Abstract
An investigation of margination dependence on hematocrit, platelet shape, and viscosity ratio of plasma to cytoplasm is presented. Whole blood is modeled as a suspension of deformable red blood cells (RBCs) and rigid platelets in a viscous liquid. The fluid phase is simulated using the lattice-Boltzmann method, the RBC membranes are modeled with a coarse-grained spectrin-link method, and the dynamics of rigid particles are updated using Newton’s equations of motion for axisymmetric shapes. The results emphasize that an increase in hematocrit increases the rate of margination. The viscosity ratio between the interior cytoplasm and suspending fluid can considerably alter the rate of margination. The aspect ratio of surrogate platelet particles influences the rate of margination as well. Spherical particles tend to migrate more quickly than disks. Highly viscous or rigid RBCs slow down margination.
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Abbreviations
- RBC:
-
Red blood cell
- LB:
-
Lattice-Boltzmann
- SL:
-
Spectrin link
References
Aarts, P. A. M. M., P. Steendijk, J. J. Sixma, and R. M. Heethaar. Fluid shear as a possible mechanism for platelet diffusivity in flowing blood. J. Biomech. 19(10):799–805, 1986.
Aarts, P. A., S. A. van den Brock, G. W. Prins, G. D. Kuiken, J. J. Sixma, and R. M. Heethaar. Blood platelets are concentrated near the wall and red blood cells, in the center in flowing blood. Arterioscl. Thrombosis Vasc. Biol. 8:819–824, 1988.
Aidun, C. K., and J. R. Clausen. Lattice-Boltzmann method for complex flows. Annu. Rev. Fluid Mech. 42:439–472, 2010.
Aidun, C. K., Y. Lu, and E.-J. Ding. Direct analysis of particulate suspensions with inertia using the discrete Boltzmann equation. J. Fluid Mech. 373:287–311, 1998.
Bark, D. L. The Hemodynamics During Thrombosis and Impact on Thrombus Growth. Atlanta: Biomedical/Mechanical Engineering, Georgia Institute of Technology, 2010.
Brady, J. F. Stokesian dynamics. Annu. Rev. Fluid Mech. 20:111–157, 1988.
Cadroy, Y., T. A. Horbett, and S. R. Hanson. Discrimination between platelet-mediated and coagulation-mediated mechanisms in a model of complex thrombus formation in vivo. J. Lab. Clin. Med. 113(4):436–448, 1989.
Chen, S., and G. D. Doolen. Lattice Boltzmann method for fluid flows. Annu. Rev. Fluid Mech. 30:329–364, 1998.
Clausen, J. R. The Effect of Particle Deformation on the Rheology of Noncolloidal Suspensions. Ph.D. Thesis, Georgia Institute of Technology, 2010.
Clausen, J. R., and C. K. Aidun. Galilean invariance in the lattice-Boltzmann method and its effect on the calculation of rheological properties in suspension. Int. J. Multiph. Flow 35:307–311, 2009.
Clausen, J. R., and C. K. Aidun. Capsule dynamics and rheology in shear flow: particle pressure and normal stress. Phys. Fluids 22(123302):1–11, 2010.
Clausen, J. R., D. A. Reasor, and C. K. Aidun. Parallel performance of a lattice-Boltzmann/finite element cellular blood flow solver on the IBM Blue Gene/P architecture. Comput. Phys. Commun. 181:1013–1020, 2010.
Clausen, J. R., D. A. Reasor, and C. K. Aidun. The rheology and microstructure of concentrated non-colloidal suspensions of deformable capsules. J. Fluid Mech. 685:202–234, 2011.
Crowl, L., and A. L. Fogelson. Analysis of mechanisms for platelet near-wall excess under arterial blood flow conditions. J. Fluid Mech. 676:348–375, 2011.
Dao, M., J. Li, and S. Suresh. Molecularly based analysis of deformation of spectrin network and human erythrocyte. Mater. Sci. Eng. C 26:1232–1244, 2006.
Davies, M. J., and A. C. Thomas. Thrombosis and acute coronary-artery lesions in sudden cardiac ischemic death. New Engl. J. Med. 310: 1137–1140, 1984.
Davies, M. J., and A. C. Thomas. Plaque fissuring–the cause of acute myocardial infarction, sudden ischaemic death, and crescendo angina. Br. Heart J. 53(4):363–373, 1985.
Diaz, A., and D. Barthès-Biesel. Entrance of bioartificial capsule in a pore. Comput. Model. Eng. Sci. 3:321–338, 2002.
Ding, E. J., and C. K. Aidun. The dynamics and scaling law for particles suspended in flow with inertia. J. Fluid Mech. 423:317–344, 2000.
Doddi, S. K., and P. Bagchi. Three-dimensional computational modeling of multiple deformable cells flowing in microvessels. Phys. Rev. E 79:046318, 2009.
Dupin, M. M., I. Halliday, C. M. Care, L. Alboul, and L. L. Munn. Modeling the flow of dense suspensions of deformable particles in three dimensions. Phys. Rev. E 75:066707, 2007.
Dupin, M. M., I. Halliday, C. M. Care, and L. L. Munn. Efficiency oriented, hybrid approach for modeling deformable particles in three dimensions. Prog. Comput. Fluid Dyn. 8(1–4):109–120, 2008.
Eckstein, E. C., A. W. Tilles, and F. J. Mellero. Conditions for the occurrence of large near-wall excesses of small particles during blood flow. Microvasc. Res. 36:31–39, 1988.
Fedosov, D. A., B. Caswell, and G. E. Karniadakis. A multiscale red blood cell model with accurate mechanics, rheology, and dynamics. Biophys. J. 98:2215–2225, 2010.
Freund, J. B., and M. M. Orescanin. Cellular flow in a small blood vessel. J. Fluid Mech. 671:466–490, 2011.
Ginzburg, I., and P. Adler. Boundary flow condition analysis for the 3-dimensional lattice Boltzmann Model. J. Phys. II 4:191–214, 1994.
Goldsmith, H., and J. Marlow. Flow behavior of erythrocytes. II. Particle motions in concentrated suspensions of ghost cells. J. Colloid Interface Sci. 7(2):383–407, 1979.
Haga, J., A. Beaudoin, J. White, and J. Stony. Quantification of the passive mechanical properties of the resting platelet. Ann. Biomed. Eng. 26:268–277, 1998.
Jackson, S. P. The growing complexity of platelet aggregation. Blood 109(12):5087–5095, 2007.
Junk, M., and W.-A. Jong. Rigorous Navier–Stokes limit of the lattice Boltzmann equation. Asympt. Anal. 35(2):165–185, 2003.
Junk, M., A. Klar, and L.-S. Luo. Asymptotic analysis of the lattice Boltzmann equation. J. Comput. Phys. 210(2):676–704, 2005.
Kumar, A., and M. D. Graham. Segregation by membrane rigidity in flowing binary suspensions of elastic capsules. Phys. Rev. E 84:066316, 2011.
Liu, Y., and W. K. Liu. Rheology of red blood cell aggregation by computer simulation. J. Comput. Phys. 220:139–154, 2006.
MacMeccan, R. M., J. R. Clausen, G. P. Neitzel, and C. K. Aidun. Simulating deformable particle suspensions using a coupled lattice-Boltzmann and finite-element method. J. Fluid Mech. 618:13–39, 2009.
Maxwell, M. J., E. Westein, W. S. Nesbitt, S. Giuliano, S. M. Dopheide, and S. P. Jackson. Identification of a 2-stage platelet aggregation process mediating shear-dependent thrombus formation. Blood 109:566–576, 2007.
McEver, R. P., and C. Zhu. Rolling cell adhesion. Annu. Rev. Cell Dev. Biol. 26:363–396, 2010.
McWhirter, J. L., H. Noguchi, and G. Gompper. Flow-induced clustering and alignment of vesicles and red blood cells in microcapillaries. PNAS 106(15):6039–6043, 2009.
Mody, N., and M. R. King. Platelet adhesive dynamics. Part I. Characterization of platelet hydrodynamic collisions and wall effects. Biophys. J. 95(5):2539–2555, 2008.
Nijhof, E. J., W. S. J. Uijttewal, and R. M. Heethaar. A Laser-Doppler system for measuring distributions of blood particles in narrow flow channels. IEEE Trans. Instrum. Meas. 43(3):430–435, 1994.
Noble, D. R., S. Chen, J. G. Georgiadis, and R. O. Buckius. A consistent hydrodynamic boundary condition for the lattice Boltzmann method. Phys. Fluids 7:203–209, 1995.
Pivkin, I. V., and G. E. Karniadakis. Accurate coarse-grained modeling of red blood cells. Phys. Rev. Lett. 101:118105, 2008.
Pozrikidis, C. Numerical simulation of the flow-induced deformation of red blood cells. Ann. Biomed. Eng. 31:1194–1205, 2003.
Pozrikidis, C. Axisymmetric motion of a file of red blood cells through capillaries. Phys. Fluids 17(031503):1–14, 2005.
Pozrikidis, C. Flipping of an adherent blood platelet over a substrate. J. Fluid Mech. 568:161–172, 2006.
Reasor, D. A., J. R. Clausen, and C. K. Aidun. Coupling the lattice-Boltzmann and spectrin-link methods for the direct numerical simulation of cellular blood flow. Int. J. Numer. Methods Fluids 68:767–781, 2012.
Segré, G., and A. Silberberg. Behavior of macroscopic rigid spheres in Poiseuille flow: Part 2. Experimental results and interpretation. J. Fluid Mech. 14(2):284–304, 1962.
Tilles, A. W., and E. C. Eckstein. The near-wall excess of platelet-sized particles in blood flow: its dependence on hematocrit and wall shear rate. Microvasc. Res. 33:218–223, 1987.
Tokarev, A. A., A. A. Butylin, and F. I. Ataullakhanov. Platelet adhesion from shear blood flow is controlled by near-wall rebounding collisions with erythrocytes. Biophys. J. 100(4):799–808, 2011.
Tsubota, K., and S. Wada. Elastic force of red blood cell membrane during tank-treading motion: consideration of the membrane’s natural state. Int. J. Mech. Sci. 52:356–364, 2010.
Turitto, V. T., and H. R. Baumgartner. Platelet deposition on subendothelium exposed to flowing blood: mathematical analysis of physical parameters. Trans. Am. Soc. Artif. Intern. Org. 21:593–601, 1975.
Turitto, V. T., A. M. Benis, and L. F. Leonard. Platelet diffusion in flowing blood. Ind. Eng. Chem. Fundam. 11(2):216–223, 1972.
Uijttewaal, W. S. J., E. J. Nijhof, and R. M. Heethaar. Lateral migration of blood cells and microspheres in two-dimensional Poiseuille flow: a Laser-Doppler study. J. Biomech. 27(1):35–42, 1994.
Womersley, J. R. Oscillatory Flow in Arteries: The Constrained Elastic Tube as a Model of Arterial Flow and Pulse Transmission. Technical Report, Aeronautical Research Laboratory, Wright Air Development Center, Dayton, OH, 1955.
Wu, J., and C. K. Aidun. Simulating 3D deformable particle suspensions using lattice Boltzmann method with discrete external boundary force. Int. J. Numer. Methods Fluids 62(7):765–783, 2009.
Yazdani, A. Z. K., and P. Bagchi. Phase diagram and breathing dynamics of a single red blood cell and a biconcave capsule in dilute shear flow. Phys. Rev. E 84:026314, 2011.
Zhang, J., P. C. Johnson, and A. S. Popel. An immersed boundary lattice Boltzmann approach to simulate deformable liquid capsules and its application to microscopic blood flows. Phys. Biol. 4:285–295, 2007.
Zhao, H., A. H. G. Isfahani, L. N. Olson, and J. B. Freund. A spectral boundary integral method for flowing blood cells. J. Comput. Phys. 229:3726–3744, 2010.
Zhao, R., M. V. Kameneva, and J. F. Antaki. Investigation of platelet margination phenomena at elevated shear stress. Biorheology 44:161–177, 2007.
Zhao, H., and E. S. G. Shaqfeh. Shear-induced platelet margination in a microchannel. Phys. Rev. E 83(061924):1–6, 2011.
Ziegler, D. P. Boundary conditions for lattice Boltzmann simulations. J. Stat. Phys. 71:1171–1177, 1993.
Zydney, A. L., and C. K. Colton. Augmented solute transport in the shear flow of a concentrated suspension. Physicochem. Hydrodyn. 10(1):77–96, 1988.
Acknowledgments
The authors thank the National Science Foundation for use of the TeraGrid under grant number TG-CTS100012 and the Texas Advanced Computing Center for the use of Ranger. D.R. was funded by the United States Department of Defense through the ASEE SMART fellowship.
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Associate Editor Konstantinos Konstantopoulos oversaw the review of this article.
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Reasor, D.A., Mehrabadi, M., Ku, D.N. et al. Determination of Critical Parameters in Platelet Margination. Ann Biomed Eng 41, 238–249 (2013). https://doi.org/10.1007/s10439-012-0648-7
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DOI: https://doi.org/10.1007/s10439-012-0648-7