Acute and Chronic Changes in Diffusivity Measures after Sports Concussion
Abstract
Despite negative neuroimaging findings in concussed athletes, studies indicate that the acceleration and deceleration of the brain after concussive impacts result in metabolic and electrophysiological alterations that may be attributable to changes in white matter resulting from biomechanical strain. In the present study we investigated the effects of sports concussion on white matter using three different diffusion tensor imaging (DTI) measures: fractional anisotropy (FA), mean diffusivity (MD), and axial diffusivity (AD). We compared a group of 10 non-concussed athletes with a group of 18 concussed athletes of the same age (mean age 22.5 years) and education (mean 16 years) using a voxel-based approach (VBA) in both the acute and chronic post-injury phases. All concussed athletes were scanned 1–6 days post-concussion and again 6 months later in a 3T Siemens Trio™ MRI. Three 2×2 repeated-measures analyses of variance (ANOVAs) were conducted, one for each measure of DTI used in the current study. There was a main group effect of FA, which was increased in dorsal regions of both corticospinal tracts (CST) and in the corpus callosum in concussed athletes at both time points. There was a main group effect of AD in the right CST, where concussed athletes showed elevated values relative to controls at both time points. MD values were decreased in concussed athletes, in whom analyses revealed significant group differences in the CST and corpus callosum at both time points. Although the use of VBA does limit the analyses to large tracts, and it has clinical limitations with regard to individual analyses, our results nevertheless indicate that sports concussions do result in changes in diffusivity in the corpus callosum and CST that are not detected using conventional neuroimaging techniques.
Get full access to this article
View all available purchase options and get full access to this article.
References
Alexander D.C.Pierpaoli C.Gee J.C.2001. Spatial transformations of diffusion tensor magnetic resonance imagesIEEE Trans. Med. Imaging201131-1139. Alexander, D.C., Pierpaoli, C., Basser, P.J., and Gee, J.C. (2001). Spatial transformations of diffusion tensor magnetic resonance images. IEEE Trans. Med. Imaging 20, 1131–1139.
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 injuryAJNR Am. J. Neuroradiol.23794-802. Arfanakis, K., Haughton, V.M., Carew, J.D., Rogers, B.P., Dempsey, R.J., and Meyerand, M.E. (2002). Diffusion tensor MR imaging in diffuse axonal injury. AJNR Am. J. Neuroradiol. 23, 794–802.
Aubry M.Cantu R.Dvorak J.Graf-Baumann T.Johnston K.Kelly J.Lovell M.McCrory P.Meeuwisse W.Schamasch P.2002. Summary and agreement statement of the First International Conference on Concussion in Sport, Vienna 2001. Recommendations for the improvement of safety and health of athletes who may suffer concussive injuriesBr. J. Sports Med.366-10. Aubry, M., Cantu, R., Dvorak, J., Graf-Baumann, T., Johnston, K., Kelly, J., Lovell, M., McCrory, P., Meeuwisse, W., and Schamasch, P. (2002). Summary and agreement statement of the First International Conference on Concussion in Sport, Vienna 2001. Recommendations for the improvement of safety and health of athletes who may suffer concussive injuries. Br. J. Sports Med. 36, 6–10.
Bain A.C.Meaney D.F.2000. Tissue-level thresholds for axonal damage in an experimental model of central nervous system white matter injuryJ. Biomech. Eng.122615-622. Bain, A.C., and Meaney, D.F. (2000). Tissue-level thresholds for axonal damage in an experimental model of central nervous system white matter injury. J. Biomech. Eng. 122, 615–622.
Barr M.2005The Human Nervous System: An Anatomical Viewpoint8thLippincott Williams & WilkinsBaltimore. Barr, M. (2005). The Human Nervous System: An Anatomical Viewpoint, 8th ed. Lippincott Williams & Wilkins: Baltimore.
Bhagat Y.A.Emery D.J.Shuaib A.Sher F.Rizvi N.H.Akhtar N.Clare T.L.Leatherdale T.Beaulieu C.2006. The relationship between diffusion anisotropy and time of onset after strokeJ. Cereb. Blood Flow Metab.261442-1450. Bhagat, Y.A., Emery, D.J., Shuaib, A., Sher, F., Rizvi, N.H., Akhtar, N., Clare, T.L., Leatherdale, T., and Beaulieu, C. (2006). The relationship between diffusion anisotropy and time of onset after stroke. J. Cereb. Blood Flow Metab. 26, 1442–1450.
Bigler E.D.1999. Neuroimaging in pediatric traumatic head injury: diagnostic considerations and relationships to neurobehavioral outcomeJ. Head Trauma Rehabil.14406-423. Bigler, E.D. (1999). Neuroimaging in pediatric traumatic head injury: diagnostic considerations and relationships to neurobehavioral outcome. J. Head Trauma Rehabil. 14, 406–423.
Bruce J.M.Echemendia R.J.2009. History of multiple self-reported concussions is not associated with reduced cognitive abilitiesNeurosurgery64100-106discussion 106. Bruce, J.M., and Echemendia, R.J. (2009). History of multiple self-reported concussions is not associated with reduced cognitive abilities. Neurosurgery 64, 100–106; discussion 106.
Buki A.Povlishock J.T.2006. All roads lead to disconnection?—Traumatic axonal injury revisitedActa Neurochir. (Wien.)148181-193discussion 193–194. Buki, A., and Povlishock, J.T. (2006). All roads lead to disconnection?—Traumatic axonal injury revisited. Acta Neurochir. (Wien.) 148, 181–193; discussion 193–194.
Chappell M.H.Ulug A.M.Zhang L.Heitger M.H.Jordan B.D.Zimmerman R.D.Watts R.2006. Distribution of microstructural damage in the brains of professional boxers: a diffusion MRI studyJ. Magn. Reson. Imaging24537-542. Chappell, M.H., Ulug, A.M., Zhang, L., Heitger, M.H., Jordan, B.D., Zimmerman, R.D., and Watts, R. (2006). Distribution of microstructural damage in the brains of professional boxers: a diffusion MRI study. J. Magn. Reson. Imaging 24, 537–542.
Chu Z.Wilde E.A.Hunter J.V.McCauley S.R.Bigler E.D.Troyanskaya M.Yallampalli R.Chia J.M.Levin H.S.2010. Voxel-based analysis of diffusion tensor imaging in mild traumatic brain injury in adolescentsAJNR Am. J. Neuroradiol.31340-346. Chu, Z., Wilde, E.A., Hunter, J.V., McCauley, S.R., Bigler, E.D., Troyanskaya, M., Yallampalli, R., Chia, J.M., and Levin, H.S. (2010). Voxel-based analysis of diffusion tensor imaging in mild traumatic brain injury in adolescents. AJNR Am. J. Neuroradiol. 31, 340–346.
Cubon V.A.Putukian M.Boyer C.Dettwiler A.2011. A diffusion tensor imaging study on the white matter skeleton in individuals with sports-related concussionJ. Neurotrauma28189-201. Cubon, V.A., Putukian, M., Boyer, C., and Dettwiler, A. (2011). A diffusion tensor imaging study on the white matter skeleton in individuals with sports-related concussion. J. Neurotrauma 28, 189–201.
De Beaumont L.Brisson B.Lassonde M.Jolicoeur P.2007. Long-term electrophysiological changes in athletes with a history of multiple concussionsBrain Inj.21631-644. De Beaumont, L., Brisson, B., Lassonde, M., and Jolicoeur, P. (2007). Long-term electrophysiological changes in athletes with a history of multiple concussions. Brain Inj. 21, 631–644.
De Beaumont L.Lassonde M.Leclerc S.Theoret H.2007. Long-term and cumulative effects of sports concussion on motor cortex inhibitionNeurosurgery61329-336discussion 336–327. De Beaumont, L., Lassonde, M., Leclerc, S., and Theoret, H. (2007). Long-term and cumulative effects of sports concussion on motor cortex inhibition. Neurosurgery 61, 329–336; discussion 336–327.
De Beaumont L.Mongeon D.Tremblay S.Messier J.Prince F.Leclerc S.Lassonde M.Theoret H.(accepted). Persistent motor system abnormalities in active concussed athletesNeurology. De Beaumont, L., Mongeon, D., Tremblay, S., Messier, J., Prince, F., Leclerc, S., Lassonde, M., and Theoret, H. (accepted). Persistent motor system abnormalities in active concussed athletes. Neurology.
De Beaumont L.Theoret H.Mongeon D.Messier J.Leclerc S.Tremblay S.Ellemberg D.Lassonde M.2009. Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthoodBrain132695-708. De Beaumont, L., Theoret, H., Mongeon, D., Messier, J., Leclerc, S., Tremblay, S., Ellemberg, D., and Lassonde, M. (2009). Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood. Brain 132, 695–708.
Dikmen S.McLean A.Temkin N.1986. Neuropsychological and psychosocial consequences of minor head injuryJ. Neurol. Neurosurg. Psychiatry491227-1232. Dikmen, S., McLean, A., and Temkin, N. (1986). Neuropsychological and psychosocial consequences of minor head injury. J. Neurol. Neurosurg. Psychiatry 49, 1227–1232.
Ducreux D.Huynh I.Fillard P.Renoux J.Petit-Lacour M.C.Marsot-Dupuch K.Lasjaunias P.2005. Brain MR diffusion tensor imaging and fibre tracking to differentiate between two diffuse axonal injuriesNeuroradiology47604-608. Ducreux, D., Huynh, I., Fillard, P., Renoux, J., Petit-Lacour, M.C., Marsot-Dupuch, K., and Lasjaunias, P. (2005). Brain MR diffusion tensor imaging and fibre tracking to differentiate between two diffuse axonal injuries. Neuroradiology 47, 604–608.
Ducreux D.Nasser G.Lacroix C.Adams D.Lasjaunias P.2005. MR diffusion tensor imaging, fiber tracking, and single-voxel spectroscopy findings in an unusual MELAS caseAJNR Am. J. Neuroradiol.261840-1844. Ducreux, D., Nasser, G., Lacroix, C., Adams, D., and Lasjaunias, P. (2005). MR diffusion tensor imaging, fiber tracking, and single-voxel spectroscopy findings in an unusual MELAS case. AJNR Am. J. Neuroradiol. 26, 1840–1844.
Ellemberg D.Henry L.C.Macciocchi S.N.Guskiewicz K.M.Broglio S.P.2009. Advances in sport concussion assessment: from behavioral to brain imaging measuresJ. Neurotrauma262365-2382. Ellemberg, D., Henry, L.C., Macciocchi, S.N., Guskiewicz, K.M., and Broglio, S.P. (2009). Advances in sport concussion assessment: from behavioral to brain imaging measures. J. Neurotrauma 26, 2365–2382.
Farkas O.Lifshitz J.Povlishock J.T.2006. Mechanoporation induced by diffuse traumatic brain injury: an irreversible or reversible response to injury? JNeurosci.263130-3140. Farkas, O., Lifshitz, J., and Povlishock, J.T. (2006). Mechanoporation induced by diffuse traumatic brain injury: an irreversible or reversible response to injury? J. Neurosci. 26, 3130–3140.
Gaetz M.Goodman D.Weinberg H.2000. Electrophysiological evidence for the cumulative effects of concussionBrain Inj.141077-1088. Gaetz, M., Goodman, D., and Weinberg, H. (2000). Electrophysiological evidence for the cumulative effects of concussion. Brain Inj. 14, 1077–1088.
Gasparovic C.Yeo R.Mannell M.Ling J.Elgie R.Phillips J.Doezema D.Mayer A.R.2009. Neurometabolite concentrations in gray and white matter in mild traumatic brain injury: an 1H-magnetic resonance spectroscopy studyJ. Neurotrauma261635-1643. Gasparovic, C., Yeo, R., Mannell, M., Ling, J., Elgie, R., Phillips, J., Doezema, D., and Mayer, A.R. (2009). Neurometabolite concentrations in gray and white matter in mild traumatic brain injury: an 1H-magnetic resonance spectroscopy study. J. Neurotrauma 26, 1635–1643.
Gennarelli T.A.1996. The spectrum of traumatic axonal injuryNeuropathol. Appl. Neurobiol.22509-513. Gennarelli, T.A. (1996). The spectrum of traumatic axonal injury. Neuropathol. Appl. Neurobiol. 22, 509–513.
Gennarelli T.A.Thibault L.E.Tipperman R.Tomei G.Sergot R.Brown M.Maxwell W.L.Graham D.I.Adams J.H.Irvine A.1989. Axonal injury in the optic nerve: a model simulating diffuse axonal injury in the brainJ. Neurosurg.71244-253. Gennarelli, T.A., Thibault, L.E., Tipperman, R., Tomei, G., Sergot, R., Brown, M., Maxwell, W.L., Graham, D.I., Adams, J.H., and Irvine, A. (1989). Axonal injury in the optic nerve: a model simulating diffuse axonal injury in the brain. J. Neurosurg. 71, 244–253.
Gentry L.R.1994. Imaging of closed head injuryRadiology1911-17. Gentry, L.R. (1994). Imaging of closed head injury. Radiology 191, 1–17.
Gerberding J.L.Binder S.2003. Report to Congress on Mild Traumatic Brain Injury in the United States: Steps to Prevent a Serious Public Health ProblemNational Center for Injury Prevention and Control, Centers for Disease Control and PreventionAtlanta56. Gerberding, J.L., and Binder, S. (2003). Report to Congress on Mild Traumatic Brain Injury in the United States: Steps to Prevent a Serious Public Health Problem. National Center for Injury Prevention and Control, Centers for Disease Control and Prevention: Atlanta, p. 56.
Giza C.C.Hovda D.A.2001. The neurometabolic cascade of concussionJ. Athl. Train.36228-235. Giza, C.C., and Hovda, D.A. (2001). The neurometabolic cascade of concussion. J. Athl. Train. 36, 228–235.
Green H.A.Pena A.Price C.J.Warburton E.A.Pickard J.D.Carpenter T.A.Gillard J.H.2002. Increased anisotropy in acute stroke: a possible explanationStroke331517-1521. Green, H.A., Pena, A., Price, C.J., Warburton, E.A., Pickard, J.D., Carpenter, T.A., and Gillard, J.H. (2002). Increased anisotropy in acute stroke: a possible explanation. Stroke 33, 1517–1521.
Guskiewicz K.M.Bruce S.L.Cantu R.C.Ferrara M.S.Kelly J.P.McCrea M.Putukian M.McLeod T.C.2004. Recommendations on management of sport-related concussion: summary of the National Athletic Trainers' Association position statementNeurosurgery55891-895discussion 896. Guskiewicz, K.M., Bruce, S.L., Cantu, R.C., Ferrara, M.S., Kelly, J.P., McCrea, M., Putukian, M., and McLeod, T.C. (2004). Recommendations on management of sport-related concussion: summary of the National Athletic Trainers' Association position statement. Neurosurgery 55, 891–895; discussion 896.
Guskiewicz K.M.Bruce S.L.Cantu R.C.Ferrara M.S.Kelly J.P.McCrea M.Putukian M.Valovich McLeod T.C.2004. National Athletic Trainers' Association Position Statement: Management of Sport-Related ConcussionJ. Athl. Train.39280-297. Guskiewicz, K.M., Bruce, S.L., Cantu, R.C., Ferrara, M.S., Kelly, J.P., McCrea, M., Putukian, M., and Valovich McLeod, T.C. (2004). National Athletic Trainers' Association Position Statement: Management of Sport-Related Concussion. J. Athl. Train. 39, 280–297.
Guskiewicz K.M.McCrea M.Marshall S.W.Cantu R.C.Randolph C.Barr W.Onate J.A.Kelly J.P.2003. Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion StudyJAMA2902549-2555. Guskiewicz, K.M., McCrea, M., Marshall, S.W., Cantu, R.C., Randolph, C., Barr, W., Onate, J.A., and Kelly, J.P. (2003). Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA 290, 2549–2555.
Hartikainen K.M.Waljas M.Isoviita T.Dastidar P.Liimatainen S.Solbakk A.K.Ogawa K.H.Soimakallio S.Ylinen A.Ohman J.2010. Persistent symptoms in mild to moderate traumatic brain injury associated with executive dysfunctionJ. Clin. Exp. Neuropsychol.32767-774. Hartikainen, K.M., Waljas, M., Isoviita, T., Dastidar, P., Liimatainen, S., Solbakk, A.K., Ogawa, K.H., Soimakallio, S., Ylinen, A., and Ohman, J. (2010). Persistent symptoms in mild to moderate traumatic brain injury associated with executive dysfunction. J. Clin. Exp. Neuropsychol. 32, 767–774.
Henry L.C.Tremblay S.Boulanger Y.Ellemberg D.Lassonde M.2010. Neurometabolic changes in the acute phase after sports concussions correlate with symptom severityJ. Neurotrauma2765-76. Henry, L.C., Tremblay, S., Boulanger, Y., Ellemberg, D., and Lassonde, M. (2010). Neurometabolic changes in the acute phase after sports concussions correlate with symptom severity. J. Neurotrauma 27, 65–76.
Henry L.C.Tremblay S.Leclerc S.Khiat A.Boulanger Y.Ellemberg D.Lassonde M.(submitted). Metabolic changes in concussed athletes during the acute and chronic post-injury phases. Henry, L.C., Tremblay, S., Leclerc, S., Khiat, A., Boulanger, Y., Ellemberg, D., and Lassonde, M. (submitted). Metabolic changes in concussed athletes during the acute and chronic post-injury phases.
Hinton-Bayre A.D.Geffen G.2002. Severity of sports-related concussion and neuropsychological test performanceNeurology591068-1070. Hinton-Bayre, A.D., and Geffen, G. (2002). Severity of sports-related concussion and neuropsychological test performance. Neurology 59, 1068–1070.
Hofer S.Frahm J.2006. Topography of the human corpus callosum revisited—comprehensive fiber tractography using diffusion tensor magnetic resonance imagingNeuroimage32989-994. Hofer, S., and Frahm, J. (2006). Topography of the human corpus callosum revisited—comprehensive fiber tractography using diffusion tensor magnetic resonance imaging. Neuroimage 32, 989–994.
Holbourn A.1943. Mechanisms of head injuriesLancet2438-441. Holbourn, A. (1943). Mechanisms of head injuries. Lancet 2, 438–441.
Holbourn A.1945. The mechanics of brain injuriesBr. Med. Bulletin3147-149. Holbourn, A. (1945). The mechanics of brain injuries. Br. Med. Bulletin 3, 147–149.
Holm L.Cassidy J.D.Carroll L.J.Borg J.2005. Summary of the WHO Collaborating Centre for Neurotrauma Task Force on Mild Traumatic Brain InjuryJ. Rehabil. Med.37137-141. Holm, L., Cassidy, J.D., Carroll, L.J., and Borg, J. (2005). Summary of the WHO Collaborating Centre for Neurotrauma Task Force on Mild Traumatic Brain Injury. J. Rehabil. Med. 37, 137–141.
Huisman T.A.Schwamm L.H.Schaefer P.W.Koroshetz W.J.Shetty-Alva N.Ozsunar Y.Wu O.Sorensen A.G.2004. Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injuryAJNR Am. J. Neuroradiol.25370-376. Huisman, T.A., Schwamm, L.H., Schaefer, P.W., Koroshetz, W.J., Shetty-Alva, N., Ozsunar, Y., Wu, O., and Sorensen, A.G. (2004). Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. AJNR Am. J. Neuroradiol. 25, 370–376.
Hurley R.A.McGowan J.C.Arfanakis K.Taber K.H.2004. Traumatic axonal injury: novel insights into evolution and identificationJ. Neuropsychiatry Clin. Neurosci.161-7. Hurley, R.A., McGowan, J.C., Arfanakis, K., and Taber, K.H. (2004). Traumatic axonal injury: novel insights into evolution and identification. J. Neuropsychiatry Clin. Neurosci. 16, 1–7.
Jenkinson M.Smith S.2001. A global optimisation method for robust affine registration of brain imagesMed. Image Anal.5143-156. Jenkinson, M., and Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Med. Image Anal. 5, 143–156.
Johnston K.M.Ptito A.Chankowsky J.Chen J.K.2001. New frontiers in diagnostic imaging in concussive head injuryClin. J. Sport Med.11166-175. Johnston, K.M., Ptito, A., Chankowsky, J., and Chen, J.K. (2001). New frontiers in diagnostic imaging in concussive head injury. Clin. J. Sport Med. 11, 166–175.
Kochunov P.Lancaster J.L.Thompson P.Woods R.Mazziotta J.Hardies J.Fox P.2001. Regional spatial normalization: toward an optimal targetJ. Comput. Assist. Tomogr.25805-816. Kochunov, P., Lancaster, J.L., Thompson, P., Woods, R., Mazziotta, J., Hardies, J., and Fox, P. (2001). Regional spatial normalization: toward an optimal target. J. Comput. Assist. Tomogr. 25, 805–816.
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 studyBrain1302508-2519. Kraus, M.F., Susmaras, T., Caughlin, B.P., Walker, C.J., Sweeney, J.A., and Little, D.M. (2007). White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain 130, 2508–2519.
Kumar R.Gupta R.K.Husain M.Chaudhry C.Srivastava A.Saksena S.Rathore R.K.2009. Comparative evaluation of corpus callosum DTI metrics in acute mild and moderate traumatic brain injury: its correlation with neuropsychometric testsBrain Inj.23675-685. Kumar, R., Gupta, R.K., Husain, M., Chaudhry, C., Srivastava, A., Saksena, S., and Rathore, R.K. (2009). Comparative evaluation of corpus callosum DTI metrics in acute mild and moderate traumatic brain injury: its correlation with neuropsychometric tests. Brain Inj. 23, 675–685.
Lang F.Busch G.L.Ritter M.Volkl H.Waldegger S.Gulbins E.Haussinger D.1998. Functional significance of cell volume regulatory mechanismsPhysiol. Rev.78247-306. Lang, F., Busch, G.L., Ritter, M., Volkl, H., Waldegger, S., Gulbins, E., and Haussinger, D. (1998). Functional significance of cell volume regulatory mechanisms. Physiol. Rev. 78, 247–306.
Lee J.W.Choi C.G.Chun M.H.2006. Usefulness of diffusion tensor imaging for evaluation of motor function in patients with traumatic brain injury: three case studiesJ. Head Trauma Rehabil.21272-278. Lee, J.W., Choi, C.G., and Chun, M.H. (2006). Usefulness of diffusion tensor imaging for evaluation of motor function in patients with traumatic brain injury: three case studies. J. Head Trauma Rehabil. 21, 272–278.
Lepore N.Brun C.A.Chiang M.C.Chou Y.Y.Dutton R.A.Hayashi K.M.Lopez O.L.Aizenstein H.J.Toga A.W.Becker J.T.Thompson P.M.2006. Multivariate statistics of the Jacobian matrices in tensor based morphometry and their application to HIV/AIDSMed. Image Comput. Comput. Assist. Interv. Int. Conf. Med. Image Comput. Comput. Assist. Interv.9191-198. Lepore, N., Brun, C.A., Chiang, M.C., Chou, Y.Y., Dutton, R.A., Hayashi, K.M., Lopez, O.L., Aizenstein, H.J., Toga, A.W., Becker, J.T., and Thompson, P.M. (2006). Multivariate statistics of the Jacobian matrices in tensor based morphometry and their application to HIV/AIDS. Med. Image Comput. Comput. Assist. Interv. Int. Conf. Med. Image Comput. Comput. Assist. Interv. 9, 191–198.
Lepore N.Brun C.Chou Y.Y.Chiang M.C.Dutton R.A.Hayashi K.M.Luders E.Lopez O.L.Aizenstein H.J.Toga A.W.Becker J.T.Thompson P.M.2008. Generalized tensor-based morphometry of HIV/AIDS using multivariate statistics on deformation tensorsIEEE Trans. Med. Imaging27129-141. Lepore, N., Brun, C., Chou, Y.Y., Chiang, M.C., Dutton, R.A., Hayashi, K.M., Luders, E., Lopez, O.L., Aizenstein, H.J., Toga, A.W., Becker, J.T., and Thompson, P.M. (2008). Generalized tensor-based morphometry of HIV/AIDS using multivariate statistics on deformation tensors. IEEE Trans. Med. Imaging 27, 129–141.
Le T.H.Mukherjee P.Henry R.G.Berman J.I.Ware M.Manley G.T.2005. Diffusion tensor imaging with three-dimensional fiber tractography of traumatic axonal shearing injury: an imaging correlate for the posterior callosal “disconnection” syndrome: case reportNeurosurgery56189. Le, T.H., Mukherjee, P., Henry, R.G., Berman, J.I., Ware, M., and Manley, G.T. (2005). 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 56, 189.
Maxwell W.L.Kansagra A.M.Graham D.I.Adams J.H.Gennarelli T.A.1988. Freeze-fracture studies of reactive myelinated nerve fibres after diffuse axonal injuryActa Neuropathol.76395-406. Maxwell, W.L., Kansagra, A.M., Graham, D.I., Adams, J.H., and Gennarelli, T.A. (1988). Freeze-fracture studies of reactive myelinated nerve fibres after diffuse axonal injury. Acta Neuropathol. 76, 395–406.
Mayer A.R.Ling J.Mannell M.V.Gasparovic C.Phillips J.P.Doezema D.Reichard R.Yeo R.A.2010. A prospective diffusion tensor imaging study in mild traumatic brain injuryNeurology74643-650. Mayer, A.R., Ling, J., Mannell, M.V., Gasparovic, C., Phillips, J.P., Doezema, D., Reichard, R., and Yeo, R.A. (2010). A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology 74, 643–650.
McCrory P.Johnston K.Meeuwisse W.Aubry M.Cantu R.Dvorak J.Graf-Baumann T.Kelly J.Lovell M.Schamasch P.2005. Summary and agreement statement of the 2nd International Conference on Concussion in Sport, Prague 2004Br. J. Sports Med.39196-204. McCrory, P., Johnston, K., Meeuwisse, W., Aubry, M., Cantu, R., Dvorak, J., Graf-Baumann, T., Kelly, J., Lovell, M., and Schamasch, P. (2005). Summary and agreement statement of the 2nd International Conference on Concussion in Sport, Prague 2004. Br. J. Sports Med. 39, 196–204.
McCrory P.Meeuwisse W.Johnston K.Dvorak J.Aubry M.Molloy M.Cantu R.2009. Consensus statement on Concussion in Sport 3rd International Conference on Concussion in Sport held in Zurich, November 2008Clin. J. Sport Med.19185-200. McCrory, P., Meeuwisse, W., Johnston, K., Dvorak, J., Aubry, M., Molloy, M., and Cantu, R. (2009). Consensus statement on Concussion in Sport 3rd International Conference on Concussion in Sport held in Zurich, November 2008. Clin. J. Sport Med. 19, 185–200.
Messé A.Caplain S.Paradot G.Garrigue D.Mineo J.F.Soto Ares G.Ducreuy D.Vignaud F.Rozec G.Desal H.Pélègrini-Issac M.Montreuil M.Benail H.Lehéricy S.2010. Diffusion tensor imaging and white matter lesions at the subacute stage in mild traumatic brain injury with persistent neurobehavioral impairmentHuman Brain Mapping32999-1011. Messé, A., Caplain, S., Paradot, G., Garrigue, D., Mineo, J.F., Soto Ares, G., Ducreuy, D., Vignaud, F., Rozec, G., Desal, H., Pélègrini-Issac, M., Montreuil, M., Benail, H., Lehéricy, S. (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.
Meythaler J.M.Peduzzi J.D.Eleftheriou E.Novack T.A.2001. Current concepts: diffuse axonal injury-associated traumatic brain injuryArch. Phys. Med. Rehabil.821461-1471. Meythaler, J.M., Peduzzi, J.D., Eleftheriou, E., and Novack, T.A. (2001). Current concepts: diffuse axonal injury-associated traumatic brain injury. Arch. Phys. Med. Rehabil. 82, 1461–1471.
Miles L.Grossman R.I.Johnson G.Babb J.S.Diller L.Inglese M.2008. Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injuryBrain Inj.22115-122. Miles, L., Grossman, R.I., Johnson, G., Babb, J.S., Diller, L., and Inglese, M. (2008). Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injury. Brain Inj. 22, 115–122.
Newcombe V.F.Williams G.B.Nortje J.Bradley P.G.Chatfield D.A.Outtrim J.G.Harding S.G.Coles J.P.Maiya B.Gillard J.H.Hutchinson P.J.Pickard J.D.Carpenter T.A.Menon D.K.2008. Concordant biology underlies discordant imaging findings: diffusivity behaves differently in grey and white matter post acute neurotraumaActa Neurochir. Suppl.102247-251. Newcombe, V.F., Williams, G.B., Nortje, J., Bradley, P.G., Chatfield, D.A., Outtrim, J.G., Harding, S.G., Coles, J.P., Maiya, B., Gillard, J.H., Hutchinson, P.J., Pickard, J.D., Carpenter, T.A., and Menon, D.K. (2008). Concordant biology underlies discordant imaging findings: diffusivity behaves differently in grey and white matter post acute neurotrauma. Acta Neurochir. Suppl. 102, 247–251.
Newcombe V.F.Williams G.B.Nortje J.Bradley P.G.Harding S.G.Smielewski P.Coles J.P.Maiya B.Gillard J.H.Hutchinson P.J.Pickard J.D.Carpenter T.A.Menon D.K.2007. Analysis of acute traumatic axonal injury using diffusion tensor imagingBr. J. Neurosurg.21340-348. Newcombe, V.F., Williams, G.B., Nortje, J., Bradley, P.G., Harding, S.G., Smielewski, P., Coles, J.P., Maiya, B., Gillard, J.H., Hutchinson, P.J., Pickard, J.D., Carpenter, T.A., and Menon, D.K. (2007). Analysis of acute traumatic axonal injury using diffusion tensor imaging. Br. J. Neurosurg. 21, 340–348.
Niogi S.N.Mukherjee P.Ghajar J.Johnson C.Kolster R.A.Sarkar R.Lee H.Meeker M.Zimmerman R.D.Manley G.T.McCandliss B.D.2008. 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 injuryAJNR Am. J. Neuroradiol.29967-973. Niogi, S.N., Mukherjee, P., Ghajar, J., Johnson, C., Kolster, R.A., Sarkar, R., Lee, H., Meeker, M., Zimmerman, R.D., Manley, G.T., and McCandliss, B.D. (2008). 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. AJNR Am. J. Neuroradiol. 29, 967–973.
Okumura A.Yasokawa Y.Nakayama N.Miwa K.Shinoda J.Iwama T.2005. The clinical utility of MR diffusion tensor imaging and spatially normalized PET to evaluate traumatic brain injury patients with memory and cognitive impairmentsNo To Shinkei57115-122. Okumura, A., Yasokawa, Y., Nakayama, N., Miwa, K., Shinoda, J., and Iwama, T. (2005). [The clinical utility of MR diffusion tensor imaging and spatially normalized PET to evaluate traumatic brain injury patients with memory and cognitive impairments]. No To Shinkei 57, 115–122.
Ommaya A.K.Gennarelli T.A.1974. Cerebral concussion and traumatic unconsciousness. Correlation of experimental and clinical observations of blunt head injuriesBrain97633-654. Ommaya, A.K., and Gennarelli, T.A. (1974). Cerebral concussion and traumatic unconsciousness. Correlation of experimental and clinical observations of blunt head injuries. Brain 97, 633–654.
Peerless S.J.Rewcastle N.B.1967. Shear injuries of the brainCan. Med. Assoc. J.96577-582. Peerless, S.J., and Rewcastle, N.B. (1967). Shear injuries of the brain. Can. Med. Assoc. J. 96, 577–582.
Pfefferbaum A.Sullivan E.V.2003. Increased brain white matter diffusivity in normal adult aging: relationship to anisotropy and partial volumingMagn. Reson. Med.49953-961. Pfefferbaum, A., and Sullivan, E.V. (2003). Increased brain white matter diffusivity in normal adult aging: relationship to anisotropy and partial voluming. Magn. Reson. Med. 49, 953–961.
Pierpaoli C.Jezzard P.Basser P.J.Barnett A.Di Chiro G.1996. Diffusion tensor MR imaging of the human brainRadiology201637-648. Pierpaoli, C., Jezzard, P., Basser, P.J., Barnett, A., and Di Chiro, G. (1996). Diffusion tensor MR imaging of the human brain. Radiology 201, 637–648.
Pudenz R.H.Shelden C.H.1946. The lucite calvarium; a method for direct observation of the brain; cranial trauma and brain movementJ. Neurosurg.3487-505. Pudenz, R.H., and Shelden, C.H. (1946). The lucite calvarium; a method for direct observation of the brain; cranial trauma and brain movement. J. Neurosurg. 3, 487–505.
Quality Standards Subcommittee and Neurology AAo1997. Practice parameterNeurobiology (Bp)1-5. Quality Standards Subcommittee and Neurology AAo. (1997). Practice parameter. Neurobiology (Bp). 1–5.
Shen S.Szameitat A.J.Sterr A.2007. VBM lesion detection depends on the normalization template: a study using simulated atrophyMagn. Reson. Imaging251385-1396. Shen, S., Szameitat, A.J., and Sterr, A. (2007). VBM lesion detection depends on the normalization template: a study using simulated atrophy. Magn. Reson. Imaging 25, 1385–1396.
Song S.K.Sun S.W.Ramsbottom M.J.Chang C.Russell J.Cross A.H.2002. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of waterNeuroimage171429-1436. Song, S.K., Sun, S.W., Ramsbottom, M.J., Chang, C., Russell, J., and Cross, A.H. (2002). Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17, 1429–1436.
Strange K.1992. Regulation of solute and water balance and cell volume in the central nervous systemJ. Am. Soc. Nephrol.312-27. Strange, K. (1992). Regulation of solute and water balance and cell volume in the central nervous system. J. Am. Soc. Nephrol. 3, 12–27.
Theriault M.De Beaumont L.Tremblay S.Lassonde M.Jolicoeur P.2010. Cumulative effects of concussions in athletes revealed by electrophysiological abnormalities on visual working memoryJ. Clin. Exp. Neuropsychol.1-12. Theriault, M., De Beaumont, L., Tremblay, S., Lassonde, M., and Jolicoeur, P. (2010). Cumulative effects of concussions in athletes revealed by electrophysiological abnormalities on visual working memory. J. Clin. Exp. Neuropsychol. 1–12.
Toga A.W.Mazziotta J.C.2002Brain Mapping: The Methods2ndAcademic PressSan Diego. Toga, A.W., and Mazziotta, J.C. (2002). Brain Mapping: The Methods, 2nd ed. Academic Press: San Diego.
Vagnozzi R.Signoretti S.Cristofori L.Alessandrini F.Floris R.Isgro E.Ria A.Marziale S.Zoccatelli G.Tavazzi B.Del Bolgia F.Sorge R.Broglio S.P.McIntosh T.K.Lazzarino G.2010. Assessment of metabolic brain damage and recovery following mild traumatic brain injury: a multicentre, proton magnetic resonance spectroscopic study in concussed patientsBrain1333232-3242. Vagnozzi, R., Signoretti, S., Cristofori, L., Alessandrini, F., Floris, R., Isgro, E., Ria, A., Marziale, S., Zoccatelli, G., Tavazzi, B., Del Bolgia, F., Sorge, R., Broglio, S.P., McIntosh, T.K., and Lazzarino, G. (2010). Assessment of metabolic brain damage and recovery following mild traumatic brain injury: a multicentre, proton magnetic resonance spectroscopic study in concussed patients. Brain 133, 3232–3242.
Vagnozzi R.Signoretti S.Tavazzi B.Floris R.Ludovici A.Marziali S.Tarascio G.Amorini A.M.Di Pietro V.Delfini R.Lazzarino G.2008. Temporal window of metabolic brain vulnerability to concussion: a pilot 1H-magnetic resonance spectroscopic study in concussed athletes—part IIINeurosurgery621286-1295discussion 1295–1286. Vagnozzi, R., Signoretti, S., Tavazzi, B., Floris, R., Ludovici, A., Marziali, S., Tarascio, G., Amorini, A.M., Di Pietro, V., Delfini, R., and Lazzarino, G. (2008). Temporal window of metabolic brain vulnerability to concussion: a pilot 1H-magnetic resonance spectroscopic study in concussed athletes—part III. Neurosurgery 62, 1286–1295; discussion 1295–1286.
Westlye L.T.Walhovd K.B.Dale A.M.Bjornerud A.Due-Tonnessen P.Engvig A.Grydeland H.Tamnes C.K.Ostby Y.Fjell A.M.2010. Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetryCereb. Cortex202055-2068. Westlye, L.T., Walhovd, K.B., Dale, A.M., Bjornerud, A., Due-Tonnessen, P., Engvig, A., Grydeland, H., Tamnes, C.K., Ostby, Y., and Fjell, A.M. (2010). Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetry. Cereb. Cortex 20, 2055–2068.
Wilde E.A.McCauley S.R.Hunter J.V.Bigler E.D.Chu Z.Wang Z.J.Hanten G.R.Troyanskaya M.Yallampalli R.Li X.Chia J.Levin H.S.2008. Diffusion tensor imaging of acute mild traumatic brain injury in adolescentsNeurology70948-955. Wilde, E.A., McCauley, S.R., Hunter, J.V., Bigler, E.D., Chu, Z., Wang, Z.J., Hanten, G.R., Troyanskaya, M., Yallampalli, R., Li, X., Chia, J., and Levin, H.S. (2008). Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology 70, 948–955.
Wilde E.A.Ramos M.A.Yallampalli R.Bigler E.D.McCauley S.R.Chu Z.Wu T.C.Hanten G.Scheibel R.S.Li X.Vasquez A.C.Hunter J.V.Levin H.S.2010. Diffusion tensor imaging of the cingulum bundle in children after traumatic brain injuryDev. Neuropsychol.35333-351. Wilde, E.A., Ramos, M.A., Yallampalli, R., Bigler, E.D., McCauley, S.R., Chu, Z., Wu, T.C., Hanten, G., Scheibel, R.S., Li, X., Vasquez, A.C., Hunter, J.V., and Levin, H.S. (2010). Diffusion tensor imaging of the cingulum bundle in children after traumatic brain injury. Dev. Neuropsychol. 35, 333–351.
Wozniak J.R.Lim K.O.2006. Advances in white matter imaging: a review of in vivo magnetic resonance methodologies and their applicability to the study of development and agingNeurosci. Biobehav. Rev.30762-774. Wozniak, J.R., and Lim, K.O. (2006). Advances in white matter imaging: a review of in vivo magnetic resonance methodologies and their applicability to the study of development and aging. Neurosci. Biobehav. Rev. 30, 762–774.
Wozniak J.R.Krach L.Ward E.Mueller B.A.Muetzel R.Schnoebelen S.Kiragu A.Lim K.O.2007. Neurocognitive and neuroimaging correlates of pediatric traumatic brain injury: a diffusion tensor imaging (DTI) studyArch. Clin. Neuropsychol.22555-568. Wozniak, J.R., Krach, L., Ward, E., Mueller, B.A., Muetzel, R., Schnoebelen, S., Kiragu, A., and Lim, K.O. (2007). Neurocognitive and neuroimaging correlates of pediatric traumatic brain injury: a diffusion tensor imaging (DTI) study. Arch. Clin. Neuropsychol. 22, 555–568.
Zhang H.Yushkevich P.A.Alexander D.C.Gee J.C.2006. Deformable registration of diffusion tensor MR images with explicit orientation optimizationMed. Image Anal.10764-785. Zhang, H., Yushkevich, P.A., Alexander, D.C., and Gee, J.C. (2006). Deformable registration of diffusion tensor MR images with explicit orientation optimization. Med. Image Anal. 10, 764–785.
Zillmer E.A.Spiers M.V.2001Principles of Neuropsychology1stWadsworthBelmont, CA. Zillmer, E.A., and Spiers, M.V. (2001). Principles of Neuropsychology, 1st ed. Wadsworth: Belmont, CA.
Information & Authors
Information
Published In
Copyright
Copyright 2011, Mary Ann Liebert, Inc.
History
Published online: 17 October 2011
Published ahead of print: 4 October 2011
Published in print: October 2011
Published ahead of production: 24 August 2011
Topics
Authors
Author Disclosure Statement
No competing financial interests exist.
Metrics & Citations
Metrics
Citations
Export Citation
Export citation
Select the format you want to export the citations of this publication.
View Options
Get Access
Access content
To read the fulltext, please use one of the options below to sign in or purchase access.⚠ Society Access
If you are a member of a society that has access to this content please log in via your society website and then return to this publication.