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Research Article

Moderate–severe traumatic brain injury causes delayed loss of white matter integrity: Evidence of fornix deterioration in the chronic stage of injury

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Pages 1415-1422 | Received 20 Nov 2012, Accepted 10 Jun 2013, Published online: 08 Oct 2013

References

  • Lipton ML, Gulko E, Zimmerman ME, Friedman BW, Kim M, Gellella E, Gold T, Shifteh K, Ardekani BA, Branch CA. Diffusion-tensor imaging implicates prefrontal axonal injury in executive function impairment following very mild traumatic brain injury. Radiology 2009;252:816–824
  • Povlishock JT, Katz DI. Update of neuropathology and neurological recovery after traumatic brain injury. Journal of Head Trauma Rehabilitation 2005;20:76–94
  • Buki A, Povlishock JT. All roads lead to disconnection? - Traumatic axonal injury revisited. Acta Neurochirurgica (Wien) 2006;148:181–194
  • Adams JH, Graham DI, Murray LS, Scott G. Diffuse axonal injury due to nonmissile head injury in humans: An analysis of 45 cases. Annals of Neurology 1982;12:557–563
  • Gennarelli TA, Thibault LE, Adams HJ, Graham DI, Thompson CJ, Marcincin RP. Diffuse axonal injury and traumatic coma in the primate. Annals of Neurology 1982;12:564–574
  • Bendlin BB, Ries ML, Lazar M, Alexander AL, Dempsey RJ, Rowley HA, Sherman JE, Johnson SC. Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neuroimage 2008;42:503–514
  • Bigler ED, Kurth SM, Blatter D, Abildskov TJ. Degenerative changes in traumatic brain injury: Post-injury magnetic resonance identified ventricular expansion compared to pre-injury levels. Brain Research Bulletin 1992;28:651–653
  • Greenberg G, Mikulis DJ, Ng K, DeSouza D, Green RE. Use of diffusion tensor imaging to examine subacute white matter injury progression in moderate to severe traumatic brain injury. Archives of Physical Medicine & Rehabilitation 2008;89:S45–S50
  • Ng K, Mikulis DJ, Glazer J, Kabani N, Till C, Greenberg G, Thompson A, Lazinski D, Agid R, Colella B, et al. Magnetic resonance imaging evidence of progression of subacute brain atrophy in moderate to severe traumatic brain injury. Archives of Physical Medicine & Rehabilitation 2008;89:S35–S44
  • Sidaros A, Skimminge A, Liptrot MG, Sidaros K, Engberg AW, Herning M, Paulson OB, Jernigan TL, Rostrup E. Long-term global and regional brain volume changes following severe traumatic brain injury: A longitudinal study with clinical correlates. Neuroimage 2009;44:1–8
  • Sidaros A, Engberg AW, Sidaros K, Liptrot MG, Herning M, Petersen P, Paulson OB, Jernigan TL, Rostrup E. Diffusion tensor imaging during recovery from severe traumatic brain injury and relation to clinical outcome: A longitudinal study. Brain 2008;131:559–572
  • Kolb B, Muhammad A, Gibb R. Searching for factors underlying cerebral plasticity in the normal and injured brain. Journal of Communication Disorders 2011;44:503–514
  • Niogi SN, Mukherjee P, Ghajar J, Johnson C, Kolster RA, Sarkar R, Lee H, Meeker M, Zimmerman RD, Manley GT, 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. American Journal of Neuroradiology 2008;29:967–973
  • Arfanakis K, Haughton VM, Carew JD, Rogers BP, Dempsey RJ, Meyerand ME. Diffusion tensor MR imaging in diffuse axonal injury. Am J Neuroradiol 2002;23:794–802
  • Chan JH, Tsui EY, Peh WC, Fong D, Fok KF, Leung KM, Yuen MK, Fung KK. Diffuse axonal injury: Detection of changes in anisotropy of water diffusion by diffusion-weighted imaging. Neuroradiology 2003;45:34–38
  • Fox RJ, Cronin T, Lin J, Wang X, Sakaie K, Ontaneda D, Mahmoud SY, Lowe MJ, Phillips MD. Measuring myelin repair and axonal loss with diffusion tensor imaging. American Journal of Neuroradiology 2011;32:85–91
  • Huisman TA, Schwamm LH, Schaefer PW, Koroshetz WJ, Shetty-Alva N, Ozsunar Y, Wu O, Sorensen AG. Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. American Journal of Neuroradiology 2004;25:370–376
  • Inglese M, Makani S, Johnson G, Cohen BA, Silver JA, Gonen O, Grossman RI. Diffuse axonal injury in mild traumatic brain injury: A diffusion tensor imaging study. Journal of Neurosurgery 2005;103:298–303
  • Nakayama N, Okumura A, Shinoda J, Yasokawa YT, Miwa K, Yoshimura SI, Iwama T. Evidence for white matter disruption in traumatic brain injury without macroscopic lesions. Journal of Neurology, Neurosurgery & Psychiatry 2006;77:850–855
  • Ptak T, Sheridan RL, Rhea JT, Gervasini AA, Yun JH, Curran MA, Borszuk P, Petrovick L, Novelline RA. Cerebral fractional anisotropy score in trauma patients: A new indicator of white matter injury after trauma. American Journal of Roentgenology 2003;181:1401–1407
  • Rugg-Gunn FJ, Symms MR, Barker GJ, Greenwood R, Duncan JS. Diffusion imaging shows abnormalities after blunt head trauma when conventional magnetic resonance imaging is normal. Journal of Neurology, Neurosurgery & Psychiatry 2001;70:530–533
  • Salmond CH, Menon DK, Chatfield DA, Williams GB, Pena A, Sahakian BJ, Pickard JD. Diffusion tensor imaging in chronic head injury survivors: Correlations with learning and memory indices. Neuroimage 2006;29:117–124
  • Tate DF, Bigler ED. Fornix and hippocampal atrophy in traumatic brain injury. Learning & Memory 2000;7:442–446
  • Tsivilis D, Vann SD, Denby C, Roberts N, Mayes AR, Montaldi D, Aggleton JP. A disproportionate role for the fornix and mammillary bodies in recall versus recognition memory. Nature Neuroscience 2008;11:834–842
  • Chang MC, Kim SH, Kim OL, Bai DS, Jang SH. The relation between fornix injury and memory impairment in patients with diffuse axonal injury: A diffusion tensor imaging study. Neurorehabilitation 2010;26:347–353
  • Hong JH, Jang SH. Degeneration of cingulum and fornix in a patient with traumatic brain injury: Diffuse tensor tractography study. Journal of Rehabilitation Medicine 2010;42:979–981
  • Palacios EM, Fernandez-Espejo D, Junque C, Sanchez-Carrion R, Roig T, Tormos JM, Bargallo N, Vendrell P. Diffusion tensor imaging differences relate to memory deficits in diffuse traumatic brain injury. BMC Neurology 2011;23:11--24
  • Wang JY, Bakhadirov K, Devous MD Sr, Abdi H, McColl R, Moore C, Marquez de la Plata CD, Ding K, Whittemore A, Babcock E, et al. Diffusion tensor tractography of traumatic diffuse axonal injury. Archives of Neurology 2008;65:619–626
  • Xu J, Rasmussen IA, Lagopoulos J, Haberg A. Diffuse axonal injury in severe traumatic brain injury visualized using high-resolution diffusion tensor imaging. Journal of Neurotrauma 2007;24:753–765
  • Zhan W, Boreta L, Gauger G. Magnetic resonance imaging for white matter degradation in fornix following mild traumatic brain injury. San Diego, CA: Medical Imaging 2010: Biomedical Applications in Molecular, Structural, and Functional Imaging Conference; 2010. p 1–7
  • Farbota KD, Bendlin BB, Alexander AL, Rowley HA, Dempsey RJ, Johnson SC. Longitudinal diffusion tensor imaging and neuropsychological correlates in traumatic brain injury patients. Frontiers in Human Neuroscience 2012;6:1006--1018
  • Rorden C, Karnath HO, Bonilha L. Improving lesion-symptom mapping. Journal of Cognitive Neuroscience 2007;19:1081–1088
  • Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004;23:S208–S219
  • Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, Beckmann C, Jenkinson M, Smith SM. Bayesian analysis of neuroimaging data in FSL. Neuroimage 2009;45:S173–S186
  • Smith SM. Fast robust automated brain extraction. Human Brain Mapping 2002;17:143–155
  • Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, et al. Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. Neuroimage 2006;31:1487–1505
  • Andersson JLR, Jenkinson M, Smith S. Non-linear optimisation. FMRIB technical report TR07JA1. FMRIB Centre, Oxford, United Kingdom. 2007. Available online at: www.fmrib.ox.ac.uk/analysis/techrep, accessed 2012
  • Andersson JLR, Jenkinson M, Smith S. Non-linear registration, aka Spatial normalisation FMRIB technical report TR07JA2. FMRIB Centre, Oxford, United Kingdom. 2007. Available online at: www.fmrib.ox.ac.uk/analysis/techrep, accessed 2012
  • Rueckert D, Sonoda LI, Hayes C, Hill DL, Leach MO, Hawkes DJ. Nonrigid registration using free-form deformations: Application to breast MR images. IEEE Transactions in Medical Imaging 1999;18:712–721
  • Jang SH, Cho SH, Chang MC. Age-related degeneration of the fornix in the human brain: A diffusion tensor imaging study. International Journal of Neuroscience 2011;121:94–100
  • Mori S, Oishi K, Jiang H, Jiang L, Li X, Akhter K, Hua K, Faria AV, Mahmood A, Woods R, et al. Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 2008;40:570–582
  • Rodriguez-Paez AC, Brunschwig JP, Bramlett HM. Light and electron microscopic assessment of progressive atrophy following moderate traumatic brain injury in the rat. Acta Neuropathologica 2005;109:603–616
  • Johnson VE, Stewart JE, Begbie FD, Trojanowski JQ, Smith DH, Stewart W. Inflammation and white matter degeneration persist for years after a single traumatic brain injury. Brain 2013;136:28–42
  • Smith C, Gentleman SM, Leclercq PD, Murray LS, Griffin WST, Graham DI, Nicoll JAR. The neuroinflammatory response in humans after traumatic brain injury. Neuropathology and Applied Neurobiology 2012:n/a–n/a
  • Bigler ED. Neuroinflammation and the dynamic lesion in traumatic brain injury. Brain 2013;136:9–11
  • Bramlett HM, Dietrich WD, Green EJ, Busto R. Chronic histopathological consequences of fluid-percussion brain injury in rats: Effects of post-traumatic hypothermia. Acta Neuropathologica 1997;93:190–199
  • Williams S, Raghupathi R, MacKinnon MA, McIntosh TK, Saatman KE, Graham DI. In situ DNA fragmentation occurs in white matter up to 12 months after head injury in man. Acta Neuropathologica 2001;102:581–590
  • Bramlett HM, Kraydieh S, Green EJ, Dietrich WD. Temporal and regional patterns of axonal damage following traumatic brain injury: A beta-amyloid precursor protein immunocytochemical study in rats. Journal of Neuropathology & Experimental Neurology 1997;56:1132–1141
  • Colicos MA, Dixon CE, Dash PK. Delayed, selective neuronal death following experimental cortical impact injury in rats: Possible role in memory deficits. Brain Research 1996;739:111–119
  • Smith DH, Chen XH, Pierce JE, Wolf JA, Trojanowski JQ, Graham DI, McIntosh TK. Progressive atrophy and neuron death for one year following brain trauma in the rat. Journal of Neurotrauma 1997;14:715–727
  • Smith DH, Uryu K, Saatman KE, Trojanowski JQ, McIntosh TK. Protein accumulation in traumatic brain injury. Neuromolecular Medicine 2003;4:59–72
  • Uryu K, Chen XH, Martinez D, Browne KD, Johnson VE, Graham DI, Lee VM, Trojanowski JQ, Smith DH. Multiple proteins implicated in neurodegenerative diseases accumulate in axons after brain trauma in humans. Experimental Neurology 2007;208:185–192
  • Johnson VE, Stewart W, Smith DH. Widespread tau and amyloid-Beta pathology many years after a single traumatic brain injury in humans. Brain Pathology 2012;22:142–149
  • Smith DH, Johnson VE, Stewart W. Chronic neuropathologies of single and repetitive TBI: Substrates of dementia? Nature Reviews Neurology 2013;9:211--221
  • Greer JE, McGinn MJ, Povlishock JT. Diffuse traumatic axonal injury in the mouse induces atrophy, c-Jun activation, and axonal outgrowth in the axotomized neuronal population. Journal of Neuroscience 2011;31:5089–5105
  • Bigler ED, Maxwell WL. Neuroimaging and neuropathology of TBI. NeuroRehabilitation 2011;28:63–74
  • Masel BE, DeWitt DS. Traumatic brain injury: A disease process, not an event. Journal of Neurotrauma 2010;27:1529–1540
  • Hannay HJ, Howieson DB, Loring DW, Fischer JS, Lezak MD. “Neuropathology for neuropsychologists”. In: Lezak MD, Howieson DB, Loring DW, editors. Neuropsychological assessment. Oxford, Oxfordshire: Oxford University Press; 2004. p 160
  • Bach-y-Rita, P. Theoretical basis for brain plasticity after a TBI. Brain Injury 2003;17:643--651

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