Sodium channel block by ranolazine in an experimental model of stretch-related atrial fibrillation: Prolongation of interatrial conduction time and increase in post-repolarization refractoriness

Europace

Volumn 15, Issue 5, 2013, Pages 761-769

  Milberg, Peter ^a   Frommeyer, Gerrit ^a   Ghezelbash, Shokoufeh ^a   Rajamani, Sridharan ^b   Osada, Nani ^c   Razvan, Radu ^d   Belardinelli, Luiz ^b   Breithardt, Günter ^a   Eckardt, Lars ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b Gilead Sciences ^*  (United States)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d UNIVERSITY OF MEDICINE AND PHARMACY OF CRAIOVA   (Romania)

Author keywords

Atrial fibrillation; Atrial stretch; Flecainide; Ranolazine

Indexed keywords

FLECAINIDE; RANOLAZINE; SODIUM CHANNEL; SOTALOL;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG RESPONSE; EXPERIMENTAL RABBIT; FEEDBACK SYSTEM; FEMALE; HEART ATRIUM CONDUCTION; HEART ATRIUM ENLARGEMENT; HEART ATRIUM FIBRILLATION; HEART HEMODYNAMICS; HEART LEFT ATRIUM; HEART MUSCLE POTENTIAL; HEART MUSCLE REFRACTORY PERIOD; HEART REPOLARIZATION; ISOLATED HEART; MORBIDITY; MUSCLE STRETCHING; NONHUMAN; PRIORITY JOURNAL;

ACETANILIDES; ADMINISTRATION, ORAL; ANIMALS; ANTI-ARRHYTHMIA AGENTS; ATRIAL FIBRILLATION; FEMALE; FLECAINIDE; HEART CONDUCTION SYSTEM; HEART RATE; NEURAL CONDUCTION; PIPERAZINES; RABBITS; REFRACTORY PERIOD, ELECTROPHYSIOLOGICAL; SODIUM CHANNEL BLOCKERS; SOTALOL; TREATMENT OUTCOME;

EID: 84877296675     PISSN: 10995129     EISSN: 15322092     Source Type: Journal    
DOI: 10.1093/europace/eus399     Document Type: Article

References (57)

1. Frommeyer G, Milberg P, Witte P, Stypmann J, Koopmann M, Lücke M et al. A new mechanism preventing proarrhythmia in chronic heart failure: rapid phase-III repolarization explains the low proarrhythmic potential of amiodarone in contrast to sotalol in a model of pacing-induced heart failure. Eur J Heart Fail 2011; 13: 1060-9.
2. Burashnikov A, Di Diego JM, Zygmunt AC, Belardinelli L, Antzelevitch C. Atriumselective sodium channel block as a strategy for suppression of atrial fibrillation: differences in sodium channel inactivation between atria and ventricles and the role of ranolazine. Circulation 2007;116: 1449-57.
3. Sicouri S, Glass A, Belardinelli L, Antzelevitch C. Antiarrhythmic effects of ranolazine in canine pulmonary vein sleeve preparations. Heart Rhythm 2008;5: 1019-26.
4. Murdock DK, Overton N, Kersten M, Kaliebe J, Devecchi F. The effect of ranolazine on maintaining sinus rhythm in patients with resistant atrial fibrillation. Indian Pacing Electrophysiol J 2008;8: 175-81.
5. Antzelevitch C, Belardinelli L, Zygmunt AC, Burashnikov A, Di Diego JM, Fish JM et al. Electrophysiological effects of ranolazine, a novel antianginal agent with antiarrhythmic properties. Circulation 2004;110: 904-10.
6. Fredj S, Sampson KJ, Liu H, Kass RS. Molecular basis of ranolazine block of LQT-3 mutant sodium channels: evidence for site of action. Br J Pharmacol 2006;148: 16-24.
7. Kloner RA, Dow JS, Bhandari A. The antianginal agent ranolazine is a potent antiarrhythmic agent that reduces ventricular arrhythmias: through a mechanism favoring inhibition of late sodium channel. Cardiovasc Ther 2011;29:e36-41.
8. Kumar K, Nearing BD, Carvas M, Nascimento BC, Acar M, Belardinelli L et al. Ranolazine exerts potent effects on atrial electrical properties and abbreviates atrial fibrillation duration in the intact porcine heart. J Cardiovasc Electrophysiol 2009;20: 796-802.
9. Sossalla S, Kallmeyer B, Wagner S, Mazur M, Maurer U, Toischer K et al. Altered Na(+) currents in atrial fibrillation effects of ranolazine on arrhythmias and contractility in human atrial myocardium. J Am Coll Cardiol 2010;55: 2330-42.
10. Miles RH, Passman R, Murdock DK. Comparison of effectiveness and safety of ranolazine versus amiodarone for preventing atrial fibrillation after coronary artery bypass grafting. Am J Cardiol 2011;108: 673-6.
11. Murdock DK, Kersten M, Kaliebe J, Larrain G. The use of oral ranolazine to convert new or paroxysmal atrial fibrillation: A review of experience with implications for possible "pill in the pocket" approach to atrial fibrillation. Indian Pacing Electrophysiol J 2009;9: 260-7.
12. Eckardt L, Kirchhof P, Mönnig G, Breithardt G, Borggrefe M, Haverkamp W. Modification of stretch-induced shortening of repolarization by streptomycin in the isolated rabbit heart. J Cardiovasc Pharmacol 2000;36: 711-21.
13. Eckardt L, Kirchhof P, Breithardt G, Haverkamp W. Load-induced changes in repolarization: evidence from experimental and clinical data. Basic Res Cardiol 2001;96: 369-80.
14. Kannel WB, Abbott RD, Savage DD, McNamara PM. Epidemiologic features of chronic atrial fibrillation: the Framingham study. N Engl J Med 1982;306: 1018-22.
15. Ravelli F, Allessie M. Effects of atrial dilatation on refractory period and vulnerability to atrial fibrillation in the isolated Langendorff-perfused rabbit heart. Circulation 1997;96: 1686-95.
16. Bode F, Sachs F, Franz MR. Tarantula peptide inhibits atrial fibrillation. Nature 2001;409: 35-6.
17. Zarse M, Stellbrink C, Athanatou E, Robert J, Schotten U, Hanrath P. Verapamil prevents stretch-induced shortening of atrial effective refractory period in Langendorff-perfused rabbit heart. J Cardiovasc Electrophysiol 2001;12: 85-92.
18. Chen YJ, Chen SA, Tai CT, Wen ZC, Feng AN, Ding YA et al. Role of atrial electrophysiology and autonomic nervous system in patients with supraventricular tachycardia and paroxysmal atrial fibrillation. J Am Coll Cardiol 1998;32: 732-8.
19. Klein LS, Miles WM, Zipes DP. Effect of atrioventricular interval during pacing or reciprocating tachycardia on atrial size, pressure, and refractory period. Contraction-excitation feedback in human atrium. Circulation 1990;82: 60-8.
20. Calkins H, el-Atassi R, Kalbfleisch S, Langberg J, Morady F. Effects of an acute increase in atrial pressure on atrial refractoriness in humans. Pacing Clin Electrophysiol 1992;15: 1674-80.
21. Calkins H, el-Atassi R, Leon A, Kalbfleisch S, Borganelli M, Langberg J et al. Effect of the atrioventricular relationship on atrial refractoriness in humans. Pacing Clin Electrophysiol 1992;15: 771-8.
22. Milberg P, Eckardt L, Bruns HJ, Biertz J, Ramtin S, Reinsch N et al. Divergent proarrhythmic potential of macrolide antibiotics despite similar QT prolongation: fast phase 3 repolarization prevents early afterdepolarizations and torsade de pointes. J Pharmacol Exp Ther 2002;303: 218-25.
23. Eckardt L, Breithardt G, Haverkamp W. Electrophysiologic characterization of the antipsychotic drug sertindole in a rabbit heart model of Torsade de pointes: low torsadogenic potential despite QT prolongation. J Pharmacol Exp Ther 2002;300: 64-71.
24. Milberg P, Hilker E, Ramtin S, Cakir Y, Stypmann J, Engelen MA et al. Proarrhythmia as a class effect of quinolones: increased dispersion of repolarization and triangulation of action potential predict Torsades de pointes. J Cardiovasc Electrophysiol 2007;18: 647-54.
25. Zarse M, Deharo JC, Mast F, Allessie MA. Importance of right and left atrial dilation and linear ablation for perpetuation of sustained atrial fibrillation. J Cardiovasc Electrophysiol 2002;13: 164-71.
26. Kirchhof PF, Fabritz CL, Franz MR. Postrepolarization refractoriness versus conduction slowing caused by class I antiarrhythmic drugs: antiarrhythmic and proarrhythmic effects. Circulation 1998;97: 2567-74.
27. Clements-Jewery H, Kanaganayagam GS, Kabra R, Curtis MJ. Actions of flecainide on susceptibility to phase-2 ventricular arrhythmias during infarct evolution in rat isolated perfused hearts. Br J Pharmacol 2006;147: 468-75.
28. Elonen E, Neuvonen PJ, Tarssanen L, Kala R. Sotalol intoxication with prolonged Q-T interval and severe tachyarrhythmias. Br Med J 1979;1: 1184.
29. Eijsbouts SC, Houben RP, Blaauw Y, Schotten U, Allessie MA. Synergistic action of atrial dilation and sodium channel blockade on conduction in rabbit atria. J Cardiovasc Electrophysiol 2004;15: 1453-61.
30. Kalifa J, Bernard M, Gout B, Bril A, Cozma D, Laurent P et al. Anti-arrhythmic effects of I (Na), I (Kr), and combined I (Kr)-I (Ca L) blockade in an experimental model of acute stretch-related atrial fibrillation. Cardiovasc Drugs Ther 2007;21: 47-53.
31. Hale SL, Mehra A, Leeka J, Kloner RA. Post-conditioning fails to improve no reflow or alter infarct size in an open-chest rabbit model of myocardial ischemia-reperfusion. Am J Physiol Heart Circ Physiol 2008;294:H421-5.
32. Hale SL, Shryock JC, Belardinelli L, Sweeney M, Kloner RA. Late sodium current inhibition as a new cardioprotective approach. J Mol Cell Cardiol 2008;44: 954-67.
33. Undrovinas AI, Belardinelli L, Undrovinas NA, Sabbah HN. Ranolazine improves abnormal repolarization and contraction in left ventricular myocytes of dogs with heart failure by inhibiting late sodium current. J Cardiovasc Electrophysiol 2006;17(Suppl 1):S169-77.
34. Wang GK, Calderon J, Wang SY. State- and use-dependent block of muscle Nav1.4 and neuronal Nav1.7 voltage-gated Na+ channel isoforms by ranolazine. Mol Pharmacol 2008;73: 940-8.
35. Ravelli F. Mechano-electric feedback and atrial fibrillation. Prog Biophys Mol Biol 2003;82: 137-49.
36. Kalifa J, Jalife J, Zaitsev AV, Bagwe S, Warren M, Moreno J et al. Intra-atrial pressure increases rate and organization of waves emanating from the superior pulmonary veins during atrial fibrillation. Circulation 2003;108: 668-71.
37. Nazir SA, Lab MJ. Mechanoelectric feedback in the atrium of the isolated guineapig heart. Cardiovasc Res 1996;32: 112-9.
38. Yamane T, Shah DC, Jais P, Hocini M, Peng JT, Deisenhofer I et al. Dilatation as a marker of pulmonary veins initiating atrial fibrillation. J Interv Card Electrophysiol 2002;6: 245-9.
39. Kim D, Fu C. Activation of a nonselective cation channel by swelling in atrial cells. J Membr Biol 1993;135: 27-37.
40. Kim D. A mechanosensitive K+ channel in heart cells. Activation by arachidonic acid. J Gen Physiol 1992;100: 1021-40.
41. Watanabe H, Watanabe I, Nakai T, Oshikawa N, Kunimoto S, Masaki R et al. Frequency-dependent electrophysiological effects of flecainide, nifekalant and d, l-sotalol on the human atrium. Jpn Circ J 2001;65: 1-6.
42. Tse HF, Pelosi F, Oral H, Knight BP, Strickberger SA, Morady F. Effects of simultaneous atrioventricular pacing on atrial refractoriness and atrial fibrillation inducibility: role of atrial mechanoelectrical feedback. J Cardiovasc Electrophysiol 2001; 12: 43-50.
43. Allessie MA, Schalij MJ, Kirchhof CJ, Boersma L, Huyberts M, Hollen J. Electrophysiology of spiral waves in two dimensions: the role of anisotropy. Ann N Y Acad Sci 1990;591: 247-56.
44. Kirchhof P, Engelen M, Franz MR, Ribbing M, Wasmer K, Breithardt G et al. Electrophysiological effects of flecainide and sotalol in the human atrium during persistent atrial fibrillation. Basic Res Cardiol 2005;100: 112-21.
45. Kirchhof P, Degen H, Franz MR, Eckardt L, Fabritz L, Milberg P et al. Amiodarone-induced postrepolarization refractoriness suppresses induction of ventricular fibrillation. J Pharmacol Exp Ther 2003;305: 257-63.
46. Zygmunt AC, Nesterenko VV, Rajamani S, Hu D, Barajas-Martinez H, Belardinelli L et al. Mechanisms of atrial-selective block of Na(+) channels by ranolazine: I. Experimental analysis of the use-dependent block. Am J Physiol Heart Circ Physiol 2011;301:H1606-14.
47. Rajamani S, El-Bizri N, Shryock JC, Makielski JC, Belardinelli L. Use-dependent block of cardiac late Na(+) current by ranolazine. Heart Rhythm 2009;6: 1625-31.
48. Cerrone M, Noujaim S, Jalife J. The short QT syndrome as a paradigm to understand the role of potassium channels in ventricular fibrillation. J Intern Med 2006; 259: 24-38.
49. Regan CP, Kiss L, Stump GL, McIntyre CJ, Beshore DC, Liverton NJ et al. Atrial antifibrillatory effects of structurally distinct IKur blockers 3-[(dimethylamino)methyl]- 6-methoxy-2-methyl-4-phenylisoquinolin-1(2H)-one and 2-phenyl-1,1-dipyridin- 3-yl-2-pyrrolidin-1-yl-ethanol in dogs with underlying heart failure. J Pharmacol Exp Ther 2008;324: 322-30.
50. Christ T, Wettwer E, Voigt N, Hala O, Radicke S, Matschke K et al. Pathologyspecific effects of the IKur/Ito/IK, ACh blocker AVE0118 on ion channels in human chronic atrial fibrillation. Br J Pharmacol 2008;154: 1619-30.
51. Camm AJ, Lip GY, De Caterina R, Savelieva I, Atar D, Hohnloser SH et al. 2012 focused update of the ESC Guidelines for the management of atrial fibrillation: An update of the 2010 ESC Guidelines for the management of atrial fibrillation. Developed with the special contribution of the European Heart Rhythm Association. Europace 2012;14: 1385-413.
52. Antoons G, Oros A, Beekman JD, Engelen MA, Houtman MJ, Belardinelli L et al. Late Na(+) current inhibition by ranolazine reduces torsades de pointes in the chronic atrioventricular block dog model. J Am Coll Cardiol 2010;55: 801-9.
53. Dhalla AK, Wang WQ, Dow J, Shryock JC, Belardinelli L, Bhandari A et al. Ranolazine, an antianginal agent, markedly reduces ventricular arrhythmias induced by ischemia and ischemia-reperfusion. Am J Physiol Heart Circ Physiol 2009;297: H1923-9.
54. Moss AJ, Zareba W, Schwarz KQ, Rosero S, McNitt S, Robinson JL. Ranolazine shortens repolarization in patients with sustained inward sodium current due to type-3 long-QT syndrome. J Cardiovasc Electrophysiol 2008;19: 1289-93.
55. Scirica BM, Morrow DA, Hod H, Murphy SA, Belardinelli L, Hedgepeth CM et al. Effect of ranolazine, an antianginal agent with novel electrophysiological properties, on the incidence of arrhythmias in patients with non ST-segment elevation acute coronary syndrome: results from the Metabolic Efficiency with Ranolazine for Less Ischemia in Non ST-Elevation Acute Coronary Syndrome Thrombolysis in Myocardial Infarction 36 (MERLIN-TIMI 36) randomized controlled trial. Circulation 2007;116: 1647-52.
56. Bunch TJ, Mahapatra S, Murdock D, Molden J, Weiss JP, May HT et al. Ranolazine reduces ventricular tachycardia burden and ICD shocks in patients with drug-refractory ICD shocks. Pacing Clin Electrophysiol 2011;34: 1600-6.
57. Frommeyer G, Schmidt M, Clauß C, Stypmann J, Kaese S, Pott C et al. Further insights into the underlying electrophysiologic mechanisms for reduction of atrial fibrillation by ranolazine in an experimental model of chronic heart failure. Eur J Heart Fail 2012 Oct 25. [Epub ahead of print]. PMID: 23099358.