Reversible cardiac conduction block and defibrillation with high-frequency electric field

Science Translational Medicine

Volumn 3, Issue 102, 2011, Pages

  Tandri, Harikrishna ^a   Weinberg, Seth H ^b   Chang, Kelly C ^b   Zhu, Renjun ^b   Trayanova, Natalia A ^b   Tung, Leslie ^b   Berger, Ronald D ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; COMPUTER PROGRAM; CONTROLLED STUDY; DEFIBRILLATION; ELECTRIC FIELD; EXPERIMENTAL RABBIT; GUINEA PIG; HEART ARRHYTHMIA; HEART CONDUCTION; HEART DEPOLARIZATION; HEART FIBRILLATION; HEART MUSCLE CELL; HEART MUSCLE FIBER MEMBRANE POTENTIAL; HEART MUSCLE REFRACTORY PERIOD; HEART REPOLARIZATION; NERVE BLOCK; NONHUMAN; PRIORITY JOURNAL; SIMULATION; SURVIVAL RATE; ANIMAL; CARDIOVERSION; COMPUTER SIMULATION; ELECTRICITY; ELECTROSTIMULATION; HEART MUSCLE CONDUCTION SYSTEM; IN VITRO STUDY; MALE; METABOLISM; METHODOLOGY; PATHOPHYSIOLOGY; RABBIT; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; ARRHYTHMIAS, CARDIAC; COMPUTER SIMULATION; ELECTRIC COUNTERSHOCK; ELECTRIC STIMULATION; ELECTRICITY; GUINEA PIGS; HEART CONDUCTION SYSTEM; MALE; MYOCYTES, CARDIAC; RABBITS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 80053269110     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3002445     Document Type: Article

References (41)

1. L. Tung, O. Tovar, M. Neunlist, S. K. Jain, R. J. O'Neill, Effects of strong electrical shock on cardiac muscle tissue. Ann. N. Y. Acad. Sci. 720, 160-175 (1994).
2. A. Al-Khadra, V. Nikolski, I. R. Efimov, The role of electroporation in defibrillation. Circ. Res. 87, 797-804 (2000).
3. S. B. Eysmann, F. E. Marchlinski, A. E. Buxton, M. E. Josephson, Electrocardiographic changes after cardioversion of ventricular arrhythmias. Circulation 73, 73-81 (1986).
4. T. Tokano, D. Bach, J. Chang, J. Davis, J. J. Souza, A. Zivin, B. P. Knight, R. Goyal, K. C. Man, F. Morady, S. A. Strickberger, Effect of ventricular shock strength on cardiac hemodynamics. J. Cardiovasc. Electrophysiol. 9, 791-797 (1998).
5. M. Mollerus, L. Naslund, Myocardial stunning following defibrillation threshold testing. J. Interv. Card. Electrophysiol. 19, 213-216 (2007).
6. A. J. Moss, W. Zareba, W. J. Hall, H. Klein, D. J. Wilber, D. S. Cannom, J. P. Daubert, S. L. Higgins, M. W. Brown, M. L. Andrews; Multicenter Automatic Defibrillator Implantation Trial II Investigators, Prophylactic implantation of a defibrillator in patients with myocardial infarction and reduced ejection fraction. N. Engl. J. Med. 346, 877-883 (2002).
7. J. A. Tanner, Reversible blocking of nerve conduction by alternating-current excitation. Nature 195, 712-713 (1962).
8. D. M. Ackermann Jr., E. L. Foldes, N. Bhadra, K. L. Kilgore, Conduction block of peripheral nerve using high-frequency alternating currents delivered through an intrafascicular electrode. Muscle Nerve 41, 117-119 (2010).
9. N. Bhadra, E. A. Lahowetz, S. T. Foldes, K. L. Kilgore, Simulation of high-frequency sinusoidal electrical block of mammalian myelinated axons. J. Comput. Neurosci. 22, 313-326 (2007).
10. X. Zhang, J. R. Roppolo, W. C. De Groat, C. Tai, Mechanismof nerve conduction block induced by high-frequency biphasic electrical currents. IEEE Trans. Biomed. Eng. 53, 2445-2454 (2006).
11. A. Boger, N. Bhadra, K. J. Gustafson, Bladder voiding by combined high frequency electrical pudendal nerve block and sacral root stimulation. Neurourol. Urodyn. 27, 435-439 (2008).
12. R. M. Shaw, Y. Rudy, Ionic mechanisms of propagation in cardiac tissue. Roles of the sodium and L-type calcium currents during reduced excitability and decreased gap junction coupling. Circ. Res. 81, 727-741 (1997).
13. T. Ashihara, J. Constantino, N. A. Trayanova, Tunnel propagation of postshock activations as a hypothesis for fibrillation induction and isoelectric window. Circ. Res. 102, 737-745 (2008).
14. B. Rodríguez, L. Li, J. C. Eason, I. R. Efimov, N. A. Trayanova, Differences between left and right ventricular chamber geometry affect cardiac vulnerability to electric shocks. Circ. Res. 97, 168-175 (2005).
15. I. R. Efimov, Y. Cheng, Y. Yamanouchi, P. J. Tchou, Direct evidence of the role of virtual electrode-induced phase singularity in success and failure of defibrillation. J. Cardiovasc. Electrophysiol. 11, 861-868 (2000).
16. M. W. Kroll, C. D. Swerdlow, Optimizing defibrillation waveforms for ICDs. J. Interv. Card. Electrophysiol. 18, 247-263 (2007).
17. G. T. Smith, R. Beeuwkes, M. Tomkiewicz, T. Abe, B. Lown, Pathological changes in skin and skeletal muscle following alternating current and capacitor discharge. Am. J. Pathol. 47, 1-17 (1965).
18. B. Lown, J. Neuman, R. Amarasingham, B. V. Berkovits, Comparison of alternating current with direct electroshock across the closed chest. Am. J. Cardiol. 10, 223-233 (1962).
19. J. Weirich, S. Hohnloser, H. Antoni, Factors determining the susceptibility of the isolated guinea pig heart to ventricular fibrillation induced by sinusoidal alternating current at frequencies from 1 to 1000 Hz. Basic Res. Cardiol. 78, 604-616 (1983).
20. S. J. Roberts, D. Guan, R. Malkin, The defibrillation efficacy of high frequency alternating current sinusoidal waveforms in guinea pigs. Pacing Clin. Electrophysiol. 26, 599-604 (2003).
21. W. Li, C. M. Ripplinger, Q. Lou, I. R. Efimov, Multiple monophasic shocks improve electrotherapy of ventricular tachycardia in a rabbit model of chronic infarction. Heart Rhythm 6, 1020-1027 (2009).
22. C. M. Ambrosi, C. M. Ripplinger, I. R. Efimov, V. V. Fedorov, Termination of sustained atrial flutter and fibrillation using low-voltage multiple-shock therapy. Heart Rhythm 8, 101-108 (2011).
23. R. J. Sweeney, R. M. Gill, J. L. Jones, P. R. Reid, Defibrillation using a high-frequency series of monophasic rectangular pulses: Observations and model predictions. J. Cardiovasc. Electrophysiol. 7, 134-143 (1996).
24. J. M. Meunier, N. A. Trayanova, R. A. Gray, Sinusoidal stimulation of myocardial tissue: Effects on single cells. J. Cardiovasc. Electrophysiol. 10, 1619-1630 (1999).
25. J. M. Meunier, N. A. Trayanova, R. A. Gray, Entrainment by an extracellular AC stimulus in a computational model of cardiac tissue. J. Cardiovasc. Electrophysiol. 12, 1176-1184 (2001).
26. O. V. Aslanidi, A. P. Benson, M. R. Boyett, H. Zhang, Mechanisms of defibrillation by standing waves in the bidomain ventricular tissue with voltage applied in an external bath. Phys. D Nonlinear Phenom. 238, 984-991 (2009).
27. J. M. Meunier, J. C. Eason, N. A. Trayanova, Termination of reentry by a long-lasting AC shock in a slice of canine heart: A computational study. J. Cardiovasc. Electrophysiol. 13, 1253-1261 (2002).
28. R. A. Gray, O. A. Mornev, J. Jalife, O. V. Aslanidi, A. M. Pertsov, Standing excitation waves in the heart induced by strong alternating electric fields. Phys. Rev. Lett. 87, 168104 (2001).
29. J. M. Davidenko, M. Delmar, J. Beaumont, D. C. Michaels, P. Lorente, J. Jalife, Electrotonic inhibition and active facilitation of excitability in ventricular muscle. J. Cardiovasc. Electrophysiol. 5, 945-960 (1994).
30. L.M. Loew, L. B. Cohen, J. Dix, E. N. Fluhler, V. Montana, G. Salama, J. Y. Wu, A naphthyl analog of the aminostyryl pyridinium class of potentiometric membrane dyes shows consistent sensitivity in a variety of tissue, cell, and model membrane preparations. J. Membr. Biol. 130, 1-10 (1992).
31. T. Watanabe, P. M. Rautaharju, T. F. McDonald, Ventricular action potentials, ventricular extracellular potentials, and the ECG of guinea pig. Circ. Res. 57, 362-373 (1985).
32. S. Iravanian, Y. Nabutovsky, C. R. Kong, S. Saha, N. Bursac, L. Tung, Functional reentry in cultured monolayers of neonatal rat cardiac cells. Am. J. Physiol. Heart Circ. Physiol. 285, H449-H456 (2003).
33. Z. Y. Lim, B. Maskara, F. Aguel, R. Emokpae Jr., L. Tung, Spiral wave attachment to millimetersized obstacles. Circulation 114, 2113-2121 (2006).
34. S. Weinberg, E. A. Lipke, L. Tung, In vitro electrophysiological mapping of stem cells. Methods Mol. Biol. 660, 215-237 (2010).
35. E. Entcheva, S. N. Lu, R. H. Troppman, V. Sharma, L. Tung, Contact fluorescence imaging of reentry in monolayers of cultured neonatal rat ventricular myocytes. J. Cardiovasc. Electrophysiol. 11, 665-676 (2000).
36. R. Plonsey, Bioelectric sources arising in excitable fibers (ALZA lecture). Ann. Biomed. Eng. 16, 519-546 (1988).
37. C. H. Luo, Y. Rudy, A model of the ventricular cardiac action potential. Depolarization, repolarization, and their interaction. Circ. Res. 68, 1501-1526 (1991).
38. N. Trayanova, J. Eason, F. Aguel, Computing and Visualization in Science (Springer, Berlin/Heidelberg, 2002), vol. 4, pp. 259-270.
39. T. Ashihara, N. A. Trayanova, Asymmetry in membrane responses to electric shocks: Insights from bidomain simulations. Biophys. J. 87, 2271-2282 (2004).
40. J. Constantino, Y. Long, T. Ashihara, N. A. Trayanova, Tunnel propagation following defibrillation with ICD shocks: Hidden postshock activations in the left ventricular wall underlie isoelectric window. Heart Rhythm 7, 953-961 (2010).
41. Funding: This work was supported by NIH grants R21 HL104338 (L.T. and R.D.B.) and S10 RR025544 (L.T.), a Maryland Technology Development Corporation University Technology Development Fund award (R.D.B.), and The Michel Mirowski MD Discovery Fund (H.T.). Author contributions: The studies were designed by H.T., S.H.W., N.A.T., L.T., and R.D.B. Cell preparation, isolated heart, and intact animal experiments were conducted by S.H.W., H.T., R.Z., L.T., and R.D.B. Computational modeling work was conducted by K.C.C. and N.A.T. Themanuscript waswritten primarily by H.T., S.H.W., N.A.T., L.T., and R.D.B. Competing interests: H.T., R.D.B., S.H.W., L.T., and N.A.T. are coinventors on a pending patent application for a device to treat cardiac arrhythmias using HFAC fields. The other authors declare that they have no competing interests.