Penetrating ballistic-like brain injury in the rat: Differential time courses of hemorrhage, cell death, inflammation, and remote degeneration

Journal of Neurotrauma

Volumn 23, Issue 12, 2006, Pages 1828-1846

  Williams, Anthony J ^a   Hartings, Jed A ^a   Lu, Xi Chun M ^a   Rolli, Michael L ^a   Tortella, Frank C ^a  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

Axonal injury; Inflammation; Military injury; Models of injury; Traumatic brain injury

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HEMORRHAGE; BRAIN INJURY; BRAIN REGION; CAPSULA INTERNA; CELL DEATH; CELL DEGENERATION; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE COURSE; ENCEPHALITIS; FRONTAL CORTEX; GUNSHOT INJURY; MACROPHAGE; MALE; NERVE CELL DEGENERATION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PENETRATING TRAUMA; RAT; THALAMUS; TRAUMATIC BRAIN INJURY; VOLUMETRY;

ANIMALS; BRAIN INJURIES; CEREBRAL HEMORRHAGE, TRAUMATIC; DISEASE MODELS, ANIMAL; ENCEPHALITIS; MALE; NECROSIS; NERVE DEGENERATION; NEUTROPHIL INFILTRATION; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS; WOUNDS, GUNSHOT;

EID: 33845915777     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2006.23.1828     Document Type: Article

References (74)

1. ADAMS, J.H. (1982). Diffuse axonal injury in non-missile head injury. Injury 13, 444-445.
2. AL-ABDULLA, N.A., and MARTIN, L.J. (2002). Projection neurons and interneurons in the lateral geniculate nucleus undergo distinct forms of degeneration ranging from retrograde and transsynaptic apoptosis to transient atrophy after cortical ablation in rat. Neuroscience 115, 7-14.
3. ALLEN, I.V., SCOTT, R., and TANNER, J.A. (1982). Experimental high-velocity missile head injury. Injury 14, 183-193.
4. AWASTHI, D., ROCK, W.A., CAREY, M.E., and FARRELL, J.B. (1991). Coagulation changes after an experimental missile wound to the brain in the cat. Surg. Neurol. 36, 441-446.
5. BELLAMY, R., and ZAJTCHUK, R. (1998). The physics and biophysics of wound ballistics, in: The Textbook of Military Medicine, Part 1, Volume 5. Office of the Surgeon General: Washington, DC, pps. 107-144.
6. BETHEA, J.R., and DIETRICH, W.D. (2002). Targeting the host inflammatory response in traumatic spinal cord injury. Curr. Opin. Neurol. 15, 355-360.
7. BOYA, J., CALVO, J., CARBONELL, A.L., and GARCIA-MAURINO, E. (1986). Nature of macrophages in rat brain. A histochemical study. Acta Anat. (Basel) 127, 142-145.
8. BRAMLETT, H.M., and DIETRICH, W.D. (2004). Pathophysiology of cerebral ischemia and brain trauma: similarities and differences. J. Cereb. Blood Flow Metab. 24, 133-150.
9. BUTLER, E., PUCKETT, W., HARVEY, E., and McMILLAN, J. (1945). Experiments on head wounding by high velocity missiles. J. Neurosurg. 2, 358-363.
10. BUTLER, T.L., KASSED, C.A., SANBERG, P.R., WILLING, A.E., and PENNYPACKER, K.R. (2002). Neurodegeneration in the rat hippocampus and striatum after middle cerebral artery occlusion. Brain Res. 929, 252-260.
11. CAREY, M.E., SARNA, G.S., and FARRELL, J.B. (1990). Brain edema following an experimental missile wound to the brain. J. Neurotrauma 7, 13-20.
12. CAREY, M.E., SARNA, G.S., FARRELL, J.B., and HAPPEL, L.T. (1989). Experimental missile wound to the brain. J. Neurosurg. 71, 754-764.
13. CHEN, S., PICKARD, J.D., and HARRIS, N.G. (2003). Time course of cellular pathology after controlled cortical impact injury. Exp. Neurol. 182, 87-102.
14. CHURCH, A.J., and ANDREW, R.D. (2005). Spreading depression expands traumatic injury in neocortical brain slices. J. Neurotrauma 22, 277-290.
15. CLARK, R., LEE, E., FISH, C., et al. (1993). Development of tissue damage, inflammation and resolution following stroke: an immunohistochemical and quantitative planimetric study. Brain Res. Bull. 31, 565-572.
16. CLARK, R., LEE, E., WHITE, R., JONAK, Z., FEUERSTEIN, G., and BARONE, F. (1994a). Reperfusion following focal stroke hastens inflammation and resolution of ischemic injured tissue. Brain Res. Bull. 35, 387-392.
17. CLARK, R.S., SCHIDING, J.K., KACZOROWSKI, S.L., MARION, D.W., and KOCHANEK, P.M. (1994b). Neutrophil accumulation after traumatic brain injury in rats: comparison of weight drop and controlled cortical impact models. J. Neurotrauma 11, 499-506.
18. CLEMEDSON, C.J., FALCONER, B., FRANKENBERG, L., JONSSON, A., and WENNERSTRAND, J. (1973). Head injuries caused by small-calibre, high velocity bullets. An experimental study. Z. Rechtsmed. 73, 103-114.
19. COLICOS, M.A., DIXON, C.E., and DASH, P.K. (1996). Delayed, selective neuronal death following experimental cortical impact injury in rats: possible role in memory deficits. Brain Res. 739, 111-119.
20. CONTI, A.C., RAGHUPATHI, R., TROJANOWSKI, J.Q., and McINTOSH, T.K. (1998). Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post-traumatic period. J. Neurosci. 18, 5663-5672.
21. CROCKARD, H.A., BROWN, F.D., JOHNS, L.M., and MULLAN, S. (1977). An experimental cerebral missile injury model in primates. J. Neurosurg. 46, 776-783.
22. DIXON, C.E., LIGHTHALL, J.W., and ANDERSON, T.E. (1988). Physiologic, histopathologic, and cineradiographic characterization of a new fluid-percussion model of experimental brain injury in the rat. J. Neurotrauma 5, 91-104.
23. DREIER, J.P., EBERT, N., PRILLER, J., et al. (2000). Products of hemolysis in the subarachnoid space inducing spreading ischemia in the cortex and focal necrosis in rats: a model for delayed ischemic neurological deficits after subarachnoid hemorrhage? J. Neurosurg. 93, 658-666.
24. EMERICH, D., DEAN, R., and BARTUS, R. (2002). The role of leukocytes following cerebral ischemia: pathogenic variable or bystander reaction to emerging infarct? Exp. Neurol. 173, 168-181.
25. FREYTAG, E. (1963). Autopsy findings in head injuries from firearms. Statistical evaluation of 254 cases. Arch. Pathol. 76, 215-225.
26. FUJITA, T., YOSHIMINE, T., MARUNO, M., and HAYAKAWA, T. (1998). Cellular dynamics of macrophages and microglial cells in reaction to stab wounds in rat cerebral cortex. Acta Neurochir. (Wien.) 140, 275-279.
27. HALLAM, T.M., FLOYD, C.L., FOLKERTS, M.M., et al. (2004). Comparison of behavioral deficits and acute neuronal degeneration in rat lateral fluid percussion and weight-drop brain injury models. J. Neurotrauma 21, 521-539.
28. HARTINGS, J., MAZZEO, A., FABRICUS, M., TORTELLA, F., and BULLOCK, M. (2005). Temperature effect of spreading depression incidence in the traumatically injured human brain. J. Neurotrauma 22, 1201.
29. HARTINGS, J.A., ROLLI, M.L., LU, X.C., and TORTELLA, F.C. (2003a). Delayed secondary phase of peri-infarct depolarizations after focal cerebral ischemia: relation to infarct growth and neuroprotection. J. Neurosci. 23, 11602-11610.
30. HARTINGS, J.A., WILLIAMS, A.J., and TORTELLA, F.C. (2003b). Occurrence of non-convulsive seizures, periodic lateralized epileptiform discharges, and rhythmic delta activity in rat focal ischemia. Exp. Neurol. 179, 139-149.
31. HOTZ, G.A., STEWART, K.J., PETRIN, D., et al. (2000). Neurobehavioural outcomes of penetrating and tangential gunshot wounds to the head. Brain Inj. 14, 649-657.
32. HSU, S.M., RAINE, L., and FANGER, H. (1981). Use of avidin-biotin- peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 29, 577-580.
33. HUANG, F.P., XI, G., KEEP, R.F., HUA, Y., NEMOIANU, A., and HOFF, J.T. (2002). Brain edema after experimental intracerebral hemorrhage: role of hemoglobin degradation products. J. Neurosurg. 96, 287-293.
34. IIZUKA, H., SAKATANI, K., and YOUNG, W. (1990). Neural damage in the rat thalamus after cortical infarcts. Stroke 21, 790-794.
35. KEANE, R.W., KRAYDIEH, S., LOTOCKI, G., ALONSO, O.F., ALDANA, P., and DIETRICH, W.D. (2001). Apoptotic and antiapoptotic mechanisms after traumatic brain injury. J. Cereb. Blood Flow Metab. 21, 1189-1198.
36. KIERNAN, J. (1999) Histological & Histochemical Methods: Theory & Practice. Butterworth-Heinemann: Oxford, UK.
37. KOTWICA, Z., PERSSON, L., and THUOMAS, K.A. (1989). The effects of brain edema on intracranial pressure in focal cerebral ischemia. An experimental study in a rat using magnetic resonance imaging. Zentralbl. Neurochir. 50, 68-71.
38. KROPPENSTEDT, S.N., SCHNEIDER, G.K., THOMALE, U.W., and UNTERBERG, A.W. (1998). Protective effects of aptiganel HCl (Cerestat) following controlled cortical impact injury in the rat. J. Neurotrauma 15, 191-197.
39. LI, Y., POWERS, C., JIANG, N., and CHOPP, M. (1998). Intact, injured, necrotic and apoptotic cells after focal cerebral ischemia in the rat. J. Neurol. Sci. 156, 119-132.
40. LU, X., WILLIAMS, A., and TORTELLA, F. (2001). Quantitative electroencephalography spectral analysis and topographic mapping in a rat model of middle cerebral artery occlusion. Neuropathol. Appl. Neurobiol. 27, 481-495.
41. MARIN, R., WILLIAMS, A., HALE, S., et al. (2003). The effect of voluntary exercise exposure on histological and neurobehavioral outcomes after ischemic brain injury in the rat. Physiol. Behav. 80, 167-175.
42. MARTINS, R.S., SIQUEIRA, M.G., SANTOS, M.T., et al. (2003). Prognostic factors and treatment of penetrating gunshot wounds to the head. Surg. Neurol. 60, 98-104.
43. MATTHEWS, M.A., CAREY, M.E., SOBLOSKY, J.S., DAVIDSON, J.F., and TABOR, S.L. (1998). Focal brain injury and its effects on cerebral mantle, neurons, and fiber tracks. Brain Res. 794, 1-18.
44. MAXWELL, W.L., POVLISHOCK, J.T., and GRAHAM, D.L. (1997). A mechanistic analysis of nondisruptive axonal injury: a review. J. Neurotrauma 14, 419-440.
45. MOSHANG, E., LING, G., and GROER, J. (2003). A model of penetrating traumatic brain injury using an air inflation technique. National Technical Information Service: Springfield, VA.
46. NILSSON, P., RONNE-ENGSTROM, E., FLINK, R., UNGERSTEDT, U., CARLSON, H., and HILLERED, L. (1994). Epileptic seizure activity in the acute phase following cortical impact trauma in rat. Brain Res. 637, 227-232.
47. OKONKWO, D., and POVLISHOCK, J. (1999). An intrathecal bolus of cyclosporin A before injury preserves mitochondrial integrity and attenuates axonal disruption in traumatic brain injury. J. Cereb. Blood Flow Metab. 19, 443-451.
48. PANTONI, L., SARTI, C., and INZITARI, D. (1998). Cytokines and cell adhesion molecules in cerebral ischemia: experimental bases and therapeutic perspectives. Arterioscler. Thromb. Vasc. Biol. 18, 503-513.
49. PERSSON, L. (1976). Cellular reactions to small cerebral stab wounds in the rat frontal lobe. An ultrastructural study. Virchows. Arch. B Cell. Pathol. 22, 21-37.
50. PINTAR, F.A., KUMARESAN, S., YOGANANDAN, N., YANG, A., STEMPER, B., and GENNARELLI, T.A. (2001). Biomechanical modeling of penetrating traumatic head injuries: a finite element approach. Biomed. Sci. Instrum. 37, 429-434.
51. PRINS, M.L., LEE, S.M., CHENG, C.L., BECKER, D.P., and HOVDA, D.A. (1996). Fluid percussion brain injury in the developing and adult rat: a comparative study of mortality, morphology, intracranial pressure and mean arterial blood pressure. Brain Res. Dev. Brain Res. 95, 272-282.
52. SAPSFORD, W. (2003). Penetrating brain injury in military conflict: does it merit more research? J. R. Army Med. Corps 149, 5-14.
53. SCHMUED, L., ALBERTSON, C., and SLIKKER, W. (1997). Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res. 751, 37-46.
54. SINGLETON, R.H., ZHU, J., STONE, J.R., and POVLISHOCK, J.T. (2002). Traumatically induced axotomy adjacent to the soma does not result in acute neuronal death. J. Neurosci. 22, 791-802.
55. SMITH, W.S. (2004). Pathophysiology of focal cerebral ischemia: a therapeutic perspective. J. Vasc. Interv. Radiol. 15, S3-12.
56. SOARES, H.D., HICKS, R.R., SMITH, D., and MCINTOSH, T.K. (1995). Inflammatory leukocytic recruitment and diffuse neuronal degeneration are separate pathological processes resulting from traumatic brain injury. J. Neurosci. 15, 8223-8233.
57. STANIMIROVIC, D., and SATOH, K. (2000). Inflammatory mediators of cerebral endothelium: a role in ischemic brain inflammation. Brain Pathol. 10, 113-126.
58. SUNAMI, K., NAKAMURA, T., KUBOTA, M., et al. (1989). Spreading depression following experimental head injury in the rat. Neurol. Med. Chir. (Tokyo) 29, 975-980.
59. SUTTON, R.L., LESCAUDRON, L., and STEIN, D.G. (1993). Unilateral cortical contusion injury in the rat: vascular disruption and temporal development of cortical necrosis. J. Neurotrauma 10, 135-149.
60. VOLGAS, D.A., STANNARD, J.P., and ALONSO, J.E. (2005). Current orthopaedic treatment of ballistic injuries. Injury 36, 380-386.
61. WADA, K., ALONSO, O.F., BUSTO, R., et al. (1999). Early treatment with a novel inhibitor of lipid peroxidation (LY341122) improves histopathological outcome after moderate fluid percussion brain injury in rats. Neurosurgery 45, 601-608.
62. WADA, K., CHATZIPANTELI, K., BUSTO, R., and DIETRICH, W.D. (1998). Role of nitric oxide in traumatic brain injury in the rat. J. Neurosurg. 89, 807-818.
63. WEI, H., LU, X., WILLIAMS, A., CONNORS, R., PULCIFUR, A., TORTELLA, F., and DAVE, J. (2006). NNZ-2566 treatment inhibits inflammatory and apoptotic gene up-regulation induced by experimental penetrating ballistic brain injury. Advanced Technology Applications for Combat Casualty Care Conference, St. Petersburg, FL.
64. WILLIAMS, A., DAVE, J., PHILLIPS, J., LIN, Y., McCABE, R., and TORTELLA, F. (2000). Neuroprotective efficacy and therapeutic window of the high-affinity N-methyl-D-aspartate antagonist conantokin-G: in vitro (primary cerebellar neurons) and in vivo (rat model of transient focal brain ischemia) studies. J. Pharmacol. Exp. Ther. 294, 378-386.
65. WILLIAMS, A.J., BERTI, R., DAVE, J.R., ELLIOT, P.J., ADAMS, J., and TORTELLA, F.C. (2004a). Delayed treatment of ischemia/reperfusion brain injury: extended therapeutic window with the proteosome inhibitor MLN519. Stroke 35, 1186-1191.
66. WILLIAMS, A.J., HALE, S.L., MOFFETT, J.R., et al. (2003). Delayed treatment with MLN519 reduces infarction and associated neurologic deficit caused by focal ischemic brain injury in rats via antiinflammatory mechanisms involving nuclear factor-kappaB activation, gliosis, and leukocyte infiltration. J. Cereb. Blood Flow Metab. 23, 75-87.
67. WILLIAMS, A.J., HARTINGS, J.A., LU, X.C., ROLLI, M.L., DAVE, J.R., and TORTELLA, F.C. (2005). Characterization of a new rat model of penetrating ballistic brain injury. J. Neurotrauma 22, 313-331.
68. WILLIAMS, A.J., TORTELLA, F.C., LU, X.C., MORETON, J.E., and HARTINGS, J.A. (2004b). Anti-epileptic drug treatment of non-convulsive seizures induced by experimental focal brain ischemia. J. Pharmacol. Exp. Ther. 311, 220-227.
69. WOLF, J.A., STYS, P.K., LUSARDI, T., MEANEY, D., and SMITH, D.H. (2001). Traumatic axonal injury induces calcium influx modulated by tetrodotoxin- sensitive sodium channels. J. Neurosci. 21, 1923-1930.
70. WU, J., HUA, Y., KEEP, R.F., SCHALLERT, T., HOFF, J.T., and XI, G. (2002). Oxidative brain injury from extravasated erythrocytes after intracerebral hemorrhage. Brain Res. 953, 45-52.
71. ZAFONTE, R.D., WOOD, D.L., HARRISON-FELIX, C.L., MILLIS, S.R., and VALENA, N.V. (2001). Severe penetrating head injury: a study of outcomes. Arch. Phys. Med. Rehabil. 82, 306-310.
72. ZANIER, E.R., LEE, S.M., VESPA, P.M., GIZA, C.C., and HOVDA, D.A. (2003). Increased hippocampal CA3 vulnerability to low-level kainic acid following lateral fluid percussion injury. J. Neurotrauma 20, 409-420.
73. ZAUNER, A., BULLOCK, R., KUTA, A., WOODWARD, J., and YOUNG, H. (1996). Glutamate release and cerebral blood flow after severe human head injury. Acta Neurochir. Suppl. (Wien.) 67, 40-44.
74. ZHANG, F., SPRAGUE, S.M., FARROKHI, F., HENRY, M.N., SON, M.G., and VOLLMER, D.G. (2002). Reversal of attenuation of cerebrovascular reactivity to hypercapnia by a nitric oxide donor after controlled cortical impact in a rat model of traumatic brain injury. J. Neurosurg. 97, 963-969.