Coupling multi-physics models to cardiac mechanics.

We outline and review the mathematical framework for representing mechanical deformation and contraction of the cardiac ventricles, and how this behaviour integrates with other processes crucial for understanding and modelling heart function. Building on general conservation principles of space, mass and momentum, we introduce an arbitrary Eulerian-Lagrangian framework governing the behaviour of both fluid and solid components. Exploiting the natural alignment of cardiac mechanical properties with the tissue microstructure, finite deformation measures and myocardial constitutive relations are referred to embedded structural axes. Coupling approaches for solving this large deformation mechanics framework with three dimensional fluid flow, coronary hemodynamics and electrical activation are described. We also discuss the potential of cardiac mechanics modelling for clinical applications.

[1]  Y. Fung,et al.  Transmural Myocardial Deformation in the Canine Left Ventricle: Normal in Vivo Three‐Dimensional Finite Strains , 1985, Circulation research.

[2]  Roy C. P. Kerckhoffs,et al.  Effect of transmurally heterogeneous myocyte excitation–contraction coupling on canine left ventricular electromechanics , 2009, Experimental physiology.

[3]  C. Peskin,et al.  A three-dimensional computational method for blood flow in the heart. II. contractile fibers , 1989 .

[4]  Harold T. Dodge,et al.  Left Ventricular Tension and Stress in Man , 1963, Circulation research.

[5]  Andrew D. McCulloch,et al.  Effect of Laminar Orthotropic Myofiber Architecture on Regional Stress and Strain in the Canine Left Ventricle , 2000 .

[6]  J. Halleux,et al.  An arbitrary lagrangian-eulerian finite element method for transient dynamic fluid-structure interactions , 1982 .

[7]  D. Peric,et al.  A computational framework for fluid–structure interaction: Finite element formulation and applications , 2006 .

[8]  Antonio Huerta,et al.  Viscous flow with large free surface motion , 1988 .

[9]  P J Hunter,et al.  Analytical models of propagation in excitable cells. , 1975, Progress in biophysics and molecular biology.

[10]  Theo Arts,et al.  A model of the mechanics of the left ventricle. , 1979, Annals of biomedical engineering.

[11]  H. T. ter Keurs,et al.  Tension Development and Sarcomere Length in Rat Cardiac Trabeculae: Evidence of Length‐Dependent Activation , 1980, Circulation research.

[12]  C. Peskin,et al.  A three-dimensional computational method for blood flow in the heart. 1. Immersed elastic fibers in a viscous incompressible fluid , 1989 .

[13]  P. Hunter,et al.  Modelling the mechanical properties of cardiac muscle. , 1998, Progress in biophysics and molecular biology.

[14]  H Suga,et al.  The effects of cardiac infarction on realistic three-dimensional left ventricular blood ejection. , 1996, Journal of biomechanical engineering.

[15]  D N Firmin,et al.  The influence of inflow boundary conditions on intra left ventricle flow predictions. , 2003, Journal of biomechanical engineering.

[16]  R. van Heuningen,et al.  Tension development and sarcomere length in rat cardiac trabeculae. Evidence of length-dependent activation. , 1980 .

[17]  D Ghista,et al.  In vivo stresses in the human left ventricular wall: analysis accounting for the irregular 3-dimensional geometry and comparison with idealised geometry analyses. , 1972, Journal of biomechanics.

[18]  A P Yoganathan,et al.  A computational study of a thin-walled three-dimensional left ventricle during early systole. , 1994, Journal of biomechanical engineering.

[19]  I. Sheinman,et al.  Nonlinear incompressible finite element for simulating loading of cardiac tissue--Part II: Three dimensional formulation for thick ventricular wall segments. , 1988, Journal of biomechanical engineering.

[20]  A. Katz Physiology of the heart , 1977 .

[21]  Quan Long,et al.  Combined CFD/MRI Analysis of Left Ventricular Flow , 2004, Medical Imaging and Augmented Reality.

[22]  Kevin F. Augenstein,et al.  Method and apparatus for soft tissue material parameter estimation using tissue tagged Magnetic Resonance Imaging. , 2005, Journal of biomechanical engineering.

[23]  E. McVeigh,et al.  Electromechanics of paced left ventricle simulated by straightforward mathematical model: comparison with experiments. , 2005, American journal of physiology. Heart and circulatory physiology.

[24]  M P Nash,et al.  Drift and breakup of spiral waves in reaction–diffusion–mechanics systems , 2007, Proceedings of the National Academy of Sciences.

[25]  A. Quarteroni,et al.  Numerical Approximation of Partial Differential Equations , 2008 .

[26]  Purva Joshi,et al.  Surface imaging microscopy using an ultramiller for large volume 3D reconstruction of wax‐ and resin‐embedded tissues , 2007, Microscopy research and technique.

[27]  David Nordsletten,et al.  Coupling contraction, excitation, ventricular and coronary blood flow across scale and physics in the heart , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[28]  David Nordsletten,et al.  A non-conforming monolithic finite element method for problems of coupled mechanics , 2010, J. Comput. Phys..

[29]  Robert C Gorman,et al.  Effect of ventricular size and patch stiffness in surgical anterior ventricular restoration: a finite element model study. , 2005, The Annals of thoracic surgery.

[30]  H. Oertel,et al.  Fluid-Structure Coupled CFD Simulation of the Left Ventricular Flow During Filling Phase , 2005, Annals of Biomedical Engineering.

[31]  P. J. Hunter,et al.  Generation of an Anatomically Based Geometric Coronary Model , 2004, Annals of Biomedical Engineering.

[32]  Roy C. P. Kerckhoffs,et al.  Homogeneity of Cardiac Contraction Despite Physiological Asynchrony of Depolarization: A Model Study , 2003, Annals of Biomedical Engineering.

[33]  R Krams,et al.  Varying elastance concept may explain coronary systolic flow impediment. , 1989, The American journal of physiology.

[34]  Arthur E. Weyman,et al.  Numerical modeling of ventricular filling , 2006, Annals of Biomedical Engineering.

[35]  Miguel Cervera,et al.  On the computational efficiency and implementation of block-iterative algorithms for nonlinear coupled Problems , 1996 .

[36]  C. Gans,et al.  Biomechanics: Motion, Flow, Stress, and Growth , 1990 .

[37]  I. LeGrice,et al.  Shear properties of passive ventricular myocardium. , 2002, American journal of physiology. Heart and circulatory physiology.

[38]  J. M. Crolet,et al.  Numerical simulation of the blood-wall interaction in the human left ventricle , 1998 .

[39]  Martin J Bishop,et al.  Soft Tissue Modelling of Cardiac Fibres for Use in Coupled Mechano-Electric Simulations , 2007, Bulletin of mathematical biology.

[40]  K. Bathe,et al.  Finite element developments for general fluid flows with structural interactions , 2004 .

[41]  J. Rice,et al.  Approximate model of cooperative activation and crossbridge cycling in cardiac muscle using ordinary differential equations. , 2008, Biophysical journal.

[42]  A. E. Ehret,et al.  A polyconvex anisotropic strain–energy function for soft collagenous tissues , 2006, Biomechanics and modeling in mechanobiology.

[43]  A. McCulloch,et al.  Finite element stress analysis of left ventricular mechanics in the beating dog heart. , 1995, Journal of biomechanics.

[44]  Y. Huo,et al.  A hybrid one-dimensional/Womersley model of pulsatile blood flow in the entire coronary arterial tree. , 2007, American journal of physiology. Heart and circulatory physiology.

[45]  A. Grimm,et al.  Deformation of the diastolic left ventricle--II. Nonlinear geometric effects. , 1974, Journal of biomechanics.

[46]  Jürgen Hennig,et al.  Fluid-dynamic modeling of the human left ventricle: methodology and application to surgical ventricular reconstruction. , 2009, The Annals of thoracic surgery.

[47]  N. Westerhof,et al.  How to Quantify Pump Function of the Heart: The Value of Variables Derived from Measurements on Isolated Muscle , 1979, Circulation research.

[48]  Jordi Alastruey,et al.  Theoretical models for coronary vascular biomechanics: progress & challenges. , 2011, Progress in biophysics and molecular biology.

[49]  A. McCulloch,et al.  Passive material properties of intact ventricular myocardium determined from a cylindrical model. , 1991, Journal of biomechanical engineering.

[50]  Kawal S. Rhode,et al.  The Importance of Model Parameters and Boundary Conditions in Whole Organ Models of Cardiac Contraction , 2009, FIMH.

[51]  P. Tallec,et al.  Load and motion transfer algorithms for fluid/structure interaction problems with non-matching discrete interfaces: Momentum and energy conservation, optimal discretization and application to aeroelasticity , 1998 .

[52]  David Nordsletten,et al.  Conservative and non-conservative arbitrary Lagrangian-Eulerian forms for ventricular flows , 2008 .

[53]  P. Hunter,et al.  New developments in a strongly coupled cardiac electromechanical model. , 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.

[54]  J. S. Janicki,et al.  Ejection pressure and the diastolic left ventricular pressure-volume relation. , 1977, The American journal of physiology.

[55]  P. Hunter,et al.  Laminar structure of the heart: a mathematical model. , 1997, The American journal of physiology.

[56]  R H Woods,et al.  A Few Applications of a Physical Theorem to Membranes in the Human Body in a State of Tension. , 1892, Journal of anatomy and physiology.

[57]  Toshiaki Hisada,et al.  The looped heart does not save energy by maintaining the momentum of blood flowing in the ventricle. , 2008, American journal of physiology. Heart and circulatory physiology.

[58]  P. Hunter,et al.  Integration from proteins to organs: the Physiome Project , 2003, Nature Reviews Molecular Cell Biology.

[59]  H Zhang,et al.  Models of cardiac tissue electrophysiology: progress, challenges and open questions. , 2011, Progress in biophysics and molecular biology.

[60]  Gianni Pedrizzetti,et al.  Model and influence of mitral valve opening during the left ventricular filling. , 2003, Journal of biomechanics.

[61]  Guang-Zhong Yang,et al.  Progress Towards Patient-Specific Computational Flow Modeling of the Left Heart via Combination of Magnetic Resonance Imaging with Computational Fluid Dynamics , 2004, Annals of Biomedical Engineering.

[62]  P. Hunter,et al.  Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog. , 1995, The American journal of physiology.

[63]  Hervé Delingette,et al.  An electromechanical model of the heart for image analysis and simulation , 2006, IEEE Transactions on Medical Imaging.

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

[65]  J. Ross,et al.  Fiber Orientation in the Canine Left Ventricle during Diastole and Systole , 1969, Circulation research.

[66]  D. L. Bassett,et al.  An engineering analysis of myocardial fiber orientation in pig's left ventricle in systole , 1966 .

[67]  P. Hunter,et al.  A quantitative analysis of cardiac myocyte relaxation: a simulation study. , 2006, Biophysical journal.

[68]  Herbert Oertel,et al.  Modelling the human cardiac fluid mechanics , 2005 .

[69]  Dimitris N. Metaxas,et al.  Patient-Specific Analysis of Left Ventricular Blood Flow , 1998, MICCAI.

[70]  J D Laird,et al.  Diastolic‐Systolic Coronary Flow Differences are Caused by Intramyocardial Pump Action in the Anesthetized Dog , 1981, Circulation research.

[71]  Andrew D McCulloch,et al.  Electromechanical model of cardiac resynchronization in the dilated failing heart with left bundle branch block. , 2003, Journal of electrocardiology.

[72]  J Lee,et al.  Development and application of a one-dimensional blood flow model for microvascular networks , 2008, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[73]  A. D. Gosman,et al.  Computational Flow Modeling of the Left Ventricle Based on In Vivo MRI Data: Initial Experience , 2001, Annals of Biomedical Engineering.

[74]  Theo Arts,et al.  Optimizing ventricular fibers: uniform strain or stress, but not ATP consumption, leads to high efficiency. , 2002, American journal of physiology. Heart and circulatory physiology.

[75]  E S Kirk,et al.  Inhibition of Coronary Blood Flow by a Vascular Waterfall Mechanism , 1975, Circulation research.

[76]  Henggui Zhang,et al.  Cardiac cell modelling: observations from the heart of the cardiac physiome project. , 2011, Progress in biophysics and molecular biology.

[77]  Mirza Faisal Beg,et al.  Measuring and Mapping Cardiac Fiber and Laminar Architecture Using Diffusion Tensor MR Imaging , 2005, Annals of the New York Academy of Sciences.

[78]  C. Peskin,et al.  A three-dimensional computer model of the human heart for studying cardiac fluid dynamics , 2000, SIGGRAPH 2000.

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

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

[81]  I. Mirsky,et al.  Ventricular and arterial wall stresses based on large deformation analyses. , 1973, Biophysical journal.

[82]  Gianni Pedrizzetti,et al.  Nature optimizes the swirling flow in the human left ventricle. , 2005, Physical review letters.

[83]  R. Natarajan,et al.  Finite-element method of stress analysis in the human left ventricular layered wall structure , 2006, Medical and Biological Engineering and Computing.

[84]  A P Yoganathan,et al.  Computational modeling of left heart diastolic function: examination of ventricular dysfunction. , 2000, Journal of biomechanical engineering.

[85]  C. Peskin,et al.  Modelling cardiac fluid dynamics and diastolic function , 2001, Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[86]  J. Hyvärinen,et al.  An Arbitrary Lagrangian-Eulerian finite element method , 1998 .

[87]  F. Yin,et al.  A multiaxial constitutive law for mammalian left ventricular myocardium in steady-state barium contracture or tetanus. , 1998, Journal of biomechanical engineering.

[88]  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.

[89]  H. Suga,et al.  Ventricular systolic pressure-volume area as predictor of cardiac oxygen consumption. , 1981, The American journal of physiology.

[90]  Alistair A. Young,et al.  Parameter distribution models for estimation of population based left ventricular deformation using sparse fiducial markers , 2005, IEEE Transactions on Medical Imaging.

[91]  R S Reneman,et al.  Porous medium finite element model of the beating left ventricle. , 1992, The American journal of physiology.

[92]  Y C Fung,et al.  Mathematical representation of the mechanical properties of the heart muscle. , 1970, Journal of biomechanics.

[93]  S. Niederer,et al.  An improved numerical method for strong coupling of excitation and contraction models in the heart. , 2008, Progress in biophysics and molecular biology.

[94]  A. Grimm,et al.  Finite‐Element Model for the Mechanical Behavior of the Left Ventricle: PREDICTION OF DEFORMATION IN THE POTASSIUM-ARRESTED RAT HEART , 1972, Circulation research.

[95]  Gianni Pedrizzetti,et al.  Fluid dynamics of the left ventricular filling in dilated cardiomyopathy. , 2002, Journal of biomechanics.

[96]  F W Prinzen,et al.  Transmural gradients of cardiac myofiber shortening in aortic valve stenosis patients using MRI tagging. , 2002, American journal of physiology. Heart and circulatory physiology.

[97]  H. T. ter Keurs,et al.  Modelling and measuring electromechanical coupling in the rat heart , 2009, Experimental physiology.

[98]  Roy C. P. Kerckhoffs,et al.  Timing of Depolarization and Contraction in the Paced Canine Left Ventricle: , 2003, Journal of cardiovascular electrophysiology.

[99]  Nicolas P Smith,et al.  A computational study of the interaction between coronary blood flow and myocardial mechanics. , 2004, Physiological measurement.

[100]  Gianni Pedrizzetti,et al.  Three-dimensional filling flow into a model left ventricle , 2005, Journal of Fluid Mechanics.

[101]  P. Hunter,et al.  Ventricular mechanics in diastole: material parameter sensitivity. , 2003, Journal of biomechanics.

[102]  Daniel B Ennis,et al.  Myofiber angle distributions in the ovine left ventricle do not conform to computationally optimized predictions. , 2008, Journal of biomechanics.

[103]  R S Reneman,et al.  Dependence of local left ventricular wall mechanics on myocardial fiber orientation: a model study. , 1992, Journal of biomechanics.

[104]  A D McCulloch,et al.  Homogenization modeling for the mechanics of perfused myocardium. , 1998, Progress in biophysics and molecular biology.

[105]  Andrew J. Pullan,et al.  An Anatomically Based Model of Transient Coronary Blood Flow in the Heart , 2002, SIAM J. Appl. Math..

[106]  Klaus-Jürgen Bathe,et al.  Benchmark problems for incompressible fluid flows with structural interactions , 2007 .

[107]  Frederick J. Vetter,et al.  Three-Dimensional Stress and Strain in Passive Rabbit Left Ventricle: A Model Study , 2000, Annals of Biomedical Engineering.

[108]  Alistair A. Young,et al.  Modelling passive diastolic mechanics with quantitative MRI of cardiac structure and function , 2009, Medical Image Anal..

[109]  Shunichi Homma,et al.  Parameterization of Left Ventricular Wall Motion for Detection of Regional Ischemia , 2005, Annals of Biomedical Engineering.

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

[111]  Toshiaki Hisada,et al.  Computer Simulation of Blood Flow, Left Ventricular Wall Motion and Their Interrelationship by Fluid-Structure Interaction Finite Element Method , 2002 .

[112]  Steven Niederer,et al.  The Role of the Frank–Starling Law in the Transduction of Cellular Work to Whole Organ Pump Function: A Computational Modeling Analysis , 2009, PLoS Comput. Biol..

[113]  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.

[114]  Toshiaki Hisada,et al.  Analysis of fluid-structure interaction problems with structural buckling and large domain changes by ALE finite element method , 2001 .

[115]  L. E. Malvern Introduction to the mechanics of a continuous medium , 1969 .

[116]  R. Nicolaides Existence, Uniqueness and Approximation for Generalized Saddle Point Problems , 1982 .

[117]  P. Rautaharju,et al.  Stress distribution within the left ventricular wall approximated as a thick ellipsoidal shell. , 1968, American heart journal.

[118]  C. Peskin Flow patterns around heart valves: A numerical method , 1972 .