SpringerLink
Log in

An Image Registration-Based Morphing Technique for Generating Subject-Specific Brain Finite Element Models

  • Original Article
  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Finite element (FE) models of the brain are crucial for investigating the mechanisms of traumatic brain injury (TBI). However, FE brain models are often limited to a single neuroanatomy because the manual development of subject-specific models is time consuming. The objective of this study was to develop a pipeline to automatically generate subject-specific FE brain models using previously developed nonlinear image registration techniques, preserving both external and internal neuroanatomical characteristics. To verify the morphing-induced mesh distortions did not influence the brain deformation response, strain distributions predicted using the morphed model were compared to those from manually created voxel models of the same subject. Morphed and voxel models were generated for 44 subjects ranging in age, and simulated using head kinematics from a football concussion case. For each subject, brain strain distributions predicted by each model type were consistent, and differences in strain prediction was less than 4% between model type. This automated technique, taking approximately 2 h to generate a subject-specific model, will facilitate interdisciplinary research between the biomechanics and neuroimaging fields and could enable future use of biomechanical models in the clinical setting as a tool for improving diagnosis.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Alshareef, A., J. S. Giudice, J. Forman, R. S. Salzar, and M. B. Panzer. A novel method for quantifying human in situ whole brain deformation under rotational loading using sonomicrometry. J. Neurotrauma 35:780–789, 2018.

    Article  PubMed  Google Scholar 

  2. Alshareef, A., J. S. Giudice, J. Forman, D. F. Shedd, K. A. Reynier, T. Wu, S. Sochor, M. R. Sochor, R. S. Salzar, and M. B. Panzer. Biomechanics of the human brain during dynamic rotation of the head. J. Neurotrauma 2020. https://doi.org/10.1089/neu.2019.6847.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Avants, B., C. Epstein, M. Grossman, and J. Gee. Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain. Med. Image Anal. 12:26–41, 2008.

    Article  CAS  PubMed  Google Scholar 

  4. Avants, B. B., P. T. Schoenemann, and J. C. Gee. Lagrangian frame diffeomorphic image registration: morphometric comparison of human and chimpanzee cortex. Med. Image Anal. 10:397–412, 2006.

    Article  PubMed  Google Scholar 

  5. Avants, B. B., N. J. Tustison, G. Song, P. A. Cook, A. Klein, and J. C. Gee. A reproducible evaluation of ANTs similarity metric performance in brain image registration. NeuroImage 54:2033–2044, 2011.

    Article  PubMed  Google Scholar 

  6. Avants, B. B., N. J. Tustison, J. Wu, P. A. Cook, and J. C. Gee. An open source multivariate framework for n-tissue segmentation with evaluation on public data. Neuroinformatics 9:381–400, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Avants, B. B., P. Yushkevich, J. Pluta, D. Minkoff, M. Korczykowski, J. Detre, and J. C. Gee. The optimal template effect in hippocampus studies of diseased populations. NeuroImage 49:2457–2466, 2010.

    Article  PubMed  Google Scholar 

  8. Beckwith, J. G., W. Zhao, S. Ji, A. G. Ajamil, R. P. Bolander, J. J. Chu, T. W. McAllister, J. J. Crisco, S. M. Duma, S. Rowson, S. P. Broglio, K. M. Guskiewicz, J. P. Mihalik, S. Anderson, B. Schnebel, P. Gunnar Brolinson, M. W. Collins, and R. M. Greenwald. Estimated brain tissue response following impacts associated with and without diagnosed concussion. Ann. Biomed. Eng. 46:819–830, 2018.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Bendlin, B. B., M. L. Ries, M. Lazar, A. L. Alexander, R. J. Dempsey, H. A. Rowley, J. E. Sherman, and S. C. Johnson. Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. NeuroImage 42:503–514, 2008.

    Article  PubMed  Google Scholar 

  10. Centers for Disease Control and Prevention. Report to Congress on Traumatic Brain Injury in the United States: Epidemiology and Rehabilitation., 2015.

  11. Crum, W. R., L. D. Griffin, D. L. G. Hill, and D. J. Hawkes. Zen and the art of medical image registration: correspondence, homology, and quality. NeuroImage 20:1425–1437, 2003.

    Article  CAS  PubMed  Google Scholar 

  12. Darling, T., J. Muthuswamy, and S. D. Rajan. Finite element modeling of human brain response to football helmet impacts. Comput. Methods Biomech. Biomed. Eng. 19:1432–1442, 2016.

    Article  CAS  Google Scholar 

  13. de Grau, S., A. Post, T. B. Hoshizaki, and M. D. Gilchrist. Effects of surface compliance on the dynamic response and strains sustained by a player’s helmeted head during ice hockey impacts. Proc. Inst. Mech. Eng. Part P J. Sports Eng. Technol. 1754337119871866, 2019.

  14. Dennis, E. L., X. Hua, J. Villalon-Reina, L. M. Moran, C. Kernan, T. Babikian, R. Mink, C. Babbitt, J. Johnson, C. C. Giza, P. M. Thompson, and R. F. Asarnow. Tensor-based morphometry reveals volumetric deficits in moderate/severe pediatric traumatic brain injury. J. Neurotrauma 33:840–852, 2016.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Farbota, K. D. M., A. Sodhi, B. B. Bendlin, D. G. McLaren, G. Xu, H. A. Rowley, and S. C. Johnson. Longitudinal volumetric changes following traumatic brain injury: a tensor-based morphometry study. J. Int. Neuropsychol. Soc. 18:1006–1018, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Faul, M., M. M. Wald, L. Xu, and V. G. Coronado. Traumatic brain injury in the United States; emergency department visits, hospitalizations, and deaths, 2002-2006., 2010.

  17. Fonov, V., A. C. Evans, K. Botteron, C. R. Almli, R. C. McKinstry, D. L. Collins, and Brain Development Cooperative Group. Unbiased average age-appropriate atlases for pediatric studies. Neuroimage 54(1):313–327, 2011.

    Article  PubMed  Google Scholar 

  18. Gabler, L. F., J. R. Crandall, and M. B. Panzer. Investigating brain injury tolerance in the Sagittal Plane using a finite element model of the human head. Int. J. Automot. Eng. 7:37–43, 2016.

    Article  Google Scholar 

  19. Gabler, L. F., J. R. Crandall, and M. B. Panzer. Development of a metric for predicting brain strain responses using head kinematics. Ann. Biomed. Eng. 46:972–985, 2018.

    Article  PubMed  Google Scholar 

  20. Ghosh, S. S., S. Kakunoori, J. Augustinack, A. Nieto-Castanon, I. Kovelman, N. Gaab, J. A. Christodoulou, C. Triantafyllou, J. D. E. Gabrieli, and B. Fischl. Evaluating the validity of volume-based and surface-based brain image registration for developmental cognitive neuroscience studies in children 4 to 11years of age. NeuroImage 53:85–93, 2010.

    Article  PubMed  Google Scholar 

  21. Giudice, J. S., W. Zeng, T. Wu, A. Alshareef, D. F. Shedd, and M. B. Panzer. An analytical review of the numerical methods used for finite element modeling of traumatic brain injury. Ann. Biomed. Eng. 47:1855–1872, 2019.

    Article  PubMed  Google Scholar 

  22. Glaister, J., A. Carass, D. L. Pham, J. A. Butman, and J. L. Prince. Automatic falx cerebri and tentorium cerebelli segmentation from magnetic resonance images., 2017.

  23. Hanson, J. L., M. K. Chung, B. B. Avants, E. A. Shirtcliff, J. C. Gee, R. J. Davidson, and S. D. Pollak. Early stress is associated with alterations in the orbitofrontal cortex: a tensor-based morphometry investigation of brain structure and behavioral risk. J. Neurosci. 30:7466–7472, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hua, X., A. D. Leow, N. Parikshak, S. Lee, M.-C. Chiang, A. W. Toga, C. R. Jack, M. W. Weiner, and P. M. Thompson. Tensor-based morphometry as a neuroimaging biomarker for Alzheimer’s disease: an MRI study of 676 AD, MCI, and normal subjects. NeuroImage 43:458–469, 2008.

    Article  PubMed  Google Scholar 

  25. Ji, S., H. Ghadyani, R. P. Bolander, J. G. Beckwith, J. C. Ford, T. W. McAllister, L. A. Flashman, K. D. Paulsen, K. Ernstrom, S. Jain, R. Raman, L. Zhang, and R. M. Greenwald. Parametric comparisons of intracranial mechanical responses from three validated finite element models of the human Head. Ann. Biomed. Eng. 42:11–24, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Johnson, B., K. Zhang, M. Gay, S. Horovitz, M. Hallett, W. Sebastianelli, and S. Slobounov. Alteration of brain default network in subacute phase of injury in concussed individuals: resting-state fMRI study. Neuroimage 59:511–518, 2012.

    Article  PubMed  Google Scholar 

  27. Kim, J., B. Avants, S. Patel, J. Whyte, B. H. Coslett, J. Pluta, J. A. Detre, and J. C. Gee. Structural consequences of diffuse traumatic brain injury: a large deformation tensor-based morphometry study. NeuroImage 39:1014–1026, 2008.

    Article  PubMed  Google Scholar 

  28. Kim, J. J., and A. D. Gean. Imaging for the diagnosis and management of traumatic brain injury. Neurotherapeutics 8:39–53, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kimpara, H., Y. Nakahira, M. Iwamoto, K. Miki, et al. Investigation of anteroposterior head-neck responses during severe frontal impacts using a brain-spinal cord complex FE model. Stapp Car Crash J. 50:509, 2006.

    PubMed  Google Scholar 

  30. Kipps, C. M., A. J. Duggins, N. Mahant, L. Gomes, J. Ashburner, and E. A. McCusker. Progression of structural neuropathology in preclinical Huntington’s disease: a tensor based morphometry study. J. Neurol. Neurosurg. Psychiatry 76:650–655, 2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Klein, A., J. Andersson, B. A. Ardekani, J. Ashburner, B. Avants, M.-C. Chiang, G. E. Christensen, D. L. Collins, J. Gee, P. Hellier, J. H. Song, M. Jenkinson, C. Lepage, D. Rueckert, P. Thompson, T. Vercauteren, R. P. Woods, J. J. Mann, and R. V. Parsey. Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. NeuroImage 46:786–802, 2009.

    Article  PubMed  Google Scholar 

  32. Lepore, N., C. Brun, Y.-Y. Chou, M.-C. Chiang, R. A. Dutton, K. M. Hayashi, E. Luders, O. L. Lopez, H. J. Aizenstein, and A. W. Toga. Generalized tensor-based morphometry of HIV/AIDS using multivariate statistics on deformation tensors. IEEE Trans. Med. Imaging 27:129–141, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Madhukar, A., and M. Ostoja-Starzewski. Finite element methods in human head impact simulations: a review. Ann. Biomed. Eng. 47:1832–1854, 2019.

    Article  PubMed  Google Scholar 

  34. Mao, H., L. Zhang, B. Jiang, V. V. Genthikatti, X. **, F. Zhu, R. Makwana, A. Gill, G. Jandir, A. Singh, et al. Development of a finite element human head model partially validated with thirty five experimental cases. J. Biomech. Eng. 135:111002, 2013.

    Article  PubMed  Google Scholar 

  35. McAllister, T. W., J. C. Ford, S. Ji, J. G. Beckwith, L. A. Flashman, K. Paulsen, and R. M. Greenwald. Maximum principal strain and strain rate associated with concussion diagnosis correlates with changes in corpus callosum white matter indices. Ann. Biomed. Eng. 40:127–140, 2012.

    Article  PubMed  Google Scholar 

  36. McDonald, B. C., A. J. Saykin, and T. W. McAllister. Functional MRI of mild traumatic brain injury (mTBI): progress and perspectives from the first decade of studies. Brain Imaging Behav. 6:193–207, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Miles, L., R. I. Grossman, G. Johnson, J. S. Babb, L. Diller, and M. Inglese. Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injury. Brain Inj. 22:115–122, 2008.

    Article  PubMed  Google Scholar 

  38. Miller, L. E., J. E. Urban, and J. D. Stitzel. Development and validation of an atlas-based finite element brain model. Biomech. Model. Mechanobiol. 15:1201–1214, 2016.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Miller, L. E., J. E. Urban, and J. D. Stitzel. Validation performance comparison for finite element models of the human brain. Comput. Methods Biomech. Biomed. Eng. 2017. https://doi.org/10.1080/10255842.2017.1340462.

    Article  Google Scholar 

  40. Nooner, K. B., et al. The NKI-rockland sample: a model for accelerating the Pace of discovery science in psychiatry. Front. Neurosci. 6:152, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Panzer, M. B., B. S. Myers, B. P. Capehart, and C. R. Bass. Development of a finite element model for blast brain injury and the effects of CSF cavitation. Ann. Biomed. Eng. 40:1530–1544, 2012.

    Article  PubMed  Google Scholar 

  42. Park, G., T. Kim, J. Forman, M. B. Panzer, and J. R. Crandall. Prediction of the structural response of the femoral shaft under dynamic loading using subject-specific finite element models. Comput. Methods Biomech. Biomed. Engin. 20:1151–1166, 2017.

    Article  PubMed  Google Scholar 

  43. Pellman, E. J., D. C. Viano, A. M. Tucker, I. R. Casson, and J. F. Waeckerle. Concussion in professional football: reconstruction of game impacts and injuries. Neurosurgery 53:799–814, 2003.

    Article  PubMed  Google Scholar 

  44. Pulsipher, D. T., R. A. Campbell, R. Thoma, and J. H. King. A critical review of neuroimaging applications in sports concussion. Curr. Sports Med. Rep. 10:14–20, 2011.

    Article  PubMed  Google Scholar 

  45. Reynier, K., A. Alshareef, E. J. Sanchez, D. F. Shedd, S. R. Walton, N. K. Erdman, B. T. Newman, J. S. Giudice, M. J. Higgins, J. R. Funk, D. K. Broshek, T. J. Druzgal, J. E. Resch, and M. B. Panzer. The effect of muscle activation on head kinematics during non-injurious head impacts in human subjects. Ann. Biomed. Eng (in review). 2020.

  46. Rosenbaum, S. B., and M. L. Lipton. Embracing chaos: the scope and importance of clinical and pathological heterogeneity in mTBI. Brain Imaging Behav. 6:255–282, 2012.

    Article  PubMed  Google Scholar 

  47. Sanchez, E. J., L. F. Gabler, A. B. Good, J. R. Funk, J. R. Crandall, and M. B. Panzer. A reanalysis of football impact reconstructions for head kinematics and finite element modeling. Clin. Biomech. 2018. https://doi.org/10.1016/j.clinbiomech.2018.02.019.

    Article  Google Scholar 

  48. Sanchez, E. J., L. F. Gabler, J. S. McGhee, A. V. Olszko, V. C. Chancey, J. Crandall, and M. B. Panzer. Evaluation of head and brain injury risk functions using sub-injurious human volunteer data. J. Neurotrauma 2017. https://doi.org/10.1089/neu.2016.4681.

    Article  PubMed  Google Scholar 

  49. Scheibel, R. S., D. A. Pearson, L. P. Faria, K. J. Kotrla, E. Aylward, J. Bachevalier, and H. S. Levin. An fMRI study of executive functioning after severe diffuse TBI. Brain Inj. 17:919–930, 2003.

    Article  CAS  PubMed  Google Scholar 

  50. Siegkas, P., D. J. Sharp, and M. Ghajari. The traumatic brain injury mitigation effects of a new viscoelastic add-on liner. Sci. Rep. 9:1–10, 2019.

    Article  CAS  Google Scholar 

  51. Slobounov, S., M. Gay, B. Johnson, and K. Zhang. Concussion in athletics: ongoing clinical and brain imaging research controversies. Brain Imaging Behav. 6:224–243, 2012.

    Article  PubMed  Google Scholar 

  52. Takhounts, E. G., R. H. Ep**er, J. Q. Campbell, R. E. Tannous, et al. On the development of the SIMon finite element head model. Stapp Car Crash J. 47:107, 2003.

    PubMed  Google Scholar 

  53. Takhounts, E. G., S. A. Ridella, V. Hasija, R. E. Tannous, J. Q. Campbell, D. Malone, K. Danelson, J. Stitzel, S. Rowson, and S. Duma. Investigation of traumatic brain injuries using the next generation of simulated injury monitor (SIMon) finite element head model. Stapp Car Crash J. 52:1, 2008.

    PubMed  Google Scholar 

  54. Toga, A. W., and P. M. Thompson. The role of image registration in brain map**. Image Vis. Comput. 19:3–24, 2001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Viano, D. C., I. R. Casson, E. J. Pellman, L. Zhang, A. I. King, and K. H. Yang. Concussion in Professional Football: Brain Responses By Finite Element Analysis: Part 9. Neurosurgery 57:891–916, 2005.

    Article  PubMed  Google Scholar 

  56. Wilde, E. A., S. R. McCauley, J. V. Hunter, E. D. Bigler, Z. Chu, Z. J. Wang, G. R. Hanten, M. Troyanskaya, R. Yallampalli, X. Li, J. Chia, and H. S. Levin. Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology 70:948–955, 2008.

    Article  CAS  PubMed  Google Scholar 

  57. Wu, T., A. Alshareef, J. S. Giudice, and M. B. Panzer. Explicit modeling of white matter axonal fiber tracts in a finite element brain model. Ann. Biomed. Eng. 47:1908–1922, 2019.

    Article  PubMed  Google Scholar 

  58. Wu, T., J. Antona-Makoshi, A. Alshareef, J. S. Giudice, and M. B. Panzer. Investigation of cross-species scaling methods for traumatic brain injury using finite element analysis. J. Neurotrauma. 2019. https://doi.org/10.1089/neu.2019.6576.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Zhang, K., B. Johnson, D. Pennell, W. Ray, W. Sebastianelli, and S. Slobounov. Are functional deficits in concussed individuals consistent with white matter structural alterations: combined FMRI & DTI study. Exp. Brain Res. 204:57–70, 20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Zhang, L., K. H. Yang, R. Dwarampudi, K. Omori, T. Li, K. Chang, W. N. Hardy, T. B. Khalil, and A. I. King. Recent advances in brain injury research: a new human head model development and validation. Stapp Car Crash J 45:369–394, 2001.

    CAS  PubMed  Google Scholar 

  61. Zhao, W., and S. Ji. Mesh convergence behavior and the effect of element integration of a human head injury model. Ann. Biomed. Eng. 47:475–486, 2019.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the UVA Brain Institute and Achievement Rewards for College Scientists Foundation (ARCS) for supporting this research. We would also like to thank Grant Kim for his assistance. The authors are thankful to Dr. Alayna Panzer for her thorough revisions to the manuscript.

Author information

Authors and Affiliations

  1. Department of Mechanical and Aerospace Engineering, Center for Applied Biomechanics, University of Virginia, 4040 Lewis and Clark Dr., Charlottesville, VA, 229011, USA

    J. Sebastian Giudice, Ahmed Alshareef, Taotao Wu, Kristen A. Reynier & Matthew B. Panzer

  2. Advanced Research Computing, University of Virginia, Charlottesville, VA, USA

    Christina A. Gancayco

  3. Department of Radiology and Medical Imaging, University of Virginia, Charlottesville, VA, USA

    Nicholas J. Tustison & T. Jason Druzgal

  4. Brain Injury and Sports Concussion Center, University of Virginia, Charlottesville, VA, USA

    Matthew B. Panzer

Authors
  1. J. Sebastian Giudice
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ahmed Alshareef
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Taotao Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christina A. Gancayco
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kristen A. Reynier
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nicholas J. Tustison
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. T. Jason Druzgal
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Matthew B. Panzer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthew B. Panzer.

Additional information

Associate Editor Joel D. Stitzel oversaw the review of this article.

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

Giudice, J.S., Alshareef, A., Wu, T. et al. An Image Registration-Based Morphing Technique for Generating Subject-Specific Brain Finite Element Models. Ann Biomed Eng 48, 2412–2424 (2020). https://doi.org/10.1007/s10439-020-02584-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-020-02584-z

Keywords

Search

Navigation