Brain tissue strains vary with head impact location: A possible explanation for increased concussion risk in struck versus striking football players

  • Author Footnotes
    1 MEA Forensic Engineers & Scientists Ltd. 22 Voyager Court South, Toronto, ON, M9W 5M7, Canada.
    Benjamin S. Elkin
    Footnotes
    1 MEA Forensic Engineers & Scientists Ltd. 22 Voyager Court South, Toronto, ON, M9W 5M7, Canada.
    Affiliations
    MEA Forensic Engineers & Scientists, Toronto, ON, Canada
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  • Author Footnotes
    2 University of Virginia Center for Applied Biomechanics 4040 Lewis and Clark Drive, Charlottesville, VA, 22911, USA.
    Lee F. Gabler
    Footnotes
    2 University of Virginia Center for Applied Biomechanics 4040 Lewis and Clark Drive, Charlottesville, VA, 22911, USA.
    Affiliations
    University of Virginia Center for Applied Biomechanics, Charlottesville, VA, USA
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  • Author Footnotes
    2 University of Virginia Center for Applied Biomechanics 4040 Lewis and Clark Drive, Charlottesville, VA, 22911, USA.
    Matthew B. Panzer
    Footnotes
    2 University of Virginia Center for Applied Biomechanics 4040 Lewis and Clark Drive, Charlottesville, VA, 22911, USA.
    Affiliations
    University of Virginia Center for Applied Biomechanics, Charlottesville, VA, USA
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  • Gunter P. Siegmund
    Correspondence
    Corresponding author at: MEA Forensic Engineers & Scientists, 11-11151 Horseshoe Way, Richmond, BC, V7A 4S5, Canada.
    Affiliations
    MEA Forensic Engineers & Scientists, Richmond, BC, Canada

    School of Kinesiology, University of British Columbia, Vancouver, BC, Canada
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  • Author Footnotes
    1 MEA Forensic Engineers & Scientists Ltd. 22 Voyager Court South, Toronto, ON, M9W 5M7, Canada.
    2 University of Virginia Center for Applied Biomechanics 4040 Lewis and Clark Drive, Charlottesville, VA, 22911, USA.

      Abstract

      Background

      On-field football helmet impacts over a large range of severities have caused concussions in some players but not in other players. One possible explanation for this variability is the struck player's helmet impact location.

      Methods

      We examined the effect of impact location on regional brain tissue strain when input energy was held constant. Laboratory impacts were performed at 12 locations distributed over the helmet and the resulting head kinematics were simulated in two finite element models of the brain: the Simulated Injury Monitor and the Global Human Body Model Consortium brain model.

      Findings

      Peak kinematics, injury metrics and brain strain varied significantly with impact location. Differences in impact location explained 33 to 37% of the total variance in brain strain for the whole brain and cerebrum, considerably more than the variance explained by impact location for the peak resultant head kinematics (8 to 23%) and slightly more than half of the variance explained by the difference in closing speed (57 to 61%). Both finite element models generated similar strain results, with minor variations for impacts that generated multi-axial rotations, larger variations in brainstem strains for some impact locations and a small bias for the cerebellum.

      Interpretation

      Based on this experimental and computational simulation study, impact location on the football helmet has a large effect on regional brain tissue strain. We also found that the lowest strains consistently occurred in impacts to the crown and forehead, helmet locations commonly associated with the striking player.

      Keywords

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      References

        • Bandak F.A.
        • Eppinger R.H.
        A Three-dimensional Finite Element Analysis of the Human Brain Under Combined Rotational and Translational Accelerations.
        SAE International, Warrendale, PA1994https://doi.org/10.4271/942215 (SAE Technical Paper No. 942215)
        • Beckwith J.G.
        • Greenwald R.M.
        • Chu J.J.
        • Crisco J.J.
        • Rowson S.
        • Duma S.M.
        • Broglio S.P.
        • McAllister T.W.
        • Guskiewicz K.M.
        • Mihalik J.P.
        • Anderson S.
        • Schnebel B.
        • Brolinson P.G.
        • Collins M.W.
        Head impact exposure sustained by football players on days of diagnosed concussion.
        Med. Sci. Sports Exerc. 2013; 45: 737-746https://doi.org/10.1249/MSS.0b013e3182792ed7
        • Cater H.L.
        • Sundstrom L.E.
        • Morrison B.
        Temporal development of hippocampal cell death is dependent on tissue strain but not strain rate.
        J. Biomech. 2006; 39: 2810-2818https://doi.org/10.1016/j.jbiomech.2005.09.023
        • Eckner J.T.
        • Oh Y.K.
        • Joshi M.S.
        • Richardson J.K.
        • Ashton-Miller J.A.
        Effect of neck muscle strength and anticipatory cervical muscle activation on the kinematic response of the head to impulsive loads.
        Am. J. Sports Med. 2014; 42: 566-576https://doi.org/10.1177/0363546513517869
        • Elkin B.S.
        • Morrison 3rd, B.
        Region-specific tolerance criteria for the living brain.
        Stapp Car Crash J. 2007; 51: 127-138
        • Funk J.R.
        • Duma S.M.
        • Manoogian S.J.
        • Rowson S.
        Biomechanical risk estimates for mild traumatic brain injury.
        in: Annual Proceedings/Association for the Advancement of Automotive Medicine. Association for the Advancement of Automotive Medicine, 2007: 343
        • Funk J.R.
        • Rowson S.
        • Daniel R.W.
        • Duma S.M.
        Validation of concussion risk curves for collegiate football players derived from HITS data.
        Ann. Biomed. Eng. 2012; 40: 79-89https://doi.org/10.1007/s10439-011-0400-8
        • Gabler L.F.
        • Crandall J.R.
        • Panzer M.B.
        Assessment of kinematic brain injury metrics for predicting strain responses in diverse automotive impact conditions.
        Ann. Biomed. Eng. 2016; 44: 3705-3718https://doi.org/10.1007/s10439-016-1697-0
        • Gennarelli T.A.
        • Thibault L.E.
        • Adams J.H.
        • Graham D.I.
        • Thompson C.J.
        • Marcincin R.P.
        Diffuse axonal injury and traumatic coma in the primate.
        Ann. Neurol. 1982; 12: 564-574https://doi.org/10.1002/ana.410120611
        • Gennarelli T.A.
        • Thibault L.E.
        • Tomei G.
        • Wiser R.
        • Graham D.
        • Adams J.
        Directional Dependence of Axonal Brain Injury Due to Centroidal and Non-centroidal Acceleration.
        SAE International, Warrendale, PA1987https://doi.org/10.4271/872197 (SAE Technical Paper No. 872197)
        • Greenwald R.M.
        • Gwin J.T.
        • Chu J.J.
        • Crisco J.J.
        Head impact severity measures for evaluating mild traumatic brain injury risk exposure.
        Neurosurgery. 2008; 62: 789-798https://doi.org/10.1227/01.neu.0000318162.67472.ad
        • Guskiewicz K.M.
        • McCrea M.
        • Marshall S.W.
        • Cantu R.C.
        • Randolph C.
        • Barr W.
        • Onate J.A.
        • Kelly J.P.
        Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study.
        JAMA. 2003; 290: 2549-2555https://doi.org/10.1001/jama.290.19.2549
        • Hardy W.N.
        • Foster C.D.
        • Mason M.J.
        • Yang K.H.
        • King A.I.
        • Tashman S.
        Investigation of head injury mechanisms using neutral density technology and high-speed biplanar X-ray.
        Stapp Car Crash J. 2001; 45: 337-368
        • Hardy W.N.
        • Mason M.J.
        • Foster C.D.
        • Shah C.S.
        • Kopacz J.M.
        • Yang K.H.
        • King A.I.
        • Bishop J.
        • Bey M.
        • Anderst W.
        • Tashman S.
        A study of the response of the human cadaver head to impact.
        Stapp Car Crash J. 2007; 51: 17-80
        • Hodgson V.R.
        • Thomas L.M.
        • Khalil T.B.
        The Role of Impact Location in Reversible Cerebral Concussion.
        SAE International, Warrendale, PA1983https://doi.org/10.4271/831618 (SAE Technical Paper No. 831618)
        • Holbourn A.H.S.
        Mechanics of head injuries.
        Lancet. 1943; vol. 2: 438-441https://doi.org/10.1016/S0140-6736(00)87453-X
        • Ji S.
        • Ghadyani H.
        • Bolander R.P.
        • Beckwith J.G.
        • Ford J.C.
        • McAllister T.W.
        • Flashman L.A.
        • Paulsen K.D.
        • Ernstrom K.
        • Jain S.
        • et al.
        Parametric comparisons of intracranial mechanical responses from three validated finite element models of the human head.
        Ann. Biomed. Eng. 2014; 42: 11-24
        • Ji S.
        • Zhao W.
        • Li Z.
        • McAllister T.W.
        Head impact accelerations for brain strain-related responses in contact sports: a model-based investigation.
        Biomech. Model. Mechanobiol. 2014; 13: 1121-1136https://doi.org/10.1007/s10237-014-0562-z
        • Ji S.
        • Zhao W.
        • Ford J.C.
        • Beckwith J.G.
        • Bolander R.P.
        • Greenwald R.M.
        • Flashman L.A.
        • Paulsen K.D.
        • McAllister T.W.
        Group-wise evaluation and comparison of white matter Fiber strain and maximum principal strain in sports-related concussion.
        J. Neurotrauma. 2015; 32: 441-454https://doi.org/10.1089/neu.2013.3268
        • Jin X.
        • Feng Z.
        • Mika V.
        • Li H.
        • Viano D.C.
        • Yang K.H.
        The role of neck muscle activities on the risk of mild traumatic brain injury in American football.
        J. Biomech. Eng. 2017; 139https://doi.org/10.1115/1.4037399
        • Kleiven S.
        Influence of direction and duration of impacts to the human head evaluated using the finite element method.
        in: International IRCOBI Conference on the Biomechanics of Impact, Prague; 21 September 2005 Through 23 September 2005. 2005: 41-57
        • 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. 2006; 11: 65-79
        • Mao H.
        • Zhang L.
        • Jiang B.
        • Genthikatti V.V.
        • Jin X.
        • Zhu F.
        • Makwana R.
        • Gill A.
        • Jandir G.
        • Singh A.
        • Yang K.H.
        Development of a finite element human head model partially validated with thirty five experimental cases.
        J. Biomech. Eng. 2013; 135111002https://doi.org/10.1115/1.4025101
        • McIntosh A.S.
        • Patton D.A.
        • Fréchède B.
        • Pierré P.-A.
        • Ferry E.
        • Barthels T.
        The biomechanics of concussion in unhelmeted football players in Australia: a case-control study.
        BMJ Open. 2014; 4e005078https://doi.org/10.1136/bmjopen-2014-005078
        • Miller L.E.
        • Urban J.E.
        • Stitzel J.D.
        Validation performance comparison for finite element models of the human brain.
        Comput. Meth. Biomech. Biomed. Eng. 2017; : 1-16https://doi.org/10.1080/10255842.2017.1340462
        • Morrison 3rd, B.
        • Elkin B.S.
        • Dollé J.-P.
        • Yarmush M.L.
        In vitro models of traumatic brain injury.
        Annu. Rev. Biomed. Eng. 2011; 13: 91-126https://doi.org/10.1146/annurev-bioeng-071910-124706
        • Panzer M.B.
        • Myers B.S.
        • Capehart B.P.
        • Bass C.R.
        Development of a finite element model for blast brain injury and the effects of CSF cavitation.
        Ann. Biomed. Eng. 2012; 40: 1530-1544https://doi.org/10.1007/s10439-012-0519-2
        • Pellman E.J.
        • Viano D.C.
        • Tucker A.M.
        • Casson I.R.
        • Waeckerle J.F.
        Concussion in professional football: reconstruction of game impacts and injuries.
        Neurosurgery. 2003; 53 (discussion 812-814): 799-812
        • Rowson S.
        • Duma S.M.
        • Beckwith J.G.
        • Chu J.J.
        • Greenwald R.M.
        • Crisco J.J.
        • Brolinson P.G.
        • Duhaime A.-C.
        • McAllister T.W.
        • Maerlender A.C.
        Rotational head kinematics in football impacts: an injury risk function for concussion.
        Ann. Biomed. Eng. 2012; 40: 1-13https://doi.org/10.1007/s10439-011-0392-4
        • Siegmund G.P.
        • Guskiewicz K.M.
        • Marshall S.W.
        • DeMarco A.L.
        • Bonin S.J.
        A headform for testing helmet and mouthguard sensors that measure head impact severity in football players.
        Ann. Biomed. Eng. 2014; 42: 1834-1845https://doi.org/10.1007/s10439-014-1052-2
        • Siegmund G.P.
        • Guskiewicz K.M.
        • Marshall S.W.
        • DeMarco A.L.
        • Bonin S.J.
        Laboratory validation of two wearable sensor systems for measuring head impact severity in football players.
        Ann. Biomed. Eng. 2015; https://doi.org/10.1007/s10439-015-1420-6
        • Takhounts E.G.
        • Ridella S.A.
        • Hasija V.
        • Tannous R.E.
        • Campbell J.Q.
        • Malone D.
        • Danelson K.
        • Stitzel J.
        • Rowson S.
        • Duma S.
        Investigation of traumatic brain injuries using the next generation of simulated injury monitor (SIMon) finite element head model.
        Stapp Car Crash J. 2008; 52: 1-31
        • Takhounts E.G.
        • Hasija V.
        • Ridella S.A.
        • Rowson S.
        • Duma S.M.
        Kinematic rotational brain injury criterion (BRIC).
        in: Proceedings of the 22nd Enhanced Safety of Vehicles Conference. 2011 (Paper)
        • Takhounts E.G.
        • Craig M.J.
        • Moorhouse K.
        • McFadden J.
        • Hasija V.
        Development of brain injury criteria (BrIC).
        Stapp Car Crash J. 2013; 57: 243-266
        • Viano D.C.
        • Casson I.R.
        • Pellman E.J.
        Concussion in professional football: biomechanics of the struck player—part 14.
        Neurosurgery. 2007; 61 (discussion 327-328): 313-327https://doi.org/10.1227/01.NEU.0000279969.02685.D0
        • Viceconti M.
        • Olsen S.
        • Nolte L.-P.
        • Burton K.
        Extracting clinically relevant data from finite element simulations.
        Clin. Biomech. 2005; 20: 451-454https://doi.org/10.1016/j.clinbiomech.2005.01.010
        • Weaver A.A.
        • Danelson K.A.
        • Stitzel J.D.
        Modeling brain injury response for rotational velocities of varying directions and magnitudes.
        Ann. Biomed. Eng. 2012; 40: 2005-2018https://doi.org/10.1007/s10439-012-0553-0
        • Wonnacott M.
        • Withnall C.
        Development of an Articulating Mandible Headform Having Force Sensing Temporomandibular Joints.
        2010 (SAE Technical Paper No. 2010-01-0136)
        • Zhang L.
        • Yang K.H.
        • King A.I.
        Comparison of brain responses between frontal and lateral impacts by finite element modeling.
        J. Neurotrauma. 2001; 18: 21-30https://doi.org/10.1089/089771501750055749
        • Zhao W.
        • Ji S.
        Parametric investigation of regional brain strain responses via a pre-computed atlas.
        in: IRCOBI Conf. 2015: 208-220