A mouse model of blast-induced mild traumatic brain injury

Experimental Neurology

Volumn 232, Issue 2, 2011, Pages 280-289

  Rubovitch, Vardit ^a   Ten Bosch, Meital ^a   Zohar, Ofer ^b   Harrison, Catherine R ^c   Tempel Brami, Catherine ^a   Stein, Elliot ^d   Hoffer, Barry J ^d   Balaban, Carey D ^e   Schreiber, Shaul ^a   Chiu, Wen Ta ^f   Pick, Chaim G ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AIR FORCE RESEARCH LABORATORY   (United States)

^d NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^e University of Pittsburgh School of Medicine   (United States)

^f TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Behavior; Low level blast induced brain injury; MRI

Indexed keywords

CHEMOKINE RECEPTOR CCR3; MANGANESE SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLAST INJURY; BLOOD BRAIN BARRIER; COGNITION; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; DIFFUSION WEIGHTED IMAGING; DISEASE SEVERITY; EXPLOSION; FRACTIONAL ANISOTROPY; MALE; MAZE TEST; MOUSE; NEUROPROTECTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OBJECT RELATION; OPEN FIELD TEST; PRIORITY JOURNAL; RECOGNITION; TRAUMATIC BRAIN INJURY;

ANIMALS; BLAST INJURIES; BRAIN; BRAIN INJURIES; DIFFUSION TENSOR IMAGING; DISEASE MODELS, ANIMAL; EXPLOSIONS; MALE; MAZE LEARNING; MICE; MICE, INBRED ICR; MILD COGNITIVE IMPAIRMENT; MOTOR ACTIVITY; RECOGNITION (PSYCHOLOGY); RECOVERY OF FUNCTION; TRAUMA SEVERITY INDICES;

EID: 80055006041     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.09.018     Document Type: Article

References (69)

1. Aggleton J.P., Keen S., Warburton E.C., Bussey T.J. Extensive cytotoxic lesions involving both the rhinal cortices and area TE impair recognition but spare spatial alternation in the rat. Brain Res. Bull. 1997, 43:279-287.
2. Andreasen N.C. Acute and delayed posttraumatic stress disorders: a history and some issues. Am. J. Psychiatry 2004, 161:1321-1323.
3. Arciniegas D., et al. Attention and memory dysfunction after traumatic brain injury: cholinergic mechanisms, sensory gating, and a hypothesis for further investigation. Brain Inj. 1999, 13:1-13.
4. Basser P.J., Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. 1996, 111:209-219.
5. Bazarian J.J., Zhong J., Blyth B., et al. Diffusion tensor imaging detects clinically important axonal damage after mild traumatic brain injury: a pilot study. J. Neurotrauma 2007, 24:1447-1459.
6. Beaumont A., Marmarou A., Hayasaki K., et al. The permissive nature of blood brain barrier (BBB) opening in edema formation following traumatic brain injury. Acta Neurochir. 2000, 76:125-129.
7. Bidmon H.J., Kato K., Schleicher A., Witte O.W., Zilles K. Transient changes in the presence of nitric oxide synthases and nitrotyrosine immunoreactivity after focal cortical lesions. Stroke 1998, 29(1):203-210.
8. Bigler E.D. Neuropsychology and clinical neuroscience of persistent post-concussive syndrome. J. Int. Neuropsychol. Soc. 2008, 14:1-22.
9. Brenner L.A., Vanderploeg R.D., Terrio H. Assessment and diagnosis of mild traumatic brain injury, posttraumatic stress disorder, and other polytrauma conditions: burden of adversity hypothesis. Rehabil. Psychol. 2009, 54:239-246.
10. Cernak I., Noble-Haeusslein L.J. Traumatic brain injury: an overview of pathobiology with emphasis on military populations. J. Cereb. Blood Flow Metab. 2010, 30:255-266.
11. Cheng J., Gu J., Ma Y., et al. Development of a rat model for studying blast induced traumatic brain injury. J. Neurol. Sci. 2010, 294:23-28.
12. Chu Z., Wilde E.A., Hunter J.V., et al. Voxel-based analysis of diffusion tensor imaging in mild traumatic brain injury in adolescents. AJNR 2010, 31:340-346.
13. Coleman M.P., Perry V.H. Axon pathology in neurological disease: a neglected therapeutic target. Trends Neurosci. 2002, 25:53.
14. Conrad C.D., Galea L.A., Kuroda Y., McEwen B.S. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 1996, 110:1321-1334.
15. Courtney A.C., Courtney M.W. A thoracic mechanism of mild traumatic brain injury due to blast pressure waves. Med. Hypotheses 2009, 72:76-83.
16. Crabtree J. Terrorist homicide bombings: a primer for preparation. J. Burn Care Res. 2006, 27:576-588.
17. de Vries H.E., Kuiper J., de Boer A.G., et al. The blood-brain barrier in neuroinflammatory diseases. Pharmacol. Rev. 1997, 49:143-155.
18. DeKosky S.T., Ikonomovic M.D., Gandy S. Traumatic brain injury - football, warfare, and long-term effects. N. Engl. J. Med. 2010, 363:14.
19. Dellu F., Mayo W., Cherkaoui J., Le Moal M., Simon H. A two-trial memory task with automated recording: study in young and aged rats. Brain Res. 1992, 588:132-139.
20. Dolberg O.T., Barkai G., Leor A., et al. Injured civilian survivors of suicide bomb attacks: from partial PTSD to recovery or to traumatisation. Where is the turning point?. World J. Biol. Psychiatry 2007, 1-8.
21. Elder G.A., Cristian A. Blast-related mild traumatic brain injury: mechanisms of injury and impact on clinical care. Mt. Sinai J. Med. 2009, 76:111-118.
22. Finset A., et al. Cognitive performance in multiple trauma patients 3years after injury. Psychosom. Med. 1999, 61:576-583.
23. Hoffer M.E., Donaldson C., Gottshall K.R., Balaban C.D., Balough B.J. Blunt and blast trauma: different entities. Int. Tinnitus J. 2009, 15:115-118.
24. Hoffer M.E., Balaban C., Gottshall K.R., et al. Blast exposure: vestibular consequences and associated characteristics. Otol. Neurotol. 2010, 31:232-236.
25. Hoge C.W., Goldberg H.M., Castro C.A. Care of war veterans with mild traumatic brain injury-flawed perspectives. N. Engl. J. Med. 2009, 360:1588-1591.
26. Jiang Y., Johnson G.A. Microscopic diffusion tensor imaging of the mouse brain. Neuroimage 2010, 50:465-471.
27. Jiang Q., Zhang Z.G., Ding G.L., et al. MRI detects white matter reorganization after neural progenitor cell treatment of stroke. Neuroimage 2006, 32:1080-1089.
28. Kibby M.Y., Long C.J. Minor head injury: attempts at clarifying the confusion. Brain Inj. 1996, 10:159-186.
29. Knake S., Belke M., Menzler K., et al. In vivo demonstration of microstructural brain pathology in progressive supranuclear palsy: a DTI study using TBSS. Mov. Disord. 2010, 25:1232-1238.
30. Lacotte S., Brun S., Muller S., et al. CXCR3, inflammation and autoimmune diseases. Contemporary challenges in autoimmunity. Ann. N. Y. Acad. Sci. 2009, 1173:310-317.
31. Levin H.S., et al. Neurobehavioral outcome following minor head injury: a three-center study. J. Neurosurg. 1987, 66:234-243.
32. Levin H.S., Wilde E., Troyanskaya M., et al. Diffusion tensor imaging of mild to moderate blast-related traumatic brain injury and its sequelae. J. Neurotrauma 2010, 27:683-694.
33. Liu X.H., Kato H., Nakata N., Kogure K., Kato K. An immunohistochemical study of copper/zinc superoxide dismutase and manganese superoxide dismutase in rat hippocampus after transient cerebral ischemia. Brain. Res. 1993, 625(1):29-37.
34. Long J.B., Bentley T.L., Wessner K.A., Cerone C., Sweeney S., Bauman R.A. Blast overpressure in rats: recreating a battlefield injury in the laboratory. J. Neurotrauma 2009, 26(6):827-840.
35. MacDonald C.L., Johnson A.M., Cooper D., Nelson E.C., Werner N.J., Shimony J.S., Snyder A.Z., Raichle M.E., Witherow J.R., Fang R., Flaherty S.F., Brody D.L. Detection of blast related traumatic brain injury in U.S. military personnel. N. Engl. J. Med. 2011, 364:2091-2100.
36. Margulies S. The postconcussion syndrome after mild head trauma: is brain damage over diagnosed?. J. Clin. Neurosci. 2002, 7:400-408.
37. McTighe Stephanie M., Cowell Rosemary A., Winters Boyer D., et al. Paradoxical false memory for objects after brain damage. Science 2010, 330:1408-1410.
38. Mekel M., Bumenfeld A., Feigenberg Z., et al. Terrorist suicide bombings: lessons learned in Metropolitan Haifa from September 2000 to January 2006. Am. J. Disaster Med. 2009, 4:233-248.
39. Messier C. Object recognition in mice: improvement of memory by glucose. Neurobiol. Learn. Mem. 1997, 67:172-175.
40. Mintz Y., Shapira S.C., Pikarsky A.J., et al. The experience of one institution dealing with terror: the El Aqsa Intifada riots. Isr. Med. Assoc. J. 2002, 4:554-556.
41. Mori S., Zhang J., Bulte J.W. Magnetic resonance microscopy of mouse brain development. Methods Mol. Med. 2006, 124:129-147.
42. Moss W.C., King M.J., Blackman E.G. Skull flexure from blast waves: a mechanism for brain injury with implications for helmet design. Phys. Rev. Lett. 2009, 103:108702.
43. Omari K.M., John G.R., Sealfon S.C., et al. CXC chemokine receptors on human oligodendrocytes: implications for multiple sclerosis. Brain 2005, 128:1003-1015.
44. Pietrzak R.H., Johnson D.C., Goldstein M.B., et al. Posttraumatic stress disorder mediates the relationship between mild traumatic brain injury and health and psychosocial functioning in veterans of Operations Enduring Freedom and Iraqi Freedom. J. Nerv. Ment. Dis. 2009, 197:748-753.
45. Ratiu P., Talos I.F., Haker S., et al. The tale of Phineas Gage, digitally remastered. J. Neurotrauma 2004, 21:637-643.
46. Rotondi M., Chiovato L., Romagnani S., Serio M., Romagnani P. Role of chemokines in endocrine autoimmune diseases. Endocr. Rev. 2007, 28:492-520.
47. Ruff R. Two decades of advances in understanding of mild traumatic brain injury. J. Head Trauma Rehabil. 2005, 20:5-18.
48. Ryan L.M., Warden D.L. Post concussion syndrome. Int. Rev. Psychiatry 2003, 15:310-316.
49. Saha R.N., Pahan K. Differential regulation of Mn-superoxide dismutase in neurons and astroglia by HIV-1 gp120: implications for HIV-associated dementia. Free Radic. Biol. Med. 2007, 42:1866-1878.
50. Saljo A., Bao F., Haglid K.G., Hansson H.A. Blast exposure causes a redistribution of phosphorylated neurofilament subunits in neurons of the adult rat brain. J. Neurotrauma 2000, 17:719-726.
51. Saljo A., Bao F., Hamberger A., Haglid K.G., Hansson H.A. Exposure to short-lasting impulse noise causes microglial and astroglial cell activation in the adult rat brain. Pathophysiology 2001, 8:105-111.
52. Saljo A., Bao F., Shi J., Hamberger A., Hansson H.A., Haglid K.G. 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. Neurotrauma 2002, 19:379-385.
53. Saljo A., Jingshan S., Hamberger A., Hansson H.A., Haglid K.G. Exposure to short-lasting impulse noise causes neuronal c-Jun expression and induction of apoptosis in the adult rat brain. J. Neurotrauma 2002, 19:985-991.
54. Saljo A., Huang Y.L., Hansson H.A. Impulse noise transiently increased the permeability of nerve and glial cell membranes, an effect accentuated by a recent brain injury. J. Neurotrauma 2003, 20:787-794.
55. Saljo A., Arrhen F., Bolouri H., Mayorga M., Hamberger A. Neuropathology and pressure in the pig brain resulting from low-impulse noise exposure. J. Neurotrauma 2008, 25:1397-1406.
56. Saljo A., Svensson B., Mayorga M., Hamberger A., Bolouri H. Low-level blasts raise intracranial pressure and impair cognitive function in rats. J. Neurotrauma 2009, 26:1345-1352.
57. Schnaar R.L. Brain gangliosides in axon-myelin stability and axon regeneration. FEBS Lett. 2010, 584:1741-1747.
58. Schreiber S., Dolberg O.T., Barkai, et al. Primary intervention for memory structuring and meaning acquisition (PIMSMA): study of a mental health first-aid intervention in the ED with injured survivors of suicide bombing attacks. Am. J. Disaster Med. 2007, 2:307-320.
59. Simiand J., Keane P.E., Morre M. The staircase test in mice: a simple and efficient procedure for primary screening of anxiolytic agents. Psychopharmacology 1984, 84:48-53.
60. Song S.K., Sun S.W., Ramsbottom M.J., et al. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 2002, 17:1429-1436.
61. Sponheim S.R., McGuire K.A., Kang S.S., et al. Evidence of disrupted functional connectivity in the brain after combat-related blast injury. Neuroimage 2011, 54:S21-S29.
62. Sterr A., Herron K.A., Hayward C., Montaldi D. Are mild head injuries as mild as we think? Neurobehavioral concomitants of chronic post-concussion syndrome. BMC Neurol. 2006, 6:7.
63. Tashlykov V., Katz Y., Gazit, et al. Apoptotic changes in the cortex and hippocampus following minimal brain trauma in mice. Brain Res. 2007, 1130:197-205.
64. Tashlykov V., Katz Y., Volkov A., et al. Minimal traumatic brain injury induce apoptotic cell death in mice. J. Mol. Neurosci. 2009, 37:16-24.
65. Thompson J.M., Scott K.C., Dubinsky L. Battlefield brain: unexplained symptoms and blast-related mild traumatic brain injury. Can. Fam. Physician 2008, 54:1549-1551.
66. Vajtr D., Benada O., Kukacka J., et al. Correlation of ultrastructural changes of endothelial cells and astrocytes occurring during blood brain barrier damage after traumatic brain injury with biochemical markers of BBB leakage and inflammatory response. Physiol. Res. 2009, 58:263-268.
67. Vyas A.A., Patel H.V., Fromholt S.E., et al. Gangliosides are functional nerve cell ligands for myelin-associated glycoprotein (MAG), an inhibitor of nerve regeneration. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:8412-8417.
68. Wilde E.A., McCauley S.R., Hunter J.V., et al. Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology 2008, 70:948-955.
69. Zohar O., Schreiber S., Getslev V., et al. Closed-head minimal traumatic brain injury produces long-term cognitive deficits in mice. Neuroscience 2003, 118:949-955.