Annals of Biomedical Engineering

, Volume 43, Issue 8, pp 1918–1934 | Cite as

Six Degree-of-Freedom Measurements of Human Mild Traumatic Brain Injury

  • Fidel Hernandez
  • Lyndia C. Wu
  • Michael C. Yip
  • Kaveh Laksari
  • Andrew R. Hoffman
  • Jaime R. Lopez
  • Gerald A. Grant
  • Svein Kleiven
  • David B. Camarillo
Article

Abstract

This preliminary study investigated whether direct measurement of head rotation improves prediction of mild traumatic brain injury (mTBI). Although many studies have implicated rotation as a primary cause of mTBI, regulatory safety standards use 3 degree-of-freedom (3DOF) translation-only kinematic criteria to predict injury. Direct 6DOF measurements of human head rotation (3DOF) and translation (3DOF) have not been previously available to examine whether additional DOFs improve injury prediction. We measured head impacts in American football, boxing, and mixed martial arts using 6DOF instrumented mouthguards, and predicted clinician-diagnosed injury using 12 existing kinematic criteria and 6 existing brain finite element (FE) criteria. Among 513 measured impacts were the first two 6DOF measurements of clinically diagnosed mTBI. For this dataset, 6DOF criteria were the most predictive of injury, more than 3DOF translation-only and 3DOF rotation-only criteria. Peak principal strain in the corpus callosum, a 6DOF FE criteria, was the strongest predictor, followed by two criteria that included rotation measurements, peak rotational acceleration magnitude and Head Impact Power (HIP). These results suggest head rotation measurements may improve injury prediction. However, more 6DOF data is needed to confirm this evaluation of existing injury criteria, and to develop new criteria that considers directional sensitivity to injury.

Keywords

Concussion Mild traumatic brain injury (mTBI) Instrumented mouthguard Six degree-of-freedom (6DOF) kinematics Finite element model Brain strain 

Supplementary material

10439_2014_1212_MOESM1_ESM.pdf (22 kb)
Supplemental Fig. 1. Distribution of 6DOF head impact measurements by sport. Kinematics histograms were plotted for the non-injury American football, boxing, and mixed martial arts head impacts. The distributions of each sport were similar for all measures. In the left-right and coronal directions, the LOC injury was very high percentile. For the other directions, the LOC injury was less distinguishable from non-injury. The self-reported injury was generally less distinguishable than the LOC injury. (PDF 22 kb)
10439_2014_1212_MOESM2_ESM.pdf (33 kb)
Supplemental Fig. 2. Distribution of head impact acceleration directions. Rotational histograms of head impacts are plotted in each plane for maximum translational acceleration (A), and maximum rotational acceleration (B). Head impacts occurred over a broad spectrum of directions. In each plane, the injuries lie in directions where only a small percentage of noninjuries occurred, supporting the use of multidimensional analysis to helps distinguish injury from non-injury. (PDF 33 kb)
10439_2014_1212_MOESM3_ESM.mov (9.2 mb)
Supplemental Movie 1. Video of American football mTBI impact. Video of the head impact was recorded at 40 frames s−1 and is compared to an animation of the device recordings. Time synchronized measurements of translational acceleration and angular acceleration are shown below. (MOV 9403 kb)
10439_2014_1212_MOESM4_ESM.mov (9.1 mb)
Supplemental Movie 2. Video of a mixed martial arts non-injury head impact. Video of the head impact was recorded at 1300 frames s−1 and is compared to an animation of the device recordings. Time synchronized measurements of translational acceleration and angular acceleration are shown below. (MOV 9280 kb)
10439_2014_1212_MOESM5_ESM.mov (19.8 mb)
Supplemental Movie 3. Simulation of brain during loss of consciousness (LOC). A finite element simulation of an LOC head impact (Methods) reveals maximum tensile strain of 30% occurs at t = 30 ms in the corpus callosum and brainstem. Damage to these regions is thought to affect perception and consciousness. Sagittal and coronal views of the brain are provided in the video. (MOV 20295 kb)

References

  1. 1.
    Abrahams, S., S. Mc Fie, J. Patricios, M. Posthumus, and A. V. September. Risk factors for sports concussion: an evidence-based systematic review. Br. J. Sports Med. 2013. doi:10.1136/bjsports-2013-092734.
  2. 2.
    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(1):115–123, 2014.CrossRefPubMedGoogle Scholar
  3. 3.
    Arbogast, K. B., and S. S. Margulies. Material characterization of the brainstem from oscillatory shear tests. J. Biomech. 31(9):801–807, 1998.CrossRefPubMedGoogle Scholar
  4. 4.
    Arenth, P. M., K. C. Russell, J. M. Scanlon, L. J. Kessler, and J. H. Ricker. Corpus callosum integrity and neuropsychological performance after traumatic brain injury: a diffusion tensor imaging study. J. Head Trauma Rehabil. 29(2):E1–E10, 2014.Google Scholar
  5. 5.
    Bartsch, A., and S. Samorezov. A new technology to accurately measure head impact in athletes and soldiers. Environmental Monitoring 1:2, 2013.Google Scholar
  6. 6.
    Bayly, P. V., T. Cohen, E. Leister, D. Ajo, E. Leuthhardt, and G. Genin. Deformation of the human brain induced by mild acceleration. J. Neurotrauma 22(8):845–856, 2005.PubMedCentralCrossRefPubMedGoogle Scholar
  7. 7.
    Beckwith, J. G., J. J. Chu, and R. M. Greenwald. Validation of a noninvasive system for measuring head acceleration for use during boxing competition. J. Appl. Biomech. 23(3):238–244, 2007.PubMedGoogle Scholar
  8. 8.
    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(1):237–248, 2012.PubMedCentralCrossRefPubMedGoogle Scholar
  9. 9.
    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, and P. G. Brolinson. Timing of concussion diagnosis is related to head impact exposure prior to injury. Med. Sci. Sports Exerc. 45(4):747–754, 2013.PubMedCentralCrossRefPubMedGoogle Scholar
  10. 10.
    Bianchi, A., B. Bhanu, and A. Obenaus. Dynamic low-level context for the detection of mild traumatic brain injury. IEEE Trans. Biomed. Eng. 2014. doi:10.1109/TBME.2014.2342653.
  11. 11.
    Browne, K. D., X. Chen, D. F. Meaney, and D. H. Smith. Mild traumatic brain injury and diffuse axonal injury in swine. J. Neurotrauma 28(9):1747–1755, 2011.PubMedCentralCrossRefPubMedGoogle Scholar
  12. 12.
    Caccese, V., J. Ferguson, J. Lloyd, M. Edgecomb, M. Seidi, and M. Hajiaghamemar. Response of an impact test apparatus for fall protective headgear testing using a Hybrid-III head/neck assembly. Exp. Tech. 2014. doi:10.1111/ext.12079.
  13. 13.
    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(9):1939–1949, 2013.PubMedCentralCrossRefPubMedGoogle Scholar
  14. 14.
    Cao, C., R. L. Tutwiler, and S. Slobounov. Automatic classification of athletes with residual functional deficits following concussion by means of EEG signal using support vector machine. IEEE Trans. Neural Syst. Rehabil. Eng. 16(4):327–335, 2008.CrossRefPubMedGoogle Scholar
  15. 15.
    Cassidy, J. D., L. J. Carroll, P. M. Peloso, J. Borg, H. von Holst, L. Holm, J. Kraus, and V. Coronado. Incidence, risk factors and prevention of mild traumatic brain injury: results of the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. J Rehabil Med 43(Suppl):28–60, 2004.CrossRefPubMedGoogle Scholar
  16. 16.
    Coats, B., S. A. Eucker, S. Sullivan, and S. S. Margulies. Finite element model predictions of intracranial hemorrhage from non-impact, rapid head rotations in the piglet. Int. J. Dev. Neurosci. 30(3):191–200, 2012.PubMedCentralCrossRefPubMedGoogle Scholar
  17. 17.
    DeKosky, S. T., K. Blennow, M. D. Ikonomovic, and S. Gandy. Acute and chronic traumatic encephalopathies: pathogenesis and biomarkers. Nat. Rev. Neurol. 9(4):192–200, 2013.PubMedCentralCrossRefPubMedGoogle Scholar
  18. 18.
    Denny-Brown, D. E., and W. R. Russell. Experimental cerebral concussion. Brain 64(2–3):93–164, 1941.CrossRefGoogle Scholar
  19. 19.
    Duma, S. M., S. J. Manoogian, W. R. Bussone, P. G. Brolinson, M. W. Goforth, J. J. Donnenwerth, R. M. Greenwald, J. J. Chu, and J. J. Crisco. Analysis of real-time head accelerations in collegiate football players. Clin. J. Sports Med. 15(1):3–8, 2005.CrossRefGoogle Scholar
  20. 20.
    Eucker, S. A., C. Smith, J. Ralston, S. H. Friess, and S. S. Margulies. Physiological and histopathological responses following closed rotational head injury depend on direction of head motion. Exp. Neurol. 227(1):79–88, 2011.PubMedCentralCrossRefPubMedGoogle Scholar
  21. 21.
    Federal Motor Vehicle Safety Standards (FMVSS). Part 571, Standard No. 202a–Head restraints. pp. 531–545, 2014.Google Scholar
  22. 22.
    Feng, Y., R. J. Okamoto, R. Namani, G. M. Genin, and P. V. Bayly. Measurements of mechanical anisotropy in brain tissue and implications for transversely isotropic material models of white matter. J. Mech. Behav. Biomed. Mater. 23:117–132, 2013.PubMedCentralCrossRefPubMedGoogle Scholar
  23. 23.
    Gadd, C. Use of a weighted impulse criterion for estimating injury hazard. Proceedings of the 10th Stapp Car Crash Conference, 1966, pp. 164–174.Google Scholar
  24. 24.
    Gazzaniga, M., R. B. Irvy, and G. R. Mangun. Cognitive Neuroscience The Biology of the Mind. New York: W. W. Norton & Company, 1998.Google Scholar
  25. 25.
    Gennarelli, T. A. Mechanisms of brain injury. J. Emerg. Med. 11:5–11, 1992.Google Scholar
  26. 26.
    Gennarelli, T. A., L. E. Thibault, J. H. Adams, D. I. Graham, C. J. Thompson, and R. P. Marcincin. Diffuse axonal injury and traumatic coma in the primate. Ann. Neurol. 12(6):564–574, 1982.CrossRefPubMedGoogle Scholar
  27. 27.
    Giordano, C., and S. Kleiven. Connecting fractional anisotropy from medical images with mechanical anisotropy of a hyperviscoelastic fibre-reinforced constitutive model for brain tissue. J. R. Soc. Interface 11:20130914, 2013.CrossRefPubMedGoogle Scholar
  28. 28.
    Goldstein, L. E., A. M. Fisher, C. A. Tagge, X.-L. Zhang, L. Velisek, J. A. Sullivan, C. Upreti, J. M. Kracht, M. Ericsson, M. W. Wojnarowicz, C. J. Goletiani, G. M. Maglakelidze, N. Casey, J. A. Moncaster, O. Minaeva, R. D. Moir, C. J. Nowinski, R. A. Stern, R. C. Cantu, J. Geiling, J. K. Blusztajn, B. L. Wolozin, T. Ikezu, T. D. Stein, A. E. Budson, N. W. Kowall, D. Chargin, A. Sharon, S. Saman, G. F. Hall, W. C. Moss, R. O. Cleveland, R. E. Tanzi, P. K. Stanton, and A. C. McKee. Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model. Sci. Transl. Med. 4(134):134–160, 2012.CrossRefGoogle Scholar
  29. 29.
    Greenwald, R., J. Gwin, J. Chu, and J. Crisco. Head impact severity measures for evaluating mild traumatic brain injury risk exposure. Neurosurgery 62(4):789–798, 2008.PubMedCentralCrossRefPubMedGoogle Scholar
  30. 30.
    Gurdjian, E. S., H. R. Lissner, F. R. Latimer, B. F. Haddad, and J. E. Webster. Quantitative determination of acceleration and intracranial pressure in experimental head injury; preliminary report. Neurology 3(6):417–423, 1953.CrossRefPubMedGoogle Scholar
  31. 31.
    Guskiewicz, K. M., M. McCrea, S. W. Marshall, R. C. Cantu, C. Randolph, W. Barr, J. A. Onate, and J. P. Kelly. Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA 290(19):2549–2555, 2003.CrossRefPubMedGoogle Scholar
  32. 32.
    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.PubMedGoogle Scholar
  33. 33.
    Hardy, W. N., M. J. Mason, C. D. Foster, C. S. Shah, J. M. Kopacz, H. Yang, A. I. King, J. Bishop, and M. Bey. A study of the response of the human cadaver head to impact. Stapp Car Crash J. 51:17–80, 2008.Google Scholar
  34. 34.
    Harmon, K. G., J. A. Drezner, M. Gammons, K. M. Guskiewicz, M. Halstead, S. A. Herring, J. S. Kutcher, A. Pana, M. Putukian, and W. O. Roberts. American Medical Society for Sports Medicine position statement: concussion in sport. Br. J. Sports Med. 47(1):15–26, 2013.CrossRefPubMedGoogle Scholar
  35. 35.
    Higgins, M., P. D. Halstead, L. Snyder-Mackler, and D. Barlow. Measurement of impact acceleration: mouthpiece accelerometer versus helmet accelerometer. J. Athl. Train. 42(1):5–10, 2007.PubMedCentralPubMedGoogle Scholar
  36. 36.
    Hoge, C. W., D. McGurk, J. L. Thomas, A. L. Cox, C. C. Engel, and C. A. Castro. Mild traumatic brain injury in U.S. Soldiers returning from Iraq. N. Engl. J. Med. 358(5):453–463, 2008.CrossRefPubMedGoogle Scholar
  37. 37.
    Holbourn, A. H. S. Mechanics of head injuries. Lancet 242(6267):438–441, 1943.CrossRefGoogle Scholar
  38. 38.
    Hosmer, D. W., S. Lemeshow, and R. X. Sturdivant. Applied Logistic Regression (3rd ed.). Hoboken, NJ: Wiley, 2013.CrossRefGoogle Scholar
  39. 39.
    Jadischke, R., D. C. Viano, N. Dau, A. I. King, and J. McCarthy. On the accuracy of the Head Impact Telemetry (HIT) System used in football helmets. J. Biomech. 46(13):2310–2315, 2013.CrossRefPubMedGoogle Scholar
  40. 40.
    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(1):11–24, 2014.PubMedCentralCrossRefPubMedGoogle Scholar
  41. 41.
    Kang, Y., 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 (6aω configuration). J. Biomech. Eng. 133(11):111007, 2011.CrossRefPubMedGoogle Scholar
  42. 42.
    Kimpara, H., and M. Iwamoto. Mild traumatic brain injury predictors based on angular accelerations during impacts. Ann. Biomed. Eng. 40(1):114–126, 2012.CrossRefPubMedGoogle Scholar
  43. 43.
    Kimpara, H., Y. Nakahira, and M. Iwamoto. Head injury prediction methods based on 6 degree of freedom head acceleration measurements during impact. Int. J. Automot. Eng. 2:13–19, 2011.Google Scholar
  44. 44.
    King, A. I., K. H. Yang, L. Zhang, W. Hardy, and D. C. Viano. Is head injury caused by linear or angular acceleration? Proceedings of the 2003 International IRCOBI Conference on the Biomechanics of Impact, pp. 1–12, 2003.Google Scholar
  45. 45.
    Kleinberger, M., E. Sun, R. Eppinger, S. Kuppa, and R. Saul. Head Injury Criteria. Development of Improved Injury Criteria for the Assessment of Advanced Automotive Restraint Systems, Washington, D.C.: National Highway Traffic Safety Administration, 1998, pp. 12–17.Google Scholar
  46. 46.
    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. Crashworthines 11(1):65–79, 2006.CrossRefGoogle Scholar
  47. 47.
    Kleiven, S. Predictors for traumatic brain injuries evaluated through accident reconstructions. Stapp Car Crash J. 51:81–114, 2007.PubMedGoogle Scholar
  48. 48.
    Margulies, S. S., and L. E. Thubault. A proposed tolerance criterion for diffuse axonal injury in man. J. Biomech. 25(8):917–923, 1992.CrossRefPubMedGoogle Scholar
  49. 49.
    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(3):1135–1148, 2008.CrossRefPubMedGoogle Scholar
  50. 50.
    Moon, D. W., C. W. Beedle, and C. R. Kovacic. Peak head acceleration of athletes during competition—football. Med. Sci. Sports 3(1):44–50, 1971.PubMedGoogle Scholar
  51. 51.
    National Operating Committee on Standards for Athletic Equipment (NOCSAE). Paper No. ND001-11m12. Standard Test Method and Equipment Used in Evaluating the Performance Characteristics of Protective Headgear/Equipment. 2012.Google Scholar
  52. 52.
    Naunheim, R. S., P. V. Bayly, J. Standeven, J. S. Neubauer, L. M. Lewis, and G. M. Genin. Linear and angular head accelerations during heading of a soccer ball. Med. Sci. Sports Exerc. 35(8):1406–1412, 2003.CrossRefPubMedGoogle Scholar
  53. 53.
    Naunheim, R. S., J. Standeven, C. Richter, and L. M. Lewis. Comparison of impact data in hockey, football, and soccer. J. Trauma 48(5):938–941, 2000.CrossRefPubMedGoogle Scholar
  54. 54.
    Newman, J. A generalized acceleration model for brain injury threshold (GAMBIT). Proceedings of the 1986 International IRCOBI Conference on the Biomechanics of Impact, 1986, pp. 121–131.Google Scholar
  55. 55.
    Newman, J. A., C. Barr, M. Beusenberg, E. Fournier, N. Shewchenko, E. Welbourne, and C. Withnall. A new biomechanical assessment of mild traumatic brain injury. Part 2: Results and conclusions. Proceedings of the 2000 International IRCOBI Conference on the Biomechanics of Impact, 2000, pp. 223–233.Google Scholar
  56. 56.
    Newman, J. A., M. C. Beusenberg, N. Shewchenko, C. Withnall, and E. Fournier. Verification of biomechanical methods employed in a comprehensive study of mild traumatic brain injury and the effectiveness of American football helmets. J. Biomech. 38(7):1469–1481, 2005.CrossRefPubMedGoogle Scholar
  57. 57.
    Newman, J., N. Shewchenko, and E. Welbourne. A proposed new biomechanical head injury assessment function-the maximum power index. Stapp Car Crash J. 44:215–247, 2000.PubMedGoogle Scholar
  58. 58.
    Newman, J. A., N. Shewchenko, and E. Welbourne. A proposed new biomechanical head injury assessment function—The Maximum Power Index. Stapp Car Crash J. 44(724):362, 2000.Google Scholar
  59. 59.
    Ommaya, A. K., F. Faas, and P. Yarnell. Whiplash injury and brain damage: an experimental study. JAMA 204(4):285–289, 1968.CrossRefPubMedGoogle Scholar
  60. 60.
    Ommaya, A. K., and T. A. Gennarelli. Cerebral concussion and traumatic unconsciousness. Correlation of experimental and clinical observations of blunt head injuries. Brain 97(4):633–654, 1974.CrossRefPubMedGoogle Scholar
  61. 61.
    Ommaya, A., and A. Hirsch. Tolerances for cerebral concussion from head impact and whiplash in primates. J. Biomech. 4(1):13–21, 1971.CrossRefPubMedGoogle Scholar
  62. 62.
    Ommaya, A., A. Hirsch, E. Flamm, and R. Mahone. Cerebral concussion in the monkey: an experimental model. Science 153(3732):211–212, 1966.CrossRefPubMedGoogle Scholar
  63. 63.
    Pellman, E. J., D. C. Viano, A. M. Tucker, and I. R. Casson. Concussion in professional football, Part 1: reconstruction of game impacts and injuries. Neurosurgery 53(4):799–812, 2003.PubMedGoogle Scholar
  64. 64.
    Pincemaille, Y., X. Trosseille, P. Mack, C. Tarriere, F. Breton, B. Renault, U. R. A. U. D. Recherche, and C. Pathologie. Some new data related to human tolerance obtained from volunteer boxers. Proceedings of the 33rd Stapp Car Crash Conference, SAE Paper No. 892435, 1989, pp. 177–190.Google Scholar
  65. 65.
    Prichep, L., and A. Jacquin. Classification of traumatic brain injury severity using informed data reduction in a series of binary classifier algorithms. IEEE Trans. Neural Syst. Rehabil. Eng. 20(6):806–822, 2012.Google Scholar
  66. 66.
    Qian, H., Y. Mao, W. Xiang, and Z. Wang. Home environment fall detection system based on a cascaded multi-SVM classifier. Proceedings of the 10th IEEE Conference on Control, Automation, Robotics and Vision, 2008, pp. 17–20.Google Scholar
  67. 67.
    Reid, S. E., H. M. Epstein, T. J. O’Dea, and M. W. Louis. Head protection in football. J. Sports Med. 2(2):86–92, 1974.CrossRefPubMedGoogle Scholar
  68. 68.
    Roth, T. L., D. Nayak, T. Atanasijevic, A. P. Koretsky, L. L. Latour, and D. B. McGavern. Transcranial amelioration of inflammation and cell death after brain injury. Nature 505(7482):223–228, 2014.PubMedCentralCrossRefPubMedGoogle Scholar
  69. 69.
    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. J. Appl. Biomech. 27(1):8–14, 2011.PubMedGoogle Scholar
  70. 70.
    Rowson, S., G. Brolinson, M. Goforth, D. Dietter, and S. M. Duma. Linear and angular head acceleration measurements in collegiate football. J. Biomech. Eng. 131(6):061016, 2009.CrossRefPubMedGoogle Scholar
  71. 71.
    Rowson, S., and S. M. Duma. Development of the STAR evaluation system for football helmets: integrating player head impact exposure and risk of concussion. Ann. Biomed. Eng. 39(8):2130–2140, 2011.CrossRefPubMedGoogle Scholar
  72. 72.
    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):1–13, 2012.CrossRefPubMedGoogle Scholar
  73. 73.
    Smith, D. H., V. E. Johnson, and W. Stewart. Chronic neuropathologies of single and repetitive TBI: substrates of dementia? Nat. Rev. Neurol. 9(4):211–221, 2013.PubMedCentralCrossRefPubMedGoogle Scholar
  74. 74.
    Smith, D. H., M. Nonaka, R. Miller, M. Leoni, X. H. Chen, D. Alsop, and D. F. Meaney. Immediate coma following inertial brain injury dependent on axonal damage in the brainstem. J. Neurosurg. 93(2):315–322, 2000.CrossRefPubMedGoogle Scholar
  75. 75.
    Takhounts, E. G., M. J. Craig, K. Moorhouse, J. Mcfadden, and V. Hasija. Development of brain injury criteria (BrIC). Stapp Car Crash J. 57:1–24, 2013.Google Scholar
  76. 76.
    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. 52:1–31, 2008.PubMedGoogle Scholar
  77. 77.
    Ungerleider, L. G., and M. Mishkin. Two cortical visual systems. Analysis of Visual Behavior, Cambridge, MA: MIT Press, 1982, pp. 549–586.Google Scholar
  78. 78.
    Versace, J. A review of the Severity Index. Proceedings of the 15th Stapp Car Crash Conference, SAE Paper No. 710881, 1971, pp. 771–796.Google Scholar
  79. 79.
    Ward, C., M. Chan, and A. Nahum. Intracranial pressure–a brain injury criterion. Stapp Car Crash J. 801304:163–185, 1980.Google Scholar
  80. 80.
    Zhang, L., K. H. Yang, and A. I. King. A proposed injury threshold for mild traumatic brain injury. J. Biomech. Eng. 126(2):226, 2004.CrossRefPubMedGoogle Scholar

Copyright information

© Biomedical Engineering Society 2014

Authors and Affiliations

  • Fidel Hernandez
    • 1
  • Lyndia C. Wu
    • 2
  • Michael C. Yip
    • 2
  • Kaveh Laksari
    • 2
  • Andrew R. Hoffman
    • 3
  • Jaime R. Lopez
    • 4
  • Gerald A. Grant
    • 5
  • Svein Kleiven
    • 6
  • David B. Camarillo
    • 1
    • 2
  1. 1.Department of Mechanical EngineeringStanford UniversityStanfordUSA
  2. 2.Department of BioengineeringStanford UniversityStanfordUSA
  3. 3.Department of MedicineStanford UniversityStanfordUSA
  4. 4.Department of NeurologyStanford UniversityStanfordUSA
  5. 5.Department of NeurosurgeryStanford UniversityStanfordUSA
  6. 6.Department of Neuronic EngineeringKTH Royal Institute of TechnologyStockholmSweden

Personalised recommendations