Spatial and temporal organization in ventricular fibrillation.

Ventricular fibrillation (VF) is the leading heart rhythm alteration that results in sudden cardiac death, yet the detailed mechanisms of the arrhythmia remain elusive. Fibrillation has been defined as "turbulent" cardiac electrical activity, which conjures up the idea of totally random and disorganized activation of the ventricles. I review theoretical concepts and recently published results based on a newly developed algorithm, "two-dimensional phase mapping," which demonstrates that VF is not random and may be analyzed quantitatively. The approach is based on video imaging of voltage-sensitive dye fluorescence to record transmembrane potential simultaneously from 20,000 sites on the epicardial surface of rabbit and sheep ventricles. During VF, activity shows a strong periodic component centered near approximately 500 beats/min. Phase maps reveal that VF depends on the organization of electrical waves around a small number of "phase singularities" that have relatively short lifespans and form as a result of interactions of wavefronts with obstacles in their paths. Overall, the evidence demonstrates that there is a high degree of temporal and spatial organization in cardiac fibrillation. The results may pave the way for a better understanding of the mechanisms of VF in normal, as well as in diseased, hearts.

[1]  G. Mitchell,et al.  Long QT and ventricular arrhythmias in transgenic mice expressing the N terminus and first transmembrane segment of a voltage-gated potassium channel. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[2]  C. Starmer,et al.  Wavelet formation in excitable cardiac tissue: the role of wavefront-obstacle interactions in initiating high-frequency fibrillatory-like arrhythmias. , 1996, Biophysical journal.

[3]  M S Spach,et al.  The Functional Role of Structural Complexities in the Propagation of Depolarization in the Atrium of the Dog: Cardiac Conduction Disturbances Due to Discontinuities of Effective Axial Resistivity , 1982, Circulation research.

[4]  G. Breithardt,et al.  Genetic basis and molecular mechanism for idiopathic ventricular fibrillation , 1998, Nature.

[5]  M. Allessie,et al.  Circus Movement in Rabbit Atrial Muscle as a Mechanism of Tachycardia: II. The Role of Nonuniform Recovery of Excitability in the Occurrence of Unidirectional Block, as Studied with Multiple Microelectrodes , 1976, Circulation research.

[6]  F. Witkowski,et al.  Activation Patterns During Ventricular Fibrillation a , 1990, Annals of the New York Academy of Sciences.

[7]  Arun V. Holden,et al.  Resonant drift of an autowave vortex in a bounded medium , 1993 .

[8]  J Jalife,et al.  Drifting vortices of electrical waves underlie ventricular fibrillation in the rabbit heart. , 1996, Acta physiologica Scandinavica.

[9]  James P. Keener,et al.  Rotating Spiral Waves Created by Geometry , 1994, Science.

[10]  A. Winfree.  When time breaks down , 1987 .

[11]  L. J. Leon,et al.  Spatiotemporal evolution of ventricular fibrillation , 1998, Nature.

[12]  P. Touboul,et al.  Atrial Arrhythmias: Current Concepts and Management , 1990 .

[13]  D. Zipes,et al.  Radiofrequency catheter ablation of the atria eliminates pacing-induced sustained atrial fibrillation and reduces connexin 43 in dogs. , 1997, Circulation.

[14]  M Delmar,et al.  Characterization of Conduction in the Ventricles of Normal and Heterozygous Cx43 Knockout Mice Using Optical Mapping , 1999, Journal of cardiovascular electrophysiology.

[15]  A. Winfree.  Electrical instability in cardiac muscle: phase singularities and rotors. , 1989, Journal of theoretical biology.

[16]  V. Krinsky.  Mathematical models of cardiac arrhythmias (spiral waves). , 1978, Pharmacology & therapeutics. Part B: General & systematic pharmacology.

[17]  M. Allessie,et al.  Circus Movement in Rabbit Atrial Muscle as a Mechanism of Tachycardia , 1973, Circulation research.

[18]  I R Efimov,et al.  Virtual electrode-induced phase singularity: a basic mechanism of defibrillation failure. , 1998, Circulation research.

[19]  R. Gray,et al.  Spatial and temporal organization during cardiac fibrillation , 1998, Nature.

[20]  J Jalife,et al.  Vortex shedding as a precursor of turbulent electrical activity in cardiac muscle. , 1996, Biophysical journal.

[21]  S M Dillon,et al.  Anisotropic Reentry in the Epicardial Border Zone of Myocardial Infarcts a , 1990, Annals of the New York Academy of Sciences.

[22]  R. A. Gray,et al.  Mechanisms of Cardiac Fibrillation , 1995, Science.

[23]  W. Baxter,et al.  Spiral waves of excitation underlie reentrant activity in isolated cardiac muscle. , 1993, Circulation research.

[24]  M. Allessie,et al.  Altered Pattern of Connexin40 Distribution in Persistent Atrial Fibrillation in the Goat , 1998, Journal of cardiovascular electrophysiology.

[25]  N. El-Sherif,et al.  Canine Ventricular Arrhythmias in the Late Myocardial Infarction Period , 1981, Circulation research.

[26]  W. Rheinboldt,et al.  A COMPUTER MODEL OF ATRIAL FIBRILLATION. , 1964, American heart journal.

[27]  W. Baxter,et al.  Stationary and drifting spiral waves of excitation in isolated cardiac muscle , 1992, Nature.

[28]  Pérez-Muñuzuri,et al.  Parametric resonance of a vortex in an active medium. , 1994, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[29]  E. Ermakova,et al.  On the diffraction of autowaves , 1990 .

[30]  J J Heger,et al.  Sudden cardiac death. , 1998, Circulation.

[31]  J Jalife,et al.  Reentry and fibrillation in the mouse heart. A challenge to the critical mass hypothesis. , 1999, Circulation research.

[32]  José Jalife.  Mathematical approaches to cardiac arrhythmias. , 1990, Annals of the New York Academy of Sciences.

[33]  J. .. Abildskov,et al.  AN EXPERIMENTAL STUDY OF CONCEALED CONDUCTION. , 1964, American heart journal.

[34]  D. Rosenbaum,et al.  Modulation of ventricular repolarization by a premature stimulus. Role of epicardial dispersion of repolarization kinetics demonstrated by optical mapping of the intact guinea pig heart. , 1996, Circulation research.

[35]  Allessie,et al.  Circus movement in rabbit atrial muscle as a mechanism of tachycardia. III. The "leading circle" concept: a new model of circus movement in cardiac tissue without the involvement of an anatomical obstacle. , 1977, Circulation research.

[36]  G. Fishman,et al.  Conditional lineage ablation to model human diseases. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[37]  A V Holden,et al.  Design principles of a low voltage cardiac defibrillator based on the effect of feedback resonant drift. , 1994, Journal of theoretical biology.

[38]  J Jalife,et al.  Wave-front curvature as a cause of slow conduction and block in isolated cardiac muscle. , 1994, Circulation research.

[39]  A. Panfilov,et al.  Nonstationary vortexlike reentrant activity as a mechanism of polymorphic ventricular tachycardia in the isolated rabbit heart. , 1995, Circulation.

[40]  A. M. Pertsov,et al.  Autowave Approaches to Cessation of Reentrant Arrhythmias , 1990, Annals of the New York Academy of Sciences.

[41]  M S Spach,et al.  Multiple regional differences in cellular properties that regulate repolarization and contraction in the right atrium of adult and newborn dogs. , 1989, Circulation research.

[42]  M S Spach,et al.  Interaction of Inhomogeneities of Repolarization With Anisotropic Propagation in Dog Atria: Mechanism for Both Preventing and Initiating Reentry , 1989, Circulation research.

[43]  J. Jalife,et al.  Cardiac Electrophysiology: From Cell to Bedside , 1990 .

[44]  M. Allessie,et al.  Atrial Electrophysiologic Remodeling: Another Vicious Circle? , 1998, Journal of cardiovascular electrophysiology.