An optimization based 3D-1D coupling strategy for tissue perfusion and chemical transport during tumor-induced angiogenesis

A new mathematical model and numerical approach are proposed for the simulation of fluid and chemical exchanges between a growing capillary network and the surrounding tissue, in the context of tumor-induced angiogenesis. Thanks to proper modeling assumptions the capillaries are reduced to their centerline: a well posed mathematical model is hence worked out, based on the coupling between a three-dimensional and a one-dimensional equation (3D-1D coupled problem). Also the application of a PDE-constrained optimization formulation is here proposed for the first time for angiogenesis simulations. Under this approach no mesh conformity is required, thus making the method particularly suitable for this kind of application, since no remeshing is required as the capillary network grows. In order to handle both the evolution of the quantities of interest and the changes in the geometry, a discrete-hybrid strategy is adopted, combining a continuous modeling of the tissue and of the chemicals with a discrete tip-tracking model to account for the vascular network growth. The tip-tracking strategy, together with some proper rules for branching and anastomosis, is able to provide a realistic representation of the capillary network.

[1]  S. Berrone,et al.  A PDE-constrained optimization method for 3D-1D coupled problems with discontinuous solutions , 2022, Numerical Algorithms.

[2]  Stefano Berrone,et al.  3D-1D coupling on non conforming meshes via three-field optimization based domain decomposition , 2021, J. Comput. Phys..

[3]  Kent-Andre Mardal,et al.  Analysis and approximation of mixed-dimensional PDEs on 3D-1D domains coupled with Lagrange multipliers , 2020, SIAM J. Numer. Anal..

[4]  P. Jenny,et al.  Modeling tissue perfusion in terms of 1d-3d embedded mixed-dimension coupled problems with distributed sources , 2019, J. Comput. Phys..

[5]  Paolo Zunino,et al.  Derivation and analysis of coupled PDEs on manifolds with high dimensionality gap arising from topological model reduction , 2019, ESAIM: Mathematical Modelling and Numerical Analysis.

[6]  Luca Heltai,et al.  Multiscale modeling of vascularized tissues via nonmatching immersed methods , 2019, International journal for numerical methods in biomedical engineering.

[7]  Ingeborg G. Gjerde,et al.  A singularity removal method for coupled 1D–3D flow models , 2018, Computational Geosciences.

[8]  J. Nordbotten,et al.  Well Modelling By Means Of Coupled 1D-3D Flow Models , 2018, ECMOR XVI - 16th European Conference on the Mathematics of Oil Recovery.

[9]  Joel s. Brown,et al.  The Warburg effect as an adaptation of cancer cells to rapid fluctuations in energy demand , 2017, PloS one.

[10]  Ignasi Colominas,et al.  A mathematical model of tumour angiogenesis: growth, regression and regrowth , 2017, Journal of The Royal Society Interface.

[11]  Ignasi Colominas,et al.  Computational Modeling of Tumor-Induced Angiogenesis , 2017, Archives of Computational Methods in Engineering.

[12]  Aleksander S. Popel,et al.  Effects of endothelial cell proliferation and migration rates in a computational model of sprouting angiogenesis , 2016, Scientific Reports.

[13]  C. Giverso,et al.  Tumour angiogenesis as a chemo-mechanical surface instability , 2016, Scientific Reports.

[14]  C. Ruhrberg,et al.  The Embryonic Mouse Hindbrain and Postnatal Retina as In Vivo Models to Study Angiogenesis. , 2015, Methods in molecular biology.

[15]  P. Zunino,et al.  A computational model of drug delivery through microcirculation to compare different tumor treatments , 2014, International journal for numerical methods in biomedical engineering.

[16]  Laura Cattaneo,et al.  Computational models for fluid exchange between microcirculation and tissue interstitium , 2014, Networks Heterog. Media.

[17]  S. McKeown,et al.  Defining normoxia, physoxia and hypoxia in tumours-implications for treatment response. , 2014, The British journal of radiology.

[18]  Ignasi Colominas,et al.  Capillary networks in tumor angiogenesis: From discrete endothelial cells to phase‐field averaged descriptions via isogeometric analysis , 2013, International journal for numerical methods in biomedical engineering.

[19]  L Preziosi,et al.  A review of mathematical models for the formation of vascular networks. , 2013, Journal of theoretical biology.

[20]  Heiko Rieger,et al.  Interstitial Fluid Flow and Drug Delivery in Vascularized Tumors: A Computational Model , 2013, PloS one.

[21]  Arndt F. Siekmann,et al.  The tip cell concept 10 years after: new players tune in for a common theme. , 2013, Experimental cell research.

[22]  Axel R. Pries,et al.  Angiogenesis: An Adaptive Dynamic Biological Patterning Problem , 2013, PLoS Comput. Biol..

[23]  Carlo D'Angelo,et al.  Finite Element Approximation of Elliptic Problems with Dirac Measure Terms in Weighted Spaces: Applications to One- and Three-dimensional Coupled Problems , 2012, SIAM J. Numer. Anal..

[24]  R. Adams,et al.  Dynamics of endothelial cell behavior in sprouting angiogenesis. , 2010, Current opinion in cell biology.

[25]  Paul A. Bates,et al.  Tipping the Balance: Robustness of Tip Cell Selection, Migration and Fusion in Angiogenesis , 2009, PLoS Comput. Biol..

[26]  T. Miura,et al.  In vitro Vasculogenesis Models Revisited - Measurement of VEGF Diffusion in Matrigel , 2009 .

[27]  Michael Bergdorf,et al.  A hybrid model for three-dimensional simulations of sprouting angiogenesis. , 2008, Biophysical journal.

[28]  A. Quarteroni,et al.  On the coupling of 1D and 3D diffusion-reaction equations. Applications to tissue perfusion problems , 2008 .

[29]  H. Dvorak,et al.  Vascular permeability, vascular hyperpermeability and angiogenesis , 2008, Angiogenesis.

[30]  H Rieger,et al.  Emergent vascular network inhomogeneities and resulting blood flow patterns in a growing tumor. , 2008, Journal of theoretical biology.

[31]  Arjan W. Griffioen,et al.  Tumour vascularization: sprouting angiogenesis and beyond , 2007, Cancer and Metastasis Reviews.

[32]  A. Bikfalvi,et al.  Tumor angiogenesis , 2020, Advances in cancer research.

[33]  Alexander R. A. Anderson,et al.  Mathematical modelling of the influence of blood rheological properties upon adaptative tumour-induced angiogenesis , 2006, Math. Comput. Model..

[34]  H Rieger,et al.  Vascular network remodeling via vessel cooption, regression and growth in tumors. , 2005, Journal of theoretical biology.

[35]  Alexander R. A. Anderson,et al.  Mathematical modelling of flow in 2D and 3D vascular networks: Applications to anti-angiogenic and chemotherapeutic drug strategies , 2005, Math. Comput. Model..

[36]  Shuyu Sun,et al.  A deterministic model of growth factor-induced angiogenesis , 2005, Bulletin of mathematical biology.

[37]  B. Weichman Inflammation: basic principles and clinical correlates , 1988, Agents and Actions.

[38]  B. Engquist,et al.  Numerical approximations of singular source terms in differential equations , 2004 .

[39]  Russell Hughes,et al.  Current methods for assaying angiogenesis in vitro and in vivo , 2004, International journal of experimental pathology.

[40]  H. Othmer,et al.  Mathematical modeling of tumor-induced angiogenesis , 2004, Journal of mathematical biology.

[41]  P. Maini,et al.  A cellular automaton model for tumour growth in inhomogeneous environment. , 2003, Journal of theoretical biology.

[42]  Rakesh K Jain,et al.  Molecular regulation of vessel maturation , 2003, Nature Medicine.

[43]  P. Carmeliet Angiogenesis in health and disease , 2003, Nature Medicine.

[44]  L. Preziosi,et al.  Modeling the early stages of vascular network assembly , 2003, The EMBO journal.

[45]  L. Preziosi,et al.  Modelling Solid Tumor Growth Using the Theory of Mixtures , 2001, Mathematical medicine and biology : a journal of the IMA.

[46]  TUMOR ANGIOGENESIS Rapid Induction of Endothelial Mitoses Demonstrated by Autoradiography , 2003 .

[47]  P. Jonesb,et al.  A Mathematical Model of an In Vitro Experiment to Investigate Endothelial Cell Migration , 2003 .

[48]  S. McDougall,et al.  Mathematical modelling of flow through vascular networks: Implications for tumour-induced angiogenesis and chemotherapy strategies , 2002, Bulletin of mathematical biology.

[49]  S. Negrotto,et al.  [Angiogenesis in cancer]. , 2002, Medicina.

[50]  B. Sleeman,et al.  Mathematical modeling of capillary formation and development in tumor angiogenesis: Penetration into the stroma , 2001, Bulletin of mathematical biology.

[51]  F. Yuan,et al.  Numerical simulations of angiogenesis in the cornea. , 2001, Microvascular research.

[52]  M. Markus,et al.  Simulation of vessel morphogenesis using cellular automata. , 1999, Mathematical biosciences.

[53]  D. Walsh,et al.  Angiogenesis and arthritis. , 1999, Rheumatology.

[54]  M. Chaplain,et al.  Continuous and discrete mathematical models of tumor-induced angiogenesis , 1998, Bulletin of mathematical biology.

[55]  W. Risau,et al.  Mechanisms of angiogenesis , 1997, Nature.

[56]  M. Chaplain,et al.  A mathematical model of the first steps of tumour-related angiogenesis: capillary sprout formation and secondary branching. , 1996, IMA journal of mathematics applied in medicine and biology.

[57]  F Nekka,et al.  A model of growing vascular structures. , 1996, Bulletin of mathematical biology.

[58]  J. Folkman Angiogenesis in cancer, vascular, rheumatoid and other disease , 1995, Nature Medicine.

[59]  H M Byrne,et al.  Mathematical models for tumour angiogenesis: numerical simulations and nonlinear wave solutions. , 1995, Bulletin of mathematical biology.

[60]  M. Chaplain,et al.  A model mechanism for the chemotactic response of endothelial cells to tumour angiogenesis factor. , 1993, IMA journal of mathematics applied in medicine and biology.

[61]  C. Graham,et al.  Mechanisms of placental invasion of the uterus and their control. , 1992, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[62]  F. Arnold,et al.  Angiogenesis in wound healing. , 1991, Pharmacology & therapeutics.

[63]  O. Hudlická,et al.  What makes blood vessels grow? , 1991, The Journal of physiology.

[64]  D A Lauffenburger,et al.  Analysis of the roles of microvessel endothelial cell random motility and chemotaxis in angiogenesis. , 1991, Journal of theoretical biology.

[65]  R K Jain,et al.  Transport of fluid and macromolecules in tumors. IV. A microscopic model of the perivascular distribution. , 1991, Microvascular research.

[66]  R K Jain,et al.  Transport of fluid and macromolecules in tumors. II. Role of heterogeneous perfusion and lymphatics. , 1990, Microvascular research.

[67]  M. Chaplain,et al.  A mathematical model for the production and secretion of tumour angiogenesis factor in tumours. , 1990, IMA journal of mathematics applied in medicine and biology.

[68]  R. Hamlin,et al.  Capillary Basement Membrane Thickness and Capillary Density in Sedentary and Trained Obese Zucker Rats , 1989, Diabetes.

[69]  N Paweletz,et al.  Tumor-related angiogenesis. , 1989, Critical reviews in oncology/hematology.

[70]  R K Jain,et al.  Transport of fluid and macromolecules in tumors. I. Role of interstitial pressure and convection. , 1989, Microvascular research.

[71]  J. Folkman,et al.  Angiogenic factors. , 1987, Science.

[72]  J. Madri,et al.  Endothelial cell-matrix interactions: in vitro models of angiogenesis. , 1986, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[73]  D. Balding,et al.  A mathematical model of tumour-induced capillary growth. , 1985, Journal of theoretical biology.

[74]  J. Wilson,et al.  Mechanisms of neovascularization. Vascular sprouting can occur without proliferation of endothelial cells. , 1984, Laboratory investigation; a journal of technical methods and pathology.

[75]  L. Liotta,et al.  Basement membrane collagen: degradation by migrating endothelial cells. , 1983, Science.

[76]  R. Auerbach,et al.  Tumor-induced neovascularization in the mouse eye. , 1982, Journal of the National Cancer Institute.

[77]  J. Folkman,et al.  Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. , 1977, Microvascular research.

[78]  J. Folkman,et al.  Inhibition of tumor angiogenesis mediated by cartilage , 1975, The Journal of experimental medicine.

[79]  J. Folkman,et al.  Tumor angiogenesis: iris neovascularization at a distance from experimental intraocular tumors. , 1973, Journal of the National Cancer Institute.

[80]  B. Waaler [Vascular permeability]. , 1972, Tidsskrift for den Norske laegeforening : tidsskrift for praktisk medicin, ny raekke.