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Review Article

Oxidative stress and atrial fibrillation: an update

, , , &
Pages 1199-1209 | Received 31 Dec 2017, Accepted 11 Jul 2018, Published online: 10 Sep 2018

References

  • Ball J, Carrington MJ, McMurray JJV, et al. Atrial fibrillation: profile and burden of an evolving epidemic in the 21st century. Int J Cardiol. 2013;167:1807–1824.
  • Rahman F, Kwan GF, Benjamin EJ. Global epidemiology of atrial fibrillation. Nat Rev Cardiol. 2014;11:639–654.
  • Staerk L, Sherer JA, Ko D, et al. Atrial fibrillation: epidemiology, pathophysiology, and clinical outcomes. Circ Res. 2017;120:1501–1517.
  • Nattel S, Harada M. Atrial remodeling and atrial fibrillation: recent advances and translational perspectives. J Am Coll Cardiol. 2014;63:2335–2345.
  • Heijman J, Algalarrondo V, Voigt N, et al. The value of basic research insights into atrial fibrillation mechanisms as a guide to therapeutic innovation: a critical analysis. Cardiovasc Res. 2016;109:467–479.
  • Schotten U, Dobrev D, Platonov PG, et al. Current controversies in determining the main mechanisms of atrial fibrillation. J Intern Med. 2016;279:428–438.
  • Nattel S, Dobrev D. Controversies about atrial fibrillation mechanisms: aiming for order in chaos and whether it matters. Circ Res. 2017;120:1396–1398.
  • Korantzopoulos P, Kolettis TM, Galaris D, et al. The role of oxidative stress in the pathogenesis and perpetuation of atrial fibrillation. Int J Cardiol. 2007;115:135–143.
  • Negi S, Sovari AA, Dudley SC. Jr. Atrial fibrillation: the emerging role of inflammation and oxidative stress. Chddt. 2010;10:262–268.
  • Gutierrez A, Van Wagoner DR. Oxidant and Inflammatory Mechanisms and Targeted Therapy in atrial fibrillation: an update. J Cardiovasc Pharmacol. 2015;66:523–529.
  • Wolke C, Bukowska A, Goette A, et al. Redox control of cardiac remodeling in atrial fibrillation. Biochim Biophys Acta. 2015;1850:1555–1565.
  • Liu T, Korantzopoulos P, Li G. Antioxidant therapies for the management of atrial fibrillation. Cardiovasc Diagn Ther. 2012;2:298–307.
  • Sovari AA, Dudley SC. Jr. Reactive oxygen species-targeted therapeutic interventions for atrial fibrillation. Front Physiol. 2012;3:311.
  • Violi F, Pastori D, Pignatelli P, et al. Antioxidants for prevention of atrial fibrillation: a potentially useful future therapeutic approach? A review of the literature and meta-analysis. Europace. 2014;16:1107–1116.
  • Gasparova I, Kubatka P, Opatrilova R, et al. Perspectives and challenges of antioxidant therapy for atrial fibrillation. Naunyn-Schmiedeberg's Arch Pharmacol. 2017;390:1–14.
  • Antonopoulos AS, Goliopoulou A, Oikonomou E, et al. Redox state in atrial fibrillation pathogenesis and relevant therapeutic approaches. Curr Med Chem. 2017. [Epub ahead of print]. doi: 10.2174/0929867324666170718130408
  • Savelieva I, Kakouros N, Kourliouros A, et al. Upstream therapies for management of atrial fibrillation: review of clinical evidence and implications for European Society of Cardiology guidelines. part I: Primary prevention. Europace. 2011;13:308–328.
  • Savelieva I, Kakouros N, Kourliouros A, et al. Upstream therapies for management of atrial fibrillation: review of clinical evidence and implications for European Society of Cardiology guidelines. part II: Secondary prevention. Europace. 2011;13:610–625.
  • Zakeri R, Van Wagoner DR, Calkins H, et al. The burden of proof: the current state of atrial fibrillation prevention and treatment trials. Heart Rhythm. 2017;14:763–782.
  • Van Wagoner DR. Molecular basis of atrial fibrillation: a dream or a reality? J Cardiovasc Electrophysiol. 2003;14:667–669.
  • Van Wagoner DR. Electrophysiological remodeling in human atrial fibrillation. Pacing Clin Electrophysiol. 2003;26:1572–1575.
  • Mihm MJ, Yu F, Carnes CA, et al. Impaired myofibrillar energetics and oxidative injury during human atrial fibrillation. Circulation. 2001;104:174–180.
  • Dhalla NS, Temsah RM. Sarcoplasmic reticulum and cardiac oxidative stress: an emerging target for heart disease. Expert Opin Ther Targets. 2001;5:205–217.
  • Carnes CA, Chung MK, Nakayama T, et al. Ascorbate attenuates atrial pacing-induced peroxynitrite formation and electrical remodeling and decreases the incidence of postoperative atrial fibrillation. Circ Res. 2001;89:E32–E38.
  • Carnes CA, Janssen PML, Ruehr ML, et al. Atrial glutathione content, calcium current, and contractility. J Biol Chem. 2007;282:28063–28073.
  • Corradi D, Callegari S, Manotti L, et al. Persistent lone atrial fibrillation: clinicopathologic study of 19 cases. Heart Rhythm. 2014;11:1250–1258.
  • Elahi MM, Flatman S, Matata BM. Tracing the origins of postoperative atrial fibrillation: the concept of oxidative stress-mediated myocardial injury phenomenon. Eur J Cardiovasc Prev Rehabil. 2008;15:735–741.
  • Zakkar M, Ascione R, James AF, et al. Inflammation, oxidative stress and postoperative atrial fibrillation in cardiac surgery. Pharmacol Ther. 2015;154:13–20.
  • Kim YM, Guzik TJ, Zhang YH, et al. A myocardial Nox2 containing NAD(P)H oxidase contributes to oxidative stress in human atrial fibrillation. Circ Res. 2005;97:629–636.
  • Kim YM, Kattach H, Ratnatunga C, et al. Association of atrial nicotinamide adenine dinucleotide phosphate oxidase activity with the development of atrial fibrillation after cardiac surgery. J Am Coll Cardiol. 2008;51:68–74.
  • Adam O, Lavall D, Theobald K, et al. Rac1-induced connective tissue growth factor regulates connexin 43 and N-cadherin expression in atrial fibrillation. J Am Coll Cardiol. 2010;55:469–480.
  • Antoniades C, Demosthenous M, Reilly S, et al. Myocardial redox state predicts in-hospital clinical outcome after cardiac surgery effects of short-term pre-operative statin treatment. J Am Coll Cardiol. 2012;59:60–70.
  • Zhang J, Youn JY, Kim AY, et al. NOX4-dependent hydrogen peroxide overproduction in human atrial fibrillation and HL-1 atrial cells: relationship to hypertension. Front Physio. 2012;3:140.
  • Cangemi R, Celestini A, Calvieri C, et al. Different behaviour of NOX2 activation in patients with paroxysmal/persistent or permanent atrial fibrillation. Heart. 2012;98:1063–1066.
  • Liu T, Shao Q, Korantzopoulos P, et al. Serum levels of nicotinamide-adenine dinucleotide phosphate oxidase 4 are associated with non-valvular atrial fibrillation. Biomed Rep. 2015;3:864–868.
  • Dudley SC, Hoch NE, McCann LA, et al. Atrial fibrillation increases production of superoxide by the left atrium and left atrial appendage: role of the NADPH and xanthine oxidases. Circulation. 2005;112:1266–1273.
  • Reilly SN, Jayaram R, Nahar K, et al. Atrial sources of reactive oxygen species vary with the duration and substrate of atrial fibrillation: implications for the antiarrhythmic effect of statins. Circulation. 2011;124:1107–1117.
  • Xie W, Santulli G, Reiken SR, et al. Mitochondrial oxidative stress promotes atrial fibrillation. Sci Rep. 2015;5:11427.
  • Bukowska A, Schild L, Keilhoff G, et al. Mitochondrial dysfunction and redox signaling in atrial tachyarrhythmia. Exp Biol Med (Maywood). 2008;233:558–574.
  • Friedrichs K, Baldus S, Klinke A. Fibrosis in atrial fibrillation – role of reactive species and MPO. Front Physiol. 2012;203:214.
  • Rudolph V, Andrié RP, Rudolph TK, et al. Myeloperoxidase acts as a profibrotic mediator of atrial fibrillation. Nat Med. 2010;16:470–474.
  • Anderson EJ, Efird JT, Davies SW, et al. Monoamine oxidase is a major determinant of redox balance in human atrial myocardium and is associated with postoperative atrial fibrillation. J Am Heart Assoc. 2014;3:e000713.
  • Sovari AA. Cellular and molecular mechanisms of arrhythmia by oxidative stress. Cardiol Res Pract. 2016;2016:1.
  • Purohit A, Rokita AG, Guan X, et al. Oxidized Ca(2+)/calmodulin-dependent protein kinase II triggers atrial fibrillation. Circulation. 2013;128:1748–1757.
  • Dzeshka MS, Shahid F, Shantsila A, et al. Hypertension and atrial fibrillation: an intimate association of epidemiology, pathophysiology, and outcomes. Am J Hypertens. 2017;30:733–755.
  • Münzel T, Gori T, Keaney JF, et al. Pathophysiological role of oxidative stress in systolic and diastolic heart failure and its therapeutic implications. Eur Heart J. 2015;36:2555–2564.
  • Karam BS, Chavez-Moreno A, Koh W, et al. Oxidative stress and inflammation as central mediators of atrial fibrillation in obesity and diabetes. Cardiovasc Diabetol. 2017;16:120.
  • Wong CX, Ganesan AN, Selvanayagam JB. Epicardial fat and atrial fibrillation: current evidence, potential mechanisms, clinical implications, and future directions. Eur Heart J. 2017;38:1294–1302.
  • Niemann B, Rohrbach S, Miller MR, et al. Oxidative stress and cardiovascular risk: obesity, diabetes, smoking, and pollution: part 3 of a 3-part series. J Am Coll Cardiol. 2017;70:230–251.
  • Neuman RB, Bloom HL, Shukrullah I, et al. Oxidative stress markers are associated with persistent atrial fibrillation. Clin Chem. 2007;53:1652–1657.
  • Xia W, Qu X, Yu Y, et al. Asymmetric dimethylarginine concentration and early recurrence of atrial fibrillation after electrical cardioversion. Pacing Clin Electrophysiol. 2008;31:1036–1040.
  • Leftheriotis DI, Fountoulaki KT, Flevari PG, et al. The predictive value of inflammatory and oxidative markers following the successful cardioversion of persistent lone atrial fibrillation. Int J Cardiol. 2009;135:361–369.
  • Shimano M, Shibata R, Inden Y, et al. Reactive oxidative metabolites are associated with atrial conduction disturbance in patients with atrial fibrillation. Heart Rhythm. 2009;6:935–940.
  • Li J, Solus J, Chen Q, et al. Role of inflammation and oxidative stress in atrial fibrillation. Heart Rhythm. 2010;7:438–444.
  • Toyama K, Yamabe H, Uemura T, et al. Analysis of oxidative stress expressed by urinary level of 8-hydroxy-2′-deoxyguanosine and biopyrrin in atrial fibrillation: effect of sinus rhythm restoration. Int J Cardiol. 2013;168:80–85.
  • Li S-b, Yang F, Jing L, et al. Myeloperoxidase and risk of recurrence of atrial fibrillation after catheter ablation. J Investig Med. 2013;61:722–727.
  • Negi SI, Greener I, Anand A, et al. A circulating biomarker risk-prediction model correlates with CHADS-2 risk score in chronic atrial fibrillation. IJC Metab Endocr. 2015;6:24–26.
  • Wu JHY, Marchioli R, Silletta MG, et al. Oxidative stress biomarkers and incidence of postoperative atrial fibrillation in the omega-3 fatty acids for prevention of postoperative atrial fibrillation (OPERA) trial. J Am Heart Assoc. 2015;4:e001886.
  • Adamsson Eryd S, Sjögren M, Smith JG, et al. Ceruloplasmin and atrial fibrillation: evidence of causality from a population-based Mendelian randomization study. J Intern Med. 2014;275:164–171.
  • Okada A, Kashima Y, Tomita T, et al. Characterization of cardiac oxidative stress levels in patients with atrial fibrillation. Heart Vessels. 2016;31:80–87.
  • Samman Tahhan A, Sandesara PB, Hayek SS, et al. Association between oxidative stress and atrial fibrillation. Heart Rhythm. 2017;14:1849–1855.
  • Letsas KP, Korantzopoulos P, Filippatos GS, et al. Uric acid elevation in atrial fibrillation. Hellenic J Cardiol. 2010;51:209–213.
  • Liu T, Zhang X, Korantzopoulos P, et al. Uric acid levels and atrial fibrillation in hypertensive patients. Intern Med. 2011;50:799–803.
  • Korantzopoulos P, Letsas KP, Liu T. Xanthine oxidase and uric acid in atrial fibrillation. Front Physio. 2012;243:150.
  • Tamariz L, Hernandez F, Bush A, et al. Association between serum uric acid and atrial fibrillation: a systematic review and meta-analysis. Heart Rhythm. 2014;11:1102–1108.
  • Zhao J, Liu T, Korantzopoulos P, et al. Association between serum uric acid and atrial fibrillation recurrence following catheter ablation: a meta-analysis. Int J Cardiol. 2016;204:103–105.
  • Ndrepepa G, Kastrati A. Gamma-glutamyl transferase and cardiovascular disease. Ann Transl Med. 2016;4:481.
  • Lee DH, Blomhoff R, Jacobs DR. Jr. Is serum gamma glutamyltransferase a marker of oxidative stress? Free Radic Res. 2004;38:535–539.
  • Alonso A, Misialek JR, Amiin MA, et al. Circulating levels of liver enzymes and incidence of atrial fibrillation: the Atherosclerosis Risk in Communities cohort. Heart. 2014;100:1511–1516.
  • Ndrepepa G, Xhepa E, Colleran R, et al. Gamma-glutamyl transferase and atrial fibrillation in patients with coronary artery disease. Clin Chim Acta. 2017;465:17–21.
  • Lee S-R, Choi E-K, Han K-D, et al. Association between γ-glutamyltransferase level and incidence of atrial fibrillation: a nationwide population-based study. Int J Cardiol. 2017;245:149–155.
  • Uçar FM, Ýpek EG, Burak A, et al. Gamma-glutamyl transferase predicts recurrences of atrial fibrillation after catheter ablation. Acta Cardiol. 2016;71: 205–210.
  • Bas HA, Aksoy F, Icli A, et al. The association of plasma oxidative status and inflammation with the development of atrial fibrillation in patients presenting with ST elevation myocardial infarction. Scand J Clin Lab Invest. 2017;77:77–82.
  • Rabus M, Demirbag R, Yildiz A, et al. Association of prolidase activity, oxidative parameters, and presence of atrial fibrillation in patients with mitral stenosis. Arch Med Res. 2008;39:519–524.
  • McDonald C, Fraser J, Shekar K, et al. Low preoperative selenium is associated with post-operative atrial fibrillation in patients having intermediate-risk coronary artery surgery. Eur J Clin Nutr. 2016;70:1138–1143.
  • Ferro D, Franciosa P, Cangemi R, et al. Serum levels of vitamin E are associated with early recurrence of atrial fibrillation after electric cardioversion. Circ Arrhythm Electrophysiol. 2012;5:327–333.
  • Pfister R, Michels G, Brägelmann J, et al. 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;177:830–835.
  • Traber MG, Stevens JF. Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic Biol Med. 2011;51:1000–1013.
  • Korantzopoulos P, Kolettis TM, Kountouris E, et al. Oral vitamin C administration reduces early recurrence rates after electrical cardioversion of persistent atrial fibrillation and attenuates associated inflammation. Int J Cardiol. 2005;102:321–326.
  • Harling L, Rasoli S, Vecht JA, et al. Do antioxidant vitamins have an anti-arrhythmic effect following cardiac surgery? A meta-analysis of randomised controlled trials. Heart. 2011;97:1636–1642.
  • Ali-Hassan-Sayegh S, Mirhosseini SJ, Rezaeisadrabadi M, et al. 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;18:646–654.
  • Hemilä H, Suonsyrjä T. Vitamin C for preventing atrial fibrillation in high risk patients: a systematic review and meta-analysis. BMC Cardiovasc Disord. 2017;17:49.
  • Rodrigo R. Prevention of postoperative atrial fibrillation: novel and safe strategy based on the modulation of the antioxidant system. Front Physiol. 2012;3:93.
  • Rodrigo R, Gutierrez R, Fernandez R, et al. Ageing improves the antioxidant response against postoperative atrial fibrillation: a randomized controlled trial. Interact Cardiovasc Thorac Surg. 2012;15:209–214.
  • Rodrigo R, Korantzopoulos P, Cereceda M, et al. A randomized controlled trial to prevent post-operative atrial fibrillation by antioxidant reinforcement. J Am Coll Cardiol. 2013;62:1457–1465.
  • Guo X-Y, Yan X-L, Chen Y-W, et al. Omega-3 fatty acids for postoperative atrial fibrillation: alone or in combination with antioxidant vitamins?. Heart Lung Circ. 2014;23:743–750.
  • Ozaydin M, Peker O, Erdogan D, et al. N-acetylcysteine for the prevention of postoperative atrial fibrillation: a prospective, randomized, placebo-controlled pilot study. Eur Heart J. 2008;29:625–631.
  • Ozaydin M, Icli A, Yucel H, et al. 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;34:597–604.
  • Ozaydin M, Peker O, Erdogan D, et al. Oxidative status, inflammation, and postoperative atrial fibrillation with metoprolol vs carvedilol or carvedilol plus N-acetyl cysteine treatment. Clin Cardiol. 2014;37:300–306.
  • Fu H, Li G, Liu C, et al. Probucol prevents atrial remodeling by inhibiting oxidative stress and TNF-α/NF-κB/TGF-β signal transduction pathway in alloxan-induced diabetic rabbits. J Cardiovasc Electrophysiol. 2015;26:211–222.
  • Fu H, Li G, Liu C, et al. Probucol prevents atrial ion channel remodeling in an alloxan-induced diabetes rabbit model. Oncotarget. 2016;7:83850–83858.
  • Shao Q, Korantzopoulos P, Fu H, et al. Effects of Probucol on left atrial remodeling in patients with paroxysmal atrial fibrillation. Int J Cardiol. 2016;207:117–119.
  • Sakabe M, Fujiki A, Sakamoto T, et al. Xanthine oxidase inhibition prevents atrial fibrillation in a canine model of atrial pacing-induced left ventricular dysfunction. J Cardiovasc Electrophysiol. 2012;23:1130–1135.
  • Singh JA, Yu S. Allopurinol and the risk of atrial fibrillation in the elderly: a study using Medicare data. Ann Rheum Dis. 2017;76:72–78.
  • Qiu J, Zhao J, Li J, et al. NADPH oxidase inhibitor apocynin prevents atrial remodeling in alloxan-induced diabetic rabbits. Int J Cardiol. 2016;221:812–819.
  • Cavolli R, Kaya K, Aslan A, et al. Does sodium nitroprusside decrease the incidence of atrial fibrillation after myocardial revascularization?: a pilot study. Circulation. 2008;118:476–481.
  • Bolesta S, Aungst TD, Kong F. Effect of sodium nitroprusside on the occurrence of atrial fibrillation after cardiothoracic surgery. Ann Pharmacother. 2012;46:785–792.
  • Youn J-Y, Zhang J, Zhang Y, et al. Oxidative stress in atrial fibrillation: an emerging role of NADPH oxidase. J Mol Cell Cardiol. 2013;62:72–79.
  • Chaugai S, Meng WY, Ali Sepehry A. Effects of RAAS blockers on atrial fibrillation prophylaxis: an updated systematic review and meta-analysis of randomized controlled trials. J Cardiovasc Pharmacol Ther. 2016;21:388–404.
  • Kirchhof P, Benussi S, Kotecha D, et al. 2016 ESC Guidelines for the management of atrial fibrillation developed in collaboration with EACTS. Eur Heart J. 2016;37:2893–2962.
  • Nakashima H, Kumagai K. Reverse-remodeling effects of angiotensin II type 1 receptor blocker in a canine atrial fibrillation model. Circ J. 2007;71:1977–1982.
  • Yamabe H, Kaikita K, Matsumura T, et al. Study on the Effect of irbesartan on atrial fibrillation Recurrence in Kumamoto: atrial Fibrillation Suppression Trial (SILK study). J Cardiol. 2018;71:129–134.
  • Mayyas F, Alzoubi KH, Van Wagoner DR. Impact of aldosterone antagonists on the substrate for atrial fibrillation: aldosterone promotes oxidative stress and atrial structural/electrical remodeling. Int J Cardiol. 2013;168:5135–5142.
  • Liu T, Korantzopoulos P, Shao Q, et al. Mineralocorticoid receptor antagonists and atrial fibrillation: a meta-analysis. Europace. 2016;18:672–678. [doi:10.1093/europace/euv366].
  • Neefs J, van den Berg NWE, Limpens J, et al. Aldosterone pathway blockade to prevent atrial fibrillation: a systematic review and meta-analysis. Int J Cardiol. 2017;231:155–161.
  • Pinho-Gomes AC, Reilly S, Brandes RP, et al. Targeting inflammation and oxidative stress in atrial fibrillation: role of 3-hydroxy-3-methylglutaryl-coenzyme a reductase inhibition with statins. Antioxid Redox Signal. 2014;20:1268–1285.
  • Liu T, Li L, Korantzopoulos P, et al. Statin use and development of atrial fibrillation: a systematic review and meta-analysis of randomized clinical trials and observational studies. Int J Cardiol. 2008;126:160–170.
  • An JH, Shi FW, Liu S, et al. Preoperative statins as modifiers of cardiac and inflammatory outcomes following coronary artery bypass graft surgery: a meta-analysis. Interact Cardiovasc Thorac Surg. 2017;25:958–965.
  • Liu T, Korantzopoulos P, Li L, et al. Preventive effects of rosuvastatin on atrial fibrillation: a meta-analysis of randomized controlled trials. Int J Cardiol. 2013;167:3058–3060.
  • Yan P, Dong P, Li Z, et al. Statin therapy decreased the recurrence frequency of atrial fibrillation after electrical cardioversion: a meta-analysis. Med Sci Monit. 2014;20:2753–2758.
  • Tosti V, Bertozzi B, Fontana L. Health benefits of the mediterranean diet: metabolic and molecular mechanisms. J Gerontol A Biol Sci Med Sci. 2018;73:318–326.
  • Mattioli AV, Miloro C, Pennella S, et al. Adherence to Mediterranean diet and intake of antioxidants influence spontaneous conversion of atrial fibrillation. Nutr Metab Cardiovasc Dis. 2013;23:115–121.
  • Martinez-Gonzalez MA, Toledo E, Aros F, et al. Extravirgin olive oil consumption reduces risk of atrial fibrillation: the PREDIMED (Prevención con Dieta Mediterránea) trial. Circulation. 2014;130:18–26.
  • Cicerale S, Lucas LJ, Keast RS. Antimicrobial, antioxidant and anti-inflammatory phenolic activities in extra virgin olive oil. Curr Opin Biotechnol. 2012;23:129–135.
  • Pastori D, Carnevale R, Bartimoccia S, et al. Does mediterranean diet reduce cardiovascular events and oxidative stress in atrial fibrillation? Antioxid Redox Signal. 2015;23:682–687.
  • Costanzo S, De Curtis A, di Niro V, et al. Postoperative atrial fibrillation and total dietary antioxidant capacity in patients undergoing cardiac surgery: The Polyphemus Observational Study. J Thorac Cardiovasc Surg. 2015;149:1175–1182.e1.
  • Sovari AA, Dudley SC. Antioxidant therapy for atrial fibrillation: lost in translation? Heart. 2012;98:1615–1616.
  • Sovari AA, Bonini MG, Dudley SC. Effective antioxidant therapy for the management of arrhythmia. Expert Rev Cardiovasc Ther. 2011;9:797–800.
  • Tse G, Yan BP, Chan YWF, et al. Reactive oxygen species, endoplasmic reticulum stress and mitochondrial dysfunction: the link with cardiac arrhythmogenesis. Front Physiol. 2016;7:313.

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