Towards an efficient computational strategy for electro-activation in cardiac mechanics

Abstract The computational modelling of the heart motion within a cardiac cycle is an extremely challenging problem due to (a) the complex multi-scale interaction that takes place between the electrophysiology and electrochemistry at cellular level and the macro-scale response of the heart muscle, and (b) the large deformations and the strongly anisotropic and quasi-incompressible behaviour of the myocardium. These pose an extreme challenge to the scalability of electro-mechanical solvers due to the size and conditioning of the system of equations required to obtain accurate solutions, both in terms of wall deformation and transmembrane potential propagation. In the search towards an efficient modelling of electro-activation, this paper presents a coupled electromechanical computational framework whereby, first, we explore the use of an efficient stabilised low order tetrahedral Finite Element methodology and compare it against a very accurate super enhanced mixed formulation previously introduced by the authors in Garcia-Blanco et al. (2019) and, second, we exploit the use of tailor-made staggered and staggered linearised solvers in order to assess their feasibility against a fully monolithic approach. Through a comprehensive set of examples, culminating in a realistic ventricular geometry, we aim to put forward some suggestions regarding the level of discretisation and coupling required to ensure sufficiently reliable results yet with an affordable computational time.

[1]  P. Neff,et al.  Invariant formulation of hyperelastic transverse isotropy based on polyconvex free energy functions , 2003 .

[2]  Bradley J. Roth,et al.  A Bidomain Model for the Extracellular Potential and Magnetic Field of Cardiac Tissue , 1986, IEEE Transactions on Biomedical Engineering.

[3]  S. I. Solov’eva,et al.  Numerical Solution of the Inverse Problem for the Mathematical Model of Cardiac Excitation , 2016 .

[4]  Renato Perucchio,et al.  Modeling Heart Development , 2000 .

[5]  S. Allender,et al.  European cardiovascular disease statistics , 2008 .

[6]  Rogelio Ortigosa,et al.  A new framework for large strain electromechanics based on convex multi-variable strain energies: Finite Element discretisation and computational implementation , 2016 .

[7]  Gerhard A Holzapfel,et al.  Constitutive modelling of passive myocardium: a structurally based framework for material characterization , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[8]  Rogelio Ortigosa,et al.  On a tensor cross product based formulation of large strain solid mechanics , 2016 .

[9]  Stefano Zampini,et al.  Newton–Krylov-BDDC solvers for nonlinear cardiac mechanics , 2015 .

[10]  A. Hodgkin,et al.  Propagation of electrical signals along giant nerve fibres , 1952, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[11]  Peter Wriggers,et al.  Finite element formulations for large strain anisotropic material with inextensible fibers , 2016, Adv. Model. Simul. Eng. Sci..

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

[13]  P. Neff,et al.  A variational approach for materially stable anisotropic hyperelasticity , 2005 .

[14]  M. Courtemanche,et al.  Ionic mechanisms underlying human atrial action potential properties: insights from a mathematical model. , 1998, The American journal of physiology.

[15]  Mark Potse,et al.  A Comparison of Monodomain and Bidomain Reaction-Diffusion Models for Action Potential Propagation in the Human Heart , 2006, IEEE Transactions on Biomedical Engineering.

[16]  Alan Weinstein,et al.  Geometry, Mechanics, and Dynamics , 2002 .

[17]  B M Horácek,et al.  Computer model of excitation and recovery in the anisotropic myocardium. I. Rectangular and cubic arrays of excitable elements. , 1991, Journal of electrocardiology.

[18]  S. Yoshizawa,et al.  An Active Pulse Transmission Line Simulating Nerve Axon , 1962, Proceedings of the IRE.

[19]  Bruce H. Smaill,et al.  Structure and Function of the Diastolic Heart: Material Properties of Passive Myocardium , 1991 .

[20]  Y. Fung,et al.  Biomechanics: Mechanical Properties of Living Tissues , 1981 .

[21]  Rogelio Ortigosa,et al.  A computational framework for polyconvex large strain elasticity for geometrically exact beam theory , 2015, Computational Mechanics.

[22]  Michel Fortin,et al.  Mixed and Hybrid Finite Element Methods , 2011, Springer Series in Computational Mathematics.

[23]  Rogelio Ortigosa,et al.  A first order hyperbolic framework for large strain computational solid dynamics. Part I: Total Lagrangian isothermal elasticity , 2015 .

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

[25]  J. Ball Convexity conditions and existence theorems in nonlinear elasticity , 1976 .

[26]  R. Aliev,et al.  A simple two-variable model of cardiac excitation , 1996 .

[27]  Toshiaki Hisada,et al.  Multiphysics simulation of left ventricular filling dynamics using fluid-structure interaction finite element method. , 2004, Biophysical journal.

[28]  S. Göktepe,et al.  Computational modeling of chemo‐electro‐mechanical coupling: A novel implicit monolithic finite element approach , 2013, International journal for numerical methods in biomedical engineering.

[29]  B. Taccardi,et al.  Simulating patterns of excitation, repolarization and action potential duration with cardiac Bidomain and Monodomain models. , 2005, Mathematical biosciences.

[30]  R. FitzHugh Mathematical models of threshold phenomena in the nerve membrane , 1955 .

[31]  M. Nash,et al.  Electromechanical model of excitable tissue to study reentrant cardiac arrhythmias. , 2004, Progress in biophysics and molecular biology.

[32]  Ricardo Ruiz-Baier,et al.  A Three-dimensional Continuum Model of Active Contraction in Single Cardiomyocytes , 2015 .

[33]  Rogelio Ortigosa,et al.  A new framework for large strain electromechanics based on convex multi-variable strain energies: Conservation laws, hyperbolicity and extension to electro-magneto-mechanics , 2016 .

[34]  J. Humphrey,et al.  Determination of a constitutive relation for passive myocardium: I. A new functional form. , 1990, Journal of biomechanical engineering.

[35]  Edward J Vigmond,et al.  Effect of bundle branch block on cardiac output: a whole heart simulation study. , 2008, Progress in biophysics and molecular biology.

[36]  S. Göktepe,et al.  Electromechanics of the heart: a unified approach to the strongly coupled excitation–contraction problem , 2010 .

[37]  Rogelio Ortigosa,et al.  A computational framework for polyconvex large strain elasticity for geometrically exact beam theory , 2016 .

[38]  I. Babuska The finite element method with Lagrangian multipliers , 1973 .

[39]  Rogelio Ortigosa,et al.  A first order hyperbolic framework for large strain computational solid dynamics. Part II: Total Lagrangian compressible, nearly incompressible and truly incompressible elasticity , 2016 .

[40]  S. Göktepe,et al.  Computational modeling of electrochemical coupling: A novel finite element approach towards ionic models for cardiac electrophysiology , 2011 .

[41]  Alfio Quarteroni,et al.  Orthotropic active strain models for the numerical simulation of cardiac biomechanics , 2012, International journal for numerical methods in biomedical engineering.

[42]  Alfio Quarteroni,et al.  Integrated Heart—Coupling multiscale and multiphysics models for the simulation of the cardiac function , 2017 .

[43]  Hilmi Demiray On the Constitutive Equations of Biological Materials , 1975 .

[44]  Rogelio Ortigosa,et al.  A new framework for large strain electromechanics based on convex multi-variable strain energies: Variational formulation and material characterisation , 2016 .

[45]  Julius M. Guccione,et al.  Finite Element Modeling of Ventricular Mechanics , 1991 .

[46]  Rogelio Ortigosa,et al.  A new computational framework for electro-activation in cardiac mechanics , 2019, Computer Methods in Applied Mechanics and Engineering.

[47]  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.

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

[49]  Ellen Kuhl,et al.  The Living Heart Project: A robust and integrative simulator for human heart function. , 2014, European journal of mechanics. A, Solids.

[50]  Antonio J. Gil,et al.  Solution of an industrially relevant coupled magneto–mechanical problem set on an axisymmetric domain , 2016 .

[51]  Reint Boer,et al.  Vektor- und Tensorrechnung für Ingenieure , 1982 .

[52]  Rogelio Ortigosa,et al.  A curvilinear high order finite element framework for electromechanics: From linearised electro-elasticity to massively deformable dielectric elastomers , 2018 .

[53]  A. Quarteroni,et al.  Thermodynamically consistent orthotropic activation model capturing ventricular systolic wall thickening in cardiac electromechanics , 2014 .

[54]  David Gavaghan,et al.  A Bidomain Model of the Ventricular Specialized Conduction System of the Heart , 2012, SIAM J. Appl. Math..

[55]  Alfio Quarteroni,et al.  FaCSI: A block parallel preconditioner for fluid-structure interaction in hemodynamics , 2016, J. Comput. Phys..

[56]  F. Fenton,et al.  Minimal model for human ventricular action potentials in tissue. , 2008, Journal of theoretical biology.

[57]  J. Ball,et al.  W1,p-quasiconvexity and variational problems for multiple integrals , 1984 .

[58]  J. Wong,et al.  Generating fibre orientation maps in human heart models using Poisson interpolation , 2014, Computer methods in biomechanics and biomedical engineering.

[59]  F. Fenton,et al.  Vortex dynamics in three-dimensional continuous myocardium with fiber rotation: Filament instability and fibrillation. , 1998, Chaos.

[60]  H. Huxley,et al.  Structural Basis of the Cross-Striations in Muscle , 1953, Nature.

[61]  S. Göktepe,et al.  Computational modeling of passive myocardium , 2011 .

[62]  T. Hughes,et al.  A new finite element formulation for computational fluid dynamics: V. Circumventing the Babuscka-Brezzi condition: A stable Petrov-Galerkin formulation of , 1986 .

[63]  A. McCulloch,et al.  Modelling cardiac mechanical properties in three dimensions , 2001, Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[64]  C. Luo,et al.  A dynamic model of the cardiac ventricular action potential. II. Afterdepolarizations, triggered activity, and potentiation. , 1994, Circulation research.

[65]  P. Hunter,et al.  Computational Mechanics of the Heart , 2000 .

[66]  Cosmin G. Petra,et al.  An Augmented Incomplete Factorization Approach for Computing the Schur Complement in Stochastic Optimization , 2014, SIAM J. Sci. Comput..

[67]  A. J. Gil,et al.  A unified approach for a posteriori high-order curved mesh generation using solid mechanics , 2016 .