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Intermittency and synchronized motion of red blood cell dynamics in shear flow

Published online by Cambridge University Press:  24 October 2014

Daniel Cordasco
Affiliation:
Mechanical and Aerospace Engineering Department, Rutgers, The State University of New Jersey, Piscataway, NJ 08854, USA
Prosenjit Bagchi*
Affiliation:
Mechanical and Aerospace Engineering Department, Rutgers, The State University of New Jersey, Piscataway, NJ 08854, USA
*
Email address for correspondence: [email protected]

Abstract

We present the first full-scale computational evidence of intermittent and synchronized dynamics of red blood cells in shear flow. These dynamics are characterized by the coexistence of a tumbling motion in which the cell behaves like a rigid body and a tank-treading motion in which the cell behaves like a liquid drop. In the intermittent dynamics, we observe sequences of tumbling interrupted by swinging, as well as sequences of swinging interrupted by tumbling. In the synchronized dynamics, the tumbling and membrane rotation are observed to occur simultaneously with integer ratios of the rotational frequencies. These dynamics are shown to be dependent on the stress-free state of the cytoskeleton, and are explained based on the cell membrane energy landscape.

Type
Papers
Copyright
© 2014 Cambridge University Press 

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References

Abkarian, M., Faivre, M. & Viallat, A. 2007 Swinging of red blood cells under shear flow. Phys. Rev. Lett. 98, 188302.Google Scholar
Abreu, D. & Seifert, U. 2012 Effect of thermal noise on vesicles and capsules in shear flow. Phys. Rev. E 86, 010902.Google Scholar
Chien, S. 1987 Red cell deformability and its relevance to blood flow. Annu. Rev. Physiol. 49, 177192.Google Scholar
Cordasco, D. & Bagchi, P. 2013 Orbital drift of capsules and red blood cells in shear flow. Phys. Fluids 25, 091902.Google Scholar
Cordasco, D., Yazdani, A. & Bagchi, P. 2014 Comparison of erythrocyte dynamics in shear flow under different stress-free configurations. Phys. Fluids 26, 041902.Google Scholar
Dupire, J., Socol, M. & Viallat, A. 2012 Full dynamics of a red blood cell in shear flow. Proc. Natl Acad. Sci. USA 109, 2080820813.Google Scholar
Fedosov, D., Caswell, B. & Karniadakis, G. 2010 A multiscale red blood cell model with accurate mechanics, rheology, and dynamics. Biophys. J. 98, 22152225.Google Scholar
Finken, R., Kessler, S. & Seifert, U. 2011 Micro-capsules in shear flow. J. Phys.: Condens. Matter 23, 184113.Google Scholar
Fischer, T. M. & Korzeniewski, R. 2013 Threshold shear stress for the transition between tumbling and tank-treading of red blood cells in shear flow – dependence on the viscosity of the suspending medium. J. Fluid Mech. 376, 351365.Google Scholar
Fischer, T. M., Stohr-Liesen, M. & Schmid-Schonbein, H. 1978 The red cell as a fluid droplet: tank tread-like motion of the human erythrocyte membrane in shear flow. Science 202, 894896.Google Scholar
Goldsmith, H. L. & Marlow, J. 1972 Flow behavior of erythrocytes. I. Rotation and deformation in dilute suspensions. Proc. R. Soc. Lond. B 182, 351384.Google Scholar
Kessler, S., Finken, R. & Seifert, U. 2008 Swinging and tumbling of elastic capsules in shear flow. J. Fluid Mech. 605, 207226.Google Scholar
Lim, G., Wortis, M. & Mukhopadhyay, R. 2002 Stomatocyte–discocyte–echinocyte sequence of the human red blood cell: evidence for the bilayer-couple hypothesis from membrane mechanics. Proc. Natl Acad. Sci. USA 99, 16766.Google Scholar
Mills, J. P., Qie, L., Dao, M., Lim, C. T. & Suresh, S. 2004 Nonlinear elastic and viscoelastic deformation of the human red blood cell with optical tweezers. Mech. Chem. Biosyst. 1, 169180.Google Scholar
Noguchi, H. 2009 Swinging and synchronized rotations of red blood cells in simple shear flow. Phys. Rev. E 80, 021902.Google Scholar
Noguchi, H. 2010 Dynamic modes of microcapsules in steady shear flow: effects of bending and shear elasticities. Phys. Rev. E 81, 056319.Google Scholar
Peng, Z., Mashayekh, A. & Zhu, Q. 2014 Erythrocyte responses in low-shear-rate flows: effects of non-biconcave stress-free state in the cytoskeleton. J. Fluid Mech. 742, 96118.Google Scholar
Seifert, U., Berndl, K. & Lipowsky, R. 1991 Shape transformation of vesicles: phase diagram for spontaneous curvature and bilayer-coupling models. Phys. Rev. A 44, 11821202.Google Scholar
Skalak, R., Tozeren, A., Zarda, P. R. & Chien, S. 1973 Strain energy function of red blood cell membrane. Biophys. J. 13, 245264.Google Scholar
Skotheim, J. M. & Secomb, T. W. 2007 Red blood cells and other nonspherical capsules in shear flow: oscillatory dynamics and the tank-treading-to-tumbling transition. Phys. Rev. Lett. 98, 078301.Google Scholar
Tsubota, K., Wada, S. & Liu, H. 2013 Elastic behaviour of a red blood cell with the membrane’s nonuniform natural state: equilibrium shape, motion transition under shear flow, and elongation during tank-treading motion. Biomech. Model. Mechanobiol. 13, 112.Google Scholar
Viallat, A. & Abkarian, M. 2014 Red blood cell: from its mechanics to its motion in shear flow. Intl J. Lab. Hematol. 36, 237243.Google Scholar
Vlahovska, P. M., Young, Y.-N., Danker, G. & Misbah, C. 2011 Dynamics of a non-spherical microcapsule with incompressible interface in shear flow. J. Fluid Mech. 678, 221247.Google Scholar
Wang, X., Zhao, H., Zhuang, F. Y. & Stoltz, J. F. 1999 Measurement of erythrocyte deformability by two laser diffraction methods. J. Clin. Hemorheol. Microcirc. 21, 291295.Google Scholar
Yazdani, A. & Bagchi, P. 2011 Phase diagram and breathing dynamics of a single red blood cell and a biconcave capsule in dilute shear flow. Phys. Rev. E 84, 026314.Google Scholar
Yazdani, A. & Bagchi, P. 2013 Influence of membrane viscosity on capsule dynamics in shear flow. J. Fluid Mech. 718, 569595.Google Scholar
Zhong-can, O.-Y. & Helfrich, W. 1989 Bending energy of vesicle membranes: general expressions for the first, second, and third variation of the shape energy and applications to spheres and cylinders. Phys. Rev. A 39, 5280.Google Scholar

Cordasco and Bagchi supplementary movie

Intermittent dynamics corresponding to Figure 2a.

Download Cordasco and Bagchi supplementary movie(Video)
Video 14.1 MB
Supplementary material: File

Cordasco and Bagchi supplementary material

Supplementary figures

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File 1.8 MB

Cordasco and Bagchi supplementary movie

Intermittent dynamics corresponding to Figure 2a.

Download Cordasco and Bagchi supplementary movie(Video)
Video 2.6 MB

Cordasco and Bagchi supplementary movie

Animation corresponding to Figure 2c.

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Video 18.6 MB

Cordasco and Bagchi supplementary movie

Synchronized motion corresponding to Figure 5.

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Video 1.8 MB

Cordasco and Bagchi supplementary movie

Synchronized dynamics with frequency ratio of 3.

Download Cordasco and Bagchi supplementary movie(Video)
Video 13.1 MB