Academic Radiology
Volume 15, Issue 11 , Pages 1360-1375 , November 2008

Multivariate Analysis of Structural and Diffusion Imaging in Traumatic Brain Injury

  • Brian Avants, PhD

      Affiliations

    • Department of Radiology, University of Pennsylvania, 3600 Market St, Suite 320, Philadelphia, PA 19104
  • ,
  • Jeffrey T. Duda, MS

      Affiliations

    • Department of Radiology, University of Pennsylvania, 3600 Market St, Suite 320, Philadelphia, PA 19104
    • Corresponding Author InformationAddress correspondence to: J.T.D.
  • ,
  • Junghoon Kim, PhD

      Affiliations

    • Moss Rehabilitation Research Institute, Albert Einstein Healthcare Network, Philadelphia, PA
  • ,
  • Hui Zhang, PhD

      Affiliations

    • Department of Radiology, University of Pennsylvania, 3600 Market St, Suite 320, Philadelphia, PA 19104
  • ,
  • John Pluta, BS

      Affiliations

    • Department of Neurology, University of Pennsylvania, 3600 Market St, Suite 320, Philadelphia, PA 19104
  • ,
  • James C. Gee, PhD

      Affiliations

    • Department of Radiology, University of Pennsylvania, 3600 Market St, Suite 320, Philadelphia, PA 19104
  • ,
  • John Whyte, MD

      Affiliations

    • Moss Rehabilitation Research Institute, Albert Einstein Healthcare Network, Philadelphia, PA

Received 1 March 2008 ,Accepted 1 July 2008.

References 

  1. Furlow B. Diagnostic imaging of traumatic brain injury. Radiol Technol. 2006;78:145–156quiz 157–159.
  2. Hoge CW, McGurk D, Thomas JL, et al. Mild traumatic brain injury in U.S. Soldiers returning from Iraq. N Engl J Med. 2008;358:453–463
  3. Kraus MF, Susmaras T, Caughlin BP, et al. White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain. 2007;130:2508–2519
  4. Mendez CV, Hurley RA, Lassonde M, et al. Mild traumatic brain injury: neuroimaging of sports-related concussion. J Neuropsychiatry Clin Neurosci. 2005;17:297–303
  5. Chen JK, Johnston KM, Petrides M, et al. Neural substrates of symptoms of depression following concussion in male athletes with persisting postconcussion symptoms. Arch Gen Psychiatry. 2008;65:81–89
  6. Kim J, Avants B, Patel S, et al. Structural consequences of diffuse traumatic brain injury: a large deformation tensor-based morphometry study. Neuroimage. 2008;39:1014–1026
  7. Levin HS. Neuroplasticity following non-penetrating traumatic brain injury. Brain Inj. 2003;17:665–674
  8. Miles L, Grossman RJ, Johnson G, et al. Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injury. Brain Inj. 2008;22:115–122
  9. Sidaros A, Engberg AW, Sidaros K, et al. Diffusion tensor imaging during recovery from severe traumatic brain injury and relation to clinical outcome: a longitudinal study. Brain. 2008;131:559–572
  10. Gale SD, Baxter L, Roundy N, et al. Traumatic brain injury and grey matter concentration: a preliminary voxel based morphometry study. J Neurol Neurosurg Psychiatry. 2005;76:984–988
  11. Tomaiuolo F, Carlesimo GA, Di Paola M, 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. J Neurol Neurosurg Psychiatry. 2004;75:1314–1322
  12. Salmond CH, Chatfield DA, Menon DK, et al. Cognitive sequelae of head injury: involvement of basal forebrain and associated structures. Brain. 2005;128:189–200
  13. Graham DI, Maxwell WL, Adams JH, et al. Novel aspects of the neuropathology of the vegetative state after blunt head injury. Prog Brain Res. 2005;150:445–455
  14. Zhang L, Yang KH, King AI. A proposed injury threshold for mild traumatic brain injury. J Biomech Eng. 2004;126:226–236
  15. Maxwell WL, Pennington K, MacKinnon MA, et al. Differential responses in three thalamic nuclei in moderately disabled, severely disabled and vegetative patients after blunt head injury. Brain. 2004;127:2470–2478
  16. Adams JH, Graham DI, Jennett B. The neuropathology of the vegetative state after an acute brain insult. Brain. 2000;123:1327–1338
  17. Maxwell WL, MacKinnon MA, Smith DH, et al. Thalamic nuclei after human blunt head injury. J Neuropathol Exp Neurol. 2006;65:478–488
  18. Kotapka MJ, Graham DI, Adams JH, et al. Hippocampal pathology in fatal human head injury without high intracranial pressure. J Neurotrauma. 1994;11:317–324
  19. Ahn HY, Kim SH, Han BS, et al. Focal lesions of the corticospinal tract demonstrated by diffusion tensor imaging in patients with diffuse axonal injury. NeuroRehabilitation. 2006;21:239–243
  20. Bazarian JJ, Zhong J, Blyth B, et al. Diffusion tensor imaging detects clinically important axonal damage after mild traumatic brain injury: a pilot study. J Neurotrauma. 2007;24:1447–1459
  21. Mac Donald CL, Dikranian K, Bayly P, et al. Diffusion tensor imaging reliably detects experimental traumatic axonal injury and indicates approximate time of injury. J Neurosci. 2007;27:11869–11876
  22. Lee HW, Choi CG, Chun MH. Usefulness of diffusion tensor imaging for evaluation of motor function in patients with traumatic brain injury: three case studies. J Head Trauma Rehabil. 2006;21:272–278
  23. Song SK, Sun SW, Ramsbottom MJ, et al. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage. 2002;17:1429–1436
  24. Mori S, Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron. 2006;51:527–539
  25. Ardekani AB, Bappal A, D'Angelo D, et al. Brain morphometry using diffusion-weighted magnetic resonance imaging: application to schizophrenia. Neuroreport. 2005;16:1455–1459
  26. Sugiyama S, Kondo T, Higano S, et al. Diffusion tensor imaging fiber tractography for evaluating diffuse axonal injury. Brain Inj. 2007;21:413–419
  27. Levin HS, Benavidez DA, Verger-Maestre K, et al. Reduction of corpus callosum growth after severe traumatic brain injury in children. Neurology. 2000;54:647–653
  28. Ewing-Cobbs LE, Hasan KM, Prasad MR, et al. Corpus callosum diffusion anisotropy correlates with neuropsychological outcomes in twins disconcordant for traumatic brain injury. AJNR Am J Neuroradiol. 2006;27:879–881
  29. Hashimoto K, Okumura A, Shinoda J, et al. Tensor magnetic resonance imaging in a case of mild traumatic brain injury with lowered verbal intelligence quotient. J Rehabil Med. 2007;39:418–420
  30. Inglese M, Makani S, Johnson G, et al. Diffuse axonal injury in mild traumatic brain injury: a diffusion tensor imaging study. J Neurosurg. 2005;103:298–303
  31. Nakayama N, Okumura A, Shinoda J, et al. Evidence for white matter disruption in traumatic brain injury without macroscopic lesions. J Neurol Neurosurg Psychiatry. 2006;77:850–855
  32. Xu J, Rasmussen IA, Lagopoulos J, et al. Diffuse axonal injury in severe traumatic brain injury visualized using high-resolution diffusion tensor imaging. J Neurotrauma. 2007;24:753–765
  33. Le TH, Mukherjee P, Henry RG, 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. Neurosurgery. 2005;56:189
  34. Yasokawa YT, Shinoda J, Okumura A, et al. Correlation between diffusion-tensor magnetic resonance imaging and motor-evoked potential in chronic severe diffuse axonal injury. J Neurotrauma. 2007;24:163–173
  35. Han BS, Kim SH, Kim OL, et al. Recovery of corticospinal tract with diffuse axonal injury: a diffusion tensor image study. NeuroRehabilitation. 2007;22:151–155
  36. Kantarci K, Jack CR, Xu YC, et al. Mild cognitive impairment and Alzheimer disease: regional diffusivity of water. Radiology. 2001;219:101–107
  37. Chappell MH, Ulug AM, Zhang L, et al. Distribution of microstructural damage in the brains of professional boxers: a diffusion MRI study. J Magn Reson Imaging. 2006;
  38. Ray KM, Wang H, Chu Y, et al. Mild cognitive impairment: apparent diffusion coefficient in regional gray matter and white matter structures. Radiology. 2006;241:197–205
  39. Salmond CH, Menon DK, Chatfield DA, et al. Diffusion tensor imaging in chronic head injury survivors: correlations with learning and memory indices. Neuroimage. 2006;29:117–124
  40. Duan Y, Li X, Xi Y. Thalamus segmentation from diffusion tensor magnetic resonance imaging. Int J Biomed Imaging. 2007;2007:90216
  41. Wiegell MR, Tuch DS, Larsson HBW, et al. Automatic segmentation of thalamic nuclei from diffusion tensor magnetic resonance imaging. Neuroimage. 2003;19:391–401
  42. Miller MI, Christensen GE, Amit Y, et al. Mathematical textbook of deformable neuroanatomies. Proc Natl Acad Sci U S A. 1993;90:11944–11948
  43. Park H-J, Kubicki M, Shenton ME, et al. Spatial normalization of diffusion tensor MRI using multiple channels. Neuroimage. 2003;20:1995–2009
  44. Studholme C. Dense feature deformation morphometry: incorporating DTI data into conventional MRI morphometry. Med Image Anal. 2008;Apr 16. Epub ahead of print.
  45. Miller MI, Beg MF, Ceritoglu C, et al. Increasing the power of functional maps of the medial temporal lobe by using large deformation diffeomorphic metric mapping. PNAS. 2005;102:9685–9690
  46. Yan C, Miller MI, Winslow RL, et al. Large deformation diffeomorphic metric mapping of vector fields. TMI. 2005;24:1216–1230
  47. Zhang H, Yushkevich PA, Alexander DC, et al. Deformable registration of diffusion tensor MR images with explicit orientation optimization. Med Image Anal. 2006;10:764–785
  48. Zhang H, Avants BB, Yushkevich PA, et al. High-dimensional spatial normalization of diffusion tensor images improves the detection of white matter differences: an example study using amyotrophic lateral sclerosis. IEEE Trans Med Imaging. 2007;26:1585–1597
  49. Mangin J, Poupon C, Clark C, et al. Distortion correction and robust tensor estimation for MR diffusion imaging. Med Image Anal. 2003;6:191–198
  50. Miller M, Trouve A, Younes L. On the metrics and Euler-Lagrange equations of computational anatomy. Annu Rev Biomed Eng. 2002;4:375–405
  51. Avants BB, Epstein CL, Grossman M, et al. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal. 2008;12:26–41
  52. Alexander DC, Pierpaoli C, Basser PJ, et al. Spatial transformations of diffusion tensor magnetic resonance images. IEEE Trans Med Imaging. 2001;20:1131–1139
  53. Arsigny V, Fillard P, Pennec X, et al. Log-Euclidean metrics for fast and simple calculus on diffusion tensors. Magn Reson Med. 2006;56:411–421
  54. Kindlmann G, Estepar RS, Niethammer M, et al. Geodesic-loxodromes for diffusion tensor interpolation and difference measurement. Conference on Medical Image Computing and Computer Aided Intervention. 2007;10:1–9
  55. Avants BB, Gee JC. Formulation and evaluation of variational curve matching with prior constraints. In:  Gee JC,  Maintz JBA,  Vannier MW editor. Biomedical image registration. Heidelberg, Germany: Springer-Verlag; 2003;p. 21–30
  56. Hermosillo G, Chefd'Hotel C, Faugeras O. A variational approach to multi-modal image matching. Intl J Comp Vis. 2002;50:329–343
  57. Avants BB, Giannetta J, Gee JC, et al. Analyzing long term effects of cocaine exposure on adolescent brain structure with symmetric diffeomorphisms (Mathematical Methods in Biomedical Image Analysis). 2006;New York City.
  58. Beg MF, Khan A. Symmetric data attachment terms for large deformation image registration. IEEE Trans Med Imaging. 2007;26:1179–1189
  59. Thirion JP. Non-rigid matching using demons. IEEE Computer Vision and Pattern Recognition. 1996;245–251
  60. Yushkevich PA, Detre JA, Mechanic-Hamilton A, et al. Hippocampus-specific fMRI group activation analysis using the continuous medial representation. Neuroimage. 2007;35:1516–1530
  61. Langers DRM, Jansen JFA, Backes WH. Enhanced signal detection in neuroimaging by means of regional control of the global false discovery rate. Neuroimage. 2007;38:43–56
  62. Hammers A, Heckemann R, Koepp MJ, et al. Automatic detection and quantification of hippocampal atrophy on MRI in temporal lobe epilepsy: a proof-of-principle study. Neuroimage. 2007;36:38–47
  63. O'Sullivan M, Singhal S, Charlton R, et al. Diffusion tensor imaging of thalamus correlates with cognition in CADASIL without dementia. Neurology. 2004;62:702–707
  64. Schiff ND, Giacino JT, Kalmar K, et al. Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature. 2007;448:600–603
  65. Drevets WC. Neuroimaging studies of mood disorders. Biol Psychiatry. 2000;48:813–829
  66. McAllister TW. Traumatic brain injury and psychosis: what is the connection?. Semin Clin Neuropsychiatry. 1998;3:211–223
  67. Sydykova D, Stahl R, Dietrich O, et al. Fiber connections between the cerebral cortex and the corpus callosum in Alzheimer's disease: a diffusion tensor imaging and voxel-based morphometry study. Cereb Cortex. 2007;17:2276–2282
  68. Naganawa S, Sato C, Ishihra S, et al. Serial evaluation of diffusion tensor brain fiber tracking in a patient with severe diffuse axonal injury. AJNR Am J Neuroradiol. 2004;25:1553–1556
  69. Rutgers DR, Toulgoat F, Cazejust J, et al. White matter abnormalities in mild traumatic brain injury: a diffusion tensor imaging study. AJNR Am J Neuroradiol. 2008;29:514–519
  70. Wilde EA, Bigler ED, Haider JM, et al. Vulnerability of the anterior commissure in moderate to severe pediatric traumatic brain injury. J Child Neurol. 2006;21:769–776

1 This study is supported by grant R24HD39621 from the NCMRR, NICHD, NIH, H133G050219 from the NIDRR, US Department of Education, and P30NS045839 from the NINDS, NIH. Additional support is provided by NIH T32 CA 74781 and a grant with the Pennsylvania Department of Health. The Department specifically disclaims responsibility for any analyses, interpretations, or conclusions.

PII: S1076-6332(08)00395-4

doi: 10.1016/j.acra.2008.07.007

Academic Radiology
Volume 15, Issue 11 , Pages 1360-1375 , November 2008