The significant effect of the choice of ionic current integration method in cardiac electro‐physiological simulations

Finite element (FE) cardiac electro-physiology solvers commonly have ionic current determined at mesh nodes but required element interiors. We consider two interpolation approaches: (i) ionic current interpolation (ICI), where nodal ionic currents are linearly interpolated into the element and (ii) state variable interpolation (SVI), where cell model state variables are interpolated instead, from which the ionic current is evaluated. We explain why SVI leads to a method which is massively more computationally demanding than ICI (more than might originally be expected), and then demonstrate that the difference in results can be surprisingly large even on what are generally considered suitably fine meshes. We explain why the conduction velocity in ICI simulations is generally too large, identify how ICI can give ‘accidentally’ accurate conduction velocities through two particular sources of error balancing, and illustrate how the difference between ICI and SVI can be huge in anisotropic problems. We also characterize the ICI/SVI difference over a range of cell models, in terms of model upstroke-velocity and formulation of the fast sodium current. Finally, we propose and evaluate a hybrid method which provides the accuracy of SVI, while retaining the efficiency of ICI. Copyright © 2011 John Wiley & Sons, Ltd.

[1]  A. Garfinkel,et al.  An advanced algorithm for solving partial differential equation in cardiac conduction , 1999, IEEE Transactions on Biomedical Engineering.

[2]  Israel A. Byrd,et al.  Comparison of Conventional and Biventricular Antitachycardia Pacing in a Geometrically Realistic Model of the Rabbit Ventricle , 2004, Journal of cardiovascular electrophysiology.

[3]  J. Trangenstein,et al.  Operator splitting and adaptive mesh refinement for the Luo-Rudy I model , 2004 .

[4]  H Zhang,et al.  Mathematical models of action potentials in the periphery and center of the rabbit sinoatrial node. , 2000, American journal of physiology. Heart and circulatory physiology.

[5]  Joseph L Greenstein,et al.  Mathematical simulations of ligand-gated and cell-type specific effects on the action potential of human atrium. , 2008, Progress in biophysics and molecular biology.

[6]  D. Noble,et al.  A model of the single atrial cell: relation between calcium current and calcium release , 1990, Proceedings of the Royal Society of London. B. Biological Sciences.

[7]  Andrew J. Pullan,et al.  Solving the cardiac bidomain equations for discontinuous conductivities , 2006, IEEE Transactions on Biomedical Engineering.

[8]  D. Bers,et al.  A novel computational model of the human ventricular action potential and Ca transient. , 2010, Journal of Molecular and Cellular Cardiology.

[9]  Alan Garny,et al.  A numerical guide to the solution of the bi-domain equations of cardiac electrophysiology. , 2010, Progress in biophysics and molecular biology.

[10]  Yoram Rudy,et al.  Rate Dependence and Regulation of Action Potential and Calcium Transient in a Canine Cardiac Ventricular Cell Model , 2004, Circulation.

[11]  Robert F Gilmour,et al.  Ionic mechanism of electrical alternans. , 2002, American journal of physiology. Heart and circulatory physiology.

[12]  A V Panfilov,et al.  A guide to modelling cardiac electrical activity in anatomically detailed ventricles. , 2008, Progress in biophysics and molecular biology.

[13]  D. Beuckelmann,et al.  Simulation study of cellular electric properties in heart failure. , 1998, Circulation research.

[14]  J. Restrepo,et al.  A rabbit ventricular action potential model replicating cardiac dynamics at rapid heart rates. , 2007, Biophysical journal.

[15]  S. Göktepe,et al.  Computational modeling of electrocardiograms: A finite element approach toward cardiac excitation , 2010 .

[16]  J. Clark,et al.  Mathematical model of an adult human atrial cell: the role of K+ currents in repolarization. , 1998, Circulation research.

[17]  J. Clark,et al.  A mathematical model of a rabbit sinoatrial node cell. , 1994, The American journal of physiology.

[18]  N Lovell,et al.  Ion currents underlying sinoatrial node pacemaker activity: a new single cell mathematical model. , 1996, Journal of theoretical biology.

[19]  Yoram Rudy,et al.  Properties and ionic mechanisms of action potential adaptation, restitution, and accommodation in canine epicardium. , 2009, American journal of physiology. Heart and circulatory physiology.

[20]  Edward Vigmond,et al.  Towards predictive modelling of the electrophysiology of the heart , 2009, Experimental physiology.

[21]  Rodrigo Weber dos Santos,et al.  Parallel multigrid preconditioner for the cardiac bidomain model , 2004, IEEE Transactions on Biomedical Engineering.

[22]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[23]  R. Winslow,et al.  Mechanisms of altered excitation-contraction coupling in canine tachycardia-induced heart failure, II: model studies. , 1999, Circulation research.

[24]  Alexander G. Fletcher,et al.  Chaste: A test-driven approach to software development for biological modelling , 2009, Comput. Phys. Commun..

[25]  G Plank,et al.  Solvers for the cardiac bidomain equations. , 2008, Progress in biophysics and molecular biology.

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

[27]  Gernot Plank,et al.  Development of an anatomically detailed MRI-derived rabbit ventricular model and assessment of its impact on simulations of electrophysiological function , 2009, American journal of physiology. Heart and circulatory physiology.

[28]  Jonathan P. Whiteley,et al.  An Efficient Numerical Technique for the Solution of the Monodomain and Bidomain Equations , 2006, IEEE Transactions on Biomedical Engineering.

[29]  D DiFrancesco,et al.  A model of cardiac electrical activity incorporating ionic pumps and concentration changes. , 1985, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[30]  D. Noble,et al.  Distribution of a Persistent Sodium Current Across the Ventricular Wall in Guinea Pigs , 2000, Circulation research.

[31]  Eric Kerfoot,et al.  Verification of cardiac tissue electrophysiology simulators using an N-version benchmark , 2011, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[32]  Donald M Bers,et al.  A mathematical treatment of integrated Ca dynamics within the ventricular myocyte. , 2004, Biophysical journal.

[33]  T. Lincoln,et al.  Myosin phosphatase regulatory pathways: different functions or redundant functions? , 2007, Circulation research.

[34]  K. T. ten Tusscher,et al.  Alternans and spiral breakup in a human ventricular tissue model. , 2006, American journal of physiology. Heart and circulatory physiology.

[35]  D. Noble,et al.  The Role of Sodium ‐ Calcium Exchange during the Cardiac Action Potential a , 1991, Annals of the New York Academy of Sciences.

[36]  Antonis A Armoundas,et al.  Mechanisms of Abnormal Calcium Homeostasis in Mutations Responsible for Catecholaminergic Polymorphic Ventricular Tachycardia , 2007, Circulation research.

[37]  D. Noble,et al.  A model for human ventricular tissue. , 2004, American journal of physiology. Heart and circulatory physiology.

[38]  Natalia Trayanova,et al.  Defibrillation of the heart: insights into mechanisms from modelling studies , 2006, Experimental physiology.

[39]  R. Winslow,et al.  A computational model of the human left-ventricular epicardial myocyte. , 2004, Biophysical journal.

[40]  D. Noble,et al.  A model of sino-atrial node electrical activity based on a modification of the DiFrancesco-Noble (1984) equations , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[41]  Yoram Rudy,et al.  Regulation of Ca2+ and electrical alternans in cardiac myocytes: role of CAMKII and repolarizing currents. , 2007, American journal of physiology. Heart and circulatory physiology.

[42]  Leon Espinosa L'échange Na+-Ca2+ dans l'hypertrophie ventriculaire d'altitude chez le rat : étude électrophysiologique et utilisation du modèle "oxsoft heart" , 1998 .

[43]  D. Noble,et al.  Excitation-contraction coupling and extracellular calcium transients in rabbit atrium: reconstruction of basic cellular mechanisms , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[44]  Denis Noble,et al.  Contributions of HERG K+ current to repolarization of the human ventricular action potential. , 2008, Progress in biophysics and molecular biology.