Redox State in Atrial Fibrillation Pathogenesis and Relevant Therapeutic Approaches

Author(s): Alexios S. Antonopoulos*, Athina Goliopoulou, Evangelos Oikonomou, Sotiris Tsalamandris, Georgios-Angelos Papamikroulis, George Lazaros, Eleftherios Tsiamis, George Latsios, Stella Brili, Spyridon Papaioannou, Vasiliki Gennimata, Dimitris Tousoulis.

Journal Name: Current Medicinal Chemistry

Volume 26 , Issue 5 , 2019

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Abstract:

Background: Myocardial redox state is a critical determinant of atrial biology, regulating cardiomyocyte apoptosis, ion channel function, and cardiac hypertrophy/fibrosis and function. Nevertheless, it remains unclear whether the targeting of atrial redox state is a rational therapeutic strategy for atrial fibrillation prevention.

Objective: To review the role of atrial redox state and anti-oxidant therapies in atrial fibrillation.

Method: Published literature in Medline was searched for experimental and clinical evidence linking myocardial redox state with atrial fibrillation pathogenesis as well as studies looking into the role of redoxtargeting therapies in the prevention of atrial fibrillation.

Results: Data from animal models have shown that altered myocardial nitroso-redox balance and NADPH oxidases activity are causally involved in the pathogenesis of atrial fibrillation. Similarly experimental animal data supports that increased reactive oxygen / nitrogen species formation in the atrial tissue is associated with altered electrophysiological properties of atrial myocytes and electrical remodeling, favoring atrial fibrillation development. In humans, randomized clinical studies using redox-related therapeutic approaches (e.g. statins or antioxidant agents) have not documented any benefits in the prevention of atrial fibrillation development (mainly post-operative atrial fibrillation risk).

Conclusion: Despite strong experimental and translational data supporting the role of atrial redox state in atrial fibrillation pathogenesis, such mechanistic evidence has not been translated to clinical benefits in atrial fibrillation risk in randomized clinical studies using redox-related therapies.

Keywords: Myocardial redox, oxidative stress, superoxide, NADPH, nitric oxide, atrial fibrillation.

[1]
Bonilla, I.M.; Sridhar, A.; Györke, S.; Cardounel, A.J.; Carnes, C.A. Nitric oxide synthases and atrial fibrillation. Front. Physiol., 2012, 3, 105.
[2]
Reilly, S.N.; Liu, X.; Carnicer, R.; Recalde, A.; Muszkiewicz, A.; Jayaram, R.; Carena, M.C.; Wijesurendra, R.; Stefanini, M.; Surdo, N.C.; Lomas, O.; Ratnatunga, C.; Sayeed, R.; Krasopoulos, G.; Rajakumar, T.; Bueno-Orovio, A.; Verheule, S.; Fulga, T.A.; Rodriguez, B.; Schotten, U.; Casadei, B. Up-regulation of miR-31 in human atrial fibrillation begets the arrhythmia by depleting dystrophin and neuronal nitric oxide synthase. Sci. Transl. Med., 2016, 8(340), 340ra74.
[3]
Simon, J.N.; Ziberna, K.; Casadei, B. Compromised redox homeostasis, altered nitroso-redox balance, and therapeutic possibilities in atrial fibrillation. Cardiovasc. Res., 2016, 109(4), 510-518.
[4]
Antoniades, C.; Antonopoulos, A.S.; Bendall, J.K.; Channon, K.M. Targeting redox signaling in the vascular wall: From basic science to clinical practice. Curr. Pharm. Des., 2009, 15(3), 329-342.
[5]
Antoniades, C.; Demosthenous, M.; Reilly, S.; Margaritis, M.; Zhang, M.H.; Antonopoulos, A.; Marinou, K.; Nahar, K.; Jayaram, R.; Tousoulis, D.; Bakogiannis, C.; Sayeed, R.; Triantafyllou, C.; Koumallos, N.; Psarros, C.; Miliou, A.; Stefanadis, C.; Channon, K.M.; Casadei, B. Myocardial redox state predicts in-hospital clinical outcome after cardiac surgery effects of short-term pre-operative statin treatment. J. Am. Coll. Cardiol., 2012, 59(1), 60-70.
[6]
Antonopoulos, A.S.; Margaritis, M.; Lee, R.; Channon, K.; Antoniades, C. Statins as anti-inflammatory agents in atherogenesis: Molecular mechanisms and lessons from the recent clinical trials. Curr. Pharm. Des., 2012, 18(11), 1519-1530.
[7]
Antonopoulos, A.S.; Margaritis, M.; Shirodaria, C.; Antoniades, C. Translating the effects of statins: from redox regulation to suppression of vascular wall inflammation. Thromb. Haemost., 2012, 108(5), 840-848.
[8]
Jia, N.; Dong, P.; Ye, Y.; Qian, C.; Dai, Q. Allopurinol attenuates oxidative stress and cardiac fibrosis in angiotensin II-induced cardiac diastolic dysfunction. Cardiovasc. Ther., 2012, 30(2), 117-123.
[9]
Saavedra, W.F.; Paolocci, N.; St John, M.E.; Skaf, M.W.; Stewart, G.C.; Xie, J.S.; Harrison, R.W.; Zeichner, J.; Mudrick, D.; Marbán, E.; Kass, D.A.; Hare, J.M. Imbalance between xanthine oxidase and nitric oxide synthase signaling pathways underlies mechanoenergetic uncoupling in the failing heart. Circ. Res., 2002, 90(3), 297-304.
[10]
Takano, H.; Zou, Y.; Hasegawa, H.; Akazawa, H.; Nagai, T.; Komuro, I. Oxidative stress-induced signal transduction pathways in cardiac myocytes: involvement of ROS in heart diseases. Antioxid. Redox Signal., 2003, 5(6), 789-794.
[11]
Antoniades, C.; Shirodaria, C.; Crabtree, M.; Rinze, R.; Alp, N.; Cunnington, C.; Diesch, J.; Tousoulis, D.; Stefanadis, C.; Leeson, P.; Ratnatunga, C.; Pillai, R.; Channon, K.M. Altered plasma versus vascular biopterins in human atherosclerosis reveal relationships between endothelial nitric oxide synthase coupling, endothelial function, and inflammation. Circulation, 2007, 116(24), 2851-2859.
[12]
Antoniades, C.; Shirodaria, C.; Warrick, N.; Cai, S.; de Bono, J.; Lee, J.; Leeson, P.; Neubauer, S.; Ratnatunga, C.; Pillai, R.; Refsum, H.; Channon, K.M. 5-methyltetrahydrofolate rapidly improves endothelial function and decreases superoxide production in human vessels: Effects on vascular tetrahydrobiopterin availability and endothelial nitric oxide synthase coupling. Circulation, 2006, 114(11), 1193-1201.
[13]
Carnicer, R.; Crabtree, M.J.; Sivakumaran, V.; Casadei, B.; Kass, D.A. Nitric oxide synthases in heart failure. Antioxid. Redox Signal., 2013, 18(9), 1078-1099.
[14]
Carnicer, R.; Hale, A.B.; Suffredini, S.; Liu, X.; Reilly, S.; Zhang, M.H.; Surdo, N.C.; Bendall, J.K.; Crabtree, M.J.; Lim, G.B.; Alp, N.J.; Channon, K.M.; Casadei, B. Cardiomyocyte GTP cyclohydrolase 1 and tetrahydrobiopterin increase NOS1 activity and accelerate myocardial relaxation. Circ. Res., 2012, 111(6), 718-727.
[15]
Idigo, W.O.; Reilly, S.; Zhang, M.H.; Zhang, Y.H.; Jayaram, R.; Carnicer, R.; Crabtree, M.J.; Balligand, J.L.; Casadei, B. Regulation of endothelial nitric-oxide synthase (NOS) S-glutathionylation by neuronal NOS: Evidence of a functional interaction between myocardial constitutive NOS isoforms. J. Biol. Chem., 2012, 287(52), 43665-43673.
[16]
Antoniades, C.; Cunnington, C.; Antonopoulos, A.; Neville, M.; Margaritis, M.; Demosthenous, M.; Bendall, J.; Hale, A.; Cerrato, R.; Tousoulis, D.; Bakogiannis, C.; Marinou, K.; Toutouza, M.; Vlachopoulos, C.; Leeson, P.; Stefanadis, C.; Karpe, F.; Channon, K.M. Induction of vascular GTP-cyclohydrolase I and endogenous tetrahydrobiopterin synthesis protect against inflammation-induced endothelial dysfunction in human atherosclerosis. Circulation, 2011, 124(17), 1860-1870.
[17]
Schramm, A.; Matusik, P.; Osmenda, G.; Guzik, T.J. Targeting NADPH oxidases in vascular pharmacology. Vascul. Pharmacol., 2012, 56(5-6), 216-231.
[18]
Kim, Y.M.; Guzik, T.J.; Zhang, Y.H.; Zhang, M.H.; Kattach, H.; Ratnatunga, C.; Pillai, R.; Channon, K.M.; Casadei, B. A myocardial Nox2 containing NAD(P)H oxidase contributes to oxidative stress in human atrial fibrillation. Circ. Res., 2005, 97(7), 629-636.
[19]
Guzik, T.J.; Sadowski, J.; Guzik, B.; Jopek, A.; Kapelak, B.; Przybylowski, P.; Wierzbicki, K.; Korbut, R.; Harrison, D.G.; Channon, K.M. Coronary artery superoxide production and nox isoform expression in human coronary artery disease. Arterioscler. Thromb. Vasc. Biol., 2006, 26(2), 333-339.
[20]
Antoniades, C.; Bakogiannis, C.; Tousoulis, D.; Reilly, S.; Zhang, M.H.; Paschalis, A.; Antonopoulos, A.S.; Demosthenous, M.; Miliou, A.; Psarros, C.; Marinou, K.; Sfyras, N.; Economopoulos, G.; Casadei, B.; Channon, K.M.; Stefanadis, C. Preoperative atorvastatin treatment in CABG patients rapidly improves vein graft redox state by inhibition of Rac1 and NADPH-oxidase activity. Circulation, 2010, 122(11)(Suppl.), S66-S73.
[21]
Antonopoulos, A.S.; Margaritis, M.; Coutinho, P.; Shirodaria, C.; Psarros, C.; Herdman, L.; Sanna, F.; De Silva, R.; Petrou, M.; Sayeed, R.; Krasopoulos, G.; Lee, R.; Digby, J.; Reilly, S.; Bakogiannis, C.; Tousoulis, D.; Kessler, B.; Casadei, B.; Channon, K.M.; Antoniades, C. Adiponectin as a link between type 2 diabetes and vascular NADPH oxidase activity in the human arterial wall: the regulatory role of perivascular adipose tissue. Diabetes, 2015, 64(6), 2207-2219.
[22]
Becker, L.B. vanden Hoek, T.L.; Shao, Z.H.; Li, C.Q.; Schumacker, P.T. Generation of superoxide in cardiomyocytes during ischemia before reperfusion. Am. J. Physiol., 1999, 277(6), H2240-H2246.
[23]
Berry, C.E.; Hare, J.M. Xanthine oxidoreductase and cardiovascular disease: molecular mechanisms and pathophysiological implications. J. Physiol., 2004, 555(Pt 3), 589-606.
[24]
Dieterich, S.; Bieligk, U.; Beulich, K.; Hasenfuss, G.; Prestle, J. Gene expression of antioxidative enzymes in the human heart: increased expression of catalase in the end-stage failing heart. Circulation, 2000, 101(1), 33-39.
[25]
Nojiri, H.; Shimizu, T.; Funakoshi, M.; Yamaguchi, O.; Zhou, H.; Kawakami, S.; Ohta, Y.; Sami, M.; Tachibana, T.; Ishikawa, H.; Kurosawa, H.; Kahn, R.C.; Otsu, K.; Shirasawa, T. Oxidative stress causes heart failure with impaired mitochondrial respiration. J. Biol. Chem., 2006, 281(44), 33789-33801.
[26]
Zelko, I.N.; Mariani, T.J.; Folz, R.J. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic. Biol. Med., 2002, 33(3), 337-349.
[27]
Brigelius-Flohé, R.; Maurer, S.; Lötzer, K.; Böl, G.; Kallionpää, H.; Lehtolainen, P.; Viita, H.; Ylä-Herttuala, S. Overexpression of PHGPx inhibits hydroperoxide-induced oxidation, NFkappaB activation and apoptosis and affects oxLDL-mediated proliferation of rabbit aortic smooth muscle cells. Atherosclerosis, 2000, 152(2), 307-316.
[28]
Venardos, K.M.; Perkins, A.; Headrick, J.; Kaye, D.M. Myocardial ischemia-reperfusion injury, antioxidant enzyme systems, and selenium: a review. Curr. Med. Chem., 2007, 14(14), 1539-1549.
[29]
Gao, G.; Dudley, S.C. Jr Redox regulation, NF-kappaB, and atrial fibrillation. Antioxid. Redox Signal., 2009, 11(9), 2265-2277.
[30]
Wann, L.S.; Curtis, A.B.; Ellenbogen, K.A.; Estes, N.A.; Ezekowitz, M.D.; Jackman, W.M.; January, C.T.; Lowe, J.E.; Page, R.L.; Slotwiner, D.J.; Stevenson, W.G.; Tracy, C.M.; Fuster, V.; Rydén, L.E.; Cannom, D.S.; Crijns, H.J.; Curtis, A.B.; Ellenbogen, K.A.; Halperin, J.L.; Le Heuzey, J.; Kay, G.N.; Lowe, J.E.; Olsson, S.B.; Prystowsky, E.N.; Tamargo, J.L.; Wann, L.S. Management of patients with atrial fibrillation (compilation of 2006 ACCF/AHA/ESC and 2011 ACCF/AHA/HRS recommendations): A report of the American College of Cardiology/American Heart Association Task Force on practice guidelines. Circulation, 2013, 127(18), 1916-1926.
[31]
Dudley, S.C., Jr; Hoch, N.E.; McCann, L.A.; Honeycutt, C.; Diamandopoulos, L.; Fukai, T.; Harrison, D.G.; Dikalov, S.I.; Langberg, J. Atrial fibrillation increases production of superoxide by the left atrium and left atrial appendage: Role of the NADPH and xanthine oxidases. Circulation, 2005, 112(9), 1266-1273.
[32]
Carnes, C.A.; Chung, M.K.; Nakayama, T.; Nakayama, H.; Baliga, R.S.; Piao, S.; Kanderian, A.; Pavia, S.; Hamlin, R.L.; McCarthy, P.M.; Bauer, J.A.; Van Wagoner, D.R. Ascorbate attenuates atrial pacing-induced peroxynitrite formation and electrical remodeling and decreases the incidence of postoperative atrial fibrillation. Circ. Res., 2001, 89(6), E32-E38.
[33]
Kim, Y.H.; Lim, D.S.; Lee, J.H.; Shim, W.J.; Ro, Y.M.; Park, G.H.; Becker, K.G.; Cho-Chung, Y.S.; Kim, M.K. Gene expression profiling of oxidative stress on atrial fibrillation in humans. Exp. Mol. Med., 2003, 35(5), 336-349.
[34]
Emelyanova, L.; Ashary, Z.; Cosic, M.; Negmadjanov, U.; Ross, G.; Rizvi, F.; Olet, S.; Kress, D.; Sra, J.; Tajik, A.J.; Holmuhamedov, E.L.; Shi, Y.; Jahangir, A. Selective downregulation of mitochondrial electron transport chain activity and increased oxidative stress in human atrial fibrillation. Am. J. Physiol. Heart Circ. Physiol., 2016, 311(1), H54-H63.
[35]
Reilly, S.N.; Jayaram, R.; Nahar, K.; Antoniades, C.; Verheule, S.; Channon, K.M.; Alp, N.J.; Schotten, U.; Casadei, B. Atrial sources of reactive oxygen species vary with the duration and substrate of atrial fibrillation: Implications for the antiarrhythmic effect of statins. Circulation, 2011, 124(10), 1107-1117.
[36]
Kim, Y.M.; Kattach, H.; Ratnatunga, C.; Pillai, R.; Channon, K.M.; Casadei, B. Association of atrial nicotinamide adenine dinucleotide phosphate oxidase activity with the development of atrial fibrillation after cardiac surgery. J. Am. Coll. Cardiol., 2008, 51(1), 68-74.
[37]
Carnes, C.A.; Janssen, P.M.; Ruehr, M.L.; Nakayama, H.; Nakayama, T.; Haase, H.; Bauer, J.A.; Chung, M.K.; Fearon, I.M.; Gillinov, A.M.; Hamlin, R.L.; Van Wagoner, D.R. Atrial glutathione content, calcium current, and contractility. J. Biol. Chem., 2007, 282(38), 28063-28073.
[38]
Purohit, A.; Rokita, A.G.; Guan, X.; Chen, B.; Koval, O.M.; Voigt, N.; Neef, S.; Sowa, T.; Gao, Z.; Luczak, E.D.; Stefansdottir, H.; Behunin, A.C.; Li, N.; El-Accaoui, R.N.; Yang, B.; Swaminathan, P.D.; Weiss, R.M.; Wehrens, X.H.; Song, L.S.; Dobrev, D.; Maier, L.S.; Anderson, M.E. Oxidized Ca(2+)/calmodulin-dependent protein kinase II triggers atrial fibrillation. Circulation, 2013, 128(16), 1748-1757.
[39]
Xie, W.; Santulli, G.; Reiken, S.R.; Yuan, Q.; Osborne, B.W.; Chen, B.X.; Marks, A.R. Mitochondrial oxidative stress promotes atrial fibrillation. Sci. Rep., 2015, 5, 11427.
[40]
Redpath, C.J.; Bou Khalil, M.; Drozdzal, G.; Radisic, M.; McBride, H.M. Mitochondrial hyperfusion during oxidative stress is coupled to a dysregulation in calcium handling within a C2C12 cell model. PLoS One, 2013, 8(7), e69165.
[41]
Adam, O.; Frost, G.; Custodis, F.; Sussman, M.A.; Schäfers, H.J.; Böhm, M.; Laufs, U. Role of Rac1 GTPase activation in atrial fibrillation. J. Am. Coll. Cardiol., 2007, 50(4), 359-367.
[42]
Adam, O.; Lavall, D.; Theobald, K.; Hohl, M.; Grube, M.; Ameling, S.; Sussman, M.A.; Rosenkranz, S.; Kroemer, H.K.; Schäfers, H.J.; Böhm, M.; Laufs, U. Rac1-induced connective tissue growth factor regulates connexin 43 and N-cadherin expression in atrial fibrillation. J. Am. Coll. Cardiol., 2010, 55(5), 469-480.
[43]
Johar, S.; Cave, A.C.; Narayanapanicker, A.; Grieve, D.J.; Shah, A.M. Aldosterone mediates angiotensin II-induced interstitial cardiac fibrosis via a Nox2-containing NADPH oxidase. FASEB J., 2006, 20(9), 1546-1548.
[44]
Cucoranu, I.; Clempus, R.; Dikalova, A.; Phelan, P.J.; Ariyan, S.; Dikalov, S.; Sorescu, D. NAD(P)H oxidase 4 mediates transforming growth factor-beta1-induced differentiation of cardiac fibroblasts into myofibroblasts. Circ. Res., 2005, 97(9), 900-907.
[45]
Ago, T.; Kuroda, J.; Pain, J.; Fu, C.; Li, H.; Sadoshima, J. Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ. Res., 2010, 106(7), 1253-1264.
[46]
Moens, A.L.; Takimoto, E.; Tocchetti, C.G.; Chakir, K.; Bedja, D.; Cormaci, G.; Ketner, E.A.; Majmudar, M.; Gabrielson, K.; Halushka, M.K.; Mitchell, J.B.; Biswal, S.; Channon, K.M.; Wolin, M.S.; Alp, N.J.; Paolocci, N.; Champion, H.C.; Kass, D.A. Reversal of cardiac hypertrophy and fibrosis from pressure overload by tetrahydrobiopterin: efficacy of recoupling nitric oxide synthase as a therapeutic strategy. Circulation, 2008, 117(20), 2626-2636.
[47]
Sheng, L.; Shen, Q.; Huang, K.; Liu, G.; Zhao, J.; Xu, W.; Liu, Y.; Li, W.; Li, Y. Upregulation of beta3-adrenergic receptors contributes to atrial structural remodeling in rapid pacing induced atrial fi-brillation canines. Cell. Physiol. Biochem., 2012, 30, 372-381.
[48]
Antonopoulos, A.S.; Margaritis, M.; Coutinho, P.; Digby, J.; Patel, R.; Psarros, C.; Ntusi, N.; Karamitsos, T.D.; Lee, R.; De Silva, R.; Petrou, M.; Sayeed, R.; Demosthenous, M.; Bakogiannis, C.; Wordsworth, P.B.; Tousoulis, D.; Neubauer, S.; Channon, K.M.; Antoniades, C. Reciprocal effects of systemic inflammation and brain natriuretic peptide on adiponectin biosynthesis in adipose tissue of patients with ischemic heart disease. Arterioscler. Thromb. Vasc. Biol., 2014, 34(9), 2151-2159.
[49]
Antonopoulos, A.S.; Margaritis, M.; Verheule, S.; Recalde, A.; Sanna, F.; Herdman, L.; Psarros, C.; Nasrallah, H.; Coutinho, P.; Akoumianakis, I.; Brewer, A.C.; Sayeed, R.; Krasopoulos, G.; Petrou, M.; Tarun, A.; Tousoulis, D.; Shah, A.M.; Casadei, B.; Channon, K.M.; Antoniades, C. Mutual regulation of epicardial adipose tissue and myocardial redox state by ppar-gamma/adiponectin signalling. Circ. Res., 2016, 118(5), 842-855.
[50]
Margaritis, M.; Antonopoulos, A.S.; Digby, J.; Lee, R.; Reilly, S.; Coutinho, P.; Shirodaria, C.; Sayeed, R.; Petrou, M.; De Silva, R.; Jalilzadeh, S.; Demosthenous, M.; Bakogiannis, C.; Tousoulis, D.; Stefanadis, C.; Choudhury, R.P.; Casadei, B.; Channon, K.M.; Antoniades, C. Interactions between vascular wall and perivascular adipose tissue reveal novel roles for adiponectin in the regulation of endothelial nitric oxide synthase function in human vessels. Circulation, 2013, 127(22), 2209-2221.
[51]
Blumensatt, M.; Greulich, S.; Herzfeld de Wiza, D.; Mueller, H.; Maxhera, B.; Rabelink, M.J.; Hoeben, R.C.; Akhyari, P.; Al-Hasani, H.; Ruige, J.B.; Ouwens, D.M. Activin A impairs insulin action in cardiomyocytes via up-regulation of miR-143. Cardiovasc. Res., 2013, 100(2), 201-210.
[52]
Burgeiro, A.; Fuhrmann, A.; Cherian, S.; Espinoza, D.; Jarak, I.; Carvalho, R.A.; Loureiro, M.; Patrício, M.; Antunes, M.; Carvalho, E. Glucose uptake and lipid metabolism are impaired in epicardial adipose tissue from heart failure patients with or without diabetes. Am. J. Physiol. Endocrinol. Metab., 2016, 310(7), E550-E564.
[53]
Greulich, S.; de Wiza, D.H.; Preilowski, S.; Ding, Z.; Mueller, H.; Langin, D.; Jaquet, K.; Ouwens, D.M.; Eckel, J. Secretory products of guinea pig epicardial fat induce insulin resistance and impair primary adult rat cardiomyocyte function. J. Cell. Mol. Med., 2011, 15(11), 2399-2410.
[54]
Greulich, S.; Maxhera, B.; Vandenplas, G.; de Wiza, D.H.; Smiris, K.; Mueller, H.; Heinrichs, J.; Blumensatt, M.; Cuvelier, C.; Akhyari, P.; Ruige, J.B.; Ouwens, D.M.; Eckel, J. Secretory products from epicardial adipose tissue of patients with type 2 diabetes mellitus induce cardiomyocyte dysfunction. Circulation, 2012, 126(19), 2324-2334.
[55]
Venteclef, N.; Guglielmi, V.; Balse, E.; Gaborit, B.; Cotillard, A.; Atassi, F.; Amour, J.; Leprince, P.; Dutour, A.; Clément, K.; Hatem, S.N. Human epicardial adipose tissue induces fibrosis of the atrial myocardium through the secretion of adipo-fibrokines. Eur. Heart J., 2015, 36(13), 795-805a.
[56]
Pfister, R.; Michels, G.; Brägelmann, J.; Sharp, S.J.; Luben, R.; Wareham, N.J.; Khaw, K.T. Plasma vitamin C and risk of hospitalisation with diagnosis of atrial fibrillation in men and women in EPIC-Norfolk prospective study. Int. J. Cardiol., 2014, 177(3), 830-835.
[57]
Antonic, M.; Lipovec, R.; Gregorcic, F.; Juric, P.; Kosir, G. Perioperative ascorbic acid supplementation does not reduce the incidence of postoperative atrial fibrillation in on-pump coronary artery bypass graft patients. J. Cardiol., 2017, 69(1), 98-102.
[58]
Bjordahl, P.M.; Helmer, S.D.; Gosnell, D.J.; Wemmer, G.E.; O’Hara, W.W.; Milfeld, D.J. Perioperative supplementation with ascorbic acid does not prevent atrial fibrillation in coronary artery bypass graft patients. Am. J. Surg., 2012, 204(6), 862-867.
[59]
Korantzopoulos, P.; Kolettis, T.M.; Kountouris, E.; Dimitroula, V.; Karanikis, P.; Pappa, E.; Siogas, K.; Goudevenos, J.A. Oral vitamin C administration reduces early recurrence rates after electrical cardioversion of persistent atrial fibrillation and attenuates associated inflammation. Int. J. Cardiol., 2005, 102(2), 321-326.
[60]
Dehghani, M.R.; Majidi, N.; Rahmani, A.; Asgari, B.; Rezaei, Y. Effect of oral vitamin C on atrial fibrillation development after isolated coronary artery bypass grafting surgery: A prospective randomized clinical trial. Cardiol. J., 2014, 21(5), 492-499.
[61]
Papoulidis, P.; Ananiadou, O.; Chalvatzoulis, E.; Ampatzidou, F.; Koutsogiannidis, C.; Karaiskos, T.; Madesis, A.; Drossos, G. The role of ascorbic acid in the prevention of atrial fibrillation after elective on-pump myocardial revascularization surgery: a single-center experience--a pilot study. Interact. Cardiovasc. Thorac. Surg., 2011, 12(2), 121-124.
[62]
Samadikhah, J.; Golzari, S.E.; Sabermarouf, B.; Karimzadeh, I.; Tizro, P.; Mohammad Khanli, H.; Ghabili, K. Efficacy of combination therapy of statin and vitamin c in comparison with statin in the prevention of post-cabg atrial fibrillation. Adv. Pharm. Bull., 2014, 4(1), 97-100.
[63]
Sarzaeem, M.A.S. Nasim. Vitamin c in prevention of atrial fibrillation after coronary artery bypass graft: Double blind randomized clinical trial. Tehran Univ. Med. J., 2014, 71, 787-793.
[64]
Eslami, M.; Badkoubeh, R.S.; Mousavi, M.; Radmehr, H.; Salehi, M.; Tavakoli, N.; Avadi, M.R. Oral ascorbic acid in combination with beta-blockers is more effective than beta-blockers alone in the prevention of atrial fibrillation after coronary artery bypass grafting. Tex. Heart Inst. J., 2007, 34(3), 268-274.
[65]
Stanger, O.; Aigner, I.; Schimetta, W.; Wonisch, W. Antioxidant supplementation attenuates oxidative stress in patients undergoing coronary artery bypass graft surgery. Tohoku J. Exp. Med., 2014, 232(2), 145-154.
[66]
Rodrigo, R.; Korantzopoulos, P.; Cereceda, M.; Asenjo, R.; Zamorano, J.; Villalabeitia, E.; Baeza, C.; Aguayo, R.; Castillo, R.; Carrasco, R.; Gormaz, J.G. A randomized controlled trial to prevent post-operative atrial fibrillation by antioxidant reinforcement. J. Am. Coll. Cardiol., 2013, 62(16), 1457-1465.
[67]
Guo, X.Y.; Yan, X.L.; Chen, Y.W.; Tang, R.B.; Du, X.; Dong, J.Z.; Ma, C.S. Omega-3 fatty acids for postoperative atrial fibrillation: Alone or in combination with antioxidant vitamins? Heart Lung Circ., 2014, 23(8), 743-750.
[68]
Ali-Hassan-Sayegh, S.; Mirhosseini, S.J.; Rezaeisadrabadi, M.; Dehghan, H.R.; Sedaghat-Hamedani, F.; Kayvanpour, E.; Popov, A.F.; Liakopoulos, O.J. Antioxidant supplementations for prevention of atrial fibrillation after cardiac surgery: an updated comprehensive systematic review and meta-analysis of 23 randomized controlled trials. Interact. Cardiovasc. Thorac. Surg., 2014, 18(5), 646-654.
[69]
Baker, W.L.; Coleman, C.I. Meta-analysis of ascorbic acid for prevention of postoperative atrial fibrillation after cardiac surgery. Am. J. Health Syst. Pharm., 2016, 73(24), 2056-2066.
[70]
Sánchez-Quiñones, J.; Marín, F.; Roldán, V.; Lip, G.Y. The impact of statin use on atrial fibrillation. QJM, 2008, 101(11), 845-861.
[71]
Laufs, U.; Kilter, H.; Konkol, C.; Wassmann, S.; Böhm, M.; Nickenig, G. Impact of HMG CoA reductase inhibition on small GTPases in the heart. Cardiovasc. Res., 2002, 53(4), 911-920.
[72]
Vaquero, M.; Caballero, R.; Gómez, R.; Núñez, L.; Tamargo, J.; Delpón, E. Effects of atorvastatin and simvastatin on atrial plateau currents. J. Mol. Cell. Cardiol., 2007, 42(5), 931-945.
[73]
Shiroshita-Takeshita, A.; Brundel, B.J.; Burstein, B.; Leung, T.K.; Mitamura, H.; Ogawa, S.; Nattel, S. Effects of simvastatin on the development of the atrial fibrillation substrate in dogs with congestive heart failure. Cardiovasc. Res., 2007, 74(1), 75-84.
[74]
Shiroshita-Takeshita, A.; Schram, G.; Lavoie, J.; Nattel, S. Effect of simvastatin and antioxidant vitamins on atrial fibrillation promotion by atrial-tachycardia remodeling in dogs. Circulation, 2004, 110(16), 2313-2319.
[75]
Kumagai, K.; Nakashima, H.; Saku, K. The HMG-CoA reductase inhibitor atorvastatin prevents atrial fibrillation by inhibiting inflammation in a canine sterile pericarditis model. Cardiovasc. Res., 2004, 62(1), 105-111.
[76]
Amit, G.; Katz, A.; Bar-On, S.; Gilutz, H.; Wagshal, A.; Ilia, R.; Henkin, Y. Association of statin therapy and the risk of atrial fibrillation in patients with a permanent pacemaker. Clin. Cardiol., 2006, 29(6), 249-252.
[77]
Richter, B.; Derntl, M.; Marx, M.; Lercher, P.; Gössinger, H.D. Therapy with angiotensin-converting enzyme inhibitors, angiotensin II receptor blockers, and statins: no effect on ablation outcome after ablation of atrial fibrillation. Am. Heart J., 2007, 153(1), 113-119.
[78]
Adabag, A.S.; Nelson, D.B.; Bloomfield, H.E. Effects of statin therapy on preventing atrial fibrillation in coronary disease and heart failure. Am. Heart J., 2007, 154(6), 1140-1145.
[79]
García-Fernández, A.; Marín, F.; Mainar, L.; Roldán, V.; Martínez, J.G. Effect of statins on preventing recurrence of atrial fibrillation after electrical cardioversion. Am. J. Cardiol., 2006, 98(9), 1299-1300.
[80]
Tveit, A.; Grundtvig, M.; Gundersen, T.; Vanberg, P.; Semb, A.G.; Holt, E.; Gullestad, L. Analysis of pravastatin to prevent recurrence of atrial fibrillation after electrical cardioversion. Am. J. Cardiol., 2004, 93(6), 780-782.
[81]
Baran, Ç.; Durdu, S.; Dalva, K.; Zaim, Ç.; Dogan, A.; Ocakoglu, G.; Gürman, G.; Arslan, Ö.; Akar, A.R. Effects of preoperative short term use of atorvastatin on endothelial progenitor cells after coronary surgery: a randomized, controlled trial. Stem Cell Rev., 2012, 8(3), 963-971.
[82]
Dehghani, M.R.; Kasianzadeh, M.; Rezaei, Y.; Sepehrvand, N. Atorvastatin reduces the incidence of postoperative atrial fibrillation in statin-naive patients undergoing isolated heart valve surgery: A double-blind, placebo-controlled randomized trial. J. Cardiovasc. Pharmacol. Ther., 2015, 20(5), 465-472.
[83]
Ji, Q.; Mei, Y.; Wang, X.; Sun, Y.; Feng, J.; Cai, J.; Xie, S.; Chi, L. Effect of preoperative atorvastatin therapy on atrial fibrillation following off-pump coronary artery bypass grafting. Circ. J., 2009, 73, 2244-2249.
[84]
Ozaydin, M.; Varol, E.; Aslan, S.M.; Kucuktepe, Z.; Dogan, A.; Ozturk, M.; Altinbas, A. Effect of atorvastatin on the recurrence rates of atrial fibrillation after electrical cardioversion. Am. J. Cardiol., 2006, 97(10), 1490-1493.
[85]
Song, Y.B.; On, Y.K.; Kim, J.H.; Shin, D.H.; Kim, J.S.; Sung, J.; Lee, S.H.; Kim, W.S.; Lee, Y.T. The effects of atorvastatin on the occurrence of postoperative atrial fibrillation after off-pump coronary artery bypass grafting surgery. Am. Heart J., 2008, 156373, e379-e316.
[86]
Sun, Y.; Ji, Q.; Mei, Y.; Wang, X.; Feng, J.; Cai, J.; Chi, L. Role of preoperative atorvastatin administration in protection against postoperative atrial fibrillation following conventional coronary artery bypass grafting. Int. Heart J., 2011, 52(1), 7-11.
[87]
Patti, G.; Chello, M.; Candura, D.; Pasceri, V.; D’Ambrosio, A.; Covino, E.; Di Sciascio, G. Randomized trial of atorvastatin for reduction of postoperative atrial fibrillation in patients undergoing cardiac surgery: Results of the ARMYDA-3 (Atorvastatin for Reduction of MYocardial Dysrhythmia After cardiac surgery) study. Circulation, 2006, 114(14), 1455-1461.
[88]
Dotani, M.I.; Elnicki, D.M.; Jain, A.C.; Gibson, C.M. Effect of preoperative statin therapy and cardiac outcomes after coronary artery bypass grafting. Am. J .Cardiol., 2000, 86, 1128-1130, A6..
[89]
Zheng, Z.; Jayaram, R.; Jiang, L.; Emberson, J.; Zhao, Y.; Li, Q.; Du, J.; Guarguagli, S.; Hill, M.; Chen, Z.; Collins, R.; Casadei, B. Perioperative rosuvastatin in cardiac surgery. N. Engl. J. Med., 2016, 374(18), 1744-1753.
[90]
Barakat, A.F.; Mahmoud, A.N.; Elgendy, I.Y. Atrial fibrillation post coronary artery bypass surgery: is there still a role for perioperative statins after STICS? J. Thorac. Dis., 2016, 8(8), 1880-1882.
[91]
Deftereos, S.; Giannopoulos, G.; Kossyvakis, C.; Efremidis, M.; Panagopoulou, V.; Kaoukis, A.; Raisakis, K.; Bouras, G.; Angelidis, C.; Theodorakis, A.; Driva, M.; Doudoumis, K.; Pyrgakis, V.; Stefanadis, C. Colchicine for prevention of early atrial fibrillation recurrence after pulmonary vein isolation: A randomized controlled study. J. Am. Coll. Cardiol., 2012, 60(18), 1790-1796.
[92]
Imazio, M.; Brucato, A.; Ferrazzi, P.; Rovere, M.E.; Gandino, A.; Cemin, R.; Ferrua, S.; Belli, R.; Maestroni, S.; Simon, C.; Zingarelli, E.; Barosi, A.; Sansone, F.; Patrini, D.; Vitali, E.; Trinchero, R.; Spodick, D.H.; Adler, Y.; Investigators, C. Colchicine reduces postoperative atrial fibrillation: Results of the Colchicine for the Prevention of the Postpericardiotomy Syndrome (COPPS) atrial fibrillation substudy. Circulation, 2011, 124(21), 2290-2295.
[93]
Singhal, R.; Chang, S.L.; Chong, E.; Hsiao, Y.W.; Liu, S.H.; Tsai, Y.N.; Hsu, C.P.; Lin, Y.J.; Lo, L.W.; Ha, T.L.; Chen, Y.C.; Chen, Y.J.; Chiou, C.W.; Chen, S.A. Colchicine suppresses atrial fibrillation in failing heart. Int. J. Cardiol., 2014, 176(3), 651-660.
[94]
Cavolli, R.; Kaya, K.; Aslan, A.; Emiroglu, O.; Erturk, S.; Korkmaz, O.; Oguz, M.; Tasoz, R.; Ozyurda, U. Does sodium nitroprusside decrease the incidence of atrial fibrillation after myocardial revascularization? A pilot study. Circulation, 2008, 118(5), 476-481.
[95]
Nishijima, Y.; Sridhar, A.; Bonilla, I.; Velayutham, M.; Khan, M.; Terentyeva, R.; Li, C.; Kuppusamy, P.; Elton, T.S.; Terentyev, D.; Györke, S.; Zweier, J.L.; Cardounel, A.J.; Carnes, C.A. Tetrahydrobiopterin depletion and NOS2 uncoupling contribute to heart failure-induced alterations in atrial electrophysiology. Cardiovasc. Res., 2011, 91(1), 71-79.
[96]
Sakabe, M.; Fujiki, A.; Sakamoto, T.; Nakatani, Y.; Mizumaki, K.; Inoue, H. Xanthine oxidase inhibition prevents atrial fibrillation in a canine model of atrial pacing-induced left ventricular dysfunction. J. Cardiovasc. Electrophysiol., 2012, 23(10), 1130-1135.
[97]
Qiu, J.; Zhao, J.; Li, J.; Liang, X.; Yang, Y.; Zhang, Z.; Zhang, X.; Fu, H.; Korantzopoulos, P.; Liu, T.; Li, G. NADPH oxidase inhibitor apocynin prevents atrial remodeling in alloxan-induced diabetic rabbits. Int. J. Cardiol., 2016, 221, 812-819.
[98]
Schramm, A.; Matusik, P.; Osmenda, G.; Guzik, T.J. Targeting NADPH oxidases in vascular pharmacology. Vascul. Pharmacol., 2012, 56(5-6), 216-231.
[99]
Ozaydin, M.; Peker, O.; Erdogan, D.; Kapan, S.; Turker, Y.; Varol, E.; Ozguner, F.; Dogan, A.; Ibrisim, E. N-acetylcysteine for the prevention of postoperative atrial fibrillation: a prospective, randomized, placebo-controlled pilot study. Eur. Heart J., 2008, 29(5), 625-631.
[100]
Kazemi, B.; Akbarzadeh, F.; Safaei, N.; Yaghoubi, A.; Shadvar, K.; Ghasemi, K. Prophylactic high-dose oral-N-acetylcysteine does not prevent atrial fibrillation after heart surgery: a prospective double blind placebo-controlled randomized clinical trial. Pacing Clin. Electrophysiol., 2013, 36(10), 1211-1219.
[101]
Ozaydin, M.; Icli, A.; Yucel, H.; Akcay, S.; Peker, O.; Erdogan, D.; Varol, E.; Dogan, A.; Okutan, H. Metoprolol vs. carvedilol or carvedilol plus N-acetyl cysteine on post-operative atrial fibrillation: A randomized, double-blind, placebo-controlled study. Eur. Heart J., 2013, 34(8), 597-604.
[102]
Sandesara, C.M.; Chung, M.K.; Van Wagoner, D.R.; Barringer, T.A.; Allen, K.; Ismail, H.M.; Zimmerman, B.; Olshansky, B. A randomized, placebo-controlled trial of omega-3 fatty acids for inhibition of supraventricular arrhythmias after cardiac surgery: The fish trial. J. Am. Heart Assoc., 2012, 1(3), e000547.
[103]
Heidarsdottir, R.; Arnar, D.O.; Skuladottir, G.V.; Torfason, B.; Edvardsson, V.; Gottskalksson, G.; Palsson, R.; Indridason, O.S. Does treatment with n-3 polyunsaturated fatty acids prevent atrial fibrillation after open heart surgery? Europace, 2010, 12, 356-363.
[104]
Heidt, M.C.; Vician, M.; Stracke, S.K.; Stadlbauer, T.; Grebe, M.T.; Boening, A.; Vogt, P.R.; Erdogan, A. Beneficial effects of intravenously administered N-3 fatty acids for the prevention of atrial fibrillation after coronary artery bypass surgery: A prospective randomized study. Thorac. Cardiovasc. Surg., 2009, 57(5), 276-280.
[105]
Calò, L.; Bianconi, L.; Colivicchi, F.; Lamberti, F.; Loricchio, M.L.; de Ruvo, E.; Meo, A.; Pandozi, C.; Staibano, M.; Santini, M. N-3 Fatty acids for the prevention of atrial fibrillation after coronary artery bypass surgery: a randomized, controlled trial. J. Am. Coll. Cardiol., 2005, 45(10), 1723-1728.
[106]
Sorice, M.; Tritto, F.P.; Sordelli, C.; Gregorio, R.; Piazza, L. N-3 polyunsaturated fatty acids reduces post-operative atrial fibrillation incidence in patients undergoing “on-pump” coronary artery bypass graft surgery. Monaldi Arch. Chest Dis., 2011, 76(2), 93-98.
[107]
Saravanan, P.; Bridgewater, B.; West, A.L.; O’Neill, S.C.; Calder, P.C.; Davidson, N.C. Omega-3 fatty acid supplementation does not reduce risk of atrial fibrillation after coronary artery bypass surgery: A randomized, double-blind, placebo-controlled clinical trial. Circ Arrhythm Electrophysiol, 2010, 3(1), 46-53.
[108]
Mozaffarian, D.; Marchioli, R.; Macchia, A.; Silletta, M.G.; Ferrazzi, P.; Gardner, T.J.; Latini, R.; Libby, P.; Lombardi, F.; O’Gara, P.T.; Page, R.L.; Tavazzi, L.; Tognoni, G.; Investigators, O. Fish oil and postoperative atrial fibrillation: The Omega-3 Fatty Acids for Prevention of Post-operative Atrial Fibrillation (OPERA) randomized trial. JAMA, 2012, 308(19), 2001-2011.
[109]
Farquharson, A.L.; Metcalf, R.G.; Sanders, P.; Stuklis, R.; Edwards, J.R.; Gibson, R.A.; Cleland, L.G.; Sullivan, T.R.; James, M.J.; Young, G.D. Effect of dietary fish oil on atrial fibrillation after cardiac surgery. Am. J. Cardiol., 2011, 108(6), 851-856.
[110]
Rodrigo, R.; Gutiérrez, R.; Fernández, R.; Guzmán, P. Ageing improves the antioxidant response against postoperative atrial fibrillation: A randomized controlled trial. Interact. Cardiovasc. Thorac. Surg., 2012, 15(2), 209-214.


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VOLUME: 26
ISSUE: 5
Year: 2019
Page: [765 - 779]
Pages: 15
DOI: 10.2174/0929867324666170718130408
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