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Diffusion Tensor Imaging Biomarkers for Traumatic Axonal Injury: Analysis of Three Analytic Methods

Published online by Cambridge University Press:  12 November 2010

Carlos D. Marquez de la Plata ,
Fanpei Gloria Yang ,
Jun Yi Wang ,
Kamini Krishnan ,
Khamid Bakhadirov ,
Christopher Paliotta ,
Sina Aslan ,
Michael D. Devous Sr. ,
Carol Moore  and
Caryn Harper
...Show all authors
Carlos D. Marquez de la Plata
Affiliation:
Center for Brain Health, University of Texas at Dallas, Richardson, Texas University of Texas Southwestern Medical Center, Dallas, Texas
Fanpei Gloria Yang
Affiliation:
Center for Brain Health, University of Texas at Dallas, Richardson, Texas
Jun Yi Wang
Affiliation:
Center for Brain Health, University of Texas at Dallas, Richardson, Texas
Kamini Krishnan
Affiliation:
Center for Brain Health, University of Texas at Dallas, Richardson, Texas
Khamid Bakhadirov
Affiliation:
Center for Brain Health, University of Texas at Dallas, Richardson, Texas
Christopher Paliotta
Affiliation:
University of Texas Southwestern Medical Center, Dallas, Texas
Sina Aslan
Affiliation:
University of Texas Southwestern Medical Center, Dallas, Texas
Michael D. Devous Sr.
Affiliation:
University of Texas Southwestern Medical Center, Dallas, Texas
Carol Moore
Affiliation:
University of Texas Southwestern Medical Center, Dallas, Texas
Caryn Harper
Affiliation:
University of Texas Southwestern Medical Center, Dallas, Texas
Roderick McColl
Affiliation:
University of Texas Southwestern Medical Center, Dallas, Texas
C. Munro Cullum
Affiliation:
University of Texas Southwestern Medical Center, Dallas, Texas
Ramon Diaz-Arrastia*
Affiliation:
University of Texas Southwestern Medical Center, Dallas, Texas
*
Correspondence and reprint requests to: Ramon Diaz-Arrastia, Department of Neurology, University of Texas Southwestern Medical Center at Dallas, 5323 Harry Hines Blvd., Dallas, TX 75390. E-mail: [email protected]
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Abstract

Traumatic axonal injury (TAI) is a common mechanism of traumatic brain injury not readily identified using conventional neuroimaging modalities. Novel imaging modalities such as diffusion tensor imaging (DTI) can detect microstructural compromise in white matter (WM) in various clinical populations including TAI. DTI-derived data can be analyzed using global methods (i.e., WM histogram or voxel-based approaches) or a regional approach (i.e., tractography). While each of these methods produce qualitatively comparable results, it is not clear which is most useful in clinical research and ultimately in clinical practice. This study compared three methods of analyzing DTI-derived data with regard to detection of WM injury and their association with clinical outcomes. Thirty patients with TAI and 19 demographically similar normal controls were scanned using a 3 Tesla magnet. Patients were scanned approximately eight months postinjury, and underwent an outcomes assessment at that time. Histogram analysis of fractional anisotropy (FA) and mean diffusivity showed global WM integrity differences between patients and controls. Voxel-based and tractography analyses showed significant decreases in FA within centroaxial structures involved in TAI. All three techniques were associated with functional and cognitive outcomes. DTI measures of microstructural integrity appear robust, as the three analysis techniques studied showed adequate utility for detecting WM injury. (JINS, 2011, 17, 000–000)

Keywords

DTITAITraumatic Brain injuryMemoryTractographyCognitive outcomes
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 17 , Issue 1 , January 2011 , pp. 24 - 35
Copyright
Copyright © The International Neuropsychological Society 2010

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References

Adams, J.H., Graham, D.I., Gennarelli, T.A., Maxwell, W.L. (1991). Diffuse axonal injury in non-missile head injury. Journal of Neurology, Neurosurgery, and Psychiatry, 54, 481–483. doi:10.1136/jnnp.54.6.481CrossRefGoogle ScholarPubMed
Adams, J.H., Graham, D.I., Murray, L.S., Scott, G. (1982). Diffuse axonal injury due to non-missile head injury in humans: An analysis of 45 cases. Annals of Neurology, 12, 557–563. doi:10.1002/ana.410120610Google Scholar
Adams, J.H., Graham, D.I., Scott, G., Parker, L.S., Doyle, D. (1980). Brain damage in fatal non-missile head injury. Journal of Clinical Pathology, 33, 1132–1145. doi:10.1136/jcp.33.12.1132Google Scholar
Anbeek, P., Vincken, K.L., van Osch, M.J., Bisschops, R.H., van der Grond, J. (2004). Probabilistic segmentation of white matter lesions in MR imaging. Neuroimage, 21, 1037–1044. doi:10.1016/j.neuroimage.2003.10.012CrossRefGoogle ScholarPubMed
Arfanakis, K., Haughton, V.M., Carew, J.D., Rogers, B.P., Dempsey, R.J., Meyerand, M.E. (2002). Diffusion tensor MR imaging in diffuse axonal injury. American Journal of Neuroradiology, 23, 794–802. Retrieved from http://www.ajnr.org/Google Scholar
Bazarian, J.J., Zhong, J., Blyth, B., Zhu, T., Kavcic, V., Peterson, D. (2007). Diffusion tensor imaging detects clinically important axonal damage after mild traumatic brain injury: A pilot study. Journal of Neurotrauma, 24, 1447–1459. doi:10.1089/neu.2007.0241Google Scholar
Bendlin, B.B., Ries, M.L., Lazar, M., Alexander, A.L., Dempsey, R.J., Rowley, H.A., Johnson, S.C. (2008). Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neuroimage, 42, 503–514. doi:10.1016/J.neuroimage.2008.04.254Google Scholar
Benson, R.R., Meda, S.A., Vasudevan, S., Kou, Z., Govindarajan, K.A., Hanks, R.A., Haacke, E.M. (2007). Global white matter analysis of diffusion tensor images is predictive of injury severity in traumatic brain injury. Journal of Neurotrauma, 24, 446–459. doi:10.1089/neu.2006.0153Google Scholar
Benton, A.L., Hamsher, K., Sivan, A.B. (1976). Multilingual aphasia examination. Iowa City, IA: AJA Associates.Google Scholar
Brooks, N., Campsie, L., Symongton, C., Beattie, A., McKinlay, W. (1986). The five year outcome of severe blunt head injury: A relative’s view. Journal of Neurology, Neurosurgery, and Psychiatry, 49, 764–770. doi:10.1136/jnnp.49.7.764CrossRefGoogle ScholarPubMed
Budde, M.D., Kim, J.H., Liang, H.F., Schmidt, R.E., Russell, J.H., Cross, A.H., Song, S.K. (2007). Toward accurate diagnosis of white matter pathology using diffusion tensor imaging. Magnetic Resonance in Medicine, 57, 688–695. doi:10.1002/mrm.21200Google Scholar
Catheline, G., Periot, O., Amirault, M., Braun, M., Dartigues, J.F., Auriacombe, S., Allard, M. (2008). Distinctive alterations of the cingulum bundle during aging and Alzheimer’s disease. Neurobiology of Aging, 31, 1582–1592. doi:10.1016/j.neurobiolaging.2008.08.012Google Scholar
Delis, D., Kramer, J., Kaplan, E., Ober, B. (2000). California verbal learning test-Second Edition. San Antonio, TX: The Psychological Corporation; 2000.Google Scholar
Diaz-Marchan, P.G., Hayman, L.A., Carrier, D.A., Feldman, D.J. (1996). Computed tomography of closed head injury. In R.K. Narayan, J.E. Wilburger & J.T. Povlishock (Eds.), Neurotrauma (pp. 137–149). New York: McGraw-Hill.Google Scholar
Ding, K., Marquez de la Plata, C., Wang, J.Y., Mumphrey, M., Moore, C., Harper, C., Diaz-Arrastia, R. (2008). Cerebral atrophy after traumatic white matter injury: Correlation with acute neuroimaging and outcome. Journal of Neurotrauma, 25, 1433–1440. doi:10.1089/neu.2008.0683CrossRefGoogle ScholarPubMed
Dodrill, C.B. (1978). A neuropsychological battery for epilepsy. Epilepsia, 19, 611–623.Google Scholar
Gentry, L.R., Godersky, J.C., Thompson, E. (1988). MR imaging of head trauma: Review of the distribution and radiopathologic features of traumatic lesions. American Journal of Neuroradiology, 9, 101–110. Retrieved from http://www.ajronline.org/Google Scholar
Hagler, D.J. Jr, Ahmadi, M.E., Kuperman, J., Holland, D., McDonald, C., Halgren, E., Dale, A.M. (2009). Automated white-matter tractography using a probabilistic diffusion tensor atlas: Application to temporal lobe epilepsy. Human Brain Mapping, 30, 1535–1547. doi:10.1002/hbm.20619CrossRefGoogle ScholarPubMed
Huisman, T.A., Schwamm, L.H., Schafer, P.W., Koroshetz, W.J., Shetty-Alva, N., Ozsunar, Y., Sorenson, A.G. (2004). Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. American Journal of Neuroradiology, 25, 370–376. Retrieved from http://www.ajnr.org/Google Scholar
Hyman, B.T., Hoesen, G.W., Kromer, L.J., Damasio, A.R. (1986). Perforant pathway changes and the memory impairment of Alzheimer’s disease. Annals of Neurology, 20, 472–481. doi:10.1002/ana.410200406Google Scholar
Inglese, M., Makani, S., Johnson, G., Cohen, B.A., Silver, J.A., Gonen, O., Grossman, R.I. (2005). Diffuse axonal injury in mild traumatic brain injury: A diffusion tensor imaging study. Journal of Neurosurgery, 103, 298–303. doi:10.3171/jns.2005.103.2.0298CrossRefGoogle ScholarPubMed
Leclercq, P.D., McKenzie, J.E., Graham, D.I., Gentleman, S.M. (2001). Axonal injury is accentuated in the caudal corpus callosum of head-injured patients. Journal of Neurotrauma, 18, 1–9. doi:10.1089/089771501750055721CrossRefGoogle ScholarPubMed
Lee, J.S., Han, M.K., Kim, S.H., Kwon, O.K., Kim, J.H. (2005). Fiber tracking by diffusion tensor imaging in corticospinal tract stroke: Topographical correlation with clinical symptoms. Neuroimage, 26, 771–776. doi:10.1016/j.neuroimage.2005.02.036Google Scholar
Levin, H.S. (1990). Memory deficit after closed head injury. Journal of Clinical & Experimental Neuropsychology, 12(1), 129–153. doi:10.1080/01688639008400960Google Scholar
Lipton, M.L., Gellella, E., Lo, C., Gold, T., Ardekani, B.A., Shifteh, K., Bello, C.A. (2008). Multifocal white matter ultrastructural abnormalities in mild traumatic brain injury with cognitive disability: A voxel-wise analysis of diffusion tensor imaging. Journal of Neurotrauma, 25, 1335–1342. doi:10.1089/neu.2008.0547Google Scholar
Mark, L.P., Daniels, D.L., Naidich, T.P., Hendrix, L.E. (1995). Limbic connections. American Journal of Neuroradiology, 16, 1303–1306. Retrieved from http://www.ajnr.org/Google Scholar
Marquez de la Plata, C., Ardelean, A., Kovakkattu, D., Srinivasan, P., Miller, A., Phuong, V., Devous, M. (2007). Magnetic resonance imaging of diffuse axonal injury: Quantitative assessment of white matter lesion volume. Journal of Neurotrauma, 24, 591–598. doi:10.1089/neu.2006.0214Google Scholar
Mathias, J.L., Wheaton, P. (2007). Changes in attention and information-processing speed following severe traumatic brain injury: A meta-analytic review. Neuropsychology, 21, 212–223. doi:10.1037/0894-4105.21.2.212CrossRefGoogle ScholarPubMed
McAllister, T., Flashman, L.A., McDonald, B.C., Saykin, A.J. (2006). Mechanisms of working memory dysfunction after mild and moderate TBI: Evidence from functional MRI and neurogenetics. Journal of Neurotrauma, 23, 1450–1467. doi:10.1089/neu.2006.23.1450Google Scholar
Mori, S., Wakana, S., Nagae-Poetscher, L.M., van Zijl, P.C. (2005). MRI atlas of human white matter. New York: Elsevier.Google Scholar
Nakayama, N., Okumura, A., Shinoda, J., Yasokawa, Y.T., Miwa, K., Yoshimura, S.I., Iwama, T. (2006). Evidence for white matter disruption intraumatic brain injury without macroscopic lesions. Journal of Neurology, Neurosurgery, and Psychiatry, 77, 850–855. doi:10.1136/jnnp.2005.077875CrossRefGoogle Scholar
Newcombe, V.F.J., Williams, G.B., Nortje, J., Bradley, P.G., Harding, S.G., Smielewski, P., Menon, D.K. (2007). Analysis of acute traumatic axonal injury using diffusion tensor imaging. British Journal of Neurosurgery, 21, 340–348. doi:10.1080/02688690701400882Google Scholar
Ogawa, T., Sekino, H., Uzura, M., Sakamoto, T., Taguchi, Y., Yamaguchi, Y., Imaki, S. (1992). Comparative study of magnetic resonance and CT scan imaging in cases of severe head injury. Acta Neurochirurgica. Supplement, 55, 8–10. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1414552Google Scholar
Pannek, K., Mathias, J.L., Bigler, E.D., Brown, G., Taylor, J.D., Rose, S. (2010). An automated strategy for the delineation and parcellation of commissural pathways suitable for clinical populations utilising high angular resolution diffusion imaging tractography. Neuroimage, 30, 1044–1053. doi:10.1016/j.neuroimage.2010.01.020Google Scholar
Pfefferbaum, A., Rosenbloom, M.J., Adalsteinsson, E., Sullivan, E.V. (2007). Diffusion tensor imaging with quantitative fibre tracking in HIV infection and alcoholism comorbidity: Synergistic white matter damage. Brain, 130, 48–64. doi:10.1093/brain/awl242Google Scholar
Reitan, R.M. (1958). Validity of the Trail Making test as an indicator of organic brain damage. Perceptual and Motor Skills, 8, 271–276. Retrieved from http://ammons.ammonsscientific.com/php/toc.phpGoogle Scholar
Rutgers, D.R., Fillard, P., Paradot, G., Tadie, M., Lasjaunias, P., Ducreux, D. (2008). Diffusion tensor imaging characteristics of the corpus callosum in mild, moderate, and severe traumatic brain injury. American Journal of Neuroradiology, 29, 1730–1735. doi:10.3174/ajnr.A1213Google Scholar
Saindane, A.M., Law, M., Ge, Y., Johnson, G., Babb, J.S., Grossman, R.I. (2007). Correlation of diffusion tensor and dynamic perfusion MR imaging metrics in normal appearing corpus callosum: Support for primary hypoperfusion in multiple sclerosis. American Journal of Neuroradiology, 28, 467–772. Retrieved from http://www.ajnr.org/Google Scholar
Schmierer, K., Wheeler-Kinshott, C.A., Boulby, P.A., Scaravilli, F., Altman, D.R., Barker, G.J., Miller, D.H. (2007). Diffusion tensor imaging of post mortem multiple sclerosis brain. Neuroimage, 35, 467–477. doi:10.1016/j.neuroimage.2006.12.010Google Scholar
Thurnher, M.M., Castillo, M., Stadler, A., Rieger, A., Schmid, B., Sundgren, P.C. (2005). Diffusion-Tensor MR imaging of the brain in human immunodeficiency virus-positive patients. AJNR American Journal of Neuroradiology, 26, 2275–2281. Retrieved from http://www.ajnr.org/Google Scholar
Wakana, S., Jlang, H., Nagae-Poetscher, L.M., van Zijl, P.C., Mori, S. (2004). Fiber tract-based atlas of human white matter anatomy. Radiology, 230, 77–87. doi:10.1148/radiol.2301021640Google Scholar
Wang, J.Y., Bakhadirov, K., Devous, M.D., Abdi, H., McColl, R., Moore, C., Diaz-Arrastia, R. (2008). Diffusion tensor tractography of traumatic diffuse axonal injury. Archives of Neurology, 65, 619–626. Retrieved from http://archneur.ama-assn.org/Google Scholar
Wechsler, D. (1997). WAIS-III administration and scoring manual. San Antonio, TX: The Psychological Corporation.Google Scholar
Wilson, J.T., Pettigrew, L.E., Teasdale, G.M. (1998). Structured interview for the Glasgow Outcome Scale and the Extended Glasgow Outcome Scale. Journal of Neurotrauma, 15, 573–585. doi:10.1089/neu.1998.15.573Google Scholar
Wozniak, J.R., Krach, L., Ward, E., Mueller, B.A., Muetzel, R., Schnoebelen, S., Lim, K.O. (2007). Neurocognitive and neuroimaging correlates of pediatric traumatic brain injury: A diffusion tensor imaging (DTI) study. Archives of Clinical Neuropsychology, 22, 555–568. doi:10.1016/j.acn.2007.03.004Google Scholar
Wu, Y., Storey, P., Cohen, B.A., Epstein, L.G., Edelman, R.R., Ragin, A.B. (2006). Diffusion alterations in corpus callosum of patients with HIV. AJNR American Journal of Neuroradiology, 27, 656–660. Retrieved from http://www.ajnr.org/Google Scholar
Xu, J., Rasmussen, I.A., Lagopoulos, J., Haberg, A. (2007). Diffuse axonal injury in severe traumatic brain injury visualized using high-resolution diffusion tensor imaging. Journal of Neurotrauma, 24, 753–765. doi:10.1089/neu.2006.0208Google Scholar
Ylvisaker, M., Feeney, T. (1996). Executive functions after traumatic brain injury: Supported cognition and self-advocacy. Seminars in Speech and Language, 17, 217–232. doi:10.1055/s-2008-1064100Google Scholar
Zhang, W., Olivi, A., Hertig, S., van Zijl, P., Mori, S. (2008). Automated fiber tracking of human brain white matter using diffusion tensor imaging. Neuroimage, 42, 771–777. doi:10.1016/j.neuroimage.2008.04.241Google Scholar