Mechanical properties of porcine brain tissue in vivo and ex vivo estimated by MR elastography.

The mechanical properties of brain tissue in vivo determine the response of the brain to rapid skull acceleration. These properties are thus of great interest to the developers of mathematical models of traumatic brain injury (TBI) or neurosurgical simulations. Animal models provide valuable insight that can improve TBI modeling. In this study we compare estimates of mechanical properties of the Yucatan mini-pig brain in vivo and ex vivo using magnetic resonance elastography (MRE) at multiple frequencies. MRE allows estimations of properties in soft tissue, either in vivo or ex vivo, by imaging harmonic shear wave propagation. Most direct measurements of brain mechanical properties have been performed using samples of brain tissue ex vivo. It has been observed that direct estimates of brain mechanical properties depend on the frequency and amplitude of loading, as well as the time post-mortem and condition of the sample. Using MRE in the same animals at overlapping frequencies, we observe that porcine brain tissue in vivo appears stiffer than porcine brain tissue samples ex vivo at frequencies of 100 Hz and 125 Hz, but measurements show closer agreement at lower frequencies.

[1]  Hillary D. Schwarb,et al.  Viscoelasticity of subcortical gray matter structures , 2016, Human brain mapping.

[2]  G. Genin,et al.  Measurements of mechanical anisotropy in brain tissue and implications for transversely isotropic material models of white matter. , 2013, Journal of the mechanical behavior of biomedical materials.

[3]  N. Phan-Thien,et al.  Large strain behaviour of brain tissue in shear: some experimental data and differential constitutive model. , 2001, Biorheology.

[4]  Rémy Willinger,et al.  Magnetic resonance elastography compared with rotational rheometry for in vitro brain tissue viscoelasticity measurement , 2007, Magnetic Resonance Materials in Physics, Biology and Medicine.

[5]  D. Shepherd,et al.  Frequency dependent viscoelastic properties of porcine bladder. , 2015, Journal of the mechanical behavior of biomedical materials.

[6]  P V Bayly,et al.  Magnetic resonance elastography of slow and fast shear waves illuminates differences in shear and tensile moduli in anisotropic tissue. , 2016, Journal of biomechanics.

[7]  van der Tpj Tom Sande,et al.  Mechanical properties of brain tissue by indentation: interregional variation. , 2010, Journal of the mechanical behavior of biomedical materials.

[8]  Ralph Sinkus,et al.  Demyelination reduces brain parenchymal stiffness quantified in vivo by magnetic resonance elastography , 2012, Proceedings of the National Academy of Sciences.

[9]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[10]  K D Paulsen,et al.  Viscoelastic power law parameters of in vivo human brain estimated by MR elastography. , 2017, Journal of the mechanical behavior of biomedical materials.

[11]  J. van Dommelen,et al.  The influence of test conditions on characterization of the mechanical properties of brain tissue. , 2008, Journal of biomechanical engineering.

[12]  P V Bayly,et al.  Viscoelastic properties of the ferret brain measured in vivo at multiple frequencies by magnetic resonance elastography. , 2013, Journal of biomechanics.

[13]  G. Grant,et al.  Mild traumatic brain injury in U.S. soldiers returning from Iraq. , 2008, The New England journal of medicine.

[14]  Curtis L. Johnson,et al.  Observation of direction-dependent mechanical properties in the human brain with multi-excitation MR elastography. , 2016, Journal of the mechanical behavior of biomedical materials.

[15]  Mickael Tanter,et al.  Viscoelastic shear properties of in vivo breast lesions measured by MR elastography. , 2005, Magnetic resonance imaging.

[16]  P V Bayly,et al.  Frequency-dependent viscoelastic parameters of mouse brain tissue estimated by MR elastography , 2011, Physics in medicine and biology.

[17]  B. V. Van Beers,et al.  MR elastography. , 2008, Gastroenterologie clinique et biologique.

[18]  Rémy Willinger,et al.  Assessment of in vivo and post-mortem mechanical behavior of brain tissue using magnetic resonance elastography. , 2008, Journal of biomechanics.

[19]  J. Langlois,et al.  The Epidemiology and Impact of Traumatic Brain Injury: A Brief Overview , 2006, The Journal of head trauma rehabilitation.

[20]  M. Gilchrist,et al.  Mechanical characterization of brain tissue in compression at dynamic strain rates. , 2012, Journal of the mechanical behavior of biomedical materials.

[21]  E. H. Clayton,et al.  Transmission, attenuation and reflection of shear waves in the human brain , 2012, Journal of The Royal Society Interface.

[22]  P V S Lee,et al.  Modified Bilston nonlinear viscoelastic model for finite element head injury studies. , 2006, Journal of biomechanical engineering.

[23]  J. F. Greenleaf,et al.  Magnetic resonance elastography: Non-invasive mapping of tissue elasticity , 2001, Medical Image Anal..

[24]  A. Manduca,et al.  Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. , 1995, Science.

[25]  P. Asbach,et al.  Noninvasive assessment of the rheological behavior of human organs using multifrequency MR elastography: a study of brain and liver viscoelasticity , 2007, Physics in medicine and biology.

[26]  P. Bovendeerd,et al.  The large shear strain dynamic behaviour of in-vitro porcine brain tissue and a silicone gel model material. , 2000, Stapp car crash journal.

[27]  I. Sack,et al.  Algebraic Helmholtz inversion in planar magnetic resonance elastography , 2008, Physics in medicine and biology.

[28]  Dagmar Krefting,et al.  The Influence of Physiological Aging and Atrophy on Brain Viscoelastic Properties in Humans , 2011, PloS one.

[29]  Abbas Samani,et al.  MR elastography of the human heart: Noninvasive assessment of myocardial elasticity changes by shear wave amplitude variations , 2009, Magnetic resonance in medicine.

[30]  Curtis L. Johnson,et al.  The Relationship of Three-Dimensional Human Skull Motion to Brain Tissue Deformation in Magnetic Resonance Elastography Studies. , 2017, Journal of biomechanical engineering.

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

[32]  J. van Dommelen,et al.  The mechanical behaviour of brain tissue: large strain response and constitutive modelling. , 2006, Biorheology.

[33]  Philip V Bayly,et al.  Measurement of the dynamic shear modulus of mouse brain tissue in vivo by magnetic resonance elastography. , 2008, Journal of biomechanical engineering.

[34]  S. Margulies,et al.  Age-dependent material properties of the porcine cerebrum: effect on pediatric inertial head injury criteria. , 1998, Journal of biomechanics.

[35]  R. Willinger,et al.  Shear Properties of Brain Tissue over a Frequency Range Relevant for Automotive Impact Situations: New Experimental Results. , 2004, Stapp car crash journal.

[36]  Curtis L. Johnson,et al.  Magnetic resonance elastography of the brain using multishot spiral readouts with self‐navigated motion correction , 2013, Magnetic resonance in medicine.

[37]  A. Constantinesco,et al.  Fifty years of brain tissue mechanical testing: from in vitro to in vivo investigations. , 2010, Biorheology.

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

[39]  A K Ommaya,et al.  Mechanical properties of tissues of the nervous system. , 1968, Journal of biomechanics.

[40]  M. Rajadhyaksha,et al.  Confocal imaging-guided laser ablation of basal cell carcinomas: an ex vivo study. , 2015, The Journal of investigative dermatology.

[41]  Philip V Bayly,et al.  Estimation of material parameters from slow and fast shear waves in an incompressible, transversely isotropic material. , 2015, Journal of biomechanics.

[42]  K B Arbogast,et al.  Material characterization of the brainstem from oscillatory shear tests. , 1998, Journal of biomechanics.

[43]  Dieter Klatt,et al.  Wide-range dynamic magnetic resonance elastography. , 2011, Journal of biomechanics.

[44]  P V Bayly,et al.  Viscoelastic properties of soft gels: comparison of magnetic resonance elastography and dynamic shear testing in the shear wave regime , 2011, Physics in medicine and biology.

[45]  Dieter Klatt,et al.  The impact of aging and gender on brain viscoelasticity , 2009, NeuroImage.

[46]  A. Holbourn MECHANICS OF HEAD INJURIES , 1943 .

[47]  小林 英津子,et al.  305 Magnetic Resonance Elastographyのための加振装置の開発とその評価(OS3-(2) バイオメカニクスにおける新分野の開拓 : 組織粘弾性の無侵襲計測,オーガナイズドセッション) , 2009 .

[48]  K Darvish,et al.  Frequency dependence of complex moduli of brain tissue using a fractional Zener model , 2005, Physics in medicine and biology.

[49]  J. Georgiadis,et al.  Suitability of poroelastic and viscoelastic mechanical models for high and low frequency MR elastography. , 2015, Medical physics.

[50]  S. Aoki,et al.  Magnetic resonance , 2012, International Journal of Computer Assisted Radiology and Surgery.

[51]  N. Phan-Thien,et al.  Linear viscoelastic properties of bovine brain tissue in shear. , 1997, Biorheology.