Hostname: page-component-745bb68f8f-hvd4g Total loading time: 0 Render date: 2025-01-28T02:18:55.902Z Has data issue: false hasContentIssue false
  • English
  • Français

Longitudinal Volumetric Changes following Traumatic Brain Injury: A Tensor-Based Morphometry Study

Published online by Cambridge University Press:  13 August 2012

Kimberly D.M. Farbota ,
Aparna Sodhi ,
Barbara B. Bendlin ,
Donald G. McLaren ,
Guofan Xu ,
Howard A. Rowley  and
Sterling C. Johnson
Kimberly D.M. Farbota*
Affiliation:
Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veterans Hospital, Madison, Wisconsin Neuroscience Training Program, University of Wisconsin, Madison, Wisconsin
Aparna Sodhi
Affiliation:
Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veterans Hospital, Madison, Wisconsin Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
Barbara B. Bendlin
Affiliation:
Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veterans Hospital, Madison, Wisconsin Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
Donald G. McLaren
Affiliation:
Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veterans Hospital, Madison, Wisconsin Neuroscience Training Program, University of Wisconsin, Madison, Wisconsin
Guofan Xu
Affiliation:
Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veterans Hospital, Madison, Wisconsin Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
Howard A. Rowley
Affiliation:
Department of Radiology, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
Sterling C. Johnson
Affiliation:
Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veterans Hospital, Madison, Wisconsin Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin
*
Correspondence and reprint requests to: Kimberly D.M. Farbota, Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veterans Hospital, J5M/162 CSC, 600 Highland Avenue, Madison, Wisconsin, 53792. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

After traumatic injury, the brain undergoes a prolonged period of degenerative change that is paradoxically accompanied by cognitive recovery. The spatiotemporal pattern of atrophy and the specific relationships of atrophy to cognitive changes are ill understood. The present study used tensor-based morphometry and neuropsychological testing to examine brain volume loss in 17 traumatic brain injury (TBI) patients and 13 controls over a 4-year period. Patients were scanned at 2 months, 1 year, and 4 years post-injury. High-dimensional warping procedures were used to create change maps of each subject's brain for each of the two intervals. TBI patients experienced volume loss in both cortical areas and white matter regions during the first interval. We also observed continuing volume loss in extensive regions of white matter during the second interval. Neuropsychological correlations indicated that cognitive tasks were associated with subsequent volume loss in task-relevant regions. The extensive volume loss in brain white matter observed well beyond the first year post-injury suggests that the injured brain remains malleable for an extended period, and the neuropsychological relationships suggest that this volume loss may be associated with subtle cognitive improvements. (JINS, 2012, 18, 1–13)

Keywords

Longitudinal studiesRecovery of functionBrain injurieshumansNeurosciencesMagnetic resonance imagingChronic brain injuriesBrain mappingApoptosisNecrosis
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 18 , Issue 6 , November 2012 , pp. 1006 - 1018
Copyright
Copyright © The International Neuropsychological Society 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, C.V., Bigler, E.D., Blatter, D.D. (1995). Frontal lobe lesions, diffuse damage, and neuropsychological functioning in traumatic brain-injured patients. Journal of Clinical and Experimental Neuropsychology, 17(6), 900–908.CrossRefGoogle ScholarPubMed
Anderson, V., Godfrey, C., Rosenfeld, J.V., Catroppa, C. (2012). Intellectual ability 10 years after traumatic brain injury in infancy and childhood: What predicts outcome? Journal of Neurotrauma, 29(1), 143–153.CrossRefGoogle ScholarPubMed
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(2), 503–514.CrossRefGoogle ScholarPubMed
Bigler, E.D., Anderson, C.V., Blatter, D.D. (2002). Temporal lobe morphology in normal aging and traumatic brain injury. AJNR American Journal of Neuroradiology, 23(2), 255–266.Google ScholarPubMed
Bigler, E.D., Maxwell, W.L. (2011). Neuroimaging and neuropathology of TBI. Neurorehabilitation, 28(2), 63–74.CrossRefGoogle ScholarPubMed
Bombardier, C.H., Fann, J.R., Temkin, N.R., Esselman, P.C., Barber, J., Dikmen, S.S. (2010). Rates of major depressive disorder and clinical outcomes following traumatic brain injury. Journal of the American Medical Association, 303(19), 1938–1945.CrossRefGoogle ScholarPubMed
Cernich, A.N., Kurtz, S.M., Mordecai, K.L., Ryan, P.B. (2010). Cognitive rehabilitation in traumatic brain injury. Current Treatment Options in Neurology, 12(5), 412–423.CrossRefGoogle ScholarPubMed
Chen, H.C., Fong, T.H., Lee, A.W., Chiu, W.T. (2011). Autophagy is activated in injured neurons and inhibited by methylprednisolone after experimental spinal cord injury. Spine, 37(6), 470–475.CrossRefGoogle Scholar
Clark, R.S., Bayir, H., Chu, C.T., Alber, S.M., Kochanek, P.M., Watkins, S.C. (2008). Autophagy is increased in mice after traumatic brain injury and is detectable in human brain after trauma and critical illness. Autophagy, 4(1), 88–90.CrossRefGoogle ScholarPubMed
Demir, S.O., Altinok, N., Aydin, G., Koseoglu, F. (2006). Functional and cognitive progress in aphasic patients with traumatic brain injury during post-acute phase. Brain Injury, 20(13-14), 1383–1390.CrossRefGoogle ScholarPubMed
Dikmen, S.S., Corrigan, J.D., Levin, H.S., Machamer, J., Stiers, W., Weisskopf, M.G. (2009). Cognitive outcome following traumatic brain injury. Journal of Head Trauma and Rehabilitation, 24(6), 430–438.CrossRefGoogle ScholarPubMed
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(12), 1433–1440.CrossRefGoogle ScholarPubMed
Engel, S., Schluesener, H., Mittelbronn, M., Seid, K., Adjodah, D., Wehner, H.D., Meyermann, R. (2000). Dynamics of microglial activation after human traumatic brain injury are revealed by delayed expression of macrophage-related proteins MRP8 and MRP14. Acta Neuropathologica, 100(3), 313–322.CrossRefGoogle ScholarPubMed
Farkas, O., Povlishock, J.T. (2007). Cellular and subcellular change evoked by diffuse traumatic brain injury: A complex web of change extending far beyond focal damage. Progress in Brain Research, 161, 43–59.CrossRefGoogle ScholarPubMed
Fox, G.B., Faden, A.I. (1998). Traumatic brain injury causes delayed motor and cognitive impairment in a mutant mouse strain known to exhibit delayed Wallerian degeneration. Journal of Neuroscience Research, 53(6), 718–727.3.0.CO;2-8>CrossRefGoogle Scholar
Frencham, K.A., Fox, A.M., Maybery, M.T. (2005). Neuropsychological studies of mild traumatic brain injury: A meta-analytic review of research since 1995. Journal of Clinical and Experimental Neuropsychology, 27(3), 334–351.CrossRefGoogle ScholarPubMed
Gale, S.D., Burr, R.B., Bigler, E.D., Blatter, D. (1993). Fornix degeneration and memory in traumatic brain injury. Brain Research Bulletin, 32(4), 345–349.CrossRefGoogle ScholarPubMed
Gale, S.D., Johnson, S.C., Bigler, E.D., Blatter, D.D. (1995). Nonspecific white matter degeneration following traumatic brain injury. Journal of the International Neuropsychological Society, 1(1), 17–28.CrossRefGoogle ScholarPubMed
Hua, X., Leow, A.D., Lee, S., Klunder, A.D., Toga, A.W., Lepore, N., Thompson, P.M. (2008). 3D characterization of brain atrophy in Alzheimer's disease and mild cognitive impairment using tensor-based morphometry. Neuroimage, 41(1), 19–34.CrossRefGoogle ScholarPubMed
Johanson, C., Stopa, E., Baird, A., Sharma, H. (2011). Traumatic brain injury and recovery mechanisms: Peptide modulation of periventricular neurogenic regions by the choroid plexus-CSF nexus. Journal of Neural Transmission, 118(1), 115–133.CrossRefGoogle ScholarPubMed
Kelley, B.J., Farkas, O., Lifshitz, J., Povlishock, J.T. (2006). Traumatic axonal injury in the perisomatic domain triggers ultrarapid secondary axotomy and Wallerian degeneration. Experimental Neurology, 198(2), 350–360.CrossRefGoogle ScholarPubMed
Kelley, B.J., Lifshitz, J., Povlishock, J.T. (2007). Neuroinflammatory responses after experimental diffuse traumatic brain injury. Journal of Neuropathology and Experimental Neurology, 66(11), 989–1001.CrossRefGoogle ScholarPubMed
Keren, O., Reznik, J., Groswasser, Z. (2001). Combined motor disturbances following severe traumatic brain injury: An integrative long-term treatment approach. Brain Injury, 15(7), 633–638.CrossRefGoogle ScholarPubMed
Kim, J., Avants, B., Patel, S., Whyte, J., Coslett, B.H., Pluta, J., Gee, J.C. (2008). Structural consequences of diffuse traumatic brain injury: A large deformation tensor-based morphometry study. Neuroimage, 39(3), 1014–1026.CrossRefGoogle ScholarPubMed
Kiraly, M., Kiraly, S.J. (2007). Traumatic brain injury and delayed sequelae: A review--traumatic brain injury and mild traumatic brain injury (concussion) are precursors to later-onset brain disorders, including early-onset dementia. Scientific World Journal, 7, 1768–1776.CrossRefGoogle ScholarPubMed
Leow, A.D., Klunder, A.D., Jack, C.R. Jr., Toga, A.W., Dale, A.M., Bernstein, M.A., Thompson, P.M. (2006). Longitudinal stability of MRI for mapping brain change using tensor-based morphometry. Neuroimage, 31(2), 627–640.CrossRefGoogle ScholarPubMed
Leow, A.D., Yanovsky, I., Parikshak, N., Hua, X., Lee, S., Toga, A.W., Thompson, P.M. (2009). Alzheimer's disease neuroimaging initiative: A one-year follow up study using tensor-based morphometry correlating degenerative rates, biomarkers and cognition. Neuroimage, 45(3), 645–655.CrossRefGoogle Scholar
Levine, B., Kovacevic, N., Nica, E.I., Cheung, G., Gao, F., Schwartz, M.L., Black, S.E. (2008). The Toronto traumatic brain injury study: Injury severity and quantified MRI. Neurology, 70(10), 771–778.CrossRefGoogle ScholarPubMed
Lifshitz, J., Kelley, B.J., Povlishock, J.T. (2007). Perisomatic thalamic axotomy after diffuse traumatic brain injury is associated with atrophy rather than cell death. Journal of Neuropathology and Experimental Neurology, 66(3), 218–229.CrossRefGoogle ScholarPubMed
Liu, C.L., Chen, S., Dietrich, D., Hu, B.R. (2008). Changes in autophagy after traumatic brain injury. Journal of Cerebral Blood Flow and Metabolism, 28(4), 674–683.CrossRefGoogle ScholarPubMed
MacKenzie, J.D., Siddiqi, F., Babb, J.S., Bagley, L.J., Mannon, L.J., Sinson, G.P., Grossman, R.I. (2002). Brain atrophy in mild or moderate traumatic brain injury: A longitudinal quantitative analysis. AJNR American Journal of Neuroradiology, 23(9), 1509–1515.Google ScholarPubMed
Masel, B.E., DeWitt, D.S. (2010). Traumatic brain injury: A disease process, not an event. Journal of Neurotrauma, 27(8), 1529–1540.CrossRefGoogle ScholarPubMed
Maxwell, W.L., Povlishock, J.T., Graham, D.L. (1997). A mechanistic analysis of nondisruptive axonal injury: A review. Journal of Neurotrauma, 14(7), 419–440.CrossRefGoogle ScholarPubMed
Povlishock, J.T. (1993). Pathobiology of traumatically induced axonal injury in animals and man. Annals of Emergency Medicine, 22(6), 980–986.CrossRefGoogle ScholarPubMed
Povlishock, J.T., Christman, C.W. (1995). The pathobiology of traumatically induced axonal injury in animals and humans: A review of current thoughts. Journal of Neurotrauma, 12(4), 555–564.CrossRefGoogle ScholarPubMed
Sidaros, A., Skimminge, A., Liptrot, M.G., Sidaros, K., Engberg, A.W., Herning, M., Rostrup, E. (2009). Long-term global and regional brain volume changes following severe traumatic brain injury: A longitudinal study with clinical correlates. Neuroimage, 44(1), 1–8.CrossRefGoogle ScholarPubMed
Singleton, R.H., Zhu, J., Stone, J.R., Povlishock, J.T. (2002). Traumatically induced axotomy adjacent to the soma does not result in acute neuronal death. Journal of Neuroscience, 22(3), 791–802.CrossRefGoogle Scholar
Siren, A.L., Radyushkin, K., Boretius, S., Kammer, D., Riechers, C.C., Natt, O., Ehrenreich, H. (2006). Global brain atrophy after unilateral parietal lesion and its prevention by erythropoietin. Brain, 129(Pt 2), 480–489.CrossRefGoogle ScholarPubMed
Stern, B., Stern, J.M. (1985). Neuropsychological outcome during late stage of recovery from brain injury: A proposal. Scandinavian Journal of Rehabilitation Medicine (Supplement), 12, 27–30.Google ScholarPubMed
Takeuchi, S., Nawashiro, H. (2011). Atrophy after traumatic axonal injury. Archives of Neurology, 68(8), 1090.CrossRefGoogle ScholarPubMed
Tao, G., Datta, S., He, R., Nelson, F., Wolinsky, J.S., Narayana, P.A. (2009). Deep gray matter atrophy in multiple sclerosis: A tensor based morphometry study. Journal of Neurological Science, 282(1-2), 39–46.CrossRefGoogle Scholar
Trivedi, M.A., Ward, M.A., Hess, T.M., Gale, S.D., Dempsey, R.J., Rowley, H.A., Johnson, S.C. (2007). Longitudinal changes in global brain volume between 79 and 409 days after traumatic brain injury: Relationship with duration of coma. Journal of Neurotrauma, 24(5), 766–771.CrossRefGoogle ScholarPubMed
Warner, M.A., Youn, T.S., Davis, T., Chandra, A., Marquez de la Plata, C., Moore, C., Diaz-Arrastia, R. (2010). Regionally selective atrophy after traumatic axonal injury. Archives of Neurology, 67(11), 1336–1344.CrossRefGoogle ScholarPubMed
Whitnall, L., McMillan, T.M., Murray, G.D., Teasdale, G.M. (2006). Disability in young people and adults after head injury: 5-7 year follow up of a prospective cohort study. J Neurology, Neurosurgery, and Psychiatry, 77(5), 640–645.CrossRefGoogle ScholarPubMed
Zhang, Y.B., Li, S.X., Chen, X.P., Yang, L., Zhang, Y.G., Liu, R., Tao, L.Y. (2008). Autophagy is activated and might protect neurons from degeneration after traumatic brain injury. Neuroscience Bulletin, 24(3), 143–149.CrossRefGoogle ScholarPubMed