Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-26T19:34:04.671Z Has data issue: false hasContentIssue false
  • English
  • Français

Microstructure of the Corpus Callosum Long after Pediatric Concussion

Published online by Cambridge University Press:  18 March 2020

Maya N. Sohn ,
Shane Virani Open the ORCID record for Shane Virani [Opens in a new window] ,
Helen L. Carlson ,
Shelby MacPhail ,
Trevor A. Low ,
Vickie Plourde Open the ORCID record for Vickie Plourde [Opens in a new window] ,
Keith Owen Yeates ,
Catherine Lebel  and
Brian L. Brooks
Maya N. Sohn
Affiliation:
Department of Neurosciences, University of Calgary, Calgary, AB, Canada
Shane Virani
Affiliation:
Alberta Children’s Hospital Research Institute, Calgary, AB, Canada Faculty of Kinesiology, University of Calgary, Calgary, AB, Canada Neuropsychology Service, Alberta Children’s Hospital, Calgary, AB, Canada
Helen L. Carlson
Affiliation:
Alberta Children’s Hospital Research Institute, Calgary, AB, Canada Department of Pediatrics, University of Calgary, Calgary, AB, Canada Hotchkiss Brain Institute, Calgary, AB, Canada
Shelby MacPhail
Affiliation:
Department of Neuroscience, Muhlenberg College, Allentown, Pennsylvania, United States of America
Trevor A. Low
Affiliation:
Department of Clinical Neurosciences, University of Calgary, Calgary, AB, Canada
Vickie Plourde
Affiliation:
École de Psychologie, Faculté des sciences de la santé et des services communautaires, Université de Moncton, Moncton, NB, Canada
Keith Owen Yeates
Affiliation:
Alberta Children’s Hospital Research Institute, Calgary, AB, Canada Department of Pediatrics, University of Calgary, Calgary, AB, Canada Department of Clinical Neurosciences, University of Calgary, Calgary, AB, Canada Department of Psychology, University of Calgary, Calgary, AB, Canada Hotchkiss Brain Institute, Calgary, AB, Canada
Catherine Lebel
Affiliation:
Alberta Children’s Hospital Research Institute, Calgary, AB, Canada Hotchkiss Brain Institute, Calgary, AB, Canada Department of Radiology, University of Calgary, Calgary, AB, Canada
Brian L. Brooks*
Affiliation:
Alberta Children’s Hospital Research Institute, Calgary, AB, Canada Neuropsychology Service, Alberta Children’s Hospital, Calgary, AB, Canada Department of Pediatrics, University of Calgary, Calgary, AB, Canada Department of Clinical Neurosciences, University of Calgary, Calgary, AB, Canada Department of Psychology, University of Calgary, Calgary, AB, Canada
*
*Correspondence and reprint requests to: Dr. Brian L. Brooks, Alberta Children’s Hospital, 28 Oki Drive NW, Calgary, AB, Canada, T3B 6A8. Phone: 403-955-2597. Fax: 403-955-7086. Email: brian.brooks@ahs.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

The long-term effects of pediatric concussion on white matter microstructure are poorly understood. This study investigated long-term changes in white matter diffusion properties of the corpus callosum in youth several years after concussion.

Methods:

Participants were 8–19 years old with a history of concussion (n = 36) or orthopedic injury (OI) (n = 21). Mean time since injury for the sample was 2.6 years (SD = 1.6). Participants underwent diffusion magnetic resonance imaging, completed cognitive testing, and rated their post-concussion symptoms. Measures of diffusivity (fractional anisotropy, mean, axial, and radial diffusivity) were extracted from white matter tracts in the genu, body, and splenium regions of the corpus callosum. The genu and splenium tracts were further subdivided into 21 equally spaced regions along the tract and diffusion values were extracted from each of these smaller regions.

Results:

White matter tracts in the genu, body, and splenium did not differ in diffusivity properties between youth with a history of concussion and those with a history of OI. No significant group differences were found in subdivisions of the genu and splenium after correcting for multiple comparisons. Diffusion metrics did not significantly correlate with symptom reports or cognitive performance.

Conclusions:

These findings suggest that at approximately 2.5 years post-injury, youth with prior concussion do not have differences in their corpus callosum microstructure compared to youth with OI. Although these results are promising from the perspective of long-term recovery, further research utilizing longitudinal study designs is needed to confirm the long-term effects of pediatric concussion on white matter microstructure.

Keywords

Mild traumatic brain injuryAdolescenceWhite matterLong-termDiffusion tensor imagingPost-concussion syndrome
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 26 , Issue 8 , September 2020 , pp. 763 - 775
Copyright
Copyright © INS. Published by Cambridge University Press, 2020

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.)

Footnotes

†

Equal co-first authors

References

REFERENCES

Aoki, Y., Inokuchi, R., Gunshin, M., Yahagi, N., & Suwa, H. (2012). Diffusion tensor imaging studies of mild traumatic brain injury: A meta-analysis. Journal of Neurology, Neurosurgery and Psychiatry, 83(9), 870–876. doi: 10.1136/jnnp-2012-302742CrossRefGoogle ScholarPubMed
Barlow, K.M., Crawford, S., Brooks, B.L., Turley, B., & Mikrogianakis, A. (2015). The incidence of postconcussion syndrome remains stable following mild traumatic brain injury in children. Pediatric Neurology, 53(6), 491–497. doi: 10.1016/j.pediatrneurol.2015.04.011CrossRefGoogle ScholarPubMed
Barlow, K.M., Crawford, S., Stevenson, A., Sandhu, S.S., Belanger, F., & Dewey, D. (2010). Epidemiology of postconcussion syndrome in pediatric mild traumatic brain injury. Pediatrics, 126(2), e374–e381. doi: 10.1542/peds.2009-0925CrossRefGoogle ScholarPubMed
Beaulieu, C. (2002). The basis of anisotropic water diffusion in the nervous system - A technical review. NMR in Biomedicine, 15(7–8), 435–455. doi: 10.1002/nbm.782CrossRefGoogle ScholarPubMed
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 (Methodological), 51(1), 289–300. doi: 10.2307/2346101CrossRefGoogle Scholar
Bigler, E. D. (2013). Neuroimaging biomarkers in mild traumatic brain injury (mTBI). Neuropsychology Review, 23(3), 169–209. doi: 10.1007/s11065-013-9237-2CrossRefGoogle Scholar
Brooks, B.L., & Barlow, K.M. (2011). A methodology for assessing treatment response in hashimoto’s encephalopathy: A case study demonstrating repeated computerized neuropsychological testing. Journal of Child Neurology, 26(6), 786–791. doi: 10.1177/0883073810391532CrossRefGoogle ScholarPubMed
Brooks, B.L., Iverson, G.L., Atkins, J.E., Zafonte, R., & Berkner, P.D. (2016). Sex differences and self-reported attention problems during baseline concussion testing. Applied Neuropsychology: Child, 5(2), 119–126. doi: 10.1080/21622965.2014.1003066CrossRefGoogle ScholarPubMed
Brooks, B.L., Khan, S., Daya, H., Mikrogianakis, A., & Barlow, K.M. (2014). Neurocognition in the emergency department after a mild traumatic brain injury in youth. Journal of Neurotrauma, 31(20), 1744–1749. doi: 10.1089/neu.2014.3356CrossRefGoogle ScholarPubMed
Brooks, B.L., & Sherman, E.M.S. (2012). Computerized neuropsychological testing to rapidly evaluate cognition in pediatric patients with neurologic disorders. Journal of Child Neurology, 27(8), 982–991. doi: 10.1177/0883073811430863CrossRefGoogle ScholarPubMed
Brooks, B.L., Sherman, E.M.S., & Krol, A.L. (2012). Utility of TOMM trial 1 as an indicator of effort in children and adolescents. Archives of Clinical Neuropsychology, 27(1), 23–29. doi: 10.1093/arclin/acr086CrossRefGoogle ScholarPubMed
Carlson, H.L., Laliberté, C., Brooks, B.L., Hodge, J., Kirton, A., Bello-Espinosa, L., Hader, W., & Sherman, E.M.S. (2014). Reliability and variability of diffusion tensor imaging (DTI) tractography in pediatric epilepsy. Epilepsy and Behavior, 37, 116–122. doi: 10.1016/j.yebeh.2014.06.020CrossRefGoogle ScholarPubMed
Carroll, L.J., Cassidy, J.D., Holm, L., Kraus, J., Coronado, V.G., & WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. (2004). Methodological issues and research recommendations for mild traumatic brain injury: the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. Journal of Rehabilitation Medicine, (43 Suppl), 113–125. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/15083875 10.1080/16501960410023877CrossRefGoogle ScholarPubMed
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. doi: 10.1089/neu.2015.3948CrossRefGoogle ScholarPubMed
Churchill, N.W., Hutchison, M.G., Richards, D., Leung, G., Graham, S.J., & Schweizer, T.A. (2017). Neuroimaging of sport concussion: Persistent alterations in brain structure and function at medical clearance. Scientific Reports, 7(1), 8297. doi: 10.1038/s41598-017-07742-3CrossRefGoogle ScholarPubMed
Colby, J.B., Soderberg, L., Lebel, C., Dinov, I.D., Thompson, P.M., & Sowell, E.R. (2012). Along-tract statistics allow for enhanced tractography analysis. NeuroImage, 59(4), 3227–3242. doi: 10.1016/j.neuroimage.2011.11.004CrossRefGoogle ScholarPubMed
Davis, G.A., Anderson, V., Babl, F.E., Gioia, G.A., Giza, C.C., Meehan, W., Moser, R.S., Purcell, L., Schatz, P., Schneider, P.J., Takagi, M., Yeates, K.O., & Zemek, R. (2017). What is the difference in concussion management in children as compared with adults? A systematic review. British Journal of Sports Medicine, 51(12), 949–957. doi: 10.1136/bjsports-2016-097415CrossRefGoogle ScholarPubMed
Dean, P.J.A., Sato, J.R., Vieira, G., McNamara, A., & Sterr, A. (2015). Long-term structural changes after mTBI and their relation to post-concussion symptoms. Brain Injury, 29(10), 1211–1218. doi: 10.3109/02699052.2015.1035334CrossRefGoogle ScholarPubMed
Dodd, A.B., Epstein, K., Ling, J.M., & Mayer, A.R. (2014). Diffusion tensor imaging findings in semi-acute mild traumatic brain injury. Journal of Neurotrauma, 31(14), 1235–1248. doi: 10.1089/neu.2014.3337CrossRefGoogle ScholarPubMed
Eierud, C., Craddock, R.C., Fletcher, S., Aulakh, M., King-Casas, B., Kuehl, D., & Laconte, S.M. (2014). Neuroimaging after mild traumatic brain injury: Review and meta-analysis. NeuroImage: Clinical, 4, 283–294. doi: 10.1016/j.nicl.2013.12.009CrossRefGoogle ScholarPubMed
Garthe, E., & States, J.D. (1999). Abbreviated injury scale unification: the case for a unified injury system for global use. The Journal of Trauma, 47(2), 309–323.CrossRefGoogle ScholarPubMed
Geary, E.K., Kraus, M.F., Pliskin, N.H., & Little, D.M. (2010). Verbal learning differences in chronic mild traumatic brain injury. Journal of the International Neuropsychological Society, 16(3), 506–516. doi: 10.1017/S135561771000010XCrossRefGoogle ScholarPubMed
Gioia, G.A., Schneider, J.C., Vaughan, C.G., & Isquith, P.K. (2009). Which symptom assessments and approaches are uniquely appropriate for paediatric concussion? British Journal of Sports Medicine, 43(Suppl 1), i13–22. doi: 10.1136/bjsm.2009.058255CrossRefGoogle ScholarPubMed
Groeschel, S., Tournier, J.D., Northam, G.B., Baldeweg, T., Wyatt, J., Vollmer, B., & Connelly, A. (2014). Identification and interpretation of microstructural abnormalities in motor pathways in adolescents born preterm. NeuroImage, 87, 209–219. doi: 10.1016/j.neuroimage.2013.10.034CrossRefGoogle ScholarPubMed
Grohs, M.N., Reynolds, J.E., Dewey, D., & Lebel, C. (2018). Corpus callosum microstructure is associated with motor function in preschool children. NeuroImage, 183, 828–835. doi: 10.1016/j.neuroimage.2018.09.004CrossRefGoogle ScholarPubMed
Grossman, E.J., Ge, Y., Jensen, J.H., Babb, J.S., Miles, L., Reaume, J., Silver, J.M., Grossman, R.I., & Inglese, M. (2012). Thalamus and cognitive impairment in mild traumatic brain injury: A Diffusional Kurtosis imaging study. Journal of Neurotrauma, 29(13), 2318–2327. doi: 10.1089/neu.2011.1763CrossRefGoogle ScholarPubMed
Gualtieri, C.T., & Johnson, L.G. (2006). Reliability and validity of a computerized neurocognitive test battery, CNS Vital Signs. Archives of Clinical Neuropsychology, 21(7), 623–643. doi: 10.1016/j.acn.2006.05.007CrossRefGoogle ScholarPubMed
Hart, J., Kraut, M.A., Womack, K.B., Strain, J., Didehbani, N., Bartz, E., Conover, H., Mansinghani, S., Lu, H., & Cullum, C.M. (2013). Neuroimaging of cognitive dysfunction and depression in aging retired national football league players. JAMA Neurology, 70(3), 326. doi: 10.1001/2013.jamaneurol.340CrossRefGoogle ScholarPubMed
Hellstrøm, T., Westlye, L.T., Kaufmann, T., Trung Doan, N., Søberg, H.L., Sigurdardottir, S., Nordhøy, W., Helseth, E., Andreassen, O.A., & Andelic, N. (2017). White matter microstructure is associated with functional, cognitive and emotional symptoms 12 months after mild traumatic brain injury. Scientific Reports, 7(1), 13795. doi: 10.1038/s41598-017-13628-1CrossRefGoogle ScholarPubMed
Henry, L.C., Tremblay, J., Tremblay, S., Lee, A., Brun, C., Lepore, N., Theoret, H., Ellemberg, D., & Lassonde, M. (2011). Acute and chronic changes in diffusivity measures after sports concussion. Journal of Neurotrauma, 28(10), 2049–2059. doi: 10.1089/neu.2011.1836CrossRefGoogle ScholarPubMed
Honce, J.M., Nyberg, E., Jones, I., & Nagae, L. (2016). Neuroimaging of concussion. Physical Medicine and Rehabilitation Clinics of North America, 27(2), 411–428. doi: 10.1016/j.pmr.2016.01.002CrossRefGoogle ScholarPubMed
Ilie, G., Boak, A., Adlaf, E.M., Asbridge, M., & Cusimano, M.D. (2013). Prevalence and correlates of traumatic brain injuries among adolescents. Journal of the American Medical Association, 309(24):2550–2552. doi: 10.1001/jama.2013.6750CrossRefGoogle ScholarPubMed
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(2), 298–303. doi: 10.3171/jns.2005.103.2.0298CrossRefGoogle ScholarPubMed
Iverson, G.L., Atkins, J.E., Zafonte, R., & Berkner, P.D. (2016). Concussion history in adolescent athletes with attention-deficit hyperactivity disorder. Journal of Neurotrauma, 33(23), 2077–2080. doi: 10.1089/neu.2014.3424CrossRefGoogle ScholarPubMed
Iverson, G.L., Wojtowicz, M., Brooks, B.L., Maxwell, B.A., Atkins, J.E., Zafonte, R., & Berkner, P.D. (2016). High school athletes with ADHD and learning difficulties have a greater lifetime concussion history. Journal of Attention Disorders, 108705471665741. doi: 10.1177/1087054716657410Google ScholarPubMed
Khong, E., Odenwald, N., Hashim, E., & Cusimano, M.D. (2016). Diffusion tensor imaging findings in post-concussion syndrome patients after mild traumatic brain injury: A systematic review. Frontiers in Neurology, 7, 156. doi: 10.3389/fneur.2016.00156CrossRefGoogle ScholarPubMed
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(10), 2508–2519. doi: 10.1093/brain/awm216CrossRefGoogle ScholarPubMed
Lebel, C., & Beaulieu, C. (2011). Longitudinal development of human brain wiring continues from childhood into adulthood. Journal of Neuroscience, 31(30), 10937–10947. doi: 10.1523/JNEUROSCI.5302-10.2011CrossRefGoogle ScholarPubMed
Lee, L.K. (2007). Controversies in the sequelae of pediatric mild traumatic brain injury. Pediatric Emergency Care, 23(8), 580–583. doi: 10.1097/PEC.0b013e31813444eaCrossRefGoogle ScholarPubMed
Lipton, M.L., Kim, N., Park, Y.K., Hulkower, M.B., Gardin, T.M., Shifteh, K., Kim, M., Zimmerman, M.E., Lipton, R.B., & Branch, C.A. (2012). Robust detection of traumatic axonal injury in individual mild traumatic brain injury patients: Intersubject variation, change over time and bidirectional changes in anisotropy. Brain Imaging and Behavior, 6(2), 329–342. doi: 10.1007/s11682-012-9175-2CrossRefGoogle ScholarPubMed
Lo, C., Shifteh, K., Gold, T., Bello, J.A., & Lipton, M.L. (2009). Diffusion tensor imaging abnormalities in patients with mild traumatic brain injury and neurocognitive impairment. Journal of Computer Assisted Tomography, 33(2), 293–297. doi: 10.1097/RCT.0b013e31817579d1CrossRefGoogle ScholarPubMed
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. doi: 10.1542/peds.2011-2083CrossRefGoogle ScholarPubMed
Mayer, A.R., Ling, J.M., Yang, Z., Pena, A., Yeo, R.A., & Klimaj, S. (2012). Diffusion abnormalities in pediatric mild traumatic brain injury. Journal of Neuroscience, 32(50), 17961–17969. doi: 10.1523/JNEUROSCI.3379-12.2012CrossRefGoogle ScholarPubMed
McCauley, S.R., Wilde, E.A., Anderson, V.A., Bedell, G., Beers, S.R., Campbell, T.F., Chapman, S.B., Ewing-Cobbs, L., Gerring, J.P., Gioia, J.A., Levin, H.S., Michaud, L.J., Prasad, M.R., Swaine, B.R., Turkstra, L.S., Wade, S.L., Yeates, K.O., & Pediatric TBI Outcomes Workgroup. (2012). Recommendations for the use of common outcome measures in pediatric traumatic brain injury research. Journal of Neurotrauma, 29(4), 678–705. doi: 10.1089/neu.2011.1838CrossRefGoogle ScholarPubMed
Moore, R.D., Kay, J.J., & Ellemberg, D. (2018). The long-term outcomes of sport-related concussion in pediatric populations. International Journal of Psychophysiology, 132, 14–24. doi: 10.1016/j.ijpsycho.2018.04.003CrossRefGoogle ScholarPubMed
Narayana, P.A. (2017). White matter changes in patients with mild traumatic brain injury: MRI perspective. Concussion, 2(2), CNC35. doi: 10.2217/cnc-2016-0028CrossRefGoogle ScholarPubMed
Orr, C.A., Albaugh, M.D., Watts, R., Garavan, H., Andrews, T., Nickerson, J.P., Gonyea, J., Hipko, S., Zweber, C., Logan, K., & Hudziak, J.J. (2016). Neuroimaging biomarkers of a history of concussion observed in asymptomatic young athletes. Journal of Neurotrauma, 33(9), 803–810. doi: 10.1089/neu.2014.3721CrossRefGoogle ScholarPubMed
Plourde, V., & Brooks, B.L. (2017). Is computerized cognitive testing useful in children and adolescents with moderate-to-severe traumatic brain injury? Journal of the International Neuropsychological Society, 23(4), 304–313. doi: 10.1017/S1355617717000066CrossRefGoogle ScholarPubMed
Plourde, V., Hrabok, M., Sherman, E.M.S., & Brooks, B. L. (2018). Validity of a computerized cognitive battery in children and adolescents with neurological diagnoses. Archives of Clinical Neuropsychology, 33(2), 247–253. doi: 10.1093/arclin/acx067CrossRefGoogle ScholarPubMed
Rutgers, D.R., Fillard, P., Paradot, G., Tadié, 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(9), 1730–1735. doi: 10.3174/ajnr.A1213CrossRefGoogle ScholarPubMed
Rutland-Brown, W., Langlois, J.A., Thomas, K.E., & Xi, Y.L. (2006). Incidence of traumatic brain injury in the United States, 2003. Journal of Head Trauma Rehabilitation, 21(6), 544–548. doi: 10.1097/00001199-200611000-00009CrossRefGoogle ScholarPubMed
Schmidt, J., Hayward, K.S., Brown, K.E., Zwicker, J.G., Ponsford, J., van Donkelaar, P., Babul, S., & Boyd, L.A. (2018). Imaging in pediatric concussion: A systematic review. Pediatrics, 141(5), e20173406. doi: 10.1542/peds.2017-3406CrossRefGoogle ScholarPubMed
Shenton, M.E., Hamoda, H.M., Schneiderman, J.S., Bouix, S., Pasternak, O., Rathi, Y., Vu, M.A., Purohit, M.P., Helmer, K., Koerte, I., Lin, A.P., Westin, C.F., Kikinis, R., Kubicki, M., Stern, R.A., & Zafonte, R. (2012). A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging and Behavior, 6(2), 137–192. doi: 10.1007/s11682-012-9156-5CrossRefGoogle ScholarPubMed
Snook, L., Plewes, C., & Beaulieu, C. (2007). Voxel based versus region of interest analysis in diffusion tensor imaging of neurodevelopment. NeuroImage, 34(1), 243–252. doi: 10.1016/j.neuroimage.2006.07.021CrossRefGoogle ScholarPubMed
Strain, J., Didehbani, N., Cullum, C.M., Mansinghani, S., Conover, H., Kraut, M.A., Hart, J., & Womack, K.B. (2013). Depressive symptoms and white matter dysfunction in retired NFL players with concussion history. Neurology, 81(1), 25–32. doi: 10.1212/WNL.0b013e318299ccf8CrossRefGoogle ScholarPubMed
Teasdale, G., & Jennett, B. (1974). Assessment of coma and impaired consciousness. A practical scale. The Lancet, 2(7872), 81–84. doi: 10.1016/S0140-6736(74)91639-0CrossRefGoogle ScholarPubMed
Terry, D.P., Mewborn, C.M., & Miller, L.S. (2018). Repeated sport-related concussion shows only minimal white matter differences many years after playing high school football. Journal of the International Neuropsychological Society, 25(9), 950–960. doi: 10.1016/j.ijpsycho.2018.04.003CrossRefGoogle Scholar
Tombaugh, T. (1996). Test of Memory of Malingering (TOMM). North Tonawanda, NY: Multi-Health Systems.Google Scholar
Tournier, J.D., Calamante, F., & Connelly, A. (2012). MRtrix: Diffusion tractography in crossing fiber regions. International Journal of Imaging Systems and Technology, 22(1), 53–66. doi: 10.1002/ima.22005CrossRefGoogle Scholar
Treble, A., Hasan, K.M., Iftikhar, A., Stuebing, K.K., Kramer, L.A., Cox, C.S., Swank, P.R., & Ewing-Cobbs, L. (2013). Working memory and corpus callosum microstructural integrity after pediatric traumatic brain injury: A diffusion tensor tractography study. Journal of Neurotrauma, 30(19), 1609–1619. doi: 10.1089/neu.2013.2934CrossRefGoogle ScholarPubMed
Tremblay, S., Henry, L.C., Bedetti, C., Larson-Dupuis, C., Gagnon, J.-F., Evans, A.C., Théoret, H., Lassonde, M., & De Beaumont, L. (2014). Diffuse white matter tract abnormalities in clinically normal ageing retired athletes with a history of sports-related concussions. Brain, 137(11), 2997–3011. doi: 10.1093/brain/awu236CrossRefGoogle ScholarPubMed
Van Beek, L., Vanderauwera, J., Ghesquière, P., Lagae, L., & De Smedt, B. (2015). Longitudinal changes in mathematical abilities and white matter following paediatric mild traumatic brain injury. Brain Injury, 29(13–14), 1701–1710. doi: 10.3109/02699052.2015.1075172CrossRefGoogle ScholarPubMed
Veeramuthu, V., Narayanan, V., Kuo, T.L., Delano-Wood, L., Chinna, K., Bondi, M.W., Waran, V., Ganesan, D., & 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. doi: 10.1089/neu.2014.3750CrossRefGoogle ScholarPubMed
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. doi: 10.1016/j.pediatrneurol.2012.09.005CrossRefGoogle ScholarPubMed
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 adolescents. Neurology, 70(12), 948–955. doi: 10.1212/01.wnl.0000305961.68029.54CrossRefGoogle ScholarPubMed
Womack, K.B., Paliotta, C., Strain, J.F., Ho, J.S., Skolnick, Y., Lytton, W.W., Turtzo, L.C., McColl, R., Diaz-Arrastia, R., & Bergold, P.J. (2017). Measurement of peripheral vision reaction time identifies white matter disruption in patients with mild traumatic brain injury. Journal of Neurotrauma, 34(8), 1539–1545. doi: 10.1089/neu.2016.4670CrossRefGoogle ScholarPubMed
Woolrich, M.W., Jbabdi, S., Patenaude, B., Chappell, M., Makni, S., Behrens, T., Beckmann, C., Jenkinson, M., & Smith, S.M. (2009). Bayesian analysis of neuroimaging data in FSL. NeuroImage, 45(1 Suppl), S173–S186. doi: 10.1016/j.neuroimage.2008.10.055CrossRefGoogle ScholarPubMed
Zemek, R., Barrowman, N., Freedman, S.B., Gravel, J., Gagnon, I., McGahern, C., Aglipay, M., Sangha, G., Boutis, K., Beer, D., Craig, W., Burns, E., Farion, K.J., Mikrogianakis, A., Barlow, K., Dubrovsky, A.S., Meeuwisse, W., Gioia, G., Meehan, W.P., Beauchamp, M.H., Kamil, Y., Grool, A.M., Hoshizaki, B., Anderson, P., Brooks, B.L., Yeates, K.O., Vassilyadi, M., Klassen, T., Keightley, M., Richer, L., De Matteo, C., Osmond, M.H., Xie, J., Chatfield, J., Dow, N., Papadimitropoulos, R., Levesque, T., Langford, C., Tran, T.T., McGahern, C., DiGirolamo, V., Mazza, J., Lagace, M., Cook, R., Fitzpatrick, E., MacIntyre, J., & Moore, J. (2016). Clinical risk score for persistent postconcussion symptomsamong children with acute concussion in the ED. Journal of the American Medical Association, 315(10), 1014–1025. doi: 10.1001/jama.2016.1203CrossRefGoogle ScholarPubMed
Zemek, R., Farion, K.J., Sampson, M., & McGahern, C. (2013). Prognosticators of Persistent Symptoms Following Pediatric Concussion. JAMA Pediatrics, 167(3), 259. doi: 10.1001/2013.jamapediatrics.216CrossRefGoogle ScholarPubMed
Zhang, K., Johnson, B., Pennell, D., Ray, W., Sebastianelli, W., & Slobounov, S. (2010). Are functional deficits in concussed individuals consistent with white matter structural alterations: combined FMRI & DTI study. Experimental Brain Research, 204(1), 57–70. doi: 10.1007/s00221-010-2294-3CrossRefGoogle ScholarPubMed
Zhang, S., & Arfanakis, K. (2018). Evaluation of standardized and study-specific diffusion tensor imaging templates of the adult human brain: Template characteristics, spatial normalization accuracy, and detection of small inter-group FA differences. NeuroImage, 172, 40–50. doi: 10.1016/j.neuroimage.2018.01.046CrossRefGoogle ScholarPubMed