Tightly coupled repetitive blast-induced traumatic brain injury: Development and characterization in mice

Journal of Neurotrauma

Volumn 28, Issue 10, 2011, Pages 2171-2183

  Wang, Ying ^a   Wei, Yanling ^a   Oguntayo, Samuel ^a   Wilkins, William ^a   Arun, Peethambaran ^a   Valiyaveettil, Manojkumar ^a   Song, Jian ^a   Long, Joseph B ^a   Nambiar, Madhusoodana P ^a  

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

Author keywords

blast exposure; neurobehavioral; neurobiological effects; neuropathology; traumatic brain injury

Indexed keywords

REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLAST INDUCED TRAUMATIC BRAIN INJURY; BLAST OVERPRESSURE; BRAIN CORTEX; BRAIN EDEMA; DIFFUSE AXONAL INJURY; MALE; MORTALITY; MOUSE; NERVE DEGENERATION; NEUROPATHOLOGY; NONHUMAN; PRESSURE; TRAUMATIC BRAIN INJURY; WEIGHT REDUCTION;

ANIMALS; BLAST INJURIES; BRAIN; BRAIN CHEMISTRY; BRAIN EDEMA; BRAIN INJURIES; CEREBRAL CORTEX; COLORING AGENTS; MALE; MICE; MICE, INBRED C57BL; POSTURAL BALANCE; PRESSURE; REACTIVE OXYGEN SPECIES; RECURRENCE; SURVIVAL; WEIGHT LOSS;

EID: 80054720511     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.1990     Document Type: Article

References (92)

1. Armonda, R.A., Bell, R.S., Vo, A.H., Ling, G., DeGraba, T.J., Crandall, B., Ecklund, J., and Campbell, W.W. (2006). Wartime traumatic cerebral vasospasm: recent review of combat casualties. Neurosurgery 59, 1215-1225. (Pubitemid 44949729)
2. Bauman, R.A., Elsayed, N., Petras, J.M., and Widholm, J. (1997). Exposure to sublethal blast overpressure reduces the food intake and exercise performance of rats. Toxicology 121, 65-79. (Pubitemid 27259675)
3. Bauman, R.A., Ling, G., Tong, L., Januszkiewicz, A., Agoston, D., Delanerolle, N., Kim, Y., Ritzel, D., Bell, R., Ecklund, J., Armonda, R., Bandak, F., and Parks, S. (2009). 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.
4. Bell, M.K. (2008). Standardized model is needed to study the neurological effects of primary blast wave exposure. Mil. Med. 173, v-viii. (Pubitemid 351874244)
5. Bhattacharjee, Y. (2008). Neuroscience. Shell shock revisited: solving the puzzle of blast trauma. Science 319, 406-408. (Pubitemid 351160556)
6. Blennow, K., Jonsson, M., Andreasen, N., Rosengren, L., Wallin, A., Hellstrom, P.A., and Zetterberg, H. (2011). No neuro-chemical evidence of brain injury after blast overpressure by repeated explosions or firing heavy weapons. Acta Neurol. Scand. 123, 245-251.
7. Cantu, R.C., and Gean, A.D. (2010). Second-impact syndrome and a small subdural hematoma: an uncommon catastrophic result of repetitive head injury with a characteristic imaging appearance. J. Neurotrauma 27, 1557-1564.
8. Cernak, I. (2010). The importance of systemic response in the pathobiology of blast-induced neurotrauma. Front. Neurol. 1, 151.
9. Cernak, I., Merkle, A.C., Koliatsos, V.E., Bilik, J.M., Luong, Q.T., Mahota, T.M., Xu, L., Slack, N., Windle, D., and Ahmed, F.A. (2011). 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.
10. Cernak, I., and Noble-Haeusslein, L.J. (2010). Traumatic brain injury: an overview of pathobiology with emphasis on military populations. J. Cereb. Blood Flow Metab. 30, 255-266.
11. Cernak, I., Savic, J., Malicevic, Z., Zunic, G., Radosevic, P., Iva-novic, I., and Davidovic, L. (1996). Involvement of the central nervous system in the general response to pulmonary blast injury. J. Trauma 40, S100-S104. (Pubitemid 26089718)
12. Cernak, I., Wang, Z., Jiang, J., Bian, X., and Savic, J. (2001a). Cognitive deficits following blast injury-induced neurotrauma: possible involvement of nitric oxide. Brain Inj. 15, 593-612. (Pubitemid 32640293)
13. Cernak, I., Wang, Z., Jiang, J., Bian, X. and Savic, J. (2001b). Ultrastructural and functional characteristics of blast injury-induced neurotrauma. J. Trauma 50, 695-706. (Pubitemid 32336257)
14. Chavko, M., Koller, W.A., Prusaczyk, W.K., and McCarron, R.M. (2007). Measurement of blast wave by a miniature fiber optic pressure transducer in the rat brain. J. Neurosci. Methods 159, 277-281. (Pubitemid 44908659)
15. Chavko, M., Watanabe, T., Adeeb, S., Lankasky, J., Ahlers, S.T., and McCarron, R.M. (2011). Relationship between orientation to a blast and pressure wave propagation inside the rat brain. J. Neurosci. Methods 195, 61-66.
16. Chen, Y.C., Smith, D.H., and Meaney, D.F. (2009). In-vitro approaches for studying blast-induced traumatic brain injury. J. Neurotrauma 26, 861-876.
17. Connell, S., Ouyang, H., and Shi, R. (2010). Modeling blast induced neurotrauma in isolated spinal cord white matter. J. Med. Syst. DOI: 10.1007/s10916-010-9464-5.
18. Courtney, A.C., and Courtney, M.W. (2009). A thoracic mechanism of mild traumatic brain injury due to blast pressure waves. Med. Hypotheses 72, 76-83.
19. Courtney, M.W., and Courtney, A.C. (2010). Note: A table-top blast driven shock tube. Rev. Sci. Instrum. 81, 126103.
20. Courtney, M.W., and Courtney, A.C. (2011). Working toward exposure thresholds for blast-induced traumatic brain injury: thoracic and acceleration mechanisms. Neuroimage 54, Suppl. 1, S55-S61.
21. Cripps, N.P., Glover, M.A., and Guy, R.J. (1999). The patho-physiology of primary blast injury and its implications for treatment. Part II: The auditory structures and abdomen. J. R. Nav. Med. Serv. 85, 13-24.
22. Elder, G.A., and Cristian, A. (2009). Blast-related mild traumatic brain injury: mechanisms of injury and impact on clinical care. Mt. Sinai J. Med. 76, 111-118.
23. Elder, G.A., Mitsis, E.M., Ahlers, S.T. and Cristian, A. (2010). Blast-induced mild traumatic brain injury. Psychiatr. Clin. North Am. 33, 757-781.
24. Elsayed, N.M., and Gorbunov, N.V. (2007). Pulmonary biochemical and histological alterations after repeated low-level blast overpressure exposures. Toxicol. Sci. 95, 289-296. (Pubitemid 44942798)
25. Fabrizio, K.S., and Keltner, N.L. (2010). Traumatic brain injury in operation enduring freedom/operation iraqi freedom: a primer. Nurs. Clin. North Am. 45, 569-80, vi.
26. Fausti, S.A., Wilmington, D.J., Gallun, F.J., Myers, P.J., and Henry, J.A. (2009). Auditory and vestibular dysfunction associated with blast-related traumatic brain injury. J. Rehabil. Res. Dev. 46, 797-810.
27. French, L.M. (2010). Military traumatic brain injury: an examination of important differences. Ann. N.Y. Acad. Sci. 1208, 38-45.
28. Garman, R.H., Jenkins, L.W., Switzer Iii, R.C., Bauman, R.A., Tong, L.C., Swauger, P.V., Parks, S., Ritzel, D.V., Dixon, C.E., Clark, R., Bayir, H., Kagan, V., Jackson, E., and Kochanek, P.M. (2011). Blast exposure in rats with body shielding is characterized by diffuse axonal injury. J. Neurotrauma 28, 947-959.
29. Garth, R.J. (1994). Blast injury of the auditory system: a review of the mechanisms and pathology. J. Laryngol. Otol. 108, 925-929. (Pubitemid 24350767)
30. Gorbunov, N.V., Elsayed, N.M., Kisin, E.R., Kozlov, A.V., and Kagan, V.E. (1997). Air blast-induced pulmonary oxidative stress: interplay among hemoglobin, antioxidants, and lipid peroxidation. Am. J. Physiol 272, L320-L334.
31. Guy, R.J., Glover, M.A., and Cripps, N.P. (1998). The patho-physiology of primary blast injury and its implications for treatment. Part I: The thorax. J. R. Nav. Med. Serv. 84, 79-86.
32. Hoane, M.R., Kaplan, S.A., and Ellis, A.L. (2006). The effects of nicotinamide on apoptosis and blood-brain barrier breakdown following traumatic brain injury. Brain Res. 1125, 185-193. (Pubitemid 44848321)
33. Hoge, C.W., McGurk, D., Thomas, J.L., Cox, A.L., Engel, C.C., and Castro, C.A. (2008). Mild traumatic brain injury in U.S. Soldiers returning from Iraq. N. Engl. J. Med. 358, 453-463. (Pubitemid 351185801)
34. Jones, E., Fear, N.T., and Wessely, S. (2007). Shell shock and mild traumatic brain injury: a historical review. Am. J. Psychiatry 164, 1641-1645. (Pubitemid 350205337)
35. Kato, K., Fujimura, M., Nakagawa, A., Saito, A., Ohki, T., Ta-kayama, K., and Tominaga, T. (2007). Pressure-dependent effect of shock waves on rat brain: induction of neuronal apoptosis mediated by a caspase-dependent pathway. J. Neurosurg. 106, 667-676. (Pubitemid 46536465)
36. Kennedy, J.E., Leal, F.O., Lewis, J.D., Cullen, M.A., and Amador, R.R. (2010). Posttraumatic stress symptoms in OIF/OEF service members with blast-related and non-blast-related mild TBI. NeuroRehabilitation 26, 223-231.
37. Khil'ko, V.A., Gofman, V.R., Grechko, A.T., Glaznikov, L.A., and Shulev, I. (1997). [The early diagnosis of the severity of blast trauma to the brain and auditory system]. Zh. Vopr. Neirokhir. Im N. N. Burdenko 3, 35-37.
38. Kocsis, J.D., and Tessler, A. (2009). Pathology of blast-related brain injury. J. Rehabil. Res. Dev. 46, 667-672.
39. Koliatsos, V.E., Cernak, I., Xu, L., Song, Y., Savonenko, A., Crain, B.J., Eberhart, C.G., Frangakis, C.E., Melnikova, T., Kim, H., and Lee, D. (2011). A mouse model of blast injury to brain: initial pathological, neuropathological, and behavioral characterization. J. Neuropathol. Exp. Neurol. 70, 399-416.
40. Leibovici, D., Gofrit, O.N., Stein, M., Shapira, S.C., Noga, Y., Heruti, R.J., and Shemer, J. (1996). Blast injuries: bus versus open-air bombings-a comparative study of injuries in survivors of open-air versus confined-space explosions. J. Trauma 41, 1030-1035. (Pubitemid 26424899)
41. Leonardi, A.D., Bir, C.A., Ritzel, D.V., and VandeVord, P.J. (2011a). Intracranial pressure increases during exposure to a shock wave. J. Neurotrauma 28, 85-94.
42. Leonardi, A.D., Bir, C.A., Ritzel, D.V., and VandeVord, P.J. (2011b). Intracranial pressure increases during exposure to a shock wave. J. Neurotrauma 28, 85-94.
43. Lew, H.L., Garvert, D.W., Pogoda, T.K., Hsu, P.T., Devine, J.M., White, D.K., Myers, P.J., and Goodrich, G.L. (2009). Auditory and visual impairments in patients with blast-related traumatic brain injury: Effect of dual sensory impairment on Functional Independence Measure. J. Rehabil. Res. Dev. 46, 819-826.
44. Ling, G., Bandak, F., Armonda, R., Grant, G., and Ecklund, J. (2009). Explosive blast neurotrauma. J. Neurotrauma 26, 815-825.
45. Ling, G.S. and Ecklund, J.M. (2011). Traumatic brain injury in modern war. Curr. Opin. Anaesthesiol. 24, 124-130.
46. Long, J.B., Bentley, T.L., Wessner, K.A., Cerone, C., Sweeney, S., and Bauman, R.A. (2009). Blast overpressure in rats: recreating a battlefield injury in the laboratory. J. Neurotrauma 26, 827-840.
47. Matthews, S., Simmons, A., and Strigo, I. (2011a). The effects of loss versus alteration of consciousness on inhibition-related brain activity among individuals with a history of blast-related concussion. Psychiatry Res. 191, 76-79.
48. Matthews, S.C., Strigo, I.A., Simmons, A.N., O'Connell, R.M., Reinhardt, L.E., and Moseley, S.A. (2011b). A multimodal imaging study in U.S. veterans of Operations Iraqi and Enduring Freedom with and without major depression after blast-related concussion. Neuroimage 54, Suppl. 1, S69-S75.
49. Mazurkiewicz-Kwilecki, I.M. (1980). Single and repeated air blast stress and brain histamine. Pharmacol. Biochem. Behav. 12, 35-39. (Pubitemid 10155081)
50. McKee, A.C., Cantu, R.C., Nowinski, C.J., Hedley-Whyte, E.T., Gavett, B.E., Budson, A.E., Santini, V.E., Lee, H.S., Kubilus, C.A., and Stern, R.A. (2009). Chronic traumatic encephalopa-thy in athletes: progressive tauopathy after repetitive head injury. J. Neuropathol. Exp. Neurol. 68, 709-735.
51. Mellor, S.G. (1988). The pathogenesis of blast injury and its management. Br. J. Hosp. Med. 39, 536-539.
52. Mori, T., Katayama, Y., and Kawamata, T. (2006). Acute hemispheric swelling associated with thin subdural hematomas: pathophysiology of repetitive head injury in sports. Acta Neurochir. Suppl 96, 40-43.
53. Nakagawa, A., Fujimura, M., Kato, K., Okuyama, H., Hashimoto, T., Takayama, K., and Tominaga, T. (2008). Shock wave-induced brain injury in rat: novel traumatic brain injury animal model. Acta Neurochir. Suppl. 102, 421-424.
54. Nakagawa, A., Manley, G.T., Gean, A., Ohtani, K., Armonda, R., Tsukamoto, A., Yamamoto, H., Takayama, K., and Tominaga, T. (2011). Mechanisms of primary blast-induced traumatic brain injury: Insights from shock wave research. J. Neuro-trauma 28, 1101-1119.
55. Okie, S. (2005). Traumatic brain injury in the war zone. N. Engl. J. Med. 352, 2043-2047. (Pubitemid 40664304)
56. Owen-Smith, M. (1982). Wound care No. 13. The traumatic wounds of warfare. Nurs. Times 78, Suppl. 52, 49-52.
57. Park, E., Gottlieb, J.J., Cheung, B., Shek, P.N., and Baker, A.J. (2011). A model of low-level primary blast brain trauma results in cytoskeletal proteolysis and chronic functional impairment in the absence of lung barotrauma. J. Neurotrauma 28, 343-357.
58. Peskind, E.R., Petrie, E.C., Cross, D.J., Pagulayan, K., McCraw, K., Hoff, D., Hart, K., Yu, C.E., Raskind, M.A., Cook, D.G., and Minoshima, S. (2011). Cerebrocerebellar hypometabolism associated with repetitive blast exposure mild traumatic brain injury in 12 Iraq war Veterans with persistent post-concussive symptoms. Neuroimage 54, Suppl. 1, S76-S82.
59. Pratt, H., Goldsher, M., Netzer, A., and Shenhav, R. (1985). Auditory brainstem evoked potentials in blast injury. Audiology 24, 297-304. (Pubitemid 15045432)
60. Pun, P.B., Kan, E.M., Salim, A., Li, Z., Ng, K.C., Moochhala, S.M., Ling, E.A., Tan, M.H., and Lu, J. (2011). Low level primary blast injury in rodent brain. Front. Neurol. 2, 19.
61. Readnower, R.D., Chavko, M., Adeeb, S., Conroy, M.D., Pauly, J.R., McCarron, R.M., and Sullivan, P.G. (2010). Increase in blood-brain barrier permeability, oxidative stress, and activated microglia in a rat model of blast-induced traumatic brain injury. J. Neurosci. Res. 88, 3530-3539.
62. Richmond, D.R. (1991). Blast criteria for open spaces and enclosures. Scand. Audiol. Suppl 34, 49-76.
63. Risdall, J.E., and Menon, D.K. (2011). Traumatic brain injury. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 241-250.
64. Ritenour, A.E., and Baskin, T.W. (2008). Primary blast injury: update on diagnosis and treatment. Crit. Care Med. 36, S311-S317.
65. Roberto, M., Hamernik, R.P., and Turrentine, G.A. (1989). Damage of the auditory system associated with acute blast trauma. Ann. Otol. Rhinol. Laryngol. Suppl. 140, 23-34. (Pubitemid 19133157)
66. Saljo, A., Arrhen, F., Bolouri, H., Mayorga, M., and Hamberger, A. (2008). Neuropathology and pressure in the pig brain resulting from low-impulse noise exposure. J.Neurotrauma 25, 1397-1406.
67. Saljo, A., Bao, F., Haglid, K.G., and Hansson, H.A. (2000). Blast exposure causes redistribution of phosphorylated neurofila-ment subunits in neurons of the adult rat brain. J.Neuro-trauma 17, 719-726.
68. Saljo, A., Bao, F., Hamberger, A., Haglid, K.G., Hansson, H.A. (2001). Exposure to short-lasting impulse noise causes micro-glial and astroglial cell activation in the adult rat brain. Pa-thophysiology 8, 105-111. (Pubitemid 33108987)
69. Saljo, A., Bao, F., Jingshan, S., Hamberger, A., Hansson, H.A., and Haglid, K.G. (2002a). Exposure to short-lasting impulse noise causes neuronal c-Jun expression and induction of ap-optosis in the adult rat brain. J. Neurotrauma 19, 985-991.
70. Saljo, A., Bao, F., Shi, J., Hamberger, A., Hansson, H.A., and Haglid, K.G. (2002b). Expression of c-Fos and c-Myc and deposition of beta-APP in neurons in the adult rat brain as a result of exposure to short-lasting impulse noise. J. Neuro-trauma 19, 379-385. (Pubitemid 34246124)
71. Saljo, A., Bolouri, H., Mayorga, M., Svensson, B., and Hamber-ger, A. (2010). Low-level blast raises intracranial pressure and impairs cognitive function in rats: prophylaxis with processed cereal feed. J. Neurotrauma 27, 383-389.
72. Saljo, A., Mayorga, M., Bolouri, H., Svensson, B., and Hamber-ger, A. (2011). Mechanisms and pathophysiology of the low-level blast brain injury in animal models. Neuroimage 54, Suppl. 1, S83-S88.
73. Saljo, A., Svensson, B., Mayorga, M., Hamberger, A., and Bolouri, H. (2009). Low levels of blast raises intracranial pressure and impairs cognitive function in rats. J. Neuro-trauma 26, 1345-1352.
74. Saunders, L.L., Selassie, A.W., Hill, E.G., Nicholas, J.S., Horner, M.D., Corrigan, J.D., and Lackland, D.T. (2009). A population-based study of repetitive traumatic brain injury among persons with traumatic brain injury. Brain Inj. 23, 866-872.
75. Sayer, N.A., Chiros, C.E., Sigford, B., Scott, S., Clothier, B., Pickett, T., and Lew, H.L. (2008). Characteristics and rehabilitation outcomes among patients with blast and other injuries sustained during the Global War on Terror. Arch. Phys. Med. Rehabil. 89, 163-170. (Pubitemid 350298990)
76. Schoettle, R.J., Kochanek, P.M., Magargee, M.J., Uhl, M.W., and Nemoto, E.M. (1990). Early polymorphonuclear leukocyte accumulation correlates with the development of posttrau-matic cerebral edema in rats. J. Neurotrauma 7, 207-217.
77. Scott, S.G., Belanger, H.G., Vanderploeg, R.D., Massengale, J., and Scholten, J. (2006). Mechanism-of-injury approach to evaluating patients with blast-related polytrauma. J. Am. Osteopath. Assoc. 106, 265-270. (Pubitemid 43765314)
78. Shitaka, Y., Tran, H.T., Bennett, R.E., Sanchez, L., Levy, M.A., Dikranian, K., and Brody, D.L. (2011). Repetitive closed-skull traumatic brain injury in mice causes persistent multifocal axonal injury and microglial reactivity. J. Neuropathol. Exp. Neurol. 70, 551-567.
79. Snell, F.I., and Halter, M.J. (2010). A signature wound of war: mild traumatic brain injury. J. Psychosoc. Nurs. Ment. Health Serv. 48, 22-28.
80. Suneson, A., Hansson, H.A., and Seeman, T. (1990). Pressure wave injuries to the nervous system caused by high-energy missile extremity impact: Part II. Distant effects on the central nervous system-a light and electron microscopic study on pigs. J. Trauma 30, 295-306. (Pubitemid 20117369)
81. Svetlov, S.I., Prima, V., Kirk, D.R., Gutierrez, H., Curley, K.C., Hayes, R.L., and Wang, K.K. (2010). Morphologic and Biochemical Characterization of Brain Injury in a Model of Controlled Blast Overpressure Exposure. J. Trauma 69, 795-804.
82. Terrio, H., Brenner, L.A., Ivins, B.J., Cho, J.M., Helmick, K., Schwab, K., Scally, K., Bretthauer, R., and Warden, D. (2009). Traumatic brain injury screening: preliminary findings in a US Army Brigade Combat Team. J. Head Trauma Rehabil. 24, 14-23.
83. Unterberg, A.W., Stover, J., Kress, B., and Kiening, K.L. (2004). Edema and brain trauma. Neuroscience 129, 1021-1029. (Pubitemid 39556253)
84. Vink, R., Young, A., Bennett, C.J., Hu, X., Connor, C.O., Cernak, I., and Nimmo, A.J. (2003). Neuropeptide release influences brain edema formation after diffuse traumatic brain injury. Acta Neurochir. Suppl. 86, 257-260.
85. Wang, H., and Joseph, J.A. (1999a). Quantifying cellular oxida-tive stress by dichlorofluorescein assay using microplate reader. Free Radic. Biol. Med. 27, 612-616. (Pubitemid 29408648)
86. Wang, H., and Joseph, J.A. (1999b). Quantifying cellular oxida-tive stress by dichlorofluorescein assay using microplate reader. Free Radic. Biol. Med. 27, 612-616. (Pubitemid 29408648)
87. Warden, D. (2006). Military TBI during the Iraq and Afghanistan wars. J. Head Trauma Rehabil. 21, 398-402. (Pubitemid 44413113)
88. Wilk, J.E., Thomas, J.L., McGurk, D.M., Riviere, L.A., Castro, C.A., and Hoge, C.W. (2010). Mild traumatic brain injury (concussion) during combat: lack of association of blast mechanism with persistent postconcussive symptoms. J. Head Trauma Rehabil. 25, 9-14.
89. Wolf, S.J., Bebarta, V.S., Bonnett, C.J., Pons, P.T., and Cantrill, S.V. (2009). Blast injuries. Lancet 374, 405-415.
90. Xydakis, M.S., Robbins, A.S., and Grant, G.A. (2008). Mild traumatic brain injury in U.S. soldiers returning from Iraq. N. Engl. J. Med. 358, 2177. (Pubitemid 351679609)
91. Yang, Z., Wang, Z., Tang, C., and Ying, Y. (1996). Biological effects of weak blast waves and safety limits for internal organ injury in the human body. J. Trauma 40, S81-S84. (Pubitemid 26089714)
92. Ylikoski, M.E., and Ylikoski, J.S. (1994). Hearing loss and handicap of professional soldiers exposed to gunfire noise. Scand. J. Work Environ. Health 20, 93-100. (Pubitemid 24146936)