Abstract
A pre-computed brain response atlas (pcBRA) may have the potential to accelerate the investigation of the biomechanical mechanisms of traumatic brain injury on a large-scale. In this study, we further enhance the technique and evaluate its performance using six degree-of-freedom angular velocity profiles from dummy head impacts. Using the pcBRA to simplify profiles into acceleration-only shapes, sufficiently accurate strain estimates were obtained for impacts with a major dominating velocity peak. However, they were largely under-estimated when substantial deceleration occurred that reversed the direction of the angular velocity. For these impacts, estimation accuracy was substantially improved with a biphasic profile simplification (average correlation coefficient and linear regression slope of 0.92 ± 0.03 and 0.95 ± 0.07 for biphasic shapes, respectively, vs. 0.80 ± 0.06 and 0.80 ± 0.08 for acceleration-only shapes). Peak maximum principal strain (ɛ p) and cumulative strain damage measure (CSDM) from the estimated strains consistently correlated stronger than kinematic metrics with respect to the baseline ɛ p and CSDM from the directly simulated responses, regardless of the brain region, and by a large margin (e.g., correlation of 0.93 vs. 0.75 compared to Brain Injury Criterion (BrIC) for ɛ p in the whole-brain, and 0.91 vs. 0.47 compared to BrIC for CSDM in the corpus callosum). These findings further support the pre-computation technique for accurate, real-time strain estimation, which could be important to accelerate model-based brain injury studies in the future.
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References
Allison, M. A., Y. S. Kang, J. H. Bolte, M. R. Maltese, and K. B. Arbogast. Validation of a helmet-based system to measure head impact biomechanics in ice hockey. Med. Sci. Sports Exerc. 46:115–123, 2014.
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.
Beckwith, J. G., R. M. Greenwald, and J. J. Chu. Measuring head kinematics in football: correlation between the head impact telemetry system and Hybrid III headform. Ann. Biomed. Eng. 40:237–248, 2012.
Bigler, E. D. Systems biology, neuroimaging, neuropsychology, neuroconnectivity and traumatic brain injury. Front. Syst. Neurosci. 10:1–23, 2016.
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.
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.
Cai, Y., W. Zhao, Z. Li, and S. Ji. Concussion classification via deep learning using whole-brain white matter fiber strains, 2017
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.
Carson, J. D., D. W. Lawrence, S. A. Kraft, A. Garel, C. L. Snow, A. Chatterjee, P. Libfeld, H. M. MacKenzie, J. S. Thornton, R. Moineddin, and P. Frémont. Premature return to play and return to learn after a sport-related concussion: physician’s chart review. Can. Fam. Physician 60:310–315, 2014.
CDC. Report to congress on traumatic brain injury in the United States: epidemiology and rehabilitation. Atlanta: National Center for Injury Prevention and Control, 2015. doi:10.1161/HYPERTENSIONAHA.111.186106.
Chrisman, S., M. Schiff, S. Chung, S. Herring, and F. Rivara. Implementation of concussion legislation and extent of concussion education for athletes, parents, and coaches in washington state. Am. J. Sports Med. 42:1190–1196, 2014.
Davenport, E. M., C. T. Whitlow, J. E. Urban, M. A. Espeland, Y. Jung, D. A. Rosenbaum, G. A. Gioia, A. K. Powers, J. D. Stitzel, and J. A. Maldjian. Abnormal white matter integrity related to head impact exposure in a season of high school varsity football. J. Neurotrauma 31:1617–1624, 2014.
Franklyn, M., B. Fildes, L. Zhang, K. Yang, and L. Sparke. Analysis of finite element models for head injury investigation: reconstruction of four real-world impacts. Stapp Car Crash J. 49:1–32, 2005.
Gabler, L. F., J. R. Crandall, and M. B. Panzer. Assessment of kinematic brain injury metrics for predicting strain responses in diverse automotive impact conditions. Ann. Biomed. Eng. 44:3705–3718, 2016. doi:10.1007/s10439-016-1697-0.
Garimella, H. T., R. H. R. H. Kraft, H. T. Carimella, and R. H. R. H. Kraft. Modeling the mechanics of axonal fiber tracts using the embedded finite element method. Int. J. Numer. Method. Biomed. Eng. 2823:26–35, 2016.
Giordano, C., and S. Kleiven. Evaluation of axonal strain as a predictor for mild traumatic brain injuries using finite element modeling. Stapp Car Crash J. 58:29–61, 2014.
Goriely, A., M. G. D. Geers, G. A. Holzapfel, J. Jayamohan, A. Jérusalem, S. Sivaloganathan, W. Squier, J. A. W. Van Dommelen, S. Waters, and E. Kuhl. Mechanics of the brain: perspectives, challenges, and opportunities. Biomech. Model. Mechanobiol. 14:931–965, 2015. doi:10.1007/s10237-015-0662-4.
Hernandez, F., L. C. Wu, M. C. Yip, A. R. Hoffman, J. Lopez, G. Grant, S. Kleiven, and D. B. Camarillo. Six degree of freedom measurements of human mild traumatic brain injury. Ann. Biomed. Eng. 43:1918–1934, 2014.
Hernandez, F., L. C. Wu, M. C. Yip, K. Laksari, A. R. Hoffman, J. R. Lopez, G. A. Grant, S. Kleiven, and D. B. Camarillo. Erratum to: six degree-of-freedom measurements of human mild traumatic brain injury (Annals of Biomedical Engineering Vol. (43:8),1918–1934), 2016, DOI: 10.1007/s10439-014-1212-4. Ann. Biomed. Eng. 44:828–829, 2015.
Iraji, A., R. R. Benson, R. D. Welch, B. J. O. Neil, J. L. Woodard, I. Ayaz, A. Kulek, P. Medado, H. Soltanian-Zadeh, T. Liu, M. Haacke, and Z. Kou. Resting state functional connectivity in mild traumatic brain injury at the acute stage: independent component and seed based analyses. J. Neurotrauma 32:1031–1045, 2014.
Ji, S., and S. Margulies. Brainstem motion within the skull: measurement of the pons displacement in vivo. J. Biomech 40:92–99, 2007.
Ji, S., and W. Zhao. A pre-computed brain response atlas for instantaneous strain estimation in contact sports. Ann. Biomed. Eng. 43:1877–1895, 2015.
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 32:441–454, 2015.
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.
Kang, Y.-S., K. Moorhouse, and J. H. Bolte. Measurement of six degrees of freedom head kinematics in impact conditions employing six accelerometers and three angular rate sensors (6a? configuration). J. Biomech. Eng. 133:111007, 2011.
Kimpara, H., and M. Iwamoto. Mild traumatic brain injury predictors based on angular accelerations during impacts. Ann. Biomed. Eng. 40:114–126, 2012.
King, A. I., K. H. Yang, L. Zhang, W. Hardy, and D. C. Viano. Is head injury caused by linear or angular acceleration? IRCOBI Conference, 2003.
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.
Kleiven, S. Predictors for traumatic brain injuries evaluated through accident reconstructions. Stapp Car Crash J. 51:81–114, 2007.
Kroshus, E., L. Kubzansky, R. Goldman, and S. Austin. Norms, athletic identity, and concussion symptom under-reporting among male collegiate ice hockey players: a prospective cohort study. Ann. Behav. Med. 49:95–103, 2014.
Kuo, C., L. C. Wu, B. T. Hammoor, J. F. Luck, H. C. Cutcliffe, R. C. Lynall, J. R. Kait, K. R. Campbell, J. P. Mihalik, C. R. Bass, and D. B. Camarillo. Effect of the mandible on mouthguard measurements of head kinematics. J. Biomech. 49:1845–1853, 2016.
Marjoux, D., D. Baumgartner, C. Deck, and R. Willinger. Head injury prediction capability of the HIC, HIP, SIMon and ULP criteria. Accid. Anal. Prev. 40:1135–1148, 2008.
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.
McCrea, M., T. Hammeke, G. Olsen, P. Leo, and K. Guskiewicz. Unreported concussion in high school football players: implications for prevention. Clin J Sport Med 14:13–17, 2004.
Montenigro, P. H., M. L. Alosco, B. Martin, D. H. Daneshvar, J. Mez, C. Chaisson, C. J. Nowinski, R. Au, A. C. McKee, R. C. Cantu, M. D. McClean, R. A. Stern, and Y. Tripodis. Cumulative head impact exposure predicts later-life depression, apathy, executive dysfunction, and cognitive impairment in former high school and college football players. J. Neurotrauma 34:328–340, 2017.
NRC, and IOM. Sports-related concussions in youth: improving the science, changing the culture. Washington, DC: National Academies Press, 2014.
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.
Rapp, P. E., D. O. Keyser, A. Albano, R. Hernandez, D. B. Gibson, R. A. Zambon, W. D. Hairston, J. D. Hughes, A. Krystal, and A. S. Nichols. Traumatic brain injury detection using electrophysiological methods. Front. Hum. Neurosci. 9:11, 2015.
Sullivan, S., S. A. Eucker, D. Gabrieli, C. Bradfield, B. Coats, M. R. Maltese, J. Lee, C. Smith, and S. S. Margulies. White matter tract-oriented deformation predicts traumatic axonal brain injury and reveals rotational direction-specific vulnerabilities. Biomech. Model. Mechanobiol. 14:877–896, 2014. doi:10.1007/s10237-014-0643-z.
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.
Ward, C., M. Chan, and A. Nahum. Intracranial pressure-A brain injury criterion, 1980. doi:10.4271/801304
Yanaoka, T., Y. Dokko, and Y. Takahashi. Investigation on an injury criterion related to traumatic brain injury primarily induced by head rotation, 2015. doi:10.4271/2015-01-1439.
Zhang, J., N. Yoganandan, F. A. Pintar, and T. A. Gennarelli. Role of translational and rotational accelerations on brain strain in lateral head impact. Biomed. Sci. Instrum. 42:501–506, 2006.
Zhao, W., Y. Cai, Z. Li, and S. Ji. Injury prediction and vulnerability assessment using strain and susceptibility measures of the deep white matter. Biomech. Model. Mechanobiol. 2017. doi:10.1007/s10237-017-0915-5.
Zhao, W., J. C. Ford, L. A. Flashman, T. W. McAllister, and S. Ji. White matter injury susceptibility via fiber strain evaluation using whole-brain tractography. J. Neurotrauma 33:1834–1847, 2016.
Zhao, W., and S. Ji. Parametric investigation of regional brain strain responses via a pre-computed atlas. IRCOBI Conference, 2015.
Zhao, W., and S. Ji. Feasibility of a pressure response superposition scheme in blunt head impact. IRCOBI Conferences, 2015.
Zhao, W., and S. Ji. Brain strain uncertainty due to shape variation in and simplification of head angular velocity profiles. Biomech. Model. Mechanobiol. 16:449–461, 2017.
Zonfrillo, M., K. Kim, and K. B. Arbogast. Emergency department visits and head computed tomography utilization for concussion patients from, 2006 to 2011. Acad. Emerg. Med. 22:872–877, 2015.
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Funding is provided by the NIH Grants R01 NS092853 and R21 NS088781.
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Associate Editor Joel D. Stitzel oversaw the review of this article.
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Zhao, W., Kuo, C., Wu, L. et al. Performance Evaluation of a Pre-computed Brain Response Atlas in Dummy Head Impacts. Ann Biomed Eng 45, 2437–2450 (2017). https://doi.org/10.1007/s10439-017-1888-3
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DOI: https://doi.org/10.1007/s10439-017-1888-3