Deficits in saccades and smooth-pursuit eye movements in adults with traumatic brain injury: a systematic review and meta-analysis

ABSTRACT Purpose: To conduct a review of literature and quantify the effect that traumatic brain injury (TBI) has on oculomotor functions (OM). Methods: A systematic review and meta-analysis was conducted from papers that objectively measured saccades and smooth-pursuit eye movements in mild and severe TBI. Results: The overall impact of TBI on OM functions was moderate and significant with an effect size of 0.42 from 181 OM case-control comparisons. The heterogeneity, determined using the random effect model, was found to be significant (Q (180) = 367, p < 0.0001, I2 = 51) owing to the variety of OM functions (reflexive saccades, antisaccades, memory-guided saccades, self-paced saccades and pursuits) measured and varying post-injury periods.The overall effect on OM functions were similar in mild and severe TBI despite differences in combined effect size of various OM functions. OM functions involving complex cognitive skills such as antisaccades (in mild and severe TBI) and memory-guided saccades (in mild TBI) were the most adversely affected, suggesting that OM deficits may be associated with cognitive deficits in TBI. Conclusion: TBI often results in long-standing OM deficits. Experimental measures of OM assessment reflect neural integrity and may provide a sensitive and objective biomarker to detect OM deficits following TBI.

[1]  Steven Scott,et al.  Clinical practice guideline: Management of Concussion/Mild Traumatic Brain Injury , 2009 .

[2]  Saumil S. Patel,et al.  Detection of Subtle Cognitive Changes after mTBI Using a Novel Tablet-Based Task. , 2016, Journal of neurotrauma.

[3]  Glenn Curtiss,et al.  Long-term morbidities following self-reported mild traumatic brain injury , 2007, Journal of clinical and experimental neuropsychology.

[4]  K. Ciuffreda,et al.  Occurrence of oculomotor dysfunctions in acquired brain injury: a retrospective analysis. , 2006, Optometry.

[5]  Steven P Broglio,et al.  National Athletic Trainers' Association position statement: management of sport concussion. , 2014, Journal of athletic training.

[6]  Michelle Keightley,et al.  Oculomotor-Based Vision Assessment in Mild Traumatic Brain Injury: A Systematic Review , 2016, The Journal of head trauma rehabilitation.

[7]  H. Levin,et al.  Diagnosis, prognosis, and clinical management of mild traumatic brain injury , 2015, The Lancet Neurology.

[8]  Richard D. Jones,et al.  Motor deficits and recovery during the first year following mild closed head injury , 2006, Brain injury.

[9]  Glenn Curtiss,et al.  Factors moderating neuropsychological outcomes following mild traumatic brain injury: A meta-analysis , 2005, Journal of the International Neuropsychological Society.

[10]  I. Selesnick,et al.  Objectifying eye movements during rapid number naming: Methodology for assessment of normative data for the King–Devick test , 2016, Journal of the Neurological Sciences.

[11]  M. Ettenhofer,et al.  Saccadic Impairment Associated With Remote History of Mild Traumatic Brain Injury. , 2016, The Journal of neuropsychiatry and clinical neurosciences.

[12]  S. Galetta,et al.  Diagnostic Tests for Concussion: Is Vision Part of the Puzzle? , 2015, Journal of neuro-ophthalmology : the official journal of the North American Neuro-Ophthalmology Society.

[13]  N. Shimizu [Neurology of eye movements]. , 2000, Rinsho shinkeigaku = Clinical neurology.

[14]  T. Schweizer,et al.  Saccadic Eye Movements in Mild Traumatic Brain Injury: A Pilot Study OPEN ACCESS , 2014, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[15]  Richard D. Jones,et al.  Eye movement and visuomotor arm movement deficits following mild closed head injury , 2003 .

[16]  Jian-ning Zhang,et al.  Epidemiology of Traumatic Brain Injury over the World: A Systematic Review , 2016 .

[17]  Peter Herscovitch,et al.  A Review of the Effectiveness of Neuroimaging Modalities for the Detection of Traumatic Brain Injury. , 2015, Journal of neurotrauma.

[18]  H. Levin,et al.  The frontal lobes and traumatic brain injury. , 1994, The Journal of neuropsychiatry and clinical neurosciences.

[19]  Henk van Rhee,et al.  User manual for Meta-Essentials: Workbooks for meta-analyses , 2018 .

[20]  P. Siddall,et al.  Biopsychosocial perspective on a mechanisms-based approach to assessment and treatment of pain following spinal cord injury. , 2009, Journal of rehabilitation research and development.

[21]  D. Altman,et al.  Measuring inconsistency in meta-analyses , 2003, BMJ : British Medical Journal.

[22]  M. Walker,et al.  Imaging Modalities in Mild Traumatic Brain Injury and Sports Concussion , 2011, PM & R : the journal of injury, function, and rehabilitation.

[23]  Minah Suh,et al.  Increased oculomotor deficits during target blanking as an indicator of mild traumatic brain injury , 2006, Neuroscience Letters.

[24]  Charles H Tator,et al.  Longitudinal Study of Postconcussion Syndrome: Not Everyone Recovers. , 2017, Journal of neurotrauma.

[25]  Amanda R. Rabinowitz,et al.  Intraindividual cognitive variability before and after sports-related concussion. , 2013, Neuropsychology.

[26]  Richard D. Jones,et al.  Impaired eye movements in post-concussion syndrome indicate suboptimal brain function beyond the influence of depression, malingering or intellectual ability. , 2009, Brain : a journal of neurology.

[27]  H. Dhaliwal,et al.  The International Incidence of Traumatic Brain Injury: A Systematic Review and Meta-Analysis , 2016, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[28]  V. Nell,et al.  An extended Glasgow Coma Scale (GCS-E) with enhanced sensitivity to mild brain injury. , 2000, Archives of physical medicine and rehabilitation.

[29]  Andy P Field,et al.  How to do a meta-analysis. , 2010, The British journal of mathematical and statistical psychology.

[30]  M. Tartaglia,et al.  Assessment of Oculomotor Function in Patients With Postconcussion Syndrome: A Systematic Review , 2017, The Journal of head trauma rehabilitation.

[31]  Richard D. Jones,et al.  Saccade sequences as markers for cerebral dysfunction following mild closed head injury. , 2002, Progress in brain research.

[32]  Ingram Olkin,et al.  Estimation of a Single Effect Size: Parametric and Nonparametric Methods , 1985 .

[33]  Jacob Cohen,et al.  A power primer. , 1992, Psychological bulletin.

[34]  T. Schweizer,et al.  Saccadic eye movements in mild traumatic brain injury: a pilot study. , 2014, The Canadian journal of neurological sciences. Le journal canadien des sciences neurologiques.

[35]  Josef Ling,et al.  Functional connectivity in mild traumatic brain injury , 2011, Human brain mapping.

[36]  M. Wald,et al.  Traumatic brain injury in the United States; emergency department visits, hospitalizations, and deaths, 2002-2006 , 2010 .

[37]  V. Coronado,et al.  Methodological issues and research recommendations for mild traumatic brain injury: the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. , 2004, Journal of rehabilitation medicine.

[38]  T. Schweizer,et al.  Antisaccadic Eye Movements Are Correlated with Corpus Callosum White Matter Mean Diffusivity, Stroop Performance, and Symptom Burden in Mild Traumatic Brain Injury and Concussion , 2016, Front. Neurol..

[39]  J. Sweeney,et al.  Procedural Learning Impairments Identified via Predictive Saccades in Chronic Traumatic Brain Injury , 2010, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[40]  M. Hallett,et al.  Functional neuroimaging of acute oculomotor deficits in concussed athletes , 2014, Brain Imaging and Behavior.

[41]  Jamshid Ghajar,et al.  Clinical evaluation of concussion: the evolving role of oculomotor assessments. , 2016, Neurosurgical focus.

[42]  Lora T. Likova,et al.  Deficits in the Activation of Human Oculomotor Nuclei in Chronic Traumatic Brain Injury , 2015, Front. Neurol..

[43]  Tania B. Huedo-Medina,et al.  Assessing heterogeneity in meta-analysis: Q statistic or I2 index? , 2006, Psychological methods.

[44]  Jennine Kirby,et al.  Visual Impairment and Dysfunction in Combat-Injured Servicemembers With Traumatic Brain Injury , 2009, Optometry and vision science : official publication of the American Academy of Optometry.

[45]  Bruce D. McCandliss,et al.  Deficits in predictive smooth pursuit after mild traumatic brain injury , 2006, Neuroscience Letters.

[46]  Li-Shan Chou,et al.  Attentional disengagement dysfunction following mTBI assessed with the gap saccade task , 2007, Neuroscience Letters.

[47]  D. Moher,et al.  Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement , 2009, BMJ : British Medical Journal.

[48]  Kenneth J Ciuffreda,et al.  Versional eye tracking in mild traumatic brain injury (mTBI): Effects of oculomotor training (OMT) , 2014, Brain injury.

[49]  Matthew A. Eisenberg,et al.  Duration and Course of Post-Concussive Symptoms , 2014, Pediatrics.

[50]  A. Maas,et al.  The reliability of the Glasgow Coma Scale: a systematic review , 2015, Intensive Care Medicine.

[51]  L. Crevits,et al.  Antisaccades and remembered saccades in mild traumatic brain injury , 2000, Journal of Neurology.

[52]  J R Hodges,et al.  Cognitive assessment for clinicians , 1994, Journal of Neurology, Neurosurgery & Psychiatry.

[53]  J. Fielding,et al.  Cognition and Eye Movements: Assessment of Cerebral Dysfunction , 2012, Journal of neuro-ophthalmology : the official journal of the North American Neuro-Ophthalmology Society.

[54]  Patrick Nalepka,et al.  Quantification and analysis of saccadic and smooth pursuit eye movements and fixations to detect oculomotor deficits , 2017, Behavior research methods.

[55]  J. Ghajar,et al.  Predictive visual tracking: specificity in mild traumatic brain injury and sleep deprivation. , 2014, Military medicine.

[56]  N. Landre,et al.  Cognitive functioning and postconcussive symptoms in trauma patients with and without mild TBI. , 2006, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[57]  Jeruza L Neyeloff,et al.  Meta-analyses and Forest plots using a microsoft excel spreadsheet: step-by-step guide focusing on descriptive data analysis , 2012, BMC Research Notes.

[58]  D Kushner,et al.  Mild traumatic brain injury: toward understanding manifestations and treatment. , 1998, Archives of internal medicine.

[59]  John A Sweeney,et al.  Oculomotor Function in Chronic Traumatic Brain Injury , 2007, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[60]  Laura J. Balcer,et al.  Ocular motor assessment in concussion: Current status and future directions , 2016, Journal of the Neurological Sciences.

[61]  Tim J Anderson,et al.  Eye movements in neurodegenerative diseases. , 2016, Current opinion in neurology.

[62]  Lippincott Williams Wilkins,et al.  Practice Parameter , 1997, Neurology.

[63]  G. Manley,et al.  Classification of traumatic brain injury for targeted therapies. , 2008, Journal of neurotrauma.

[64]  R. Cameron Craddock,et al.  Neuroimaging after mild traumatic brain injury: Review and meta-analysis☆ , 2014, NeuroImage: Clinical.

[65]  J. Ponsford,et al.  Cerebral control of saccades and neuropsychological test results after head injury , 1997, Journal of Clinical Neuroscience.

[66]  K. Hall,et al.  Incidence and treatment of visual dysfunction in traumatic brain injury. , 1993, Brain injury.

[67]  K. Guskiewicz,et al.  National Athletic Trainers' Association Position Statement: Management of Sport-Related Concussion. , 2004, Journal of athletic training.

[68]  Roland R. Lee,et al.  Filling in the gaps: Anticipatory control of eye movements in chronic mild traumatic brain injury , 2015, NeuroImage: Clinical.

[69]  J. Langlois,et al.  Traumatic brain injury in the United States; emergency department visits, hospitalizations, and deaths , 2006 .

[70]  Joanna R. Wares,et al.  Differential Eye Movements in Mild Traumatic Brain Injury Versus Normal Controls , 2015, The Journal of head trauma rehabilitation.

[71]  L. Osternig,et al.  Cancelling planned actions following mild traumatic brain injury , 2007, Neuropsychologia.

[72]  M. Hallett,et al.  Follow-up evaluation of oculomotor performance with fMRI in the subacute phase of concussion , 2015, Neurology.

[73]  Ashley Safford,et al.  Eye-Tracking Technology for Estimation of Cognitive Load After Traumatic Brain Injury , 2015, HCI.