You are here

Article Text

Article menu
Ophthalmology
Protocol
Ocular motor disorders in children and adults with mTBI: a scoping review protocol
  1. Jacqueline Theis1,2,
  2. Angela M Chen3,
  3. Allegra P Burgher3,
  4. Lynn D Greenspan4,
  5. Andrew Morgenstern5,
  6. Aaron D Salzano6,
  7. Tiong Peng Yap7,
  8. Mitchell Scheiman4,
  9. Tawna L Roberts8
  1. 1Physical Medicine and Rehabilitation, Uniformed Services University of the Health Sciences F Edward Hébert School of Medicine, Bethesda, Maryland, USA
  2. 2Concussion Care Centre of Virginia, Richmond, Virginia, USA
  3. 3Southern California College of Optometry, Marshall B Ketchum University, Fullerton, California, USA
  4. 4Salus University Pennsylvania College of Optometry, Elkins Park, Pennsylvania, USA
  5. 5Department of Surgery, Walter Reed National Military Medical Center, Bethesda, Maryland, USA
  6. 6College of Optometry, Pacific University, Forest Grove, Oregon, USA
  7. 7IGARD Vision Therapy Center, Singapore
  8. 8Spencer Center for Vision Research, Byers Eye Institute, Stanford University, Stanford, California, USA
  1. Correspondence to Dr Jacqueline Theis; drtheisod{at}virginianeurooptometry.com

Abstract

Introduction Ocular motor function is susceptible to neurological injury because it requires a large portion of brain circuitry including every lobe of the brain, brainstem, thalamus, basal ganglia, cerebellum, cranial nerves and visual tracts. While reports of a high frequency of ocular motor dysfunctions after mild traumatic brain injury (mTBI) span multidisciplinary journals, there is no scoping review of the signs, diagnostic assessments and criteria, and appropriate management of ocular motor disorders post-mTBI. Post-mTBI ocular motor dysfunction has been reported to respond to active treatment. The objective of this scoping review is to map the available evidence on the diagnostic assessment and treatment modalities currently used in the management of mTBI-related ocular motor disorders in children and adults. This scoping review also aims to identify gaps in the current literature and provide suggestions for future research.

Methods and analysis This review will include populations with reported concussion and/or mTBI without restrictions on age, race, sex or time since injury. The review will evaluate the reported symptoms related to ocular motor dysfunction, types of assessments and diagnostic criteria used, reported treatments, and the level of evidence supporting the reported treatments. This review will exclude literature on brain injury of non-traumatic aetiology and moderate/severe traumatic brain injury. Ocular motor dysfunction after mTBI appears in journals across multiple disciplines. Thus, multiple databases will be evaluated including Pubmed, Embase, PEDro, OVID, Clinical Key, Google Scholar and REHABDATA. Literature will be searched from inception to present day. Evidence sources will include experimental study designs including randomised controlled trials, non-randomised controlled trials and interrupted time-series. Additionally, analytical observational studies including prospective and retrospective cohort studies, case series, cross-sectional studies and clinical practice guidelines will be considered for inclusion. Data will be extracted on clinical presentation, frequency, assessment, diagnostic criteria management strategies and outcomes of concussion and mTBI-related ocular motor disorders.

Ethics and dissemination This scoping review will use data from existing publications and does not require ethical approval by an institutional review board. Results will be disseminated through publication in a peer-reviewed scientific journal and presented at relevant conferences and as part of future workshops with professionals involved with diagnosis and management of patients with mTBI.

  • neurological injury
  • neuro-ophthalmology
  • paediatric ophthalmology
  • strabismus
http://creativecommons.org/licenses/by-nc/4.0/

This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

https://doi.org/10.1136/bmjopen-2023-073656

Statistics from Altmetric.com

    Request Permissions

    If you wish to reuse any or all of this article please use the link below which will take you to the Copyright Clearance Center’s RightsLink service. You will be able to get a quick price and instant permission to reuse the content in many different ways.

    STRENGTHS AND LIMITATIONS OF THIS STUDY

    • The study protocol outlines a rigorous design that includes the use of the established Preferred Reporting Items for Systematic Reviews and Meta-Analyses scoping review methodology and search strategy.

    • The broad search strategy is designed to capture all articles relevant to mild traumatic brain injury (mTBI)-related ocular motor disorders.

    • The review is limited to articles published in English, which may influence the types of diagnostic and treatment modalities in the studies reviewed.

    • A universal definition of mTBI is not currently available and continues to evolve over time, which may result in diagnostic misclassification across studies.

    Introduction

    Mild traumatic brain injury (mTBI) is a prevalent injury that impacts up to and possibly more than 600/100 000 population per year globally and represents 70%–90% of all TBI.1 The most common aetiology of mTBI includes sports, motor vehicle accidents, bicycle accidents, falls and assaults.1 2 The majority of epidemiological data sources depend on patients seeking medical attention; therefore are often underestimated in national epidemiological studies leading to gaps in the incidence and prevalence of mTBI.3

    A universal definition of mTBI is not currently available and the definition is consistently being updated by expert working groups.4 In general, an mTBI is considered clinical sequelae of neurological dysfunction that occurs after an acute traumatic brain injury due to mechanical energy to the head from external physical forces.5 The acute pathophysiology involves a transient disruption of cellular membranes in the brain due to focal and/or diffuse damage to neuronal dendrites, axons and astrocytes leading to a release of neurotransmitters. This altered neurotransmission has numerous consequences, including a diffuse change in intracellular and extracellular ionic equilibrium causing subsequent metabolic crisis to re-establish homeostasis, as well as persistent neuroinflammation and cell loss.6 To be classified as ‘mild’ TBI, the Glasgow coma scale (if employed) should range from 13 to 15, and if present, loss of consciousness should persist no longer than 30 min, and post-traumatic amnesia should last less than 24 hours postinjury.7 8 Due to the low risk for intracranial injury, diagnostic neuroimaging like CT and MRI scans are not routinely employed in the acute evaluation of mTBI, unless clinical risk factors support the need for imaging.9 Concussion is a type of mTBI, and the term is colloquially used interchangeably with mTBI in the scientific literature and clinical care.8 10 Concussion, a subtype of mTBI, will be included within the scoping review search, and will be hereafter referred to as mTBI.

    Due to the complicated pathophysiology and heterogeneity of the condition, patients with mTBI can present with a constellation of symptoms including but not limited to cognitive, psychological/mood, vestibular, headache/migraine and visual.11 Symptoms of concussion can persist for months and years after injury, impacting quality of life, and causing significant financial burden to individuals and society.12–14 Visual symptoms are common in up to 68% of patients with chronic mTBI.15 16 Vision is a crucial neurological sensory and motor system needed to interpret and interact with the world, and therefore visual dysfunction can significantly impact the ability for patients to return to activities like work, sport, school and military duty.17 Ocular motor impairments like difficulties converging the eyes have been associated with prolonged recovery18 and worse neurocognitive impairment,19 directly impacting a patient’s ability to learn and work.20 21 Visual symptoms post-mTBI may include but are not limited to blurry vision, double vision, difficulties with reading, light sensitivity, and physical symptoms like headache or dizziness triggered by visual tasks like computer or reading.20 22

    Vision problems due to ocular motor dysfunction in mTBI are common.23–25 A large portion of brain circuitry, including every lobe of the brain, brainstem, thalamus, basal ganglia, cerebellum, cranial nerves and visual tracts, is related to visual function, making the visual system susceptible to neurological injury.26 Visual symptoms, such as blur, double vision, dizziness and headaches associated with visual tasks, may be signs of post-concussion ocular motor dysfunction.27 Ocular motor function describes the overall ability of the eyes to focus on objects of interest, track targets and maintain binocular alignment to ensure clear, stable and single vision as an individual moves through space. Ocular motor function includes smooth pursuits (ability for the eyes to track a slowly moving object), saccades (ability to move the eyes from one object to another), vergences (ability for the eyes to turn inward and outward together to fixate far and near objects) and accommodation (ability to change the focus of each eye to objects at different distances from the eyes). The ocular motor system interacts with the vestibular system through the vestibular-ocular reflex, where the eyes move in response to head and body movement as indicated by vestibular input. Post-mTBI ocular motor dysfunction is highly responsive to active participation in treatments.28 29 Thus, ocular motor dysfunction may serve as an objective biomarker for neurological impairment following mTBI.30–33

    Reports of a high frequency of ocular motor dysfunction(s) after mTBI span multidisciplinary journals.23–25 31–34 Comparison of the published research and reports across journals highlights the lack of knowledge of the evaluation of vision, poor standardisation of techniques across studies, and an overall lack of consistency in methodology and diagnostic criteria both across and within disciplines in the assessment and management of visual dysfunctions in mTBI.33 The objective of this scoping review is to map the available evidence on the diagnostic assessment and treatment modalities that are currently being used in the management of mTBI-related ocular motor disorders in children and adults.35 This scoping review also aims to identify any gaps in the current literature, provide suggestions for future research and to serve as a precursor to a systematic review.

    Review questions

    1. What are the criteria used to diagnose ocular motor dysfunction* after mTBI in children and adults?

    2. Based on these diagnostic criteria, what is the reported frequency of ocular motor dysfunction and associated symptoms after concussion?

    3. What is the natural history of post-concussion ocular motor dysfunction in children and adults?

    4. What treatment modalities are currently being used in the management of concussion-related ocular motor disorders in children and adults?

      1. What has been proposed, and what was the reported treatment response?

    5. Are there differences across healthcare disciplines in clinical guidelines and recommendations for evaluation and treatment of ocular motor dysfunction after concussion in children and adults?

    *Ocular motor dysfunction will include disorders of vergence, accommodation, saccades, smooth pursuit and vestibular-ocular reflex.

    Keywords

    Concussion; mTBI; vergence dysfunction; accommodative disorders; oculomotor dysfunction, ocular motor.

    Methods

    We will perform the scoping review in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses Extension for Scoping Reviews (PRISMA-sCR) methodology.36

    Eligibility criteria

    We will include original research, clinical practice guidelines and reports on ocular motor dysfunction. All databases will be searched from inception to achieve the largest scope possible and to detail early innovations in this field. We will use the Population/Participants, Concept and Context framework to inform our inclusion criteria, search and data charting strategies.36 37

    Patient and public involvement

    None.

    Population/Participants

    Studies eligible for inclusion in this review include participants with mTBI without restrictions on age, race or sex. There will be no limits on the time from the injury. Studies evaluating brain injury of non-traumatic aetiology or moderate/severe traumatic brain injury will be excluded from this review. This review will classify the severity of mTBI using the categorisations used in the included articles. This will guide the selection of articles that pertain to mTBI.

    Concept

    Literature will be reviewed regarding the diagnostic assessments currently being performed, the diagnostic criteria used, and the individuals performing these assessments, as well as the translatability of these assessments across disciplines. The symptoms of ocular motor dysfunction and reported relative frequency of these disorders in the post-concussion population will be evaluated. The types of treatment and the evidence supporting the interventions will be reviewed including vision or orthoptic therapy, vestibular-oculomotor and/or vestibular therapy, refractive lenses, patching/occlusion therapy, tinted lenses, prism, school and work accommodations, lifestyle adaptations, surgical interventions, pharmaceutical interventions, other medical interventions and observation.

    Context

    Articles will be limited to those written in English, but there are no restrictions on the country of origin of the study/article. The review will evaluate ‘mTBI’, including concussion, as diagnosed by clinical standard of care, which is to be further defined after the review of the literature. All time points from the mTBI will be included across disciplines.

    This scoping review will consider experimental study designs including randomised controlled trials, non-randomised controlled trials and interrupted time-series studies. In addition, analytical observational studies including prospective and retrospective cohort studies, case series with at least three or more mTBI, cross-sectional studies, as well as clinical practice guidelines will be considered for inclusion. This study will exclude conference proceedings.

    Search strategy

    Identification of studies relevant to this review will be achieved by searching the following electronic bibliographic databases: Pubmed, Embase, PEDro, OVID, Clinical Key, Google Scholar and REHABDATA. Reference lists of included studies will also be searched to identify additional relevant studies. In addition to the bibliographic database searches, relevant grey literature sources will be searched including: relevant national and international organisations’ websites and clinical practice guidelines.

    Search terms will be developed with input from the review team in collaboration with an experienced research librarian.

    Keywords to be searched will be a combination of one of the following:

    1. oculomotor, ocular motor, vergence, convergence, divergence, accommodation, accommodative, insufficiency, spasm, visual, vision, visual dysfunction, visual disorder, visual tracking, tracking, saccade, saccadic, microsaccade, fixation, eye movement, smooth pursuit, vestibular-ocular, vestibular-oculomotor, phoria, esophoria, exophoria, vertical phoria, strabismus, vision therapy, visual therapy, vestibular therapy, lenses, refractive, tints, tinted lenses, prism, patching, occlusion, binasal, font size, Botox, botulinum, blur, blurred vision, double vision, diplopia, eye strain, eyestrain, eye pain, VOMS, OMAT, NPC, King Devick, Developmental eye movement, CISS, BIVSS, oculomotor treatment, oculomotor intervention, oculomotor natural history, orthoptics, vision rehabilitation, ocular motor rehabilitation, ocular motor treatment.

    AND one of the following:

    1. Concussion, Mild traumatic brain injury, Mild TBI, mTBI, Whiplash.

    Study/source of evidence selection

    Following the bibliographic searches, all identified citations except grey literature will be collated and uploaded into Covidence and duplicates removed. Following a pilot test, each title and abstract will then be screened by two independent reviewers for assessment against the inclusion criteria for the review. Potentially relevant sources will be retrieved in full and imported into Covidence for further assessment and review. Each full text report will be assessed by two independent reviewers. Reasons for exclusion of sources of evidence at full text that do not meet the inclusion criteria will be recorded and reported in the scoping review. Any disagreements that arise between the reviewers at each stage of the selection process will be resolved through discussion, or with an additional reviewer/s. The aforementioned process will also be performed on grey literature search but not included in Covidence. The results of the search and the study inclusion and exclusion process will be reported in full in the final scoping review and presented in a PRISMA-ScR flow diagram. It will include the number of articles retrieved, description of types of study design and number of studies ultimately included in the review. An example of a database search can be found in table 1, and all databases searched can be found in online supplemental material.

    View this table:
    Table 1

    Search strategy for Pubmed, Results 6045

    Data extraction

    After a piloting step, data will be extracted from papers included in the scoping review by two independent reviewers using Covidence data extraction tool. The data extracted will include specific details about the participants, concept, context, study methods and key findings relevant to the review questions. Specifically, the scoping review will look at any data regarding frequency, prevalence, definitions, diagnostics, and treatment options for ocular motor dysfunction post-mTBI.

    Data will be extracted into tables (tables 2–4). Data extracted will include first author, year of publication, study location, sample size, study design, type of discipline/provider involved in the study, age of participants, definition criteria for mTBI, time since injury to evaluation, aetiology of mTBI, and the types of ocular motor dysfunctions evaluated including accommodation, vergence, saccades, smooth pursuits, vestibular-ocular reflex and any others noted. Each ocular motor dysfunction will have further data extracted as applicable to the study including symptoms, diagnostic tests and instruments used, diagnostic criteria including cut-off values, results (including reported frequency and/or prevalence of disorder(s)), treatment type employed and treatment results. There will also be a section to list any confounding factors such as possible comorbidities, including but not limited to repeated mTBI, attention deficit hyperactivity disorder, depression or learning disabilities which could also have concomitant ocular motor disorders and thus influence the data related to exact aetiology of ocular motor disorders. The tables will be modified and revised as necessary during the process of extracting data from each included evidence source. Modifications will be detailed in the scoping review. Any disagreements that arise between the reviewers will be resolved through discussion, or with an additional reviewer/s. If appropriate, authors of papers will be contacted to request missing or additional data, where required. Each ocular motor dysfunction category will have a separate table detailing the diagnostic assessments and criteria used, frequency and prevalence of ocular motor dysfunction studied, treatment options employed and results. Data from clinical practice guidelines including definitions, diagnostic criteria, diagnostic test recommendations and treatment recommendations will be extracted into a separate table.

    View this table:
    Table 2

    Data extraction instrument for study characteristics

    View this table:
    Table 3

    Data extraction instrument for diagnostic testing

    View this table:
    Table 4

    Data extraction instrument for treatment interventions

    Data analysis and presentation

    A summary table of patient population demographics, discipline and mTBI definition/characteristics will be presented.

    Data will be analysed for each type of ocular motor disorder in regards to its frequency post-mTBI, the diagnostic criteria and tests used, symptoms reported, as well as the treatments employed and efficacy of the treatment. Where applicable, quantitative evidence will be aggregated using summary statistics. Data from observational studies or studies with control will be evaluated to assess the natural history of ocular motor dysfunction in mTBI and presented in separate tables (tables 2–4).

    Ethics statements

    Patient consent for publication

    References

    1. ↵
      1. Cassidy JD,
      2. Carroll LJ,
      3. Peloso PM, et al
      . Incidence, risk factors and prevention of mild traumatic brain injury: results of the WHO collaborating centre task force on mild traumatic brain injury. J Rehabil Med 2004:28–60. doi:10.1080/16501960410023732
    2. ↵
      1. Hon KL,
      2. Leung AKC,
      3. Torres AR
      . Concussion: A global perspective. Semin Pediatr Neurol 2019;30:117–27. doi:10.1016/j.spen.2019.03.017
      OpenUrlCrossRef
    3. ↵
      1. Centers for Disease Control and Prevention
      . National Center for Injury Prevention and Control; Division of Unintentional Injury Prevention. Atlanta, GA, 2015.
    4. ↵
      1. Silverberg ND,
      2. Iverson GL,
      3. Cogan A, et al
      . The American Congress of rehabilitation medicine diagnostic criteria for mild traumatic brain injury. Arch Phys Med Rehabil 2023;104:1343–55. doi:10.1016/j.apmr.2023.03.036
      OpenUrl
    5. ↵
      1. Centers for Disease Control and Prevention
      . Report to Congress on Mild Traumatic Brain Injury in the United States: Steps to Prevent a Serious Public Health Problem. Atlanta, GA: National Center for Injury Prevention and Control, 2003.
    6. ↵
      1. Romeu-Mejia R,
      2. Giza CC,
      3. Goldman JT
      . Concussion pathophysiology and injury Biomechanics. Curr Rev Musculoskelet Med 2019;12:105–16. doi:10.1007/s12178-019-09536-8
      OpenUrlPubMed
    7. ↵
      1. Teasdale G,
      2. Jennett B
      . Assessment of coma and impaired consciousness. A practical scale. Lancet 1974;2:81–4. doi:10.1016/s0140-6736(74)91639-0
      OpenUrlCrossRefPubMedWeb of Science
    8. ↵
      1. Sussman ES,
      2. Pendharkar AV,
      3. Ho AL, et al
      . Mild traumatic brain injury and concussion: terminology and classification. Handb Clin Neurol 2018;158:21–4. doi:10.1016/B978-0-444-63954-7.00003-3
      OpenUrl
    9. ↵
      1. Lumba-Brown A,
      2. Yeates KO,
      3. Sarmiento K, et al
      . Diagnosis and management of mild traumatic brain injury in children: A systematic review. JAMA Pediatr 2018;172:e182847. doi:10.1001/jamapediatrics.2018.2847
    10. ↵
      1. Pearce JMS
      . Observations on concussion. A review. Eur Neurol 2008;59:113–9. doi:10.1159/000111872
      OpenUrlPubMed
    11. ↵
      1. Kontos AP,
      2. Sufrinko A,
      3. Sandel N, et al
      . Sport-related concussion clinical profiles: clinical characteristics, targeted treatments, and preliminary evidence. Curr Sports Med Rep 2019;18:82–92. doi:10.1249/JSR.0000000000000573
      OpenUrl
    12. ↵
      1. Rockhill CM,
      2. Fann JR,
      3. Fan M-Y, et al
      . Healthcare costs associated with mild traumatic brain injury and psychological distress in children and adolescents. Brain Injury 2010;24:1051–60. doi:10.3109/02699052.2010.494586
      OpenUrlCrossRefPubMed
    13. ↵
      1. Frick KD,
      2. Singman EL
      . Cost of military eye injury and vision impairment related to traumatic brain injury: 2001-2017. Mil Med 2019;184:e338–43. doi:10.1093/milmed/usy420
      OpenUrl
    14. ↵
      1. Pavlov V,
      2. Thompson-Leduc P,
      3. Zimmer L, et al
      . Mild traumatic brain injury in the United States: demographics, brain imaging procedures, health-care utilization and costs. Brain Inj 2019;33:1151–7. doi:10.1080/02699052.2019.1629022
      OpenUrlPubMed
    15. ↵
      1. Magone MT,
      2. Kwon E,
      3. Shin SY
      . Chronic visual dysfunction after blast-induced mild traumatic brain injury. J Rehabil Res Dev 2014;51:71–80. doi:10.1682/JRRD.2013.01.0008
      OpenUrlCrossRefPubMed
    16. ↵
      1. Master CL,
      2. Scheiman M,
      3. Gallaway M, et al
      . Vision diagnoses are common after concussion in adolescents. Clin Pediatr (Phila) 2016;55:260–7. doi:10.1177/0009922815594367
      OpenUrlCrossRefPubMed
    17. ↵
      1. Schmitz B,
      2. Smulligan KL,
      3. Wingerson MJ, et al
      . Double vision and light sensitivity symptoms are associated with return-to-school timing after pediatric concussion. Clin J Sport Med 2023;33:264–9. doi:10.1097/JSM.0000000000001106
      OpenUrl
    18. ↵
      1. Master CL,
      2. Master SR,
      3. Wiebe DJ, et al
      . Vision and vestibular system dysfunction predicts prolonged concussion recovery in children. Clin J Sport Med 2018;28:139–45. doi:10.1097/JSM.0000000000000507
      OpenUrlPubMed
    19. ↵
      1. Pearce KL,
      2. Sufrinko A,
      3. Lau BC, et al
      . Near point of convergence after a sport-related concussion: measurement Reliability and relationship to Neurocognitive impairment and symptoms. Am J Sports Med 2015;43:3055–61. doi:10.1177/0363546515606430
      OpenUrlCrossRefPubMed
    20. ↵
      1. Swanson MW,
      2. Weise KK,
      3. Dreer LE, et al
      . Academic difficulty and vision symptoms in children with concussion. Optom Vis Sci 2017;94:60–7. doi:10.1097/OPX.0000000000000977
      OpenUrlCrossRef
    21. ↵
      1. Sherry N,
      2. Trbovich A,
      3. Holland C, et al
      . Predictors of poor reading performance in student-athletes following sport-related concussion. Appl Neuropsychol Child 2022;11:364–72. doi:10.1080/21622965.2020.1850449
      OpenUrl
    22. ↵
      1. Laukkanen H,
      2. Scheiman M,
      3. Hayes JR
      . Brain injury vision symptom survey (BIVSS) questionnaire. Optom Vis Sci 2017;94:43–50. doi:10.1097/OPX.0000000000000940
      OpenUrl
    23. ↵
      1. Brahm KD,
      2. Wilgenburg HM,
      3. Kirby J, et al
      . Visual impairment and dysfunction in combat-injured Servicemembers with traumatic brain injury. Optom Vis Sci 2009;86:817–25. doi:10.1097/OPX.0b013e3181adff2d
      OpenUrlCrossRefPubMed
    24. ↵
      1. Capó-Aponte JE,
      2. Urosevich TG,
      3. Temme LA, et al
      . 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
      OpenUrlCrossRefPubMed
    25. ↵
      1. Scheiman M,
      2. Grady MF,
      3. Jenewein E, et al
      . Frequency of Oculomotor disorders in adolescents 11 to 17 years of age with concussion, 4 to 12 weeks post injury. Vision Res 2021;183:73–80. doi:10.1016/j.visres.2020.09.011
      OpenUrlPubMed
    26. ↵
      1. Coiner B,
      2. Pan H,
      3. Bennett ML, et al
      . Functional Neuroanatomy of the human eye movement network: a review and Atlas. Brain Struct Funct 2019;224:2603–17. doi:10.1007/s00429-019-01932-7
      OpenUrl
    27. ↵
      1. Debacker J,
      2. Ventura R,
      3. Galetta SL, et al
      . Neuro-ophthalmologic disorders following concussion. Handb Clin Neurol 2018;158:145–52. doi:10.1016/B978-0-444-63954-7.00015-X
      OpenUrl
    28. ↵
      1. Collins MW,
      2. Kontos AP,
      3. Okonkwo DO, et al
      . Statements of agreement from the targeted evaluation and active management (TEAM) approaches to treating concussion meeting held in Pittsburgh, October 15-16, 2015. Neurosurgery 2016;79:912–29. doi:10.1227/NEU.0000000000001447
      OpenUrlCrossRefPubMed
    29. ↵
      1. Berryman A,
      2. Rasavage K,
      3. Politzer T, et al
      . Brief report—Oculomotor treatment in traumatic brain injury rehabilitation: A randomized controlled pilot trial. Am J Occup Ther 2020;74:7401185050p1–7. doi:10.5014/ajot.2020.026880
      OpenUrl
    30. ↵
      1. Zahid AB,
      2. Hubbard ME,
      3. Lockyer J, et al
      . Eye tracking as a biomarker for concussion in children. Clin J Sports Med 2018;00:1–11.
      OpenUrl
    31. ↵
      1. Mani R,
      2. Asper L,
      3. 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
      OpenUrl
    32. ↵
      1. Mani R,
      2. Ngo S,
      3. Walz J, et al
      . Evaluating the extent of change in near point of convergence in traumatic brain injury: a systematic review and meta-analysis. Brain Inj 2022;36:306–20. doi:10.1080/02699052.2022.2034188
      OpenUrl
    33. ↵
      1. Hunt AW,
      2. Mah K,
      3. Reed N, et al
      . 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
      OpenUrl
    34. ↵
      1. Raghuram A,
      2. Cotter SA,
      3. Gowrisankaran S, et al
      . Postconcussion: receded near point of convergence is not diagnostic of convergence insufficiency. Am J Ophthalmol 2019;206:235–44. doi:10.1016/j.ajo.2019.04.008
      OpenUrl
    35. ↵
      1. Kapoor N,
      2. Ciuffreda KJ
      . Vision disturbances following traumatic brain injury. Curr Treat Options Neurol 2002;4:271–80. doi:10.1007/s11940-002-0027-z
      OpenUrlCrossRefPubMed
    36. ↵
      1. Tricco AC,
      2. Lillie E,
      3. Zarin W, et al
      . PRISMA extension for Scoping reviews (PRISMA-SCR): checklist and explanation. Ann Intern Med 2018;169:467–73. doi:10.7326/M18-0850
      OpenUrlCrossRefPubMed
    37. ↵
      1. Peters MDJ,
      2. Godfrey C,
      3. McInerney P, et al
      . Chapter 11: Scoping reviews (2020 version). In: Aromataris E, Munn Z, eds. JBI Manual for Evidence Synthesis, JBI. 2020. doi:10.46658/JBIMES-20-01

    Supplementary materials

    • Supplementary Data

      This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

    Footnotes

    • Contributors JT, AC, APB, LDG, AM, ADS, TPY, TR and MS conceived and designed the review, and the search strategies. TR and MS were instrumental in guiding the concept and revising the manuscript for critical intellectual content. JT wrote the first draft of the protocol manuscript, AC, APB, LDG, AM, ADS, TPY, TR and MS edited the manuscript. JT revised the draft(s) into the final manuscript. All authors JT, AC, APB, LDG, AM, ADS, TPY, TR and MS read and approved of the final manuscript prior to submission for publication and agree to be accountable for all aspects of the work in ensuring that all questions related to the accuracy and integrity of the work are investigated and resolved.

    • Funding American Academy of Optometry (award/grant no: NA).

    • Competing interests None declared.

    • Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.