Perspective: A dynamics-based classification of ventricular arrhythmias

Journal of Molecular and Cellular Cardiology

Volumn 82, Issue , 2015, Pages 136-152

  Weiss, James N ^a   Garfinkel, Alan ^a   Karagueuzian, Hrayr S ^a   Nguyen, Thao P ^a   Olcese, Riccardo ^a   Chen, Peng Sheng ^b   Qu, Zhilin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ca signaling; Fibrillation; Nonlinear dynamics; Reentry; Repolarization reserve; Sudden cardiac death

Indexed keywords

CALCIUM CHANNEL; POTASSIUM CHANNEL; ANTIARRHYTHMIC AGENT;

ACTION POTENTIAL DURATION; ARRHYTHMOGENESIS; BRUGADA SYNDROME; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CATECHOLAMINERGIC POLYMORPHIC VENTRICULAR TACHYCARDIA; DISEASE CLASSIFICATION; EXCITATION CONTRACTION COUPLING; HEART ATRIUM FIBRILLATION; HEART FAILURE; HEART MUSCLE FIBROSIS; HEART MUSCLE ISCHEMIA; HEART REPOLARIZATION; HEART SUPRAVENTRICULAR ARRHYTHMIA; HEART VENTRICLE ARRHYTHMIA; HEART VENTRICLE EXTRASYSTOLE; HEART VENTRICLE FIBRILLATION; HEART VENTRICLE TACHYCARDIA; HUMAN; LONG QT SYNDROME; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; REVIEW; SARCOPLASMIC RETICULUM; SHORT QT SYNDROME; TORSADE DES POINTES; ANIMAL; ARRHYTHMIAS, CARDIAC; DRUG DEVELOPMENT; HEART VENTRICLE FUNCTION; PATHOPHYSIOLOGY;

ANIMALS; ANTI-ARRHYTHMIA AGENTS; ARRHYTHMIAS, CARDIAC; DRUG DISCOVERY; HUMANS; VENTRICULAR DYSFUNCTION;

EID: 84925127686     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.02.017     Document Type: Review

References (120)

1. Hoffman B.F., Rosen M.R. Cellular mechanisms for cardiac arrhythmias. Circ Res 1981, 49:1-15.
2. Rosen M.R. Mechanisms for arrhythmias. Am J Cardiol 1988, 61:2A-8A.
3. Jalife J. Ventricular fibrillation: mechanisms of initiation and maintenance. Ann Rev Physiol 2000, 62:25-50.
4. Keating M.T., Sanguinetti M.C. Molecular and cellular mechanisms of cardiac arrhythmias. Cell 2001, 104:569-580.
5. Rubart M., Zipes D.P. Mechanisms of sudden cardiac death. J Clin Invest 2005, 115:2305-2315.
6. Qu Z., Weiss J.N. Mechanisms of ventricular arrhythmias: from molecular fluctuations to electrical turbulence. Ann Rev Physiol 2015, 77. [in press].
7. Echt D.S., Liebson P.R., Mitchell L.B., Peters R.W., Obias-Manno D., Barker A.H., et al. Mortality and morbidity in patients receiving encainide, flecainide, or placebo. The Cardiac Arrhythmia Suppression Trial. N Engl J Med 1991, 324:781-788.
8. Waldo A.L., Camm A.J., deRuyter H., Friedman P.L., MacNeil D.J., Pauls J.F., et al. Effect of d-sotalol on mortality in patients with left ventricular dysfunction after recent and remote myocardial infarction. The SWORD Investigators. Survival With Oral d-Sotalol. Lancet 1996, 348:7-12.
9. Myerburg R.J., Mitrani R., Interian A., Castellanos A. Interpretation of outcomes of antiarrhythmic clinical trials: design features and population impact. Circulation 1998, 97:1514-1521.
10. Bardy G.H., Lee K.L., Mark D.B., Poole J.E., Packer D.L., Boineau R., et al. Amiodarone or an implantable cardioverter-defibrillator for congestive heart failure. N Engl J Med 2005, 352:225-237.
11. Fonarow G.C., Yancy C.W., Hernandez A.F., Peterson E.D., Spertus J.A., Heidenreich P.A. Potential impact of optimal implementation of evidence-based heart failure therapies on mortality. Am Heart J 2011, 161:1024-1030.
12. Qu Z., Hu G., Garfinkel A., Weiss J.N. Nonlinear and stochastic dynamics in the heart. Phys Rep 2014, 543:61-162.
13. Sarkar A.X., Sobie E.A. Regression analysis for constraining free parameters in electrophysiological models of cardiac cells. PLoS Comput Biol 2010, 6:e1000914.
14. Britton O.J., Bueno-Orovio A., Van Ammel K., Lu H.R., Towart R., Gallacher D.J., et al. Experimentally calibrated population of models predicts and explains intersubject variability in cardiac cellular electrophysiology. Proc Natl Acad Sci U S A 2013, 110:E2098-E2105.
15. Sato D., Xie L.H., Sovari A.A., Tran D.X., Morita N., Xie F., et al. Synchronization of chaotic early afterdepolarizations in the genesis of cardiac arrhythmias. Proc Natl Acad Sci U S A 2009, 106:2983-2988.
16. Gyorke S. Molecular basis of catecholaminergic polymorphic ventricular tachycardia. Heart Rhythm 2009, 6:123-129.
17. Mohamed U., Napolitano C., Priori S.G. Molecular and electrophysiological bases of catecholaminergic polymorphic ventricular tachycardia. J Cardiovasc Electrophysiol 2007, 18:791-797.
18. Swaminathan P.D., Purohit A., Hund T.J., Anderson M.E. Calmodulin-dependent protein kinase II: linking heart failure and arrhythmias. Circ Res 2012, 110:1661-1677.
19. Tomaselli G.F., Zipes D.P. What causes sudden death in heart failure?. Circ Res 2004, 95:754-763.
20. Cerrone M., Noujaim S.F., Tolkacheva E.G., Talkachou A., O'Connell R., Berenfeld O., et al. Arrhythmogenic mechanisms in a mouse model of catecholaminergic polymorphic ventricular tachycardia. Circ Res 2007, 101:1039-1048.
21. Katra R.P., Laurita K.R. Cellular mechanism of calcium-mediated triggered activity in the heart. Circ Res 2005, 96:535-542.
22. Xie Y., Sato D., Garfinkel A., Qu Z., Weiss J.N. So little source, so much sink: requirements for afterdepolarizations to propagate in tissue. Biophys J 2010, 99:1408-1415.
23. Fujiwara K., Tanaka H., Mani H., Nakagami T., Takamatsu T. Burst emergence of intracellular Ca waves evokes arrhythmogenic oscillatory depolarization via the Na-Ca exchanger: simultaneous confocal recording of membrane potential and intracellular Ca in the heart. Circ Res 2008, 103:509-518.
24. Wasserstrom J.A., Shiferaw Y., Chen W., Ramakrishna S., Patel H., Kelly J.E., et al. Variability in timing of spontaneous calcium release in the intact rat heart is determined by the time course of sarcoplasmic reticulum calcium load. Circ Res 2010, 107:1117-1126.
25. de Jong S., van Veen T.A.B., van Rijen H.V.M., de Bakker J.M.T. Fibrosis and cardiac arrhythmias. J Cardiovasc Pharmacol 2011, 57:630-810.
26. Nguyen T.P., Qu Z., Weiss J.N. Cardiac fibrosis and arrhythmogenesis: the road to repair is paved with perils. J Mol Cell Cardiol 2014, 70:83-91.
27. Kummer J.L., Nair R., Krishnan S.C. Images in cardiovascular medicine. Bidirectional ventricular tachycardia caused by digitalis toxicity. Circulation 2006, 113:e156-e157.
28. Valent S., Kelly P. Images in clinical medicine. Digoxin-induced bidirectional ventricular tachycardia. N Engl J Med 1997, 336:550.
29. Baher A.A., Uy M., Xie F., Garfinkel A., Qu Z., Weiss J.N. Bidirectional ventricular tachycardia: ping pong in the His-Purkinje system. Heart Rhythm 2011, 8:599-605.
30. de Lange E., Garfinkel A., Weiss J.N., Qu Z. Delayed afterdepolarizations provide the trigger and substrate for reentrant arrhythmias in cardiac tissue: a modeling study. Heart Rhythm 2011, 8:S325.
31. Rosen M.R., Wit A.L., Hoffman B.F. Electrophysiology and pharmacology of cardiac arrhythmias. IV. Cardiac antiarrhythmic and toxic effects of digitalis. Am Heart J 1975, 89:391-399.
32. Weiss J.N., Karma A., Shiferaw Y., Chen P.S., Garfinkel A., Qu Z. From pulsus to pulseless: the saga of cardiac alternans. Circ Res 2006, 98:1244-1253.
33. Qu Z., Garfinkel A., Chen P.S., Weiss J.N. Mechanisms of discordant alternans and induction of reentry in simulated cardiac tissue. Circulation 2000, 102:1664-1670.
34. Watanabe M.A., Fenton F.H., Evans S.J., Hastings H.M., Karma A. Mechanisms for discordant alternans. J Cardiovasc Electrophysiol 2001, 12:196-206.
35. Pastore J.M., Girouard S.D., Laurita K.R., Akar F.G., Rosenbaum D.S. Mechanism linking T-wave alternans to the genesis of cardiac fibrillation. Circulation 1999, 99:1385-1394.
36. Rosenbaum D.S., Jackson L.E., Smith J.M., Garan H., Ruskin J.N., Cohen R.J. Electrical alternans and vulnerability to ventricular arrhythmias. N Engl J Med 1994, 330:235-241.
37. Wilson L.D., Jeyaraj D., Wan X., Hoeker G.S., Said T.H., Gittinger M., et al. Heart failure enhances susceptibility to arrhythmogenic cardiac alternans. Heart Rhythm 2009, 6:251-259.
38. Wasserstrom J.A., Sharma R., Kapur S., Kelly J.E., Kadish A.H., Balke C.W., et al. multiple defects in intracellular calcium cycling in whole failing rat heart. Circulation: heart failure 2009, 2:223-232.
39. Weiss J.N., Nivala M., Garfinkel A., Qu Z. Alternans and arrhythmias: from cell to heart. Circ Res 2011, 108:98-112.
40. Bassani J.W., Yuan W., Bers D.M. Fractional SR Ca release is regulated by trigger Ca and SR Ca content in cardiac myocytes. Am J Physiol 1995, 268:C1313-C1319.
41. Shannon T.R., Ginsburg K.S., Bers D.M. Potentiation of fractional sarcoplasmic reticulum calcium release by total and free intra-sarcoplasmic reticulum calcium concentration. Biophys J 2000, 78:334-343.
42. Diaz M.E., O'Neill S.C., Eisner D.A. Sarcoplasmic reticulum calcium content fluctuation is the key to cardiac alternans. Circ Res 2004, 94:650-656.
43. Picht E., Desantiago J., Blatter L.A., Bers D.M. Cardiac alternans do not rely on diastolic sarcoplasmic reticulum calcium content fluctuations. Circ Res 2006, 99:740-748.
44. Shiferaw Y., Sato D., Karma A. Coupled dynamics of voltage and calcium in paced cardiac cells. Phys Rev E Stat Nonlin Soft Matter Phys 2005, 71:021903.
45. Diaz M.E., Eisner D.A., O'Neill S.C. Depressed ryanodine receptor activity increases variability and duration of the systolic Ca transient in rat ventricular myocytes. Circ Res 2002, 91:585-593.
46. Gaeta S.A., Bub G., Abbott G.W., Christini D.J. Dynamical mechanism for subcellular alternans in cardiac myocytes. Circ Res 2009, 105:335-342.
47. Nolasco J.B., Dahlen R.W. A graphic method for the study of alternation in cardiac action potentials. J Appl Physiol 1968, 25:191-196.
48. Tolkacheva E.G., Schaeffer D.G., Gauthier D.J., Krassowska W. Condition for alternans and stability of the 1:1 response pattern in a "memory" model of paced cardiac dynamics. Phys Rev E Stat Nonlin Soft Matter Phys 2003, 67:031904.
49. Cao J.M., Qu Z., Kim Y.H., Wu T.J., Garfinkel A., Weiss J.N., et al. Spatiotemporal heterogeneity in the induction of ventricular fibrillation by rapid pacing: importance of cardiac restitution properties. Circ Res 1999, 84:1318-1331.
50. Qu Z., Karagueuzian H.S., Garfinkel A., Weiss J.N. Effects of Na channel and cell coupling abnormalities on vulnerability to reentry: a simulation study. Am J Physiol Heart Circ Physiol 2004, 286:H1310-H1321.
51. Qu Z., Xie Y., Garfinkel A., Weiss J.N. T-wave Alternans and arrhythmogenesis in cardiac diseases. Front Physiol 2010, 1.
52. Qu Z., Nivala M., Weiss J.N. Calcium alternans in cardiac myocytes: order from disorder. J Mol Cell Cardiol 2013, 58:100-109.
53. Maruyama M., Joung B., Tang L., Shinohara T., On Y.K., Han S., et al. Diastolic intracellular calcium-membrane voltage coupling gain and postshock arrhythmias: role of purkinje fibers and triggered activity. Circ Res 2010, 106:399-408.
54. Pogwizd S.M., Schlotthauer K., Li L., Yuan W., Bers D.M. Arrhythmogenesis and contractile dysfunction in heart failure: roles of sodium-calcium exchange, inward rectifier potassium current, and residual beta-adrenergic responsiveness. Circ Res 2001, 88:1159-1167.
55. Karma A. Spiral breakup in model equations of action potential propagation in cardiac tissue. Phys Rev Lett 1993, 71:1103-1106.
56. Saitoh H., Bailey J.C., Surawicz B. Alternans of action potential duration after abrupt shortening of cycle length: differences between dog Purkinje and ventricular muscle fibers. Circ Res 1988, 62:1027-1040.
57. Rovetti R., Cui X., Garfinkel A., Weiss J.N., Qu Z. Spark-induced sparks as a mechanism of intracellular calcium alternans in cardiac myocytes. Circ Res 2010, 106:1582-1591.
58. Mahajan A., Sato D., Shiferaw Y., Baher A., Xie L.-H., Peralta R., et al. Modifying L-type calcium current kinetics: consequences for cardiac excitation and arrhythmia dynamics. Biophys J 2008, 94:411-423.
59. Pu J., Balser J.R., Boyden P.A. Lidocaine action on Na currents in ventricular myocytes from the epicardial border zone of the infarcted heart. Circ Res 1998, 83:431-440.
60. Joyner R.W., Ramza B.M., Osaka T., Tan R.C. Cellular mechanisms of delayed recovery of excitability in ventricular tissue. Am J Physiol 1991, 260:H225-H233.
61. Pu J., Boyden P.A. Alterations of Na currents in myocytes from epicardial border zone of the infarcted heart. A possible ionic mechanism for reduced excitability and postrepolarization refractoriness. Circ Res 1997, 81:110-119.
62. Roden D.M. Taking the "idio" out of "idiosyncratic": predicting Torsades de Pointes. Pacing Clin Electrophysiol 1998, 21:1029-1034.
63. Roden D.M. Long QT, syndrome: reduced repolarization reserve and the genetic link. J Int Med 2006, 259:59-69.
64. Nattel S., Maguy A., Le Bouter S., Yeh Y.-H. Arrhythmogenic ion-channel remodeling in the heart: heart failure, myocardial infarction, and atrial fibrillation. Physiol Rev 2007, 87:425-456.
65. January C.T., Moscucci A. Cellular mechanisms of early afterdepolarizations. Ann N Y Acad Sci 1992, 644:23-32.
66. Weiss J.N., Garfinkel A., Karagueuzian H.S., Chen P.S., Qu Z. Early afterdepolarizations and cardiac arrhythmias. Heart Rhythm 2010, 7:1891-1899.
67. Chang M.G., Sato D., de Lange E., Lee J.H., Karagueuzian H.S., Garfinkel A., et al. Bi-stable wave propagation and early afterdepolarization-mediated cardiac arrhythmias. Heart Rhythm 2012, 9:115-122.
68. Choi B.R., Burton F., Salama G. Cytosolic Ca triggers early afterdepolarizations and Torsade de Pointes in rabbit hearts with type 2 long QT syndrome. J Physiol 2002, 543:615-631.
69. Zhao Z., Wen H., Fefelova N., Allen C., Baba A., Matsuda T., et al. Revisiting the ionic mechanisms of early afterdepolarizations in cardiomyocytes: predominant by Ca waves or Ca currents?. Am J Physiol Heart Circ Physiol 2012, 302:H1636-H1644.
70. Volders P.G., Vos M.A., Szabo B., Sipido K.R., de Groot S.H., Gorgels A.P., et al. Progress in the understanding of cardiac early afterdepolarizations and torsades de pointes: time to revise current concepts. Cardiovasc Res 2000, 46:376-392.
71. Clancy C.E., Rudy Y. Na channel mutation that causes both Brugada and long-QT syndrome phenotypes: a simulation study of mechanism. Circulation 2002, 105:1208-1213.
72. Luo C.H., Rudy Y. A dynamic model of the cardiac ventricular action potential.2. Afterdepolarizations, triggered activity, and potentiation. Circ Res 1994, 74:1097-1113.
73. Tran D.X., Sato D., Yochelis A., Weiss J.N., Garfinkel A., Qu Z. Bifurcation and chaos in a model of cardiac early afterdepolarizations. Phys Rev Lett 2009, 102:258103.
74. Channell P., Cymbalyuk G., Shilnikov A. Origin of bursting through homoclinic spike adding in a neuron model. Phys Rev Lett 2007, 98:134101.
75. Shilnikov A., Cymbalyuk G. Transition between tonic spiking and bursting in a neuron model via the blue-sky catastrophe. Phys Rev Lett 2005, 94:048101.
76. Hondeghem L.M., Dujardin K., De Clerck F. Phase 2 prolongation, in the absence of instability and triangulation, antagonizes class III proarrhythmia. Cardiovasc Res 2001, 50:345-353.
77. Zhao Z., Xie Y., Wen H., Xiao D., Allen C., Fefelova N., et al. Role of the transient outward potassium current in the genesis of early afterdepolarizations in cardiac cells. Cardiovasc Res 2012, 95:308-316.
78. Nguyen T.P., Xie Y., Garfinkel A., Qu Z., Weiss J.N. Arrhythmogenic consequences of myofibroblast-myocyte coupling. Cardiovasc Res 2012, 93:242-251.
79. Gadsby D.C., Cranefield P.F. Two levels of resting potential in cardiac Purkinje fibers. J Gen Physiol 1977, 70:725-746.
80. Kim T.Y., Kunitomo Y., Pfeiffer Z., Patel D., Hwang J., Harrison K., et al. Complex excitation dynamics underlie polymorphic ventricular tachycardia in a transgenic rabbit model of long QT syndrome type 1. Heart Rhythm 2015, 12:220-228.
81. Chang M.G., de Lange E., Calmettes G., Garfinkel A., Qu Z., Weiss J.N. Pro- and antiarrhythmic effects of ATP-sensitive potassium current activation on reentry during early afterdepolarization-mediated arrhythmias. Heart Rhythm 2013, 10:575-582.
82. Maruyama M., Lin S.F., Xie Y., Chua S.K., Joung B., Han S., et al. Genesis of phase 3 early afterdepolarizations and triggered activity in acquired long-QT syndrome. Circ Arrhythm Electrophysiol 2011, 4:103-111.
83. Zareba W., Moss A.J., le Cessie S., Hall W.J. T wave alternans in idiopathic long QT syndrome. J Am Coll Cardiol 1994, 23:1541-1546.
84. Qu Z., Xie L.H., Olcese R., Karagueuzian H.S., Chen P.S., Garfinkel A., et al. Early afterdepolarizations in cardiac myocytes: beyond reduced repolarization reserve. Cardiovasc Res 2013, 99:6-15.
85. Bennett P.B., Yazawa K., Makita N., George A.L. Molecular mechanism for an inherited cardiac arrhythmia. Nature 1995, 376:683-685.
86. Wagner S., Dybkova N., Rasenack E.C., Jacobshagen C., Fabritz L., Kirchhof P., et al. Ca/calmodulin-dependent protein kinase II regulates cardiac Na channels. J Clin Invest 2006, 116:3127-3138.
87. Kr block is insufficient to detect Torsades de Pointes liability: role of late sodium current. Circulation 2014, 130:224-234.
88. Na augmentation leading to cellular Na and Ca overload. Circ Res 2011, 108:555-565.
89. Hale S.L., Shryock J.C., Belardinelli L., Sweeney M., Kloner R.A. Late sodium current inhibition as a new cardioprotective approach. J Mol Cell Cardiol 2008, 44:954-967.
90. Morita N., Lee J.H., Xie Y., Sovari A., Qu Z., Weiss J.N., et al. Suppression of re-entrant and multifocal ventricular fibrillation by the late sodium current blocker ranolazine. J Am Coll Cardiol 2011, 57:366-375.
91. Wu L., Shryock J.C., Song Y., Li Y., Antzelevitch C., Belardinelli L. Antiarrhythmic effects of ranolazine in a guinea pig in vitro model of long-QT syndrome. J Pharmacol Exp Ther 2004, 310:599-605.
92. Hennessey J.A., Boczek N.J., Jiang Y.H., Miller J.D., Patrick W., Pfeiffer R., et al. A CACNA1C variant associated with reduced voltage-dependent inactivation, increased CaV1.2 channel window current, and arrhythmogenesis. PLoS One 2014, 9:e106982.
93. Madhvani R.V., Xie Y., Pantazis A., Garfinkel A., Qu Z., Weiss J.N., et al. Shaping a new Ca conductance to suppress early afterdepolarizations in cardiac myocytes. J Physiol 2011, 589:6081-6092.
94. Colecraft H.M., Alseikhan B., Takahashi S.X., Chaudhuri D., Mittman S., Yegnasubramanian V., et al. Novel functional properties of Ca channel beta subunits revealed by their expression in adult rat heart cells. J Physiol 2002, 541:435-452.
95. Morita N., Sovari A.A., Xie Y., Fishbein M.C., Mandel W.J., Garfinkel A., et al. Increased susceptibility of aged hearts to ventricular fibrillation during oxidative stress. Am J Physiol Heart Circ Physiol 2009, 297:H1594-H1605.
96. Giudicessi J.R., Ackerman M.J. Potassium-channel mutations and cardiac arrhythmias-diagnosis and therapy. Nat Rev Cardiol 2012, 9:319-332.
97. Antzelevitch C., Yan G.X. J wave syndromes. Heart Rhythm 2010, 7:549-558.
98. Lukas A., Antzelevitch C. Phase 2 reentry as a mechanism of initiation of circus movement reentry in canine epicardium exposed to simulated ischemia. Cardiovasc Res 1996, 32:593-603.
99. Lukas A., Antzelevitch C. Differences in the electrophysiological response of canine ventricular epicardium and endocardium to ischemia. Role of the transient outward current. Circulation 1993, 88:2903-2915.
100. Hoogendijk M.G., Opthof T., Postema P.G., Wilde A.A., de Bakker J.M., Coronel R. The Brugada ECG pattern: a marker of channelopathy, structural heart disease, or neither? Toward a unifying mechanism of the Brugada syndrome. Circ Arrhythm Electrophysiol 2010, 3:283-290.
101. Jeyaraj D., Wilson L.D., Zhong J., Flask C., Saffitz J.E., Deschenes I., et al. Mechanoelectrical feedback as novel mechanism of cardiac electrical remodeling. Circulation 2007, 115:3145-3155.
102. Burashnikov A., Antzelevitch C. Reinduction of atrial fibrillation immediately after termination of the arrhythmia is mediated by late phase 3 early afterdepolarization-induced triggered activity. Circulation 2003, 107:2355-2360.
103. Chua S.K., Chang P.C., Maruyama M., Turker I., Shinohara T., Shen M.J., et al. Small-conductance calcium-activated potassium channel and recurrent ventricular fibrillation in failing rabbit ventricles. Circ Res 2011, 108:971-979.
104. Maoz A., Christini D.J., Krogh-Madsen T. Dependence of phase-2 reentry and repolarization dispersion on epicardial and transmural ionic heterogeneity: a simulation study. Europace 2014, 16:458-465.
105. Maoz A., Krogh-Madsen T., Christini D.J. Instability in action potential morphology underlies phase 2 reentry: a mathematical modeling study. Heart Rhythm 2009, 6:813-822.
106. to on guinea pig and canine ventricular action potential morphology. Am J Physiol Heart Circ Physiol 2006, 291:H631-H637.
107. to1 in shaping action potential morphology and duration. Circ Res 2000, 87:1026-1033.
108. Miyoshi S., Mitamura H., Fujikura K., Fukuda Y., Tanimoto K., Hagiwara Y., et al. A mathematical model of phase 2 reentry: role of L-type Ca current. Am J Physiol Heart Circ Physiol 2003, 284:H1285-H1294.
109. Hsieh Y.C., Chang P.C., Hsueh C.H., Lee Y.S., Shen C., Weiss J.N., et al. Apamin-sensitive potassium current modulates action potential duration restitution and arrhythmogenesis of failing rabbit ventricles. Circ Arrhythm Electrophysiol 2013, 6:410-418.
110. Chi K.R. Revolution dawning in cardiotoxicity testing. Nat Rev Drug Discov 2013, 12:565-567.
111. Moreno J.D., Zhu Z.I., Yang P.C., Bankston J.R., Jeng M.T., Kang C., et al. A computational model to predict the effects of class I anti-arrhythmic drugs on ventricular rhythms. Sci Transl Med 2011, 3:98ra83.
112. Na-linked arrhythmias: in silico pharmacological screening. Circ Res 2013, 113:e50-e61.
113. Tenenbaum J.B., Vd Silva, Langford J.C. A global geometric framework for nonlinear dimensionality reduction. Science 2000, 290:2319-2323.
114. Piccini J.P., Hammill B.G., Sinner M.F., Jensen P.N., Hernandez A.F., Heckbert S.R., et al. Incidence and prevalence of atrial fibrillation and associated mortality among Medicare beneficiaries, 1993-2007. Circ Cardiovasc Qual Outcomes 2012, 5:85-93.
115. Calkins H. Catheter ablation to maintain sinus rhythm. Circulation 2012, 125:1439-1445.
116. Cappato R., Calkins H., Chen S.A., Davies W., Iesaka Y., Kalman J., et al. Updated worldwide survey on the methods, efficacy, and safety of catheter ablation for human atrial fibrillation. Circ Arrhythm Electrophysiol 2010, 3:32-38.
117. Song Y., Shryock J.C., Belardinelli L. An increase of late sodium current induces delayed afterdepolarizations and sustained triggered activity in atrial myocytes. Am J Physiol Heart Circ Physiol 2008, 294:H2031-H2039.
118. Hiromoto K., Shimizu H., Furukawa Y., Kanemori T., Mine T., Masuyama T., et al. Discordant repolarization alternans-induced atrial fibrillation is suppressed by verapamil. Circ J 2005, 69:1368-1373.
119. Atienza F., Martins R.P., Jalife J. Translational research in atrial fibrillation: a quest for mechanistically based diagnosis and therapy. Circ Arrhythm Electrophysiol 2012, 5:1207-1215.
120. Wijffels M., Kirchhof C., Dorland R., Allessie M.A. Atrial fibrillation begets atrial fibrillation - a study in awake chronically instrumented goats. Circulation 1995, 92:1954-1968.