Structural and functional connectivity (FC) after sports-related concussion (SRC) may remain altered in adolescent athletes despite symptom resolution. Little is known, however, about how alterations in structural connectivity and FC co-present in female athletes whose symptom recovery tends to be prolonged. Despite resolution of symptoms, one month after her second SRC, an 18-year-old female athlete had decreased structural connectivity in the corpus callosum and cingulum, with altered FC near those regions, compared with other SRC and orthopedically injured athletes. Findings show persistent effects of SRC on advanced brain imaging and the possibility of greater vulnerability of white matter tracts in females.
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References
1.
NewsomeM.R., LiX., LinX., WildeE.A., OttS., BiekmanB., HunterJ.V., DashP.K., TaylorB.A., and LevinH.S. (2016). Functional connectivity is altered in concussed adolescent athletes despite medical clearance to return to play: a preliminary report. Front. Neurol. 7, 116.
2.
DennisE.L., EllisM.U., MarionS.D., JinY., MoranL., OlsenA., KernanC., BabikianT., MinkR., BabbittC., JohnsonJ., GizaC.C., ThompsonP.M., and AsarnowR.F. (2015). Callosal function in pediatric traumatic brain injury linked to disrupted white matter integrity. J. Neurosci. 35, 10202–10211.
3.
ChurchillN.W., HutchisonM.G., RichardsD., LeungG., GrahamS.J., and SchweizerT.A. (2017). Neuroimaging of sport concussion: persistent alterations in brain structure and function at medical clearance. Sci. Rep. 7, 8297.
4.
MeierT.B., BergaminoM., BellgowanP.S., TeagueT.K., LingJ.M., JerominA., and MayerA.R. (2016). Longitudinal assessment of white matter abnormalities following sports-related concussion. Hum. Brain Mapp. 37, 833–845.
5.
KoerteI.K., NicholsE., TripodisY., SchultzV., LehnerS., IgbinobaR., ChuangA.Z., MayingerM., KlierE.M., MuehlmannM., KaufmannD., LepageC., HeinenF., Schulte-KorneG., ZafonteR., ShentonM.E., and SerenoA.B. (2017). Impaired cognitive performance in youth athletes exposed to repetitive head impacts. J. Neurotrauma, 34, 2389–2395.
6.
MeierT.B., LancasterM.A., MayerA.R., TeagueT.K., and SavitzJ. (2017). Abnormalities in functional connectivity in collegiate football athletes with and without a concussion history: implications and role of euroactive kynurenine pathway metabolites. J. Neurotrauma, 34, 824–837.
7.
CovassinT., MoranR., and ElbinR.J. (2016). Sex differences in reported concussion injury rates and time loss from participation: an update of the National Collegiate Athletic Association Injury Surveillance Program from 2004–2005 through 2008–2009. J. Athl. Train. 51, 189–194.
8.
BryanM.A., Rowhani-RahbarA., ComstockR.D., RivaraF., and Seattle Sports Concussion ResearchCollaborative. (2016). Sports- and recreation-related concussions in US youth. Pediatrics 138, pii:. e20154635.
9.
DolleJ.P., JayeA., AndersonS.A., AhmadzadehH., ShenoyV.B., and SmithD.H. (2018). Newfound sex differences in axonal structure underlie differential outcomes from in vitro traumatic axonal injury. Exp. Neurol. 300, 121–134.
10.
McCroryP., MeeuwisseW., DvorakJ., AubryM., BailesJ., BroglioS., CantuR.C., CassidyD., EchemendiaR.J., CastellaniR.J., DavisG.A., EllenbogenR., EmeryC., EngebretsenL., Feddermann-DemontN., GizaC.C., GuskiewiczK.M., HerringS., IversonG.L., JohnstonK.M., KissickJ., KutcherJ., LeddyJ.J., MaddocksD., MakdissiM., ManleyG.T., McCreaM., MeehanW.P., NagahiroS., PatriciosJ., PutukianM., SchneiderK.J., SillsA., TatorC.H., TurnerM., and VosP.E. (2017). Consensus statement on concussion in sport—the 5th international conference on concussion in sport held in Berlin, October 2016. Br. J. Sports Med. 51, 838–847.
11.
McCroryP., Feddermann-DemontN., DvorakJ., CassidyJ.D., McIntoshA., VosP.E., EchemendiaR.J., MeeuwisseW., and TarnutzerA.A. (2017). What is the definition of sports-related concussion: a systematic review. Br. J. Sports Med. 51, 877–887.
12.
WildeE.A., LiX., HunterJ.V., NarayanaP.A., HasanK., BiekmanB., SwankP., RobertsonC., MillerE., McCauleyS.R., ChuZ.D., FaberJ., McCarthyJ., and LevinH.S. (2016). Loss of consciousness is related to white matter injury in mild traumatic brain injury. J. Neurotrauma, 33, 2000–2010.
13.
GardnerA., Kay-LambkinF., StanwellP., DonnellyJ., WilliamsW.H., HilesA., SchofieldP., LeviC., and JonesD.K. (2012). A systematic review of diffusion tensor imaging findings in sports-related concussion. J. Neurotrauma, 29, 2521–2538.
14.
ChamardE., LefebvreG., LassondeM., and TheoretH. (2016). Long-term abnormalities in the corpus callosum of female concussed athletes. J. Neurotrauma, 33, 1220–1226.
15.
ChamardE., LassondeM., HenryL., TremblayJ., BoulangerY., De BeaumontL., and TheoretH. (2013). Neurometabolic and microstructural alterations following a sports-related concussion in female athletes. Brain Inj. 27, 1038–1046.
16.
WildeE.A., ChuZ., BiglerE.D., HunterJ.V., FearingM.A., HantenG., NewsomeM.R., ScheibelR.S., LiX., and LevinH.S. (2006). Diffusion tensor imaging in the corpus callosum in children after moderate to severe traumatic brain injury. J. Neurotrauma, 23, 1412–1426.
17.
MoriS., CrainB.J., ChackoV.P., and van ZijlP.C. (1999). Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann. Neurol. 45, 265–269.
18.
ShroutP.E. and FleissJ.L. (1979). Intraclass correlations: uses in assessing rater reliability. Psychol. Bull. 86, 420–428.
19.
Whitfield-GabrieliS. and Nieto-CastanonA. (2012). Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2, 125–141.
20.
EklundA., NicholsT.E., and KnutssonH. (2016). Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proc. Natl. Acad. Sci. U.S.A. 113, 7900–7905.
21.
SchmithorstV.J. and YuanW. (2010). White matter development during adolescence as shown by diffusion MRI. Brain, Cogn.72, 16–25.
22.
NewsomeM.R., ScheibelR.S., ChuZ., HunterJ.V., LiX., WildeE.A., LuH., WangZ.J., LinX., SteinbergJ.L., VasquezA.C., CookL., and LevinH.S. (2012). The relationship of resting cerebral blood flow and brain activation during a social cognition task in adolescents with chronic moderate to severe traumatic brain injury: a preliminary investigation. Int. J. Dev. Neurosci. 30, 255–266.
23.
TalavageT.M., NaumanE.A., BreedloveE.L., YorukU., DyeA.E., MorigakiK.E., FeuerH., and LeverenzL.J. (2014). Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion. J. Neurotrauma, 31, 327–338.
24.
BazarianJ.J., ZhuT., BlythB., BorrinoA., and ZhongJ. (2012). Subject-specific changes in brain white matter on diffusion tensor imaging after sports-related concussion. Magn. Reson. Imaging, 30, 171–180.
25.
SlobounovS. (2014). Metabolic integrity of primary motor cortex may be compromised in clinically asymptomatic concussed athletes. Clin. Neurophysiol. 125, 1291–1292.
26.
SlobounovS.M., WalterA., BreiterH.C., ZhuD.C., BaiX., BreamT., SeidenbergP., MaoX., JohnsonB., and TalavageT.M. (2017). The effect of repetitive subconcussive collisions on brain integrity in collegiate football players over a single football season: a multi-modal neuroimaging study. Neuroimage Clin. 14, 708–718.
27.
LancasterM.A., MeierT.B., OlsonD.V., McCreaM.A., NelsonL.D., and MuftulerL.T. (2018). Chronic differences in white matter integrity following sport-related concussion as measured by diffusion MRI: 6-month follow-up. Hum. Brain Mapp. 39,4276-–4289.
28.
GieddJ.N., BlumenthalJ., JeffriesN.O., CastellanosF.X., LiuH., ZijdenbosA., PausT., EvansA.C., and RapoportJ.L. (1999). Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 2, 861–863.
29.
HenryL.C., TremblayS., and De BeaumontL. (2017). Long-term effects of sports concussions: bridging the neurocognitive repercussions of the injury with the newest neuroimaging data. Neuroscientist, 23, 567–578.
