Regionally selective atrophy after traumatic axonal injury.

OBJECTIVES To determine the spatial distribution of cortical and subcortical volume loss in patients with diffuse traumatic axonal injury and to assess the relationship between regional atrophy and functional outcome. DESIGN Prospective imaging study. Longitudinal changes in global and regional brain volumes were assessed using high-resolution magnetic resonance imaging-based morphometric analysis. SETTING Inpatient traumatic brain injury unit. PATIENTS OR OTHER PARTICIPANTS Twenty-five patients with diffuse traumatic axonal injury and 22 age- and sex-matched controls. MAIN OUTCOME MEASURE Changes in global and regional brain volumes between initial and follow-up magnetic resonance imaging were used to assess the spatial distribution of posttraumatic volume loss. The Glasgow Outcome Scale-Extended score was the primary measure of functional outcome. RESULTS Patients underwent substantial global atrophy with mean whole-brain parenchymal volume loss of 4.5% (95% confidence interval, 2.7%-6.3%). Decreases in volume (at a false discovery rate of 0.05) were seen in several brain regions including the amygdala, hippocampus, thalamus, corpus callosum, putamen, precuneus, postcentral gyrus, paracentral lobule, and parietal and frontal cortices, while other regions such as the caudate and inferior temporal cortex were relatively resistant to atrophy. Loss of whole-brain parenchymal volume was predictive of long-term disability, as was atrophy of particular brain regions including the inferior parietal cortex, pars orbitalis, pericalcarine cortex, and supramarginal gyrus. CONCLUSION Traumatic axonal injury leads to substantial posttraumatic atrophy that is regionally selective rather than diffuse, and volume loss in certain regions may have prognostic value for functional recovery.

[1]  E. Halgren,et al.  Subcortical and cerebellar atrophy in mesial temporal lobe epilepsy revealed by automatic segmentation , 2008, Epilepsy Research.

[2]  T. Jernigan,et al.  Diffusion tensor imaging during recovery from severe traumatic brain injury and relation to clinical outcome: a longitudinal study. , 2008, Brain : a journal of neurology.

[3]  Benjamin J. Shannon,et al.  Molecular, Structural, and Functional Characterization of Alzheimer's Disease: Evidence for a Relationship between Default Activity, Amyloid, and Memory , 2005, The Journal of Neuroscience.

[4]  D. Katz,et al.  Update of Neuropathology and Neurological Recovery After Traumatic Brain Injury , 2005, The Journal of head trauma rehabilitation.

[5]  M. Wald,et al.  Traumatic brain injury in the United States; emergency department visits, hospitalizations, and deaths, 2002-2006 , 2010 .

[6]  Hidenao Fukuyama,et al.  Comparison of the pattern of atrophy of the corpus callosum in frontotemporal dementia, progressive supranuclear palsy, and Alzheimer's disease , 2000, Journal of neurology, neurosurgery, and psychiatry.

[7]  Andrew J. Saykin,et al.  Regionally specific atrophy of the corpus callosum in AD, MCI and cognitive complaints , 2006, Neurobiology of Aging.

[8]  Guy B. Williams,et al.  Comparative Reliability of Total Intracranial Volume Estimation Methods and the Influence of Atrophy in a Longitudinal Semantic Dementia Cohort , 2009, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[9]  R. Mccoll,et al.  Cerebral atrophy after traumatic white matter injury: correlation with acute neuroimaging and outcome. , 2008, Journal of neurotrauma.

[10]  J. C. Pruessner,et al.  Comprehensive dissection of the medial temporal lobe in AD: measurement of hippocampus, amygdala, entorhinal, perirhinal and parahippocampal cortices using MRI , 2006, Journal of Neurology.

[11]  Juan Sahuquillo,et al.  Hippocampal head atrophy after traumatic brain injury , 2006, Neuropsychologia.

[12]  Eui-Cheol Nam,et al.  Validation of hippocampal volumes measured using a manual method and two automated methods (FreeSurfer and IBASPM) in chronic major depressive disorder , 2008, Neuroradiology.

[13]  Erin D Bigler,et al.  Diffuse changes in cortical thickness in pediatric moderate-to-severe traumatic brain injury. , 2008, Journal of neurotrauma.

[14]  E. Bigler,et al.  MR-based brain and cerebrospinal fluid measurement after traumatic brain injury: correlation with neuropsychological outcome. , 1997, AJNR. American journal of neuroradiology.

[15]  D. Graham,et al.  Stereology of cerebral cortex after traumatic brain injury matched to the Glasgow outcome score. , 2010, Brain : a journal of neurology.

[16]  André J. W. van der Kouwe,et al.  Brain morphometry with multiecho MPRAGE , 2008, NeuroImage.

[17]  Tomás Paus,et al.  Changes in white matter in long-term survivors of severe non-missile traumatic brain injury: a computational analysis of magnetic resonance images. , 2005, Journal of neurotrauma.

[18]  G. Alexander,et al.  Regional pattern of hippocampus and corpus callosum atrophy in Alzheimer’s disease in relation to dementia severity: evidence for early neocortical degeneration , 2003, Neurobiology of Aging.

[19]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[20]  C Caltagirone,et al.  Gross morphology and morphometric sequelae in the hippocampus, fornix, and corpus callosum of patients with severe non-missile traumatic brain injury without macroscopically detectable lesions: a T1 weighted MRI study , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[21]  L. Baxter,et al.  Traumatic brain injury and grey matter concentration: a preliminary voxel based morphometry study , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[22]  Harald Hampel,et al.  Progression of corpus callosum atrophy in Alzheimer disease. , 2002, Archives of neurology.

[23]  Sterling C. Johnson,et al.  Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging , 2008, NeuroImage.

[24]  S. Morikawa,et al.  Different Atrophic Patterns in Early- and Late-Onset Alzheimer’s Disease and Evaluation of Clinical Utility of a Method of Regional z-Score Analysis Using Voxel-Based Morphometry , 2008, Dementia and Geriatric Cognitive Disorders.

[25]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[26]  J. Langlois,et al.  Traumatic brain injury in the United States; emergency department visits, hospitalizations, and deaths , 2006 .

[27]  Christopher J. A. Cowie,et al.  Quantitative magnetic resonance imaging in traumatic brain injury , 2012 .

[28]  A. Dale,et al.  Subregional neuroanatomical change as a biomarker for Alzheimer's disease , 2009, Proceedings of the National Academy of Sciences.

[29]  Massimo Filippi,et al.  Apolipoprotein E ε4 is associated with disease-specific effects on brain atrophy in Alzheimer's disease and frontotemporal dementia , 2009, Proceedings of the National Academy of Sciences.

[30]  J D Pickard,et al.  Cognitive sequelae of head injury: involvement of basal forebrain and associated structures. , 2004, Brain : a journal of neurology.

[31]  Nick C Fox,et al.  Mapping the evolution of regional atrophy in Alzheimer's disease: Unbiased analysis of fluid-registered serial MRI , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Christopher H. van Dyck,et al.  Volumetry of amygdala and hippocampus and memory performance in Alzheimer's disease , 2006, Psychiatry Research: Neuroimaging.

[33]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Egill Rostrup,et al.  Long-term global and regional brain volume changes following severe traumatic brain injury: A longitudinal study with clinical correlates , 2009, NeuroImage.

[35]  Brian B. Avants,et al.  Structural consequences of diffuse traumatic brain injury: A large deformation tensor-based morphometry study , 2008, NeuroImage.

[36]  Sterling C. Johnson,et al.  Longitudinal changes in global brain volume between 79 and 409 days after traumatic brain injury: relationship with duration of coma. , 2007, Journal of neurotrauma.

[37]  E. Bigler,et al.  Day-of-Injury Computerized Tomography, Rehabilitation Status, and Development of Cerebral Atrophy in Persons with Traumatic Brain Injury , 2006, American journal of physical medicine & rehabilitation.

[38]  James S Babb,et al.  Brain atrophy in mild or moderate traumatic brain injury: a longitudinal quantitative analysis. , 2002, AJNR. American journal of neuroradiology.

[39]  D. McArthur,et al.  Early Nonischemic Oxidative Metabolic Dysfunction Leads to Chronic Brain Atrophy in Traumatic Brain Injury , 2010, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.