Computational analysis reveals increased blood deposition following repeated mild traumatic brain injury

NeuroImage: Clinical

Volumn 1, Issue 1, 2012, Pages 18-28

  Donovan, Virginia ^a,b   Bianchi, Anthony ^a   Hartman, Richard ^c   Bhanu, Bir ^a   Carson, Monica J ^a,b   Obenaus, Andre ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LOMA LINDA UNIVERSITY   (United States)

Author keywords

Edema; Hemorrhagic progression; Histogram; Quantitative magnetic resonance imaging; T2

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CIRCULATION; BRAIN DAMAGE; BRAIN EDEMA; BRAIN REGION; CONTROLLED STUDY; HISTOGRAM; HISTOLOGY; MALE; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL; RAT; TEMPORAL CORTEX; TRAUMATIC BRAIN INJURY;

EID: 84871977136     PISSN: None     EISSN: 22131582     Source Type: Journal    
DOI: 10.1016/j.nicl.2012.08.001     Document Type: Article

References (56)

1. Alahmadi, H., Vachhrajani, S., Cusimano, M.D., 2010. The natural history of brain contusion: an analysis of radiological and clinical progression. Journal of Neurosurgery 112, 1139-1145.
2. Belanger, H.G., Spiegel, E., Vanderploeg, R.D., 2010. Neuropsychological performance following a history of multiple self-reported concussions: a meta-analysis. Journal of International Neuropsychological Society 16, 262-267.
3. Belayev, L., Obenaus, A., Zhao, W., Saul, I., Busto, R.,Wu, C., Vigdorchik, A., Lin, B., Ginsberg, M.D., 2007. Experimental intracerebral hematoma in the rat: characterization by sequential magnetic resonance imaging, behavior, and histopathology. Effect of albumin therapy. Brain Research 1157, 146-155.
4. Benson, R.R., Meda, S.A., Vasudevan, S., Kou, Z., Govindarajan, K.A., Hanks, R.A., Millis, S.R., Makki, M., Latif, Z., Coplin, W., Meythaler, J., Haacke, E.M., 2007. Global white matter analysis of diffusion tensor images is predictive of injury severity in traumatic brain injury. Journal of Neurotrauma 24, 446-459.
5. Boje, K.M., Arora, P.K., 1992. Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Research 587, 250-256.
6. Chang, E.F.,Meeker,M., Holland,M.C., 2006. Acute traumatic intraparenchymal hemorrhage: risk factors for progression in the early post-injury period. Neurosurgery 58, 647-656 discussion 647-656.
7. Colgan, N.C., Cronin, M.M., Gobbo, O.L., O'Mara, S.M., O'Connor, W.T., Gilchrist, M.D., 2010. Quantitative MRI analysis of brain volume changes due to controlled cortical impact. Journal of Neurotrauma 27, 1265-1274.
8. Corrigan, J.D., Selassie, A.W., Orman, J.A., 2010. The epidemiology of traumatic brain injury. The Journal of Head Trauma Rehabilitation 25, 72-80.
9. DeFord, S.M., Wilson, M.S., Rice, A.C., Clausen, T., Rice, L.K., Barabnova, A., Bullock, R., Hamm, R.J., 2002. Repeated mild brain injuries result in cognitive impairment in B6C3F1 mice. Journal of Neurotrauma 19, 427-438.
10. Del Zoppo, G.J., Frankowski, H., Gu, Y.H., Osada, T., Kanazawa, M., Milner, R., Wang, X., Hosomi, N., Mabuchi, T., Koziol, J.A., 2012. Microglial cell activation is a source of metalloproteinase generation during hemorrhagic transformation. Journal of Cerebral Blood Flow and Metabolism 32, 919-932.
11. Ding, J.Y., Kreipke, C.W., Schafer, P., Schafer, S., Speirs, S.L., Rafols, J.A., 2009. Synapse loss regulated by matrix metalloproteinases in traumatic brain injury is associated with hypoxia inducible factor-1alpha expression. Brain Research 1268, 125-134.
12. Emblem, K.E., Scheie, D., Due-Tonnessen, P., Nedregaard, B., Nome, T., Hald, J.K., Beiske, K., Meling, T.R., Bjornerud, A., 2008. Histogram analysis of MR imaging-derived cerebral blood volume maps: combined glioma grading and identification of low-grade oligodendroglial subtypes. AJNR American Journal of Neuroradiology 29, 1664-1670.
13. Faul, M., Xu, L., Wald, M.M., Coronado, V.G., 2010. Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations and Deaths. Centers for Disease Control and Prevention National Center for Injury Prevention and Control, Atlanta, GA.
14. Fukuda, S., Fini, C.A., Mabuchi, T., Koziol, J.A., Eggleston Jr., L.L., del Zoppo, G.J., 2004. Focal cerebral ischemia induces active proteases that degrade microvascular matrix. Stroke 35, 998-1004.
15. Gerzanich, V., Woo, S.K., Vennekens, R., Tsymbalyuk, O., Ivanova, S., Ivanov, A., Geng, Z., Chen, Z., Nilius, B., Flockerzi, V., Freichel, M., Simard, J.M., 2009. De novo expression of Trpm4 initiates secondary hemorrhage in spinal cord injury. Nature Medicine 15, 185-191.
16. Gidday, J.M., Gasche, Y.G., Copin, J.C., Shah, A.R., Perez, R.S., Shapiro, S.D., Chan, P.H., Park, T.S., 2005. Leukocyte-derived matrix metalloproteinase-9 mediates blood-brain barrier breakdown and is proinflammatory after transient focal cerebral ischemia. American Journal of Physiology - Heart and Circulatory Physiology 289, H558-568.
17. Gong, C., Hoff, J.T., Keep, R.F., 2000. Acute inflammatory reaction following experimental intracerebral hemorrhage in rat. Brain Research 871, 57-65.
18. Gupta, R.K., Tomar, V.,Awasthi, R., Yadav, A., Husain,N., Bharadwaj, V., Ojha, B.K., Behari, S., Prasad, K.N., Rathore, R.K., 2012. T2*-weighted MR angiography substantially increases the detection of hemorrhage in the wall of brain abscess: implications in clinical interpretation. Neuroradiology 54, 565-572.
19. Hamann, G.F., Okada, Y., Fitridge, R., del Zoppo, G.J., 1995. Microvascular basal lamina antigens disappear during cerebral ischemia and reperfusion. Stroke 26, 2120-2126.
20. Hayashi, T., Kaneko, Y., Yu, S., Bae, E., Stahl, C.E., Kawase, T., van Loveren, H., Sanberg, P.R., Borlongan, C.V., 2009. Quantitative analyses of matrix metalloproteinase activity after traumatic brain injury in adult rats. Brain Research 1280, 172-177.
21. Homsi, S., Federico, F., Croci, N., Palmier, B., Plotkine, M., Marchand-Leroux, C., Jafarian-Tehrani, M., 2009. Minocycline effects on cerebral edema: relations with inflammatory and oxidative stress markers following traumatic brain injury in mice. Brain Research 1291, 122-132.
22. Immonen, R.J., Kharatishvili, I., Grohn, H., Pitkanen, A., Grohn, O.H., 2009. Quantitative MRI predicts long-term structural and functional outcome after experimental traumatic brain injury. NeuroImage 45, 1-9.
23. Inglese, M.,Makani, S., Johnson, G., Cohen, B.A., Silver, J.A., Gonen, O., Grossman, R.I., 2005. Diffuse axonal injury inmild traumatic brain injury: a diffusion tensor imaging study. Journal of Neurosurgery 103, 298-303.
24. Irimia, A., Chambers, M.C., Alger, J.R., Filippou, M., Prastawa, M.W., Wang, B., Hovda, D.A., Gerig, G., Toga, A.W., Kikinis, R., Vespa, P.M., Van Horn, J.D., 2011. Comparison of acute and chronic traumatic brain injury using semi-automatic multimodal segmentation of MR volumes. Journal of Neurotrauma 28, 2287-2306.
25. Kane, M.J., Angoa-Perez, M., Briggs, D.I., Viano, D.C., Kreipke, C.W., Kuhn, D.M., 2012. A mousemodel of human repetitivemild traumatic brain injury. Journal of Neuroscience Methods 203, 41-49.
26. Kharatishvili, I., Sierra, A., Immonen, R.J., Grohn, O.H., Pitkanen, A., 2009. Quantitative T2 mapping as a potential marker for the initial assessment of the severity of damage after traumatic brain injury in rat. Experimental Neurology 217, 154-164.
27. Kopelman, R., Lee, Y.K., Philbert, M., Moffat, B.A., Reddy, G.R., McConville, P., Hall, D., Chenevert, T.L., Bhojani, T.L., Buck, S.M., Rehemtulla, A., Ross, B.D., 2005. Multifunctional nanoparticle platforms for in vivo MRI enhancement and photodynamic therapy of a rat brain cancer. Journal of Magnetism and Magnetic Materials 293, 404-410.
28. Kurland, D., Hong, C., Aarabi, B., Gerzanich, V., Simard, J.M., 2012. Hemorrhagic progression of a contusion after traumatic brain injury: a review. Journal of Neurotrauma 29, 19-31.
29. Laurer, H.L., Bareyre, F.M., Lee, V.M., Trojanowski, J.Q., Longhi, L.,Hoover, R., Saatman, K.E., Raghupathi, R., Hoshino, S., Grady, M.S., McIntosh, T.K., 2001. Mild head injury increasing the brain's vulnerability to a second concussive impact. Journal of Neurosurgery 95, 859-870.
30. Lee, H.,Wintermark, M., Gean, A.D., Ghajar, J., Manley, G.T., Mukherjee, P., 2008. Focal lesions in acute mild traumatic brain injury and neurocognitive outcome: CT versus 3T MRI. Journal of Neurotrauma 25, 1049-1056.
31. Lipton, M.L., Gellella, E., Lo, C., Gold, T., Ardekani, B.A., Shifteh, K., Bello, J.A., Branch, C.A., 2008. Multifocal white matter ultrastructural abnormalities in mild traumatic brain injury with cognitive disability: a voxel-wise analysis of diffusion tensor imaging. Journal of Neurotrauma 25, 1335-1342.
32. Longhi, L., Saatman, K.E., Fujimoto, S., Raghupathi, R.,Meaney,D.F., Davis, J.,McMillan, B.S.A., Conte, V., Laurer, H.L., Stein, S., Stocchetti, N., McIntosh, T.K., 2005. Temporal window of vulnerability to repetitive experimental concussive brain injury. Neurosurgery 56, 364-374 discussion 364-374.
33. Marquez de la Plata, C.D., Yang, F.G., Wang, J.Y., Krishnan, K., Bakhadirov, K., Paliotta, C., Aslan, S., Devous, M.D., Moore, C., Harper, C., McColl, R., Munro Cullum, C., Diaz-Arrastia, R., 2011. Diffusion tensor imaging biomarkers for traumatic axonal injury: analysis of three analytic methods. Journal of International Neuropsychological Society 17, 24-35.
34. Narayan, R.K., Maas, A.I., Servadei, F., Skolnick, B.E., Tillinger, M.N., Marshall, L.F., 2008. Progression of traumatic intracerebral hemorrhage: a prospective observational study. Journal of Neurotrauma 25, 629-639.
35. Nevo, U., Hauben, E., Yoles, E., Agranov, E., Akselrod, S., Schwartz, M., Neeman, M., 2001. Diffusion anisotropy MRI for quantitative assessment of recovery in injured rat spinal cord. Magnetic Resonance in Medicine 45, 1-9.
36. Obenaus, A., Dilmac, N., Tone, B., Tian, H.R., Hartman, R., Digicaylioglu, M., Snyder, E.Y., Ashwal, S., 2011. Long-term magnetic resonance imaging of stem cells in neonatal ischemic injury. Annals of Neurology 69, 282-291.
37. Obenaus, A., Huang, L., Smith, A., Favre, C.J., Nelson, G., Kendall, E., 2008. Magnetic resonance imaging and spectroscopy of the rat hippocampus 1 month after exposure to 56Fe-particle radiation. Radiation Research 169, 149-161.
38. Obenaus, A., Robbins, M., Blanco, G., Galloway, N.R., Snissarenko, E., Gillard, E., Lee, S., Curras-Collazo, M., 2007. Multi-modal magnetic resonance imaging alterations in two rat models of mild neurotrauma. Journal of Neurotrauma 24, 1147-1160.
39. Oehmichen, M.,Walter, T.,Meissner, C., Friedrich, H.J., 2003. Time course of cortical hemorrhages after closed traumatic brain injury: statistical analysis of posttraumatic histomorphological alterations. Journal of Neurotrauma 20, 87-103.
40. Rosidi, N.L., Zhou, J., Pattanaik, S., Wang, P., Jin, W., Brophy, M., Olbricht, W.L., Nishimura, N., Schaffer, C.B., 2011. Cortical microhemorrhages cause local inflammation but do not trigger widespread dendrite degeneration. PLoS One 6, e26612.
41. Schmued, L.C., Hopkins, K.J., 2000. Fluoro-Jade: novel fluorochromes for detecting toxicant-induced neuronal degeneration. Toxicologic Pathology 28, 91-99.
42. Shanmuganathan, K., Gullapalli, R.P., Mirvis, S.E., Roys, S., Murthy, P., 2004. Whole-brain apparent diffusion coefficient in traumatic brain injury: correlation with Glasgow Coma Scale score. AJNR. American Journal of Neuroradiology 25, 539-544.
43. Shitaka, Y., Tran, H.T., Bennett, R.E., Sanchez, L., Levy, M.A., Dikranian, K., Brody, D.L., 2011. Repetitive closed-skull traumatic brain injury in mice causes persistent multifocal axonal injury and microglial reactivity. Journal of Neuropathology and Experimental Neurology 70, 551-567.
44. Shultz, S.R., Bao, F., Omana, V., Chiu, C., Brown, A., Cain, D.P., 2012. 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. Journal of Neurotrauma 29, 281-294.
45. Sifri, Z.C., Homnick, A.T., Vaynman, A., Lavery, R., Liao, W.,Mohr, A., Hauser, C.J.,Manniker, A., Livingston, D., 2006. A prospective evaluation of the value of repeat cranial computed tomography in patients with minimal head injury and an intracranial bleed. The Journal of Trauma 61, 862-867.
46. Sifri, Z.C., Livingston, D.H., Lavery, R.F., Homnick, A.T., Mosenthal, A.C., Mohr, A.M., Hauser, C.J., 2004. Value of repeat cranial computed axial tomography scanning in patients with minimal head injury. American Journal of Surgery 187, 338-342.
47. Simard, J.M., Kahle, K.T., Gerzanich, V., 2010. Molecular mechanisms of microvascular failure in central nervous system injury - synergistic roles of NKCC1 and SUR1/TRPM4. Journal of Neurosurgery 113, 622-629.
48. Simard, J.M., Kilbourne, M., Tsymbalyuk, O., Tosun, C., Caridi, J., Ivanova, S., Keledjian, K., Bochicchio, G., Gerzanich, V., 2009. Key role of sulfonylurea receptor 1 in progressive secondary hemorrhage after brain contusion. Journal of Neurotrauma 26, 2257-2267.
49. Tagliaferri, F., Compagnone, C., Korsic, M., Servadei, F., Kraus, J., 2006. A systematic review of brain injury epidemiology in Europe. Acta Neurochirurgica 148, 255-268 discussion 268.
50. Thulborn, K.R., Sorensen, A.G., Kowall, N.W., McKee, A., Lai, A., McKinstry, R.C., Moore, J., Rosen, B.R., Brady, T.J., 1990. The role of ferritin and hemosiderin in the MR appearance of cerebral hemorrhage: a histopathologic biochemical study in rats. AJR. American Journal of Roentgenology 154, 1053-1059.
51. VA/DoD, 2009. Management of concussion/mild traumatic brain injury. VA/DoD Evidence Based Practice: Clinical Practice Guideline.
52. Vagnozzi, R., Signoretti, S., Tavazzi, B., Floris, R., Ludovici, A., Marziali, S., Tarascio, G., Amorini, A.M., Di Pietro, V., Delfini, R., Lazzarino, G., 2008. Temporal window of metabolic brain vulnerability to concussion: a pilot 1H-magnetic resonance spectroscopic study in concussed athletes-part III. Neurosurgery 62, 1286-1295 discussion 1295-1286.
53. Vagnozzi, R., Tavazzi, B., Signoretti, S., Amorini, A.M., Belli, A., Cimatti, M., Delfini, R., Di Pietro, V., Finocchiaro, A., Lazzarino, G., 2007. Temporal window of metabolic brain vulnerability to concussions:mitochondrial- related impairment-part I. Neurosurgery 61, 379-388 discussion 388-379.
54. Veltkamp, R., Siebing, D.A., Heiland, S., Schoenffeldt-Varas, P., Veltkamp, C., Schwaninger, M., Schwab, S., 2005. Hyperbaric oxygen induces rapid protection against focal cerebral ischemia. Brain Research 1037, 134-138.
55. Wang, X., Jung, J., Asahi, M., Chwang,W., Russo, L.,Moskowitz, M.A., Dixon, C.E., Fini,M.E., Lo, E.H., 2000. Effects ofmatrixmetalloproteinase-9 gene knock-out on morphological and motor outcomes after traumatic brain injury. Journal of Neuroscience 20, 7037-7042.
56. Xue, M., Del Bigio, M.R., 2000. Intracerebral injection of autologous whole blood in rats: time course of inflammation and cell death. Neuroscience Letters 283, 230-232.