K, Chugh SS. Independent contribution of diabetes to increased prevalence and incidence of atrial fibrillation. Diabetes Care 2009; 32 (10) 1851-1856
    CrossrefPubMedGoogle Scholar
  • 142 Johansen OE, Brustad E, Enger S, Tveit A. Prevalence of abnormal glucose metabolism in atrial fibrillation: a case control study in 75-year old subjects. Cardiovasc Diabetol 2008; 7: 28
    CrossrefPubMedGoogle Scholar
  • 143 Movahed MR, Hashemzadeh M, Jamal MM. Diabetes mellitus is a strong, independent risk for atrial fibrillation and flutter in addition to other cardiovascular disease. Int J Cardiol 2005; 105 (3) 315-318
    CrossrefPubMedGoogle Scholar
  • 144 Ostgren CJ, Merlo J, Råstam L, Lindblad U. Atrial fibrillation and its association with type 2 diabetes and hypertension in a Swedish community. Diabetes Obes Metab 2004; 6 (5) 367-374
    CrossrefPubMedGoogle Scholar
  • 145 Dublin S, Glazer NL, Smith NL , et al. Diabetes mellitus, glycemic control, and risk of atrial fibrillation. J Gen Intern Med 2010; 25 (8) 853-858
    CrossrefPubMedGoogle Scholar
  • 146 Campbell AK, Wann KT, Matthews SB. Lactose causes heart arrhythmia in the water flea Daphnia pulex. Comp Biochem Physiol B Biochem Mol Biol 2004; 139 (2) 225-234
    CrossrefPubMedGoogle Scholar
  • 147 Binder G, Bosk A, Gass M, Ranke MB, Heidemann PH. Insulin tolerance test causes hypokalaemia and can provoke cardiac arrhythmias. Horm Res 2004; 62 (2) 84-87
    CrossrefPubMedGoogle Scholar
  • 148 Oikawa S, Nomura H, Nishio M, Nagata R, Hata T. Doxapram hydrochloride aggravates adrenaline-induced arrhythmias accompanied by bidirectional ventricular tachycardia. ISRN Cardiol 2014; 2014: 212045
    PubMedGoogle Scholar
  • 149 Morita N, Sovari AA, Xie Y , et al. Increased susceptibility of aged hearts to ventricular fibrillation during oxidative stress. Am J Physiol Heart Circ Physiol 2009; 297 (5) H1594-H1605
    CrossrefPubMedGoogle Scholar
  • 150 Jeong EM, Liu M, Sturdy M , et al. Metabolic stress, reactive oxygen species, and arrhythmia. J Mol Cell Cardiol 2012; 52 (2) 454-463
    CrossrefPubMedGoogle Scholar
  • 151 Sovari AA, Dudley Jr SC. Reactive oxygen species-targeted therapeutics interventions for atrial fibrillation. Front Physiol 2012; 3: 311
    PubMedGoogle Scholar
  • 152 Bonilla IM, Sridhar A, Györke S, Cardounel AJ, Carnes CA. Nitric oxide synthases and atrial fibrillation. Front Physiol 2012; 3: 105
    PubMedGoogle Scholar
  • 153 Shammas NW. Epidemiology, classification, and modifiable risk factors of peripheral arterial disease. Vasc Health Risk Manag 2007; 3 (2) 229-234
    CrossrefPubMedGoogle Scholar
  • 154 Murabito JM, D'Agostino RB, Silbershatz H, Wilson WF. Intermittent claudication. a risk profile from the Framingham heart study. Circulation 1997; 96 (1) 44-49
    CrossrefPubMedGoogle Scholar
  • 155 Yudkin J, Kakkar VV, Szanto S. Sugar intake, serum insulin and platelet adhesiveness in men with and without peripheral vascular disease. Postgrad Med J 1969; 45 (527) 608-611
    CrossrefPubMedGoogle Scholar