Quantitative MRI analysis of brain volume changes due to controlled cortical impact.

More than 85% of reported brain traumas are classified clinically as "mild" using the Glasgow Coma Scale (GCS); qualitative MRI findings are scarce and provide little correspondence to clinical symptoms. Our goal, therefore, was to establish in vivo sequelae of traumatic brain injury (TBI) following lower and higher levels of impact to the frontal lobe using quantitative MRI analysis and a mechanical model of penetrating impact injury. To investigate time-based morphological and physiological changes of living tissue requires a surrogate for the human central nervous system. The present model for TBI was a systematically varied and controlled cortical impact on deeply-anaesthetized Sprague-Dawley rats, that was designed to mimic different injury severities. Whole-brain MRI scans were performed on each rat prior to either a lower- or a higher-level of impact, and then at hourly intervals for 5 h post-impact. Both brain volume and specific anatomical structures were segmented from MR images for inter-subject comparisons post-registration. Animals subjected to lower and higher impact levels exhibited elevated intracranial pressure (ICP) in the low compensatory reserve (i.e., nearly exhausted), and terminal disturbance (i.e., exhausted) ranges, respectively. There was a statistically significant drop in cerebrospinal fluid (CSF) of 35% in the lower impacts, and 65% in the higher impacts, at 5 h compared to sham controls. There was a corresponding increase in corpus callosum volume starting at 1 h, of 60-110% and 30-40% following the lower- and higher-impact levels, respectively. A statistically significant change in the abnormal tissue from 2 h to 5 h was observed for both impact levels, with greater significance for higher impacts. Furthermore, a statistically significant difference between the lower impacts and the sham controls occurred at 3 h. These results are statistically substantiated by a fluctuation in the physical size of the corpus callosum, a decrease in the volume of CSF, and elevated levels of atrophy in the cerebral cortex.

[1]  P. Biberfeld,et al.  Intracerebral inflammation after human brain contusion. , 1998, Neurosurgery.

[2]  P. Kochanek,et al.  One-year study of spatial memory performance, brain morphology, and cholinergic markers after moderate controlled cortical impact in rats. , 1999, Journal of neurotrauma.

[3]  M. Maier.  Quantitative MRI of the brain—measuring changes caused by disease , 2004 .

[4]  B. Podolsky,et al.  The mechanism of the change in cerebrospinal fluid pressure following an induced change in the volume of the fluid space. , 1953, The Journal of laboratory and clinical medicine.

[5]  R. Moghrabi.  Intracranial pressure. , 1982, Middle East journal of anaesthesiology.

[6]  S. Chaudhury,et al.  Neuropsychiatric Sequelae of Head Injury , 2005, Indian Journal of Neurotrauma.

[7]  L. Steiner,et al.  Monitoring the injured brain: ICP and CBF. , 2006, British journal of anaesthesia.

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

[9]  A. Gefen,et al.  Age-dependent changes in material properties of the brain and braincase of the rat. , 2003, Journal of neurotrauma.

[10]  J. Ponsford,et al.  Impact of early intervention on outcome following mild head injury in adults , 2002, Journal of neurology, neurosurgery, and psychiatry.

[11]  J. Löfgren,et al.  THE PRESSURE‐VOLUME CURVE OF THE CEREBROSPINAL FLUID SPACE IN DOGS , 1973, Acta neurologica Scandinavica.

[12]  A S Morgan,et al.  Early intervention in severe head injury: long-term benefits of a formalized program. , 1992, Archives of physical medicine and rehabilitation.

[13]  E. Hall,et al.  Evolution of post-traumatic neurodegeneration after controlled cortical impact traumatic brain injury in mice and rats as assessed by the de Olmos silver and fluorojade staining methods. , 2008, Journal of neurotrauma.

[14]  J Q Trojanowski,et al.  Progressive atrophy and neuron death for one year following brain trauma in the rat. , 1997, Journal of neurotrauma.

[15]  F. Tortella,et al.  Penetrating ballistic-like brain injury in the rat: differential time courses of hemorrhage, cell death, inflammation, and remote degeneration. , 2006, Journal of neurotrauma.

[16]  Julie M Boiren,et al.  Childhood traumatic brain injury: neuropsychological status at the time of hospital discharge , 1997, Developmental medicine and child neurology.

[17]  D. McArthur,et al.  Epidemiologic aspects of brain injury. , 1996, Neurologic clinics.

[18]  D.L. Wilson,et al.  Entropy based method to correct intensity inhomogeneity in MR images , 2004, The 26th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[19]  D. Marion,et al.  Early Glasgow Outcome Scale scores predict long-term functional outcome in patients with severe traumatic brain injury. , 2005, Journal of neurotrauma.

[20]  Jamshid Dehmeshki,et al.  Histograms: measuring subtle diffuse disease , 2003 .

[21]  A. Manduca,et al.  Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. , 1995, Science.

[22]  T. McAllister,et al.  Neuropsychiatric sequelae of head injuries. , 1992, The Psychiatric clinics of North America.

[23]  C. Robertson,et al.  Lateral cortical impact injury in rats: cerebrovascular effects of varying depth of cortical deformation and impact velocity. , 1994, Journal of Neurotrauma.

[24]  Paul R. Sanberg,et al.  Severity of controlled cortical impact traumatic brain injury in rats and mice dictates degree of behavioral deficits , 2009, Brain Research.

[25]  A. V. Zomeren,et al.  Residual complaints of patients two years after severe head injury. , 1985, Journal of neurology, neurosurgery, and psychiatry.

[26]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[27]  U. Ungerstedt,et al.  Changes in Cortical Extracellular Levels of Energy-Related Metabolites and Amino Acids following Concussive Brain Injury in Rats , 1990, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[28]  B. Giordani,et al.  Neuropsychological sequelae of minor head injury. , 1983, Neurosurgery.

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

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

[31]  A. Murphy,et al.  A national census of ambulance response times to emergency calls in Ireland , 2000, Journal of accident & emergency medicine.

[32]  D. Cope,et al.  Head injury rehabilitation: benefit of early intervention. , 1982, Archives of physical medicine and rehabilitation.

[33]  S. Sorenson,et al.  Occurrence, severity, and outcomes of brain injury , 1991 .

[34]  K. Taber,et al.  Traumatic axonal injury: novel insights into evolution and identification. , 2004, The Journal of neuropsychiatry and clinical neurosciences.

[35]  D. Graham,et al.  Tissue tears in the white matter after lateral fluid percussion brain injury in the rat: relevance to human brain injury , 2000, Acta Neuropathologica.

[36]  J. Trojanowski,et al.  Experimental Brain Injury Induces Regionally Distinct Apoptosis during the Acute and Delayed Post-Traumatic Period , 1998, The Journal of Neuroscience.

[37]  F. Sklar,et al.  The pressure-volume function of brain elasticity. Physiological considerations and clinical applications. , 1977, Journal of neurosurgery.

[38]  E. Bigler,et al.  Quantitative magnetic resonance imaging in traumatic brain injury. , 2001, The Journal of head trauma rehabilitation.

[39]  H. Rusinek,et al.  Proton MR spectroscopy and MRI-volumetry in mild traumatic brain injury. , 2007, AJNR. American journal of neuroradiology.

[40]  D. Stein,et al.  Unilateral cortical contusion injury in the rat: vascular disruption and temporal development of cortical necrosis. , 1993, Journal of neurotrauma.

[41]  B. Jennett,et al.  Assessment and prognosis of coma after head injury , 2005, Acta Neurochirurgica.

[42]  T. Nagaoka,et al.  Experimental ischemic brain edema: morphological and magnetic resonance imaging findings. , 2007, Neurosurgical focus.

[43]  Sung C. Choi,et al.  Impact of ICP instability and hypotension on outcome in patients with severe head trauma , 1991 .

[44]  Ronald L. Hayes,et al.  A controlled cortical impact model of traumatic brain injury in the rat , 1991, Journal of Neuroscience Methods.

[45]  G. Timberlake,et al.  Medical complications of head injury. , 1993, The Medical clinics of North America.

[46]  R. Hamm,et al.  Cognitive Impairment following Traumatic Brain Injury , 2006 .

[47]  A. Marmarou,et al.  Compartmental analysis of compliance and outflow resistance of the cerebrospinal fluid system. , 1975, Journal of neurosurgery.

[48]  Grant L Iverson,et al.  Outcome from mild traumatic brain injury , 2005, Current opinion in psychiatry.

[49]  J. Szewczykowski,et al.  A fast method of estimating the elastance of the intracranial system. , 1977, Journal of neurosurgery.

[50]  Michael D. Gilchrist,et al.  Experimental Device for Simulating Traumatic Brain Injury Resulting from Linear Accelerations , 2004 .

[51]  P. Dash,et al.  Delayed, selective neuronal death following experimental cortical impact injury in rats: possible role in memory deficits , 1996, Brain Research.

[52]  R Bowtell,et al.  Mapping the absolute value of M0 using dipolar field effects , 2002, Magnetic resonance in medicine.

[53]  R. Douglas,et al.  Effect of general anaesthesia on the magnetic resonance imaging signal from the brain. , 1989, British journal of anaesthesia.

[54]  A. V. Zomeren,et al.  Residual complaints of patients two years after severe head injury. , 1985 .

[55]  D. Meaney,et al.  Axonal Damage in Traumatic Brain Injury , 2000 .

[56]  G. Citerio,et al.  Intracranial pressure , 2004, Intensive Care Medicine.

[57]  Helen M. Bramlett,et al.  Quantitative structural changes in white and gray matter 1 year following traumatic brain injury in rats , 2002, Acta Neuropathologica.