Diffusion tensor imaging in the corpus callosum in children after moderate to severe traumatic brain injury.

Diffusion tensor imaging (DTI) is a recent imaging technique that assesses the microstructure of the cerebral white matter (WM) based on anisotropic diffusion (i.e., water molecules move faster in parallel to nerve fibers than perpendicular to them). Fractional anisotropy (FA), which ranges from 0 to 1.0, increases with myelination of WM tracts and is sensitive to diffuse axonal injury (DAI) in adults with traumatic brain injury (TBI). However, previous DTI studies of pediatric TBI were case reports without detailed outcome measures. Using mean FA derived from DTI fiber tractography, we compared DTI findings of the corpus callosum for 16 children who were at least 1 year (mean 3.1 years) post-severe TBI and individually matched, uninjured children. Interexaminer and intraexaminer reliability in measuring FA was satisfactory. FA was significantly lower in the patients for the genu, body, and splenium of the corpus callosum. Higher FA was related to increased cognitive processing speed and faster interference resolution on an inhibition task. In the TBI patients, higher FA was related to better functional outcome as measured by the dichotomized Glasgow Outcome Scale (GOS). FA also increased as a function of the area of specific regions of the corpus callosum such as the genu and splenium, and FA in the splenium was reduced with greater volume of lesions in this region. DTI may be useful in identifying biomarkers related to DAI and outcome of TBI in children.

[1]  H. Levin,et al.  Selective Impairment of Inhibition After TBI in Children , 2004 .

[2]  H. Levin,et al.  Brain Activation during Working Memory after Traumatic Brain Injury in Children , 2007, Neurocase.

[3]  T. Gennarelli.  The Pathobiology of Traumatic Brain Injury , 1997 .

[4]  J. Pickard,et al.  Neuroimaging in trauma , 2007, Current opinion in neurology.

[5]  R. Kail,et al.  Processing time decreases globally at an exponential rate during childhood and adolescence. , 1993, Journal of experimental child psychology.

[6]  B. Jennett,et al.  ASSESSMENT OF OUTCOME AFTER SEVERE BRAIN DAMAGE A Practical Scale , 1975, The Lancet.

[7]  S. Hale,et al.  Processing Speed, Working Memory, and Fluid Intelligence: Evidence for a Developmental Cascade , 1996 .

[8]  J Brown,et al.  Extent and distribution of vascular brain injury in pediatric road fatalities. , 2001, Journal of neurotrauma.

[9]  B. Thompson,et al.  MR imaging of head trauma: review of the distribution and radiopathologic features of traumatic lesions. , 1988, AJR. American journal of roentgenology.

[10]  J. Gabrieli,et al.  Immature Frontal Lobe Contributions to Cognitive Control in Children Evidence from fMRI , 2002, Neuron.

[11]  H S Levin,et al.  Reduction of corpus callosum growth after severe traumatic brain injury in children , 2000, Neurology.

[12]  S. Pollmann,et al.  Splenial lesions lead to supramodal target detection deficits. , 2004, Neuropsychology.

[13]  E. Bigler,et al.  The role of caudate nucleus and corpus callosum atrophy in trauma-induced anterior horn dilation. , 1994, Brain injury.

[14]  J. Fletcher,et al.  Corpus Callosum Damage and InterhemispherIc Transfer of Information following Closed Head Injury in Children , 1999, Cortex.

[15]  J. Povlishock,et al.  Traumatically induced altered membrane permeability: its relationship to traumatically induced reactive axonal change. , 1994, Journal of neurotrauma.

[16]  H. Petropoulos,et al.  Metabolic and cognitive response to human traumatic brain injury: a quantitative proton magnetic resonance study. , 2000, Journal of neurotrauma.

[17]  Erin D Bigler,et al.  Neuropsychology and clinical neuroscience of persistent post-concussive syndrome , 2007, Journal of the International Neuropsychological Society.

[18]  C. Eriksen,et al.  Effects of noise letters upon the identification of a target letter in a nonsearch task , 1974 .

[19]  S. Jang,et al.  Diffusion tensor magnetic resonance imaging of microstructural abnormalities in children with brain injury. , 2003, American journal of physical medicine & rehabilitation.

[20]  G. Johnson,et al.  Diffuse axonal injury in mild traumatic brain injury: a diffusion tensor imaging study. , 2005, Journal of neurosurgery.

[21]  Andrew Blamire,et al.  Increase in apparent diffusion coefficient in normal appearing white matter following human traumatic brain injury correlates with injury severity. , 2004, Journal of neurotrauma.

[22]  S. F. Witelson.  Hand and sex differences in the isthmus and genu of the human corpus callosum. A postmortem morphological study. , 1989, Brain : a journal of neurology.

[23]  D Yves von Cramon,et al.  Diffuse axonal injury associated with chronic traumatic brain injury: evidence from T2*-weighted gradient-echo imaging at 3 T. , 2003, AJNR. American journal of neuroradiology.

[24]  B Jennett,et al.  Assessment of outcome after severe brain damage. , 1975, Lancet.

[25]  Michael S. Gazzaniga,et al.  Functional Connectivity: Integrating Behavioral, Diffusion Tensor Imaging, and Functional Magnetic Resonance Imaging Data Sets , 2005, Journal of Cognitive Neuroscience.

[26]  B. Sahakian,et al.  Head Circumference and Brain and Hippocampal Volume after Severe Traumatic Brain Injury in Childhood , 2005, Pediatric Research.

[27]  G J Barker,et al.  Diffusion imaging shows abnormalities after blunt head trauma when conventional magnetic resonance imaging is normal , 2001, Journal of neurology, neurosurgery, and psychiatry.

[28]  Harvey S. Levin,et al.  Late MRI after head injury in children: relationship to clinical features and outcome , 1992, Child's Nervous System.

[29]  R. Poldrack,et al.  Neural Activation During Response Competition , 2000, Journal of Cognitive Neuroscience.

[30]  S. Wakana,et al.  MRI Atlas of Human White Matter , 2005 .

[31]  J. Adams,et al.  Diffuse axonal injury and traumatic coma in the primate , 1982, Annals of neurology.

[32]  Claudia Pedroza,et al.  Frontal and temporal morphometric findings on MRI in children after moderate to severe traumatic brain injury. , 2005, Journal of neurotrauma.

[33]  Bart Rypma,et al.  Prefrontal modulation of working memory performance in brain injury and disease , 2006, Human brain mapping.

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

[35]  T. Tsuzuki,et al.  Semiquantitative analysis of corpus callosum injury using magnetic resonance imaging indicates clinical severity in patients with diffuse axonal injury , 2002, Journal of neurology, neurosurgery, and psychiatry.

[36]  A. Scheibel,et al.  Fiber composition of the human corpus callosum , 1992, Brain Research.

[37]  H. Moser,et al.  Imaging cortical association tracts in the human brain using diffusion‐tensor‐based axonal tracking , 2002, Magnetic resonance in medicine.

[38]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[39]  S. Wakana,et al.  Fiber tract-based atlas of human white matter anatomy. , 2004, Radiology.

[40]  K. Hasan,et al.  Diffusion tensor fractional anisotropy of the normal‐appearing seven segments of the corpus callosum in healthy adults and relapsing‐remitting multiple sclerosis patients , 2005, Journal of magnetic resonance imaging : JMRI.

[41]  D D Blatter,et al.  Nonspecific white matter degeneration following traumatic brain injury , 1995, Journal of the International Neuropsychological Society.

[42]  Pratik Mukherjee,et al.  Diffusion Tensor Imaging with Three-dimensional Fiber Tractography of Traumatic Axonal Shearing Injury: An Imaging Correlate for the Posterior Callosal “Disconnection” Syndrome: Case Report , 2005, Neurosurgery.

[43]  Erin D Bigler,et al.  Macrocephaly, Corpus Callosum Morphology, and Autism , 2005, Journal of child neurology.

[44]  E. Sullivan,et al.  Corpus callosal microstructural integrity influences interhemispheric processing: a diffusion tensor imaging study. , 2005, Cerebral cortex.

[45]  J R Moeller,et al.  Regional cerebral blood flow in mood disorders. I. Comparison of major depressives and normal controls at rest. , 1990, Archives of general psychiatry.

[46]  B. Jennett,et al.  Assessment of coma and impaired consciousness. A practical scale. , 1974, Lancet.

[47]  P. Karunanayaka,et al.  Diffusion Tensor MR Imaging Reveals Persistent White Matter Alteration after Traumatic Brain Injury Experienced during Early Childhood , 2007, American Journal of Neuroradiology.

[48]  P. Basser,et al.  Toward a quantitative assessment of diffusion anisotropy , 1996, Magnetic resonance in medicine.

[49]  Lemlih Ouchchane,et al.  Brain mapping in stereotactic surgery: A brief overview from the probabilistic targeting to the patient-based anatomic mapping , 2007, NeuroImage.

[50]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[51]  H. Levin,et al.  Corpus callosum lesions after closed head injury in children: MRI, clinical features and outcome , 2004, Neuroradiology.

[52]  Susumu Mori,et al.  Fiber tracking: principles and strategies – a technical review , 2002, NMR in biomedicine.

[53]  J. Adams,et al.  Brain damage in fatal non-missile head injury. , 1978, Journal of clinical pathology.

[54]  D. Le Bihan,et al.  Diffusion tensor imaging: Concepts and applications , 2001, Journal of magnetic resonance imaging : JMRI.

[55]  Scott A. Huettel,et al.  Diffusion tensor imaging of adult age differences in cerebral white matter: relation to response time , 2004, NeuroImage.

[56]  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.

[57]  Jürgen Weese,et al.  Towards real-time multi-modality 3-D medical image registration , 2001, Proceedings Eighth IEEE International Conference on Computer Vision. ICCV 2001.

[58]  M S Grady,et al.  Ultrastructural studies of diffuse axonal injury in humans. , 1994, Journal of neurotrauma.

[59]  Nancy K. Rollins,et al.  Clinical applications of diffusion tensor imaging and tractography in children , 2007, Pediatric Radiology.

[60]  René Westerhausen,et al.  Effects of handedness and gender on macro- and microstructure of the corpus callosum and its subregions: a combined high-resolution and diffusion-tensor MRI study. , 2004, Brain research. Cognitive brain research.

[61]  이종욱,et al.  Abbreviated Injury Scale 및 Injury severity Score분류에 의한 새로운 외상환자 표시법 , 1989 .

[62]  A. Pfefferbaum,et al.  Replicability of diffusion tensor imaging measurements of fractional anisotropy and trace in brain , 2003, Journal of magnetic resonance imaging : JMRI.

[63]  P. Fillard,et al.  Brain MR diffusion tensor imaging and fibre tracking to differentiate between two diffuse axonal injuries , 2005, Neuroradiology.

[64]  P. Basser,et al.  Statistical artifacts in diffusion tensor MRI (DT‐MRI) caused by background noise , 2000, Magnetic resonance in medicine.

[65]  Joseph A Maldjian,et al.  Diffusion anisotropy in the corpus callosum. , 2002, AJNR. American journal of neuroradiology.

[66]  T. Higuchi,et al.  Regional cerebral blood flow in mood disorders , 1997 .

[67]  J. Gerberding,et al.  Morbidity and Mortality Weekly Report Traumatic Brain Injury-related Hospital Discharges Results from a 14-state Surveillance System, 1997 Centers for Disease Control and Prevention Epidemiology Program Office Division of Public Health Surveillance and Informatics Lead Technical Writer/editor Vol. 5 , 2022 .

[68]  Emmanuel Strypstein,et al.  Dual Task Performance after Severe Diffuse Traumatic Brain Injury or Vascular Prefrontal Damage , 2000, Journal of clinical and experimental neuropsychology.

[69]  G. Pearlson,et al.  Diffusion Tensor Imaging and Axonal Tracking in the Human Brainstem , 2001, NeuroImage.

[70]  V. Haughton,et al.  Diffusion tensor MR imaging in diffuse axonal injury. , 2002, AJNR. American journal of neuroradiology.

[71]  D D Blatter,et al.  Quantitative volumetric analysis of brain MR: normative database spanning 5 decades of life. , 1995, AJNR. American journal of neuroradiology.

[72]  W. Peh,et al.  Diffuse axonal injury: detection of changes in anisotropy of water diffusion by diffusion-weighted imaging , 2002, Neuroradiology.

[73]  E. Bigler,et al.  Neuropsychological and Information Processing Performance and Its Relationship to White Matter Changes Following Moderate and Severe Traumatic Brain Injury: A Preliminary Study , 2004, Applied neuropsychology.

[74]  O. Abe,et al.  MR diffusion tensor imaging: recent advance and new techniques for diffusion tensor visualization. , 2003, European journal of radiology.

[75]  H. Eisenberg,et al.  Corpus callosal atrophy following closed head injury: detection with magnetic resonance imaging. , 1990, Journal of neurosurgery.

[76]  J. Povlishock,et al.  The pathobiology of traumatically induced axonal injury in animals and humans: a review of current thoughts. , 1995, Journal of neurotrauma.

[77]  Takeo Ishigaki,et al.  Serial evaluation of diffusion tensor brain fiber tracking in a patient with severe diffuse axonal injury. , 2004, AJNR. American journal of neuroradiology.

[78]  A. Sorensen,et al.  Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. , 2004, AJNR. American journal of neuroradiology.

[79]  Grace Scott,et al.  Diffuse axonal injury due to nonmissile head injury in humans: An analysis of 45 cases , 1982, Annals of neurology.

[80]  P Hemyari,et al.  Brain injuries among infants, children, adolescents, and young adults. , 1990, American journal of diseases of children.

[81]  Roland G Henry,et al.  DTI‐based three‐dimensional tractography detects differences in the pyramidal tracts of infants and children with congenital hemiparesis , 2003, Journal of magnetic resonance imaging : JMRI.