Skip to main content
Log in

A visco-hyperelastic model of brain tissue incorporating both tension/compression asymmetry and volume compressibility

  • Original Paper
  • Published:
Acta Mechanica Aims and scope Submit manuscript

Abstract

The understanding of the mechanical behavior of the brain tissue is essential to prevent the occurrence of potential brain damage, such as traumatic brain injury. Recent experimental results showed that brain tissue exhibits significant tension/compression asymmetry. Due to the migration and diffusion of interstitial fluid, brain tissue also shows a moderate volume compressibility during loading. These mechanical characteristics have a strong impact on the deformation response of brain tissue. In this paper, a visco-hyperelastic constitutive model incorporating both tension/compression asymmetry and volume compressibility is proposed to describe the mechanical behavior of brain tissue under various loading modes. An Ogden-type model with the addition of a viscoelastic part is used to characterize the tension/compression asymmetry as well as the viscoelastic properties. Poisson’s ratio was introduced as a phenomenological index to represent the total volume change as well as the compressibility/recoverability. The mechanical responses of brain tissue under uniaxial tension, unconfined compression, stress relaxation, and cyclic compression were reproduced with a good capture of the tension/compression asymmetry, volume compressibility, significant viscoelastic properties, and cyclic hysteresis behaviors. The good agreement with the experimental data implies that the proposed model has a strong capability to describe the complex mechanical performance of brain tissue under a variety of loading conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Taylor, C.A., Bell, J.M., Breiding, M.J., Xu, L.: Traumatic brain injury–related emergency department visits, hospitalizations, and deaths-united states, 2007 and 2013. MMWR Surveill Summ. 66(SS-9), 1–16 (2017)

  2. Miller, K., Chinzei, K.: Mechanical properties of brain tissue in tension. J. Biomech. 35(4), 483–490 (2002)

    Article  Google Scholar 

  3. Zhang, W., Zhang, R.R., Wu, F., Feng, L.I., Yu, S.B., CW, Wu: Differences in the viscoelastic features of white and grey matter in tension. J. Biomech. 49(16), 3990–3995 (2016)

    Article  Google Scholar 

  4. Labus, K.M., Puttlitz, C.M.: Viscoelasticity of brain corpus callosum in biaxial tension. J. Mech. Phys. Solids 96, 591–604 (2016)

    Article  Google Scholar 

  5. Pervin, F., Chen, W.W.: Dynamic mechanical response of bovine gray matter and white matter brain tissues under compression. J. Biomech. 42(6), 731–735 (2009)

    Article  Google Scholar 

  6. Prevost, T.P., Balakrishnan, A., Suresh, S., Socrate, S.: Biomechanics of brain tissue. Acta Biomat. 7(1), 83–95 (2011)

    Article  Google Scholar 

  7. Bilston, L.E., Liu, Z., Phan-Thien, N.: Linear viscoelastic properties of bovine brain tissue in shear. Biorheology 34(6), 377–385 (1997)

    Article  Google Scholar 

  8. Rashid, B., Destrade, M., Gilchrist, M.D.: Mechanical characterization of brain tissue in simple shear at dynamic strain rates. J. Mech. Behav. Biomed. 28, 71–85 (2013)

    Article  Google Scholar 

  9. Moran, R., Smith, J.H., García, J.J.: Fitted hyperelastic parameters for human brain tissue from reported tension, compression, and shear tests. J. Biomech. 47(15), 3762–3766 (2014)

    Article  Google Scholar 

  10. Destrade, M., Gilchrist, M., Murphy, J.G., Rashid, B., Saccomandi, G.: Extreme softness of brain matter in simple shear. Int. J. Nonlin. Mech. 75, 54–58 (2015)

    Article  Google Scholar 

  11. Li, G., Zhang, J., Wang, K., Wang, M., Gao, C., Ma, C.: Experimental research of mechanical behavior of porcine brain tissue under rotational shear stress. J. Mech. Behav. Biomed. 57, 224–234 (2016)

    Article  Google Scholar 

  12. Balakrishnan, A.: Development of novel dynamic indentation techniques for soft tissue applications. Ph.D. thesis. https://dspace.mit.edu/handle/1721.1/429872007. (2007)

  13. Van Dommelen, J., Van der Sande, T., Hrapko, M., Peters, G.: Mechanical properties of brain tissue by indentation: interregional variation. J. Mech. Behav. Biomed. Mater. 3(2), 158–166 (2010)

    Article  Google Scholar 

  14. 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 Biomat. 7(12), 4090–4101 (2011)

    Article  Google Scholar 

  15. 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, 318–330 (2015)

    Article  Google Scholar 

  16. MacManus, D.B., Pierrat, B., Murphy, J.G., Gilchrist, M.D.: A viscoelastic analysis of the P56 mouse brain under large-deformation dynamic indentation. Acta Biomat. 48, 309–318 (2017)

    Article  Google Scholar 

  17. Feng, Y., Lee, C.H., Sun, L., Ji, S., Zhao, X.: Characterizing white matter tissue in large strain via asymmetric indentation and inverse finite element modeling. J. Mech. Behav. Biomed. Mater. 65, 490–501 (2017)

    Article  Google Scholar 

  18. Budday, S., Sommer, G., Birkl, C., Langkammer, C., Haybaeck, J., Kohnert, J., Bauer, M., Paulsen, F., Steinmann, P., Kuhl, E.: Mechanical characterization of human brain tissue. Acta Biomat. 48, 319–340 (2017)

    Article  Google Scholar 

  19. 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(7), 075002 (2014)

    Article  Google Scholar 

  20. 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(110), 20150486 (2015)

    Article  Google Scholar 

  21. Mihai, L.A., Budday, S., Holzapfel, G.A., Kuhl, E., Goriely, A.: A family of hyperelastic models for human brain tissue. J. Mech. Phys. Solids 106, 60–79 (2017)

    Article  MathSciNet  Google Scholar 

  22. Lodish, H.: Molecular Cell Biology, 6th edn. Macmillan, New York (2008)

    Google Scholar 

  23. de Rooij, R., Kuhl, E.: Constitutive modeling of brain tissue: current perspectives. Appl. Mech. Rev. 68(1), 010801 (2016)

    Article  Google Scholar 

  24. Shuck, L.Z., Advani, S.H.: Rheological response of human brain tissue in shear. J. Basic Eng. 94, 905–911 (1972)

    Article  Google Scholar 

  25. Jenson, D., Unnikrishnan, V.U.: Energy dissipation of nanocomposite based helmets for blast-induced traumatic brain injury mitigation. Compos. Struct. 121, 211–216 (2015)

    Article  Google Scholar 

  26. Hrapko, M., Van Dommelen, J., Peters, G., Wismans, J.: The mechanical behaviour of brain tissue: large strain response and constitutive modelling. Biorheology 43(5), 623–636 (2006)

    Google Scholar 

  27. 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(4), 335–345 (2001)

    Google Scholar 

  28. Cloots, R., Van Dommelen, J., Nyberg, T., Kleiven, S., Geers, M.: Micromechanics of diffuse axonal injury: influence of axonal orientation and anisotropy. Biomech. Model. Mechan. 10(3), 413–422 (2011)

    Article  Google Scholar 

  29. Laksari, K., Shafieian, M., Darvish, K.: Constitutive model for brain tissue under finite compression. J. Biomech. 45(4), 642–646 (2012)

    Article  Google Scholar 

  30. Ogden, R.W.: Large deformation isotropic elasticity-on the correlation of theory and experiment for incompressible rubberlike solids. Proc. R. Soc. Lond. A 326, 565–584 (1972)

    Article  MATH  Google Scholar 

  31. Mendis, K., Stalnaker, R., Advani, S.: A constitutive relationship for large deformation finite element modeling of brain tissue. J. Biomech. Eng. 117(3), 279–285 (1995)

    Article  Google Scholar 

  32. Miller, K., Chinzei, K.: Constitutive modelling of brain tissue: experiment and theory. J. Biomech. 30(11), 1115–1121 (1997)

    Article  Google Scholar 

  33. Prange, M.T., Margulies, S.S.: Regional, directional, and age-dependent properties of the brain undergoing large deformation. J. Biomech. Eng. 124(2), 244–252 (2002)

    Article  Google Scholar 

  34. Budday, S., Sommer, G., Hayback, J., Steinmann, P., Holzapfel, G.A., Kuhl, E.: Rheological characterization of human brain tissue. Acta Biomat. 60, 315–329 (2017)

    Article  Google Scholar 

  35. Budday, S., Sommer, G., Holzapfel, G.A., Steinmann, P., Kuhl, E.: Viscoelastic parameter identification of human brain tissue. J. Mech. Behav. Biomed. Mater. 74, 463–476 (2017)

    Article  Google Scholar 

  36. Haslach Jr., H.W., Leahy, L.N., Riley, P., Gullapalli, R., Xu, S., Hsieh, A.H.: Solid-extracellular fluid interaction and damage in the mechanical response of rat brain tissue under confined compression. J. Mech. Behav. Biomed. Mater. 29, 138–150 (2014)

    Article  Google Scholar 

  37. Grandjean, A.C., Grandjean, N.R.: Dehydration and cognitive performance. J. Am. Coll. Nutr. 26(5), 549S–554S (2007)

    Article  Google Scholar 

  38. Yoon, J., Cai, S., Suo, Z., Hayward, R.C.: Poroelastic swelling kinetics of thin hydrogel layers: comparison of theory and experiment. Soft Matter 6(23), 6004–6012 (2010)

    Article  Google Scholar 

  39. Wang, Q.-M., Mohan, A.C., Oyen, M.L., Zhao, X.-H.: Separating viscoelasticity and poroelasticity of gels with different length and time scales. Acta Mech. Sinica-PRC 30(1), 20–27 (2014)

    Article  MATH  MathSciNet  Google Scholar 

  40. Hu, Y., Suo, Z.: Viscoelasticity and poroelasticity in elastomeric gels. Acta Mech. Solida Sin. 25(5), 441–458 (2012)

    Article  Google Scholar 

  41. Kaczmarek, M., Subramaniam, R.P., Neff, S.R.: The hydromechanics of hydrocephalus: steady-state solutions for cylindrical geometry. B. Math. Biol. 59, 295–323 (1997)

    Article  MATH  Google Scholar 

  42. Kyriacou, S.K., Mohamed, A., Miller, K., Neff, S.: Brain mechanics for neurosurgery: modeling issues. Biomech. Model. Mechan. 1, 151–164 (2002)

    Article  Google Scholar 

  43. Ames, N.M.: An internal variable theory for isotropic visco-elastic-plastic solids: application to indentation of amorphous polymeric solids. Master thesis. https://dspace.mit.edu/handle/1721.1/33162. (2003)

  44. Anand, L., Ames, N.: On modeling the micro-indentation response of an amorphous polymer. Int. J. Plasticity 22(6), 1123–1170 (2006)

    Article  MATH  Google Scholar 

  45. Voyiadjis, G.Z., Samadi-Dooki, A.: Hyperelastic modeling of the human brain tissue: effects of no-slip boundary condition and compressibility on the uniaxial deformation. J. Mech. Behav. Biomed. Mater. 83, 63–78 (2018)

    Article  Google Scholar 

  46. Kleiven, S.: Predictors for traumatic brain injuries evaluated through accident reconstructions (No. 2007-22-0003). SAE Technical Paper. (2007)

  47. Wang, R., Sarntinoranont, M.: Biphasic analysis of rat brain slices under creep indentation shows nonlinear tension-compression behavior. J. Mech. Behav. Biomed. Mater. 89, 1–8 (2019)

    Article  Google Scholar 

  48. Samadidooki, A.: Experimental, Analytical, and Numerical Evaluation of the Mechanical Properties of the Brain Tissue. Doctoral thesis. https://digitalcommons.lsu.edu/gradschool_dissertations/4622/. (2018)

  49. Abdulhafez, M., Kadry, K., Zaazoue, M., Goumnerova, L.C., Bedewy, M.: Biomechanical root cause analysis of complications in head immobilization devices for pediatric neurosurgery. In: ASME 2018 13th International Manufacturing Science and Engineering Conference (pp. V001T05A007-V001T05A007). American Society of Mechanical Engineers. (2018)

  50. Viano, D.C., Casson, I.R., Pellman, E.J., Zhang, L., King, A.I., Yang, K.H.: Concussion in professional football: brain responses by finite element analysis: part 9. Neurosurgery 57(5), 891–916 (2005)

    Article  Google Scholar 

  51. Gu, L., Chafi, M.S., Ganpule, S., Chandra, N.: The influence of heterogeneous meninges on the brain mechanics under primary blast loading. Compos. Part B- Eng. 43(8), 3160–3166 (2012)

    Article  Google Scholar 

  52. Nolan, D., Gower, A., Destrade, M., Ogden, R., McGarry, J.: A robust anisotropic hyperelastic formulation for the modelling of soft tissue. J. Mech. Behav. Biomed. Mater. 39, 48–60 (2014)

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 11472231, 11872322) and partially supported by Doctoral Innovation Fund Program of Southwest Jiaotong University (Grant No. D-CX201835).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Han Jiang.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhu, Z., Jiang, C. & Jiang, H. A visco-hyperelastic model of brain tissue incorporating both tension/compression asymmetry and volume compressibility. Acta Mech 230, 2125–2135 (2019). https://doi.org/10.1007/s00707-019-02383-1

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00707-019-02383-1

Navigation