Transmural Variation and Anisotropy of Microvascular Flow Conductivity in the Rat Myocardium

Transmural variations in the relationship between structural and fluid transport properties of myocardial capillary networks are determined via continuum modeling approaches using recent three-dimensional (3D) data on the microvascular structure. Specifically, the permeability tensor, which quantifies the inverse of the blood flow resistivity of the capillary network, is computed by volume-averaging flow solutions in synthetic networks with geometrical and topological properties derived from an anatomically-detailed microvascular data set extracted from the rat myocardium. Results show that the permeability is approximately ten times higher in the principal direction of capillary alignment (the “longitudinal” direction) than perpendicular to this direction, reflecting the strong anisotropy of the microvascular network. Additionally, a 30% increase in capillary diameter from subepicardium to subendocardium is shown to translate to a 130% transmural rise in permeability in the longitudinal capillary direction. This result supports the hypothesis that perfusion is preferentially facilitated during diastole in the subendocardial microvasculature to compensate for the severely-reduced systolic perfusion in the subendocardium.

[1]  A. Pries,et al.  Microvascular blood viscosity in vivo and the endothelial surface layer. , 2005, American journal of physiology. Heart and circulatory physiology.

[2]  Nicolas P Smith,et al.  Estimation of Blood Flow Rates in Large Microvascular Networks , 2012, Microcirculation.

[3]  A. McCulloch,et al.  Transmural distribution of capillary morphology as a function of coronary perfusion pressure in the resting canine heart. , 1995, Microvascular research.

[4]  I. E. Vignon-Clementel,et al.  A poroelastic model valid in large strains with applications to perfusion in cardiac modeling , 2010 .

[5]  P A Lachenbruch,et al.  Quantitative Changes in the Capillary Bed during Developing, Peak, and Stabilized Cardiac Hypertrophy in the Spontaneously Hypertensive Rat , 1982, Circulation research.

[6]  James B. Bassingthwaighte,et al.  Advection and Diffusion of Substances in Biological Tissues With Complex Vascular Networks , 2000, Annals of Biomedical Engineering.

[7]  G. S. Kassab,et al.  Analysis of coronary blood flow interaction with myocardial mechanics based on anatomical models , 2001, Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[8]  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.

[9]  Noboru Kaneko,et al.  Three-dimensional reconstruction of the human capillary network and the intramyocardial micronecrosis. , 2011, American journal of physiology. Heart and circulatory physiology.

[10]  Maria Siebes,et al.  Coronary pressure-flow relations as basis for the understanding of coronary physiology. , 2012, Journal of molecular and cellular cardiology.

[11]  Rebecca J. Shipley,et al.  Multiscale Modelling of Fluid and Drug Transport in Vascular Tumours , 2010, Bulletin of mathematical biology.

[12]  T. Secomb,et al.  Theoretical Simulation of Oxygen Transport to Brain by Networks of Microvessels: Effects of Oxygen Supply and Demand on Tissue Hypoxia , 2000, Microcirculation.

[13]  Maria Siebes,et al.  3D Imaging of vascular networks for biophysical modeling of perfusion distribution within the heart. , 2013, Journal of biomechanics.

[14]  S. J. Elliott,et al.  The H2O2‐Generating Enzyme, Xanthine Oxidase, Decreases Luminal Ca2+ Content of the IP3‐Sensitive Ca2+ Store in Vascular Endothelial Cells , 1995, Microcirculation.

[15]  Ghassan S Kassab,et al.  A hemodynamic analysis of coronary capillary blood flow based on anatomic and distensibility data. , 1999, American journal of physiology. Heart and circulatory physiology.

[16]  P. McDonagh,et al.  Microvascular Perfusion and Transport in the Diabetic Heart , 2000, Microcirculation.

[17]  R. Chabiniok,et al.  A novel porous mechanical framework for modelling the interaction between coronary perfusion and myocardial mechanics , 2012, Journal of biomechanics.

[18]  A. Groom,et al.  Capillary diameter and geometry in cardiac and skeletal muscle studied by means of corrosion casts. , 1983, Microvascular research.

[19]  A Haase,et al.  Myocardial perfusion and intracapillary blood volume in rats at rest and with coronary dilatation: MR imaging in vivo with use of a spin-labeling technique. , 2000, Radiology.

[20]  J I Hoffman,et al.  Cardiac contraction affects deep myocardial vessels predominantly. , 1991, The American journal of physiology.

[21]  J B Bassingthwaighte,et al.  Microvasculature of the dog left ventricular myocardium. , 1974, Microvascular research.

[22]  Jack Lee,et al.  Parameterisation of multi-scale continuum perfusion models from discrete vascular networks , 2012, Medical & Biological Engineering & Computing.

[23]  M. Marcus,et al.  Redistribution of coronary microvascular resistance produced by dipyridamole. , 1989, The American journal of physiology.

[24]  A. Popel,et al.  A computational study of the effect of capillary network anastomoses and tortuosity on oxygen transport. , 2000, Journal of theoretical biology.

[25]  Francis Cassot,et al.  Simulation study of brain blood flow regulation by intra-cortical arterioles in an anatomically accurate large human vascular network: Part I: Methodology and baseline flow , 2011, NeuroImage.

[26]  M. Toborg Zur Kenntnis der terminalen Strombahn im Myocard von Ratte und Katze , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[27]  J. Hoffman,et al.  Transmural myocardial perfusion. , 1987, Progress in cardiovascular diseases.

[28]  G S Kassab,et al.  Topology and dimensions of pig coronary capillary network. , 1994, The American journal of physiology.

[29]  Ayush Goyal,et al.  Multi-Scale Parameterisation of a Myocardial Perfusion Model Using Whole-Organ Arterial Networks , 2013, Annals of Biomedical Engineering.

[30]  J. Bassingthwaighte,et al.  Myocardial density and composition: a basis for calculating intracellular metabolite concentrations. , 2004, American journal of physiology. Heart and circulatory physiology.

[31]  Yasuo Ogasawara,et al.  Direct observation of epicardial coronary capillary hemodynamics during reactive hyperemia and during adenosine administration by intravital video microscopy. , 2005, American journal of physiology. Heart and circulatory physiology.

[32]  D. Poole,et al.  Capillary geometrical changes with fiber shortening in rat myocardium. , 1992, Circulation research.