Dual-porosity poroviscoelasticity and quantitative hydromechanical characterization of the brain tissue with experimental hydrocephalus data.

Hydromechanical brain models often involve constitutive relations which must account for soft tissue deformation and creep, together with the interstitial fluid movement and exchange through capillaries. The interaction of rather unknown mechanisms which produce, absorb, and circulate the cerebrospinal fluid within the central nervous system can further add to their complexity. Once proper models for these phenomena or processes are selected, estimation of the associated parameters could be even more challenging. This paper presents the results of a consistent, coupled poroviscoelastic modeling and characterization of the brain tissue as a dual-porosity system. The model draws from Biot's theory of poroviscoelasticity, and adopts the generalized Kelvin's rheological description of the viscoelastic tissue behavior. While the interstitial space serves as the primary porosity through which the bulk flow of the interstitial fluid occurs, a secondary porosity network comprising the capillaries and venous system allows for its partial absorption into the blood. The correspondence principle is used in deriving a time-dependent analytical solution to the proposed model. It allows for identical poroelastic formulation of the original poroviscoelastic problem in the Laplace transform space. Hydrocephalus generally refers to a class of medical conditions which share the ventricles enlargement as a common feature. A set of published data from induced hydrocephalus and follow-up perfusion of cats' brains is used for quantitative characterization of the proposed model. A selected portion of these data including the ventricular volume and rate of fluid absorption from the perfused brain, together with the forward model solution, is utilized via an inverse problem technique to find proper estimations of the model parameters. Results show significant improvement in model predictions of the experimental data. The convoluted and coupled solution results are presented through the time-dependent plots of the ventricular volume undergoing the perfusion experiment. The plots demonstrate the intricate interplay of viscous and poroelastic diffusive time scales, and their competition in reaching the steady state response of the system.

[1]  A. Sahar The effect of pressure on the production of cerebrospinal fluid by the choroid plexus. , 1972, Journal of the neurological sciences.

[2]  G. Hochwald,et al.  Passage of cerebrospinal fluid into cranial venous sinuses in normal and experimental hydrocephalic cats. , 1970, Experimental neurology.

[3]  M. Klarica,et al.  Development of hydrocephalus and classical hypothesis of cerebrospinal fluid hydrodynamics: Facts and illusions , 2011, Progress in Neurobiology.

[4]  Benedikt Wirth,et al.  Analytic solution during an infusion test of the linear unsteady poroelastic equations in a spherically symmetric model of the brain. , 2008, Mathematical medicine and biology : a journal of the IMA.

[5]  A. Morelli Inverse Problem Theory , 2010 .

[6]  O. Abdullah,et al.  Differential vulnerability of white matter structures to experimental infantile hydrocephalus detected by diffusion tensor imaging , 2014, Child's Nervous System.

[7]  K. Miller,et al.  Reassessment of brain elasticity for analysis of biomechanisms of hydrocephalus. , 2004, Journal of biomechanics.

[8]  R. Friendship,et al.  Development of cerebrospinal fluid absorption sites in the pig and rat: connections between the subarachnoid space and lymphatic vessels in the olfactory turbinates , 2006, Anatomy and Embryology.

[9]  G. Hochwald,et al.  Experimental hydrocephalus. Changes in cerebrospinal fluid dynamics as a function of time. , 1972, Archives of neurology.

[10]  Younane N. Abousleiman,et al.  Generalized Biot's theory and Mandel's problem of multiple‐porosity and multiple‐permeability poroelasticity , 2014 .

[11]  Jay D. Humphrey,et al.  Review Paper: Continuum biomechanics of soft biological tissues , 2003, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[12]  Y. Ventikos,et al.  Multiscale Modelling for Cerebrospinal Fluid Dynamics: Multicompartmental Poroelacticity and the Role of AQP4 , 2014 .

[13]  R. Buist,et al.  Intracranial biomechanics of acute experimental hydrocephalus in live rats. , 2012, Neurosurgery.

[14]  Y. Abousleiman,et al.  Poromechanics Response of Inclined Wellbore Geometry in Fractured Porous Media , 2005 .

[15]  D. Greitz,et al.  Cerebrospinal fluid circulation and associated intracranial dynamics. A radiologic investigation using MR imaging and radionuclide cisternography. , 1993, Acta radiologica. Supplementum.

[16]  G. Hochwald,et al.  Cerebrospinal fluid absorption in animals with experimental obstructive hydrocephalus. , 1969, Archives of neurology.

[17]  G. Hochwald,et al.  Cerebrospinal fluid production and histological observations in animals with experimental obstructive hydrocephalus. , 1969, Experimental neurology.

[18]  Dimitri E. Beskos,et al.  On the theory of consolidation with double porosity—II , 1982 .

[19]  H. Jones,et al.  Progressive Changes in Cortical Water and Electrolyte Content at Three Stages of Rat Infantile Hydrocephalus and the Effect of Shunt Treatment , 1998, Experimental Neurology.

[20]  I. Tekaya,et al.  Dynamics of hydrocephalus: a physical approach , 2012, Journal of biological physics.

[21]  Yiannis Ventikos,et al.  Coupling Poroelasticity and CFD for Cerebrospinal Fluid Hydrodynamics , 2009, IEEE Transactions on Biomedical Engineering.

[22]  M. D. Del Bigio,et al.  Cerebral water content in silicone oil-induced hydrocephalic rabbits. , 1987, Pediatric neuroscience.

[23]  D. Rall,et al.  Extracellular space of brain as determined by diffusion of inulin from the ventricular system , 1962 .

[24]  David W. Holman,et al.  In vitro model of cerebrospinal fluid outflow through human arachnoid granulations. , 2006, Investigative ophthalmology & visual science.

[25]  M. Johnston The importance of lymphatics in cerebrospinal fluid transport. , 2003, Lymphatic research and biology.

[26]  MR imaging of cerebrospinal fluid dynamics in health and disease. On the vascular pathogenesis of communicating hydrocephalus and benign intracranial hypertension. , 1994, Acta radiologica.

[27]  Y. Abousleiman,et al.  The dilative intake of poroelastic inclusions an alternative to the Mandel–Cryer effect , 2009 .

[28]  Zoltán Molnár,et al.  A hydroelastic model of hydrocephalus , 2005, Journal of Fluid Mechanics.

[29]  G. Hochwald Animal Models of Hydrocephalus: Recent Developments , 1985, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[30]  K. Miller,et al.  Constitutive model of brain tissue suitable for finite element analysis of surgical procedures. , 1999, Journal of biomechanics.

[31]  EMPIRICAL CHARACTERIZATION OF ECONOMIC MINERAL (KAOLIN) DEPOSITS FROM VERTICAL ELECTRICAL SOUNDING INVESTIGATIONS IN UBULU-UKU, DELTA STATE NIGERIA , 2012 .

[32]  D. Marquardt An Algorithm for Least-Squares Estimation of Nonlinear Parameters , 1963 .

[33]  Alina Jurcoane,et al.  Diffusion tensor imaging in patients with adult chronic idiopathic hydrocephalus. , 2010 .

[34]  G. Holzapfel,et al.  Brain tissue deforms similarly to filled elastomers and follows consolidation theory , 2006 .

[35]  Younane N. Abousleiman,et al.  A micromechanically consistent poroviscoelasticity theory for rock mechanics applications , 1993 .

[36]  P. Kitanidis Quasi‐Linear Geostatistical Theory for Inversing , 1995 .

[37]  M. Biot General Theory of Three‐Dimensional Consolidation , 1941 .

[38]  Maurice A. Biot,et al.  Nonlinear and semilinear rheology of porous solids , 1973 .

[39]  G. Hochwald,et al.  Periventricular water content. Effect of pressure in experimental chronic hydrocephalus. , 1970, Archives of neurology.

[40]  P. Taylor,et al.  On the theory of diffusion in linear viscoelastic media , 1982 .

[41]  R. Fishman,et al.  Experimental obstructive hydrocephalus. Changes in the cerebrum. , 1963, Archives of neurology.

[42]  G. Hochwald,et al.  Alternate pathway for cerebrospinal fluid absorption in animals with experimental obstructive hydrocephalus. , 1969, Experimental neurology.

[43]  Mariusz Kaczmarek,et al.  The hydromechanics of hydrocephalus: Steady-state solutions for cylindrical geometry , 1997 .

[44]  M. D. Del Bigio,et al.  Intracranial biomechanics following cortical contusion in live rats. , 2013, Journal of neurosurgery.

[45]  M. Czosnyka,et al.  Computerized infusion test compared to steady pressure constant infusion test in measurement of resistance to CSF outflow , 2005, Acta Neurochirurgica.

[46]  A. Torvik,et al.  The pathology of experimental obstructive hydrocephalus , 1976, Acta Neuropathologica.

[47]  G. Roth,et al.  Evolution of the brain and intelligence , 2005, Trends in Cognitive Sciences.

[48]  E. Strecker,et al.  Cerebrospinal fluid absorption in communicating hydrocephalus , 1973, Neurology.

[49]  R. Buist,et al.  Age-dependence of intracranial viscoelastic properties in living rats. , 2011, Journal of the mechanical behavior of biomedical materials.

[50]  Ning Liu,et al.  Inverse Theory for Petroleum Reservoir Characterization and History Matching , 2008 .

[51]  M. Biot General solutions of the equations of elasticity and consolidation for a porous material , 1956 .

[52]  L. Bilston,et al.  Unconfined compression of white matter. , 2007, Journal of biomechanics.

[53]  Younane N. Abousleiman,et al.  Poromechanics Solutions to Plane Strain and Axisymmetric Mandel-Type Problems in Dual-Porosity and Dual-Permeability Medium , 2010 .

[54]  Daniel J. R. Christensen,et al.  Sleep Drives Metabolite Clearance from the Adult Brain , 2013, Science.

[55]  Amin Mehrabian,et al.  General solutions to poroviscoelastic model of hydrocephalic human brain tissue. , 2011, Journal of theoretical biology.

[56]  G. Hochwald,et al.  Experimental hydrocephalus: cerebrospinal fluid formation and ventricular size as a function of intraventricular pressure. , 1970, Journal of the neurological sciences.

[57]  Brett J Tully,et al.  Cerebral water transport using multiple-network poroelastic theory: application to normal pressure hydrocephalus , 2010, Journal of Fluid Mechanics.

[58]  Younane N. Abousleiman,et al.  Poroviscoelastic analysis of borehole and cylinder problems , 1996 .

[59]  Nic D. Leipzig,et al.  Unconfined creep compression of chondrocytes. , 2004, Journal of biomechanics.

[60]  M. Biot THEORY OF DEFORMATION OF A POROUS VISCOELASTIC ANISOTROPIC SOLID , 1956 .

[61]  D N Levine,et al.  The pathogenesis of normal pressure hydrocephalus: A theoretical analysis , 1999, Bulletin of mathematical biology.

[62]  Younane N. Abousleiman,et al.  Gassmann equations and the constitutive relations for multiple‐porosity and multiple‐permeability poroelasticity with applications to oil and gas shale , 2015 .

[63]  Kenneth Levenberg A METHOD FOR THE SOLUTION OF CERTAIN NON – LINEAR PROBLEMS IN LEAST SQUARES , 1944 .

[64]  Brett J Tully,et al.  Multicompartmental Poroelasticity as a Platform for the Integrative Modeling of Water Transport in the Brain , 2013 .

[65]  Marek Czosnyka,et al.  Changes in Cerebral Blood Flow during Cerebrospinal Fluid Pressure Manipulation in Patients with Normal Pressure Hydrocephalus: A Methodological Study , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[66]  P. Cahill,et al.  Direct In Vivo Observation of Transventricular Absorption in the Hydrocephalic Dog Using Magnetic Resonance Imaging , 1994, Investigative radiology.

[67]  J. Pappenheimer,et al.  Perfusion of the cerebral ventricular system in unanesthetized goats , 1962 .

[68]  Janet M. Miller,et al.  Reduction of astrogliosis and microgliosis by cerebrospinal fluid shunting in experimental hydrocephalus , 2007, Cerebrospinal Fluid Research.

[69]  Herbert F. Wang Theory of Linear Poroelasticity with Applications to Geomechanics and Hydrogeology , 2000 .

[70]  J. D. Burton,et al.  The physics of the cranial cavity, hydrocephalus and normal pressure hydrocephalus: mechanical interpretation and mathematical model. , 1976, Surgical neurology.

[71]  J. Rice,et al.  Some basic stress diffusion solutions for fluid‐saturated elastic porous media with compressible constituents , 1976 .

[72]  Y. Abousleiman,et al.  Correspondence principle between anisotropic poroviscoelasticity and poroelasticity using micromechanics and application to compression of orthotropic rectangular strips , 2012 .

[73]  Giuseppe Tenti,et al.  Mathematical pressure volume models of the cerebrospinal fluid , 1998, Appl. Math. Comput..

[74]  J. Pappenheimer,et al.  Bulk flow and diffusion in the cerebrospinal fluid system of the goat. , 1962, The American journal of physiology.

[75]  M. D. Bigio,et al.  Neuropathological changes caused by hydrocephalus , 2004, Acta Neuropathologica.

[76]  Karol Miller,et al.  Brain mechanics For neurosurgery: modeling issues , 2002, Biomechanics and modeling in mechanobiology.

[77]  Gaffar Gailani,et al.  Hierarchical poroelasticity: movement of interstitial fluid between porosity levels in bones , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[78]  Dean S. Oliver,et al.  Memoir 71, Chapter 10: Reducing Uncertainty in Geostatistical Description with Well-Testing Pressure Data , 1997 .

[79]  M Czosnyka,et al.  Clinical assessment of cerebrospinal fluid dynamics in hydrocephalus. Guide to interpretation based on observational study , 2011, Acta neurologica Scandinavica.

[80]  Steven E. Katz,et al.  Cerebrospinal fluid outflow: An evolving perspective , 2008, Brain Research Bulletin.

[81]  Geoffrey T Manley,et al.  Accelerated Progression of Kaolin-Induced Hydrocephalus in Aquaporin-4-Deficient Mice , 2006, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[82]  N. Tamaki,et al.  Biomechanics of hydrocephalus: a new theoretical model. , 1987, Neurosurgery.

[83]  F. B. Hildebrand,et al.  Introduction To Numerical Analysis , 1957 .

[84]  James G. Berryman,et al.  EXTENSION OF POROELASTIC ANALYSIS TO DOUBLE-POROSITY MATERIALS: NEW TECHNIQUE IN MICROGEOMECHANICS , 2002 .

[85]  L. Edvinsson,et al.  RELATION BETWEEN INTRACRANIAL PRESSURE AND VENTRICULAR SIZE AT VARIOUS STAGES OF EXPERIMENTAL HYDROCEPHALUS , 1971, Acta neurologica Scandinavica.

[86]  G. E. Vates,et al.  A Paravascular Pathway Facilitates CSF Flow Through the Brain Parenchyma and the Clearance of Interstitial Solutes, Including Amyloid β , 2012, Science Translational Medicine.