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A Pre-computed Brain Response Atlas for Instantaneous Strain Estimation in Contact Sports

Abstract

Finite element models of the human head play an important role in investigating the mechanisms of traumatic brain injury, including sports concussion. A critical limitation, however, is that they incur a substantial computational cost to simulate even a single impact. Therefore, current simulation schemes significantly hamper brain injury studies based on model-estimated tissue-level responses. In this study, we present a pre-computed brain response atlas (pcBRA) to substantially increase the simulation efficiency in estimating brain strains using isolated rotational acceleration impulses parameterized with four independent variables (peak magnitude and duration, and rotational axis azimuth and elevation angles) with values determined from on-field measurements. Using randomly generated testing datasets, the partially established pcBRA achieved a 100% success rate in interpolation based on element-wise differences in accumulated peak strain (\(\varepsilon^{p}\)) according to a “double-10%” criterion or average regional \(\varepsilon^{p}\) in generic regions and the corpus callosum. A similar performance was maintained in extrapolation. The pcBRA performance was further successfully validated against directly simulated responses from two independently measured typical real-world rotational profiles. The computational cost to estimate element-wise whole-brain or regional \(\varepsilon^{p}\) was 6 s and <0.01 s, respectively, vs. ~50 min directly simulating a 40 ms impulse. These findings suggest the pcBRA could substantially increase the throughput in impact simulation without significant loss of accuracy from the estimation itself and, thus, its potential to accelerate the exploration of the mechanisms of sports concussion in general. If successful, the pcBRA may also become a diagnostic adjunct in conjunction with sensors that measure head impact kinematics on the field to objectively monitor and identify tissue-level brain trauma in real-time for “return-to-play” decision-making on the sideline.

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References

  1. Bain, A., and D. Meaney. Tissue-level thresholds for axonal damage in an experimental model of central nervous system white matter injury. J. Biomech. Eng. 122:615–622, 2000.

    CAS  PubMed  Article  Google Scholar 

  2. Bazarian, J. J., T. Zhu, B. Blyth, A. Borrino, and J. Zhong. Subject-specific changes in brain white matter on diffusion tensor imaging after sports-related concussion. Magn. Reson. Imaging 30:171–180, 2012.

    PubMed Central  PubMed  Article  Google Scholar 

  3. Beckwith, J. G., R. M. Greenwald, J. J. Chu, J. J. Crisco, S. Rowson, S. M. Duma, S. P. Broglio, T. W. McAllister, K. M. Guskiewicz, J. P. Mihalik, S. Anderson, B. Schnebel, P. G. Brolinson, and M. W. Collins. Timing of concussion diagnosis is related to head impact exposure prior to injury. Med. Sci. Sports Exerc. 45:747–754, 2013.

    PubMed Central  PubMed  Article  Google Scholar 

  4. Beckwith, J. G., R. M. Greenwald, J. J. Chu, J. J. Crisco, S. Rowson, S. M. Duma, S. P. Broglio, T. W. McAllister, K. M. Guskiewicz, J. P. Mihalik, S. Anderson, B. Schnebel, P. G. Brolinson, and M. W. Collins. Head impact exposure sustained by football players on days of diagnosed concussion. Med. Sci. Sports Exerc. 45:737–746, 2013.

    PubMed Central  PubMed  Article  Google Scholar 

  5. Brainard, L. L., J. G. Beckwith, J. J. Chu, J. J. Crisco, T. W. McAllister, A.-C. Duhaime, A. C. Maerlender, and R. M. Greenwald. Gender differences in head impacts sustained by collegiate ice hockey players. Med. Sci. Sports Exerc. 44:297–304, 2012.

    PubMed Central  PubMed  Article  Google Scholar 

  6. Breedlove, E. L., M. Robinson, T. M. Talavage, K. E. Morigaki, U. Yoruk, K. O’Keefe, J. King, L. J. Leverenz, J. W. Gilger, and E. A. Nauman. Biomechanical correlates of symptomatic and asymptomatic neurophysiological impairment in high school football. J. Biomech. 45:1265–1272, 2012.

  7. Broglio, S. P., T. Surma, and J. A. Ashton-Miller. High school and collegiate football athlete concussions: a biomechanical review. Ann. Biomed. Eng. 40:37–46, 2012.

  8. Broglio, S. P., B. Schnebel, J. J. Sosnoff, S. Shin, X. Fend, X. He, and J. Zimmerman. Biomechanical properties of concussions in high school football. Med. Sci. Sports Exerc. 42:2064–2071, 2010.

    PubMed Central  PubMed  Article  Google Scholar 

  9. Broglio, S. P., J. J. Sosnoff, S. Shin, X. He, C. Alcaraz, and J. Zimmerman. Head impacts during high school football: a biomechanical assessment. J. Athl. Train. 44:342–349, 2009.

    PubMed Central  PubMed  Article  Google Scholar 

  10. Camarillo, D. B., P. B. Shull, J. Mattson, R. Shultz, and D. Garza. An instrumented mouthguard for measuring linear and angular head impact kinematics in American football. Ann. Biomed. Eng. 41:1939–1949, 2013.

    PubMed Central  PubMed  Article  Google Scholar 

  11. Centers for Disease Control and Prevention. Report to congress on mild traumatic brain injury in the United States: steps to prevent a serious public health problem. GA: Atlanta, 2003.

    Google Scholar 

  12. Chatelin, S., C. Deck, F. Renard, S. Kremer, C. Heinrich, J.-P. Armspach, and R. Willinger. Computation of axonal elongation in head trauma finite element simulation. J. Mech. Behav. Biomed. Mater. 4:1905–1919, 2011.

    PubMed  Article  Google Scholar 

  13. Chen, Y., and M. Ostoja-Starzewski. MRI-based finite element modeling of head trauma: spherically focusing shear waves. Acta Mech. 213:155–167, 2010.

    Article  Google Scholar 

  14. Cloots, R. J. H., J. A. W. van Dommelen, T. Nyberg, S. Kleiven, and M. G. D. Geers. Micromechanics of diffuse axonal injury: influence of axonal orientation and anisotropy. Biomech. Model. Mechanobiol. 10:413–22, 2011.

  15. Crisco, J. J., R. Fiore, J. G. Beckwith, J. J. Chu, P. G. Brolinson, S. Duma, T. W. McAllister, A.-C. Duhaime, and R. M. Greenwald. Frequency and location of head impact exposures in individual collegiate football players. J. Athl. Train. 45:549–559, 2010.

    PubMed Central  PubMed  Article  Google Scholar 

  16. Dumpuri, P., R. C. Thompson, B. M. Dawant, A. Cao, and M. I. Miga. An atlas-based method to compensate for brain shift: preliminary results. Med. Image Anal. 11:128–45, 2007.

  17. Greenwald, R., J. Gwin, J. Chu, and J. Crisco. Head impact severity measures for evaluating mild traumatic brain injury risk exposure. Neurosurgery 62:789–798, 2008.

    PubMed Central  PubMed  Article  Google Scholar 

  18. Hakopian, H. Multivariate spline functions, B-spline basis and polynomial interpolations. SIAM J. Numer. Anal. 19:510–517, 1982.

    Article  Google Scholar 

  19. Hardy, W. N., C. D. Foster, M. J. Mason, K. H. Yang, A. I. King, and S. Tashman. Investigation of head injury mechanisms using neutral density technology and high-speed biplanar X-ray. Stapp Car Crash J. 45:337–368, 2001.

    CAS  PubMed  Google Scholar 

  20. Hardy, W. N., M. J. Mason, C. D. Foster, C. S. Shah, J. M. Kopacz, K. H. Yang, A. I. King, J. Bishop, M. Bey, W. Anderst, and S. Tashman. A Study of the Response of the Human Cadaver Head to Impact. 51:17–80, 2007.

    Google Scholar 

  21. Holbourn, A. The mechanics of brain injuries. Lancet 2:438–441, 1943.

    Article  Google Scholar 

  22. Ji, S., J. C. Ford, R. M. Greenwald, J. G. Beckwith, K. D. Paulsen, L. A. Flashman, and T. W. McAllister. Automated subject-specific, hexahedral mesh generation via image registration. Finite Elem. Anal. Des. 47:1178–1185, 2011.

    PubMed Central  PubMed  Article  Google Scholar 

  23. 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.

  24. Ji, S., W. Zhao, J. C. Ford, J. G. Beckwith, R. P. Bolander, R. M. Greenwald, L. A. Flashman, K. D. Paulsen, and T. W. McAllister. Group-wise evaluation and comparison of white matter fiber strain and maximum principal strain in sports-related concussion. J. Neurotrauma 2014. doi:10.1089/neu.2013.3268.

  25. Ji, S., W. Zhao, Z. Li, and T. W. McAllister. Head impact accelerations for brain strain-related responses in contact sports: a model-based investigation. Biomech. Model. Mechanobiol. 13:1121–1136, 2014.

    PubMed  Article  Google Scholar 

  26. Kimpara, H., and M. Iwamoto. Mild traumatic brain injury predictors based on angular accelerations during impacts. Ann. Biomed. Eng. 40:114–126, 2012.

    PubMed  Article  Google Scholar 

  27. King, A., K. Yang, and L. Zhang. Is head injury caused by linear or angular acceleration. 2003.

  28. Kleiven, S. Evaluation of head injury criteria using a finite element model validated against experiments on localized brain motion, intracerebral acceleration, and intracranial pressure. Int. J. Crashworthiness 11:65–79, 2006.

    Article  Google Scholar 

  29. Kleiven, S. Predictors for traumatic brain injuries evaluated through accident reconstructions. Stapp Car Crash J. 51:81–114, 2007.

    PubMed  Google Scholar 

  30. Kraft, R. H., P. J. McKee, A. M. Dagro, and S. T. Grafton. Combining the finite element method with structural connectome-based analysis for modeling neurotrauma: connectome neurotrauma mechanics. PLoS Comput. Biol. 8:e1002619, 2012.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  31. Loader, C. Local Regression and Likelihood. New York: Springer, 1999.

  32. Marjoux, D., D. Baumgartner, and C. Deck. Head injury prediction capability of the HIC. HIP, SIMon and ULP criteria. 40:1135–1148, 2008.

    Google Scholar 

  33. McAllister, T. W., J. C. Ford, L. A. Flashman, A. Maerlender, R. M. Greenwald, J. G. Beckwith, R. P. Bolander, T. D. Tosteson, J. H. Turco, R. Raman, and S. Jain. Effect of head impacts on diffusivity measures in a cohort of collegiate contact sport athletes. Neurology 82:63–69, 2014.

  34. 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.

  35. McCrea, M., T. Hammeke, G. Olsen, P. Leo, and K. M. Guskiewicz. Unreported concussion in high school football players. Clin. J. Sport Med. 14:385; author reply 385, 2004.

  36. McKee, A., R. Cantu, C. Nowinski, E. Hedley-Whyte, B. Gavett, A. Budson, V. Santini, H. Lee, C. Kubilus, and R. Stern. Chronic traumatic encephalopathy in athletes: progressive tauopathy following repetitive head injury. J. Neuropathol. Exp. Neurol. 68:709–735, 2009.

    PubMed Central  PubMed  Article  Google Scholar 

  37. Morrison, B. III, D. Cullen, and M. LaPlaca. In vitro models for biomechanical studies of neural tissues. Neural Tissue Biomech. Stud. Mechanobiol. Tissue Eng. Biomater. 3:247–285, 2011.

  38. Nahum, A., R. Smith, and C. Ward. Intracranial pressure dynamics during head impact. SAE Tech. Pap. No. 770922, 1977.

  39. Newman, J. A generalized acceleration model for brain injury threshold (GAMBIT). 1986.

  40. Newman, J., and N. Shewchenko. A proposed new biomechanical head injury assessment function-the maximum power index. Stapp Car Crash J. 44:215–247, 2000.

    CAS  PubMed  Google Scholar 

  41. 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.

    PubMed  Google Scholar 

  42. Post, A., B. Hoshizaki, and M. D. Gilchrist. Finite element analysis of the effect of loading curve shape on brain injury predictors. J. Biomech. 45:679–683, 2012.

    PubMed  Article  Google Scholar 

  43. Rowson, S., G. Brolinson, M. Goforth, D. Dietter, and S. Duma. Linear and angular head acceleration measurements in collegiate football. J. Biomech. Eng. 131:061016, 2009.

    PubMed  Article  Google Scholar 

  44. Rowson, S., and S. M. Duma. Brain injury prediction: assessing the combined probability of concussion using linear and rotational head acceleration. Ann. Biomed. Eng. 41:873–882, 2013.

    PubMed Central  PubMed  Article  Google Scholar 

  45. Rowson, S., S. M. Duma, J. G. Beckwith, J. J. Chu, R. M. Greenwald, J. J. Crisco, P. G. Brolinson, A.-C. Duhaime, T. W. McAllister, and A. C. Maerlender. Rotational head kinematics in football impacts: an injury risk function for concussion. Ann. Biomed. Eng. 40:1–13, 2012.

    PubMed  Article  Google Scholar 

  46. Rowson, S., J. G. Beckwith, J. J. Chu, D. S. Leonard, R. M. Greenwald, and S. M. Duma. A six degree of freedom head acceleration measurement device for use in football. 8–14, 2011.

  47. Sabet, A. A., E. Christoforou, B. Zatlin, G. M. Genin, and P. V. Bayly. Deformation of the human brain induced by mild angular head acceleration. J. Biomech. 41:307–315, 2008.

  48. Takhounts, E. G., M. J. Craig, K. Moorhouse, J. McFadden, and V. Hasija. Development of brain injury criteria (Br IC). Stapp Car Crash J. 57:243–266, 2013.

    PubMed  Google Scholar 

  49. Takhounts, E. G., S. A. Ridella, 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. 52:1–31, 2008.

  50. Talavage, T. M., E. A. Nauman, E. L. Breedlove, U. Yoruk, A. E. Dye, K. E. Morigaki, H. Feuer, and L. J. Leverenz. Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion. J. Neurotrauma 12:1–12, 2013.

  51. Trosseille, X., C. Tarriere, F. Lavaste, F. Guillon, and A. Domont. Development of a FEM of the human head according to a specific test protocol. 1992.

  52. Urban, J. E., E. M. Davenport, A. J. Golman, J. A. Maldjian, C. T. Whitlow, A. K. Powers, and J. D. Stitzel. Head impact exposure in youth football: high school ages 14 to 18 years and cumulative impact analysis. Ann. Biomed. Eng. 41:2474–2487, 2013.

  53. van Dommelen, J. A. W., T. P. J. van der Sande, M. Hrapko, and G. W. M. Peters. Mechanical properties of brain tissue by indentation: interregional variation. J. Mech. Behav. Biomed. Mater. 3:158–166, 2010.

    PubMed  Article  Google Scholar 

  54. Weaver, A. A., K. A. Danelson, and J. D. Stitzel. Modeling brain injury response for rotational velocities of varying directions and magnitudes. Ann. Biomed. Eng. 40:2005–2018, 2012.

  55. Willinger, R., and D. Baumgartner. Numerical and physical modelling of the human head under impact-towards new injury criteria. Int. J. Veh. Des. 32:94–115, 2003.

    Article  Google Scholar 

  56. Wright, R. M., A. Post, B. Hoshizaki, and K. T. Ramesh. A multiscale computational approach to estimating axonal damage under inertial loading of the head. J. Neurotrauma 30:102–118, 2013.

    PubMed  Article  Google Scholar 

  57. Yang, K., H. Mao, C. Wagner, F. Zhu, C. C. Chou, and A. I. King. Modeling of the brain for injury prevention. In: Studies in Mechanobiology, Tissue Engineering and Biomaterials. Berlin: Springer-Verlag, pp. 69–120, 2011 at http://www.springerlink.com/index/U7368378332M5820.pdf

  58. Yoganandan, N., J. Li, J. Zhang, F. A. Pintar, and T. A. Gennarelli. Influence of angular acceleration-deceleration pulse shapes on regional brain strains. J. Biomech. 41:2253–2262, 2008.

    PubMed  Article  Google Scholar 

  59. Zhang, L., K. H. Yang, and A. I. King. A proposed injury threshold for mild traumatic brain injury. J. Biomech. Eng. 126, 2004.

  60. Zhao, W., S. Ruan, and S. Ji. Brain pressure responses in translational head impact: a dimensional analysis and a further computational study. Biomech. Model. Mechanobiol. 2014. doi:10.1007/s10237-014-0634-0.

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Acknowledgments

This work was sponsored, in part, by the NIH Grant R21 NS078607 and the Dartmouth Hitchcock Foundation.

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Correspondence to Songbai Ji.

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

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Ji, S., Zhao, W. A Pre-computed Brain Response Atlas for Instantaneous Strain Estimation in Contact Sports. Ann Biomed Eng 43, 1877–1895 (2015). https://doi.org/10.1007/s10439-014-1193-3

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Keywords

  • Traumatic brain injury
  • Sports concussion
  • Rotational acceleration
  • Pre-computation
  • Dartmouth Head Injury Model