Spontaneous termination of reentrant activity under myocardial acute ischemia: Role of cellular conductivity and its relation to ischemic heterogeneities

Abstract The relation between reentrant activity and occurrence of cardiac arrhythmias still is a topic of intensive investigation. Reentries are strictly related to and enhanced by the complex structure of cardiac tissue, characterized by multi-sized electrophysiological and spatial heterogeneities. However, the structure and the function of the tissue can sometimes also promote phenomena of spontaneous termination of waves. The role played by the tissue in this scenario is not well understood and yet under investigation. In this study, we implemented a bidomain formulation of the phase I of the Luo and Rudy action potential model in 2D under ischemic conditions. We investigate how the size of ischemic heterogeneities and tissue conduction properties may affect the system dynamics and drive it towards maintenance of reentrant activity or quiescence. The main findings show that: (a) for the stability of the waves, changes of conductivity in the intracellular space are more critical than alterations in the extracellular space; (b) the maintenance or the self-termination of pinned spirals is strongly dependent not only on the size of the heterogeneities but also on the degree of intracellular anisotropy. These findings confirm and extend results obtained from previous investigations. In addition, since experimental values of conductivity tensors reported in the literature are not consistent, an overview of possible scenarios arising from a broader range of assumed anisotropy values is provided in relation to different sizes of ischemic heterogeneities. In this perspective, simulations are shown to compare the impact of different degrees of tissue anisotropy on wave dynamics.

[1]  A. M. Scher,et al.  Influence of Cardiac Fiber Orientation on Wavefront Voltage, Conduction Velocity, and Tissue Resistivity in the Dog , 1979, Circulation research.

[2]  L. Clerc Directional differences of impulse spread in trabecular muscle from mammalian heart. , 1976, The Journal of physiology.

[3]  A. Winfree,et al.  Sudden Cardiac Death: A Problem in Topology , 1983 .

[4]  J. Wikswo,et al.  Virtual electrodes in cardiac tissue: a common mechanism for anodal and cathodal stimulation. , 1995, Biophysical journal.

[5]  M. Mansour,et al.  Mother rotors and fibrillatory conduction: a mechanism of atrial fibrillation. , 2002, Cardiovascular research.

[6]  D. Durrer,et al.  Tissue Osmolality, Cell Swelling, and Reperfusion in Acute Regional Myocardial Ischemia in the Isolated Porcine Heart , 1981, Circulation research.

[7]  Elizabeth M Cherry,et al.  Mechanisms of ventricular arrhythmias: a dynamical systems-based perspective. , 2012, American journal of physiology. Heart and circulatory physiology.

[8]  Z. Qu Critical mass hypothesis revisited: role of dynamical wave stability in spontaneous termination of cardiac fibrillation. , 2006, American journal of physiology. Heart and circulatory physiology.

[9]  A ROSENBLUETH,et al.  The mathematical formulation of the problem of conduction of impulses in a network of connected excitable elements, specifically in cardiac muscle. , 1946, Archivos del Instituto de Cardiologia de Mexico.

[10]  Niels F Otani,et al.  Theory of action potential wave block at-a-distance in the heart. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[11]  P F Cranefield,et al.  Reentrant excitation as a cause of cardiac arrhythmias. , 1978, The American journal of physiology.

[12]  Z. Qu Chaos in the genesis and maintenance of cardiac arrhythmias. , 2011, Progress in biophysics and molecular biology.

[13]  L. J. Leon,et al.  Simulation of two-dimensional anisotropic cardiac reentry: Effects of the wavelength on the reentry characteristics , 1994, Annals of Biomedical Engineering.

[14]  Jorge Elorza,et al.  Shock-induced termination of reentrant cardiac arrhythmias: comparing monophasic and biphasic shock protocols. , 2013, Chaos.

[15]  Alan Garfinkel,et al.  DYNAMICS OF REENTRY AROUND A CIRCULAR OBSTACLE IN CARDIAC TISSUE , 1998 .

[16]  G. Moe,et al.  On the multiple wavelet hypothesis o f atrial fibrillation. , 1962 .

[17]  Walter E. Garrey THE NATURE OF FIBRILLARY CONTRACTION OF THE HEART.—ITS RELATION TO TISSUE MASS AND FORM , 1914 .

[18]  J. Saffitz Regulation of intercellular coupling in acute and chronic heart disease. , 2000, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[19]  A. Kléber,et al.  Electrical constants of arterially perfused rabbit papillary muscle. , 1987, The Journal of physiology.

[20]  Alexander V Panfilov,et al.  Organization of Ventricular Fibrillation in the Human Heart , 2007, Circulation research.

[21]  A Garfinkel,et al.  Spatiotemporal heterogeneity in the induction of ventricular fibrillation by rapid pacing: importance of cardiac restitution properties. , 1999, Circulation research.

[22]  N. Trayanova,et al.  Wave Front–Obstacle Interactions in Cardiac Tissue: A Computational Study , 2004, Annals of Biomedical Engineering.

[23]  Stanley Nattel,et al.  Wave block formation in homogeneous excitable media following premature excitations: dependence on restitution relations. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[24]  D. Janzing,et al.  A single-shot measurement of the energy of product states in a translation invariant spin chain can replace any quantum computation , 2007, 0710.1615.

[25]  Natalia Trayanova,et al.  Analysis of Electrically Induced Reentrant Circuits in a Sheet of Myocardium , 2003, Annals of Biomedical Engineering.

[26]  Stanley Nattel,et al.  Atrial fibrillation pathophysiology: implications for management. , 2011, Circulation.

[27]  Frank B. Sachse,et al.  Computational Cardiology , 2004, Lecture Notes in Computer Science.

[28]  J E Saffitz,et al.  Dephosphorylation and Intracellular Redistribution of Ventricular Connexin43 During Electrical Uncoupling Induced by Ischemia , 2000, Circulation research.

[29]  A. Garfinkel,et al.  From Pulsus to Pulseless: The Saga of Cardiac Alternans , 2006, Circulation research.

[30]  D. Rosenbaum,et al.  Mechanism linking T-wave alternans to the genesis of cardiac fibrillation. , 1999, Circulation.

[31]  A. Kleber,et al.  Gap junctions, slow conduction, and ventricular tachycardia after myocardial infarction. , 2012, Journal of the American College of Cardiology.

[32]  Olivier Bernus,et al.  Alternating conduction in the ischaemic border zone as precursor of reentrant arrhythmias: a simulation study. , 2005, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[33]  A. M. Scher,et al.  Effect of Tissue Anisotropy on Extracellular Potential Fields in Canine Myocardium in Situ , 1982, Circulation research.

[34]  Y. Rudy,et al.  Electrophysiologic effects of acute myocardial ischemia: a theoretical study of altered cell excitability and action potential duration. , 1997, Cardiovascular research.

[35]  A. Garfinkel,et al.  Mechanisms of Discordant Alternans and Induction of Reentry in Simulated Cardiac Tissue , 2000, Circulation.

[36]  Bradley J. Roth,et al.  The electrical potential produced by a strand of cardiac muscle: A bidomain analysis , 2006, Annals of Biomedical Engineering.

[37]  F. Fenton,et al.  Visualization of spiral and scroll waves in simulated and experimental cardiac tissue , 2008 .

[38]  Alan Garfinkel,et al.  A Tale of Two Fibrillations , 2003, Circulation.

[39]  Nicholas S Peters,et al.  Architectural Correlates of Myocardial Conduction: Changes to the Topography of Cellular Coupling, Intracellular Conductance, and Action Potential Propagation with Hypertrophy in Guinea-Pig Ventricular Myocardium , 2014, Circulation. Arrhythmia and electrophysiology.

[40]  P. Wolf,et al.  Mechanism of Ventricular Vulnerability to Single Premature Stimuli in Open‐Chest Dogs , 1988, Circulation research.

[41]  Steven Berkov Hypoxic Pulmonary Vasoconstriction in the Rat: The Necessary Role of Angiotensin II , 1974 .

[42]  C. Luo,et al.  A model of the ventricular cardiac action potential. Depolarization, repolarization, and their interaction. , 1991, Circulation research.

[43]  B. Roth Nonsustained Reentry Following Successive Stimulation of Cardiac Tissue Through a Unipolar Electrode , 1997, Journal of cardiovascular electrophysiology.