Altered white matter diffusivity and subtle motor function in a pilot cohort of adolescents with sports-related concussion

References

• Wiebe DJ, Comstock RD, Nance ML. Concussion research: a public health priority. Inj Prev. 2011;17(1):69–70. doi:10.1136/ip.2010.031211.
   PubMed Web of Science ®Google Scholar
• Giza CC, Hovda DA. The new neurometabolic cascade of concussion. Neurosurgery. 2014;75:S24–33. doi:10.1227/NEU.0000000000000505.
   PubMedGoogle Scholar
• Gardner A, Kay-Lambkin F, Stanwell P, Donnelly J, Williams WH, Hiles A, Schofield P, Levi C, and Jones DK. A systematic review of diffusion tensor imaging findings in sports-related concussion. J Neurotrauma. 2012;29(16):2521–38. doi:10.1089/neu.2012.2628.
   PubMed Web of Science ®Google Scholar
• Wilde EA, Goodrich-Hunsaker NJ, Ware AL, Taylor BA, Biekman BD, Hunter JV, Newman-Norlund R, Scarneo S, Casa DJ, Levin HS, et al. DTI indicators of white matter injury are correlated with multimodal EEG-based biomarker in slow recovering, concussed collegiate athletes. J Neurotrauma. 2020;37(19):2093–101. doi:10.1089/neu.2018.6365.
   PubMed Web of Science ®Google Scholar
• Roberts RM, Mathias JL, Rose SE. Diffusion tensor imaging (DTI) findings following pediatric non-penetrating TBI: a meta-analysis. Dev Neuropsychol. 2014;39(8):600–37. doi:10.1080/87565641.2014.973958.
   PubMed Web of Science ®Google Scholar
• Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurotherapeutics. 2007;4(3):316–29. doi:10.1016/j.nurt.2007.05.011.
   PubMed Web of Science ®Google Scholar
• Niogi SN, Mukherjee P. Diffusion tensor imaging of mild traumatic brain injury. J Head Trauma Rehabil. 2010;25(4):241–55. doi:10.1097/HTR.0b013e3181e52c2a.
   PubMed Web of Science ®Google Scholar
• Borja MJ, Chung S, Lui YW. Diffusion MR imaging in mild traumatic brain injury. Neuroimaging Clin N Am. 2018;28(1):117–26. doi:10.1016/j.nic.2017.09.009.
   PubMed Web of Science ®Google Scholar
• Mainwaring L, Ferdinand Pennock KM, Mylabathula S, Alavie BZ. Subconcussive head impacts in sport: a systematic review of the evidence. Int J Psychophysiol. 2018;132:39–54. doi:10.1016/j.ijpsycho.2018.01.007.
   PubMed Web of Science ®Google Scholar
• Narayana PA. White matter changes in patients with mild traumatic brain injury: MRI perspective. Concussion. 2017;2(2):CNC35. doi:10.2217/cnc-2016-0028.
   PubMedGoogle Scholar
• Cubon VA, Putukian M, Boyer C, Dettwiler A. A diffusion tensor imaging study on the white matter skeleton in individuals with sports-related concussion. J Neurotrauma. 2010;28(2):189–201. doi:10.1089/neu.2010.1430.
   Web of Science ®Google Scholar
• Smits M, Houston GC, Dippel DWJ, Wielopolski PA, Vernooij MW, Koudstaal PJ, Hunink MGM, and van der Lugt A Microstructural brain injury in post-concussion syndrome after minor head injury. Neuroradiology. 2011;53(8):553–63. doi:10.1007/s00234-010-0774-6.
   PubMed Web of Science ®Google Scholar
• Maugans TA, Farley C, Altaye M, Leach J, Cecil KM. Pediatric sports-related concussion produces cerebral blood flow alterations. Pediatrics. 2012;129(1):28–37. doi:10.1542/peds.2011-2083.
   PubMed Web of Science ®Google Scholar
• Zhang K, Johnson B, Pennell D, Ray W, Sebastianelli W, Slobounov S. Are functional deficits in concussed individuals consistent with white matter structural alterations: combined FMRI & DTI study. Exp Brain Res. 2010;204(1):57–70. doi:10.1007/s00221-010-2294-3.
   PubMed Web of Science ®Google Scholar
• Satchell EK, Friedman SD, Bompadre V, Poliakov A, Oron A, Jinguji TM. Use of diffusion tension imaging in the evaluation of pediatric concussions. Musculoskeletal Sci Pract. 2019;42:162–65. doi:10.1016/j.msksp.2019.05.002.
   PubMed Web of Science ®Google Scholar
• Virji-Babul N, Borich MR, Makan N, Moore T, Frew K, Emery CA, and Boyd LA. Diffusion tensor imaging of sports-related concussion in adolescents. Pediatr Neurol. 2013;48(1):24–29. doi:10.1016/j.pediatrneurol.2012.09.005.
   PubMed Web of Science ®Google Scholar
• Churchill NW, Hutchison MG, Graham SJ, Schweizer TA. Mapping brain recovery after concussion: from acute injury to 1 year after medical clearance. Neurology. 2019;93(21):e1980–92. doi:10.1212/WNL.0000000000008523.
   PubMed Web of Science ®Google Scholar
• Lancaster MA, Olson DV, McCrea MA, Nelson LD, LaRoche AA, Muftuler LT. Acute white matter changes following sport-related concussion: a serial diffusion tensor and diffusion kurtosis tensor imaging study. Hum Brain Mapp. 2016;37(11):3821–34. doi:10.1002/hbm.23278.
   PubMed Web of Science ®Google Scholar
• Wu T, Merkley TL, Wilde EA, Barnes A, Li X, and Chu ZD. A preliminary report of cerebral white matter microstructural changes associated with adolescent sports concussion acutely and subacutely using diffusion tensor imaging. Brain Imaging and Behavior 2018; 12:962–73.
   Google Scholar
• Borich M, Makan N, Boyd L, Virji-Babul N. Combining whole-brain voxel-wise analysis with in vivo tractography of diffusion behavior after sports-related concussion in adolescents: a preliminary report. J Neurotrauma. 2013;30(14):1243–49. doi:10.1089/neu.2012.2818.
   PubMed Web of Science ®Google Scholar
• Babcock L, Yuan W, Leach J, Nash T, Wade S, Suskauer S. White matter alterations in youth with acute mild traumatic brain injury. J Pediatr Rehabil Med. 2015;8(4):285–96. doi:10.3233/PRM-150347.
   PubMed Web of Science ®Google Scholar
• Murdaugh DL, King TZ, Sun B, Jones RA, Ono KE, Reisner A, and Burns TG. Longitudinal changes in resting state connectivity and white matter integrity in adolescents with sports-related concussion. J Int Neuropsychol Soc. 2018;24(8):781–92. doi:10.1017/S1355617718000413.
   PubMed Web of Science ®Google Scholar
• Kirkwood MW, Yeates KO, Taylor HG, Randolph C, McCrea M, Anderson VA. Management of pediatric mild traumatic brain injury: a neuropsychological review from injury through recovery. Clin Neuropsychol. 2008;22(5):769–800. doi:10.1080/13854040701543700.
   PubMed Web of Science ®Google Scholar
• Stephens JA, Denckla MB, McCambridge T, Slomine BS, Mahone EM, Suskauer SJ. Preliminary use of the physical and neurological examination of subtle signs for detecting subtle motor signs in adolescents with sport-related concussion. Am J Phys Med Rehabil. 2018;97(6):456. doi:10.1097/PHM.0000000000000906.
   PubMed Web of Science ®Google Scholar
• Stephens JA, Davies PL, Gavin WJ, Mostofsky SH, Slomine BS, Suskauer SJ. Evaluating motor control improves discrimination of adolescents with and without sports related concussion. J Mot Behav. 2020;52(1):13–21. doi:10.1080/00222895.2019.1570908.
   PubMed Web of Science ®Google Scholar
• McCrory P, Meeuwisse W, Dvorak J, Aubry M, Bailes J, Broglio S, Cantu RC, Cassidy D, Echemendia RJ, Castellani RJ, et al. Consensus statement on concussion in sport—the 5th international conference on concussion in sport held in Berlin, October 2016. Br J Sports Med. 2017;51(11):838–47. doi:10.1136/bjsports-2017-097699.
   PubMed Web of Science ®Google Scholar
• Denckla MB. Revised neurological examination and subtle signs. Psychopharmacol Bull. 1985;21(4):773–79.
   PubMed Web of Science ®Google Scholar
• Stephens JA, Salorio C, Denckla M, Mostofsky S, Suskauer S. Subtle motor findings during recovery from pediatric traumatic brain injury: a preliminary report. J Mot Behav. 2017;49(1):20–26. doi:10.1080/00222895.2016.1204267.
   PubMed Web of Science ®Google Scholar
• Crasta JE, Raja AE, Caffo BS, Hluchan CM, and Suskauer SJ. The effect of age and competition level on subtle motor performance in adolescents medically-cleared post-concussion: preliminary findings. Am J Phys Med Rehabil. 2021;100(6): 563–569. doi:10.1097/PHM.0000000000001589.
   PubMed Web of Science ®Google Scholar
• Mayer AR, Ling JM, Yang Z, Pena A, Yeo RA, Klimaj S. Diffusion abnormalities in pediatric mild traumatic brain injury. J Neurosci. 2012;32(50):17961–69. doi:10.1523/JNEUROSCI.3379-12.2012.
   PubMed Web of Science ®Google Scholar
• Wilde EA, McCauley SR, Hunter JV, Bigler ED, Chu Z, Wang ZJ, Hanten GR, Troyanskaya M, Yallampalli R, Li X, et al. Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology. 2008;70(12):948–55. doi:10.1212/01.wnl.0000305961.68029.54.
   PubMed Web of Science ®Google Scholar
• Wahl M, Lauterbach-Soon B, Hattingen E, Jung P, Singer O, Volz S, Klein JC, Steinmetz H, and Ziemann U. Human motor corpus callosum: topography, somatotopy, and link between microstructure and function. J Neurosci. 2007;27(45):12132–38. doi:10.1523/JNEUROSCI.2320-07.2007.
   PubMed Web of Science ®Google Scholar
• Kim JS, Pope A. Somatotopically located motor fibers in Corona radiata: evidence from subcortical small infarcts. Neurology. 2005;64(8):1438. doi:10.1212/01.WNL.0000158656.09335.E7.
   PubMed Web of Science ®Google Scholar
• Simmonds DJ, Hallquist MN, Asato M, Luna B. Developmental stages and sex differences of white matter and behavioral development through adolescence: a longitudinal diffusion tensor imaging (DTI) study. NeuroImage. 2014;92:356–68. doi:10.1016/j.neuroimage.2013.12.044.
   PubMed Web of Science ®Google Scholar
• Chun IY, Mao X, Breedlove EL, Leverenz LJ, Nauman EA, Talavage TM. DTI detection of longitudinal WM abnormalities due to accumulated head impacts. Dev Neuropsychol. 2015;40(2):92–97. doi:10.1080/87565641.2015.1020945.
   PubMed Web of Science ®Google Scholar
• Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM. FSL. NeuroImage. 2012;62(2):782–90. doi:10.1016/j.neuroimage.2011.09.015.
   PubMed Web of Science ®Google Scholar
• Andersson JLR, Skare S, Ashburner J. How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging. NeuroImage. 2003;20(2):870–88. doi:10.1016/S1053-8119(03)00336-7.
   PubMed Web of Science ®Google Scholar
• Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, et al. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage. 2004;23:S208–19.
   PubMed Web of Science ®Google Scholar
• Wu M, Chang L-C, Walker L, Lemaitre H, Barnett AS, and Marenco S. Comparison of EPI distortion correction methods in diffusion tensor MRI using a novel framework. In: Metaxas D, Axel L, Fichtinger G, and Székely G, editors. Medical image computing and computer-assisted intervention – MICCAI 2008. Berlin, Heidelberg: Springer; 2008. p. 321–29. (Lecture Notes in Computer Science).
   Google Scholar
• Tao R, Fletcher PT, Gerber S, Whitaker RT. A variational image-based approach to the correction of susceptibility artifacts in the alignment of diffusion weighted and structural MRI. In: Prince JL, Pham DL, Myers KJ, editors. Information processing in medical imaging Berlin. Heidelberg: Springer; 2009. p. 664–75. (Lecture Notes in Computer Science).
   Google Scholar
• Andersson JLR, Sotiropoulos SN. An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. NeuroImage. 2016;125:1063–78. doi:10.1016/j.neuroimage.2015.10.019.
   PubMed Web of Science ®Google Scholar
• Andersson JLR, Graham MS, Zsoldos E, Sotiropoulos SN. Incorporating outlier detection and replacement into a non-parametric framework for movement and distortion correction of diffusion MR images. NeuroImage. 2016;141:556–72. doi:10.1016/j.neuroimage.2016.06.058.
   PubMed Web of Science ®Google Scholar
• Jenkinson M, Smith S. A global optimisation method for robust affine registration of brain images. Med Image Anal. 2001;5(2):143–56. doi:10.1016/S1361-8415(01)00036-6.
   PubMed Web of Science ®Google Scholar
• Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage. 2002;17(2):825–41. doi:10.1006/nimg.2002.1132.
   PubMed Web of Science ®Google Scholar
• Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage. 2012;59(3):2142–54. doi:10.1016/j.neuroimage.2011.10.018.
   PubMed Web of Science ®Google Scholar
• R Core Team. R: a language and environment for statistical computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2014. Available from: http://www.R-project.org
   Google Scholar
• Mori S, Oishi K, Jiang H, Jiang L, Li X, Akhter K, Hua K, Faria AV, Mahmood A, Woods R, et al. Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. NeuroImage. 2008;40(2):570–82. doi:10.1016/j.neuroimage.2007.12.035.
   PubMed Web of Science ®Google Scholar
• Gidley Larson JC, Mostofsky SH, Goldberg MC, Cutting LE, Denckla MB, Mahone EM. Effects of gender and age on motor exam in typically developing children. Dev Neuropsychol. 2007;32(1):543–62. doi:10.1080/87565640701361013.
   PubMed Web of Science ®Google Scholar
• Feldt LS. A comparison of the precision of three experimental designs employing a concomitant variable. Psychometrika. 1958;23(4):335–53. doi:10.1007/BF02289783.
   Web of Science ®Google Scholar
• Lakens D. Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Front Psychol. 2013;4:863. doi:10.3389/fpsyg.2013.00863.
   PubMed Web of Science ®Google Scholar
• Fritz CO, Morris PE, Richler JJ. Effect size estimates: current use, calculations, and interpretation. [Internet]. J Exp Psychol Gen. 2020;141(1):2. doi:10.1037/a0024338. US: American Psychological Association; 20110808
   Web of Science ®Google Scholar
• Chu Z, Wilde EA, Hunter JV, McCauley SR, Bigler ED, Troyanskaya M, Yallampalli R, Chia JM, and Levin HS. Voxel-based analysis of diffusion tensor imaging in mild traumatic brain injury in adolescents. AJNR Am J Neuroradiol. 2010;31(2):340–46. doi:10.3174/ajnr.A1806.
   PubMed Web of Science ®Google Scholar
• Wu Y-C, Harezlak J, Elsaid NMH, Lin Z, Wen Q, Mustafi SM, Riggen LD, Koch KM, Nencka AS, Meier TB, et al. Longitudinal white-matter abnormalities in sports-related concussion: a diffusion MRI study. Neurology. 2020;95(7):e781–e792. doi:10.1212/WNL.0000000000009930.
   PubMed Web of Science ®Google Scholar
• Chamard E, Lichtenstein JD. A systematic review of neuroimaging findings in children and adolescents with sports-related concussion. Brain Inj. 2018;32(7):816–31. doi:10.1080/02699052.2018.1463106.
   PubMed Web of Science ®Google Scholar
• Narayana S, Charles C, Collins K, Tsao JW, Stanfill AG, Baughman B. Neuroimaging and neuropsychological studies in sports-related concussions in adolescents: current state and future directions. Front Neurol. 2019;10. doi:10.3389/fneur.2019.00538.
   Web of Science ®Google Scholar
• Murugavel M, Cubon V, Putukian M, Echemendia R, Cabrera J, Osherson D, and Dettwiler A A longitudinal diffusion tensor imaging study assessing white matter fiber tracts after sports-related concussion. J Neurotrauma. 2014;31(22):1860–71. doi:10.1089/neu.2014.3368.
   PubMed Web of Science ®Google Scholar
• Myer GD, Yuan W, Barber Foss KD, Thomas S, Smith D, Leach J, Kiefer AW, Dicesare C, Adams J, Gubanich PJ, et al. Analysis of head impact exposure and brain microstructure response in a season-long application of a jugular vein compression collar: a prospective, neuroimaging investigation in American football. Br J Sports Med. 2016;50(20):1276–85. doi:10.1136/bjsports-2016-096134.
   PubMed Web of Science ®Google Scholar
• Davenport EM, Whitlow CT, Urban JE, Espeland MA, Jung Y, Rosenbaum DA, Gioia GA, Powers AK, Stitzel JD, Maldjian JA, et al. Abnormal white matter integrity related to head impact exposure in a season of high school varsity football. J Neurotrauma. 2014;31(19):1617–24. doi:10.1089/neu.2013.3233.
   PubMed Web of Science ®Google Scholar
• Bazarian JJ, Zhu T, Blyth B, Borrino A, Zhong J. Subject-specific changes in brain white matter on diffusion tensor imaging after sports-related concussion. Magn Reson Imaging. 2012;30(2):171–80. doi:10.1016/j.mri.2011.10.001.
   PubMed Web of Science ®Google Scholar
• Wozniak J, Krach L, Ward E, Mueller B, Muetzel R, Schnoebelen S, Kiragu A, and LIM K. Neurocognitive and neuroimaging correlates of pediatric traumatic brain injury: a diffusion tensor imaging (DTI) study. Arch Clin Neuropsychol. 2007;22(5):555–68. doi:10.1016/j.acn.2007.03.004.
   PubMed Web of Science ®Google Scholar
• Caeyenberghs K, Leemans A, Geurts M, Taymans T, Vander Linden C, Smits-Engelsman BCM, Sunaert S, and Swinnen SP. Brain-Behavior relationships in young traumatic brain injury patients: fractional anisotropy measures are highly correlated with dynamic visuomotor tracking performance. Neuropsychologia. 2010;48(5):1472–82. doi:10.1016/j.neuropsychologia.2010.01.017.
   PubMed Web of Science ®Google Scholar
• Caeyenberghs K, Leemans A, Geurts M, Linden CV, Smits-Engelsman lBCM, Sunaert S, and Swinnen SP. Correlations between white matter integrity and motor function in traumatic brain injury patients. Neurorehabil Neural Repair. 2011;25(6):492–502. doi:10.1177/1545968310394870.
   PubMed Web of Science ®Google Scholar
• Mayer AR, Ling J, Mannell MV, Gasparovic C, Phillips JP, Doezema D, Reichard R, Yeo RA, et al. A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology. 2010;74(8):643–50. doi:10.1212/WNL.0b013e3181d0ccdd.
   PubMed Web of Science ®Google Scholar
• Bartnik-Olson BL, Holshouser B, Wang H, Grube M, Tong K, Wong V, and Ashwal S. Impaired neurovascular unit function contributes to persistent symptoms after concussion: a pilot study. J Neurotrauma. 2014;31(17):1497–506. doi:10.1089/neu.2013.3213.
   PubMed Web of Science ®Google Scholar