Eye movement performance and clinical outcomes among female athletes post-concussion

References

• Zuckerman SL, Kerr ZY, Yengo-Kahn A, Wasserman E, Covassin T, Solomon GS. Epidemiology of sports-related concussion in NCAA athletes from 2009-2010 to 2013-2014: incidence, recurrence, and mechanisms. Am J Sports Med. 2015;43:2654–62.
   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;51:838–47.
   PubMed Web of Science ®Google Scholar
• National Collegiate Athletic Association (NCAA). Sport sponsorship, participation and demographics search [2012-2013]. [accessed 2017 Nov 1]. http://web1.ncaa.org/rgdSearch/exec/main.
   Google Scholar
• Pennington B. Rise of college club teams creates a whole new level of success. New York Times. 2008 Dec 1. [accessed 2017 May 29]. https://www.nytimes.com/2008/12/02/sports/02club.html.
   Google Scholar
• Kerr ZY, Roos KG, Djoko A, Dalton SL, Broglio SP, Marshall SW, Dompier TP. Epidemiologic measures for quantifying the incidence of concussion in national collegiate athletic association sports. J Athl Train. 2017;52:167–74. doi:10.4085/1062-6050-51.6.05.
   PubMed Web of Science ®Google Scholar
• Putukian M, Echemendia R, Dettwiler-Danspeckgruber A, Duliba T, Bruce J, Furtado J, Murugavel M. Prospective clinical assessment using sideline concussion assessment Tool-2 testing in the evaluation of sport-related concussion in college athletes. Clin J Sport Med. 2015;25:36–42. doi:10.1097/JSM.0000000000000102.
   PubMed Web of Science ®Google Scholar
• Marinides Z, Galetta KM, Andrews CN, Wilson JA, Herman DC, Robinson CD, Smith MS, Bentley BC, Galetta SL, Balcer LJ, et al. Vision testing is additive to the sideline assessment of sports-related concussion. Neurol Clin Pract. 2015;5:25–34.
   PubMedGoogle Scholar
• McCrea M, Guskiewicz K, Randolph C, Barr WB, Hammeke TA, Marshall SW, Powell MR, Ahn KW, Wang Y, Kelly JP. Incidence, clinical course, and predictors of prolonged recovery time following sport-related concussion in high school and college athletes. J Int Neuropsychol Soc. 2013;19:22–33. doi:10.1017/S1355617712000872.
   PubMed Web of Science ®Google Scholar
• Master CL, Scheiman M, Gallaway M, Goodman A, Robinson RL, Master SR, Grady MF. Vision diagnoses are common after concussion in adolescents. Clin Pediatr (Phila). 2016;55:260–67. doi:10.1177/0009922815594367.
   PubMed Web of Science ®Google Scholar
• Howell DR, O’Brien MJ, Raghuram A, Shah AS, Meehan WP. Near point of convergence and gait deficits in adolescents after sport-related concussion. Clin J Sport Med Off J Can Acad Sport Med. 2018;28:262–67. doi:10.1097/JSM.0000000000000439.
   PubMed Web of Science ®Google Scholar
• Capó-Aponte JE, Urosevich TG, Temme LA, Tarbett AK, Sanghera NK. Visual dysfunctions and symptoms during the subacute stage of blast-induced mild traumatic brain injury. Mil Med. 2012;177:804–13. doi:10.7205/MILMED-D-12-00061.
   PubMed Web of Science ®Google Scholar
• Mani R, Asper L, Khuu SK. Deficits in saccades and smooth-pursuit eye movements in adults with traumatic brain injury: a systematic review and meta-analysis. Brain Inj. 2018;32:1315–36. doi:10.1080/02699052.2018.1483030.
   PubMed Web of Science ®Google Scholar
• McKee AC, Alosco ML. Assessing subconcussive head impacts in athletes playing contact sports—the eyes have it. JAMA Ophthalmol. 2019;137:270–71. doi:10.1001/jamaophthalmol.2018.6199.
   PubMed Web of Science ®Google Scholar
• Snegireva N, Derman W, Patricios J, Welman KE. Eye tracking technology in sports-related concussion: a systematic review and meta-analysis. Physiol Meas. 2018;39:12TR01. doi:10.1088/1361-6579/aaef44.
   PubMed Web of Science ®Google Scholar
• Hunt AW, Mah K, Reed N, Engel L, Keightley M. Oculomotor-based vision assessment in mild traumatic brain injury: a systematic review. J Head Trauma Rehabil. 2016;31:252–61. doi:10.1097/HTR.0000000000000174.
   PubMed Web of Science ®Google Scholar
• Munoz D, Armstrong I, Coe B. Using eye movements to probe development and dysfunction. In: Van Gompel R, Fischer M, Murray W, Hill R, editors. Eye Movements. Oxford: Elsevier; 2007. p. 99–124.
   Google Scholar
• Klein C, Fischer B. Instrumental and test–retest reliability of saccadic measures. Biol Psychol. 2005;68:201–13. doi:10.1016/j.biopsycho.2004.06.005.
   PubMed Web of Science ®Google Scholar
• Samadani U, Li M, Qian M, Laska E, Ritlop R, Kolecki R, Reyes M, Altomare L, Sone JY, Adem A, et al. Sensitivity and specificity of an eye movement tracking-based biomarker for concussion. Concussion. 2015;1: CNC3.
   Google Scholar
• Munoz DP, Everling S. Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci. 2004;5:218–28. doi:10.1038/nrn1345.
   PubMed Web of Science ®Google Scholar
• Curtis CE, D’Esposito M. Success and failure suppressing reflexive behavior. J Cogn Neurosci. 2003;15:409–18. doi:10.1162/089892903321593126.
   PubMed Web of Science ®Google Scholar
• McDowell JE, Dyckman KA, Austin BP, Clementz BA. Neurophysiology and neuroanatomy of reflexive and volitional saccades: evidence from studies of humans. Brain Cogn. 2008;68:255–70. doi:10.1016/j.bandc.2008.08.016.
   PubMed Web of Science ®Google Scholar
• Heitger MH, Anderson TJ, Jones RD. Saccade sequences as markers for cerebral dysfunction following mild closed head injury. Prog Brain Res. 2002;140:433–48.
   PubMed Web of Science ®Google Scholar
• Webb B, Humphreys D, Heath M. Oculomotor executive dysfunction during the early and later stages of sport-related concussion recovery. J Neurotrauma. 2018;35:1874–81. doi:10.1089/neu.2018.5673.
   PubMed Web of Science ®Google Scholar
• Johnson B, Zhang K, Hallett M, Slobounov S. Functional neuroimaging of acute oculomotor deficits in concussed athletes. Brain Imaging Behav. 2015;9(3):564-73-. https://pubmed.ncbi.nlm.nih.gov/25179246/
   Web of Science ®Google Scholar
• National College Athletic Association (NCAA). NCAA Sports Sponsorship and Participation Rates Database. 2019. [accessed 2020 Jun 20]. http://www.ncaa.org/about/resources/research/ncaa-sports-sponsorship-and-participation-rates-database.
   Google Scholar
• Davis-Hayes C, Gossett JD, Levine WN, Shams T, Harada J, Mitnick J, Noble J. Sex-specific outcomes and predictors of concussion recovery. J Am Acad Orthop Surg. 2017;25:818–28. doi:10.5435/JAAOS-D-17-00276.
   PubMed Web of Science ®Google Scholar
• Covassin T, Savage JL, Bretzin AC, Fox ME. Sex differences in sport-related concussion long-term outcomes. Int J Psychophysiol. 2018;132:9–13.
   PubMed Web of Science ®Google Scholar
• Breck J, Bohr A, Poddar S, McQueen MB, Casault T. Characteristics and Incidence of concussion among a US collegiate undergraduate population. JAMA Netw Open. 2019;2:e1917626. doi:10.1001/jamanetworkopen.2019.17626.
   PubMed Web of Science ®Google Scholar
• Gallagher VT, Kramer N, Abbott K, Alexander J, Breiter H, Herrold A, Lindley T, Mjaanes J, Reilly J. The effects of sex differences and hormonal contraception on outcomes following collegiate sports-related concussion. J Neurotrauma. 2018;35:1242–47. doi:10.1089/neu.2017.5453.
   PubMed Web of Science ®Google Scholar
• Sufrinko AM, Mucha A, Covassin T, Marchetti G, Elbin RJ, Collins MW, Kontos AP. Sex differences in vestibular/ocular and neurocognitive outcomes after sport-related concussion. Clin J Sport Med. 2017;27:133. doi:10.1097/JSM.0000000000000324.
   PubMed Web of Science ®Google Scholar
• Benedict PA, Baner NV, Harrold GK, Moehringer N, Hasanaj L, Serrano LP, Sproul M, Pagnotta G, Cardone DA, Flanagan SR, et al. Gender and age predict outcomes of cognitive, balance and vision testing in a multidisciplinary concussion center. J Neurol Sci. 2015;353:111–15.
   PubMed Web of Science ®Google Scholar
• Heitger MH, Anderson TJ, Jones RD, Dalrymple‐Alford JC, Frampton CM, Ardagh MW. Eye movement and visuomotor arm movement deficits following mild closed head injury. Brain. 2004 Mar 1;127(3):575–90. doi: 10.1093/brain/awh066.
   PubMed Web of Science ®Google Scholar
• Reilly JL, Harris MS, Khine TT, Keshavan MS, Sweeney JA. Reduced attentional engagement contributes to deficits in prefrontal inhibitory control in schizophrenia. Biol Psychiatry. 2008;63:776–83. doi:10.1016/j.biopsych.2007.11.009.
   PubMedGoogle Scholar
• Reilly JL, Frankovich K, Hill S, Gershon ES, Keefe RS, Keshavan MS, Pearlson GD, Tamminga CA, Sweeney JA. Elevated antisaccade error rate as an intermediate phenotype for psychosis across diagnostic categories. Schizophr Bull. 2014;40:1011–21. doi:10.1093/schbul/sbt132.
   PubMed Web of Science ®Google Scholar
• Lunn J, Donovan T, Litchfield D, Lewis C, Davies R, Crawford T. Saccadic eye movement abnormalities in children with epilepsy. Plos One. 2016;11:e0160508. doi:10.1371/journal.pone.0160508.
   PubMed Web of Science ®Google Scholar
• McCrory P, Meeuwisse WH, Aubry M, Cantu RC, Dvorak J, Echemendia RJ, Engebretsen L, Johnston KM, Kutcher JS, Raftery M, et al. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. Br J Sports Med. 2013;47:250–58.
   PubMed Web of Science ®Google Scholar
• Ting WK, Schweizer TA, Topolovec-Vranic J, Cusimano MD. Antisaccadic eye movements are correlated with corpus callosum white matter mean diffusivity, stroop performance, and symptom burden in mild traumatic brain injury and concussion. Front Neurol. 2016;6. doi:10.3389/fneur.2015.00271.
   PubMed Web of Science ®Google Scholar
• Hoffer ME, Balaban C, Szczupak M, Buskirk J, Snapp H, Crawford J, Wise S, Murphy S, Marshall K, Pelusso C, et al. The use of oculomotor, vestibular, and reaction time tests to assess mild traumatic brain injury (mTBI) over time. Laryngoscope Investig Otolaryngol. 2017;2:157–65.
   PubMed Web of Science ®Google Scholar
• Balaban C, Hoffer ME, Szczupak M, Snapp H, Crawford J, Murphy S, Marshall K, Pelusso C, Knowles S, Kiderman A. Oculomotor, vestibular, and reaction time tests in mild traumatic brain injury. Plos One. 2016;11:e0162168. doi:10.1371/journal.pone.0162168.
   PubMed Web of Science ®Google Scholar
• SR Research. EyeLink 1000 User Manual, Version 1.5.2. Mississauga, Ontario: Canada.
   Google Scholar
• Cui H, Liu XH, Wang KY, Zhu CY, Wang C, Xie XH. Association of saccade duration and saccade acceleration/deceleration asymmetry during visually guided saccade in schizophrenia patients. Plos One. 2014;9:e97308. doi:10.1371/journal.pone.0097308.
   PubMed Web of Science ®Google Scholar
• Pratt J, Bekkering H, Abrams RA, Adam J. The Gap effect for spatially oriented responses. Acta Psychol (Amst). 1999;102:1–12. doi:10.1016/S0001-6918(99)00014-1.
   PubMed Web of Science ®Google Scholar
• Drew AS, Langan J, Halterman C, Osternig LR, Chou LS, van Donkelaar P. Attentional disengagement dysfunction following mTBI assessed with the gap saccade task. Neurosci Lett. 2007;417:61–65. doi:10.1016/j.neulet.2007.02.038.
   PubMed Web of Science ®Google Scholar
• Kalesnykas RP, Hallett PE. The differentiation of visually guided and anticipatory saccades in gap and overlap paradigms. Exp Brain Res. 1987;68:115–21. doi:10.1007/BF00255238.
   PubMed Web of Science ®Google Scholar
• Pedersen ER, Grow J, Duncan S, Neighbors C, Larimer ME. Concurrent validity of an online version of the timeline followback assessment. Psychol Addict Behav. 2012;26:672–77. doi:10.1037/a0027945.
   PubMed Web of Science ®Google Scholar
• Robinson SM, Sobell LC, Sobell MB, Leo GI. Reliability of the timeline followback for cocaine, cannabis, and cigarette use. Psychol Addict Behav. 2014;28:154–62. doi:10.1037/a0030992.
   PubMed Web of Science ®Google Scholar
• Sobell LC, Agrawal S, Sobell MB, Leo GI, Young LJ, Cunningham JA, Simco ER. Comparison of a quick drinking screen with the timeline followback for individuals with alcohol problems. J Stud Alcohol. 2003;64:858–61. doi:10.15288/jsa.2003.64.858.
   PubMed Web of Science ®Google Scholar
• Hollingshead AB. Four factor index of social status. 1975. http://ubir.buffalo.edu/xmlui/handle/10477/1879.
   Google Scholar
• Lovell MR, Iverson GL, Collins MW, Podell K, Johnston KM, Pardini D, Pardini J, Norwig J, Maroon JC. Measurement of symptoms following sports-related concussion: reliability and normative data for the post-concussion scale. Appl Neuropsychol. 2006;13:166–74. doi:10.1207/s15324826an1303_4.
   PubMed Web of Science ®Google Scholar
• Beck AT, Steer RA, Ball R, Ranieri WF. Comparison of beck depression Inventories-IA and-II in psychiatric outpatients. J Pers Assess. 1996;67:588–97. doi:10.1207/s15327752jpa6703_13.
   PubMed Web of Science ®Google Scholar
• Sprinkle SD, Lurie D, Insko SL, Atkinson G, Jones GL, Logan AR, Bissada NN. Criterion validity, severity cut scores, and test-retest reliability of the beck depression Inventory-II in a university counseling center sample. J Couns Psychol. 2002;49:381–85. doi:10.1037/0022-0167.49.3.381.
   Web of Science ®Google Scholar
• Cohen S, Kamarck T, Mermelstein R, Global A. Measure of perceived stress. J Health Soc Behav. 1983;24:385–96. doi:10.2307/2136404.
   PubMed Web of Science ®Google Scholar
• Lee E-H. Review of the psychometric evidence of the perceived stress scale. Asian Nurs Res. 2012;6:121–27. doi:10.1016/j.anr.2012.08.004.
   PubMed Web of Science ®Google Scholar
• Song MK, Lin FC, Ward SE, Fine JP. Composite variables: when and how. Nurs Res. 2013;62:45–49. doi:10.1097/NNR.0b013e3182741948.
   PubMed Web of Science ®Google Scholar
• Wechsler D. Wechsler Test of Adult Reading: WTAR. San Antonio (TX): Psychological Corporation; 2001.
   Google Scholar
• Strauss E, Sherman EMS, Spreen O. A compendium of neuropsychological tests: administration, norms, and commentary. 3rd ed. New York, NY, US: Oxford University Press; 2006.
   Google Scholar
• IBM SPSS. Statistics of windows. Armonk, NY: IBM Corp; 2017.
   Google Scholar
• Abrahams S, Mc Fie S, Patricios J, Posthumus M, September AV. Risk factors for sports concussion: an evidence-based systematic review. Br J Sports Med. 2014;48:91–97. doi:10.1136/bjsports-2013-092734.
   PubMed Web of Science ®Google Scholar
• Landry AP, Ting WK, Zador Z, Sadeghian A, Cusimano MD. Using artificial neural networks to identify patients with concussion and postconcussion syndrome based on antisaccades. J Neurosurg. 2018;1:1–8.
   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. 2013;31:180–88. doi:10.1089/neu.2013.2983.
   PubMed Web of Science ®Google Scholar
• Karr J, Areshenkoff C, Garcia-Barrera M. The neuropsychological outcomes of concussion: a systematic review of meta-analyses on the cognitive sequelae of mild traumatic brain injury. Neuropsychology. 2014;28:321–36. doi:10.1037/neu0000037.
   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. Diffusion-tensor imaging implicates prefrontal axonal injury in executive function impairment following very mild traumatic brain injury. Radiology. 2009;252:816–24. doi:10.1148/radiol.2523081584.
   PubMed Web of Science ®Google Scholar
• McDonald BC, Saykin AJ, McAllister TW. Functional MRI of mild traumatic brain injury (mTBI): progress and perspectives from the first decade of studies. Brain Imaging Behav. 2012;6:193–207. doi:10.1007/s11682-012-9173-4.
   PubMed Web of Science ®Google Scholar
• Hutton SB, Ettinger U. The antisaccade task as a research tool in psychopathology: A critical review. Psychophysiology. 2006;43:302–13. doi:10.1111/j.1469-8986.2006.00403.x.
   PubMed Web of Science ®Google Scholar
• Klein C, Rauh R, Biscaldi M. Cognitive correlates of anti-saccade task performance. Exp Brain Res. 2010;203:759–64. doi:10.1007/s00221-010-2276-5.
   PubMed Web of Science ®Google Scholar
• Hashimoto M, Ohtsuka K. Transcranial magnetic stimulation over the posterior cerebellum during visually guided saccades in man. Brain. 1995;118:1185–93. doi:10.1093/brain/118.5.1185.
   PubMed Web of Science ®Google Scholar
• Smalianchuk I, Jagadisan UK, Gandhi NJ. Instantaneous Midbrain control of saccade velocity. J Neurosci. 2018;38:10156–67. doi:10.1523/JNEUROSCI.0962-18.2018.
   PubMed Web of Science ®Google Scholar
• Mallott JM, Palacios EM, Maruta J, Ghajar J, Mukherjee P. Disrupted white matter microstructure of the cerebelpeduncles in scholastic athletes after concussion. Front Neurol. 2019;10. doi:10.3389/fneur.2019.00518.
   PubMed Web of Science ®Google Scholar