Animal models of traumatic brain injury

Nature Reviews Neuroscience

Volumn 14, Issue 2, 2013, Pages 128-142

  Xiong, Ye ^a   Mahmood, Asim ^a   Chopp, Michael ^b,c  

^a HENRY FORD HEALTH SYSTEM   (United States)

^b HENRY FORD HOSPITAL   (United States)

^c OAKLAND UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; ERYTHROPOIETIN; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL MODEL; BEHAVIOR DISORDER; BLAST INJURY; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; COGNITION; COGNITIVE DEFECT; COMORBIDITY; CONTROLLED CORTICAL IMPACT INJURY; DIFFUSE AXONAL INJURY; EXPERIMENTAL MODEL; FIBRINOLYTIC THERAPY; FLUID PERCUSSION INJURY; FUNCTIONAL ASSESSMENT; GLASGOW COMA SCALE; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; INJURY SCALE; MORBIDITY; MORTALITY; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; PATHOPHYSIOLOGY; PENETRATING BALLISTIC LIKE BRAIN INJURY; PERSONALITY; PRIORITY JOURNAL; REVIEW; SENSORIMOTOR FUNCTION; SPORT INJURY; SURVIVOR; TAUOPATHY; TRAFFIC ACCIDENT; TRAUMATIC BRAIN INJURY; WEIGHT DROP IMPACT ACCELERATION INJURY;

ANIMALS; BLAST INJURIES; BRAIN; BRAIN INJURIES; DISEASE MODELS, ANIMAL; HUMANS; NEUROPROTECTIVE AGENTS; RECOVERY OF FUNCTION; SPECIES SPECIFICITY; TRANSLATIONAL MEDICAL RESEARCH; TREATMENT OUTCOME;

ANIMALIA;

EID: 84872528255     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn3407     Document Type: Review

References (225)

1. Maas, A. I., Stocchetti, N. & Bullock, R. Moderate and severe traumatic brain injury in adults. Lancet Neurol. 7, 728-741 (2008). (Pubitemid 351957931)
2. Langlois, J. A., Rutland-Brown, W. & Wald, M. M. The epidemiology and impact of traumatic brain injury: a brief overview. J. Head Trauma Rehabil. 21, 375-378 (2006). (Pubitemid 44413110)
3. Masel, B. E. & DeWitt, D. S. Traumatic brain injury: a disease process, not an event. J. Neurotrauma 27, 1529-1540 (2010).
4. Davis, A. E. Mechanisms of traumatic brain injury: biomechanical, structural and cellular considerations. Crit. Care Nurs. Q. 23, 1-13 (2000).
5. Cernak, I. Animal models of head trauma. NeuroRx 2, 410-422 (2005). (Pubitemid 41444875)
6. Gaetz, M. The neurophysiology of brain injury. Clin. Neurophysiol. 115, 4-18 (2004). (Pubitemid 38045590)
7. Bramlett, H. M. & Dietrich, W. D. Progressive damage after brain and spinal cord injury: pathomechanisms and treatment strategies. Prog. Brain Res. 161, 125-141 (2007). (Pubitemid 47017402)
8. Thompson, H. J. et al. Lateral fluid percussion brain injury: a 15-year review and evaluation. J. Neurotrauma 22, 42-75 (2005).
9. Marklund, N., Bakshi, A., Castelbuono, D. J., Conte, V. & McIntosh, T. K. Evaluation of pharmacological treatment strategies in traumatic brain injury. Curr. Pharm. Des. 12, 1645-1680 (2006).
10. Povlishock, J. T. & Christman, C. W. The pathobiology of traumatically induced axonal injury in animals and humans: a review of current thoughts. J. Neurotrauma 12, 555-564 (1995).
11. Raghupathi, R. Cell death mechanisms following traumatic brain injury. Brain Pathol. 14, 215-222 (2004). (Pubitemid 38656395)
12. Raghupathi, R., Graham, D. I. & McIntosh, T. K. Apoptosis after traumatic brain injury. J. Neurotrauma 17, 927-938 (2000).
13. Yakovlev, A. G. et al. Differential expression of apoptotic protease-activating factor-1 and caspase-3 genes and susceptibility to apoptosis during brain development and after traumatic brain injury. J. Neurosci. 21, 7439-7446 (2001). (Pubitemid 32904942)
14. Niogi, S. N. et al. Extent of microstructural white matter injury in postconcussive syndrome correlates with impaired cognitive reaction time: a 3T diffusion tensor imaging study of mild traumatic brain injury. Am. J. Neuroradiol. 29, 967-973 (2008). (Pubitemid 351684976)
15. Lipton, M. L. et al. Multifocal white matter ultrastructural abnormalities in mild traumatic brain injury with cognitive disability: a voxel-wise analysis of diffusion tensor imaging. J. Neurotrauma 25, 1335-1342 (2008).
16. Rubovitch, V. et al. A mouse model of blast-induced mild traumatic brain injury. Exp. Neurol. 232, 280-289 (2011).
17. Browne, K. D., Chen, X. H., Meaney, D. F. & Smith, D. H. Mild traumatic brain injury and diffuse axonal injury in swine. J. Neurotrauma 28, 1747-1755 (2011).
18. Schouten, J. W. Neuroprotection in traumatic brain injury: a complex struggle against the biology of nature. Curr. Opin. Crit. Care 13, 134-142 (2007). (Pubitemid 46328326)
19. Margulies, S. & Hicks, R. Combination therapies for traumatic brain injury: prospective considerations. J. Neurotrauma 26, 925-939 (2009).
20. Gurdjian, E. S., Lissner, H. R., Webster, J. E., Latimer, F. R. & Haddad, B. F. Studies on experimental concussion: relation of physiologic effect to time duration of intracranial pressure increase at impact. Neurology 4, 674-681 (1954).
21. Walker, A. E. The physiological basis of concussion: 50 years later. J. Neurosurg. 81, 493-494 (1994).
22. Denny-Brown, D. E. & Russell, W. R. Experimental concussion: (section of neurology). Proc. R. Soc. Med. 34, 691-692 (1941).
23. Dixon, C. E. et al. A fluid percussion model of experimental brain injury in the rat. J. Neurosurg. 67, 110-119 (1987). (Pubitemid 17085024)
24. Dixon, C. E., Clifton, G. L., Lighthall, J. W., Yaghmai, A. A. & Hayes, R. L. A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods 39, 253-262 (1991).
25. Lighthall, J. W. Controlled cortical impact: a new experimental brain injury model. J. Neurotrauma 5, 1-15 (1988).
26. Marmarou, A. et al. A new model of diffuse brain injury in rats. Part I: pathophysiology and biomechanics. J. Neurosurg. 80, 291-300 (1994). (Pubitemid 24036501)
27. Cernak, I. et al. Involvement of the central nervous system in the general response to pulmonary blast injury. J. Trauma. 40, S100-S104 (1996). (Pubitemid 26089718)
28. Leung, L. Y. et al. Blast related neurotrauma: a review of cellular injury. Mol. Cell. Biomech. 5, 155-168 (2008).
29. Potts, M. B., Adwanikar, H. & Noble-Haeusslein, L. J. Models of traumatic cerebellar injury. Cerebellum 8, 211-221 (2009).
30. McIntosh, T. K., Noble, L., Andrews, B. & Faden, A. I. Traumatic brain injury in the rat: characterization of a midline fluid-percussion model. Cent. Nerv. Syst. Trauma 4, 119-134 (1987).
31. McIntosh, T. K. et al. Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28, 233-244 (1989). (Pubitemid 19026758)
32. Hardman, J. M. & Manoukian, A. Pathology of head trauma. Neuroimaging Clin. N. Am. 12, 175-187 (2002). (Pubitemid 34832747)
33. Graham, D. I., McIntosh, T. K., Maxwell, W. L. & Nicoll, J. A. Recent advances in neurotrauma. J. Neuropathol. Exp. Neurol. 59, 641-651 (2000). (Pubitemid 30626735)
34. Sanders, M. J., Dietrich, W. D. & Green, E. J. Cognitive function following traumatic brain injury: effects of injury severity and recovery period in a parasagittal fluid-percussive injury model. J. Neurotrauma 16, 915-925 (1999). (Pubitemid 29491763)
35. Vink, R., Mullins, P. G., Temple, M. D., Bao, W. & Faden, A. I. Small shifts in craniotomy position in the lateral fluid percussion injury model are associated with differential lesion development. J. Neurotrauma 18, 839-847 (2001). (Pubitemid 32769780)
36. Floyd, C. L., Golden, K. M., Black, R. T., Hamm, R. J. & Lyeth, B. G. Craniectomy position affects morris water maze performance and hippocampal cell loss after parasagittal fluid percussion. J. Neurotrauma 19, 303-316 (2002). (Pubitemid 34246118)
37. Hayes, R. L. et al. A new model of concussive brain injury in the cat produced by extradural fluid volume loading: II. Physiological and neuropathological observations. Brain Inj. 1, 93-112 (1987). (Pubitemid 18060753)
38. Hartl, R., Medary, M., Ruge, M., Arfors, K. E. & Ghajar, J. Blood-brain barrier breakdown occurs early after traumatic brain injury and is not related to white blood cell adherence. Acta Neurochir. Suppl. 70, 40-242 (1997).
39. Stalhammar, D. et al. A new model of concussive brain injury in the cat produced by extradural fluid volume loading: I. biomechanical properties. Brain Inj. 1, 73-91 (1987). (Pubitemid 18060752)
40. Carbonell, W. S., Maris, D. O., McCall, T. & Grady, M. S. Adaptation of the fluid percussion injury model to the mouse. J. Neurotrauma 15, 217-229 (1998). (Pubitemid 28113581)
41. Sullivan, H. G. et al. Fluid-percussion model of mechanical brain injury in the cat. J. Neurosurg. 45, 521-534 (1976).
42. Millen, J. E., Glauser, F. L. & Fairman, R. P. A comparison of physiological responses to percussive brain trauma in dogs and sheep. J. Neurosurg. 62, 587-591 (1985). (Pubitemid 15079427)
43. Dixon, C. E., Lighthall, J. W. & Anderson, T. E. Physiologic, histopathologic, and cineradiographic characterization of a new fluid-percussion model of experimental brain injury in the rat. J. Neurotrauma 5, 91-104 (1988). (Pubitemid 19060501)
44. Alder, J., Fujioka, W., Lifshitz, J., Crockett, D. P. & Thakker-Varia, S. Lateral fluid percussion: model of traumatic brain injury in mice. J. Vis. Exp. 54, e3063 (2011).
45. Pfenninger, E. G., Reith, A., Breitig, D., Grunert, A. & Ahnefeld, F. W. Early changes of intracranial pressure, perfusion pressure, and blood flow after acute head injury. Part 1: an experimental study of the underlying pathophysiology. J. Neurosurg. 70, 774-779 (1989). (Pubitemid 19124191)
46. Zink, B. J., Walsh, R. F. & Feustel, P. J. Effects of ethanol in traumatic brain injury. J. Neurotrauma 10, 275-286 (1993). (Pubitemid 23319196)
47. Hicks, R., Soares, H., Smith, D. & McIntosh, T. Temporal and spatial characterization of neuronal injury following lateral fluid-percussion brain injury in the rat. Acta Neuropathol. 91, 236-246 (1996). (Pubitemid 26042215)
48. Bramlett, H. M. & Dietrich, W. D. Quantitative structural changes in white and gray matter 1 year following traumatic brain injury in rats. Acta Neuropathol. 103, 607-614 (2002). (Pubitemid 36067509)
49. Liu, Y. R. et al. Progressive metabolic and structural cerebral perturbations after traumatic brain injury: an in vivo imaging study in the rat. J. Nucl. Med. 51, 1788-1795 (2010).
50. Morales, D. M. et al. Experimental models of traumatic brain injury: do we really need to build a better mousetrap? Neuroscience 136, 971-989 (2005). (Pubitemid 41790514)
51. Hamm, R. J. Neurobehavioral assessment of outcome following traumatic brain injury in rats: an evaluation of selected measures. J. Neurotrauma 18, 1207-1216 (2001). (Pubitemid 33062544)
52. Pierce, J. E., Smith, D. H., Trojanowski, J. Q. & McIntosh, T. K. Enduring cognitive, neurobehavioral and histopathological changes persist for up to one year following severe experimental brain injury in rats. Neuroscience 87, 359-369 (1998). (Pubitemid 28370896)
53. Kabadi, S. V., Hilton, G. D., Stoica, B. A., Zapple, D. N. & Faden, A. I. Fluid-percussion-induced traumatic brain injury model in rats. Nature Protoc. 5, 1552-1563 (2010).
54. Lifshitz, J., Kelley, J. B. & Povlishock, J. T. Perisomatic thalamic axotomy after diffuse traumatic brain injury is associated with atrophy rather than cell death. J. Neuropathol. Exp. Neurol. 66, 218-229 (2007). (Pubitemid 46673277)
55. Cao, T., Thomas, T. C., Ziebell, J. M., Pauly, J. R. & Lifshitz, J. Morphological and genetic activation of microglia after diffuse traumatic brain injury in the rat. Neuroscience 225, 65-75 (2012).
56. Smith, D. H. et al. A model of parasagittal controlled cortical impact in the mouse: cognitive and histopathologic effects. J. Neurotrauma 12, 169-178 (1995).
57. Lighthall, J. W., Goshgarian, H. G. & Pinderski, C. R. Characterization of axonal injury produced by controlled cortical impact. J. Neurotrauma 7, 65-76 (1990). (Pubitemid 20300339)
58. Manley, G. T. et al. Controlled cortical impact in swine: pathophysiology and biomechanics. J. Neurotrauma 23, 128-139 (2006).
59. King, C. et al. Brain temperature profiles during epidural cooling with the ChillerPad in a monkey model of traumatic brain injury. J. Neurotrauma 27, 1895-1903 (2010).
60. Hall, E. D. et al. Spatial and temporal characteristics of neurodegeneration after controlled cortical impact in mice: more than a focal brain injury. J. Neurotrauma 22, 252-265 (2005). (Pubitemid 40333519)
61. Mao, H., Zhang, L., Yang, K. H. & King, A. I. Application of a finite element model of the brain to study traumatic brain injury mechanisms in the rat. Stapp Car Crash J. 50, 583-600 (2006).
62. Wang, H. C. & Ma, Y. B. Experimental models of traumatic axonal injury. J. Clin. Neurosci. 17, 157-162 (2010).
63. Goodman, J. C., Cherian, L., Bryan, R. M. Jr & Robertson, C. S. Lateral cortical impact injury in rats: pathologic effects of varying cortical compression and impact velocity. J. Neurotrauma 11, 587-597 (1994). (Pubitemid 24347280)
64. Saatman, K. E., Feeko, K. J., Pape, R. L. & Raghupathi, R. Differential behavioral and histopathological responses to graded cortical impact injury in mice. J. Neurotrauma 23, 1241-1253 (2006). (Pubitemid 44681479)
65. Washington, P. M. et al. The effect of injury severity on behavior: a phenotypic study of cognitive and emotional deficits after mild, moderate and severe controlled cortical impact injury in mice. J. Neurotrauma 29, 2283-2296 (2012).
66. Fox, G. B., Fan, L., Levasseur, R. A. & Faden, A. I. Sustained sensory/motor and cognitive deficits with neuronal apoptosis following controlled cortical impact brain injury in the mouse. J. Neurotrauma 15, 599-614 (1998). (Pubitemid 28413053)
67. Marklund, N. & Hillered, L. Animal modelling of traumatic brain injury in preclinical drug development: where do we go from here? Br. J. Pharmacol. 164, 1207-1229 (2011).
68. Dixon, C. E. et al. Amantadine improves water maze performance without affecting motor behavior following traumatic brain injury in rats. Restor. Neurol. Neurosci. 14, 285-294 (1999). (Pubitemid 29281707)
69. Dixon, C. E. et al. One-year study of spatial memory performance, brain morphology, and cholinergic markers after moderate controlled cortical impact in rats. J. Neurotrauma 16, 109-122 (1999). (Pubitemid 29113822)
70. Kochanek, P. M. et al. Cerebral blood flow at one year after controlled cortical impact in rats: assessment by magnetic resonance imaging. J. Neurotrauma 19, 1029-1037 (2002).
71. Alessandri, B., Heimann, A., Filippi, R., Kopacz, L. & Kempski, O. Moderate controlled cortical contusion in pigs: effects on multi-parametric neuromonitoring and clinical relevance. J. Neurotrauma 20, 1293-1305 (2003). (Pubitemid 38018366)
72. Williams, A. J. et al. Characterization of a new rat model of penetrating ballistic brain injury. J. Neurotrauma 22, 313-331 (2005). (Pubitemid 40333524)
73. Williams, A. J., Hartings, J. A., Lu, X. C., Rolli, M. L. & Tortella, F. C. Penetrating ballistic-like brain injury in the rat: differential time courses of hemorrhage, cell death, inflammation, and remote degeneration. J. Neurotrauma 23, 1828-1846 (2006). (Pubitemid 46034455)
74. Williams, A. J., Ling, G. S. & Tortella, F. C. Severity level and injury track determine outcome following a penetrating ballistic-like brain injury in the rat. Neurosci. Lett. 408, 183-188 (2006). (Pubitemid 44528863)
75. Carey, M. E., Sarna, G. S. & Farrell, J. B. Brain edema following an experimental missile wound to the brain. J. Neurotrauma 7, 13-20 (1990). (Pubitemid 20154963)
76. Carey, M. E., Sarna, G. S., Farrell, J. B. & Happel, L. T. Experimental missile wound to the brain. J. Neurosurg. 71, 754-764 (1989). (Pubitemid 19275776)
77. Davis, A. R., Shear, D. A., Chen, Z., Lu, X. C. & Tortella, F. C. A comparison of two cognitive test paradigms in a penetrating brain injury model. J. Neurosci. Methods. 189, 84-87 (2010).
78. Williams, A. J., Wei, H. H., Dave, J. R. & Tortella, F. C. Acute and delayed neuroinflammatory response following experimental penetrating ballistic brain injury in the rat. J. Neuroinflamm. 4, 17 (2007).
79. Shear, D. A., Williams, A. J., Sharrow, K., Lu, X. C. & Tortella, F. C. Neuroprotective profile of dextromethorphan in an experimental model of penetrating ballistic-like brain injury. Pharmacol. Biochem. Behav. 94, 56-62 (2009).
80. Chen, Z. et al. Human amnion-derived multipotent progenitor cell treatment alleviates traumatic brain injury-induced axonal degeneration. J. Neurotrauma 26, 1987-1997 (2009).
81. Shear, D. A. et al. Longitudinal characterization of motor and cognitive deficits in a model of penetrating ballistic-like brain injury. J. Neurotrauma 27, 1911-1923 (2010).
82. Plantman, S., Ng, K. C., Lu, J., Davidsson, J. & Risling, M. Characterization of a novel rat model of penetrating traumatic brain injury. J. Neurotrauma 29, 1219-1232 (2012).
83. Wei, G., Lu, X. C., Yang, X. & Tortella, F. C. Intracranial pressure following penetrating ballistic-like brain injury in rats. J. Neurotrauma 27, 1635-1641 (2010).
84. Foda, M. A. & Marmarou, A. A new model of diffuse brain injury in rats. Part II: morphological characterization. J. Neurosurg. 80, 301-313 (1994). (Pubitemid 24036502)
85. Shear, D. A. et al. Severity profile of penetrating ballistic-like brain injury on neurofunctional outcome, blood-brain barrier permeability, and brain edema formation. J. Neurotrauma 28, 2185-2195 (2011).
86. Feeney, D. M., Boyeson, M. G., Linn, R. T., Murray, H. M. & Dail, W. G. Responses to cortical injury: I. Methodology and local effects of contusions in the rat. Brain Res. 211, 67-77 (1981). (Pubitemid 11147211)
87. Dail, W. G., Feeney, D. M., Murray, H. M., Linn, R. T. & Boyeson, M. G. Responses to cortical injury: II. widespread depression of the activity of an enzyme in cortex remote from a focal injury. Brain Res. 211, 79-89 (1981). (Pubitemid 11147212)
88. Gasparovic, C., Arfai, N., Smid, N. & Feeney, D. M. Decrease and recovery of N-acetylaspartate/creatine in rat brain remote from focal injury. J. Neurotrauma 18, 241-246 (2001). (Pubitemid 32230628)
89. Shapira, Y. et al. Experimental closed head injury in rats: mechanical, pathophysiologic, and neurologic properties. Crit. Care Med. 16, 258-265 (1988). (Pubitemid 18081907)
90. Shohami, E., Shapira, Y. & Cotev, S. Experimental closed head injury in rats: prostaglandin production in a noninjured zone. Neurosurgery 22, 859-863 (1988).
91. Chen, Y., Constantini, S., Trembovler, V., Weinstock, M. & Shohami, E. An experimental model of closed head injury in mice: pathophysiology, histopathology, and cognitive deficits. J. Neurotrauma 13, 557-568 (1996). (Pubitemid 26377854)
92. Stahel, P. F. et al. Experimental closed head injury: analysis of neurological outcome, blood-brain barrier dysfunction, intracranial neutrophil infiltration, and neuronal cell death in mice deficient in genes for pro-inflammatory cytokines. J. Cereb. Blood Flow Metab. 20, 369-380 (2000). (Pubitemid 30108456)
93. Flierl, M. A. et al. Mouse closed head injury model induced by a weight-drop device. Nature Protoc. 4, 1328-1337 (2009).
94. Goldstein, L. E. et al. Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model. Sci. Transl. Med. 4, 134ra60 (2012).
95. Albert-Weissenberger, C., Varrallyay, C., Raslan, F., Kleinschnitz, C. & Siren, A. L. An experimental protocol for mimicking pathomechanisms of traumatic brain injury in mice. Exp. Transl. Stroke Med. 4, 1 (2012).
96. Christman, C. W., Grady, M. S., Walker, S. A., Holloway, K. L. & Povlishock, J. T. Ultrastructural studies of diffuse axonal injury in humans. J. Neurotrauma 11, 173-186 (1994). (Pubitemid 24174506)
97. Johnson, V. E., Stewart, W. & Smith, D. H. Axonal pathology in traumatic brain injury. Exp. Neurol. 20 Jan 2012 (doi:10.1016/j.expneurol.2012. 01.013).
98. Heath, D. L. & Vink, R. Impact acceleration-induced severe diffuse axonal injury in rats: characterization of phosphate metabolism and neurologic outcome. J. Neurotrauma 12, 1027-1034 (1995). (Pubitemid 26044666)
99. Schmidt, R. H., Scholten, K. J. & Maughan, P. H. Cognitive impairment and synaptosomal choline uptake in rats following impact acceleration injury. J. Neurotrauma 17, 1129-1139 (2000).
100. Shohami, E., Shapira, Y., Sidi, A. & Cotev, S. Head injury induces increased prostaglandin synthesis in rat brain. J. Cereb. Blood Flow Metab. 7, 58-63 (1987). (Pubitemid 17018315)
101. Kilbourne, M. et al. Novel model of frontal impact closed head injury in the rat. J. Neurotrauma 26, 2233-2243 (2009).
102. Warden, D. Military TBI during the Iraq and Afghanistan wars. J. Head Trauma Rehabil. 21, 398-402 (2006). (Pubitemid 44413113)
103. Benzinger, T. L. et al. Blast-related brain injury: imaging for clinical and research applications: report of the 2008 St. Louis workshop. J. Neurotrauma 26, 2127-2144 (2009).
104. Wang, Y. et al. Tightly coupled repetitive blast-induced traumatic brain injury: development and characterization in mice. J. Neurotrauma 28, 2171-2183 (2011).
105. Cheng, J. et al. Development of a rat model for studying blast-induced traumatic brain injury. J. Neurol. Sci. 294, 23-28 (2010).
106. Risling, M. & Davidsson, J. Experimental animal models for studies on the mechanisms of blast-induced neurotrauma. Front. Neurol. 3, 30 (2012).
107. Long, J. B. et al. Blast overpressure in rats: recreating a battlefield injury in the laboratory. J. Neurotrauma 26, 827-840 (2009).
108. Bauman, R. A. et al. An introductory characterization of a combat-casualty-care relevant swine model of closed head injury resulting from exposure to explosive blast. J. Neurotrauma 26, 841-860 (2009).
109. de Lanerolle, N. C. et al. Characteristics of an explosive blast-induced brain injury in an experimental model. J. Neuropathol. Exp. Neurol. 70, 1046-1057 (2011).
110. DeWitt, D. S. & Prough, D. S. Blast-induced brain injury and posttraumatic hypotension and hypoxemia. J. Neurotrauma 26, 877-887 (2009).
111. Reneer, D. V. et al. A multi-mode shock tube for investigation of blast-induced traumatic brain injury. J. Neurotrauma 28, 95-104 (2011).
112. Cernak, I. & Noble-Haeusslein, L. J. Traumatic brain injury: an overview of pathobiology with emphasis on military populations. J. Cereb. Blood Flow Metab. 30, 255-266 (2010).
113. Garman, R. H. et al. Blast exposure in rats with body shielding is characterized primarily by diffuse axonal injury. J. Neurotrauma 28, 947-959 (2011).
114. Kuehn, R. et al. Rodent model of direct cranial blast injury. J. Neurotrauma 28, 2155-2169 (2011).
115. Saljo, A., Svensson, B., Mayorga, M., Hamberger, A. & Bolouri, H. Low-level blasts raise intracranial pressure and impair cognitive function in rats. J. Neurotrauma 26, 1345-1352 (2009).
116. Cernak, I. et al. The pathobiology of blast injuries and blast-induced neurotrauma as identified using a new experimental model of injury in mice. Neurobiol. Dis. 41, 538-551 (2011).
117. Koliatsos, V. E. et al. A mouse model of blast injury to brain: initial pathological, neuropathological, and behavioral characterization. J. Neuropathol. Exp. Neurol. 70, 399-416 (2011).
118. Bhattacharjee, Y. Neuroscience. Shell shock revisited: solving the puzzle of blast trauma. Science. 319, 406-408 (2008). (Pubitemid 351160556)
119. Sundaramurthy, A. et al. Blast-induced biomechanical loading of the rat: experimental and anatomically accurate computational blast injury model. J. Neurotrauma 29, 2352-2364 (2012).
120. Daneshvar, D. H. et al. Long-term consequences: effects on normal development profile after concussion. Phys. Med. Rehabil. Clin. N. Am. 22, 683-700, ix (2011).
121. [No authors listed.] Sports-related recurrent brain injuries - United States. Centers for disease control and prevention. Int. J. Trauma Nurs. 3, 88-90 (1997).
122. Weber, J. T. Experimental models of repetitive brain injuries. Prog. Brain Res. 161, 253-261 (2007). (Pubitemid 47017409)
123. Daneshvar, D. H., Nowinski, C. J., McKee, A. C. & Cantu, R. C. The epidemiology of sport-related concussion. Clin. Sports Med. 30, 1-17 (2011).
124. DeFord, S. M. et al. Repeated mild brain injuries result in cognitive impairment in B6C3F1 mice. J. Neurotrauma 19, 427-438 (2002).
125. Creeley, C. E., Wozniak, D. F., Bayly, P. V., Olney, J. W. & Lewis, L. M. Multiple episodes of mild traumatic brain injury result in impaired cognitive performance in mice. Acad. Emerg. Med. 11, 809-819 (2004). (Pubitemid 38951088)
126. DeRoss, A. L. et al. Multiple head injuries in rats: effects on behavior. J. Trauma. 52, 708-714 (2002).
127. Raghupathi, R. & Margulies, S. S. Traumatic axonal injury after closed head injury in the neonatal pig. J. Neurotrauma 19, 843-853 (2002). (Pubitemid 34815502)
128. Kane, M. J. et al. A mouse model of human repetitive mild traumatic brain injury. J. Neurosci. Methods. 203, 41-49 (2012).
129. Shultz, S. R., MacFabe, D. F., Foley, K. A., Taylor, R. & Cain, D. P. A single mild fluid percussion injury induces short-term behavioral and neuropathological changes in the Long-Evans rat: support for an animal model of concussion. Behav. Brain Res. 224, 326-335 (2011).
130. Shultz, S. R. et al. Repeated mild lateral fluid percussion brain injury in the rat causes cumulative long-term behavioral impairments, neuroinflammation, and cortical loss in an animal model of repeated concussion. J. Neurotrauma 29, 281-294 (2012).
131. Shultz, S. R., MacFabe, D. F., Foley, K. A., Taylor, R. & Cain, D. P. Sub-concussive brain injury in the Long- Evans rat induces acute neuroinflammation in the absence of behavioral impairments. Behav. Brain Res. 229, 145-152 (2012).
132. Friess, S. H. et al. Repeated traumatic brain injury affects composite cognitive function in piglets. J. Neurotrauma 26, 1111-1121 (2009).
133. Laurer, H. L. & McIntosh, T. K. Experimental models of brain trauma. Curr. Opin. Neurol. 12, 715-721 (1999). (Pubitemid 30072353)
134. Povlishock, J. T., Hayes, R. L., Michel, M. E. & McIntosh, T. K. Workshop on animal models of traumatic brain injury. J. Neurotrauma 11, 723-732 (1994).
135. Reid, W. M. et al. Strain-related differences after experimental traumatic brain injury in rats. J. Neurotrauma 27, 1243-1253 (2010).
136. Tan, A. A., Quigley, A., Smith, D. C. & Hoane, M. R. Strain differences in response to traumatic brain injury in Long-Evans compared to Sprague-Dawley rats. J. Neurotrauma 26, 539-548 (2009).
137. Fox, G. B., LeVasseur, R. A. & Faden, A. I. Behavioral responses of C57BL/6, FVB/N, and 129/SvEMS mouse strains to traumatic brain injury: implications for gene targeting approaches to neurotrauma. J. Neurotrauma 16, 377-389 (1999). (Pubitemid 29264790)
138. Roof, R. L. & Hall, E. D. Estrogen-related gender difference in survival rate and cortical blood flow after impact-acceleration head injury in rats. J. Neurotrauma 17, 1155-1169 (2000).
139. Berry, C. et al. The effect of gender on patients with moderate to severe head injuries. J. Trauma. 67, 950-953 (2009).
140. Stein, D. G. Progesterone in the treatment of acute traumatic brain injury: a clinical perspective and update. Neuroscience 191, 101-106 (2011).
141. Junpeng, M., Huang, S. & Qin, S. Progesterone for acute traumatic brain injury. Cochrane Database Syst. Rev. CD008409 (2011).
142. Farace, E. & Alves, W. M. Do women fare worse: a metaanalysis of gender differences in traumatic brain injury outcome. J. Neurosurg. 93, 539-545 (2000). (Pubitemid 32799285)
143. Maas, A. I. & Lingsma, H. F. New approaches to increase statistical power in TBI trials: insights from the IMPACT study. Acta Neurochir. Suppl. 101, 119-124 (2008).
144. Lu, J., Marmarou, A., Lapane, K., Turf, E. & Wilson, L. A method for reducing misclassification in the extended Glasgow Outcome Score. J. Neurotrauma 27, 843-852 (2010).
145. Beit-Yannai, E., Zhang, R., Trembovler, V., Samuni, A. & Shohami, E. Cerebroprotective effect of stable nitroxide radicals in closed head injury in the rat. Brain Res. 717, 22-28 (1996). (Pubitemid 26155070)
146. Markgraf, C. G. et al. Injury severity and sensitivity to treatment after controlled cortical impact in rats. J. Neurotrauma 18, 175-186 (2001). (Pubitemid 32173425)
147. Jiang, Q. et al. MRI evaluation of axonal reorganization after bone marrow stromal cell treatment of traumatic brain injury. NMR Biomed. 24, 1119-1128 (2011).
148. Li, L. et al. MRI measurement of angiogenesis and the therapeutic effect of acute marrow stromal cell administration on traumatic brain injury. J. Neurotrauma 32, 2023-2032 (2012).
149. Kou, Z. et al. The role of advanced MR imaging findings as biomarkers of traumatic brain injury. J. Head Trauma Rehabil. 25, 267-282 (2010).
150. Benson, R. R. et al. Global white matter analysis of diffusion tensor images is predictive of injury severity in traumatic brain injury. J. Neurotrauma 24, 446-459 (2007). (Pubitemid 46598279)
151. Li, L. et al. Transplantation of marrow stromal cells restores cerebral blood flow and reduces cerebral atrophy in rats with traumatic brain injury: in vivo MRI study. J. Neurotrauma 28, 535-545 (2011).
152. Immonen, R. J., Kharatishvili, I., Grohn, H., Pitkanen, A. & Grohn, O. H. Quantitative MRI predicts long-term structural and functional outcome after experimental traumatic brain injury. Neuroimage 45, 1-9 (2009).
153. Ehrenreich, H. et al. Erythropoietin therapy for acute stroke is both safe and beneficial. Mol. Med. 8, 495-505 (2002). (Pubitemid 36337492)
154. Ehrenreich, H. et al. Recombinant human erythropoietin in the treatment of acute ischemic stroke. Stroke 40, e647-e656 (2009).
155. Jia, L., Chopp, M., Zhang, L., M. Lu & Zhang, Z. Erythropoietin in combination of tissue plasminogen activator exacerbates brain hemorrhage when treatment is initiated 6 hours after stroke. Stroke 41, 2071-2076 (2010).
156. Zechariah, A., ElAli, A. & Hermann, D. M. Combination of tissue-plasminogen activator with erythropoietin induces blood-brain barrier permeability, extracellular matrix disaggregation, and DNA fragmentation after focal cerebral ischemia in mice. Stroke 41, 1008-1012 (2010).
157. Loane, D. J. & Faden, A. I. Neuroprotection for traumatic brain injury: translational challenges and emerging therapeutic strategies. Trends Pharmacol. Sci. 31, 596-604 (2010).
158. Menon, D. K. Unique challenges in clinical trials in traumatic brain injury. Crit. Care Med. 37, S129-S135 (2009).
159. Zhang, Z. G. & Chopp, M. Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic. Lancet Neurol. 8, 491-500 (2009).
160. Fujimoto, S. T. et al. Motor and cognitive function evaluation following experimental traumatic brain injury. Neurosci. Biobehav. Rev. 28, 365-378 (2004). (Pubitemid 39077928)
161. Mahmood, A., D. Lu, C. Qu, Goussev, A. & Chopp, M. Long-term recovery after bone marrow stromal cell treatment of traumatic brain injury in rats. J. Neurosurg. 104, 272-277 (2006).
162. Smith, D. H. et al. Progressive atrophy and neuron death for one year following brain trauma in the rat. J. Neurotrauma 14, 715-727 (1997). (Pubitemid 27479412)
163. Ning, R. et al. Erythropoietin promotes neurovascular remodeling and long-term functional recovery in rats following traumatic brain injury. Brain Res. 1384, 140-150 (2011).
164. Meng, Y. et al. Dose-dependent neurorestorative effects of delayed treatment of traumatic brain injury with recombinant human erythropoietin in rats. J. Neurosurg. 115, 550-560 (2011).
165. Mahmood, A., Lu, D., Yi, L., Chen, J. L. & Chopp, M. Intracranial bone marrow transplantation after traumatic brain injury improving functional outcome in adult rats. J. Neurosurg. 94, 589-595 (2001). (Pubitemid 32799652)
166. Xiong, Y. et al. Delayed transplantation of human marrow stromal cell-seeded scaffolds increases transcallosal neural fiber length, angiogenesis, and hippocampal neuronal survival and improves functional outcome after traumatic brain injury in rats. Brain Res. 1263, 183-191 (2009).
167. Lindner, M. D. et al. Dissociable long-term cognitive deficits after frontal versus sensorimotor cortical contusions. J. Neurotrauma 15, 199-216 (1998). (Pubitemid 28113580)
168. Shear, D. A. et al. Neural progenitor cell transplants promote long-term functional recovery after traumatic brain injury. Brain Res. 1026, 11-22 (2004). (Pubitemid 39336412)
169. Salmond, C. H. & Sahakian, B. J. Cognitive outcome in traumatic brain injury survivors. Curr. Opin. Crit. Care 11, 111-116 (2005). (Pubitemid 40488608)
170. Sinson, Voddi, G. M. & McIntosh, T. K. Nerve growth factor administration attenuates cognitive but not neurobehavioral motor dysfunction or hippocampal cell loss following fluid-percussion brain injury in rats. J. Neurochem. 65, 2209-2216 (1995).
171. Hyder, A. A., Wunderlich, C. A., Puvanachandra, P., Gururaj, G. & Kobusingye, O. C. The impact of traumatic brain injuries: a global perspective. NeuroRehabilitation 22, 341-353 (2007).
172. Hellewell, S. C., Yan, E. B., Agyapomaa, D. A., Bye, N. & Morganti-Kossmann, M. C. Post-traumatic hypoxia exacerbates brain tissue damage: analysis of axonal injury and glial responses. J. Neurotrauma 27, 1997-2010 (2010).
173. Robertson, C. L. et al. No long-term benefit from hypothermia after severe traumatic brain injury with secondary insult in rats. Crit. Care Med. 28, 3218-3223 (2000).
174. Stiefel, M. F., Tomita, Y. & Marmarou, A. Secondary ischemia impairing the restoration of ion homeostasis following traumatic brain injury. J. Neurosurg. 103, 707-714 (2005). (Pubitemid 43193879)
175. Bramlett, H. M., Dietrich, W. D. & Green, E. J. Secondary hypoxia following moderate fluid percussion brain injury in rats exacerbates sensorimotor and cognitive deficits. J. Neurotrauma 16, 1035-1047 (1999).
176. Matsushita, Y., Bramlett, H. M., Kuluz, J. W., Alonso, O. & Dietrich, W. D. Delayed hemorrhagic hypotension exacerbates the hemodynamic and histopathologic consequences of traumatic brain injury in rats. J. Cereb. Blood Flow Metab. 21, 847-856 (2001). (Pubitemid 32613539)
177. Sawauchi, S., Marmarou, A., Beaumont, A., Signoretti, S. & Fukui, S. Acute subdural hematoma associated with diffuse brain injury and hypoxemia in the rat: effect of surgical evacuation of the hematoma. J. Neurotrauma 21, 563-573 (2004). (Pubitemid 38656753)
178. Keel, M. & Trentz, O. Pathophysiology of polytrauma. Injury 36, 691-709 (2005). (Pubitemid 40732303)
179. Maegele, M. et al. Differential immunoresponses following experimental traumatic brain injury, bone fracture and "two-hit"-combined neurotrauma. Inflamm. Res. 56, 318-323 (2007). (Pubitemid 47237968)
180. Prins, M. L. & Hovda, D. A. Developing experimental models to address traumatic brain injury in children. J. Neurotrauma 20, 123-137 (2003). (Pubitemid 36292823)
181. Potts, M. B. et al. Traumatic injury to the immature brain: inflammation, oxidative injury, and iron-mediated damage as potential therapeutic targets. NeuroRx 3, 143-153 (2006). (Pubitemid 44061703)
182. Giza, C. C., Kolb, B., Harris, N. G., Asarnow, R. F. & Prins, M. L. Hitting a moving target: basic mechanisms of recovery from acquired developmental brain injury. Dev. Neurorehabil. 12, 255-268 (2009).
183. Ibrahim, N. G., Ralston, J., Smith, C. & Margulies, S. S. Physiological and pathological responses to head rotations in toddler piglets. J. Neurotrauma 27, 1021-1035 (2010).
184. Hoane, M. R., Lasley, L. A. & Akstulewicz, S. L. Middle age increases tissue vulnerability and impairs sensorimotor and cognitive recovery following traumatic brain injury in the rat. Behav. Brain Res. 153, 189-197 (2004). (Pubitemid 38829301)
185. Flanagan, S. R., Hibbard, M. R. & Gordon, W. A. The impact of age on traumatic brain injury. Phys. Med. Rehabil. Clin. N. Am. 16, 163-177 (2005). (Pubitemid 39550549)
186. Thompson, H. J., McCormick, W. C. & Kagan, S. H. Traumatic brain injury in older adults: epidemiology, outcomes, and future implications. J. Am. Geriatr. Soc. 54, 1590-1595 (2006). (Pubitemid 44566364)
187. Depreitere, B., Meyfroidt, G., Roosen, G., Ceuppens, J. & Grandas, F. G. Traumatic brain injury in the elderly: a significant phenomenon. Acta Neurochir Suppl. 114, 289-294 (2012).
188. Xiong, Y., Mahmood, A. & Chopp, M. Emerging treatments for traumatic brain injury. Expert Opin. Emerg. Drugs 14, 67-84 (2009).
189. Clifton, G. L. et al. Early induction of hypothermia for evacuated intracranial hematomas: a post hoc analysis of two clinical trials. J. Neurosurg. 117, 714-720 (2012).
190. Hamm, R. J. et al. Cognitive deficits following traumatic brain injury produced by controlled cortical impact. J. Neurotrauma 9, 11-20 (1992).
191. Smith, D. H., Okiyama, K., Thomas, M. J., Claussen, B. & McIntosh, T. K. Evaluation of memory dysfunction following experimental brain injury using the Morris water maze. J. Neurotrauma 8, 259-269 (1991).
192. Richardson, R. M., Sun, D. & Bullock, M. R. Neurogenesis after traumatic brain injury. Neurosurg. Clin. N. Am. 18, 169-181 (2007). (Pubitemid 46164759)
193. Bullock, M. R. et al. Outcome measures for clinical trials in neurotrauma. Neurosurg. Focus 13, ECP1 (2002).
194. Maas, A. I. et al. IMPACT recommendations for improving the design and analysis of clinical trials in moderate to severe traumatic brain injury. Neurotherapeutics 7, 127-134 (2010).
195. Saatman, K. E. et al. Classification of traumatic brain injury for targeted therapies. J. Neurotrauma 25, 719-738 (2008).
196. Doppenberg, E. M., Choi, S. C. & Bullock, R. Clinical trials in traumatic brain injury: lessons for the future. J. Neurosurg. Anesthesiol. 16, 87-94 (2004). (Pubitemid 38057407)
197. Andriessen, T. M., Jacobs, B. & Vos, P. E. Clinical characteristics and pathophysiological mechanisms of focal and diffuse traumatic brain injury. J. Cell. Mol. Med. 14, 2381-2392 (2010).
198. Muir, K. W. Glutamate-based therapeutic approaches: clinical trials with NMDA antagonists. Curr. Opin. Pharmacol. 6, 53-60 (2006). (Pubitemid 43103819)
199. Lee, L. L., Galo, E., Lyeth, B. G., Muizelaar, J. P. & Berman, R. F. Neuroprotection in the rat lateral fluid percussion model of traumatic brain injury by SNX-185, an N-type voltage-gated calcium channel blocker. Exp. Neurol. 190, 70-78 (2004). (Pubitemid 39335707)
200. Xiong, Y., Q. Gu, Peterson, P. L., Muizelaar, J. P. & Lee, C. P. Mitochondrial dysfunction and calcium perturbation induced by traumatic brain injury. J. Neurotrauma 14, 23-34 (1997). (Pubitemid 27100278)
201. McCall, J. M., Braughler, J. M. & Hall, E. D. Lipid peroxidation and the role of oxygen radicals in CNS injury. Acta Anaesthesiol. Belg. 38, 373-379 (1987).
202. Bains, M. & Hall, E. D. Antioxidant therapies in traumatic brain and spinal cord injury. Biochim. Biophys. Acta. 1822, 675-684 (2012).
203. Raghavendra Rao, V. L., Dhodda, V. K., Song, G., Bowen, K. K. & Dempsey, R. J. Traumatic brain injury-induced acute gene expression changes in rat cerebral cortex identified by GeneChip analysis. J. Neurosci. Res. 71, 208-219 (2003). (Pubitemid 36055465)
204. Ziebell, J. M. & Morganti-Kossmann, M. C. Involvement of pro- and anti-inflammatory cytokines and chemokines in the pathophysiology of traumatic brain injury. Neurotherapeutics 7, 22-30 (2010).
205. Chen, J. et al. Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke 32, 2682-2688 (2001). (Pubitemid 33055324)
206. Mahmood, A. D. Lu & Chopp, M. Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J. Neurotrauma 21, 33-39 (2004). (Pubitemid 38141800)
207. Levin, H. S., Eisenberg, H. M., Wigg, N. R. & Kobayashi, K. Memory and intellectual ability after head injury in children and adolescents. Neurosurgery 11, 668-673 (1982). (Pubitemid 13205869)
208. Fox, G. B. & Faden, A. I. Traumatic brain injury causes delayed motor and cognitive impairment in a mutant mouse strain known to exhibit delayed Wallerian degeneration. J. Neurosci. Res. 53, 718-727 (1998). (Pubitemid 28423879)
209. Schwarzbold, M. L. et al. Effects of traumatic brain injury of different severities on emotional, cognitive, and oxidative stress-related parameters in mice. J. Neurotrauma 27, 1883-1893 (2010).
210. Pandey, D. K., Yadav, S. K., Mahesh, R. & Rajkumar, R. Depression-like and anxiety-like behavioural aftermaths of impact accelerated traumatic brain injury in rats: a model of comorbid depression and anxiety? Behav. Brain Res. 205, 436-442 (2009).
211. Jones, N. C. et al. Experimental traumatic brain injury induces a pervasive hyperanxious phenotype in rats. J. Neurotrauma 25, 1367-1374 (2008).
212. Milman, A., Rosenberg, A., Weizman, R. & Pick, C. G. Mild traumatic brain injury induces persistent cognitive deficits and behavioral disturbances in mice. J. Neurotrauma 22, 1003-1010 (2005). (Pubitemid 41362066)
213. Friess, S. H. et al. Neurobehavioral functional deficits following closed head injury in the neonatal pig. Exp. Neurol. 204, 234-243 (2007). (Pubitemid 46330274)
214. Narayan, R. K. et al. Clinical trials in head injury. J. Neurotrauma 19, 503-557 (2002). (Pubitemid 34587299)
215. Stein, D. G. & Wright, D. W. Progesterone in the clinical treatment of acute traumatic brain injury. Expert Opin. Investig. Drugs 19, 847-857 (2010).
216. Beauchamp, K., Mutlak, H., Smith, W. R., Shohami, E. & Stahel, P. F. Pharmacology of traumatic brain injury: where is the "golden bullet"? Mol. Med. 14, 731-740 (2008).
217. Lu, D. et al. Erythropoietin enhances neurogenesis and restores spatial memory in rats after traumatic brain injury. J. Neurotrauma 22, 1011-1017 (2005). (Pubitemid 41362067)
218. Lu, D. et al. Atorvastatin reduces neurological deficit and increases synaptogenesis, angiogenesis, and neuronal survival in rats subjected to traumatic brain injury. J. Neurotrauma 21, 21-32 (2004). (Pubitemid 38141799)
219. Zhang, Y. et al. Sprouting of corticospinal tract axons from the contralateral hemisphere into the denervated side of the spinal cord is associated with functional recovery in adult rat after traumatic brain injury and erythropoietin treatment. Brain Res. 1353, 249-257 (2010).
220. Oshima, T. et al. TNF-α contributes to axonal sprouting and functional recovery following traumatic brain injury. Brain Res. 1290, 102-110 (2009).
221. Xiong, Y. et al. Delayed administration of erythropoietin reducing hippocampal cell loss, enhancing angiogenesis and neurogenesis, and improving functional outcome following traumatic brain injury in rats: comparison of treatment with single and triple dose. J. Neurosurg. 113, 598-608 (2010).
222. Xiong, Y., Mahmood, A. & Chopp, M. Neurorestorative treatments for traumatic brain injury. Discov. Med. 10, 434-442 (2010).
223. Xiong, Y. et al. Treatment of traumatic brain injury with thymosin β4 in rats. J. Neurosurg. 114, 102-115 (2011).
224. Armstead, W. M. Vasopressin-induced protein kinase C-dependent superoxide generation contributes to atp-sensitive potassium channel but not calcium-sensitive potassium channel function impairment after brain injury. Stroke 32, 1408-1414 (2001). (Pubitemid 32530432)
225. Albert-Weissenberger, C. & Siren, A. L. Experimental traumatic brain injury. Exp. Transl. Stroke Med. 2, 16 (2010).