Prospective longitudinal MRI study of brain volumes and diffusion changes during the first year after moderate to severe traumatic brain injury

NeuroImage: Clinical

Volumn 5, Issue , 2014, Pages 128-140

  Brezova, Veronika ^a,b   Gøran Moen, Kent ^b,c   Skandsen, Toril ^b,c   Vik, Anne ^b,c   Brewer, James B ^d,e   Salvesen, Øyvind ^a   Håberg, Asta K ^b,c  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b TRONDHEIM UNIVERSITY HOSPITAL   (Norway)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ADC; Diffuse axonal injury; Glasgow Coma Scale; Outcome; Post traumatic amnesia

Indexed keywords

ADOLESCENT; ADULT; AGED; AMNESIA; ARTICLE; BRAIN CORTEX; BRAIN SIZE; BRAIN STEM; BRAIN VENTRICLE; CONTROLLED STUDY; DIFFUSE AXONAL INJURY; DIFFUSION; DIFFUSION COEFFICIENT; DISEASE DURATION; FEMALE; GLASGOW COMA SCALE; GLASGOW OUTCOME SCALE; GRAY MATTER; HIPPOCAMPUS; HOSPITAL ADMISSION; HUMAN; HUMAN TISSUE; INJURY SEVERITY; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; POSTTRAUMATIC AMNESIA; PREDICTION; PREDICTIVE VALUE; PRIORITY JOURNAL; PROSPECTIVE STUDY; TIME; TRAUMATIC BRAIN INJURY; WHITE MATTER; BRAIN; BRAIN INJURY; INJURY SCALE; MIDDLE AGED; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; POSTERIOR LONGITUDINAL LIGAMENT; YOUNG ADULT; BRAIN ATROPHY; BRAIN HEMATOMA; BRAIN TISSUE; INSULA; OUTCOME ASSESSMENT;

ADOLESCENT; ADULT; AGED; BRAIN; BRAIN INJURIES; FEMALE; GLASGOW COMA SCALE; HUMANS; INJURY SEVERITY SCORE; LONGITUDINAL LIGAMENTS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; ORGAN SIZE; PROSPECTIVE STUDIES; YOUNG ADULT;

EID: 84904577207     PISSN: None     EISSN: 22131582     Source Type: Journal    
DOI: 10.1016/j.nicl.2014.03.012     Document Type: Article

References (74)

1. Anderson C.V., and Bigler E.D. Ventricular dilation, cortical atrophy, and neuropsychological outcome following traumatic brain injury Journal of Neuropsychiatry and Clinical Neurosciences 7 1995 42 48 7711490
2. Bendlin B.B., Ries M.L., Lazar M., Alexander A.L., Dempsey R.J., and Rowley H.A. Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging Neuroimage 42 2008 503 514 10.1016/j.neuroimage.2008.04.254 18556217
3. Bergsneider M., Hovda D.A., McArthur D.L., Etchepare M., Huang S., and Sehati N. Metabolic recovery following human traumatic brain injury based on FDG-PET: time course and relationship to neurological disability Journal of Head Trauma Rehabilitation 16 2001 135 148 10.1097/00001199-200104000-00004 11275575 (Pubitemid 32319511)
4. Bigler E.D., Blatter D.D., Anderson C.V., Johnson S.C., Gale S.D., and Hopkins R.O. Hippocampal volume in normal aging and traumatic brain injury AJNR. American Journal of Neuroradiology 18 1997 11 23 9010515 (Pubitemid 127744392)
5. Blatter D.D., Bigler E.D., Gale S.D., Johnson S.C., Anderson C.V., and Burnett B.M. MR-based brain and cerebrospinal fluid measurement after traumatic brain injury: correlation with neuropsychological outcome AJNR. American Journal of Neuroradiology 18 1997 1 10 9010514
6. Bouilleret V., Cardamone L., Liu Y.R., Fang K., Myers D.E., and O'Brien T.J. Progressive brain changes on serial manganese-enhanced MRI following traumatic brain injury in the rat Journal of Neurotrauma 26 2009 1999 2013 10.1089/neu.2009.0943 19604101
7. Brandstack N., Kurki T., Hiekkanen H., and Tenovuo O. Diffusivity of normal-appearing tissue in acute traumatic brain injury Clinical Neuroradiology 21 2011 75 82 10.1007/s00062-011-0058-5 21394634
8. Brewer J.B., Magda S., Airriess C., and Smith M.E. Fully-automated quantification of regional brain volumes for improved detection of focal atrophy in Alzheimer disease AJNR. American Journal of Neuroradiology 30 2009 578 580 10.3174/ajnr.A1402 19112065
9. Cipolotti L., and Bird C.M. Amnesia and the hippocampus Current Opinion in Neurology 19 2006 593 598 10.1097/01.wco.0000247608.42320.f9 17102699 (Pubitemid 44760444)
10. Coleman M.P Axon degeneration mechanisms: commonality amid diversity Nature Reviews Neuroscience 6 2005 889 898 10.1038/nrn1788 (Pubitemid 41568730)
11. Coleman M.P., and Freeman M.R. Wallerian degeneration, wld(s), and nmnat Annual Review of Neuroscience 33 2010 245 267 10.1146/annurev-neuro-060909- 153248 20345246
12. Conti A.C., Raghupathi R., Trojanowski J.Q., and McIntosh T.K. Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post-traumatic period Journal of Neuroscience: the Official Journal of the Society for Neuroscience 18 1998 5663 5672 9671657 (Pubitemid 28341346)
13. Ding K., Marquez de la Plata C., M. [!(%xInRef|ce:surname)!], Wang J.Y., Mumphrey M., Moore C., and Harper C. Cerebral atrophy after traumatic white matter injury: correlation with acute neuroimaging and outcome Journal of Neurotrauma 25 2008 1433 1440 10.1089/neu.2008.0683 19072588
14. Eichenbaum H., Yonelinas A.P., and Ranganath C. The medial temporal lobe and recognition memory Annual Review of Neuroscience 30 2007 123 152 10.1146/annurev.neuro.30.051606.094328 17417939 (Pubitemid 47224758)
15. Fearing M.A., Bigler E.D., Wilde E.A., Johnson J.L., Hunter J.V., and Xiaoqi Li Morphometric MRI findings in the thalamus and brainstem in children after moderate to severe traumatic brain injury Journal of Child Neurology 23 2008 729 737 10.1177/0883073808314159 18658073 (Pubitemid 351998158)
16. Fox G.B., Fan L., Levasseur R.A., and Faden A.I. Sustained sensory/motor and cognitive deficits with neuronal apoptosis following controlled cortical impact brain injury in the mouse Journal of Neurotrauma 15 1998 599 614 10.1089/neu.1998.15.599 9726259 (Pubitemid 28413053)
17. Fox N.C., Crum W.R., Scahill R.I., Stevens J.M., Janssen J.C., and Rossor M.N. Imaging of onset and progression of Alzheimer's disease with voxel-compression mapping of serial magnetic resonance images Lancet 358 2001 201 205 10.1016/S0140-6736(01)05408-3 11476837 (Pubitemid 32718544)
18. Gao X., and Chen J. Moderate traumatic brain injury promotes neural precursor proliferation without increasing neurogenesis in the adult hippocampus Experimental Neurology 239C 2013 38 48 23022454
19. Gao X., Deng P., Xu Z.C., and Chen J. Moderate traumatic brain injury causes acute dendritic and synaptic degeneration in the hippocampal dentate gyrus PloS One 6 2011 e24566 10.1371/journal.pone.0024566 21931758
20. Gao X., Enikolopov G., and Chen J. Direct isolation of neural stem cells in the adult hippocampus after traumatic brain injury Journal of Neurotrauma 25 2008 985 995 10.1089/neu.2008.0460 18665804
21. Gentry L.R Imaging of closed head injury Radiology 191 1994 1 17 8134551 (Pubitemid 24098193)
22. Giunta B., Obregon D., Velisetty R., Sanberg P.R., Borlongan C.V., and Tan J. The immunology of traumatic brain injury: a prime target for Alzheimer's disease prevention Journal of Neuroinflammation 9 2012 185 10.1186/1742-2094-9- 185 22849382
23. Goetz P., Blamire A., Rajagopalan B., Cadoux-hudson T.O.M., Young D., and Styles P. Increase in apparent diffusion coefficient in normal appearing white matter following human traumatic brain injury correlates with injury severity Journal of Neurotrauma 21 2004 645 654 10.1089/0897715041269731 15253793 (Pubitemid 38880237)
24. Greer J.E., McGinn M.J., and Povlishock J.T. Diffuse traumatic axonal injury in the mouse induces atrophy, c-Jun activation, and axonal outgrowth in the axotomized neuronal population Journal of Neuroscience: the Official Journal of the Society for Neuroscience 31 2011 5089 5105 10.1523/JNEUROSCI.5103-10. 2011 21451046
25. Gwet, K.L., Intrarater reliability, in: Wiley Encycl., Published Online, 2008
26. Hergan K., Schaefer P.W., Sorensen A.G., Gonzalez R.G., and Huisman T.A.G.M. Diffusion-weighted MRI in diffuse axonal injury of the brain European Radiology 12 2002 2536 2541 12271396 (Pubitemid 36940361)
27. Hicks R., Soares H., Smith D., and McIntosh T. Temporal and spatial characterization of neuronal injury following lateral fluid-percussion brain injury in the rat Acta Neuropathologica 91 1996 236 246 10.1007/s004010050421 8834535 (Pubitemid 26042215)
28. Holland D., Brewer J.B., Hagler D.J., Fennema-notestine C., and Dale A.M. Subregional neuroanatomical change as a biomarker for Alzheimer's disease Proceedings of the National Academy of Sciences of the United States of America 107 2009 20954 20959 19996185
29. Holland D., McEvoy L.K., and Dale A.M. Unbiased comparison of sample size estimates from longitudinal structural measures in ADNI Human Brain Mapping 33 2012 2586 2602 10.1002/hbm.21386 21830259
30. Immonen R.J., Kharatishvili I., Gröhn H., Pitkänen A., and Gröhn O.H.J. Quantitative MRI predicts long-term structural and functional outcome after experimental traumatic brain injury Neuroimage 45 2009 1 9 10.1016/j.neuroimage.2008.11.022 19101638
31. Jenkins A., Teasdale G., Hadley M.D., Macpherson P., and Rowan J.O. Brain lesions detected by magnetic resonance imaging in mild and severe head injuries Lancet 2 1986 445 446 2874424 (Pubitemid 16039249)
32. Jennett B., and Bond M. Assessment of outcome after severe brain damage: a practical scale Lancet 305 1975 480 484 10.1016/S0140-6736(75)92830-5
33. Jennett B., Snoek J., Bond M.R., and Brooks N. Disability after severe head injury: observations on the use of the Glasgow Outcome Scale Journal of Neurology, Neurosurgery, and Psychiatry 44 1981 285 293 10.1136/jnnp.44.4.285 6453957 (Pubitemid 11070501)
34. Kim J., Avants B., Patel S., Whyte J., Coslett B.H., and Pluta J. Structural consequences of diffuse traumatic brain injury: a large deformation tensor-based morphometry study Neuroimage 39 2008 1014 1026 10.1016/j. neuroimage.2007.10.005 17999940
35. Klimas A., Drzazga Z., Kluczewska E., and Hartel M. Regional ADC measurements during normal brain aging in the clinical range of b values: a DWI study Clinical imaging 37 2013 637 644 10.1016/j.clinimag.2013.01.013 23462734
36. LeGrand S.A., Hindman B.J., Dexter F., Moss L.G., and Todd M.M. Reliability of a telephone-based Glasgow Outcome Scale assessment using a structured interview in a heterogenous population of patients and examiners Journal of Neurotrauma 24 2007 1437 1446 10.1089/neu.2007.0293 17892406 (Pubitemid 47493509)
37. Lin Y., and Wen L. Inflammatory response following diffuse axonal injury International Journal of Medical Sciences 10 2013 515 521 10.7150/ijms.5423 23532682
38. Liu Y.R., Cardamone L., Hogan R.E., Gregoire M.-C., Williams J.P., and Hicks R.J. Progressive metabolic and structural cerebral perturbations after traumatic brain injury: an in vivo imaging study in the rat Journal of Nuclear Medicine: Official Publication, Society of Nuclear Medicine 51 2010 1788 1795 10.2967/jnumed.110.078626 21051651
39. Maas A.I.R., Hukkelhoven C.W.P.M., Marshall L.F., and Steyerberg E.W. Prediction of outcome in traumatic brain injury with computed tomographic characteristics: a comparison between the Computed Tomographic Classification and Combinations of Computed Tomographic Predictors Neurosurgery 57 2005 1173 1182 10.1227/01.NEU.0000186013.63046.6B 16331165 (Pubitemid 41827403)
40. Marcoux J., McArthur D.A., Miller C., Glenn T.C., Villablanca P., and Martin N.A. Persistent metabolic crisis as measured by elevated cerebral microdialysis lactate-pyruvate ratio predicts chronic frontal lobe brain atrophy after traumatic brain injury Critical Care Medicine 36 2008 2871 2877 10.1097/CCM.0b013e318186a4a0 18766106
41. Maxwell W.L., Dhillon K., Harper L., Espin J., MacIntosh T.K., and Smith D.H. There is differential loss of pyramidal cells from the human hippocampus with survival after blunt head injury Journal of Neuropathology and Experimental Neurology 62 2003 272 279 12638731 (Pubitemid 36330678)
42. Maxwell W.L., MacKinnon M.-A., Stewart J.E., and Graham D.I. Stereology of cerebral cortex after traumatic brain injury matched to the Glasgow outcome score Brain: a Journal of Neurology 133 2010 139 160 10.1093/brain/awp264 19897544
43. Meaney D., and Smith D. Biomechanics of concussion Clinics in Sports Medicine 30 2011 19 31 10.1016/j.csm.2010.08.009 21074079
44. Moen K.G., Skandsen T., Folvik M., Brezova V., Kvistad K.A., and Rydland J. A longitudinal MRI study of traumatic axonal injury in patients with moderate and severe traumatic brain injury Journal of Neurology, Neurosurgery, and Psychiatry 83 2012 1193 1200 10.1136/jnnp-2012-302644 22933813
45. Nakase-Richardson R., Sherer M., Seel R.T., Hart T., Hanks R., and Arango-Lasprilla J.C. Utility of post-traumatic amnesia in predicting 1-year productivity following traumatic brain injury: comparison of the Russell and Mississippi PTA classification intervals Journal of Neurology, Neurosurgery, and Psychiatry 82 2011 494 499 10.1136/jnnp.2010.222489 21242285
46. Ng H., Mahaliyana R.D., and Poonb W.S. The pathological spectrum of diffuse axonal injury in blunt head trauma: assessment with axon and myelin strains Clinical Neurology and Neurosurgery 34 1994 24 31 8187378 (Pubitemid 24060029)
47. Ng K., Mikulis D.J., Glazer J., Kabani N., Till C., and Greenberg G. Magnetic resonance imaging evidence of progression of subacute brain atrophy in moderate to severe traumatic brain injury Archives of Physical Medicine and Rehabilitation 89 2008 S35 S44 19081440
48. Obenaus A., Robbins M., Blanco G., Galloway N.R., Snissarenko E., and Gillard E. Multi-modal magnetic resonance imaging alterations in two rat models of mild neurotrauma Journal of Neurotrauma 24 2007 1147 1160 10.1089/neu.2006.0211 17610354 (Pubitemid 47106288)
49. Ozturk A., Sasson A.D., Farrell J.A.D., Landman B.A., da Motta A.C.B.S., and Aralasmak A. Regional differences in diffusion tensor imaging measurements: assessment of intrarater and interrater variability AJNR. American Journal of Neuroradiology 29 2008 1124 1127 10.3174/ajnr.A0998 18356471 (Pubitemid 351954879)
50. Primus E.A., Bigler E.D., Anderson C.V., Johnson S.C., Mueller R.M., and Blatter D. Corpus striatum and traumatic brain injury Brain Injury: [BI] 11 1997 577 586 10.1080/026990597123278 9251866 (Pubitemid 27344736)
51. Rodriguez-Paez A.C., Brunschwig J.P., and Bramlett H.M. Light and electron microscopic assessment of progressive atrophy following moderate traumatic brain injury in the rat Acta Neuropathologica 109 2005 603 616 10.1007/s00401-005-1010-z 15877231 (Pubitemid 40974150)
52. Ross D Review of longitudinal studies of MRI brain volumetry in patients with traumatic brain injury Brain Injury: [BI] 25 2011 1271 1278 10.3109/02699052.2011.624568 22077533
53. Salmond C.H., Chatfield D.A., Menon D.K., Pickard J.D., and Sahakian B.J. Cognitive sequelae of head injury: involvement of basal forebrain and associated structures Brain: a Journal of Neurology 128 2005 189 200 15548553 (Pubitemid 40070532)
54. Sato M., Chang E., Igarashi T., and Noble L.J. Neuronal injury and loss after traumatic brain injury: time course and regional variability Brain Research 917 2001 45 54 10.1016/S0006-8993(01)02905-5 11602228 (Pubitemid 32972128)
55. Scheff S.W., Price D.A., Hicks R.R., Baldwin S.A., Robinson S., and Brackney C. Synaptogenesis in the hippocampal CA1 field following traumatic brain injury Journal of Neurotrauma 22 2005 719 732 10.1089/neu.2005.22.719 16004576 (Pubitemid 40995305)
56. Sidaros A., Skimminge A., Liptrot M.G., Sidaros K., Engberg A.W., and Herning M. Long-term global and regional brain volume changes following severe traumatic brain injury: a longitudinal study with clinical correlates Neuroimage 44 2009 1 8 10.1016/j.neuroimage.2008.08.030 18804539
57. Skandsen T., Kvistad K.A., Solheim O., Strand I.H., Folvik M., and Vik A. Prevalence and impact of diffuse axonal injury in patients with moderate and severe head injury: a cohort study of early magnetic resonance imaging findings and 1-year outcome Journal of Neurosurgery 113 2010 556 563 10.3171/2009.9. JNS09626 19852541
58. Smith D.H., Chen X.-H., Pierce J.E.S., Wolf J.A., Trojanowski J.Q., and Graham D.I. Progressive atrophy and neuron death for one year following brain trauma in the Rat Journal of Neurotrauma 14 1997 715 727 10.1089/neu.1997.14.715 9383090 (Pubitemid 27479412)
59. Squire L.R., Stark C.E.L., and Clark R.E. The medial temporal lobe Annual Review of Neuroscience 27 2004 279 306 10.1146/annurev.neuro.27.070203.144130 15217334 (Pubitemid 39050405)
60. Stein S.C., and Spettell C. The Head Injury Severity Scale (HISS): a practical classification of closed-head injury Brain Injury: [BI] 9 1995 437 444 10.3109/02699059509008203 7550215
61. Thompson P.M., Hayashi K.M., De Zubicaray G.I., Janke A.L., Rose S.E., and Semple J. Mapping hippocampal and ventricular change in Alzheimer disease Neuroimage 22 2004 1754 1766 10.1016/j.neuroimage.2004.03.040 15275931 (Pubitemid 38962663)
62. Tong W., Igarashi T., Ferriero D.M., and Noble L.J. Traumatic brain injury in the immature mouse brain: characterization of regional vulnerability Experimental Neurology 176 2002 105 116 10.1006/exnr.2002.7941 12093087 (Pubitemid 34762110)
63. Trivedi M.A., Ward M.A., Hess T.M., Gale S.D., Dempsey R.J., and Rowley H.A. Longitudinal changes in global brain volume between 79 and 409 days after traumatic brain injury: relationship with duration of coma Journal of Neurotrauma 24 2007 766 771 10.1089/neu.2006.0205 17518532 (Pubitemid 46799269)
64. Van Putten H.P., Bouwhuis M.G., Muizelaar J.P., and Lyeth B.G. Diffusion-weighted imaging of edema following traumatic brain injury in rats: effects of secondary hypoxia Journal of Neurotrauma 22 2005 857 872 10.1089/neu.2005.22.857 16083353 (Pubitemid 41153871)
65. Vargas M.E., and Barres B.A. Why is Wallerian degeneration in the CNS so slow? Annual Review of Neuroscience 30 2007 153 179 10.1146/annurev.neuro.30. 051606.094354 17506644 (Pubitemid 47218754)
66. Warner M.A., Marquez de la Plata C., Spence J., Wang J.Y., Harper C., and Moore C. Assessing spatial relationships between axonal integrity, regional brain volumes, and neuropsychological outcomes after traumatic axonal injury Journal of Neurotrauma 27 2010 2121 2130 10.1089/neu.2010.1429 20874032
67. Warner M.A., Youn T.S., Davis T., Chandra A., Marquez de la Plata C., and Moore C. Regionally selective atrophy after traumatic axonal injury Archives of Neurology 67 2010 1336 1344 20625067
68. Watanabe M., Sakai O., Ozonoff A., Kussman S., and Jara H. Age-related apparent diffusion coefficient changes in the normal brain Radiology 266 2013 575 582 10.1148/radiol.12112420 23143020
69. White N.S., Leergaard T.B., D'Arceuil H., Bjaalie J.G., and Dale A.M. Probing tissue microstructure with restriction spectrum imaging: histological and theoretical validation Human Brain Mapping 34 2013 327 346 10.1002/hbm.21454 23169482
70. Wilde E.A., Bigler E.D., Hunter J.V., Fearing M.A., Scheibel R.S., and Newsome M.R. Hippocampus, amygdala, and basal ganglia morphometrics in children after moderate-to-severe traumatic brain injury Developmental Medicine and Child Neurology 49 2007 294 299 10.1111/j.1469-8749.2007.00294.x 17376141 (Pubitemid 46477255)
71. Williams S., Raghupathi R., Mcintosh M.M.T.K., Saatman K.E., and Graham D.I. In situ DNA fragmentation occurs in white matter up to 12 months after head injury in man Acta Neuropathologica 102 2001 581 590 11761718 (Pubitemid 33061788)
72. Woodcock T., and Morganti-Kossmann M.C. The role of markers of inflammation in traumatic brain injury Frontiers in Neurology 4 2013 18 23459929
73. Wu H.-M., Huang S.-C., Hattori N., Glenn T.C., Vespa P.M., and Yu C.-L. Selective metabolic reduction in gray matter acutely following human traumatic brain injury Journal of Neurotrauma 21 2004 149 161 10.1089/089771504322778613 15000756 (Pubitemid 38233845)
74. Yuh E.L., Cooper S.R., Ferguson A.R., and Manley G.T. Quantitative CT improves outcome prediction in acute traumatic brain injury Journal of Neurotrauma 29 2012 735 746 10.1089/neu.2011.2008 21970562