[Skip to Content]
[Skip to Content Landing]

Neuro-Ophthalmologic Response to Repetitive Subconcussive Head ImpactsA Randomized Clinical Trial

Educational Objective
To examine whether subconcussive head impacts cause impairments in neuro-ophthalmologic function as measured by the King-Devick test (KDT) and oculomotor function as measured by the near point of convergence.
1 Credit CME
Key Points

Question  How and what extent do subconcussive head impacts from 10 soccer-ball headings influence neuro-ophthalmologic function, as measured by the King-Devick test and near point of convergence test?

Findings  This randomized clinical trial assessed King-Devick test speed and error and near point of convergence before and at 0, 2, and 24 hours after soccer-ball headings and found that 10 soccer-ball headings transiently blunted the neuro-ophthalmologic ability to learn and adapt to the King-Devick test.

Meaning  These data suggest that the neural circuitry linking cognitive and oculomotor functions may be temporarily vulnerable to acute subconcussive head impacts.


Importance  Subconcussive head impacts have emerged as a complex public health concern. The oculomotor system is sensitive to brain trauma; however, neuro-ophthalmologic response to subconcussive head impacts remains unclear.

Objective  To examine whether subconcussive head impacts cause impairments in neuro-ophthalmologic function as measured by the King-Devick test (KDT) and oculomotor function as measured by the near point of convergence.

Design, Setting, and Participants  In this randomized clinical trial, adult soccer players were randomized into either a heading group or kicking (control) group. The heading group executed 10 headers with soccer balls projected at a speed of 25 mph. The kicking-control group followed the same protocol but with 10 kicks. Peak linear and rotational head accelerations were assessed with a triaxial accelerometer. The KDT speed and error and near point of convergence were assessed at baseline (preheading or prekicking) and at 0, 2, and 24 hours after heading or kicking.

Exposures  Ten soccer-ball headings or kicks.

Main Outcomes and Measures  The primary outcome was the group-by-time interaction of KDT speed at 0 hours after heading or kicking. The secondary outcomes included KDT speed at 2 hours and 24 hours after heading or kicking, KDT error, and near point of convergence.

Results  A total of 78 individuals enrolled (heading group, n = 40; kicking-control group, n = 38). Eleven individuals (heading group: 4 women; mean [SD] age, 22.5 [1.0] years; kicking-control group, 3 women and 4 men; mean [SD] age, 20.9 [1.1] years) voluntarily withdrew from the study. Data from 67 participants with a mean (SD) age of 20.6 (1.7) years were eligible for analysis (heading, n = 36; kicking-control, n = 31). Mean (SD) peak linear accelerations and peak rotational accelerations per impact for the heading group were 33.2 (6.8) g and 3.6 (1.4) krad/s2, respectively. Conversely, soccer kicking did not induce a detectable level of head acceleration. Both groups showed improvements in KDT speed (heading group: 0 hours, −1.2 [95% CI, −2.2 to −0.1] seconds; P = .03; 2 hours, −1.3 [95% CI, −2.6 to 0] seconds; P = .05; 24 hours, −3.2 [95% CI, −4.3 to −2.2] seconds; P < .001; kicking-control group: 0 hours, −3.3 [95% CI, −4.1 to −2.5] seconds; P < .001; 2 hours, −4.1 [95% CI, −5.1 to −3.1] seconds; P < .001; 24 hours, −5.2 [95% CI, −6.2 to −4.2] seconds; P < .001). Group differences occurred at all postintervention points; the kicking-control group performed KDT faster at 0 hours (−2.2 [95% CI, −0.8 to −3.5] seconds; P = .001), 2 hours (−2.8 [95% CI, −1.2 to −4.4] seconds; P < .001), and 24 hours after the intervention (−2.0 [95% CI, −0.5 to −3.4] seconds; P = .007) compared with those of the heading group.

Conclusions and Relevance  These data support the hypothesis that neuro-ophthalmologic function is affected, at least in the short term, by subconcussive head impacts that may affect some individuals in some contact sports. Further studies may help determine if these measures can be a useful clinical tool in detecting acute subconcussive injury.

Trial Registration  ClinicalTrials.gov Identifier: NCT03488381

Sign in to take quiz and track your certificates

Buy This Activity

JN Learning™ is the home for CME and MOC from the JAMA Network. Search by specialty or US state and earn AMA PRA Category 1 Credit(s)™ from articles, audio, Clinical Challenges and more. Learn more about CME/MOC

CME Disclosure Statement: Unless noted, all individuals in control of content reported no relevant financial relationships. If applicable, all relevant financial relationships have been mitigated.

Article Information

Accepted for Publication: December 23, 2019.

Corresponding Author: Keisuke Kawata, PhD, Department of Kinesiology, Indiana University School of Public Health–Bloomington, 1025 E Seventh St, Bloomington, IN 47405 (kkawata@indiana.edu).

Published Online: February 13, 2020. doi:10.1001/jamaophthalmol.2019.6128

Author Contributions: Dr Kawata had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: Kawata.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Nowak, Ejima, Kawata.

Critical revision of the manuscript for important intellectual content: Bevilacqua, Ejima, Huibregtse, Chen, Mickleborough, Newman.

Statistical analysis: Ejima, Chen.

Obtained funding: Kawata.

Administrative, technical, or material support: Nowak, Kawata.

Supervision: Mickleborough, Kawata.

Conflict of Interest Disclosures: None reported.

Funding/Support: This work was partly supported by the Indiana Spinal Cord and Brain Injury Research Fund from the Indiana State Department of Health (0019939 [Dr Kawata]) and the Indiana University School of Public Health faculty research grant program (2246237 [Dr Kawata]).

Role of the Funder/Sponsor: The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Data Sharing Statement: See Supplement 4.

Additional Contributions: Authors would like to thank Angela Wirsching, MS, Rachel Kalbfell, Alekhya Koppineni, Joseph Kim, BS, and Aditya Belamkar, Indiana University, for their assistance in data collection. They were not compensated for their contributions.

National Collegiate Athletic Association. Estimated probability of competing in college athletics. http://www.ncaa.org/about/resources/research/estimated-probability-competing-professional-athletics. Published 2017. Accessed July 20, 2017.
Bailes  JE , Petraglia  AL , Omalu  BI , Nauman  E , Talavage  T .  Role of subconcussion in repetitive mild traumatic brain injury.   J Neurosurg. 2013;119(5):1235-1245. doi:10.3171/2013.7.JNS121822PubMedGoogle ScholarCrossref
Goldstein  LE , Fisher  AM , Tagge  CA ,  et al.  Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model.   Sci Transl Med. 2012;4(134):134ra60. doi:10.1126/scitranslmed.3003716PubMedGoogle Scholar
McKee  AC , Stern  RA , Nowinski  CJ ,  et al.  The spectrum of disease in chronic traumatic encephalopathy.   Brain. 2013;136(pt 1):43-64. doi:10.1093/brain/aws307PubMedGoogle ScholarCrossref
Mez  J , Daneshvar  DH , Kiernan  PT ,  et al.  Clinicopathological evaluation of chronic traumatic encephalopathy in players of American football.   JAMA. 2017;318(4):360-370. doi:10.1001/jama.2017.8334PubMedGoogle ScholarCrossref
Kawata  K , Tierney  R , Phillips  J , Jeka  JJ .  Effect of repetitive sub-concussive head impacts on ocular near point of convergence.   Int J Sports Med. 2016;37(5):405-410. doi:10.1055/s-0035-1569290PubMedGoogle ScholarCrossref
Kawata  K , Rubin  LH , Lee  JH ,  et al.  Association of football subconcussive head impacts with ocular near point of convergence.   JAMA Ophthalmol. 2016;134(7):763-769. doi:10.1001/jamaophthalmol.2016.1085PubMedGoogle ScholarCrossref
Zonner  SW , Ejima  K , Fulgar  CC ,  et al.  Oculomotor response to cumulative subconcussive head impacts in US high school football players: a pilot longitudinal study.   JAMA Ophthalmol. 2019;137(3):265-270. doi:10.1001/jamaophthalmol.2018.6193PubMedGoogle ScholarCrossref
Caccese  JB , Best  C , Lamond  LC ,  et al.  Effects of repetitive head impacts on a concussion assessment battery.   Med Sci Sports Exerc. 2019;51(7):1355-1361. doi:10.1249/MSS.0000000000001905PubMedGoogle ScholarCrossref
Davenport  EM , Whitlow  CT , Urban  JE ,  et al.  Abnormal white matter integrity related to head impact exposure in a season of high school varsity football.   J Neurotrauma. 2014;31(19):1617-1624. doi:10.1089/neu.2013.3233PubMedGoogle ScholarCrossref
Talavage  TM , Nauman  EA , Breedlove  EL ,  et al.  Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion.   J Neurotrauma. 2014;31(4):327-338. doi:10.1089/neu.2010.1512PubMedGoogle ScholarCrossref
Breedlove  EL , Robinson  M , Talavage  TM ,  et al.  Biomechanical correlates of symptomatic and asymptomatic neurophysiological impairment in high school football.   J Biomech. 2012;45(7):1265-1272. doi:10.1016/j.jbiomech.2012.01.034PubMedGoogle ScholarCrossref
Bevilacqua  ZW , Huibregtse  ME , Kawata  K .  In vivo protocol of controlled subconcussive head impacts for the validation of field study data.   J Vis Exp. 2019;146(146):e59381. doi:10.3791/59381PubMedGoogle Scholar
Rizzo  JR , Hudson  TE , Dai  W ,  et al.  Objectifying eye movements during rapid number naming: methodology for assessment of normative data for the King-Devick test.   J Neurol Sci. 2016;362:232-239. doi:10.1016/j.jns.2016.01.045PubMedGoogle ScholarCrossref
Wirsching  A , Chen  Z , Bevilacqua  ZW , Huibregtse  ME , Kawata  K .  Association of acute increase in plasma neurofilament light with repetitive subconcussive head impacts: a pilot randomized control trial.   J Neurotrauma. 2019;36(4):548-553. doi:10.1089/neu.2018.5836PubMedGoogle ScholarCrossref
Linthorne  NP , Everett  DJ .  Release angle for attaining maximum distance in the soccer throw-in.   Sports Biomech. 2006;5(2):243-260. doi:10.1080/14763140608522877PubMedGoogle ScholarCrossref
Oberlander  TJ , Olson  BL , Weidauer  L .  Test-retest reliability of the King-Devick test in an adolescent population.   J Athl Train. 2017;52(5):439-445. doi:10.4085/1062-6050-52.2.12PubMedGoogle ScholarCrossref
Galetta  KM , Barrett  J , Allen  M ,  et al.  The King-Devick test as a determinant of head trauma and concussion in boxers and MMA fighters.   Neurology. 2011;76(17):1456-1462. doi:10.1212/WNL.0b013e31821184c9PubMedGoogle ScholarCrossref
Davies  EC , Henderson  S , Balcer  LJ , Galetta  SL .  Residency training: the King-Devick test and sleep deprivation, study in pre- and post-call neurology residents.   Neurology. 2012;78(17):e103-e106. doi:10.1212/WNL.0b013e318251833dPubMedGoogle ScholarCrossref
Duma  SM , Manoogian  SJ , Bussone  WR ,  et al.  Analysis of real-time head accelerations in collegiate football players.   Clin J Sport Med. 2005;15(1):3-8. doi:10.1097/00042752-200501000-00002PubMedGoogle ScholarCrossref
Crisco  JJ , Fiore  R , Beckwith  JG ,  et al.  Frequency and location of head impact exposures in individual collegiate football players.   J Athl Train. 2010;45(6):549-559. doi:10.4085/1062-6050-45.6.549PubMedGoogle ScholarCrossref
Reynolds  BB , Patrie  J , Henry  EJ ,  et al.  Practice type effects on head impact in collegiate football.   J Neurosurg. 2016;124(2):501-510 PubMedGoogle ScholarCrossref
Slobounov  SM , Walter  A , Breiter  HC ,  et al.  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. 2017;14:708-718. doi:10.1016/j.nicl.2017.03.006PubMedGoogle ScholarCrossref
Reynolds  BB , Stanton  AN , Soldozy  S , Goodkin  HP , Wintermark  M , Druzgal  TJ .  Investigating the effects of subconcussion on functional connectivity using mass-univariate and multivariate approaches.   Brain Imaging Behav. 2018;12(5):1332-1345.PubMedGoogle ScholarCrossref
Bahrami  N , Sharma  D , Rosenthal  S ,  et al.  Subconcussive head impact exposure and white matter tract changes over a single season of youth football.   Radiology. 2016;281(3):919-926. doi:10.1148/radiol.2016160564PubMedGoogle ScholarCrossref
Lipton  ML , Kim  N , Zimmerman  ME ,  et al.  Soccer heading is associated with white matter microstructural and cognitive abnormalities.   Radiology. 2013;268(3):850-857. doi:10.1148/radiol.13130545PubMedGoogle ScholarCrossref
Bazarian  JJ , Zhu  T , Zhong  J ,  et al.  Persistent, long-term cerebral white matter changes after sports-related repetitive head impacts.   PLoS One. 2014;9(4):e94734. doi:10.1371/journal.pone.0094734PubMedGoogle Scholar
Gong  NJ , Kuzminski  S , Clark  M ,  et al.  Microstructural alterations of cortical and deep gray matter over a season of high school football revealed by diffusion kurtosis imaging.   Neurobiol Dis. 2018;119:79-87. doi:10.1016/j.nbd.2018.07.020PubMedGoogle ScholarCrossref
Laksari  K , Kurt  M , Babaee  H , Kleiven  S , Camarillo  D .  Mechanistic insights into human brain impact dynamics through modal analysis.   Phys Rev Lett. 2018;120(13):138101. doi:10.1103/PhysRevLett.120.138101PubMedGoogle Scholar
Di Virgilio  TG , Hunter  A , Wilson  L ,  et al.  Evidence for acute electrophysiological and cognitive changes following routine soccer heading.   EBioMedicine. 2016;13:66-71. doi:10.1016/j.ebiom.2016.10.029PubMedGoogle ScholarCrossref
Johnson  B , Hallett  M , Slobounov  S .  Follow-up evaluation of oculomotor performance with fMRI in the subacute phase of concussion.   Neurology. 2015;85(13):1163-1166. doi:10.1212/WNL.0000000000001968PubMedGoogle ScholarCrossref
Johnson  B , Zhang  K , Hallett  M , Slobounov  S .  Functional neuroimaging of acute oculomotor deficits in concussed athletes.   Brain Imaging Behav. 2015;9(3):564-573. doi:10.1007/s11682-014-9316-xPubMedGoogle ScholarCrossref
McAllister  TW , Ford  JC , Flashman  LA ,  et al.  Effect of head impacts on diffusivity measures in a cohort of collegiate contact sport athletes.   Neurology. 2014;82(1):63-69. doi:10.1212/01.wnl.0000438220.16190.42PubMedGoogle ScholarCrossref
Matser  JT , Kessels  AG , Jordan  BD , Lezak  MD , Troost  J .  Chronic traumatic brain injury in professional soccer players.   Neurology. 1998;51(3):791-796. doi:10.1212/WNL.51.3.791PubMedGoogle ScholarCrossref
Subotic  A , Ting  WK , Cusimano  MD .  Characteristics of the King-Devick test in the assessment of concussed patients in the subacute and later stages after injury.   PLoS One. 2017;12(8):e0183092. doi:10.1371/journal.pone.0183092PubMedGoogle Scholar
King  D , Hume  P , Gissane  C , Clark  T .  Use of the King-Devick test for sideline concussion screening in junior rugby league.   J Neurol Sci. 2015;357(1-2):75-79. doi:10.1016/j.jns.2015.06.069PubMedGoogle ScholarCrossref
Galetta  KM , Brandes  LE , Maki  K ,  et al.  The King-Devick test and sports-related concussion: study of a rapid visual screening tool in a collegiate cohort.   J Neurol Sci. 2011;309(1-2):34-39. doi:10.1016/j.jns.2011.07.039PubMedGoogle ScholarCrossref
King  D , Gissane  C , Hume  PA , Flaws  M .  The King-Devick test was useful in management of concussion in amateur rugby union and rugby league in New Zealand.   J Neurol Sci. 2015;351(1-2):58-64. doi:10.1016/j.jns.2015.02.035PubMedGoogle ScholarCrossref
Guskiewicz  KM , Mihalik  JP , Shankar  V ,  et al.  Measurement of head impacts in collegiate football players: relationship between head impact biomechanics and acute clinical outcome after concussion.   Neurosurgery. 2007;61(6):1244-1252. doi:10.1227/01.neu.0000306103.68635.1aPubMedGoogle ScholarCrossref
Schnebel  B , Gwin  JT , Anderson  S , Gatlin  R .  In vivo study of head impacts in football: a comparison of National Collegiate Athletic Association Division I versus high school impacts.   Neurosurgery. 2007;60(3):490-495. doi:10.1227/01.NEU.0000249286.92255.7FPubMedGoogle ScholarCrossref
AMA CME Accreditation Information

Credit Designation Statement: The American Medical Association designates this Journal-based CME activity activity for a maximum of 1.00  AMA PRA Category 1 Credit(s)™. Physicians should claim only the credit commensurate with the extent of their participation in the activity.

Successful completion of this CME activity, which includes participation in the evaluation component, enables the participant to earn up to:

  • 1.00 Medical Knowledge MOC points in the American Board of Internal Medicine's (ABIM) Maintenance of Certification (MOC) program;;
  • 1.00 Self-Assessment points in the American Board of Otolaryngology – Head and Neck Surgery’s (ABOHNS) Continuing Certification program;
  • 1.00 MOC points in the American Board of Pediatrics’ (ABP) Maintenance of Certification (MOC) program;
  • 1.00 Lifelong Learning points in the American Board of Pathology’s (ABPath) Continuing Certification program; and
  • 1.00 CME points in the American Board of Surgery’s (ABS) Continuing Certification program

It is the CME activity provider's responsibility to submit participant completion information to ACCME for the purpose of granting MOC credit.

Want full access to the AMA Ed Hub?
After you sign up for AMA Membership, make sure you sign in or create a Physician account with the AMA in order to access all learning activities on the AMA Ed Hub
Buy this activity
Want full access to the AMA Ed Hub?
After you sign up for AMA Membership, make sure you sign in or create a Physician account with the AMA in order to access all learning activities on the AMA Ed Hub
Buy this activity
With a personal account, you can:
  • Access free activities and track your credits
  • Personalize content alerts
  • Customize your interests
  • Fully personalize your learning experience
Education Center Collection Sign In Modal Right

Name Your Search

Save Search
With a personal account, you can:
  • Access free activities and track your credits
  • Personalize content alerts
  • Customize your interests
  • Fully personalize your learning experience

Lookup An Activity


My Saved Searches

You currently have no searches saved.


My Saved Courses

You currently have no courses saved.