A continuous energy-based immersed boundary method for elastic shells

Abstract The immersed boundary method is a mathematical formulation and numerical method for solving fluid–structure interaction problems. For many biological problems, such as models that include the cell membrane, the immersed structure is a two-dimensional infinitely thin elastic shell immersed in an incompressible viscous fluid. When the shell is modeled as a hyperelastic material, forces can be computed by taking the variational derivative of an energy density functional. A new method for computing a continuous force function on the entire surface of the shell is presented here. The new method is compared to a previous formulation where the surface and energy functional are discretized before forces are computed. For the case of Stokes flow, a method for computing quadrature weights is provided to ensure the integral of the elastic spread force density remains zero throughout a dynamic simulation. Tests on the method are conducted and show that it yields more accurate force computations than previous formulations as well as more accurate geometric information such as mean curvature. The method is then applied to a model of a red blood cell in capillary flow and a 3D model of cellular blebbing.

[1]  Dominique Barthès Biesel Motion and Deformation of Elastic Capsules and Vesicles in Flow , 2016 .

[2]  Michael D. Graham,et al.  Cell Distribution and Segregation Phenomena During Blood Flow , 2015 .

[3]  Ronald Fedkiw,et al.  The immersed interface method. Numerical solutions of PDEs involving interfaces and irregular domains , 2007, Math. Comput..

[4]  Evan Evans,et al.  Mechanics and Thermodynamics of Biomembranes , 2017 .

[5]  Wanda Strychalski,et al.  Intracellular Pressure Dynamics in Blebbing Cells. , 2016, Biophysical journal.

[7]  Robert Michael Kirby,et al.  A Study of Different Modeling Choices For Simulating Platelets Within the Immersed Boundary Method , 2012, Applied numerical mathematics : transactions of IMACS.

[8]  Paul J. Atzberger,et al.  Simulation of Osmotic Swelling by the Stochastic Immersed Boundary Method , 2015, SIAM J. Sci. Comput..

[9]  L Mahadevan,et al.  Life and times of a cellular bleb. , 2008, Biophysical journal.

[10]  Wanda Strychalski,et al.  A computational model of bleb formation. , 2013, Mathematical medicine and biology : a journal of the IMA.

[11]  L. Fauci,et al.  A computational model of aquatic animal locomotion , 1988 .

[12]  Christopher Jekeli,et al.  Spherical harmonic analysis, aliasing, and filtering , 1996 .

[13]  A. D. Young,et al.  An Introduction to Fluid Mechanics , 1968 .

[14]  Joseph D. Ward,et al.  Kernel based quadrature on spheres and other homogeneous spaces , 2012, Numerische Mathematik.

[15]  J. Tinevez,et al.  Role of cortical tension in bleb growth , 2009, Proceedings of the National Academy of Sciences.

[16]  C. Peskin,et al.  When vortices stick: an aerodynamic transition in tiny insect flight , 2004, Journal of Experimental Biology.

[17]  R. Peyret Spectral Methods for Incompressible Viscous Flow , 2002 .

[18]  Boyce E. Griffith,et al.  Immersed Boundary Method for Variable Viscosity and Variable Density Problems Using Fast Constant-Coefficient Linear Solvers I: Numerical Method and Results , 2013, SIAM J. Sci. Comput..

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

[20]  M. Lai,et al.  An Immersed Boundary Method with Formal Second-Order Accuracy and Reduced Numerical Viscosity , 2000 .

[21]  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.

[22]  C. Peskin Flow patterns around heart valves: A numerical method , 1972 .

[23]  Z. J. Wang,et al.  A 3D immersed interface method for fluid–solid interaction , 2008 .

[24]  Wanda Strychalski,et al.  A poroelastic immersed boundary method with applications to cell biology , 2015, J. Comput. Phys..

[25]  John M. Sullivan,et al.  Curvatures of Smooth and Discrete Surfaces , 2007, 0710.4497.

[26]  Robert Michael Kirby,et al.  Augmenting the immersed boundary method with Radial Basis Functions (RBFs) for the modeling of platelets in hemodynamic flows , 2013, ArXiv.

[27]  George Biros,et al.  A fast algorithm for simulating vesicle flows in three dimensions , 2011, J. Comput. Phys..

[28]  C. Peskin The immersed boundary method , 2002, Acta Numerica.

[29]  J. P. Beyer A computational model of the cochlea using the immersed boundary method , 1992 .

[30]  Prosenjit Bagchi,et al.  Phase diagram and breathing dynamics of a single red blood cell and a biconcave capsule in dilute shear flow. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[31]  C. Pozrikidis,et al.  Interfacial dynamics for Stokes flow , 2001 .

[32]  K. Hjelmstad Fundamentals of Structural Mechanics , 1996 .

[33]  L. Heltai,et al.  On the hyper-elastic formulation of the immersed boundary method , 2008 .

[34]  B. Alberts,et al.  Molecular Biology of the Cell (Fifth Edition) , 2008 .

[35]  Luca Heltai,et al.  On the CFL condition for the finite element immersed boundary method , 2007 .

[36]  Boyce E. Griffith,et al.  On the order of accuracy of the immersed boundary method: Higher order convergence rates for sufficiently smooth problems , 2005 .

[37]  Boyce E. Griffith,et al.  Hybrid finite difference/finite element version of the immersed boundary method , 2012 .

[38]  Roie Shlomovitz,et al.  Physical model of contractile ring initiation in dividing cells. , 2008, Biophysical journal.

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

[40]  Inderjit S. Dhillon,et al.  A non-monotonic method for large-scale non-negative least squares , 2013, Optim. Methods Softw..

[41]  Dharshi Devendran,et al.  An immersed boundary energy-based method for incompressible viscoelasticity , 2012, J. Comput. Phys..

[42]  Alain Goriely,et al.  Global contraction or local growth, bleb shape depends on more than just cell structure. , 2015, Journal of theoretical biology.

[43]  Charles S. Peskin,et al.  Tether Force Constraints in Stokes Flow by the Immersed Boundary Method on a Periodic Domain , 2009, SIAM J. Sci. Comput..

[44]  R. Capovilla Elastic bending energy: a variational approach , 2017, 1709.04399.

[45]  Stefan Kunis,et al.  On the computation of nonnegative quadrature weights on the sphere , 2009 .

[46]  Lucia Gastaldi,et al.  The immersed boundary methoda finite element approach , 2003 .

[47]  Guillaume Charras,et al.  Blebs lead the way: how to migrate without lamellipodia , 2008, Nature Reviews Molecular Cell Biology.

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

[49]  T. Ishikawa,et al.  Tension of red blood cell membrane in simple shear flow. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[50]  Ian H. Sloan,et al.  Extremal Systems of Points and Numerical Integration on the Sphere , 2004, Adv. Comput. Math..

[51]  Ian H. Sloan,et al.  How good can polynomial interpolation on the sphere be? , 2001, Adv. Comput. Math..

[52]  C. Pozrikidis,et al.  Modeling and Simulation of Capsules and Biological Cells , 2003 .

[53]  James Keener,et al.  Eulerian-Lagrangian Treatment of Nondilute Two-Phase Gels , 2016, SIAM J. Appl. Math..

[54]  Seifert,et al.  Fluid Vesicles in Shear Flow. , 1996, Physical review letters.

[55]  R. Ogden Non-Linear Elastic Deformations , 1984 .

[56]  W. Helfrich,et al.  Bending energy of vesicle membranes: General expressions for the first, second, and third variation of the shape energy and applications to spheres and cylinders. , 1989, Physical review. A, General physics.

[57]  C. Pozrikidis Boundary Integral and Singularity Methods for Linearized Viscous Flow: Index , 1992 .

[58]  Jemal Guven,et al.  Second variation of the Helfrich–Canham Hamiltonian and reparametrization invariance , 2004 .

[59]  Christopher Jekeli,et al.  Methods to Reduce Aliasing in Spherical Harmonic Analysis , 1996 .

[60]  G. Charras,et al.  The cytoplasm of living cells behaves as a poroelastic material , 2013, Nature materials.

[61]  Boyce E. Griffith,et al.  Hybrid finite difference/finite element immersed boundary method , 2016, International journal for numerical methods in biomedical engineering.