Ordering and arrangement of deformed red blood cells in flow through microcapillaries

The shapes and alignment of elastic vesicles similar to red blood cells (RBCs) in cylindrical capillary flow are investigated by mesoscopic hydrodynamic simulations. We study the collective flow behavior of many RBCs, where the capillary diameter is comparable to the diameter of the RBCs. Two essential control parameters are the RBC volume fraction (the tube hematocrit, HT), and the suspension flow velocity. Depending on HT, flow velocity and capillary radius, the RBC suspension exhibits a disordered phase and two distinct ordered phases, consisting of a single file of parachute-shaped cells and a zigzag arrangement of slipper-shaped cells, respectively. We argue that thermal fluctuations, included in the simulation method, coupled to hydrodynamic flows are important contributors to the RBC morphology. We examine the changes to the phase structures when the capillary diameter and the material properties (bending rigidity κ and stretching modulus μ) of the model RBCs are varied, constructing phase diagrams for each case. We focus on capillary diameters, which range from about 1.0 to about 1.4 times the RBC long diameter. For the smallest capillary diameter, the single-file arrangement dominates; for the largest diameter, the ordered zigzag arrangement begins to loose its stability and alternates with an asymmetric structure with two lanes of differently oriented cells. In simulations with long capillaries, the coexistence of different phases can be observed.

[1]  R. Fåhraeus THE SUSPENSION STABILITY OF THE BLOOD , 1929 .

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

[3]  S Chien,et al.  Effects of hematocrit and plasma proteins on human blood rheology at low shear rates. , 1966, Journal of applied physiology.

[4]  R. Whitmore A theory of blood flow in small vessels. , 1967, Journal of applied physiology.

[5]  Henry Wang,et al.  Viscous flow in a cylindrical tube containing a line of spherical particles , 1969, Journal of Fluid Mechanics.

[6]  R. Skalak,et al.  Deformation of Red Blood Cells in Capillaries , 1969, Science.

[7]  H. S. Lew,et al.  Plug effect of erythrocytes in capillary blood vessels. , 1970, Biophysical journal.

[8]  R. Skalak,et al.  Stokes flow in a cylindrical tube containing a line of spheroidal particles , 1970 .

[9]  S Chien,et al.  Effect of hematocrit and rouleaux on apparent viscosity in capillaries. , 1972, Biorheology.

[10]  W. Helfrich Elastic Properties of Lipid Bilayers: Theory and Possible Experiments , 1973, Zeitschrift fur Naturforschung. Teil C: Biochemie, Biophysik, Biologie, Virologie.

[11]  P. Gaehtgens,et al.  Motion, deformation, and interaction of blood cells and plasma during flow through narrow capillary tubes. , 1980, Blood cells.

[12]  R Skalak,et al.  A two-dimensional model for capillary flow of an asymmetric cell. , 1982, Microvascular research.

[13]  G Gaspari,et al.  The aspherity of random walks , 1986 .

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

[15]  R. Skalak,et al.  Numerical study of asymmetric flows of red blood cells in capillaries. , 1988, Microvascular research.

[16]  R. Skalak,et al.  Stability of particle motions in a narrow channel flow. , 1989, Biorheology.

[17]  R Skalak Poiseuille Medal lecture. Capillary flow: past, present, and future. , 1990, Biorheology.

[18]  G. Gompper,et al.  The conformation of fluid membranes: Monte Carlo simulations. , 1992, Science.

[19]  R. Bruinsma RHEOLOGY AND SHAPE TRANSITIONS OF VESICLES UNDER CAPILLARY FLOW , 1996 .

[20]  M. Soutani,et al.  Deformation of Erythrocytes in Microvessels and Glass Capillaries: Effects of Erythrocyte Deformability , 1996, Microcirculation.

[21]  Gerhard Gompper,et al.  Network models of fluid, hexatic and polymerized membranes , 1997 .

[22]  Dominique Barthès-Biesel,et al.  Axisymmetric motion of capsules through cylindrical channels , 1997, Journal of Fluid Mechanics.

[23]  D. Boal,et al.  Simulations of the erythrocyte cytoskeleton at large deformation. II. Micropipette aspiration. , 1998, Biophysical journal.

[24]  A. Malevanets,et al.  Mesoscopic model for solvent dynamics , 1999 .

[25]  P. Olla SIMPLIFIED MODEL FOR RED CELL DYNAMICS IN SMALL BLOOD VESSELS , 1998, chao-dyn/9805007.

[26]  Isabelle Cantat,et al.  Lift Force and Dynamical Unbinding of Adhering Vesicles under Shear Flow , 1999 .

[27]  H Minamitani,et al.  Direct measurement of erythrocyte deformability in diabetes mellitus with a transparent microchannel capillary model and high-speed video camera system. , 2001, Microvascular research.

[28]  T. Ihle,et al.  Erratum: Multi-particle collision dynamics: Flow around a circular and a square cylinder , 2001, cond-mat/0110148.

[29]  R. Mukhopadhyay,et al.  Stomatocyte–discocyte–echinocyte sequence of the human red blood cell: Evidence for the bilayer– couple hypothesis from membrane mechanics , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  G. Gompper,et al.  Mesoscopic solvent simulations: multiparticle-collision dynamics of three-dimensional flows. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[31]  H. Diamant,et al.  Screened hydrodynamic interaction in a narrow channel. , 2002, Physical review letters.

[32]  Witold Dzwinel,et al.  Dynamical clustering of red blood cells in capillary vessels , 2003, Journal of molecular modeling.

[33]  David R Nelson,et al.  Virus shapes and buckling transitions in spherical shells. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[34]  Witold Dzwinel,et al.  A discrete-particle model of blood dynamics in capillary vessels. , 2003, Journal of colloid and interface science.

[35]  J. F. Ryder,et al.  Transport coefficients of a mesoscopic fluid dynamics model , 2003, cond-mat/0302451.

[36]  Hiroshi Noguchi,et al.  Fluid vesicles with viscous membranes in shear flow. , 2004, Physical review letters.

[37]  Thomas Podgorski,et al.  Deformation of vesicles flowing through capillaries , 2004 .

[38]  Hiroshi Noguchi,et al.  Dynamics of fluid vesicles in shear flow: effect of membrane viscosity and thermal fluctuations. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[39]  H. Noguchi,et al.  Shape transitions of fluid vesicles and red blood cells in capillary flows. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[41]  C. Pozrikidis Axisymmetric motion of a file of red blood cells through capillaries , 2005 .

[42]  M. Abkarian,et al.  Dynamics of vesicles in a wall-bounded shear flow. , 2005, Biophysical journal.

[43]  Hiroshi Noguchi,et al.  Particle-based mesoscale hydrodynamic techniques , 2006, cond-mat/0610890.

[44]  Yaling Liu,et al.  Rheology of red blood cell aggregation by computer simulation , 2006, J. Comput. Phys..

[45]  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.

[46]  R. Kapral Multiparticle Collision Dynamics: Simulation of Complex Systems on Mesoscales , 2008 .

[47]  H. Diamant Hydrodynamic interaction in confined geometries , 2008, 0812.4971.

[48]  W. Zimmermann,et al.  Lateral migration of a two-dimensional vesicle in unbounded Poiseuille flow. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[49]  R. Winkler,et al.  Multi-Particle Collision Dynamics -- a Particle-Based Mesoscale Simulation Approach to the Hydrodynamics of Complex Fluids , 2008, 0808.2157.

[50]  Sai K. Doddi,et al.  Three-dimensional computational modeling of multiple deformable cells flowing in microvessels. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[51]  V. Martinelli,et al.  Red blood cell deformation in microconfined flow , 2009 .

[52]  J. Clausen,et al.  Simulating deformable particle suspensions using a coupled lattice-Boltzmann and finite-element method , 2009, Journal of Fluid Mechanics.

[53]  J. McWhirter,et al.  Flow-induced clustering and alignment of vesicles and red blood cells in microcapillaries , 2009, Proceedings of the National Academy of Sciences.

[54]  George Em Karniadakis,et al.  A multiscale red blood cell model with accurate mechanics, rheology, and dynamics. , 2010, Biophysical journal.

[55]  G. Karniadakis,et al.  Blood Flow and Cell‐Free Layer in Microvessels , 2010, Microcirculation.

[56]  Hong Zhao,et al.  A spectral boundary integral method for flowing blood cells , 2010, J. Comput. Phys..

[57]  J. McWhirter,et al.  Deformation and clustering of red blood cells in microcapillary flows , 2011 .

[58]  J. Freund,et al.  Cellular flow in a small blood vessel , 2010, Journal of Fluid Mechanics.

[59]  Gerhard Gompper,et al.  Predicting human blood viscosity in silico , 2011, Proceedings of the National Academy of Sciences.

[60]  C. Misbah,et al.  Red blood cell clustering in Poiseuille microcapillary flow , 2012 .

[61]  A. Thomas,et al.  Memristor-based neural networks , 2013 .

[62]  Emilio Molina,et al.  Summary and Discussion , 2014 .