A preliminary investigation of cognitive intolerance and neuroimaging among adolescents returning to school after concussion

References

• Corwin DJ, Zonfrillo MR, Master CL, Arbogast KB, Grady MF, Robinson RL, Goodman AM, Wiebe DJ. Characteristics of prolonged concussion recovery in a pediatric subspecialty referral population. J Pediatr. 2014;165(6):1207–15.doi:10.1016/j.jpeds.2014.08.034.
   PubMed Web of Science ®Google Scholar
• Ransom DM, Vaughan CG, Pratson L, Sady MD, McGill CA, Gioia GA. Academic effects of concussion in children and adolescents. Pediatrics. 2015;135(6):1043–50. doi:10.1542/peds.2014-3434.
   PubMed Web of Science ®Google Scholar
• Carson JD, Lawrence DW, Kraft SA, Garel A, Snow CL, Chatterjee A, Libfeld P, MacKenzie HM, Thornton JS, Moineddin R, et al. Premature return to play and return to learn after a sport-related concussion physician’s chart review. Can Fam Physician 2014;60:e310–e5.
   PubMed Web of Science ®Google Scholar
• Brown NJ, Mannix RC, O’Brien MJ, Gostine D, Collins MW, Meehan WP 3rd. Effect of cognitive activity level on duration of post-concussion symptoms. Pediatrics. 2014;133(2):e299–304. doi:10.1542/peds.2013-2125.
   PubMed Web of Science ®Google Scholar
• Moser RS, Glatts C, Schatz P.Efficacy of immediate and delayed cognitive and physical rest for treatment of sports-related concussion. J Pediatr. 2012;161(5):922–26. doi:10.1016/j.jpeds.2012.04.012.
   PubMed Web of Science ®Google Scholar
• Majerske CW, Mihalik JP, Ren D, Collins MW, Reddy CC, Lovell MR, Wagner AK. Concussion in sports: postconcussive activity levels, symptoms, and neurocognitive performance. J Athl Train. 2008;43(3):265.doi:10.4085/1062-6050-43.3.265.
   PubMed Web of Science ®Google Scholar
• Makki AY, Leddy JJ, Hinds A, Baker JG, Paluch R, Shucard J, Willer BS. School attendance and symptoms in adolescents after Sport-Related Concussion (SRC). Glob Pediatr Health. 2016;3:1–3. doi:10.1177/2333794X16630493.
   Google Scholar
• Leddy JJ, Baker JG, Kozlowski K, Bisson L, Willer B.Reliability of a graded exercise test for assessing recovery from concussion. Clin J Sport Med. 2011;21(2):89–94. doi:10.1097/JSM.0b013e3181fdc721.
   PubMed Web of Science ®Google Scholar
• Darling SR, Leddy JJ, Baker JG, Williams AJ, Surace A, Miecznikowski JC, Willer BS.Evaluation of the Zurich guidelines and exercise testing for return to play in adolescents following concussion. Clin J Sport Med. 2014;24(2):128–33. doi:10.1097/JSM.0000000000000026.
   PubMed Web of Science ®Google Scholar
• Leddy JJ, Kozlowski K, Donnelly JP, Pendergast DR, Epstein LH, Willer B.A preliminary study of subsymptom threshold exercise training for refractory post-concussion syndrome. Clin J Sport Med. 2010;20(1):21. doi:10.1097/JSM.0b013e3181c6c22c.
   PubMed Web of Science ®Google Scholar
• Baker JG, Freitas MS, Leddy JJ, Kozlowski KF, Willer BS. Return to full functioning after graded exercise assessment and progressive exercise treatment of postconcussion syndrome. Rehabil Res Pract. 2012;2012:1–7. doi:10.1155/2012/705309.
   Google Scholar
• Leddy JJ, Haider MN, Ellis MJ, Mannix R, Darling SR, Freitas MS, Suffoletto HN, Leiter J, Cordingley DM, Willer B, et al. Early subthreshold aerobic exercise for sport-related concussion: a randomized clinical trial. JAMA Pediatr. 2019;173(4):319–25.doi:10.1001/jamapediatrics.2018.4397.
   PubMed Web of Science ®Google Scholar
• Sady MD, Vaughan CG, Gioia GA.School and the concussed youth: recommendations for concussion education and management. Phys Med Rehabil Clin N Am. 2011;22(4):701–19. doi:10.1016/j.pmr.2011.08.008.
   PubMed Web of Science ®Google Scholar
• Gagnon I, Galli C, Friedman D, Grilli L, Iverson GL.Active rehabilitation for children who are slow to recover following sport-related concussion. Brain Inj. 2009;23(12):956–64. doi:10.3109/02699050903373477.
   PubMed Web of Science ®Google Scholar
• Gagnon I, Swaine B, Friedman D, Forget R.Exploring children’s self-efficacy related to physical activity performance after a mild traumatic brain injury. J Head Trauma Rehabil. 2005;20(5):436–49. doi:10.1097/00001199-200509000-00005.
   PubMed Web of Science ®Google Scholar
• Chen J-K, Johnston KM, Petrides M, Ptito A.Recovery from mild head injury in sports: evidence from serial functional magnetic resonance imaging studies in male athletes. Clin J Sport Med. 2008;18(3):241–47. doi:10.1097/JSM.0b013e318170b59d.
   PubMed Web of Science ®Google Scholar
• Chen J-K, Johnston KM, Collie A, McCrory P, Ptito A.A validation of the post concussion symptom scale in the assessment of complex concussion using cognitive testing and functional MRI. ‎J Neurol Neurosurg Psychiatry. 2007;78(11):1231–38. doi:10.1136/jnnp.2006.110395.
   PubMed Web of Science ®Google Scholar
• Lovell MR, Pardini JE, Welling J, Collins MW, Bakal J, Lazar N, Roush R, Eddy WF, Becker JT. Functional brain abnormalities are related to clinical recovery and time to return‐to‐play in athletes. Neurosurgery. 2007;61(2):352–60.doi:10.1227/01.NEU.0000279985.94168.7F.
   PubMed Web of Science ®Google Scholar
• Dettwiler A, Murugavel M, Putukian M, Cubon V, Furtado J, Osherson D.Persistent differences in patterns of brain activation after sports-related concussion: a longitudinal functional magnetic resonance imaging study. J Neurotrauma. 2014;31(2):180–88. doi:10.1089/neu.2013.2983.
   PubMed Web of Science ®Google Scholar
• Nelson LD, LaRoche AA, Pfaller AY, Lerner EB, Hammeke TA, Randolph C, Barr WB, Guskiewicz K, McCrea MA. Prospective, head-to-head study of three Computerized Neurocognitive Assessment Tools (CNTs): reliability and validity for the assessment of sport-related concussion. J Int Neuropsych Soc. 2016;22(1):24–37.doi:10.1017/S1355617715001101.
   PubMed Web of Science ®Google Scholar
• Meier TB, Bellgowan PSF, Singh R, Kuplicki R, Polanski DW, Mayer AR.Recovery of cerebral blood flow following sports-related concussion. JAMA Neurol. 2015;72(5):530–38. doi:10.1001/jamaneurol.2014.4778.
   PubMed Web of Science ®Google Scholar
• Tan CO, Meehan WP 3rd, Iverson GL, Taylor JA.Cerebrovascular regulation, exercise, and mild traumatic brain injury. Neurology. 2014;83(18):1665–72. doi:10.1212/WNL.0000000000000944.
   PubMed Web of Science ®Google Scholar
• Kasahara K, Hashimoto K, Abo M, Senoo A.Voxel- and atlas-based analysis of diffusion tensor imaging may reveal focal axonal injuries in mild traumatic brain injury – comparison with diffuse axonal injury. Magn Reson Imaging. 2012;30(4):496–505. doi:10.1016/j.mri.2011.12.018.
   PubMed Web of Science ®Google Scholar
• Johnson VE, Stewart W, Smith DH. Axonal pathology in traumatic brain injury. Exp Neurol. 2013;246:35–43. doi:10.1016/j.expneurol.2012.01.013.
   PubMed Web of Science ®Google Scholar
• Sorek G, Shaklai S, Meyer S, Katz-Leurer M.Autonomic cardiac control response to walking and executive cognitive task in adolescents with acquired brain injury and typically developed controls. Brain Inj. 2018;32(6):770–75. doi:10.1080/02699052.2018.1450993.
   PubMed Web of Science ®Google Scholar
• Rathbone ATL, Tharmaradinam S, Jiang S, Rathbone MP, Kumbhare DA. A review of the neuro-and systemic inflammatory responses in post concussion symptoms: introduction of the “post-inflammatory brain syndrome” PIBS. Brain Behav Immun. 2015;46:1–16. doi:10.1016/j.bbi.2015.02.009.
   PubMed Web of Science ®Google Scholar
• Henry LC, Tremblay J, Tremblay S, Lee A, Brun C, Lepore N, Theoret H, Ellemberg D, Lassonde M. Acute and chronic changes in diffusivity measures after sports concussion. J Neurotrauma. 2011;28(10):2049–59.doi:10.1089/neu.2011.1836.
   PubMed Web of Science ®Google 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. 2011;28(2):189–201. doi:10.1089/neu.2010.1430.
   PubMed Web of Science ®Google Scholar
• Lipton ML, Kim N, Park YK, Hulkower MB, Gardin TM, Shifteh K, Kim M, Zimmerman ME, Lipton RB, Branch CA, et al. 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 Behav. 2012;6(2):329–42.doi:10.1007/s11682-012-9175-2.
   PubMed Web of Science ®Google Scholar
• Eierud C, Craddock RC, Fletcher S, Aulakh M, King-Casas B, Kuehl D, LaConte SM. Neuroimaging after mild traumatic brain injury: review and meta-analysis. NeuroImage Clin. 2014;4:283–94.
   PubMed Web of Science ®Google Scholar
• Xiong K, Zhu Y, Zhang Y, Yin Z, Zhang J, Qiu M, Zhang W. White matter integrity and cognition in mild traumatic brain injury following motor vehicle accident. Brain Res. 2014;1591:86–92.
   PubMed Web of Science ®Google Scholar
• Lipton ML, Gulko E, Zimmerman ME, Friedman BW, Kim M, Gellella E, Gold T, Shifteh K, Ardekani BA, Branch CA, et al. Diffusion-tensor imaging implicates prefrontal axonal injury in executive function impairment following very mild traumatic brain injury. Radiology. 2009;252(3):816–24.doi:10.1148/radiol.2523081584.
   PubMed Web of Science ®Google Scholar
• Niogi S, Mukherjee P, Ghajar J, Johnson C, Kolster R, Sarkar R, Lee H, Meeker M, Zimmerman RD, Manley GT, et al. 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. Am J Neuroradiol. 2008;29(5):967–73.doi:10.3174/ajnr.A0970.
   PubMed Web of Science ®Google Scholar
• Sady MD, Vaughan CG, Gioia GA.Psychometric characteristics of the postconcussion symptom inventory in children and adolescents. Arch Clin Neuropsych. 2014;29(4):348–63. doi:10.1093/arclin/acu014.
   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;0:1-10.
   Web of Science ®Google Scholar
• Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage. 2006;31(4):1487–505.doi:10.1016/j.neuroimage.2006.02.024.
   PubMed Web of Science ®Google Scholar
• Smith SM.Fast robust automated brain extraction. Hum Brain Mapp. 2002;17(3):143–55. doi:10.1002/hbm.10062.
   PubMed Web of Science ®Google Scholar
• Andersson JL, Jenkinson M, Smith S. Non-linear optimisation. FMRIB technical report TR07JA1,2007, University of Oxford FMIRB Centre, Available from http://www.fmirb.ox.ac.uk/analysis/techrep/tr07ja1.pdf
   Google Scholar
• Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, et al. Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci U S A. 2009;106(31):13040–45.doi:10.1073/pnas.0905267106.
   PubMed Web of Science ®Google Scholar
• Sady MD, Vaughan CG, Gioia GA.Measuring dynamic symptom response in concussion: children’s exertional effects rating scale. J Head Trauma Rehabil. 2019;34(2):E35–E44. doi:10.1097/HTR.0000000000000424.
   PubMed Web of Science ®Google Scholar
• Ransom DM, Burns AR, Youngstrom EA, Vaughan CG, Sady MD, Gioia GA.Applying an evidence-based assessment model to identify students at risk for perceived academic problems following concussion. J Int NEUROPSYCH SOC. 2016;22(10):1038–49. doi:10.1017/S1355617716000916.
   PubMed Web of Science ®Google Scholar
• Kearney-Ramos TE, Fausett JS, Gess JL, Reno A, Peraza J, Kilts CD, James GA. Merging clinical neuropsychology and functional neuroimaging to evaluate the construct validity and neural network engagement of the n-back task. J Int NEUROPSYCH SOC. 2014;20(7):736–50.doi:10.1017/S135561771400054X.
   PubMed Web of Science ®Google Scholar
• McAllister TW, Sparling MB, Flashman LA, Guerin SJ, Mamourian AC, Saykin AJ.Differential working memory load effects after mild traumatic brain injury. Neuroimage. 2001;14(5):1004–12. doi:10.1006/nimg.2001.0899.
   PubMed Web of Science ®Google Scholar
• Mayer AR, Bellgowan PSF, Hanlon FM. Functional magnetic resonance imaging of mild traumatic brain injury. Neurosci Biobehav Rev. 2015;49:8–18. doi:10.1016/j.neubiorev.2014.11.016.
   PubMed Web of Science ®Google Scholar
• Dean PJ, Sato JR, Vieira G, McNamara A, Sterr A.Multimodal imaging of mild traumatic brain injury and persistent postconcussion syndrome. Brain Behav. 2015;5(1):e00292. doi:10.1002/brb3.292.
   Web of Science ®Google Scholar
• Hu Y, Chen X, Gu H, Yang Y.Resting-state glutamate and GABA concentrations predict task-induced deactivation in the default mode network. J Neurosci. 2013;33(47):18566–73. doi:10.1523/JNEUROSCI.1973-13.2013.
   PubMed Web of Science ®Google Scholar
• Cecil KM, Hills EC, Sandel ME, Smith DH, McIntosh TK, Mannon LJ, Sinson GP, Bagley LJ, Grossman RI, Lenkinski RE, et al. Proton magnetic resonance spectroscopy for detection of axonal injury in the splenium of the corpus callosum of brain-injured patients. J Neurosurg. 1998;88(5):795–801.doi:10.3171/jns.1998.88.5.0795.
   PubMed Web of Science ®Google Scholar
• Wu X, Kirov II, Gonen O, Ge Y, Grossman RI, Lui YW.MR imaging applications in mild traumatic brain injury: an imaging update. Radiology. 2016;279(3):693–707. doi:10.1148/radiol.16142535.
   PubMed Web of Science ®Google Scholar
• Gasparovic C, Yeo R, Mannell M, Ling J, Elgie R, Phillips J, Doezema D, Mayer AR. Neurometabolite concentrations in gray and white matter in mild traumatic brain injury: an 1H–magnetic resonance spectroscopy study. J Neurotrauma. 2009;26(10):1635–43.doi:10.1089/neu.2009.0896.
   PubMed Web of Science ®Google Scholar
• Kirov II, Whitlow CT, Zamora C.Susceptibility-weighted imaging and magnetic resonance spectroscopy in concussion. Neuroimaging Clin N Am. 2018;28(1):91–105. doi:10.1016/j.nic.2017.09.007.
   PubMed Web of Science ®Google Scholar
• Ozen LJ, Fernandes MA. Slowing down after a mild traumatic brain injury: a strategy to improve cognitive task performance? Arch Clin Neuropsych. 2012;27(1):85-100.doi:10.1093/arclin/acr087.
   Web of Science ®Google Scholar
• Cicerone KD.Attention deficits and dual task demands after mild traumatic brain injury. Brain Inj. 1996;10(2):79–90. doi:10.1080/026990596124566.
   PubMed Web of Science ®Google Scholar
• Ozen LJ, Itier RJ, Preston FF, Fernandes MA.Long-term working memory deficits after concussion: electrophysiological evidence. Brain Inj. 2013;27(11):1244–55. doi:10.3109/02699052.2013.804207.
   PubMed Web of Science ®Google Scholar
• Mayer AR, Mannell MV, Ling J, Gasparovic C, Yeo RA.Functional connectivity in mild traumatic brain injury. Hum Brain Mapp. 2011;32(11):1825–35. doi:10.1002/hbm.21151.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Milham MP, Lui YW, Miles L, Reaume J, Sodickson DK, Grossman RI, Ge Y. Default-mode network disruption in mild traumatic brain injury. Radiology. 2012;265(3):882–92.doi:10.1148/radiol.12120748.
   PubMed Web of Science ®Google Scholar
• van der Horn HJ, Liemburg EJ, Scheenen ME, de Koning ME, Spikman JM, van der Naalt J. Post-concussive complaints after mild traumatic brain injury associated with altered brain networks during working memory performance. Brain Imaging Behav. 2016;10(4):1243-1253.
   Web of Science ®Google Scholar
• Master CL, Gioia GA, Leddy JJ, Grady MF.Importance of ‘return-to-learn’ in pediatric and adolescent concussion. Pediatr Ann. 2012;41(9):1–6. doi:10.3928/00904481-20120827-09.
   Web of Science ®Google Scholar