Utility of Magnetic Resonance Findings in Elucidating Structural and Functional Brain Impairment in Traumatic Brain Injury

Traumatic brain injury (TBI) is a major cause of death and disability in the United States, contributing to about 30% of all injury-related deaths. TBI survivors often develop clinical impairments and long-term disabilities. These include impaired thinking or memory, effects on movement and sensations such as vision, hearing, or emotional functioning including personality changes, depression, burst of anger, abnormal social behavior, and insomnia. These issues not only affect individuals but can have a deleterious impact on families and communities. The advances in computer software applied to a non-invasive acquisition of images containing digital data, provides us with objective examination of brain structure and function. Magnetic resonance (MR) imaging of the brain makes it possible to investigate morphological and functional connectivity without exposing the patient to ionizing radiations. In patients with TBI, computed tomography and conventional MR scans seldom show limited or no abnormalities to explain clinical symptomatology. For these reasons, we propose an “ad hoc” protocol that exploits advances in MR sequences to predict long-term outcomes including evaluation of cortical thickness, detecting hemosiderin deposits via magnetic susceptibility weighted images, to explore indemnity of fiber tracts using diffusion tensor with fractional anisotropy measurement, to assess metabolic changes in the frontal lobe and cingulate cortex by utilizing the properties of magnetic resonance spectroscopy, and lastly to detect abnormal connectivity in the brain networks via resting-state functional magnetic resonance imaging. Meticulous application of our protocol can potentially detect subtle abnormalities in patients with mild TBI such as detection of iron or mineral deposits, abnormal cortical thickness, abnormal metabolites, disruption of white matter tracts, and decreased or loss connectivity in brain networks. Application of special MR sequences as described in our protocol can optimize clinical outcomes, offer predictive capabilities of short and long-term prognosis, and aid in risk-stratification tailored upon individual comorbidities.

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

[2]  G Broggi,et al.  Focal lesion of the right cingulum: a case report in a child. , 1981, Journal of neurology, neurosurgery, and psychiatry.

[3]  P. Marsh,et al.  Inhibition by the antimicrobial agent chlorhexidine of acid production and sugar transport in oral streptococcal bacteria. , 1983, Archives of oral biology.

[4]  Harvey S. Levin,et al.  Magnetic resonance imaging and computerized tomography in relation to the neurobehavioral sequelae of mild and moderate head injuries. , 1987, Journal of neurosurgery.

[5]  J. Hesselink,et al.  MR imaging of brain contusions: a comparative study with CT. , 1988, AJR. American journal of roentgenology.

[6]  W. Rothfus,et al.  Acute tissue tear hemorrhages of the brain: computed tomography and clinicopathological correlations. , 1990, Neurosurgery.

[7]  T. Sakamoto,et al.  Comparative study of magnetic resonance and CT scan imaging in cases of severe head injury. , 1992, Acta neurochirurgica. Supplementum.

[8]  T A Gennarelli,et al.  Prevalence of MR evidence of diffuse axonal injury in patients with mild head injury and normal head CT findings. , 1994, AJNR. American journal of neuroradiology.

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

[10]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[11]  E Schmutzhard,et al.  The persistent vegetative state after closed head injury: clinical and magnetic resonance imaging findings in 42 patients. , 1998, Journal of neurosurgery.

[12]  Stefan Golaszewski,et al.  Prediction of recovery from post-traumatic vegetative state with cerebral magnetic-resonance imaging , 1998, The Lancet.

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

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

[15]  F. Kruggel,et al.  Measuring the cortical thickness [MRI segmentation procedure] , 2000, Proceedings IEEE Workshop on Mathematical Methods in Biomedical Image Analysis. MMBIA-2000 (Cat. No.PR00737).

[16]  S. Ashwal,et al.  Predictive value of proton magnetic resonance spectroscopy in pediatric closed head injury. , 2000, Pediatric neurology.

[17]  A. Blamire,et al.  Early proton magnetic resonance spectroscopy in normal-appearing brain correlates with outcome in patients following traumatic brain injury. , 2000, Brain : a journal of neurology.

[18]  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.

[19]  P. Styles,et al.  How useful is magnetic resonance imaging in predicting severity and outcome in traumatic brain injury? , 2001, Current opinion in neurology.

[20]  J. Roesler,et al.  The epidemiology of pediatric traumatic brain injury in Minnesota. , 2001, Archives of pediatrics & adolescent medicine.

[21]  B Lane,et al.  Single- versus multi-detector row CT of the brain: quality assessment. , 2001, Radiology.

[22]  Jerry L. Prince,et al.  A PDE approach for measuring tissue thickness , 2001, Proceedings of the 2001 IEEE Computer Society Conference on Computer Vision and Pattern Recognition. CVPR 2001.

[23]  B Jennett,et al.  The structural basis of moderate disability after traumatic brain damage , 2001, Journal of neurology, neurosurgery, and psychiatry.

[24]  Xiao Han,et al.  Cortical surface reconstruction using a topology preserving geometric deformable model , 2001, Proceedings IEEE Workshop on Mathematical Methods in Biomedical Image Analysis (MMBIA 2001).

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

[26]  D. Hammoud,et al.  Diffuse axonal injuries: pathophysiology and imaging. , 2002, Neuroimaging clinics of North America.

[27]  A. Alavi,et al.  Neuroimaging in patients with head injury. , 2003, Seminars in nuclear medicine.

[28]  A. Rigby,et al.  Disability in young adults following major trauma: 5 year follow up of survivors , 2003, BMC public health.

[29]  Xiao Han,et al.  A Topology Preserving Level Set Method for Geometric Deformable Models , 2003, IEEE Trans. Pattern Anal. Mach. Intell..

[30]  A. Jackson,et al.  Abnormalities on magnetic resonance imaging seen acutely following mild traumatic brain injury: correlation with neuropsychological tests and delayed recovery , 2004, Neuroradiology.

[31]  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.

[32]  W. Katon,et al.  Psychiatric illness following traumatic brain injury in an adult health maintenance organization population. , 2004, Archives of general psychiatry.

[33]  M. Waugh,et al.  An Investigation of Neuronal Integrity in Severe Paediatric Traumatic Brain Injury , 2004, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

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

[35]  Benedicto Crespo-Facorro,et al.  Major depression following traumatic brain injury. , 2004, Archives of general psychiatry.

[36]  E. Kuhn,et al.  Quality of life and functional outcome after pediatric trauma. , 2005, The Journal of trauma.

[37]  Alan C. Evans,et al.  Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification , 2005, NeuroImage.

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

[39]  J. Langlois,et al.  The Incidence of Traumatic Brain Injury Among Children in the United States: Differences by Race , 2005, The Journal of head trauma rehabilitation.

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

[41]  S. Ashwal,et al.  MR spectroscopy: Predicting long‐term neuropsychological outcome following pediatric TBI , 2006, Journal of magnetic resonance imaging : JMRI.

[42]  A. Feinstein,et al.  The effect of major depression on subjective and objective cognitive deficits in mild to moderate traumatic brain injury. , 2006, The Journal of neuropsychiatry and clinical neurosciences.

[43]  J. Langlois,et al.  Incidence of Traumatic Brain Injury in the United States, 2003 , 2006, The Journal of head trauma rehabilitation.

[44]  N. Nakayama,et al.  Evidence for white matter disruption in traumatic brain injury without macroscopic lesions , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[45]  Yu-Chung N. Cheng,et al.  Susceptibility weighted imaging (SWI) , 2004, Zeitschrift fur medizinische Physik.

[46]  Jens Frahm,et al.  Topography of the human corpus callosum revisited—Comprehensive fiber tractography using diffusion tensor magnetic resonance imaging , 2006, NeuroImage.

[47]  A. Hyder,et al.  The impact of traumatic brain injuries: a global perspective. , 2007, NeuroRehabilitation.

[48]  J. Sweeney,et al.  White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. , 2007, Brain : a journal of neurology.

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

[50]  D. Holtzman,et al.  Diffusion Tensor Imaging Reliably Detects Experimental Traumatic Axonal Injury and Indicates Approximate Time of Injury , 2007, The Journal of Neuroscience.

[51]  J. Coles Imaging after brain injury. , 2007, British journal of anaesthesia.

[52]  Jerry L. Prince,et al.  A Hybrid Eulerian-Lagrangian Approach for Thickness, Correspondence, and Gridding of Annular Tissues , 2007, IEEE Trans. Image Process..

[53]  S. Deb,et al.  Neuropsychiatric consequences of traumatic brain injury: A comparison between two age groups , 2007, Brain injury.

[54]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[55]  L. Ketonen,et al.  Neuroimaging of pediatric diseases. , 2008, Seminars in neurology.

[56]  H. Levin,et al.  Diffusion tensor imaging of acute mild traumatic brain injury in adolescents , 2008, Neurology.

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

[58]  D. Mikulis,et al.  Use of diffusion tensor imaging to examine subacute white matter injury progression in moderate to severe traumatic brain injury. , 2008, Archives of physical medicine and rehabilitation.

[59]  Frithjof Kruggel,et al.  Automatic segmentation of human brain sulci , 2008, Medical Image Anal..

[60]  C. Till,et al.  Postrecovery cognitive decline in adults with traumatic brain injury. , 2008, Archives of physical medicine and rehabilitation.

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

[62]  Bruce D. McCandliss,et al.  Extent of Microstructural White Matter Injury in Postconcussive Syndrome Correlates with Impaired Cognitive Reaction Time: A 3T Diffusion Tensor Imaging Study of Mild Traumatic Brain Injury , 2008, American Journal of Neuroradiology.

[63]  G. Manley,et al.  Focal lesions in acute mild traumatic brain injury and neurocognitive outcome: CT versus 3T MRI. , 2008, Journal of neurotrauma.

[64]  M. P. van den Heuvel,et al.  Microstructural Organization of the Cingulum Tract and the Level of Default Mode Functional Connectivity , 2008, The Journal of Neuroscience.

[65]  Craig A Branch,et al.  Multifocal white matter ultrastructural abnormalities in mild traumatic brain injury with cognitive disability: a voxel-wise analysis of diffusion tensor imaging. , 2008, Journal of neurotrauma.

[66]  Dong-Hyun Kim,et al.  Measuring Fractional Anisotropy of the Corpus Callosum Using Diffusion Tensor Imaging: Mid-Sagittal versus Axial Imaging Planes , 2008, Korean journal of radiology.

[67]  Brian Levine,et al.  Ventral frontal cortex functions and quantified MRI in traumatic brain injury , 2008, Neuropsychologia.

[68]  N. Walz,et al.  Late proton magnetic resonance spectroscopy following traumatic brain injury during early childhood: relationship with neurobehavioral outcomes. , 2008, Journal of neurotrauma.

[69]  T. Dill Contraindications to magnetic resonance imaging , 2008, Heart.

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

[71]  Atle Bjørnerud,et al.  Error-related negativity is mediated by fractional anisotropy in the posterior cingulate gyrus--a study combining diffusion tensor imaging and electrophysiology in healthy adults. , 2009, Cerebral cortex.

[72]  Khader M Hasan,et al.  Serial changes in the white matter diffusion tensor imaging metrics in moderate traumatic brain injury and correlation with neuro-cognitive function. , 2009, Journal of neurotrauma.

[73]  Habib Benali,et al.  Relation between brain lesion location and clinical outcome in patients with severe traumatic brain injury: A diffusion tensor imaging study using voxel‐based approaches , 2009, Human brain mapping.

[74]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[75]  Timothy J. Herron,et al.  Bmc Medical Imaging Multimodal Surface-based Morphometry Reveals Diffuse Cortical Atrophy in Traumatic Brain Injury , 2009 .

[76]  Samuel Patz,et al.  Diffusion Tensor Imaging, White Matter Lesions, the Corpus Callosum, and Gait in the Elderly , 2009, Stroke.

[77]  B. Mueller,et al.  White matter and neurocognitive changes in adults with chronic traumatic brain injury , 2009, Journal of the International Neuropsychological Society.

[78]  Craig A Branch,et al.  Diffusion-tensor imaging implicates prefrontal axonal injury in executive function impairment following very mild traumatic brain injury. , 2009, Radiology.

[79]  David W Wright,et al.  Position statement: definition of traumatic brain injury. , 2010, Archives of physical medicine and rehabilitation.

[80]  A. Mayer,et al.  A prospective diffusion tensor imaging study in mild traumatic brain injury , 2010, Neurology.

[81]  Jeffrey S. Spence,et al.  Regionally selective atrophy after traumatic axonal injury. , 2010, Archives of neurology.

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

[83]  A. Pfefferbaum,et al.  MR Diffusion Tensor Imaging: A Window into White Matter Integrity of the Working Brain , 2010, Neuropsychology Review.

[84]  Stephen E. Rose,et al.  Traumatic brain injury, major depression, and diffusion tensor imaging: Making connections , 2010, Brain Research Reviews.

[85]  F. Kruggel,et al.  PDE-based reconstruction of the cerebral cortex from MR images , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[86]  Erin D Bigler,et al.  Diffusion tensor imaging , 2010, Neurology.

[87]  Jeffrey S. Spence,et al.  Deficits in functional connectivity of hippocampal and frontal lobe circuits after traumatic axonal injury. , 2011, Archives of neurology.

[88]  T. Carpenter,et al.  Traumatic brain injury alters the functional brain network mediating working memory , 2011, Brain injury.

[89]  Josef Ling,et al.  Functional connectivity in mild traumatic brain injury , 2011, Human brain mapping.

[90]  Mark Hallett,et al.  Alteration of brain functional network at rest and in response to YMCA physical stress test in concussed athletes: RsFMRI study , 2011, NeuroImage.

[91]  D C Good,et al.  Changes in resting connectivity during recovery from severe traumatic brain injury. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[92]  Robert Leech,et al.  Default mode network functional and structural connectivity after traumatic brain injury. , 2011, Brain : a journal of neurology.

[93]  Mary R. Newsome,et al.  Brain imaging correlates of verbal working memory in children following traumatic brain injury. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[94]  T. McAllister,et al.  Neurobiological consequences of traumatic brain injury , 2011, Dialogues in clinical neuroscience.

[95]  M. Raichle,et al.  Detection of blast-related traumatic brain injury in U.S. military personnel. , 2011, The New England journal of medicine.

[96]  Robert Leech,et al.  Salience network integrity predicts default mode network function after traumatic brain injury , 2012, Proceedings of the National Academy of Sciences.

[97]  Derek K. Jones,et al.  Cingulum Microstructure Predicts Cognitive Control in Older Age and Mild Cognitive Impairment , 2012, The Journal of Neuroscience.

[98]  Jeffrey S. Spence,et al.  Three approaches to investigating functional compromise to the default mode network after traumatic axonal injury , 2012, Brain Imaging and Behavior.

[99]  J. Shinoda,et al.  Decreased Fractional Anisotropy Evaluated Using Tract-Based Spatial Statistics and Correlated with Cognitive Dysfunction in Patients with Mild Traumatic Brain Injury in the Chronic Stage , 2012, American Journal of Neuroradiology.

[100]  Tricia L. Merkley,et al.  Longitudinal changes in cortical thickness in children after traumatic brain injury and their relation to behavioral regulation and emotional control , 2012, International Journal of Developmental Neuroscience.

[101]  J. Hunter,et al.  Emerging imaging tools for use with traumatic brain injury research. , 2012, Journal of neurotrauma.

[102]  P. Eslinger,et al.  Traumatic brain injury and the frontal lobes: What can we gain with diffusion tensor imaging? , 2012, Cortex.

[103]  N. Bargalló,et al.  White matter integrity related to functional working memory networks in traumatic brain injury , 2012, Neurology.

[104]  D. Norris,et al.  Abnormal whole-brain functional networks in homogeneous acute mild traumatic brain injury , 2012, Neurology.

[105]  I. Olson,et al.  Dissecting the uncinate fasciculus: disorders, controversies and a hypothesis. , 2013, Brain : a journal of neurology.

[106]  Jia Li,et al.  Detection of white matter lesions in the acute stage of diffuse axonal injury predicts long-term cognitive impairments: A clinical diffusion tensor imaging study , 2013, The journal of trauma and acute care surgery.

[107]  N. Bargalló,et al.  Long-term declarative memory deficits in diffuse TBI: Correlations with cortical thickness, white matter integrity and hippocampal volume , 2013, Cortex.

[108]  P. Expert,et al.  Traumatic brain injury impairs small-world topology , 2013, Neurology.

[109]  D. Salat,et al.  Reduced cortical thickness with increased lifetime burden of PTSD in OEF/OIF Veterans and the impact of comorbid TBI☆ , 2013, NeuroImage: Clinical.

[110]  L. Boyd,et al.  Comparative incidence of concussion and return to play time in two Canadian minor hockey groups over the 2011–2012 season , 2013, British Journal of Sports Medicine.

[111]  Kaj Blennow,et al.  Acute and chronic traumatic encephalopathies: pathogenesis and biomarkers , 2013, Nature Reviews Neurology.

[112]  T. Kurki,et al.  Quantitative diffusion-tensor tractography of long association tracts in patients with traumatic brain injury without associated findings at routine MR imaging. , 2013, Radiology.

[113]  Pratik Mukherjee,et al.  Magnetic resonance imaging improves 3‐month outcome prediction in mild traumatic brain injury , 2012, Annals of neurology.

[114]  Xin Wang,et al.  Early cortical thickness change after mild traumatic brain injury following motor vehicle collision. , 2015, Journal of neurotrauma.

[115]  M. Wintermark,et al.  Imaging Evidence and Recommendations for Traumatic Brain Injury: Advanced Neuro- and Neurovascular Imaging Techniques , 2015, American Journal of Neuroradiology.

[116]  R. Bucholz,et al.  Evaluation of Cortical Thickness after Traumatic Brain Injury in Military Veterans. , 2015, Journal of neurotrauma.

[117]  P. Kalakoti,et al.  Revisiting Traumatic Brain Injury in the Pediatric Population. , 2016, World neurosurgery.