Measurements of mechanical anisotropy in brain tissue and implications for transversely isotropic material models of white matter

Journal of the Mechanical Behavior of Biomedical Materials

Volumn 23, Issue , 2013, Pages 117-132

  Feng, Yuan ^a   Okamoto, Ruth J ^a   Namani, Ravi ^a   Genin, Guy M ^a   Bayly, Philip V ^a  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

Brain tissue; Constitutive modeling; Transverse isotropy

Indexed keywords

BRAIN TISSUE; EXPERIMENTAL MEASUREMENTS; FINITE ELEMENT MODELS; MECHANICAL ANISOTROPY; STRAIN ENERGY DENSITY FUNCTIONS; TRANSVERSE ISOTROPY; TRANSVERSELY ISOTROPIC; TRANSVERSELY ISOTROPIC MATERIALS;

ANISOTROPY; BRAIN; CONSTITUTIVE MODELS; ELASTIC MODULI; FIBERS; FINITE ELEMENT METHOD; SHEAR STRAIN; STRAIN ENERGY; TISSUE;

LOADING;

ANISOTROPY; ARTICLE; BRAIN TISSUE; ENERGY; HUMAN; LOAD CARRYING CAPACITY; MEASUREMENT; MECHANICS; NERVE FIBER; PRIORITY JOURNAL; SHEAR FLOW; STRESS STRAIN RELATIONSHIP; TENSILE STRENGTH; WHITE MATTER;

ANIMALS; ANISOTROPY; BIOMECHANICAL PHENOMENA; BRAIN; ELASTICITY; FINITE ELEMENT ANALYSIS; LINEAR MODELS; MATERIALS TESTING; MECHANICAL PROCESSES; MODELS, BIOLOGICAL; SHEAR STRENGTH; SHEEP;

EID: 84877908658     PISSN: 17516161     EISSN: 18780180     Source Type: Journal    
DOI: 10.1016/j.jmbbm.2013.04.007     Document Type: Article

References (69)

1. Abney T.M., Feng Y., Pless R., Okamoto R.J., Genin G.M., Bayly P.V. Principal component analysis of dynamic relative displacement fields estimated from MR images. PLoS One 2011, 6:e22063.
2. Alexander G.M., Godwin D.W. Presynaptic inhibition of corticothalamic feedback by metabotropic glutamate receptors. Journal of Neurophysiology 2005, 94:163-175.
3. Arbogast K.B., Margulies S.S. Material characterization of the brainstem from oscillatory shear tests. Journal of Biomechanics 1998, 31:801-807.
4. Atay S.M., Kroenke C.D., Sabet A., Bayly P.V. Measurement of the dynamic shear modulus of mouse brain tissue in vivo by magnetic resonance elastography. Journal of Biomechanical Engineering 2008, 130:21013.
5. Bayly P.V., Black E.E., Pedersen R.C., Leister E.P., Genin G.M. In vivo imaging of rapid deformation and strain in an animal model of traumatic brain injury. Journal of Biomechanics 2006, 39:1086-1095.
6. Bayly P.V., Cohen T.S., Leister E.P., Ajo D., Leuthardt E.C., Genin G.M. Deformation of the human brain induced by mild acceleration. Journal of Neurotrauma 2005, 22:845-856.
7. Bischoff J.E. Static indentation of anisotropic biomaterials using axially asymmetric indenters--a computational study. Journal of Biomechanical Engineering 2004, 126:498-505.
8. Bower A.F. Applied Mechanics of Solids 2010, CRC Press, Boca Raton, FL. 1st ed.
9. Brody D.L., Mac Donald C., Kessens C.C., Yuede C., Parsadanian M., Spinner M., Kim E., Schwetye K.E., Holtzman D.M., Bayly P.V. Electromagnetic controlled cortical impact device for precise, graded experimental traumatic brain injury. Journal of Neurotrauma 2007, 24:657-673.
10. Chatelin S., Constantinesco A., Willinger R. Fifty years of brain tissue mechanical testing: from in vitro to in vivo investigations. Biorheology 2010, 47:255-276.
11. Chatelin S., Deck C., Willinger R. An anisotropic viscous hyperelastic constitutive law for brain material finite-element modeling. Journal of Biorrheology 2012.
12. Cheng S., Clarke E.C., Bilston L.E. Rheological properties of the tissues of the central nervous system: a review. Medical Engineering & Physics 2008, 30:1318-1337.
13. Christ A.F., Franze K., Gautier H., Moshayedi P., Fawcett J., Franklin R.J., Karadottir R.T., Guck J. Mechanical difference between white and gray matter in the rat cerebellum measured by scanning force microscopy. Journal of Biomechanics 2010, 43:2986-2992.
14. Clayton E.H., Garbow J.R., Bayly P.V. Frequency-dependent viscoelastic parameters of mouse brain tissue estimated by MR elastography. Physics in Medicine & Biology 2011, 56:2391-2406.
15. Clayton E.H., Genin G.M., Bayly P.V. Transmission, attenuation and reflection of shear waves in the human brain. Journal of the Royal Society Interface 2012.
16. Cloots R.J., van Dommelen J.A., Geers M.G. A tissue-level anisotropic criterion for brain injury based on microstructural axonal deformation. Journal of the Mechanical Behavior of Biomedical Materials 2012, 5:41-52.
17. Coats B., Margulies S.S., Ji S. Parametric study of head impact in the infant. Stapp Car Crash Journal 2007, 51:1-15.
18. Coronado V.G., Xu L., Basavaraju S.V., McGuire L.C., Wald M.M., Faul M.D., Guzman B.R., Hemphill J.D. Surveillance for traumatic brain injury-related deaths-United States, 1997-2007. MMWR Surveillance Summaries 2011, 60:1-32.
19. Cox M.A., Driessen N.J., Bouten C.V., Baaijens F.P. Mechanical characterization of anisotropic planar biological soft tissues using large indentation: a computational feasibility study. Journal of Biomechanical Engineering 2006, 128:428-436.
20. van Dommelen J.A., van der Sande T.P., Hrapko M., Peters G.W. Mechanical properties of brain tissue by indentation: interregional variation. Journal of the Mechanical Behavior of Biomedical Materials 2010, 3:158-166.
21. Elkin B.S., Ilankova A., Morrison B. Dynamic, regional mechanical properties of the porcine brain: indentation in the coronal plane. Journal of Biomechanical Engineering 2011, 133:071009.
22. Elkin B.S., Ilankovan A.I., Morrison B. A detailed viscoelastic characterization of the P17 and adult rat brain. Journal of Neurotrauma 2011, 28:2235-2244.
23. Fallenstein G.T., Hulce V.D., Melvin J.W. Dynamic mechanical properties of human brain tissue. Journal of Biomechanics 1969, 2:217-226.
24. Feng Y., Abney T.M., Okamoto R.J., Pless R.B., Genin G.M., Bayly P.V. Relative brain displacement and deformation during constrained mild frontal head impact. Journal of the Royal Society Interface 2010, 7:1677-1688.
25. Galford J.E., McElhaney J.H. A viscoelastic study of scalp, brain, and dura. Journal of Biomechanics 1970, 3:211-221.
26. Garo A., Hrapko M., van Dommelen J.A., Peters G.W. Towards a reliable characterisation of the mechanical behaviour of brain tissue: the effects of post-mortem time and sample preparation. Biorheology 2007, 44:51-58.
27. Gasser T.C., Ogden R.W., Holzapfel G.A. Hyperelastic modelling of arterial layers with distributed collagen fibre orientations. Journal of the Royal Society Interface 2006, 3:15-35.
28. Gefen A., Margulies S.S. Are in vivo and in situ brain tissues mechanically similar?. Journal of Biomechanics 2004, 37:1339-1352.
29. Gennarelli T.A., Thibault L.E., Adams J.H., Graham D.I., Thompson C.J., Marcincin R.P. Diffuse axonal injury and traumatic coma in the primate. Annals of Neurology 1982, 12:564-574.
30. Green M.A., Bilston L.E., Sinkus R. In vivo brain viscoelastic properties measured by magnetic resonance elastography. NMR in Biomedicine 2008, 21:755-764.
31. Holzapfel G. Nonlinear Solid Mechanics: A Continuum Approach for Engineering 2000, John Wiley & Sons, Inc.
32. Holzapfel G.A., Ogden R.W. On planar biaxial tests for anisotropic nonlinearly elastic solids. Mathematics and Mechanics of Solids 2009, 14:474-489.
33. Hrapko M., van Dommelen J.A., Peters G.W., Wismans J.S. Characterisation of the mechanical behaviour of brain tissue in compression and shear. Biorheology 2008, 45:663-676.
34. Hrapko M., van Dommelen J.A., Peters G.W., Wismans J.S. The influence of test conditions on characterization of the mechanical properties of brain tissue. Journal of Biomechanical Engineering 2008, 130:031003.
35. Ji S., Margulies S.S. In vivo pons motion within the skull. Journal of Biomechanics 2007, 40:92-99.
36. Ji S., Zhu Q., Dougherty L., Margulies S.S. In vivo measurements of human brain displacement. Stapp Car Crash Journal 2004, 48:227-237.
37. Kaster T., Sack I., Samani A. Measurement of the hyperelastic properties of ex vivo brain tissue slices. Journal of Biomechanics 2011.
38. Kruse S.A., Rose G.H., Glaser K.J., Manduca A., Felmlee J.P., Jack C.R., Ehman R.L. Magnetic resonance elastography of the brain. NeuroImage 2008, 39:231-237.
39. LaPlaca M.C., Cullen D.K., McLoughlin J.J., Cargill R.S. High rate shear strain of three-dimensional neural cell cultures: a new in vitro traumatic brain injury model. Journal of Biomechanics 2005, 38:1093-1105.
40. Margulies S.S., Thibault L.E. A proposed tolerance criterion for diffuse axonal injury in man. Journal of Biomechanics 1992, 25:917-923.
41. McAllister T.W., Ford J.C., Ji S., Beckwith J.G., Flashman L.A., Paulsen K., Greenwald R.M. Maximum principal strain and strain rate associated with concussion diagnosis correlates with changes in corpus callosum white matter indices. Annals of Biomedical Engineering 2012, 40:127-140.
42. Meaney D.F. Relationship between structural modeling and hyperelastic material behavior: application to CNS white matter. Biomechanics and Modeling in Mechanobiology 2003, 1:279-293.
43. Merodio J., Ogden R.W. Instabilities and loss of ellipticity in fiber-reinforced compressible non-linearly elastic solids under plane deformation. International Journal of Solids and Structures 2003, 40:4707-4727.
44. Merodio J., Ogden R.W. Mechanical response of fiber-reinforced incompressible non-linearly elastic solids. International Journal of Nonlinear Mechanics 2005, 40:213-227.
45. Morrison B., Cater H.L., Wang C.C., Thomas F.C., Hung C.T., Ateshian G.A., Sundstrom L.E. A tissue level tolerance criterion for living brain developed with an in vitro model of traumatic mechanical loading. Stapp Car Crash Journal 2003, 47:93-105.
46. Namani R., Feng Y., Okamoto R.J., Jesuraj N., Sakiyama-Elbert S.E., Genin G.M., Bayly P.V. Elastic characterization of transversely isotropic soft materials by dynamic shear and asymmetric indentation. Journal of Biomechanical Engineering 2012, 134:061004.
47. Nicolle S., Lounis M., Willinger R., Palierne J.F. Shear linear behavior of brain tissue over a large frequency range. Biorheology 2005, 42:209-223.
48. Ning X., Zhu Q., Lanir Y., Margulies S.S. A transversely isotropic viscoelastic constitutive equation for brainstem undergoing finite deformation. Journal of Biomechanical Engineering 2006, 128:925-933.
49. Okamoto R.J., Clayton E.H., Bayly P.V. Viscoelastic properties of soft gels: comparison of magnetic resonance elastography and dynamic shear testing in the shear wave regime. Physics in Medicine & Biology 2011, 56:6379-6400.
50. Parker D.F. Elastic wave propagation in strongly anisotropic solids. Continuum Theory of the Mechanics of Fibre-Reinforced Composites 1984, 217-244. Springer Verlag, New York. A.J.M. Spencer (Ed.).
51. Pattison A.J., Lollis S.S., Perrinez P.R., Perreard I.M., McGarry M.D., Weaver J.B., Paulsen K.D. Time-harmonic magnetic resonance elastography of the normal feline brain. Journal of Biomechanics 2010, 43:2747-2752.
52. Prange M.T., Margulies S.S. Regional, directional, and age-dependent properties of the brain undergoing large deformation. Journal of Biomechanical Engineering 2002, 124:244-252.
53. Prange M.T., Meaney D.F., Margulies S.S. Defining brain mechanical properties: effects of region, direction, and species. Stapp Car Crash Journal 2000, 44:205-213.
54. Prevost T.P., Jin G., de Moya M.A., Alam H.B., Suresh S., Socrate S. Dynamic mechanical response of brain tissue in indentation in vivo, in situ and in vitro. Acta Biomater 2011, 7:4090-4101.
55. Qin, E.C., Sinkus, R., Geng, G., Cheng, S., Green, M., Rae, C.D., Bilston, L.E., 2012. Combining MR elastography and diffusion tensor imaging for the assessment of anisotropic mechanical properties: a phantom study. Journal of Magnetic Resonance Imaging.
56. Qiu G.Y., Pence T.J. Remarks on the behavior of simple directionally reinforced incompressible nonlinearly elastic solids. Journal of Elasticity 1997, 49:1-30.
57. Riek K., Klatt D., Nuzha H., Mueller S., Neumann U., Sack I., Braun J. Wide-range dynamic magnetic resonance elastography. Journal of Biomechanics 2011, 44:1380-1386.
58. Romano A., Scheel M., Hirsch S., Braun J., Sack I. In vivo waveguide elastography of white matter tracts in the human brain. Magnetic Resonance in Medicine 2012.
59. Sabet A.A., Christoforou E., Zatlin B., Genin G.M., Bayly P.V. Deformation of the human brain induced by mild angular head acceleration. Journal of Biomechanics 2008, 41:307-315.
60. Sack I., Beierbach B., Hamhaber U., Klatt D., Braun J. Non-invasive measurement of brain viscoelasticity using magnetic resonance elastography. NMR in Biomedicine 2008, 21:265-271.
61. Shuck L.Z., Advani S.H. Rheological response of human brain-tissue in shear. Journal of Basic Engineering 1972, 94:905-911.
62. Smith D.H., Meaney D.F. Axonal damage in traumatic brain injury. Neuroscientist 2000, 6:483-495.
63. Spencer A.J.M. Continuum Theory of the Mechanics of Fibre-Reinforced Composites 1984, Springer-Verlag, New York.
64. Ueno K., Melvin J.W., Li L., Lighthall J.W. Development of tissue level brain injury criteria by finite element analysis. Journal of Neurotrauma 1995, 12:695-706.
65. Velardi F., Fraternali F., Angelillo M. Anisotropic constitutive equations and experimental tensile behavior of brain tissue. Biomechanics and Modeling in Mechanobiology 2006, 5:53-61.
66. Weiss J.A., Maker B.N., Govindjee S. Finite element implementation of incompressible, transversely isotropic hyperelasticity. Computer Methods in Applied Mechanics and Engineering 1996, 135:107-128.
67. Wright R.M., Ramesh K.T. An axonal strain injury criterion for traumatic brain injury. Biomechanics and Modeling in Mechanobiology 2012, 11:245-260.
68. Zhang J., Green M.A., Sinkus R., Bilston L.E. Viscoelastic properties of human cerebellum using magnetic resonance elastography. Journal of Biomechanics 2011, 44:1909-1913.
69. Zhang L., Yang K.H., King A.I. A proposed injury threshold for mild traumatic brain injury. Journal of Biomechanical Engineering 2004, 126:226-236.