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Longitudinal Changes in Resting State Connectivity and White Matter Integrity in Adolescents With Sports-Related Concussion

  • Donna L. Murdaugh (a1), Tricia Z. King (a2), Binjian Sun (a3), Richard A. Jones (a3), Kim E. Ono (a4), Andrew Reisner (a5) and Thomas G. Burns (a4)...
  • Please note a correction has been issued for this article.

Abstract

Objectives: The aim of this study was to investigate alterations in functional connectivity, white matter integrity, and cognitive abilities due to sports-related concussion (SRC) in adolescents using a prospective longitudinal design. Methods: We assessed male high school football players (ages 14–18) with (n=16) and without (n=12) SRC using complementary resting state functional MRI (rs-fMRI) and diffusion tensor imaging (DTI) along with cognitive performance using the Immediate Post-Concussive Assessment and Cognitive Testing (ImPACT). We assessed both changes at the acute phase (<7 days post-SRC) and at 21 days later, as well as, differences between athletes with SRC and age- and team-matched control athletes. Results: The results revealed rs-fMRI hyperconnectivity within posterior brain regions (e.g., precuneus and cerebellum), and hypoconnectivity in more anterior areas (e.g., inferior and middle frontal gyri) when comparing SRC group to control group acutely. Performance on the ImPACT (visual/verbal memory composites) was correlated with resting state network connectivity at both time points. DTI results revealed altered diffusion in the SRC group along a segment of the corticospinal tract and the superior longitudinal fasciculus in the acute phase of SRC. No differences between the SRC group and control group were seen at follow-up imaging. Conclusions: Acute effects of SRC are associated with both hyperconnectivity and hypoconnectivity, with disruption of white matter integrity. In addition, acute memory performance was most sensitive to these changes. After 21 days, adolescents with SRC returned to baseline performance, although chronic hyperconnectivity of these regions could place these adolescents at greater risk for secondary neuropathological changes, necessitating future follow-up. (JINS, 2018, 24, 781–792)

Copyright

Corresponding author

Correspondence and reprint requests to: Donna L. Murdaugh, 1600 7th Avenue S, Lowder 500, Birmingham, AL 35233. E-mail: dlmurdaugh@gmail.com

References

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Abbas, K., Shenk, T.E., Poole, V.N., Breedlove, E.L., Leverenz, L.J., Nauman, E.A., & Robinson, M.E. (2015). Alteration of default mode network in high school football athletes due to repetitive subconcussive mild traumatic brain injury: A resting-state functional magnetic resonance imaging study. Brain Connectivity, 5(2), 91101.
Broyd, S.J., Demanuele, C., Debener, S., Helps, S.K., James, C.J., & Sonuga-Barke, E.J. (2009). Default-mode brain dysfunction in mental disorders: A systematic review. Neuroscience & Biobehavioral Reviews, 33(3), 279296.
Bryan, M.A., Rowhani-Rahbar, A., Comstock, R.D., & Rivara, F. (2016). Sports-and recreation-related concussions in US youth. Pediatrics, 138(1), e20154635.
Buckner, R.L., & Carroll, D.C. (2007). Self-projection and the brain. Trends in Cognitive Sciences, 11(2), 4957.
Calhoun, V.D., Adali, T., Pearlson, G.D., & Pekar, J.J. (2001). Spatial and temporal independent component analysis of functional MRI data containing a pair of task‐related waveforms. Human Brain Mapping, 13(1), 4353.
Calhoun, V.D., Kiehl, K.A., & Pearlson, G.D. (2008). Modulation of temporally coherent brain networks estimated using ICA at rest and during cognitive tasks. Human Brain Mapping, 29(7), 828838.
Centers for Disease Control and Prevention. (2011). Nonfatal traumatic brain injuries related to sports and recreation activities among persons aged≤19 years---United States, 2001--2009. MMWR: Morbidity and Mortality Weekly Report, 60(39), 13371342.
Churchill, N.W., Caverzasi, E., Graham, S.J., Hutchison, M.G., & Schweizer, T.A. (2017). White matter microstructure in athletes with a history of concussion: Comparing diffusion tensor imaging (DTI) and neurite orientation dispersion and density imaging (NODDI). Human Brain Mapping, 38, 42014211.
Churchill, N., Hutchison, M.G., Leung, G., Graham, S., & Schweizer, T.A. (2017). Changes in functional connectivity of the brain associated with a history of sport concussion: A preliminary investigation. Brain Injury, 31(1), 3948.
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), 189201.
Czerniak, S.M., Sikoglu, E.M., Navarro, A.A.L., McCafferty, J., Eisenstock, J., Stevenson, J.H., & Moore, C.M. (2015). A resting state functional magnetic resonance imaging study of concussion in collegiate athletes. Brain Imaging and Behavior, 9(2), 323332.
Dettwiler, A., Murugavel, M., Putukian, M., Cubon, V., Furtado, J., & Osherson, D. (2014). Persistent differences in patterns of brain activation after sports-related concussion: A longitudinal functional magnetic resonance imaging study. Journal of Neurotrauma, 31(2), 180188.
Fox, M.D., Snyder, A.Z., Vincent, J.L., Corbetta, M., Van Essen, D.C., & Raichle, M.E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences of the United States of America, 102(27), 96739678.
Fransson, P., & Marrelec, G. (2008). The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: Evidence from a partial correlation network analysis. NeuroImage, 42(3), 11781184.
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), 25212538.
Gessel, L.M., Fields, S.K., Collins, C.L., Dick, R.W., & Comstock, R.D. (2007). Concussions among United States high school and collegiate athletes. Journal of Athletic Training, 42(4), 495.
Greicius, M.D., Krasnow, B., Reiss, A.L., & Menon, V. (2003). Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences of the United States of America, 100(1), 253258.
Griffanti, L., Douaud, G., Bijsterbosch, J., Evangelisti, S., Alfaro-Almagro, F., Glasser, M.F., & Beckmann, C.F. (2017). Hand classification of fMRI ICA noise components. NeuroImage, 154, 188205.
Guskiewicz, K.M., Weaver, N.L., Padua, D.A., & Garrett, W.E. (2000). Epidemiology of concussion in collegiate and high school football players. The American Journal of Sports Medicine, 28(5), 643650.
Guskiewicz, K.M., Ross, S.E., & Marshall, S.W. (2001). Postural stability and neuropsychological deficits after concussion in collegiate athletes. Journal of Athletic Training, 36(3), 263.
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), 25492555.
Guskiewicz, K.M., Marshall, S.W., Bailes, J., McCrea, M., Cantu, R.C., Randolph, C., &Jordan, B.D. (2005). Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery, 57(4), 719726.
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), 20492059.
Hillary, F.G., & Grafman, J.H. (2017). Injured brains and adaptive networks: The benefits and costs of hyperconnectivity. Trends in Cognitive Sciences, 21(5), 385401.
Iraji, A., Benson, R.R., Welch, R.D., O’Neil, B.J., Woodard, J.L., Ayaz, S.I., & Liu, T. (2015). Resting state functional connectivity in mild traumatic brain injury at the acute stage: Independent component and seed-based analyses. Journal of Neurotrauma, 32(14), 10311045.
Jantzen, K.J., Anderson, B., Steinberg, F.L., & Kelso, J.S. (2004). A prospective functional MR imaging study of mild traumatic brain injury in college football players. AJNR American Journal of Neuroradiology, 25(5), 738745.
Johnson, B., Zhang, K., Gay, M., Horovitz, S., Hallett, M., Sebastianelli, W., &Slobounov, S. (2012). Alteration of brain default network in subacute phase of injury in concussed individuals: Resting-state fMRI study. NeuroImage, 59(1), 511518.
Kamins, J., Bigler, E., Covassin, T., Henry, L., Kemp, S., Leddy, J.J., & McLeod, T.C.V. (2017). What is the physiological time to recovery after concussion? A systematic review. British Journal of Sports Medicine, 51(12), 935940.
Keightley, M.L., Singh Saluja, R., Chen, J.K., Gagnon, I., Leonard, G., Petrides, M., &Ptito, A. (2014). A functional magnetic resonance imaging study of working memory in youth after sports-related concussion: Is it still working? Journal of Neurotrauma, 31(5), 437451.
Koziol, L.F., Budding, D.E., & Chidekel, D. (2012). From movement to thought: Executive function, embodied cognition, and the cerebellum. The Cerebellum, 11(2), 505525.
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.
Lau, B.C., Collins, M.W., & Lovell, M.R. (2011). Cutoff scores in neurocognitive testing and symptom clusters that predict protracted recovery from concussions in high school athletes. Neurosurgery, 70(2), 371379.
Li, Y.O., Adalı, T., & Calhoun, V.D. (2007). Estimating the number of independent components for functional magnetic resonance imaging data. Human Brain Mapping, 28(11), 12511266.
Lovell, M. (2015). ImPACT: An evidence-based and comprehensive concussion management program. ImPACT Research Report, 3, 12.
Manto, M., Bower, J.M., Conforto, A.B., Delgado-García, J.M., da Guarda, S.N.F., Gerwig, M., & Molinari, M. (2012). Consensus paper: Roles of the cerebellum in motor control—the diversity of ideas on cerebellar involvement in movement. The Cerebellum, 11(2), 457487.
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), 2837.
Mayer, A.R., Mannell, M.V., Ling, J., Gasparovic, C., & Yeo, R.A. (2011). Functional connectivity in mild traumatic brain injury. Human Brain Mapping, 32(11), 18251835.
McCrea, M., Guskiewicz, K.M., Marshall, S.W., Barr, W., Randolph, C., Cantu, R.C., & Kelly, J.P. (2003). Acute effects and recovery time following concussion in collegiate football players: The NCAA Concussion Study. JAMA, 290(19), 25562563.
McCrory, P., Meeuwisse, W., Aubry, M., Cantu, B., Dvorak, J., Echemendia, R., & Sills, A. (2013). Consensus statement on concussion in sport—the 4th International Conference on Concussion in Sport held in Zurich, November 2012. Journal of Science and Medicine in Sport, 16(3), 178189.
Meier, T.B., Bellgowan, P.S., & Mayer, A.R. (2017). Longitudinal assessment of local and global functional connectivity following sports-related concussion. Brain Imaging and Behavior, 11(1), 129140.
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), 18601871.
Oouchi, H., Yamada, K., Sakai, K., Kizu, O., Kubota, T., Ito, H., &Nishimura, T. (2007). Diffusion anisotropy measurement of brain white matter is affected by voxel size: Underestimation occurs in areas with crossing fibers. AJNR American Journal of Neuroradiology, 28(6), 11021106.
Orr, C.A., Albaugh, M.D., Watts, R., Garavan, H., Andrews, T., Nickerson, J.P., & Hudziak, J.J. (2016). Neuroimaging biomarkers of a history of concussion observed in asymptomatic young athletes. Journal of Neurotrauma, 33(9), 803810.
Pruim, R.H., Mennes, M., Buitelaar, J.K., & Beckmann, C.F. (2015). Evaluation of ICA-AROMA and alternative strategies for motion artifact removal in resting state fMRI. NeuroImage, 112, 278287.
Raichle, M.E., & Snyder, A.Z. (2007). A default mode of brain function: A brief history of an evolving idea. NeuroImage, 37(4), 10831090.
Raichle, M.E., MacLeod, A.M., Snyder, A.Z., Powers, W.J., Gusnard, D.A., & Shulman, G.L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98(2), 676682.
Smith, E.E., & Jonides, J. (1998). Neuroimaging analyses of human working memory. Proceedings of the National Academy of Sciences of the United States of America, 95(20), 1206112068.
Stevens, M.C., Lovejoy, D., Kim, J., Oakes, H., Kureshi, I., & Witt, S.T. (2012). Multiple resting state network functional connectivity abnormalities in mild traumatic brain injury. Brain Imaging and Behavior, 6, 293318.
Toledo, E., Lebel, A., Becerra, L., Minster, A., Linnman, C., Maleki, N., & Borsook, D. (2012). The young brain and concussion: Imaging as a biomarker for diagnosis and prognosis. Neuroscience & Biobehavioral Reviews, 36(6), 15101531.
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), 2429.
Virji-Babul, N., Hilderman, C. G., Makan, N., Liu, A., Smith-Forrester, J., Franks, C., & Wang, Z. J. (2014). Changes in functional brain networks following sports-related concussion in adolescents. Journal of neurotrauma, 31(23), 1914–1919.
Yeh, F.C., Wedeen, V.J., & Tseng, W.Y.I. (2010). Generalized q-sampling imaging. IEEE Transactions on Medical Imaging, 29(9), 16261635.
Yeh, F.C., Tang, P.F., & Tseng, W.Y.I. (2013). Diffusion MRI connectometry automatically reveals affected fiber pathways in individuals with chronic stroke. Neuroimage: Clinical, 2, 912921.
Yeh, F.C., Verstynen, T.D., Wang, Y., Fernández-Miranda, J.C., & Tseng, W.Y.I. (2013). Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS One, 8(11), e80713.
Yeh, F.C., Badre, D., & Verstynen, T. (2016). Connectometry: A statistical approach harnessing the analytical potential of the local connectome. NeuroImage, 125, 162171.
Yuh, E.L., Hawryluk, G.W., & Manley, G.T. (2014). Imaging concussion: A review. Neurosurgery, 75(Suppl 4), S50S63.
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), 5770.

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