Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-24T06:06:16.544Z Has data issue: false hasContentIssue false

Repeated Sport-Related Concussion Shows Only Minimal White Matter Differences Many Years After Playing High School Football

Published online by Cambridge University Press:  06 August 2019

Douglas P. Terry
Affiliation:
Department of Physical Medicine and Rehabilitation, Harvard Medical School, Boston, MA 02129, USA
Catherine M. Mewborn
Affiliation:
Department of Psychology, University of Georgia, Athens, GA 30602, USA
L. Stephen Miller*
Affiliation:
Department of Psychology, University of Georgia, Athens, GA 30602, USA
*
Correspondence and reprint requests to: L. Stephen Miller, 125 Baldwin Street, Psychology Bldg Rm 202, University of Georgia, Athens, GA 30602. E-mail: lsmiller@uga.edu

Abstract

Objective: Multiple concussions sustained in youth sport may be associated with later-life brain changes and worse cognitive outcomes. We examined the association between two or more concussions during high school football and later-life white matter (WM) microstructure (i.e., 22–47 years following football retirement) using diffusion tensor imaging (DTI). Method: Forty former high school football players aged 40–65 who received 2+ concussions during high school football (N = 20), or denied concussive events (N = 20) were recruited. Participants underwent neurocognitive testing and DTI scanning. Results: Groups did not statistically differ on age, education, or estimated pre-morbid intelligence. Tract-based Spatial Statistics (TBSS) correcting for Family-Wise Error (FWE)(p < .05) did not yield differences between groups at the whole-brain level. Region of interest analyses showed higher mean diffusivity (MD) in the anterior limb of the internal capsule (ALIC) in the concussed group compared to the non-concussed former players. More liberal analyses (i.e., p < .001, uncorrected for multiple comparisons, ≥8 voxels) also revealed that former players endorsing 2+ concussions had higher MD in the ALIC. Analyses that covaried for age did not reveal differences at either threshold. Concussive histories were not associated with worse cognitive functioning, nor did it impact the relationship between neuropsychological scores and DTI metrics. Discussion: Results suggest only minimal neuroanatomical brain differences in former athletes many years following original concussive injuries compared to controls.

Type
Regular Research
Copyright
Copyright © INS. Published by Cambridge University Press, 2019. 

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.)

References

REFERENCES

Alexander, A.L., Lee, J.E., Lazar, M., & Field, A.S. (2007). Diffusion tensor imaging of the brain. Neurotherapeutics, 4, 316329. doi:10.1016/j.nurt.2007.05.011 CrossRefGoogle Scholar
American Congress of Rehabilitation Medicine. (1993). Definition of mild traumatic brain injury. Journal of Head Trauma Rehabilitation, 8, 8687.CrossRefGoogle Scholar
Andersson, J.L.R., Jenkinson, M., & Smith, S. (2007a). Non-linear optimisation. FMRIB technical report TR07JA1, Retrieved from www.fmrib.ox.ac.uk/analysis/techrep Google Scholar
Andersson, J.L.R., Jenkinson, M., & Smith, S. (2007b). Non-linear registration, aka Spatial normalisation FMRIB technical report TR07JA2, Retrieved from www.fmrib.ox.ac.uk/analysis/techrep Google Scholar
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, 870876. doi:10.1136/jnnp-2012-302742 CrossRefGoogle ScholarPubMed
Arfanakis, K., Haughton, V.M., Carew, J.D., Rogers, B.P., Dempsey, R.J., & Meyerand, M.E. (2002). Diffusion tensor MR imaging in diffuse axonal injury. American Journal of Neuroradiology, 23, 794802.Google ScholarPubMed
Astafiev, S.V., Shulman, G.L., Metcalf, N.V., Rengachary, J., MacDonald, C.L., Harrington, D.L., Maruta, J., Shimony, J.S., Ghajar, J., Diwakar, M., Huang, M.X., Lee, R.R., & Corbetta, M. (2015). Abnormal white matter blood-oxygen-level-dependent signals in chronic mild traumatic brain injury. Journal of Neurotrauma, 32(16), 12541271. doi:10.1089/neu.2014.3547 CrossRefGoogle ScholarPubMed
Bazarian, J.J., Zhong, J., Blyth, B., Zhu, T., Kavcic, V., & Peterson, D. (2007). DTI detects clinically important axonal damage after mild TBI: a pilot study. Journal of Neurotrauma, 24, 14471459. doi:10.1089/neu.2007.0241 CrossRefGoogle ScholarPubMed
Bazarian, J.J., Zhu, T., Zhong, J., Janigro, D., Rozen, E., Roberts, A., Javien, H., Merchant-Borna, K., Abar, B., & Blackman, E.G. (2014). Persistent, long-term cerebral white matter changes after sports-related repetitive head impacts. PLOS ONE, 9, e94734. doi:10.1371/journal.pone.0094734 CrossRefGoogle ScholarPubMed
Beaulieu, C. & Allen, P.S., (1994). Determinants of anisotropic water diffusion in nerves. Magnetic Resonance in Medicine, 31, 394400. doi:10.1002/mrm.1910310408 CrossRefGoogle ScholarPubMed
Behrens, T.E., Woolrich, M.W., Jenkinson, M., Johansen-Berg, H., Nunes, R.G., Clare, S., Matthews, P.M., Brady, J.M., & Smith, S.M. (2003). Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magnetic Resonance in Medicine , 50, 1077–88. doi:10.1002/mrm.10609 CrossRefGoogle ScholarPubMed
Benson, R.R., Meda, S.A., Vasudevan, S., Kou, Z., Govindarajan, K.A., Hanks, R.A., Millis, S.R., Makki, M., Latif, Z., Coplin, W., Meythaler, J., & Haacke, E.M. (2007). Global white matter analysis of diffusion tensor images is predictive of injury severity in traumatic brain injury. Journal of Neurotrauma, 24, 446–459. doi:10.1089/neu.2006.0153 CrossRefGoogle ScholarPubMed
Bigler, E.D. (2013). Neuroimaging biomarkers of mild traumatic brain injury (mTBI). Neuropsychology Review, 23, 169209. doi:10.1007/s11065-013-9237-2 CrossRefGoogle Scholar
Broglio, S.P., Macciocchi, S.N., & Ferrara, M.S. (2007). Neurocognitive performance of concussed athletes when symptom free. Journal of Athletic Training, 42, 504–508.Google ScholarPubMed
Cassidy, J.D., Carroll, L.J., Peloso, P.M., Borg, J., von Holst, H., Holm, L., Kraus, J., Coronado, V.G., & WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. (2004). Incidence, risk factors and prevention of mild traumatic brain injury: results of the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. Journal of Rehabilitation Medicine, Supplement 43, 2860.CrossRefGoogle Scholar
Cubon, V.A. & Putukian, M. (2011). A diffusion tensor imaging study on the white matter skeleton in individuals with sports-related concussion. Journal of Neurotrauma, 28, 189201. doi:10.1089/neu.2010.1430 CrossRefGoogle Scholar
Davenport, E.M., Whitlow, C.T., Urban, J.E., Espeland, M.A., Jung, Y., Rosenbaum, D.A., Gioia, G.A., Powers, A.K., Stitzel, J.D., & Maldjian, J.A. (2014). Abnormal white matter integrity related to head impact exposure in a season of high school varsity football. Journal of Neurotrauma, 31, 16171624. doi:10.1089/neu.2013.3233 CrossRefGoogle Scholar
Dean, P.J., Sato, J.R., Vieira, G., McNamara, A., & Sterr, A. (2015). Long-term structural changes after mTBI and their relation to postconcussion symptoms. Brain Injury, 29(10), 12111218. doi:10.3109/02699052.2015.1035334 CrossRefGoogle Scholar
Dettwiler, A., Murugavel, M., Cubon, V., Putukian, M., Echemendia, R., Cabrera, J., & Osherson, D. (2014). A longitudinal diffusion tensor imaging study assessing white matter fiber tracts after sports related concussion. Journal of Neurotrauma, 31, 18601871. doi:10.1089/neu.2014.3368 CrossRefGoogle Scholar
Dykiert, D. & Deary, I.J. (2013). Retrospective validation of WTAR and NART scores as estimators of prior cognitive ability using the Lothian Birth Cohort 1936. Psychological Assessment, 25(4), 13611366. doi:10.1037/a0033623 CrossRefGoogle ScholarPubMed
Glenn, O.A., Henry, R.G., Berman, J.I., Chang, P.C., Miller, S.P., Vigneron, D.B., & Barkovich, A.J. (2003). DTI-based three-dimensional tractography detects differences in the pyramidal tracts of infants and children with congenital hemiparesis. Journal of Magnetic Resonance Imaging, 18(6), 641648. doi:10.1002/jmri.10420 CrossRefGoogle ScholarPubMed
Green, P. (2004). Medical Symptom Validity Test (MSVT) for Microsoft Windows: User’s manual. Edmonton: Paul Green Publishing.Google Scholar
Green, R.E., Melo, B., Christensen, B., Ngo, L.A., Monette, G., & Bradbury, C. (2008). Measuring premorbid IQ in traumatic brain injury: an examination of the validity of the Wechsler Test of Adult Reading (WTAR). Journal of Clinical and Experimental Neuropsychology, 30(2), 163172. doi:10.1080/13803390701300524 CrossRefGoogle Scholar
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: a cross-sectional study. JAMA Neurology, 70(3), 326335. doi:10.1001/2013.jamaneurol.340 CrossRefGoogle ScholarPubMed
Hayes, A.F. (2013). Methodology in the social sciences. Introduction to mediation, moderation, and conditional process analysis: A regression-based approach, New York, NY: The Guilford Press.Google Scholar
Howe, L.L., Anderson, A.M., Kaufman, D.A., Sachs, B.C., & Loring, D.W. (2007). Characterization of the Medical Symptom Validity Test in evaluation of clinically referred memory disorders clinic patients. Archives of Clinical Neuropsychology, 22, 753–61. doi: 10.1016/j.acn.2007.06.003 CrossRefGoogle ScholarPubMed
Hughes, D.G., Jackson, A., Mason, D.L., Berry, E., Hollis, S., & Yates, D.W. (2004). Abnormalities on magnetic resonance imaging seen acutely following mild traumatic brain injury: correlation with neuropsychological tests and delayed recovery. Neuroradiology, 46(7), 550558. doi:10.1007/s00234-004-1227-x CrossRefGoogle ScholarPubMed
Inglese, M., Makani, S., Johnson, G., Cohen, B.A., Silver, J.A., Gonen, O., & Grossman, R.I. (2005). Diffuse axonal injury in mildtraumatic brain injury: a diffusion tensor imaging study. Journal of Neurosurgery, 103(2), 298303. 10.3171/jns.2005.103.2.0298 CrossRefGoogle Scholar
Iverson, G.L., Lovell, M.R., Smith, S., & Franzen, M.D. (2000). Prevalence of abnormal CT – scans following mild head injury. Brain Injury, 14(12), 10571061. doi:10.1080/02699050050203559 Google ScholarPubMed
Jones, D.K., Catani, M., Pierpaoli, C., Reeves, S.J., Shergill, S.S., & O’sullivan, M. (2006). Age effects on diffusion tensor magnetic resonance imaging tractography measures of frontal cortex connections in schizophrenia. Human Brain Mapping, 27, 230238. doi:10.1002/hbm.20179 CrossRefGoogle Scholar
Kou, Z., Wu, Z., Tong, K.A., Holshouser, B., Benson, R.R., Hu, J., & Haacke, E.M. (2010). The role of advanced MR imaging findings as biomarkers of TBI. The Journal of Head Trauma Rehabilitation, 25(4), 267282. doi:10.1097/HTR.0b013e3181e54793 CrossRefGoogle Scholar
Kumar, R., Gupta, R.K., Husain, M., Chaudhry, C., Srivastava, A., Saksena, S., & Rathore, R.K. (2009). Comparative evaluation of corpus callosum DTI metrics in acute mild and moderate traumatic brain injury: its correlation with neuropsychometric tests. Brain Injury, 23(7), 675685. doi:10.1080/02699050903014915 CrossRefGoogle ScholarPubMed
Lange, R.T., Iverson, G.L., Brubacher, J.R., Madler, B., & Heran, M.K. (2012). Diffusion tensor imaging findings are not strongly associated with postconcussional disorder 2 months following mild traumatic brain injury. Journal of Head Trauma Rehabilitation, 27, 188198. doi:10.1097/HTR.0b013e318217f0ad CrossRefGoogle Scholar
Lipton, M.L., Gellella, E., Lo, C., Gold, T., Ardekani, B.A., Shifteh, K., Bello, J.A., & Branch, C.A. (2008). Multifocal white matter ultrastructural abnormalities in mild traumatic brain injury with cognitive disability: a voxel-wise analysis of diffusion tensor imaging. Journal of Neurotrauma, 25, 13351342. doi:10.1089/neu.2008.0547 CrossRefGoogle ScholarPubMed
Lipton, M.L., Gulko, E., Zimmerman, M.E., Friedman, B.W., Kim, M., Gellella, E., Gold, T., Shifteh, K., Ardekani, B.A., & Branch, C.A. (2009). Diffusion-tensor imaging implicates prefrontal axonal injury in executive function impairment following very mild traumatic brain injury. Radiology, 252(3), 816824. doi:10.1148/radiol.2523081584 CrossRefGoogle ScholarPubMed
Lipton, M.L., Kim, N., Park, Y.K., Hulkower, M.B., Gardin, T.M., Shifteh, K., … 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/s11682-012-9175-2 CrossRefGoogle ScholarPubMed
List, J., Ott, S., Bukowski, M., Lindenberg, R., & Flöel, A. (2015). Cognitive function and brain structure after recurrent mild traumatic brain injuries in young-to-middle-aged adults. Frontiers in Human Neuroscience, 9, 228. doi:10.3389/fnhum.2015.00228 CrossRefGoogle 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), 293297. doi:10.1097/RCT.0b013e31817579d1 CrossRefGoogle ScholarPubMed
Maruta, J., Palacios, E.M., Zimmerman, R.D., Ghajar, J., & Mukherjee, P. (2016). Chronic post-concussion neurocognitive deficits. I. Relationship with white matter integrity. Frontiers in Human Neuroscience, 10, 35. doi:10.3389/fnhum.2016.00035 Google ScholarPubMed
McAllister, T.W., Ford, J.C., Flashman, L.A., Maerlender, A., Greenwald, R.M., Beckwith, J.G., Bolander, R.P., Tosteson, T.D., Turco, J.H., Raman, R., & Jain, S. (2014). Effects of head impact measures in a cohort of collegiate contact sport athletes. Neurology, 82, 6369. doi:10.1212/01.wnl.0000438220.16190.42 CrossRefGoogle Scholar
McKay, C., Wertheimer, J.C., Fichtenberg, N.L., & Casey, J.E. (2008). The repeatable battery for the assessment of neuropsychological status (RBANS): clinical utility in a traumatic brain injury sample. The Clinical Neuropsychologist, 22, 228241. doi:10.1080/13854040701260370 CrossRefGoogle Scholar
Miles, L., Grossman, R. I., Johnson, G., Babb, J.S., Diller, L., &Inglese, M. (2008). Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injury. Brain Injury, 22(2), 115122. doi:10.1080/02699050801888816 CrossRefGoogle ScholarPubMed
Mori, S., Oishi, K., Jiang, H., Jiang, L., Li, X., Akhter, K., Hua, K., Faria, A.V., Mahmood, A., Woods, R., Toga, A.W., Pike, G.B., Neto, P.R., Evans, A., Zhang, J., Huang, H., Miller, M.I., van Zijl, P., & Mazziotta, J. (2008). Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. NeuroImage, 40, 570582. doi:10.1016/j.neuroimage.2007.12.035 CrossRefGoogle Scholar
Neil, J., Miller, J., Mukherjee, P., & Huppi, P.S. (2002). Diffusion tensor imaging of normal and injured developing human brain: A technical review. NMR in Biomedicine, 15, 543552. doi:10.1002/nbm.784 CrossRefGoogle ScholarPubMed
Niogi, S.N., Mukherjee, P., Ghajar, J., Johnson, C., Kolster, R.A., Sarkar, R., Lee, H., Meeker, M., Zimmerman, R.D., Manley, G.T., & McCandliss, B.D. (2008). 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. American Journal of Neuroradiology, 29(5), 967973. doi:10.3174/ajnr.A0970 CrossRefGoogle ScholarPubMed
Niogi, S.N., Mukherjee, P., Ghajar, J., Johnson, C.E., Kolster, R., Lee, H., Suh, M., Zimmerman, R.D., Manley, G.T., & McCandliss, B.D. (2008). Structural dissociation of attentional control and memory in adults with and without mild traumatic brain injury. Brain, 131(12), 32093221. doi:10.1093/brain/awn247 CrossRefGoogle ScholarPubMed
Psychological Corporation. (2001). Wechsler Test of Adult Reading. San Antonio, TX: The Psychological Corporation.Google Scholar
Randolph, C, Tierney, M, Mohr, E, & Chase, T. (1998). The Repeatable Battery for the Assessment of Neuropsychological Status (RBANS): preliminary clinical validity. Journal of Clinical and Experimental Neuropsychology, 20, 310319. doi:10.1076/jcen.20.3.310.823 CrossRefGoogle ScholarPubMed
Rueckert, D., Sonoda, L.I., Hayes, C., Hill, D.L.G., Leach, M.O., & Hawkes, D.J. (1999) Non-rigid registration using free-form deformations: Application to breast MR images. IEEE Transactions on Medical Imaging, 18(8), 712721.CrossRefGoogle Scholar
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 diffusiontensor imaging findings in mild traumatic brain injury. Brain Imaging Behavior, 6, 137192. doi:10.1007/s11682-012-9156-5 CrossRefGoogle Scholar
Smith, S.M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T.E., Mackay, C.E., Watkins, K.E., Ciccarelli, O., Cader, M.Z., Matthews, P.M., & Behrens, T.E.J. (2006). Tract-based spatial statistics: Voxelwise analysis of multi- subject diffusion data. NeuroImage, 31, 14871505. doi:10.1016/j.neuroimage.2006.02.024 CrossRefGoogle ScholarPubMed
Smith, S.M., Jenkinson, M., Woolrich, M.W., Beckmann, C.F., Behrens, T.E.J., Johansen-Berg, H., Bannister, P.R., De Luca, M., Drobnjak, I., Flitney, D.E., Niazy, R.K.., Saunders, J., Vickers, J., Zhang, Y., De Stefano, N., Brady, J.M., & Matthews, P.M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23(S1), 208219. doi:10.1016/j.neuroimage.2004.07.051 CrossRefGoogle ScholarPubMed
Smith, S.M. & Nichols, T.E. (2009). Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage, 44, 8398. doi:10.1016/j.neuroimage.2008.03.061 CrossRefGoogle ScholarPubMed
Song, S.K., Sun, S.W., Ju, W.K., Lin, S.J., Cross, A.H., & Neufeld, A.H. (2003). Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage, 20, 17141722. doi:10.1016/j.neuroimage.2003.07.005 CrossRefGoogle ScholarPubMed
Song, S.K., Sun, S.W., Ramsbottom, M.J., Chang, C., Russell, J., & Cross, A.H. (2002). Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage, 17, 14291436. doi:10.1006/nimg.2002.1267 CrossRefGoogle Scholar
Song, S.K., Yoshino, J., Le, T.Q., Lin, S.J., Sun, S.W., Cross, A.H., & Armstrong, R.C. (2005). Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage, 26, 132140. doi:10.1016/j.neuroimage.2005.01.028 CrossRefGoogle ScholarPubMed
Strain, J., Didehbani, N., Cullum, C.M., Mansinghani, S., Conover, H., Kraut, M. A., Hart, J. Jr, & Womack, K.B. (2013). Depressive symptoms and white matter dysfunction in retired NFL players with concussion history. Neurology, 81(1), 2532. doi:10.1212/WNL.0b013e318299ccf8 CrossRefGoogle ScholarPubMed
Terry, D.P., Adams, T.E., Ferrara, M.S., & Miller, L.S. (2015). FMRI hypoactivation during verbal learning and memory in former high school football players with multiple concussions. Archives of Clinical Neuropsychology, 30, 341355. doi:10.1093/arclin/acv020 CrossRefGoogle 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(Pt 11), 29973011. doi:10.1093/brain/awu236 CrossRefGoogle ScholarPubMed
Vos, S.B., Jones, D.K., Jeurissen, B., Viergever, M.A., &Leemans, A. (2012). The influence of complex white matter architecture on the mean diffusivity in diffusion tensor MRI of the human brain. Neuroimage, 59, 22082216. doi:10.1016/j.neuroimage.2011.09.086 CrossRefGoogle ScholarPubMed
Wada, T., Asano, Y., & Shinoda, J. (2012). Decreased fractional anisotropy evaluated using tract-based spatial statistics and correlated with cognitive dysfunction in patients with mild traumatic brain injury in the chronic stage. American Journal of Neuroradiology, 33, 21172122. doi:10.3174/ajnr.A3141 CrossRefGoogle ScholarPubMed
Weinberger, D.R. & Radulescu, E. (2015). Finding the elusive psychiatric “Lesion” with 21st centure neuroanatomy: A note of caution. The American Journal of Psychiatry, 173, 2733. doi:10.1176/appi.ajp.2015.15060753 CrossRefGoogle Scholar
Winkler, A.M., Ridgway, G.R., Webster, M.A., Smith, S.M., & Nichols, T.E. (2014). Permutation inference for the general linear model. Neuroimage, 92, 381397 (2014). doi:10.1016/j.neuroimage.2014.01.060 CrossRefGoogle 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, 5770. doi:10.1007/s00221-010-2294-3 CrossRefGoogle ScholarPubMed
Zuckerman, S.L., Apple, R.P., Odom, M.J., Lee, Y.M., Solomon, G.S., & Sills, A.K. (2014). Effect of sex on symptoms and return to baseline in sport-related concussion. Journal of Neurosurgery, Pediatrics, 13, 7281. doi:10.3171/2013.9.PEDS13257 CrossRefGoogle ScholarPubMed