(Circulation. 1995;91:2454-2469.)
© 1995 American Heart Association, Inc.
Articles |
Nonstationary Vortexlike Reentrant Activity as a Mechanism of Polymorphic Ventricular Tachycardia in the Isolated Rabbit Heart
From the Department of Pharmacology, SUNY Health Science Center at Syracuse, NY, and the Department of Theoretical Biology (A.P.), University of Utrecht, Utrecht, the Netherlands.
Correspondence to Richard A. Gray, SUNY Health Science Center, Department of Pharmacology, 766 Irving Ave, Syracuse, NY 13210.
Background Ventricular tachycardia may result from vortexlike reentrant excitation of the myocardium. Our general hypothesis is that in the structurally normal heart, these arrhythmias are the result of one or two nonstationary three-dimensional electrical scroll waves activating the heart muscle at very high frequencies.
Methods and Results We used a combination of high-resolution video imaging, electrocardiography, and image processing in the isolated rabbit heart, together with mathematical modeling. We characterized the dynamics of changes in transmembrane potential patterns on the epicardial surface of the ventricles using optical mapping. Image processing techniques were used to identify the surface manifestation of the reentrant organizing centers, and the location of these centers was used to determine the movement of the reentrant pathway. We also used numerical simulations incorporating Fitzhugh-Nagumo kinetics and realistic heart geometry to study how stationary and nonstationary scroll waves are manifest on the epicardial surface and in the simulated ECG. We present epicardial surface manifestations (reentrant spiral waves) and ECG patterns of nonstationary reentrant activity that are consistent with those generated by scroll waves established at the right and left ventricles. We identified the organizing centers of the reentrant circuits on the epicardial surface during polymorphic tachycardia, and these centers moved during the episodes. In addition, the arrhythmias that showed the greatest movement of the reentrant centers displayed the largest changes in QRS morphology. The numerical simulations showed that stationary scroll waves give rise to monomorphic ECG signals, but nonstationary meandering scroll waves give rise to undulating ECGs characteristic of torsade de pointes.
Conclusions Polymorphic ventricular tachycardia in the healthy, isolated rabbit heart is the result of either a single or paired ("figure-of-eight") nonstationary scroll waves. The extent of the scroll wave movement corresponds to the degree of polymorphism in the ECG. These results are consistent with our numerical simulations that showed monomorphic ECG patterns of activity for stationary scroll waves but polymorphic patterns for scroll waves that were nonstationary.
Key Words: tachycardia • reentry • arrhythmia • torsade de pointes
This article has been cited by other articles:
 |
|
 |
|
  L. Tang, G.-S. Hwang, H. Hayashi, J. Song, M. Ogawa, K. Kobayashi, B. Joung, H. S. Karagueuzian, P.-S. Chen, and S.-F. Lin Intracellular calcium dynamics at the core of endocardial stationary spiral waves in Langendorff-perfused rabbit hearts Am J Physiol Heart Circ Physiol, July 1, 2008; 295(1): H297 - H304. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. B. Huffaker, J. N. Weiss, and B. Kogan Effects of early afterdepolarizations on reentry in cardiac tissue: a simulation study Am J Physiol Heart Circ Physiol, June 1, 2007; 292(6): H3089 - H3102. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. V. Panfilov, R. H. Keldermann, and M. P. Nash Drift and breakup of spiral waves in reaction diffusion mechanics systems PNAS, May 8, 2007; 104(19): 7922 - 7926. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. F. Mironov, F. J. Vetter, and A. M. Pertsov Fluorescence imaging of cardiac propagation: spectral properties and filtering of optical action potentials Am J Physiol Heart Circ Physiol, July 1, 2006; 291(1): H327 - H335. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. H. Everett IV, E. E. Wilson, S. Foreman, and J. E. Olgin Mechanisms of Ventricular Fibrillation in Canine Models of Congestive Heart Failure and Ischemia Assessed by In Vivo Noncontact Mapping Circulation, September 13, 2005; 112(11): 1532 - 1541. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. Comtois, J. Kneller, and S. Nattel Of circles and spirals: Bridging the gap between the leading circle and spiral wave concepts of cardiac reentry Europace, January 1, 2005; 7(s2): S10 - S20. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Szumowski, P. Sanders, F. Walczak, M. Hocini, P. Jais, R. Kepski, E. Szufladowicz, P. Urbanek, P. Derejko, R. Bodalski, et al. Mapping and ablation of polymorphic ventricular tachycardia after myocardial infarction J. Am. Coll. Cardiol., October 19, 2004; 44(8): 1700 - 1706. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 I. R. Efimov, V. P. Nikolski, and G. Salama Optical Imaging of the Heart Circ. Res., July 9, 2004; 95(1): 21 - 33. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Cheng, L. Li, V. Nikolski, D. W. Wallick, and I. R. Efimov Shock-induced arrhythmogenesis is enhanced by 2,3-butanedione monoxime compared with cytochalasin D Am J Physiol Heart Circ Physiol, January 1, 2004; 286(1): H310 - H318. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. G. Akar and D. S. Rosenbaum Transmural Electrophysiological Heterogeneities Underlying Arrhythmogenesis in Heart Failure Circ. Res., October 3, 2003; 93(7): 638 - 645. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Iravanian, Y. Nabutovsky, C.-R. Kong, S. Saha, N. Bursac, and L. Tung Functional reentry in cultured monolayers of neonatal rat cardiac cells Am J Physiol Heart Circ Physiol, June 5, 2003; 285(1): H449 - H456. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. I. Berul Electrophysiological phenotyping in genetically engineered mice Physiol Genomics, May 13, 2003; 13(3): 207 - 216. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B.-R. Choi, F. Burton, and G. Salama Cytosolic Ca2+ triggers early afterdepolarizations and torsade de pointes in rabbit hearts with type 2 long QT syndrome J. Physiol., September 1, 2002; 543(2): 615 - 631. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Boersma, Z. Zetelaki, J. Brugada, and M. Allessie Polymorphic Reentrant Ventricular Tachycardia in the Isolated Rabbit Heart Studied by High-Density Mapping Circulation, June 25, 2002; 105(25): 3053 - 3061. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M.-H. Lee, S.-F. Lin, T. Ohara, C. Omichi, Y. Okuyama, E. Chudin, A. Garfinkel, J. N. Weiss, H. S. Karagueuzian, and P.-S. Chen Effects of diacetyl monoxime and cytochalasin D on ventricular fibrillation in swine right ventricles Am J Physiol Heart Circ Physiol, June 1, 2001; 280(6): H2689 - H2696. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. H Samie and J. Jalife Mechanisms underlying ventricular tachycardia and its transition to ventricular fibrillation in the structurally normal heart Cardiovasc Res, May 1, 2001; 50(2): 242 - 250. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Patwardhan, S. Moghe, K. Wang, and F. Leonelli Frequency modulation within electrocardiograms during ventricular fibrillation Am J Physiol Heart Circ Physiol, August 1, 2000; 279(2): H825 - H835. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. H. Samie, R. Mandapati, R. A. Gray, Y. Watanabe, C. Zuur, J. Beaumont, and J. Jalife A Mechanism of Transition From Ventricular Fibrillation to Tachycardia : Effect of Calcium Channel Blockade on the Dynamics of Rotating Waves Circ. Res., March 31, 2000; 86(6): 684 - 691. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. V. Zaitsev, O. Berenfeld, S. F. Mironov, J. Jalife, and A. M. Pertsov Distribution of Excitation Frequencies on the Epicardial and Endocardial Surfaces of Fibrillating Ventricular Wall of the Sheep Heart Circ. Res., March 3, 2000; 86(4): 408 - 417. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Chen, R. Mandapati, O. Berenfeld, A. C. Skanes, and J. Jalife High-Frequency Periodic Sources Underlie Ventricular Fibrillation in the Isolated Rabbit Heart Circ. Res., January 7, 2000; 86(1): 86 - 93. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Vaidya, G. E. Morley, F. H. Samie, and J. Jalife Reentry and Fibrillation in the Mouse Heart : A Challenge to the Critical Mass Hypothesis Circ. Res., July 23, 1999; 85(2): 174 - 181. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Z. Qu, J. N. Weiss, and A. Garfinkel Cardiac electrical restitution properties and stability of reentrant spiral waves: a simulation study Am J Physiol Heart Circ Physiol, January 1, 1999; 276(1): H269 - H283. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Mandapati, Y. Asano, W. T. Baxter, R. Gray, J. Davidenko, and J. Jalife Quantification of Effects of Global Ischemia on Dynamics of Ventricular Fibrillation in Isolated Rabbit Heart Circulation, October 20, 1998; 98(16): 1688 - 1696. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. A. Athill, T. Ikeda, Y.-H. Kim, T.-J. Wu, M. C. Fishbein, H. S. Karagueuzian, and P.-S. Chen Transmembrane Potential Properties at the Core of Functional Reentrant Wave Fronts in Isolated Canine Right Atria Circulation, October 13, 1998; 98(15): 1556 - 1567. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. C. Skanes, R. Mandapati, O. Berenfeld, J. M. Davidenko, and J. Jalife Spatiotemporal Periodicity During Atrial Fibrillation in the Isolated Sheep Heart Circulation, September 22, 1998; 98(12): 1236 - 1248. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Lee, G. Morley, Q. Huang, A. Fischer, S. Seiler, J. W. Horner, S. Factor, D. Vaidya, J. Jalife, and G. I. Fishman Conditional lineage ablation to model human diseases PNAS, September 15, 1998; 95(19): 11371 - 11376. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Medkour, A. E. Becker, K. Khalife, and J. Billette Anatomic and Functional Characteristics of a Slow Posterior AV Nodal Pathway : Role in Dual-Pathway Physiology and Reentry Circulation, July 14, 1998; 98(2): 164 - 174. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. J. Janse, T. Opthof, and A. G. Kleber Animal models of cardiac arrhythmias Cardiovasc Res, July 1, 1998; 39(1): 165 - 177. [Full Text] [PDF]
|
|
|
|
|
|
O. Berenfeld and J. Jalife Purkinje-Muscle Reentry as a Mechanism of Polymorphic Ventricular Arrhythmias in a 3-Dimensional Model of the Ventricles Circ. Res., June 1, 1998; 82(10): 1063 - 1077. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Ikeda, M. Yashima, T. Uchida, D. Hough, M. C. Fishbein, W. J. Mandel, P.-S. Chen, and H. S. Karagueuzian Attachment of Meandering Reentrant Wave Fronts to Anatomic Obstacles in the Atrium : Role of the Obstacle Size Circ. Res., November 19, 1997; 81(5): 753 - 764. [Abstract] [Full Text]
|
|
|
|
|
|
T. Ikeda, L. Czer, A. Trento, C. Hwang, J. J. C. Ong, D. Hough, M. C. Fishbein, W. J. Mandel, H. S. Karagueuzian, and P.-S. Chen \E Induction of Meandering Functional Reentrant Wave Front in Isolated Human Atrial Tissues Circulation, November 4, 1997; 96(9): 3013 - 3020. [Abstract] [Full Text]
|
|
|
|
|
|
R. A. Gray, G. Ayers, and J. Jalife Video Imaging of Atrial Defibrillation in the Sheep Heart Circulation, February 18, 1997; 95(4): 1038 - 1047. [Abstract] [Full Text]
|
|
|
|
|
|
R. A. Gray, A. M. Pertsov, and J. Jalife Incomplete Reentry and Epicardial Breakthrough Patterns During Atrial Fibrillation in the Sheep Heart Circulation, November 15, 1996; 94(10): 2649 - 2661. [Abstract] [Full Text]
|
|
|
|
|
|
D. M. Roden, R. Lazzara, M. Rosen, P. J. Schwartz, J. Towbin, and G. M. Vincent Multiple Mechanisms in the Long-QT Syndrome: Current Knowledge, Gaps, and Future Directions Circulation, October 15, 1996; 94(8): 1996 - 2012. [Abstract] [Full Text]
|
|
|
|
|
|
Y. Cheng, K. A. Mowrey, V. Nikolski, P. J. Tchou, and I. R. Efimov Mechanisms of shock-induced arrhythmogenesis during acute global ischemia Am J Physiol Heart Circ Physiol, June 1, 2002; 282(6): H2141 - H2151. [Abstract] [Full Text] [PDF]
|
|