Mechanical characterization of human brain tissue

Acta Biomaterialia

Volumn 48, Issue , 2017, Pages 319-340

  Budday, S ^a   Sommer, G ^b   Birkl, C ^c   Langkammer, C ^c   Haybaeck, J ^c   Kohnert, J ^a   Bauer, M ^a   Paulsen, F ^a   Steinmann, P ^a   Kuhl, E ^d   Holzapfel, G A ^b,e  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^c MEDICAL UNIVERSITY OF GRAZ   (Austria)

^d STANFORD UNIVERSITY   (United States)

^e NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

Human brain; Hyperelastic modeling; Mechanical testing; Mooney Rivlin model; Ogden model

Indexed keywords

BEHAVIORAL RESEARCH; BIOMECHANICS; CONSTITUTIVE MODELS; DIFFUSION TENSOR IMAGING; ELASTICITY; FORECASTING; HISTOLOGY; MAGNETIC RESONANCE IMAGING; MECHANICAL TESTING; PARAMETER ESTIMATION; SHEAR STRESS; STRAIN RATE; TENSORS; TISSUE;

BRAIN TISSUE; COMPRESSION TENSIONS; HUMAN BRAIN; HYPERELASTIC MODELS; LOADING CONDITION; LOADING MODES; MECHANICAL BEHAVIOR; MOONEY-RIVLIN MODEL; OGDEN MODEL; TENSION ASYMMETRY;

BRAIN;

ADULT; AGED; ARTICLE; BASAL GANGLION; BIOMECHANICS; BRAIN ASYMMETRY; BRAIN CORTEX; BRAIN FUNCTION; BRAIN TISSUE; CADAVER; CONTROLLED STUDY; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; FEMALE; HUMAN; HUMAN TISSUE; MALE; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SHEAR STRESS; VERY ELDERLY; ANISOTROPY; BRAIN; CALIBRATION; COMPRESSIVE STRENGTH; ELASTICITY; GRAY MATTER; MECHANICAL STRESS; PHYSIOLOGY; THEORETICAL MODEL; TIME FACTOR;

AGED; AGED, 80 AND OVER; ANISOTROPY; BIOMECHANICAL PHENOMENA; BRAIN; CALIBRATION; COMPRESSIVE STRENGTH; ELASTICITY; FEMALE; GRAY MATTER; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MODELS, THEORETICAL; STRESS, MECHANICAL; TIME FACTORS;

EID: 85007413942     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2016.10.036     Document Type: Article

References (72)

1. [1] Goriely, A., Geers, M.G., Holzapfel, G.A., Jayamohan, J., Jérusalem, A., Sivaloganathan, S., Squier, W., van Dommelen, J.A., Waters, S., Kuhl, E., Mechanics of the brain: perspectives, challenges, and opportunities. Biomech. Model. Mechanobiol. 14 (2015), 931–965.
2. [2] Cloots, R.J.H., Van Dommelen, J.A.W., Kleiven, S., Geers, M.G.D., Multi-scale mechanics of traumatic brain injury: predicting axonal strains from head loads. Biomech. Model. Mechanobiol. 12 (2013), 137–150.
3. [3] Harding, B., Risdon, R.A., Krous, H.F., Shaken baby syndrome. BMJ 328 (2004), 720–721.
4. [4] Kansal, A., Torquato, S., Harsh, G., Chiocca, E., Deisboeck, T., Simulated brain tumor growth dynamics using a three-dimensional cellular automaton. J. Theor. Biol. 203 (2000), 367–382.
5. [5] Richman, D.P., Stewart, R.M., Hutchinson, J., Cavincss, V.S. Jr, Mechanical mode of brain convolutional development. Science 189 (1975), 18–21.
6. [6] Budday, S., Steinmann, P., Kuhl, E., The role of mechanics during brain development. J. Mech. Phys. Solids 72 (2014), 75–92.
7. [7] Tallinen, T., Chung, J.Y., Rousseau, F., Girard, N., Lefèvre, J., Mahadevan, L., On the growth and form of cortical convolutions. Nat. Phys. 12 (2016), 588–593.
8. [8] Cloots, R.J.H., Van Dommelen, J.A.W., Geers, M.G.D., A tissue-level anisotropic criterion for brain injury based on microstructural axonal deformation. J. Mech. Behav. Biomed. Mater. 5 (2012), 41–52.
9. [9] Wu, L.C., Nangia, V., Bui, K., Hammoor, B., Kurt, M., Hernandez, F., Kuo, C., Camarillo, D.B., In vivo evaluation of wearable head impact sensors. Ann. Biomed. Eng. 44 (2016), 1234–1245.
10. [10] Wilkie, K.P., Drapaca, C.S., Sivaloganathan, S., Aging impact on brain biomechanics with applications to hydrocephalus. Math. Med. Biol. 29 (2012), 145–161.
11. [11] Goriely, A., Budday, S., Kuhl, E., Neuromechanics: from neurons to brain. Adv. Appl. Mech. 48 (2015), 79–139.
12. [12] Miller, K., Biomechanics of the Brain. 2011, Springer Science & Business Media.
13. [13] Thibault, K.L., Margulies, S.S., Age-dependent material properties of the porcine cerebrum: effect on pediatric inertial head injury criteria. J. Biomech. 31 (1998), 1119–1126.
14. [14] Shuck, L.Z., Advani, S.H., Rheological response of human brain tissue in shear. J. Basic Eng. 94 (1972), 905–911.
15. [15] Prange, M.T., Margulies, S.S., Regional, directional, and age-dependent properties of the brain undergoing large deformation. J. Biomech. Eng. 124 (2002), 244–252.
16. [16] Velardi, F., Fraternali, F., Angelillo, M., Anisotropic constitutive equations and experimental tensile behavior of brain tissue. Biomech. Model. Mechanobiol. 5 (2006), 53–61.
17. [17] Feng, Y., Okamoto, R.J., Namani, R., Genin, G.M., Bayly, P.V., Measurements of mechanical anisotropy in brain tissue and implications for transversely isotropic material models of white matter. J. Mech. Behav. Biomed. Mater. 23 (2013), 117–132.
18. [18] Jin, X., Zhu, F., Mao, H., Shen, M., Yang, K.H., A comprehensive experimental study on material properties of human brain tissue. J. Biomech. 46 (2013), 2795–2801.
19. [19] Gefen, A., Gefen, N., Zhu, Q., Raghupathi, R., Margulies, S.S., Age-dependent changes in material properties of the brain and braincase of the rat. J. Neurotrauma 20 (2003), 1163–1177.
20. [20] Elkin, B.S., Ilankovan, A., Morrison, B., Age-dependent regional mechanical properties of the rat hippocampus and cortex. J. Biomech. Eng., 132, 2010, 011010.
21. [21] Chatelin, S., Vappou, J., Roth, S., Raul, J.-S., Willinger, R., Towards child versus adult brain mechanical properties. J. Mech. Behav. Biomed. Mater. 6 (2012), 166–173.
22. [22] Finan, J.D., Elkin, B.S., Pearson, E.M., Kalbian, I.L., Morrison, B. III, Viscoelastic properties of the rat brain in the sagittal plane: effects of anatomical structure and age. Ann. Biomed. Eng. 40 (2012), 70–78.
23. [23] McCracken, P.J., Manduca, A., Felmlee, J., Ehman, R.L., Mechanical transient-based magnetic resonance elastography. Magn. Reson. Med. 53 (2005), 628–639.
24. [24] Green, M.A., Bilston, L.E., Sinkus, R., In vivo brain viscoelastic properties measured by magnetic resonance elastography. NMR Biomed. 21 (2008), 755–764.
25. [25] 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. J. Biomech. 43 (2010), 2986–2992.
26. [26] Van Dommelen, J.A.W., Van der Sande, T.P.J., Hrapko, M., Peters, G.W.M., Mechanical properties of brain tissue by indentation: interregional variation. J. Mech. Behav. Biomed. Mater. 3 (2010), 158–166.
27. [27] Johnson, C.L., McGarry, M.D., Gharibans, A.A., Weaver, J.B., Paulsen, K.D., Wang, H., Olivero, W.C., Sutton, B.P., Georgiadis, J.G., Local mechanical properties of white matter structures in the human brain. Neuroimage 79 (2013), 145–152.
28. [28] Budday, S., Nay, R., de Rooij, R., Steinmann, P., Wyrobek, T., Ovaert, T.C., Kuhl, E., Mechanical properties of gray and white matter brain tissue by indentation. J. Mech. Behav. Biomed. Mater. 46 (2015), 318–330.
29. [29] Weickenmeier, J., de Rooij, R., Budday, S., Steinmann, P., Ovaert, T.C., Kuhl, E., Brain stiffness increases with myelin content. Acta Biomater. 42 (2016), 265–272.
30. [30] Darvish, K., Crandall, J.R., Nonlinear viscoelastic effects in oscillatory shear deformation of brain tissue. Med. Eng. Phys. 9 (2001), 633–645.
31. [31] Nicolle, S., Lounis, M., Willinger, R., Shear properties of brain tissue over a frequency range relevant for automotive impact situations: new experimental results. Stapp Car Crash J. 48 (2004), 239–258.
32. [32] Garo, A., Hrapko, M., Van Dommelen, J.A.W., Peters, G.W.M., Towards a reliable characterisation of the mechanical behaviour of brain tissue: the effects of post-mortem time and sample preparation. Biorheology 44 (2007), 51–58.
33. [33] Fallenstein, G., Hulce, V.D., Melvin, J.W., Dynamic mechanical properties of human brain tissue. J. Biomech. 2 (1969), 217–226.
34. [34] M.S. Estes, J.H. McElhaney, Response of brain tissue to compressive loading, 1970. ASME Paper, No. 70-BHF-13.
35. [35] Galford, J.E., McElhaney, J.H., A viscoelastic study of scalp, brain, and dura. J. Biomech. 3 (1970), 211–221.
36. [36] Donnelly, B.R., Medige, J., Shear properties of human brain tissue. J. Biomech. Eng. 119 (1997), 423–432.
37. [37] Franceschini, G., Bigoni, D., Regitnig, P., Holzapfel, G.A., Brain tissue deforms similarly to filled elastomers and follows consolidation theory. J. Mech. Phys. Solids 54 (2006), 2592–2620.
38. [38] Miller, K., Chinzei, K., Constitutive modelling of brain tissue: experiment and theory. J. Biomech. 30 (1997), 1115–1121.
39. [39] Miller, K., Chinzei, K., Mechanical properties of brain tissue in tension. J. Biomech. 35 (2002), 483–490.
40. [40] Rashid, B., Destrade, M., Gilchrist, M.D., Mechanical characterization of brain tissue in compression at dynamic strain rates. J. Mech. Behav. Biomed. Mater. 10 (2012), 23–38.
41. [41] Rashid, B., Destrade, M., Gilchrist, M.D., Mechanical characterization of brain tissue in simple shear at dynamic strain rates. J. Mech. Behav. Biomed. Mater. 28 (2013), 71–85.
42. [42] Rashid, B., Destrade, M., Gilchrist, M.D., Mechanical characterization of brain tissue in tension at dynamic strain rates. J. Mech. Behav. Biomed. Mater. 33 (2014), 43–54.
43. [43] Bilston, L.E., Liu, Z., Phan-Thien, N., Large strain behaviour of brain tissue in shear: some experimental data and differential constitutive model. Biorheology 38 (2001), 335–345.
44. [44] Pogoda, K., Chin, L., Georges, P.C., Byfield, F.J., Bucki, R., Kim, R., Weaver, M., Wells, R.G., Marcinkiewicz, C., Janmey, P.A., Compression stiffening of brain and its effect on mechanosensing by glioma cells. New J. Phys., 16, 2014, 075002.
45. [45] Sommer, G., Schriefl, A.J., Andrä, M., Sacherer, M., Viertler, C., Wolinski, H., Holzapfel, G.A., Biomechanical properties and microstructure of human ventricular myocardium. Acta Biomater. 24 (2015), 172–192.
46. [46] de Rooij, R., Kuhl, E., Constitutive modeling of brain tissue: current perspectives. Appl. Mech. Rev., 68, 2016, 010801.
47. [47] Kaster, T., Sack, I., Samani, A., Measurement of the hyperelastic properties of ex vivo brain tissue slices. J. Biomech. 44 (2011), 1158–1163.
48. [48] Moran, R., Smith, J.H., Garća, J.J., Fitted hyperelastic parameters for human brain tissue from reported tension, compression, and shear tests. J. Biomech. 47 (2014), 3762–3766.
49. [49] Ogden, R.W., Large deformation isotropic elasticity-on the correlation of theory and experiment for incompressible rubberlike solids. Proceedings of the Royal Society of London A: Mathematical, Physical and Engineering Sciences, vol. 326, 1972, The Royal Society, 565–584.
50. [50] Demiray, H., A note on the elasticity of soft biological tissues. J. Biomech. 5 (1972), 309–311.
51. [51] Gent, A., A new constitutive relation for rubber. Rubber Chem. Technol. 69 (1996), 59–61.
52. [52] Holzapfel, G.A., Nonlinear Solid Mechanics. A Continuum Approach for Engineering. 2000, John Wiley & Sons, Chichester.
53. [53] Mihai, L.A., Chin, L., Janmey, P.A., Goriely, A., A comparison of hyperelastic constitutive models applicable to brain and fat tissues. J. R. Soc. Interface, 12, 2015, 20150486.
54. [54] Smith, S., Jenkinson, M., Woolrich, M., Beckmann, C., Behrens, T., Johansen-Berg, H., Bannister, P., De Luca, M., Drobnjak, I., Flitney, D., Niazy, R., Saunders, J., Vickers, J., Zhang, Y., De Stefano, N., Brady, J., Matthews, P., Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 (2004), 208–219.
55. [55] Woolrich, M., Jbabdi, S., Patenaude, B., Chappell, M., Makni, S., Behrens, T., Beckmann, C., Jenkinson, M., Smith, S., Bayesian analysis of neuroimaging data in FSL. Neuroimage 45 (2009), 173–186.
56. [56] Sommer, G., Eder, M., Kovacs, L., Pathak, H., Bonitz, L., Mueller, C., Regitnig, P., Holzapfel, G.A., Multiaxial mechanical properties and constitutive modeling of human adipose tissue: a basis for preoperative simulations in plastic and reconstructive surgery. Acta Biomater. 9 (2013), 9036–9048.
57. [57] Prevost, T.P., Balakrishnan, A., Suresh, S., Socrate, S., Biomechanics of brain tissue. Acta Biomater. 7 (2011), 83–95.
58. [58] Jérusalem, A., Dao, M., Continuum modeling of a neuronal cell under blast loading. Acta Biomater. 8 (2012), 3360–3371.
59. [59] Holzapfel, G.A., Ogden, R.W., Constitutive modelling of arteries. Proc. R. Soc. London A 466 (2010), 1551–1597.
60. [60] Pervin, F., Chen, W.W., Dynamic mechanical response of bovine gray matter and white matter brain tissues under compression. J. Biomech. 42 (2009), 731–735.
61. [61] Lindenberg, R., Fisher, R.S., Durlacher, S.H., Lovitt, W.V. Jr, Freytag, E., Lesions of the corpus callosum following blunt mechanical trauma to the head. Am. J. Pathol. 31 (1955), 297–317.
62. [62] Cecil, K.M., Hills, E.C., Sandel, M.E., Smith, D.H., McIntosh, T.K., Mannon, L.J., Sinson, G.P., Bagley, L.J., Grossman, R.I., Lenkinski, R.E., Proton magnetic resonance spectroscopy for detection of axonal injury in the splenium of the corpus callosum of brain-injured patients. J. Neurosurg. 88 (1998), 795–801.
63. [63] Koser, D.E., Moeendarbary, E., Hanne, J., Kuerten, S., Franze, K., CNS cell distribution and axon orientation determine local spinal cord mechanical properties. Biophys. J. 108 (2015), 2137–2147.
64. [64] 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 39 (2008), 231–237.
65. [65] Papazoglou, S., Hirsch, S., Braun, J., Sack, I., Multifrequency inversion in magnetic resonance elastography. Phys. Med. Biol., 57, 2012, 2329.
66. [66] Whittall, K.P., Mackay, A.L., Graeb, D.A., Nugent, R.A., Li, D.K., Paty, D.W., In vivo measurement of T2 distributions and water contents in normal human brain. Magn. Reson. Med. 37 (1997), 34–43.
67. [67] Baborie, A., Kuschinsky, W., Lack of relationship between cellular density and either capillary density or metabolic rate in different regions of the brain. Neurosci. Lett. 404 (2006), 20–22.
68. [68] Cavaglia, M., Dombrowski, S.M., Drazba, J., Vasanji, A., Bokesch, P.M., Janigro, D., Regional variation in brain capillary density and vascular response to ischemia. Brain Res. 910 (2001), 81–93.
69. [69] McKee, C.T., Last, J.A., Russell, P., Murphy, C.J., Indentation versus tensile measurements of Young's modulus for soft biological tissues. Tissue Eng. Part B: Rev. 17 (2011), 155–164.
70. [70] Budday, S., Raybaud, C., Kuhl, E., A mechanical model predicts morphological abnormalities in the developing human brain. Sci. Rep., 4, 2014, 5644.
71. [71] Cheng, S., Bilston, L.E., Unconfined compression of white matter. J. Biomech. 40 (2007), 117–124.
72. [72] Ehlers, W., Wagner, A., Multi-component modelling of human brain tissue: a contribution to the constitutive and computational description of deformation, flow and diffusion processes with application to the invasive drug-delivery problem. Comput. Methods Biomech. Biomed. Eng. 18 (2015), 861–879.