Scale and pattern of atrophy in the chronic stages of moderate-severe TBI

Frontiers in Human Neuroscience

Volumn 8, Issue MAR, 2014, Pages

  Green, Robin E A ^a,b   Colella, Brenda ^a   Maller, Jerome J ^c   Bayley, Mark ^a   Glazer, Joanna ^a   Mikulis, David J ^d,e  

^a TORONTO REHABILITATION INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c Brain Stimulation and Neuroimaging Laboratory Monash Alfred Psychiatry Research Centre Alfred Hospital ^*  (Australia)

^d UNIVERSITY HEALTH NETWORK   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

Atrophy; Chronic; Degeneration; MRI; Progression; Traumatic brain injury

Indexed keywords

ADOLESCENT; ADULT; AGED; ARTICLE; BRAIN ATROPHY; BRAIN SIZE; CONTROLLED STUDY; CORPUS CALLOSUM; FEMALE; GLASGOW COMA SCALE; HIPPOCAMPUS; HUMAN; LEFT HEMISPHERE; MAJOR CLINICAL STUDY; MALE; NERVE DEGENERATION; NUCLEAR MAGNETIC RESONANCE IMAGING; RIGHT HEMISPHERE; TRAUMATIC BRAIN INJURY;

EID: 84896972596     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00067     Document Type: Article

References (63)

1. Adnan, A., Crawley, A., Mikulis, D., Moscovitch, M., Colella, B., and Green, R. E. (2013). Moderate-severe traumatic brain injury causes delayed loss of white matter integrity: evidence of fornix deterioration in the chronic stage of injury. Brain Inj. 27, 1415-1422.doi: 10.3109/02699052.2013.823659
2. Amaral, O. B., Vargas, R. S., Hansel, G., Izquierdo, I., and Souza, D. O. (2008). Duration of environmental enrichment influences the magnitude and persistence of its behavioral effects on mice. Physiol. Behav. 93, 388-394.doi: 10.1016/j.physbeh.2007.09.009
3. Analysisgroup. (2012). FMRIB Software Library v4.0 [Online]. Oxford: Nuffield Department of Clinical Neurosciences, University of Oxford. Accessed 2012. Available online at: http://www.fmrib.ox.ac.uk/fsl
4. Ariza, M., Serra-Grabulosa, J. M., Junqué, C., Ramírez, B., Mataró, M., Poca, A., et al. (2006). Hippocampal head atrophy after traumatic brain injury. Neuropsychologia 44, 1956-1961.doi: 10.1016/j.neuropsychologia.2005.11.007
5. Bendlin, B. B., Ries, M. L., Lazar, M., Alexander, A. L., Dempsey, R. J., Rowley, H. A., et al. (2008). Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neuroimage 42, 503-514.doi: 10.1016/j.neuroimage.2008.04.254
6. Bennett, R. E., Esparza, T. J., Lewis, H. A., Kim, E., Mac Donald, C. L., Sullivan, P. M., et al. (2013). Human apolipoprotein E4 worsens acute axonal pathology but not amyloid-beta immunoreactivity after traumatic brain injury in 3xTG-AD mice. J. Neuropathol. Exp. Neurol. 72, 396-403.doi: 10.1097/NEN.0b013e31828e24ab
7. Bigler, E. D. (2013a). Neuroinflammation and the dynamic lesion in traumatic brain injury. Brain 136, 9-11.doi: 10.1093/brain/aws342
8. Bigler, E. D. (2013b). Traumatic brain injury, neuroimaging, and neurodegeneration. Front. Hum. Neurosci. 7:395.doi: 10.3389/fnhum.2013.00395
9. Bramlett, H. M., Dietrich, W. D., Green, E. J., and Busto, R. (1997a). Chronic histopathological consequences of fluid-percussion brain injury in rats: effects of post-traumatic hypothermia. Acta Neuropathol. 93, 190-199.doi:10.1007/s004010050602
10. Bramlett, H. M., Kraydieh, S., Green, E. J., and Dietrich, W. D. (1997b). Temporal and regional patterns of axonal damage following traumatic brain injury: a beta-amyloid precursor protein immunocytochemical study in rats. J. Neuropathol. Exp. Neurol. 56, 1132-1141.doi: 10.1097/00005072-199710000-00007
11. 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.doi: 10.1016/S0006-8993(96)00819-0
12. Collins, D. L., Neelin, P., Peters, T. M., and Evans, A. C. (1994). Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J. Comput. Assist. Tomogr. 18, 192-205.doi: 10.1097/00004728-199403000-00005
13. Coulson, E. J., May, L. M., Osborne, S. L., Reid, K., Underwood, C. K., Meunier, F. A., et al. (2008). p75 neurotrophin receptor mediates neuronal cell death by activating GIRK channels through phosphatidylinositol 4,5-bisphosphate. J. Neurosci. 28, 315-324.doi: 10.1523/JNEUROSCI.2699-07.2008
14. Curlik, D. M. II, and Shors, T. J. (2010). Learning increases the survival of newborn neurons provided that learning is difficult to achieve and successful. J. Cogn. Neurosci. 23, 2159-2170.doi: 10.1162/jocn.2010.21597
15. Curlik, D.M. II, and Shors, T. J. (2013). Training your brain: Do mental and physical (MAP) training enhance cognition through the process of neurogenesis in the hippocampus? Neuropharmacology 64, 506-514.doi: 10.1016/j.neuropharm.2012.07.027
16. Dixon, C. E., Kochanek, P. M., Yan, H. Q., Schiding, J. K., Griffith, R. G., Baum, E., et al. (1999). One-year study of spatial memory performance, brain morphology, and cholinergic markers after moderate controlled cortical impact in rats. J. Neurotrauma 16, 109-122.doi: 10.1089/neu.1999.16.109
17. Draganski, B., Gaser, C., Kempermann, G., Kuhn, H. G., Winkler, J., Buchel, C., et al. (2006). Temporal and spatial dynamics of brain structure changes during extensive learning. J. Neurosci. 26, 6314-6317.doi: 10.1523/JNEUROSCI.4628-05.2006
18. Duering, M., Righart, R., Csanadi, E., Jouvent, E., Herve, D., Chabriat, H., et al. (2012). Incident subcortical infarcts induce focal thinning in connected cortical regions. Neurology 79, 2025-2028.doi: 10.1212/WNL.0b013e3182749f39
19. Evans, J. E. A. (2008). Research digest. Neuropsychol. Rehabil. 18, 372-384.doi: 10.1080/09602010801909153
20. Fakhran, S., Yaeger, K., and Alhilali, L. (2013). Symptomatic white matter changes in mild traumatic brain injury resemble pathologic features of early Alzheimer dementia. Radiology 269, 249-257.doi: 10.1148/radiol.13122343
21. Farbota, K. D., Bendlin, B. B., Alexander, A. L., Rowley, H. A., Dempsey, R. J., and Johnson, S. C. (2012). Longitudinal diffusion tensor imaging and neuropsychological correlates in traumatic brain injury patients. Front. Hum. Neurosci. 6:160.doi: 10.3389/fnhum.2012.00160
22. Frasca, D., Tomaszczyk, J., McFadyen, B. J., and Green, R. E. A. (2013). Traumatic brain injury and post-acute decline: what role does environmental enrichment play? A scoping review. Front. Hum. Neurosci. 7:31.doi: 10.3389/fnhum.2013.00031
23. Frisoni, G. B., Fox, N. C., Jack, C. R. Jr., Scheltens, P., and Thompson, P. M. (2010). The clinical use of structural MRI in Alzheimer disease. Nat. Rev. Neurol. 6, 67-77.doi: 10.1038/nrneurol.2009.215
24. Gennarelli, T. A., and Graham, D. I. (1998). Neuropathology of the head injuries. Semin. Clin. Neuropsychiatry 3, 160-175.
25. Gentleman, S. M., Leclercq, P. D., Moyes, L., Graham, D. I., Smith, C., Griffin, W. S. T., et al. (2004). Long-term intracerebral inflammatory response after traumatic brain injury. Forensic Sci. Int. 146, 97-104.doi: 10.1016/j.forsciint.2004.06.027
26. Green, R. E., Melo, B., Christensen, B., Ngo, L. A., Monette, G., and Bradbury, C. (2008). Measuring premorbid IQ in traumatic brain injury: an examination of the validity of the Wechsler Test of Adult Reading (WTAR). J. Clin. Exp. Neuropsychol. 30, 163-172.doi: 10.1080/13803390701300524
27. Greenberg, G., Mikulis, D. J., Ng, K., Desouza, D., and Green, R. E. (2008). Use of diffusion tensor imaging to examine subacute white matter injury progression in moderate to severe traumatic brain injury. Arch. Phys. Med. Rehabil. 89, S45-S50.doi: 10.1016/j.apmr.2008.08.211
28. Greer, J. E., Povlishock, J. T., and Jacobs, K. M. (2012). Electrophysiological abnormalities in both axotomized and nonaxotomized pyramidal neurons following mild traumatic brain injury. J. Neurosci. 32, 6682-6687.doi:10.1523/JNEUROSCI.0881-12.2012
29. Griesbach, G. S., Gomez-Pinilla, F., and Hovda, D. A. (2007). Time window for voluntary exercise-induced increases in hippocampal neuroplasticity molecules after traumatic brain injury is severity dependent. J. Neurotrauma 24, 1161-1171.doi: 10.1089/neu.2006.0255
30. Hollingshead, A. B., and Redlich, F. C. (1958). Social Class and Mental Illness. New York, NY: John Wiley.doi: 10.1037/10645-000
31. Johnson, V. E., Stewart, J. E., Begbie, F. D., Trojanowski, J. Q., Smith, D. H., and Stewart, W. (2013). Inflammation and white matter degeneration persist for years after a single traumatic brain injury. Brain 136, 28-42.doi: 10.1093/brain/aws322
32. Johnson, V. E., Stewart, W., and Smith, D. H. (2012). Widespread tau and amyloidBeta pathology many years after a single traumatic brain injury in humans. Brain Pathol. 22, 142-149.doi: 10.1111/j.1750-3639.2011.00513.x
33. Lezak, M. D. (2004). Neuropsychological Assessment. New York, NY: Oxford University Press.
34. Maguire, E. A., Woollett, K., and Spiers, H. J. (2006). London taxi drivers and bus drivers: a structural MRI and neuropsychological analysis. Hippocampus 16, 1091-1101.doi: 10.1002/hipo.20233
35. Maller, J. J., Daskalakis, Z. J., and Fitzgerald, P. B. (2007). Hippocampal volumetrics in depression: the importance of the posterior tail. Hippocampus 17, 1023-1027.doi: 10.1002/hipo.20339
36. Masel, B. E., and Dewitt, D. S. (2010). Traumatic brain injury: a disease process, not an event. J. Neurotrauma 27, 1529-1540.doi: 10.1089/neu.2010.1358
37. McCarthy, M. M. (2003). Stretching the truth. Why hippocampal neurons are so vulnerable following traumatic brain injury. Exp. Neurol. 184, 40-43.doi:10.1016/j.expneurol.2003.08.020
38. Members, E. C. C., Brayne, C., Ince, P. G., Keage, H. A., McKeith, I. G., Matthews, F. E., et al. (2010). Education, the brain and dementia: neuroprotection or compensation? Brain 133, 2210-2216.doi: 10.1093/brain/ awq185
39. Miller, L. S., Colella, B., Mikulis, D., Maller, J., and Green, R. E. (2013). Environmental enrichment may protect against hippocampal atrophy in the chronic stages of traumatic brain injury. Front. Hum. Neurosci. 7:506.doi:10.3389/fnhum.2013.00506
40. Millis, S. R., Rosenthal, M., Novack, T. A., Sherer, M., Nick, T. G., Kreutzer, J. S., et al. (2001). Long-term neuropsychological outcome after traumatic brain injury. J. Head Trauma Rehabil. 16, 343-355.doi: 10.1097/00001199200108000-00005
41. Ng, K., Mikulis, D. J., Glazer, J., Kabani, N., Till, C., Greenberg, G., et al. (2008). Magnetic resonance imaging evidence of progression of subacute brain atrophy in moderate to severe traumatic brain injury. Arch. Phys. Med. Rehabil. 89, S35-S44.doi: 10.1016/j.apmr.2008.07.006
42. Ponsford, J., McLaren, A., Schonberger, M., Burke, R., Rudzki, D., Olver, J., et al. (2011). The association between apolipoprotein E and traumatic brain injury severity and functional outcome in a rehabilitation sample. J. Neurotrauma 28, 1683-1692.doi: 10.1089/neu.2010.1623
43. Povlishock, J. T., and Katz, D. I. (2005). Update of neuropathology and neurological recovery after traumatic brain injury. J. Head Trauma Rehabil. 20, 76-94.doi: 10.1097/00001199-200501000-00008
44. Rodriguez-Paez, A. C., Brunschwig, J. P., and Bramlett, H. M. (2005). Light and electron microscopic assessment of progressive atrophy following moderate traumatic brain injury in the rat. Acta Neuropathol. 109, 603-616.doi:10.1007/s00401-005-1010-z
45. Ross, D. E., Ochs, A. L., Seabaugh, J. M., Demark, M. F., Shrader, C. R., Marwitz, J. H., et al. (2012). Progressive brain atrophy in patients with chronic neuropsychiatric symptoms after mild traumatic brain injury: a preliminary study. Brain Inj. 26, 1500-1509.doi: 10.3109/02699052.2012.694570
46. Ruff, R. M., Young, D., Gautille, T., Marshall, L. F., Barth, J., Jane, J. A., et al. (1991). Verbal learning deficits following severe head injury: heterogeneity in recovery over 1 year. J. Neurosurg. 75, S50-S58.
47. Sidaros, A., Engberg, A. W., Sidaros, K., Liptrot, M. G., Herning, M., Petersen, P., et al. (2008). Diffusion tensor imaging during recovery from severe traumatic brain injury and relation to clinical outcome: a longitudinal study. Brain 131, 559-572.doi: 10.1093/brain/awm294
48. Sidaros, A., Skimminge, A., Liptrot, M. G., Sidaros, K., Engberg, A. W., Herning, M., et al. (2009). Long-term global and regional brain volume changes following severe traumatic brain injury: a longitudinal study with clinical correlates. Neuroimage 44, 1-8.doi: 10.1016/j.neuroimage.2008.08.030
49. Sled, J. G., Zijdenbos, A. P., and Evans, A. C. (1998). A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans. Med. Imaging 17, 87-97.doi: 10.1109/42.668698
50. Smith, D. H., Johnson, V. E., and Stewart, W. (2013). Chronic neuropathologies of single and repetitive TBI: substrates of dementia? Nat. Rev. Neurol. 9, 211-221.doi: 10.1038/nrneurol.2013.29
51. Smith, D. H., Uryu, K., Saatman, K. E., Trojanowski, J. Q., and McIntosh, T. K. (2003). Protein accumulation in traumatic brain injury. Neuromolecular Med. 4, 59-72.doi: 10.1385/NMM:4:1-2:59
52. Talairach, J., and Tournoux, P. (1988). Co-planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: an Approach to Cerebral Imaging. New York, NY: Thieme Medical Publishers.
53. Tate, D. F., and Bigler, E. D. (2000). Fornix and hippocampal atrophy in traumatic brain injury. Learn. Mem. 7, 442-446.doi: 10.1101/lm.33000
54. Tate, D. F., Khedraki, R., Neeley, E. S., Ryser, D. K., and Bigler, E. D. (2011). Cerebral volume loss, cognitive deficit, and neuropsychological performance: comparative measures of brain atrophy: II. Traumatic brain injury.J. Int. Neuropsychol. Soc. 17, 308-316.doi: 10.1017/S1355617710001670
55. Till, C., Colella, B., Verwegen, J., and Green, R. E. (2008). Postrecovery cognitive decline in adults with traumatic brain injury. Arch. Phys. Med. Rehabil. 89, S25-S34.doi: 10.1016/j.apmr.2008.07.004
56. Underwood, C. K., and Coulson, E. J. (2008). The p75 neurotrophin receptor. Int. J. Biochem. Cell Biol. 40, 1664-1668.doi: 10.1016/j.biocel.2007.06.010
57. Uryu, K., Chen, X. H., Martinez, D., Browne, K. D., Johnson, V. E., Graham, D. I., et al. (2007). Multiple proteins implicated in neurodegenerative diseases accumulate in axons after brain trauma in humans. Exp. Neurol. 208, 185-192.doi: 10.1016/j.expneurol.2007.06.018
58. Watson, C., Andermann, F., Gloor, P., Jones-Gotman, M., Peters, T., Evans, A., et al. (1992). Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging. Neurology 42, 1743-1750.doi:10.1212/WNL.42.9.1743
59. Watson, C., Cendes, F., Fuerst, D., Dubeau, F., Williamson, B., Evans, A., et al. (1997). Specificity of volumetric magnetic resonance imaging in detecting hippocampal sclerosis. Arch. Neurol. 54, 67-73.doi: 10.1001/archneur.1997.00550130049015
60. Weschler, D. (2001). Wechsler Test of Adult Reading (WTAR). San Antonio, TX: Harcourt Assessment.
61. Wilde, E. A., Chu, Z., Bigler, E. D., Hunter, J. V., Fearing, M. A., Hanten, G., et al. (2006). Diffusion tensor imaging in the corpus callosum in children after moderate to severe traumatic brain injury. J. Neurotrauma 23, 1412-1426.doi:10.1089/neu.2006.23.1412
62. Williams, S., Raghupathi, R., Mackinnon, M. A., McIntosh, T. K., Saatman, K. E., and Graham, D. I. (2001). In situ DNA fragmentation occurs in white matter up to 12 months after head injury in man. Acta Neuropathol. 102, 581-590.doi:10.1007/s004010100410
63. Zijdenbos, A. P., Forghani, R., and Evans, A. C. (1998). "MRI brain data sets: validation of INSECT," in Medical Image Computing and Computer-Assisted Intervetion Miccai '98, eds W. M. Wells, A. Colchester, and S. Delps (Cambridge: Springer), 439-448.