Abstract
The presence of a postconcussion syndrome (PCS) induces substantial socio-professional troubles in mild traumatic brain injury (mTBI) patients. Although the exact origin of these disorders is not known, they may be the consequence of diffuse axonal injury (DAI) impacting structural integrity. In the present study, we compared structural integrity at the subacute and late stages after mTBI and in case of PCS, using diffusion-weighted imaging (DWI). Fifty-three mTBI patients were investigated and compared with 40 healthy controls. All patients underwent a DWI examination at the subacute (8–21 days) and late (6 months) phases after injury. MTBI patients with PCS were detected at the subacute phase using the ICD-10 classification. Groupwise differences in structural integrity were investigated using Tract-Based Spatial Statistics (TBSS). A loss of structural integrity was found in mTBI patients at the subacute phase but partially resolved over time. Moreover, we observed that mTBI patients with PCS had greater and wider structural impairment than patients without PCS. These damages persisted over time for PCS patients, while mTBI patients without PCS partly recovered. In conclusion, our results strengthen the relationship between structural integrity and PCS.
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Notes
The socio-cultural level is function of the number of years of education, ranging from 1 (primary school or less) to 5 (university degree), through 3 (Bachelor) (GREFEX 2001).
FSL, FMRIB, Oxford, UK: www.fmrib.ox.ac.uk/fsl/.
There were only two patients in PCS− group with GCS = 14, all other GCS scores were equal to 15.
References
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.
Bazarian, J. (2010). Diagnosis of mild traumatic brain injury after a concussion. Journal of Head Trauma Rehabilitation, 25, 225–227.
Bazarian, 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.
Belanger, H., Vanderploeg, R., Curtiss, G., & Warden, D. (2007). Recent neuroimaging techniques in mild traumatic brain injury. Journal of Neuropsychiatry and Clinical Neurosciences, 19, 5–20.
Bendlin, B. B., Riesa, M. L., Lazar, M., Alexander, A. L., Dempsey, R. J., Rowley, H. A., et al. (2008). Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neuroimage, 42, 503–514.
Bigler, E. D. (2008). Neuropsychology and clinical neuroscience of persistent post-concussive syndrome. Journal of the International Neuropsychological Society, 14, 1–22.
Bigler, E. D. (2010). Neuroimaging in mild traumatic brain injury. Psychological Injury and Law, 3, 36–49.
Bigler, E. D., & Bazarian, J. (2010). Diffusion tensor imaging: A biomarker for mild traumatic brain injury? Neurology, 74, 626–627.
Boake, C., McCauley, S. R., Levin, H. S., Pedroza, C., Contant, C. F., Song, J. S., et al. (2005). Diagnostic criteria for postconcussional syndrome after mild to moderate traumatic brain injury. Journal of Neuropsychiatry and Clinical Neurosciences, 17, 350–356.
Budde, M. D., Kim, J. H., Liang, H.-F., Schmidt, R. E., Russell, J. H., Cross, A. H., et al. (2007). Toward accurate diagnosis of white matter pathology using diffusion tensor imaging. Magnetic Resonance in Medicine, 57, 688– 695.
Carroll, L., Cassidy, J. D., Peloso, P., Borg, J., Von Holst, H., Holm, L., et al. (2004). Prognosis for mild traumatic brain injury: Results of the WHO collaborating centre task force on mild traumatic brain injury. Journal of Rehabilitation Medicine, 36, 84–105.
Concha, L., Livy, D. J., Beaulieu, C., Wheatley, B. M., & Gross, D. W. (2010). In vivo diffusion tensor imaging and histopathology of the fimbria-fornix in temporal lobe epilepsy. Journal of Neurosciences, 30, 996–1002.
Crawford, S., Wenden, F. J., & Wade, D. T. (1996). The Rivermead head injury follow-up questionnaire. A study of a new rating scale and other measures to evaluate outcomes after head injury. Journal of Neurology, Neurosurgery, and Psychiatry, 60, 510–514.
Dikmen, S., McLean, A., & Temkin, N. (1986). Neuropsychological and psychosocial consequences of minor head injury. Journal of Neurology, Neurosurgery, and Psychiatry, 46, 1227–1232.
DSM-IV (1994). Diagnostic and Statistical Manual of Mental Disorders DSM-IV-TR Fourth Edition (Text Revision). Washington, DC: American Psychiatric Association (APA).
Eyres, S., Carey, A., Gilworth, G., Neumann, V., & Tennant, A. (2005). Contruct validity and reliability of the Rivermead Post-Concussion Questionnaire. Clinical Rehabilitation, 19, 878–887.
Fitzgerald, D. B., & Crosson, B. A. (2011). Diffusion weighted imaging and neuropsychological correlates in adults with mild traumatic brain injury. International Journal of Psychophysiology, 82, 79–85.
GREFEX (2001). Groupe de réflexion sur l’évaluation des fonctions exécutives. Revue de Neuropsychologie, 11, 383–434. in French.
Hall, R. C. W., Hall, R. C. W., & Chapman, M. J. (2005). Definition, diagnosis, and forensic implications of postconcussional syndrome. Psychosomatics, 46, 195–202.
Huisman, T. A., Schwamm, L. H., Schaefer, P. W., Koroshetz, W. J., Shetty-Alva, N., Ozsunar, Y., et al. (2004). Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. American Journal of Neuroradiology, 25, 370–376.
ICD-10 (1993). The International Classification of Diseases and Health Related Problems (10e ed.). Geneva, Switzerland: World Health Organization (WHO).
Inglese, M., Makani, S., Johnson, G., Cohen, B. A., Silver, J. A., Gonen, O., et al. (2005). Diffuse axonal injury in mild traumatic brain injury: A diffusion tensor imaging study. Journal of Neurosurgery, 103, 298–303.
Iverson, G. L. (2005). Outcome from mild traumatic brain injury. Current Opinion in Psychiatry, 18, 301–317.
Johansen-Berg, H., & Rushworth, M. (2009). Using diffusion imaging to study human connectional anatomy. Annual Review of Neurosciences, 32, 75–94.
Kay, T., Harrington, D. E., Adams, R., Anderson, T., Berrol, S., Cicerone, K., et al. (1993). Definition of mild traumatic brain injury. Journal of Head Trauma Rehabilitation, 8, 86–87.
King, N. S., Crawford, S., Wenden, F. J., Moss, N. E. G., & Wade, D. T. (1995). The rivermead post concussion symptoms questionnaire: A measure of symptoms commonly experienced after head injury and its reliability. Journal of Neurology, 242, 587–592.
Kinnunen, K. M., Greenwood, R., Powell, J. H., Leech, R., Hawkins, P. C., Bonnelle, V., et al. (2011). White matter damage and cognitive impairment after traumatic brain injury. Brain, 134, 449–463.
Kraus, J. F., MacArthur, D. L., & Silberman, T. A. (1994). Epidemiology of mild brain injury. Seminars in Neurology, 14, 1–7.
Kraus, M. F., Susmaras, T., Caughlin, B. P., Walker, C. J., Sweeney, J. A., & Little, D. M. (2007). White matter integrity and cognition in chronic traumatic brain injury: A diffusion tensor imaging study. Brain, 130, 2508–2519.
Langlois, J. A., Rutland-Brown, W., & Wald, M. M. (2006). The epidemiology and impact of traumatic brain injury: A brief review. Journal of Head Trauma Rehabilitation, 21, 375–378.
Levin, H., Wilde, E., Troyanskaya, M., Petersen, N., Scheibel, R., Newsome, M., et al. (2010). Diffusion tensor imaging of mild to moderate blast-related traumatic brain injury and its sequelae. Journal of Neurotrauma, 27, 683–694.
Lipton, M. L., Gulko, E., Zimmerman, M. E., Friedman, B. W., Kim, M., Gellella, E., et al. (2009). Diffusion-tensor imaging implicates prefrontal axonal injury in executive function impairment following very mild traumatic brain injury. Radiology, 252, 816–824.
Mayer, A. R., Ling, J., Mannell, M. V., Gasparovic, C., Phillips, J. P., Doezema, D., et al. (2010). A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology, 74, 643–650.
McCrea, M. (2008). Mild traumatic b rain injury and p ostconcussion syndrome: T he new e vidence base for d iagnosis and treatment. Oxford University Press, Oxford: United Kingdom.
Messé, A., Caplain, S., Paradot, G., Garrigue, D., Mineo, J. F., Soto Ares, G., et al. (2010). Diffusion tensor imaging and white matter lesions at the subacute stage in mild traumatic brain injury with persistent neurobehavioral impairment. Human Brain Mapping, 32, 999–1011.
Mori, S., Wakana, S., Van Zijl, P. C. M., & Nagae-Poetscher, L. M. (2005). MRI Atlas of human white matter, First edition. Amsterdam, The Netherlands: Elsevier.
Nakayama, N., Okumura, A., Shinoda, J., Yasokawa, Y.-T., Miwa, K., Yoshimura, S.-I., et al. (2006). Evidence for white matter disruption in traumatic brain injury without macroscopic lesions. Journal of Neurology, Neurosurgery, and Psychiatry, 77, 850–255.
Niogi, S., & Mukherjee, P. (2010). Diffusion tensor imaging of mild traumatic brain injury. The Journal of Head Trauma Rehabilitation, 25, 241–255.
Parizel, P. M., Van Goethem, J. W., Özsarlak, Ö., Maes, M., & Phillips, C. D. (2005). New developments in the neuroradiological diagnosis of craniocerebral trauma. European Radiology, 15, 569–281.
Rutgers, D. R., Toulgoat, F., Cazejust, J., Fillard, P., Lasjaunias, P., & Ducreux, D. (2008). White matter abnormalities in mild traumatic brain injury: A diffusion tensor imaging study. American Journal of Neuroradiology, 29, 514–219.
Salmond, C. H., Menon, D. K., Chatfield, D. A., Williams, G. B., Pena, A., Sahakian, B. J., et al. (2006). Diffusion tensor imaging in chronic head injury survivors: Correlations with learning and memory indices. Neuroimage, 29, 117–224.
Scheid, R., Walther, K., Guthke, T., Preul, C., & Von Cramon, D. Y. (2006). Cognitive sequelae of diffuse axonal injury. Archives of Neurology, 63, 418–224.
Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17, 143–255.
Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., et al. (2006). Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. Neuroimage, 31, 1487–1505.
Smith, S. M., & Nichols, T. E. (2009). Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage, 44, 83–98.
Smits, M., Houston, G. C., Dippel, D. W., Wielopolski, P. A., Vernooij, M. W., Koudstaal, P. J., et al. (2011). Microstructural brain injury in post-concussion syndrome after minor head injury. Neuroradiology, 53, 553–563.
Song, S. K., Sun, S. W., Ju, W. K., Lin, S. J., Cross, A. H., & Neufeld, A. H. (2003). Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage, 20, 1714–1722.
Stålnacke, B. M., Björnstig, U., Karlsson, K., & Sojka, P. (2005). One-year follow-up of mild traumatic brain injury: Post-concussion symptoms, disabilities and life satisfaction in relation to serum levels of S-100B and neurone-specific enolase in acute phase. Journal of Rehabilitation Medicine, 37, 300–305.
Tiret, L., Hausherr, E., Thicoipe, M., Garros, B., Maurette, P., Castel, J. P., et al. (1990). The epidemiology of head trauma in aquitaine (France), 1986: A community-based study of hospital admissions and death. International Journal of Epidemiology, 19, 133–140.
Von Wild, K. R. (2008). Posttraumatic rehabilitation and one year outcome following acute traumatic brain injury (TBI): Data from the well defined population based German prospective study 2000–2002. Acta Neurochirurgica, 101, 55–60.
Wilde, E. A., Whiteneck, G. G., Bogner, J., Bushnik, T., Cifu, D. X., Dikmen, S., et al. (2010). Recommendations for the use of common outcome measures in traumatic brain injury research. Archives of Physical Medicine and Rehabilitation, 91, 1650–1660.
Willer, B., & Leddy, J. J. (2006). Management of concussion and post-concussion syndrome. Current Treatment Options in Neurology, 8, 415–426.
Woolrich, M., Jbabdi, S., Patenaude, B., Chappell, M., Makni, S., Behrens, T., et al. (2009). Bayesian analysis of neuroimaging data in FSL. Neuroimage, 45, S173–186.
Yeates, K. O., & Taylor, H. G. (2005). Neurobehavioural outcomes of mild head injury in children and adolescents. Pedriatic Rehabilitation, 8, 5–16.
Acknowledgements
We would like to thank all study participants. The authors are grateful to the MRI acquisition team (CENIR, Paris, France) for capital support.
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This study was initiated by the IRME (Institut pour la Recherche sur la Moelle Epinière et l’Encéphale) and supported by a grant from the GMF (Garantie Mutuelle des Fonctionnaires).
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Messé, A., Caplain, S., Pélégrini-Issac, M. et al. Structural integrity and postconcussion syndrome in mild traumatic brain injury patients. Brain Imaging and Behavior 6, 283–292 (2012). https://doi.org/10.1007/s11682-012-9159-2
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DOI: https://doi.org/10.1007/s11682-012-9159-2