Three-dimensional computational modeling of multiple deformable cells flowing in microvessels.

Three-dimensional (3D) computational modeling and simulation are presented on the motion of a large number of deformable cells in microchannels. The methodology is based on an immersed boundary method, and the cells are modeled as liquid-filled elastic capsules. The model retains two important features of the blood flow in the microcirculation, that is, the particulate nature of blood and deformation of the erythrocytes. The tank-treading and tumbling motion and the lateral migration, as observed for erythrocytes in dilute suspension, are briefly discussed. We then present results on the motion of multiple cells in semidense suspension and study how their collective dynamics leads to various physiologically relevant processes such as the development of the cell-free layer and the Fahraeus-Lindqvist effect. We analyze the 3D trajectory and velocity fluctuations of individual cell in the suspension and the plug-flow velocity profile as functions of the cell deformability, hematocrit, and vessel size. The numerical results allow us to directly obtain various microrheological data, such as the width of the cell-free layer, and the variation in the apparent blood viscosity and hematocrit over the vessel cross section. We then use these results to calculate the core and plasma-layer viscosity and show that the two-phase (or core-annular) model of blood flow in microvessels underpredicts the blood velocity obtained in the simulations by as much as 40%. Based on a posteriori analysis of the simulation data, we develop a three-layer model of blood flow by taking into consideration the smooth variation in viscosity and hematocrit across the interface of the cell-free layer and the core. We then show that the blood velocity predicted by the three-layer model agrees very well with that obtained from the simulations.

[1]  E. J. Hinch,et al.  Collision of two deformable drops in shear flow , 1997, Journal of Fluid Mechanics.

[2]  Prosenjit Bagchi,et al.  Mesoscale simulation of blood flow in small vessels. , 2007, Biophysical journal.

[3]  A. Pries,et al.  Two-Dimensional Simulation of Red Blood Cell Deformation and Lateral Migration in Microvessels , 2007, Annals of Biomedical Engineering.

[4]  D. Barthès-Biesel,et al.  Motion of a deformable capsule through a hyperbolic constriction , 1994, Journal of Fluid Mechanics.

[5]  Dominique Barthès-Biesel,et al.  Hydrodynamic interaction between two identical capsules in simple shear flow , 2007, Journal of Fluid Mechanics.

[6]  Saroja Ramanujan,et al.  Deformation of liquid capsules enclosed by elastic membranes in simple shear flow: large deformations and the effect of fluid viscosities , 1998, Journal of Fluid Mechanics.

[7]  C. Peskin Numerical analysis of blood flow in the heart , 1977 .

[8]  Magalie Faivre,et al.  Swinging of red blood cells under shear flow. , 2007, Physical review letters.

[9]  G. Cokelet,et al.  Decreased Hydrodynamic Resistance in the Two‐Phase Flow of Blood Through Small Vertical Tubes at Low Flow Rates , 1991, Circulation research.

[10]  T W Secomb,et al.  Motion of nonaxisymmetric red blood cells in cylindrical capillaries. , 1989, Journal of biomechanical engineering.

[11]  G. B. Jeffery The motion of ellipsoidal particles immersed in a viscous fluid , 1922 .

[12]  T. Secomb Flow-dependent rheological properties of blood in capillaries. , 1987, Microvascular research.

[13]  Hong Zhao,et al.  A fixed-mesh method for incompressible flow-structure systems with finite solid deformations , 2008, J. Comput. Phys..

[14]  Dominique Barthès-Biesel,et al.  The time-dependent deformation of a capsule freely suspended in a linear shear flow , 1981, Journal of Fluid Mechanics.

[15]  A. Pries,et al.  Blood viscosity in tube flow: dependence on diameter and hematocrit. , 1992, The American journal of physiology.

[16]  G. Karniadakis,et al.  Blood flow velocity effects and role of activation delay time on growth and form of platelet thrombi , 2006, Proceedings of the National Academy of Sciences.

[17]  T W Secomb,et al.  Red blood cells and other nonspherical capsules in shear flow: oscillatory dynamics and the tank-treading-to-tumbling transition. , 2007, Physical review letters.

[18]  Y C Fung,et al.  Theory of sheet flow in lung alveoli. , 1969, Journal of applied physiology.

[19]  C. Pozrikidis,et al.  Numerical Simulation of Cell Motion in Tube Flow , 2005, Annals of Biomedical Engineering.

[20]  Sai K. Doddi,et al.  Lateral migration of a capsule in a plane Poiseuille flow in a channel , 2008 .

[21]  C. Peskin,et al.  A computational fluid dynamics of `clap and fling' in the smallest insects , 2005, Journal of Experimental Biology.

[22]  C. Coulliette,et al.  Motion of an array of drops through a cylindrical tube , 1998, Journal of Fluid Mechanics.

[23]  R. Skalak,et al.  Flow of axisymmetric red blood cells in narrow capillaries , 1986, Journal of Fluid Mechanics.

[24]  J. Freund Leukocyte Margination in a Model Microvessel , 2006 .

[25]  C. Pozrikidis,et al.  Numerical Simulation of the Flow-Induced Deformation of Red Blood Cells , 2003, Annals of Biomedical Engineering.

[26]  A. Popel,et al.  Large deformation of red blood cell ghosts in a simple shear flow. , 1998, Physics of fluids.

[27]  L. Munn,et al.  Particulate nature of blood determines macroscopic rheology: a 2-D lattice Boltzmann analysis. , 2005, Biophysical journal.

[28]  Robin Fåhræus,et al.  THE VISCOSITY OF THE BLOOD IN NARROW CAPILLARY TUBES , 1931 .

[29]  R. Skalak,et al.  Strain energy function of red blood cell membranes. , 1973, Biophysical journal.

[30]  J. Tang,et al.  Large deformation finite element analysis of non-linear viscoelastic membranes with reference to thermoforming , 1993 .

[31]  D. Juric,et al.  A front-tracking method for the computations of multiphase flow , 2001 .

[32]  A. Pries,et al.  Corrections and Retraction , 2004 .

[33]  Michael L. Smith,et al.  Estimation of viscosity profiles using velocimetry data from parallel flows of linearly viscous fluids: application to microvascular haemodynamics , 2004, Journal of Fluid Mechanics.

[34]  S. Suresh,et al.  Spectrin-level modeling of the cytoskeleton and optical tweezers stretching of the erythrocyte. , 2005, Biophysical journal.

[35]  From two-dimensional model networks to microcapsules , 2002 .

[36]  Cyrus K Aidun,et al.  Cluster size distribution and scaling for spherical particles and red blood cells in pressure-driven flows at small Reynolds number. , 2006, Physical review letters.

[37]  C. Smith,et al.  Anionic amino acid uptake by microvillous membrane vesicles from human placenta. , 1989, The American journal of physiology.

[38]  R. Skalak,et al.  Motion of a tank-treading ellipsoidal particle in a shear flow , 1982, Journal of Fluid Mechanics.

[39]  A. Popel,et al.  A two-phase model for flow of blood in narrow tubes with increased effective viscosity near the wall. , 2001, Biorheology.

[40]  Aleksander S Popel,et al.  Temporal and spatial variations of cell-free layer width in arterioles. , 2007, American journal of physiology. Heart and circulatory physiology.

[41]  Aleksander S Popel,et al.  Microcirculation and Hemorheology. , 2005, Annual review of fluid mechanics.

[42]  M. Dupin,et al.  Modeling the flow of dense suspensions of deformable particles in three dimensions. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[43]  Frédéric Risso,et al.  Experimental investigation of a bioartificial capsule flowing in a narrow tube , 2006, Journal of Fluid Mechanics.

[44]  Aleksander S Popel,et al.  An immersed boundary lattice Boltzmann approach to simulate deformable liquid capsules and its application to microscopic blood flows , 2007, Physical biology.