Chronic differences in white matter integrity following sport-related concussion as measured by diffusion MRI: 6-Month follow-up

Melissa A Lancaster, Timothy B Meier, Daniel V Olson, Michael A McCrea, Lindsay D Nelson, L Tugan Muftuler, Melissa A Lancaster, Timothy B Meier, Daniel V Olson, Michael A McCrea, Lindsay D Nelson, L Tugan Muftuler

Abstract

Recent studies demonstrated evidence of physiological changes in the brain following sport-related concussion (SRC) that persisted beyond the point at which athletes achieved full symptom recovery. Diffusion MRI techniques have been used to study brain white matter (WM) changes following SRC; however, longitudinal studies that follow injured athletes from the acute to chronic stages of injury are sparse. The current study explores potential persisting effects of the injury, which serves as a follow-up to our previous work that reported WM changes in the acute and subacute phase of SRC recovery. Concussed high school and collegiate football players (n = 17) and well-matched teammate controls (n = 20) were followed up at 6 months postinjury with diffusion tensor (DTI) and diffusion kurtosis imaging (DKI) as well as measures of self-reported symptoms, cognitive functioning, and balance. Results of tract-based spatial statistics (TBSS) analyses revealed continued widespread decreased mean and axial diffusivity compared to control subjects in 6-month follow-up scans. On the other hand, kurtosis metrics, which were significantly higher in concussed athletes in the acute phase, had normalized. WM tract regions-of-interest (ROIs) were created from significant clusters in the TBSS analysis, and linear mixed effects (LME) analyses were used to look at longitudinal changes in these ROIs over time. LME analyses revealed few time × group interactions indicating findings were relatively stable over time. In addition, acute concussion symptoms predicted diffusivity measures at 6 months postinjury. Findings indicate that DTI and DKI may be useful tools in assessing concussion severity, recovery, and possible long-term effects of concussion.

Keywords: concussion management; concussion symptoms; diffusion kurtosis imaging; diffusion tensor imaging; mild traumatic brain injury; sport-related concussion.

© 2018 Wiley Periodicals, Inc.

Figures

Figure 1
Figure 1
Longitudinal assessment of symptoms and cognitive performance. SAC = standardized assessment of concussion; SCAT‐3 = sport concussion assessment tool, third edition. Error bars reflect 95% confidence interval [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 2
Figure 2
Results of tract‐based spatial statistics analyses comparing mean diffusivity (MD) of concussed and control subjects at 24 hr, 8 days, and 6 months postinjury. The red‐yellow voxels represent areas of significant decreased MD in concussed athletes compared to controls corrected for family‐wise error at p < .05. Significant voxels have been inflated using tbss_fill for viewing purposes and are overlaid on the mean WM skeleton (green). Results are displayed on the MNI152‐T1‐1 mm standard image. MD = mean diffusivity [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 3
Figure 3
Results of tract‐based spatial statistics analyses comparing axial diffusivity (Dax) of concussed and control subjects at 24 hr, 8 days, and 6 months postinjury. The pink‐light pink voxels represent areas of significant decreased Dax in concussed athletes compared to controls corrected for family‐wise error at p < .05. Significant voxels have been inflated using tbss_fill for viewing purposes and are overlaid on the mean WM skeleton (green). Results are displayed on the MNI152‐T1‐1 mm standard image. Dax = axial diffusivity [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 4
Figure 4
Relationship between acute (24‐hr) symptom reporting and DTI measures at 6 months postinjury for concussed athletes (green dots) and controls (blue dots) [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 5
Figure 5
Region of interest creation using findings from TBSS analysis. Left panel shows DTI‐ICBM‐81 WM atlas that included peripheral WM. Center panel represents significant MD findings. Right panel shows regions of interest created by masking the atlas with significant voxels from the center panel [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 6
Figure 6
Longitudinal findings in mean diffusivity across a selection of white matter tracts. CGC = cingulate gyrus; PLIC = posterior limb of internal capsule; SLF = superior longitudinal fasciculus. Error bars reflect 95% confidence interval [Color figure can be viewed at http://wileyonlinelibrary.com]

References

    1. Andersson, J. L. , Skare, S. , & Ashburner, J. (2003). How to correct susceptibility distortions in spin‐echo echo‐planar images: Application to diffusion tensor imaging. NeuroImage, 20(2), 870–888. 10.1016/s1053-8119(03)00336-7
    1. Asken, B. M. , DeKosky, S. T. , Clugston, J. R. , Jaffee, M. S. , & Bauer, R. M. (2017). Diffusion tensor imaging (DTI) findings in adult civilian, military, and sport‐related mild traumatic brain injury (mTBI): A systematic critical review. Brain Imaging and Behavior, 12, 585–612. 10.1007/s11682-017-9708-9
    1. Basser, P. J. , & Pierpaoli, C. (1996). Microstructural and physiological features of tissues elucidated by quantitative‐diffusion‐tensor MRI. Journal of Magnetic Resonance. Series B, 111(3), 209–219.
    1. Bazarian, J. J. , Zhu, T. , Zhong, J. , Janigro, D. , Rozen, E. , Roberts, A. , … Blackman, E. G. (2014). Persistent, long‐term cerebral white matter changes after sports‐related repetitive head impacts. PLoS One, 9(4), e94734 10.1371/journal.pone.0094734
    1. Beaulieu, C. (2002). The basis of anisotropic water diffusion in the nervous system—A technical review. NMR in Biomedicine, 15(7–8), 435–455. 10.1002/nbm.782
    1. Benjamini, Y. , & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B: Statistical Methodology, 57, 289–300.
    1. Bernal‐Rusiel, J. L. , Greve, D. N. , Reuter, M. , Fischl, B. , Sabuncu, M. R. , & Alzheimer's Disease Neuroimaging Initiative . (2013). Statistical analysis of longitudinal neuroimage data with linear mixed effects models. NeuroImage, 66, 249–260. 10.1016/j.neuroimage.2012.10.065
    1. Blennow, K. , Hardy, J. , & Zetterberg, H. (2012). The neuropathology and neurobiology of traumatic brain injury. Neuron, 76(5), 886–899. 10.1016/j.neuron.2012.11.021
    1. Blumbergs, P. C. , Scott, G. , Manavis, J. , Wainwright, H. , Simpson, D. A. , & McLean, A. J. (1994). Staining of amyloid precursor protein to study axonal damage in mild head injury. Lancet, 344(8929), 1055–1056.
    1. Borich, M. , Makan, N. , Boyd, L. , & Virji‐Babul, N. (2013). Combining whole‐brain voxel‐wise analysis with in vivo tractography of diffusion behavior after sports‐related concussion in adolescents: A preliminary report. Journal of Neurotrauma, 30(14), 1243–1249. 10.1089/neu.2012.2818
    1. Budde, M. D. , Janes, L. , Gold, E. , Turtzo, L. C. , & Frank, J. A. (2011). The contribution of gliosis to diffusion tensor anisotropy and tractography following traumatic brain injury: Validation in the rat using Fourier analysis of stained tissue sections. Brain, 134(Pt 8), 2248–2260. 10.1093/brain/awr161
    1. Cervos‐Navarro, J. , & Lafuente, J. V. (1991). Traumatic brain injuries: Structural changes. Journal of the Neurological Sciences, 103(Suppl), S3–S14.
    1. Chamard, E. , Lassonde, M. , Henry, L. , Tremblay, J. , Boulanger, Y. , De Beaumont, L. , & Theoret, H. (2013). Neurometabolic and microstructural alterations following a sports‐related concussion in female athletes. Brain Injury, 27(9), 1038–1046. 10.3109/02699052.2013.794968
    1. Chamard, E. , Lefebvre, G. , Lassonde, M. , & Theoret, H. (2016). Long‐term abnormalities in the Corpus callosum of female concussed athletes. Journal of Neurotrauma, 33(13), 1220–1226. 10.1089/neu.2015.3948
    1. Coutu, J. P. , Chen, J. J. , Rosas, H. D. , & Salat, D. H. (2014). Non‐Gaussian water diffusion in aging white matter. Neurobiology of Aging, 35(6), 1412–1421. 10.1016/j.neurobiolaging.2013.12.001
    1. Croall, I. D. , Cowie, C. J. , He, J. , Peel, A. , Wood, J. , Aribisala, B. S. , … Blamire, A. M. (2014). White matter correlates of cognitive dysfunction after mild traumatic brain injury. Neurology, 83(6), 494–501. 10.1212/wnl.0000000000000666
    1. 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 concussion. Journal of Neurotrauma, 28(2), 189–201. 10.1089/neu.2010.1430
    1. Davenport, E. M. , Whitlow, C. T. , Urban, J. E. , Espeland, M. A. , Jung, Y. , Rosenbaum, D. A. , … Maldjian, J. A. (2014). Abnormal white matter integrity related to head impact exposure in a season of high school varsity football. Journal of Neurotrauma, 31(19), 1617–1624. 10.1089/neu.2013.3233
    1. Dimou, S. , & Lagopoulos, J. (2014). Toward objective markers of concussion in sport: A review of white matter and neurometabolic changes in the brain after sports‐related concussion. Journal of Neurotrauma, 31(5), 413–424. 10.1089/neu.2013.3050
    1. Farkas, O. , Lifshitz, J. , & Povlishock, J. T. (2006). Mechanoporation induced by diffuse traumatic brain injury: An irreversible or reversible response to injury? The Journal of Neuroscience, 26(12), 3130–3140. 10.1523/jneurosci.5119-05.2006
    1. Gardner, A. , Iverson, G. L. , & Stanwell, P. (2014). A systematic review of proton magnetic resonance spectroscopy findings in sport‐related concussion. Journal of Neurotrauma, 31(1), 1–18. 10.1089/neu.2013.3079
    1. Gardner, A. , Kay‐Lambkin, F. , Stanwell, P. , Donnelly, J. , Williams, W. H. , Hiles, A. , … Jones, D. K. (2012). A systematic review of diffusion tensor imaging findings in sports‐related concussion. Journal of Neurotrauma, 29(16), 2521–2538. 10.1089/neu.2012.2628
    1. Giza, C. C. , & Hovda, D. A. (2014). The new neurometabolic cascade of concussion. Neurosurgery, 75(Suppl 4), S24–S33. 10.1227/neu.0000000000000505
    1. Gons, R. A. , Tuladhar, A. M. , de Laat, K. F. , van Norden, A. G. , van Dijk, E. J. , Norris, D. G. , … de Leeuw, F. E. (2013). Physical activity is related to the structural integrity of cerebral white matter. Neurology, 81(11), 971–976. 10.1212/WNL.0b013e3182a43e33
    1. Gosselin, N. , Saluja, R. S. , Chen, J. K. , Bottari, C. , Johnston, K. , & Ptito, A. (2010). Brain functions after sports‐related concussion: Insights from event‐related potentials and functional MRI. The Physician and Sportsmedicine, 38(3), 27–37. 10.3810/psm.2010.10.1805
    1. Grossman, E. J. , Ge, Y. , Jensen, J. H. , Babb, J. S. , Miles, L. , Reaume, J. , … Inglese, M. (2012). Thalamus and cognitive impairment in mild traumatic brain injury: A diffusional kurtosis imaging study. Journal of Neurotrauma, 29(13), 2318–2327. 10.1089/neu.2011.1763
    1. Grossman, E. J. , Jensen, J. H. , Babb, J. S. , Chen, Q. , Tabesh, A. , Fieremans, E. , … Grossman, R. I. (2013). Cognitive impairment in mild traumatic brain injury: A longitudinal diffusional kurtosis and perfusion imaging study. AJNR. American Journal of Neuroradiology, 34(5), 951–957, S951‐953. 10.3174/ajnr.A3358
    1. Gurkoff, G. G. , Giza, C. C. , & Hovda, D. A. (2006). Lateral fluid percussion injury in the developing rat causes an acute, mild behavioral dysfunction in the absence of significant cell death. Brain Research, 1077(1), 24–36. 10.1016/j.brainres.2006.01.011
    1. Guskiewicz, K. M. , McCrea, M. , Marshall, S. W. , Cantu, R. C. , Randolph, C. , Barr, W. , … Kelly, J. P. (2003). Cumulative effects associated with recurrent concussion in collegiate football players: The NCAA concussion study. JAMA, 290(19), 2549–2555. 10.1001/jama.290.19.2549
    1. Helmick, K. , Guskiewicz, K. , Barth, J. , Cantu, R. , Kelly, J. P. , McDonald, E. , … Warden, D. (2006). Defense and Veterans Brain Injury Center Working Group on the acute management of mild traumatic brain injury in military operational settings. Retrieved from
    1. Henry, L. C. , Tremblay, J. , Tremblay, S. , Lee, A. , Brun, C. , Lepore, N. , … Lassonde, M. (2011). Acute and chronic changes in diffusivity measures after sports concussion. Journal of Neurotrauma, 28(10), 2049–2059. 10.1089/neu.2011.1836
    1. Hutchinson, E. B. , Avram, A. V. , Irfanoglu, M. O. , Koay, C. G. , Barnett, A. S. , Komlosh, M. E. , … Pierpaoli, C. (2017a). Analysis of the effects of noise, DWI sampling, and value of assumed parameters in diffusion MRI models. Magnetic Resonance in Medicine, 78, 1767–1780. 10.1002/mrm.26575
    1. Hutchinson, E. B. , Schwerin, S. C. , Avram, A. V. , Juliano, S. L. , & Pierpaoli, C. (2017b). Diffusion MRI and the detection of alterations following traumatic brain injury. Journal of Neuroscience Research, 96, 612–625. 10.1002/jnr.24065
    1. Jensen, J. H. , Helpern, J. A. , Ramani, A. , Lu, H. , & Kaczynski, K. (2005). Diffusional kurtosis imaging: The quantification of non‐Gaussian water diffusion by means of magnetic resonance imaging. Magnetic Resonance in Medicine, 53(6), 1432–1440. 10.1002/mrm.20508
    1. Johnson, N. F. , Kim, C. , Clasey, J. L. , Bailey, A. , & Gold, B. T. (2012). Cardiorespiratory fitness is positively correlated with cerebral white matter integrity in healthy seniors. NeuroImage, 59(2), 1514–1523. 10.1016/j.neuroimage.2011.08.032
    1. Kilinc, D. , Gallo, G. , & Barbee, K. A. (2008). Mechanically‐induced membrane poration causes axonal beading and localized cytoskeletal damage. Experimental Neurology, 212(2), 422–430. 10.1016/j.expneurol.2008.04.025
    1. Kilinc, D. , Gallo, G. , & Barbee, K. A. (2009). Mechanical membrane injury induces axonal beading through localized activation of calpain. Experimental Neurology, 219(2), 553–561. 10.1016/j.expneurol.2009.07.014
    1. Lancaster, M. A. , Olson, D. V. , McCrea, M. A. , Nelson, L. D. , LaRoche, A. A. , & Muftuler, L. T. (2016). Acute white matter changes following sport‐related concussion: A serial diffusion tensor and diffusion kurtosis tensor imaging study. Human Brain Mapping, 37(11), 3821–3834. 10.1002/hbm.23278
    1. LaRoche, A. A. , Nelson, L. D. , Connelly, P. K. , Walter, K. D. , & McCrea, M. A. (2015). Sport‐related concussion reporting and state legislative effects. Clinical Journal of Sport Medicine, 26, 33–39. 10.1097/jsm.0000000000000192
    1. Lyeth, B. G. , Jenkins, L. W. , Hamm, R. J. , Dixon, C. E. , Phillips, L. L. , Clifton, G. L. , … Hayes, R. L. (1990). Prolonged memory impairment in the absence of hippocampal cell death following traumatic brain injury in the rat. Brain Research, 526(2), 249–258.
    1. Maugans, T. A. , Farley, C. , Altaye, M. , Leach, J. , & Cecil, K. M. (2012). Pediatric sports‐related concussion produces cerebral blood flow alterations. Pediatrics, 129(1), 28–37. 10.1542/peds.2011-2083
    1. Mayinger, M. C. , Merchant‐Borna, K. , Hufschmidt, J. , Muehlmann, M. , Weir, I. R. , Rauchmann, B. S. , … Bazarian, J. J. (2017). White matter alterations in college football players: A longitudinal diffusion tensor imaging study. Brain Imaging and Behavior, 12, 44–53. 10.1007/s11682-017-9672-4
    1. McAllister, T. W. , Ford, J. C. , Flashman, L. A. , Maerlender, A. , Greenwald, R. M. , Beckwith, J. G. , … Jain, S. (2014). Effect of head impacts on diffusivity measures in a cohort of collegiate contact sport athletes. Neurology, 82(1), 63–69. 10.1212/01.wnl.0000438220.16190.42
    1. McCrea, M. , Guskiewicz, K. , Randolph, C. , Barr, W. B. , Hammeke, T. A. , Marshall, S. W. , & Kelly, J. P. (2009). Effects of a symptom‐free waiting period on clinical outcome and risk of reinjury after sport‐related concussion. Neurosurgery, 65(5), 876–882; discussion 882–873. 10.1227/01.Neu.0000350155.89800.00
    1. McCrea, M. , Kelly, J. P. , Kluge, J. , Ackley, B. , & Randolph, C. (1997). Standardized assessment of concussion in football players. Neurology, 48(3), 586–588.
    1. McCrory, P. , Meeuwisse, W. H. , Aubry, M. , Cantu, B. , Dvořák, J. , Echemendia, R. J. , … Turner, M. (2013). Consensus statement on concussion in sport: The 4th international conference on concussion in sport held in Zurich, November 2012. British Journal of Sports Medicine, 47(5), 250–258. 10.1136/bjsports-2013-092313
    1. Meier, T. B. , Bergamino, M. , Bellgowan, P. S. , Teague, T. K. , Ling, J. M. , Jeromin, A. , & Mayer, A. R. (2016). Longitudinal assessment of white matter abnormalities following sports‐related concussion. Human Brain Mapping, 37(2), 833–845. 10.1002/hbm.23072
    1. Mori, S. , Oishi, K. , Jiang, H. , Jiang, L. , Li, X. , Akhter, K. , … Mazziotta, J. (2008). Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. NeuroImage, 40(2), 570–582. 10.1016/j.neuroimage.2007.12.035
    1. Murphy, M. , McCutcheon, B. A. , Kerezoudis, P. , Rinaldo, L. , Shepherd, D. L. , Maloney, P. R. , … Bydon, M. (2016). 199 multiple concussions in young athletes: Identifying patients at risk for repeat injury. Neurosurgery, 63(Suppl 1), 178 10.1227/01.neu.0000489768.36395.5a
    1. Murugavel, M. , Cubon, V. , Putukian, M. , Echemendia, R. , Cabrera, J. , Osherson, D. , & Dettwiler, A. (2014). A longitudinal diffusion tensor imaging study assessing white matter fiber tracts after sports‐related concussion. Journal of Neurotrauma, 31(22), 1860–1871. 10.1089/neu.2014.3368
    1. Nelson, L. D. , Janecek, J. K. , & McCrea, M. A. (2013). Acute clinical recovery from sport‐related concussion. Neuropsychology Review, 23(4), 285–299. 10.1007/s11065-013-9240-7
    1. Nelson, L. D. , LaRoche, A. A. , Pfaller, A. Y. , Lerner, E. B. , Hammeke, T. A. , Randolph, C. , … McCrea, M. A. (2016). Prospective, head‐to‐head study of three computerized neurocognitive assessment tools (CNTs): Reliability and validity for the assessment of sport‐related concussion. Journal of the International Neuropsychological Society, 22(1), 24–37. 10.1017/s1355617715001101
    1. Nelson, L. D. , Pfaller, A. Y. , Rein, L. E. , & McCrea, M. A. (2015). Rates and predictors of invalid baseline test performance in high school and collegiate athletes for 3 computerized neurocognitive tests: ANAM, axon sports, and ImPACT. The American Journal of Sports Medicine, 43(8), 2018–2026. 10.1177/0363546515587714
    1. Pasternak, O. , Koerte, I. K. , Bouix, S. , Fredman, E. , Sasaki, T. , Mayinger, M. , … Echlin, P. S. (2014). Hockey concussion education project, part 2. Microstructural white matter alterations in acutely concussed ice hockey players: A longitudinal free‐water MRI study. Journal of Neurosurgery, 120(4), 873–881. 10.3171/2013.12.jns132090
    1. Paydar, A. , Fieremans, E. , Nwankwo, J. I. , Lazar, M. , Sheth, H. D. , Adisetiyo, V. , … Milla, S. S. (2014). Diffusional kurtosis imaging of the developing brain. AJNR. American Journal of Neuroradiology, 35(4), 808–814. 10.3174/ajnr.A3764
    1. Peerless, S. J. , & Rewcastle, N. B. (1967). Shear injuries of the brain. Canadian Medical Association Journal, 96(10), 577–582.
    1. Pfefferbaum, A. , & Sullivan, E. V. (2003). Increased brain white matter diffusivity in normal adult aging: Relationship to anisotropy and partial voluming. Magnetic Resonance in Medicine, 49(5), 953–961. 10.1002/mrm.10452
    1. Pfefferbaum, A. , Sullivan, E. V. , Hedehus, M. , Lim, K. O. , Adalsteinsson, E. , & Moseley, M. (2000). Age‐related decline in brain white matter anisotropy measured with spatially corrected echo‐planar diffusion tensor imaging. Magnetic Resonance in Medicine, 44(2), 259–268.
    1. Pierpaoli, C. , Barnett, A. , Pajevic, S. , Chen, R. , Penix, L. R. , Virta, A. , & Basser, P. (2001). Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. NeuroImage, 13(6 Pt 1), 1174–1185. 10.1006/nimg.2001.0765
    1. Pulsipher, D. T. , Campbell, R. A. , Thoma, R. , & King, J. H. (2011). A critical review of neuroimaging applications in sports concussion. Current Sports Medicine Reports, 10(1), 14–20. 10.1249/JSR.0b013e31820711b8
    1. Riemann, B. L. , & Guskiewicz, K. M. (2000). Effects of mild head injury on postural stability as measured through clinical balance testing. Journal of Athletic Training, 35(1), 19–25.
    1. 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. The Journal of Neuroscience, 22(3), 791–802.
    1. Smith, S. M. , Jenkinson, M. , Johansen‐Berg, H. , Ruckert, D. , Nichols, T. E. , & Mackay, C. E. (2006). Tract‐based spatial statistics: Voxelwise analysis of multi‐subject diffusion data. NeuroImage, 31, 1487–1505.
    1. Smith, S. M. , Jenkinson, M. , Woolrich, M. W. , Beckmann, C. F. , Behrens, T. E. , Johansen‐Berg, H. , … Matthews, P. M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23(Suppl 1), S208–S219. 10.1016/j.neuroimage.2004.07.051
    1. Smith, S. M. , & Nichols, T. E. (2009). Threshold‐free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage, 44(1), 83–98. 10.1016/j.neuroimage.2008.03.061
    1. Stokum, J. A. , Sours, C. , Zhuo, J. , Kane, R. , Shanmuganathan, K. , & Gullapalli, R. P. (2015). A longitudinal evaluation of diffusion kurtosis imaging in patients with mild traumatic brain injury. Brain Injury, 29(1), 47–57. 10.3109/02699052.2014.947628
    1. Strich, S. J. (1956). Diffuse degeneration of the cerebral white matter in severe dementia following head injury. Journal of Neurology, Neurosurgery, and Psychiatry, 19(3), 163–185.
    1. Tseng, B. Y. , Gundapuneedi, T. , Khan, M. A. , Diaz‐Arrastia, R. , Levine, B. D. , Lu, H. , … Zhang, R. (2013). White matter integrity in physically fit older adults. NeuroImage, 82, 510–516. 10.1016/j.neuroimage.2013.06.011
    1. Veeramuthu, V. , Narayanan, V. , Kuo, T. L. , Delano‐Wood, L. , Chinna, K. , Bondi, M. W. , … Ramli, N. (2015). Diffusion tensor imaging parameters in mild traumatic brain injury and its correlation with early neuropsychological impairment: A longitudinal study. Journal of Neurotrauma, 32(19), 1497–1509. 10.1089/neu.2014.3750
    1. Virji‐Babul, N. , Borich, M. R. , Makan, N. , Moore, T. , Frew, K. , Emery, C. A. , & Boyd, L. A. (2013). Diffusion tensor imaging of sports‐related concussion in adolescents. Pediatric Neurology, 48(1), 24–29. 10.1016/j.pediatrneurol.2012.09.005
    1. Winkler, A. M. , Ridgway, G. R. , Webster, M. A. , Smith, S. M. , & Nichols, T. E. (2014). Permutation inference for the general linear model. NeuroImage, 92, 381–397. 10.1016/j.neuroimage.2014.01.060
    1. Zhuo, J. , Xu, S. , Proctor, J. L. , Mullins, R. J. , Simon, J. Z. , Fiskum, G. , & Gullapalli, R. P. (2012). Diffusion kurtosis as an in vivo imaging marker for reactive astrogliosis in traumatic brain injury. NeuroImage, 59(1), 467–477. 10.1016/j.neuroimage.2011.07.050

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