Brain--Tumor Interaction Biophysical Models for Medical Image Registration

State-of-the art algorithms for deformable image registration are based on the minimization of an image similarity functional that is regularized by adding a penalty term on the deformation map. The penalty function typically represents a smoothness regularization. In this article, we use a constrained optimization formulation in which the image similarity functional is coupled to a biophysical model. This formulation is pertinent when the data have been generated by imaging tissue that undergoes deformations due to an actual biophysical phenomenon. Such is the case of coregistering tumor-bearing brain images from the same individual. We present an approximate model that couples tumor growth with the mechanical deformations of the surrounding brain tissue. We consider primary brain tumors—in particular, gliomas. Glioma growth is modeled by a reaction-advection-diffusion PDE, with a two-way coupling with the underlying tissue elastic deformation. Tumor bulk, infiltration, and subsequent mass effects are not regarded separately but are captured by the model itself in the course of its evolution. Our formulation allows for updating the tumor diffusion coefficient following structural displacements caused by tumor growth/infiltration. Our forward problem implementation builds on the *PETSc* library of Argonne National Laboratory. Our reformulation results in a very small parameter space, and we use the derivative-free optimization library *APPSPACK* of Sandia National Laboratories. We test the forward model and the optimization framework by using landmark-based similarity functions and by applying it to brain tumor data from clinical and animal studies. State-of-the-art registration algorithms fail in such problems due to excessive deformations. We compare our results with previous work in our group, and we observed up to 50% improvement in landmark deformation prediction. We present preliminary validation results in which we were able to reconstruct deformation fields using four degrees of freedom. Our study demonstrates the validity of our formulation and points to the need for richer datasets and fast optimization algorithms.

[1]  Christos Davatzikos,et al.  A robust framework for soft tissue simulations with application to modeling brain tumor mass effect in 3D MR images , 2007, Physics in medicine and biology.

[2]  Willem Hundsdorfer,et al.  Numerical time integration for air pollution models , 1998 .

[3]  Ronald Fedkiw,et al.  Level set methods and dynamic implicit surfaces , 2002, Applied mathematical sciences.

[4]  Tamara G. Kolda,et al.  Algorithm 856: APPSPACK 4.0: asynchronous parallel pattern search for derivative-free optimization , 2006, TOMS.

[5]  Helen M. Byrne,et al.  A two-phase model of solid tumour growth , 2003, Appl. Math. Lett..

[6]  Roland Glowinski,et al.  Wavelet and Finite Element Solutions for the Neumann Problem Using Fictitious Domains , 1996 .

[7]  A. Gefen,et al.  Are in vivo and in situ brain tissues mechanically similar? , 2004, Journal of biomechanics.

[8]  D. Brandt,et al.  Multi-level adaptive solutions to boundary-value problems math comptr , 1977 .

[9]  Keith D. Paulsen,et al.  Assimilating intraoperative data with brain shift modeling using the adjoint equations , 2005, Medical Image Anal..

[10]  K Miller,et al.  Mechanical properties of brain tissue in-vivo: experiment and computer simulation. , 2000, Journal of biomechanics.

[11]  R. Bajcsy,et al.  A computerized system for the elastic matching of deformed radiographic images to idealized atlas images. , 1983, Journal of computer assisted tomography.

[12]  G. Biros,et al.  Fast Solvers for Soft Tissue Simulation with Application to Construction of Brain Tumor Atlases , 2007 .

[13]  Claudio Pollo,et al.  Atlas-based segmentation of pathological MR brain images using a model of lesion growth , 2004, IEEE Transactions on Medical Imaging.

[14]  J. Murray,et al.  A quantitative model for differential motility of gliomas in grey and white matter , 2000, Cell proliferation.

[15]  Philippe Tracqui,et al.  MODELLING THREE-DIMENSIONAL GROWTH OF BRAIN TUMOURS FROM TIME SERIES OF SCANS , 1999 .

[16]  Bruce T. Murray,et al.  Modeling tumor growth: a computational approach in a continuum framework , 2005 .

[17]  Christos Davatzikos,et al.  Finite Element Modeling of Brain Tumor Mass-Effect from 3D Medical Images , 2005, MICCAI.

[18]  J. Hyman,et al.  The Black Box Multigrid Numerical Homogenization Algorithm , 1998 .

[19]  Laurent Capelle,et al.  Continuous growth of mean tumor diameter in a subset of grade II gliomas , 2003, Annals of neurology.

[20]  S Torquato,et al.  Simulated brain tumor growth dynamics using a three-dimensional cellular automaton. , 2000, Journal of theoretical biology.

[21]  L. G. Stern,et al.  Fractional step methods applied to a chemotaxis model , 2000, Journal of mathematical biology.

[22]  George Biros,et al.  Parallel Lagrange-Newton-Krylov-Schur Methods for PDE-Constrained Optimization. Part I: The Krylov-Schur Solver , 2005, SIAM J. Sci. Comput..

[23]  Jonathan Richard Shewchuk,et al.  Sweep algorithms for constructing higher-dimensional constrained Delaunay triangulations , 2000, SCG '00.

[24]  J. Murray,et al.  Virtual and real brain tumors: using mathematical modeling to quantify glioma growth and invasion , 2003, Journal of the Neurological Sciences.

[25]  M. Gurtin,et al.  An introduction to continuum mechanics , 1981 .

[26]  D. L. Sean McElwain,et al.  A Mixture Theory for the Genesis of Residual Stresses in Growing Tissues I: A General Formulation , 2005, SIAM J. Appl. Math..

[27]  Dinggang Shen,et al.  A framework for predictive modeling of anatomical deformations , 2001, IEEE Transactions on Medical Imaging.

[28]  Dimitris N. Metaxas,et al.  In vivo strain and stress estimation of the heart left and right ventricles from MRI images , 2003, Medical Image Anal..

[29]  Guangwei Yuan,et al.  Convergence and stability of explicit/implicit schemes for parabolic equations with discontinuous coefficients , 2004 .

[30]  Tamara G. Kolda,et al.  Revisiting Asynchronous Parallel Pattern Search for Nonlinear Optimization , 2005, SIAM J. Optim..

[31]  M. Westphal,et al.  Glioma invasion in the central nervous system. , 1996, Neurosurgery.

[32]  Ruzena Bajcsy,et al.  Advances in elastic matching theory and its implementation , 1997, CVRMed.

[33]  Jan Modersitzki,et al.  Numerical Methods for Image Registration , 2004 .

[34]  Keith D. Paulsen,et al.  Model-updated image guidance: initial clinical experiences with gravity-induced brain deformation , 1999, IEEE Transactions on Medical Imaging.

[35]  Nick C Fox,et al.  Computer-assisted imaging to assess brain structure in healthy and diseased brains , 2003, The Lancet Neurology.

[36]  Christos Davatzikos,et al.  Nonlinear elastic registration of brain images with tumor pathology using a biomechanical model [MRI] , 1999, IEEE Transactions on Medical Imaging.

[37]  Ron Kikinis,et al.  Real-time registration of volumetric brain MRI by biomechanical simulation of deformation during image guided neurosurgery , 2002 .

[38]  P. Roache QUANTIFICATION OF UNCERTAINTY IN COMPUTATIONAL FLUID DYNAMICS , 1997 .

[39]  Hervé Delingette,et al.  Realistic simulation of the 3-D growth of brain tumors in MR images coupling diffusion with biomechanical deformation , 2005, IEEE Transactions on Medical Imaging.

[40]  James S. Duncan,et al.  Estimation of 3-D left ventricular deformation from medical images using biomechanical models , 2002, IEEE Transactions on Medical Imaging.

[41]  Karl Rohr,et al.  Biomedical Modeling of the Human Head for Physically-based, Non-rigid Image Registration , 1999, IEEE Trans. Medical Imaging.

[42]  George Biros,et al.  Parallel Lagrange-Newton-Krylov-Schur Methods for PDE-Constrained Optimization. Part II: The Lagrange-Newton Solver and Its Application to Optimal Control of Steady Viscous Flows , 2005, SIAM J. Sci. Comput..

[43]  Alain Trouvé,et al.  The Euler-Lagrange Equation for Interpolating Sequence of Landmark Datasets , 2003, MICCAI.

[44]  K. Rohr,et al.  Biomechanical modeling of the human head for physically based, nonrigid image registration , 1999, IEEE Transactions on Medical Imaging.

[45]  L. Younes,et al.  On the metrics and euler-lagrange equations of computational anatomy. , 2002, Annual review of biomedical engineering.

[46]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[47]  Sandia Report,et al.  Revisiting Asynchronous Parallel Pattern Search for Nonlinear Optimization , 2004 .

[48]  V. Cristini,et al.  Nonlinear simulation of tumor growth , 2003, Journal of mathematical biology.

[49]  Claudio H. Sibata,et al.  Patient-specific tumor prognosis prediction via multimodality imaging , 1996, Medical Imaging.

[50]  Christos Davatzikos,et al.  An image-driven parameter estimation problem for a reaction–diffusion glioma growth model with mass effects , 2008, Journal of mathematical biology.

[51]  T. Deisboeck,et al.  Complex dynamics of tumors: modeling an emerging brain tumor system with coupled reaction–diffusion equations , 2003 .

[52]  D L S McElwain,et al.  A history of the study of solid tumour growth: The contribution of mathematical modelling , 2004, Bulletin of mathematical biology.

[53]  D. Keyes,et al.  Jacobian-free Newton-Krylov methods: a survey of approaches and applications , 2004 .

[54]  Olivier Pironneau,et al.  A FICTITIOUS DOMAIN BASED GENERAL PDE SOLVER , 2004 .

[55]  K. Chinzei,et al.  Mechanical properties of brain tissue in tension. , 2002, Journal of biomechanics.

[56]  Russell H. Taylor,et al.  Combining statistical and biomechanical models for estimation of anatomical deformations , 2006 .

[57]  Michael I. Miller,et al.  Volumetric transformation of brain anatomy , 1997, IEEE Transactions on Medical Imaging.

[58]  G. Biros,et al.  A Framework for Soft Tissue Simulations with Application to Modeling Brain Tumor Mass-Effect in 3 D Images , 2006 .