ORIGINAL RESEARCH

Gaze Stabilization Test Asymmetry Score as an Indicator of Previous Concussion in a Cohort of Collegiate Football Players Julie A. Honaker, PhD, Robin E. Criter, AuD, Jessie N. Patterson, MS, and Sherri M. Jones, PhD

Objective: Vestibular dysfunction may lead to decreased visual acuity with head movements, which may impede athletic performance and result in injury. The purpose of this study was to test the hypothesis that athletes with history of concussion would have differences in gaze stabilization test (GST) as compared with those without a history of concussion.

Design: Cross-sectional, descriptive. Setting: University Athletic Medicine Facility. Participants: Fifteen collegiate football players with a history of concussion, 25 collegiate football players without a history of concussion. Intervention: Participants completed the dizziness handicap inventory (DHI), static visual acuity, perception time test, active yaw plane GST, stability evaluation test (SET), and a bedside oculomotor examination. Main Outcome Measures: Independent samples t test was used to compare GST, SET, and DHI scores per group, with Bonferroniadjusted alpha at P , 0.01. Receiver operating characteristic curve analysis and area under the curve (AUC) were used to assess the clinical performance of the GST and SET. Results: Athletes with previous concussion had a larger GST asymmetry score [mean (M) = 12.40, SD = 9.09] than those without Submitted for publication September 9, 2013; accepted June 12, 2014. From the Department of Special Education and Communication Disorders, University of Nebraska-Lincoln, Lincoln, Nebraska. Supported by grant from the Department of Defense (to J.A.H. and S.M.J.) and from the American Academy of Audiology (to R.E.C.). J. A. Honaker has received consulting payment from Celerion, Inc. S. M. Jones has received travel reimbursement and honorarium for lectures from the National Institutes of Health, National Institute on Deafness and other Communication Disorders, Legacy Health Systems, Stanford University, and Case Western Reserve University and travel expense reimbursement for the Auditory and Vestibular Dysfunction Research Enhancement Award Program. In addition, she is currently receiving royalties from Plural Publishing for a textbook she co-authored. This work was not supported by a grant; the authors disclosed current funding related to the topic, but the funding did not support the project. The remaining authors report no conflicts of interest. Presented at the Annual Meeting of the Association for Research in Otolaryngology; February 18, 2013; Baltimore, Maryland. Corresponding Author: Julie A. Honaker, PhD, Department of Special Education and Communication Disorders, University of NebraskaLincoln, 271 Barkley Center, Lincoln, NE 68583-0738 (julie.honaker@ unl.edu). Copyright © 2014 Wolters Kluwer Health, Inc. All rights reserved.

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concussion (M = 4.92, SD = 4.67; t (18.70) = 22.955, P = 0.008, 95% CI, 212.79 to 22.18, d = 21.37). Clinical performance of the GST (AUC = 0.77) was better than the SET (AUC = 0.61).

Conclusions: Results suggest peripheral vestibular or vestibular– visual interaction deficits in collegiate athletes with a history of concussion. The results support further research on the use of GST for sport-related concussion evaluation and monitoring.

Clinical Relevance: Inclusion of objective vestibular tests in the concussion protocol may reveal the presence of peripheral vestibular or visual–vestibular deficits. Therefore, the GST may add an important perspective on the effects of concussion. Key Words: gaze stabilization test, vestibulo-ocular reflex, head injury, concussion, postural control, visual acuity (Clin J Sport Med 2015;25:361–366)

INTRODUCTION Sport-related traumatic brain injury is a growing medical concern.1,2 Concussions resulting from direct or indirect impulsive force to the head or neck3,4 can have lasting effects on brain function, balance, and behavior.5 Little is known about the effects of concussion on vestibular function. The primary function of the vestibular system is to encode head motion, which contributes to eye, head, and postural movements.6 Vestibular gravity sensors and reflexes are essential components for postural control and facilitate quiet stance even in the absence of vision.6 Thus, postural control measures with vision denied provide an indirect estimate of vestibular function. Postural control deficits have been documented in the concussion research7–12; however, examination of peripheral and central vestibular dysfunction has been limited. Early work on vestibular consequences after head injury suggests that deficits may occur in the vestibular end organs, nerve, or brainstem pathways, visual, motor, and ocular motor pathways, and cerebellum.13–16 Participation in sports requires adequate postural control and clear vision during active head movements. The vestibular system, in particular, the vestibulo-ocular reflex (VOR), is largely responsible for maintaining clear vision during head motion by producing equal but opposite eye movements relative to head movements.17 Other visual mechanisms including pursuit tracking, saccades, and optokinetic enhance VOR performance.18 This visual–vestibular interaction is imperative to maintain clear vision.18,19 www.cjsportmed.com |

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Head injury could lead to vestibular dysfunction and therefore retinal slippage with head movements, which may impede athletic performance and result in further injury. Even minor disruptions in vestibular function, including visual–vestibular interaction, may increase the likelihood of retinal slippage19 and symptoms of dizziness and imbalance. Therefore, the inclusion of objective visual–vestibular measures may be warranted for concussion assessment. The gaze stabilization test (GST) is a visual–vestibular interaction test that evaluates VOR contributions to gaze stability. Gaze stabilization test determines the maximum yaw plane head velocities (ie, fastest horizontal head movement speed) in degrees per second that an individual can perform and maintain stable vision. A GST asymmetry score reflects differences in average head velocity between rightward and leftward head movements, suggesting asymmetrical gaze impairments of visual–vestibular origin. Goebel et al20 first reported on the clinical utility of GST to reliably delineate patients with vestibular loss from healthy controls, with fair sensitivity (64%) and excellent specificity (93%). Others21–23 have also demonstrated reduced GST velocities in patients with vestibular dysfunction. Gaze stabilization test not only shows promise as a relatively inexpensive and objective tool for vestibular assessment but also as an outcome measure for monitoring recovery from vestibular loss21,22 postconcussion. The purpose of this study was to describe the performance of the GST in a cohort of collegiate football players and to examine effects of previous concussion on outcome parameters of GST. We hypothesized that athletes with a history of concussion would have differences in GST results as compared with those without. Additionally, we compared the clinical performance of GST with the stability evaluation test (SET), a postural control measure similar to the widely accepted Balance Error Scoring System for concussion identification and management. Postural control measures are recommended for concussion assessment,5 and the SET was chosen for its advantages over other measures, including portability and quantifiable measurements. Both the SET and GST can be used to make inferences regarding vestibular function. The SET assesses vestibular function by denying vision, and the GST evaluates the VOR. Thus, our goal was to assess the clinical utility of GST and its usefulness as a complementary measure for concussion identification.

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resulted in exclusion from the study: (1) orthopedic conditions that would interfere with standing balance, (2) disorders limiting horizontal rightward and leftward head movements (ie, cervical range-of-motion in the yaw plane) to less than 20 degrees, (3) acute injuries and/or disorders associated with neck or back pain, or (4) inability to visualize/read optotypes (ie, visual targets for GST) with head stationary at a distance of 10 feet. All volunteers were eligible to participate.

Measures

This study was approved by the University of Nebraska– Lincoln Institutional Review Board (Protocol #12546). Participants were recruited through presentations to the football team and recruitment flyers placed throughout the locker rooms. Specifically, athletes were informed of a volunteer, noncompensated research opportunity evaluating the effects of concussion on brain and balance function. Forty male, collegiate football players (18-23 years) participated. Fifteen athletes reported a history of concussion verified through review of athletic medical records. All participants were seen before the athletic season by 1 of 3 examiners. Any of the following

Self-reported activity restriction due to current symptoms of dizziness was obtained using the Dizziness Handicap Inventory (DHI).24 The DHI is a validated 25-item questionnaire yielding an overall score between 0 and 100 points. Higher DHI scores indicate greater perceived dizziness handicap. Additional anthropometric data regarding athletic performance (ie, weight and height) were also collected. Screening for conjugate eye movements, oculomotor system function (smooth pursuit, saccades, and gaze-evoked nystagmus testing), and normal VOR (horizontal head thrusts and head-shake test) was performed before the GST and SET measures. Micromedical RealEyes xDVR (Micromedical Technologies, Chatham, Illinois) binocular goggles were used to record eye movements. Two researchers reviewed the eye movement recordings and classified each as normal or abnormal; a third masked researcher also evaluated the recordings (interrater agreement across the 3 reviewers was 100%). Postural stability was assessed using the SET on the VSR Sport (NeuroCom International, Clackamas, Oregon) force plate (18 · 30 · 2 inches). Individuals completed 3 postural stances on both firm surface and dense foam: feet together, single-leg stance, and tandem stance (heel of the dominant foot touching the toe of the nondominant foot)25; center of gravity and average body sway in degrees per second were calculated. Throughout each subtest, participants maintained hands on hips and eyes closed. Each subtest ended after 20 seconds or when a balance error was observed.26 Errors included the participant removing one or both hands from the hips, touching another object, moving a foot out of position, opening eyes, or losing balance (ie, fall reaction). Average sway velocity of all 6 conditions resulted in a composite SET score. Static visual acuity (SVA), perception time test (PTT), and computerized GST were measured using the Neurocom VSR Sport (NeuroCom International). Participants sat in a sturdy chair exactly 10 feet from a laptop screen. The SVA was evaluated first. With the head still, the participant verbally indicated the E optotype orientation (ie, the direction of the legs of the E) when it appeared. Based on the Parameter Estimation Sequential Testing (PEST) algorithm, the smallest optotype correctly identified at 60% (3 of 5 successive trials) was recorded in log of the minimal angle of resolution (logMAR). Optotype size was set to 0.2 logMAR above the established SVA value to complete PTT and GST. For PTT, the optotype appeared for various lengths of time in milliseconds to determine the fastest threshold based on the PEST algorithm. The PTT scores #60 milliseconds were considered within normal range based on age-related normative values.27 Finally, GST was tested actively (ie, the participant moved his

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MATERIALS AND METHODS Subjects

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own head). Passive testing was used only if deemed necessary by the examiner to maintain appropriate head velocity and amplitude. The GST quantified the maximum head movement velocities at which the participant was able to maintain stable visual acuity. A head mounted rate sensor (InertiaCube2+, Sourceless 3DOF Tracker, InterSense Inc, Billerica, Massachusetts) monitored displacement of the head amplitude (ie, horizontal head movements of 20 degrees to the right and left) and head velocity. The participant was instructed to slowly increase head velocity until the optotype appeared on the screen, follow on-screen visual indicators to maintain consistent head displacement to the right and left, and to reach a trigger head velocity. The head velocity systematically increased based on correct optotype orientation response until threshold was reached (maximum yaw plane head velocity in degrees per second). All participants completed adequate practice trials to ensure compliance with the above measures.

Data Analysis Descriptive statistics [mean (M), standard deviation (SD), and range] for average yaw plane GST scores, GST asymmetry scores, SET composite scores, DHI, and anthropometric data were calculated for both groups (those with concussion history and those without concussion history). Independent samples t test was used to compare GST, SET, and DHI scores per group. Effect size (Cohen d) was calculated for each comparison (0.2 = small effect, 0.5 = medium effect, and .0.8 = large effect).28 Fisher exact tests were used to test for differences in the proportion of athletes with and without a history of concussion and normal versus abnormal bedside oculomotor and VOR function tests. Receiver operating characteristic (ROC) curve analysis was conducted to evaluate the sensitivity and specificity of the GST asymmetry score.29 Area under the curve (AUC) analysis, an index of test accuracy,30 was calculated to measure the overall performance of GST asymmetry versus SET composite score for categorizing the concussion groups. Area under the curve values closer to 1.0 indicate superior test accuracy for group discrimination.30 SPSS version 22.0 for Windows (SPSS, Inc., Chicago, Illinois) and MedCalc for Windows, version 12.7.10 (MedCalc Software, Ostend, Belgium) were used for all statistical procedures. Bonferroni adjusted statistical significance was set at P , 0.01.31

RESULTS Data analysis was based on 15 athletes (age, M = 20.93 years, SD = 1.22) with previous concussion and 25 athletes (age, M = 20.44 years, SD = 1.39) without concussion. Time since reported concussion ranged from 3 months to 9 years (M = 2.15 years, SD = 2.26). Among the athletes with previous concussion, 13% (n = 2) reported 2 concussions, 13% (n = 2) reported 3 concussions, and 6% (n = 1) reported 4 concussions. No significant differences were observed based on anthropometric characteristics between the athletes with previous concussion (height, M = 74.20 inches, SD = 2.81; weight, M = 243.07 lbs, SD = 45.34) and the athletes without concussion (height, M = 74.88 inches, SD = 2.32; weight, M = 243.16 lbs, SD = 38.85); history of concussion was the only distinguishing group feature. Oculomotor and VOR Copyright © 2014 Wolters Kluwer Health, Inc. All rights reserved.

GST Asymmetry Score

function screening revealed abnormalities for both groups (Table 1). Fisher exact tests revealed no statistically significant differences in the distribution of normal versus abnormal bedside oculomotor and VOR function measures based on those with previous concussion versus those without concussion. All participants showed average GST head velocity scores within the normal range (Table 2),20,22,27 and no significant differences were seen between groups for rightward [t (38) = 20.385, P = 0.702, 95% confidence interval (CI), 225.54 to 17.38, d = 20.12] or leftward [t (37) = 0.839, P = 0.407, 95% CI, 211.84 to 28.59, d = 0.28] GST velocities (Table 2). In contrast, athletes with a history of concussion demonstrated a significantly larger GST asymmetry score than those without concussion [t (18.70) = 22.955, P = 0.008, 95% CI, 212.79 to 22.18, d = 21.37]. The resultant effect size (d = 21.37) exceeded the guideline for a large effect (d = 0.80)28 (Figure 1, Table 2). No significant differences were observed between groups for SET composite scores [t (38) = 20.979, P = 0.334, 95% CI, 20.76 to 0.26, d = 20.31; Table 2]. Additionally, no significant difference was observed between groups based on DHI total score [t (14.42) = 21.051, P = 0.311, 95% CI, 28.98 to 3.06, d = 20.55; Table 2]. The range of DHI scores for those with previous concussion was much wider than the comparison group, with 1 participant reporting a DHI score of 42 points. Data were reanalyzed excluding this participant; significant differences were still observed between groups for the GST asymmetry value [t (16.95) = 22.997, P = 0.008, 95% CI, 213.53 to 22.35, d = 21.46]. No significant differences were observed between the groups based on GST leftward and rightward velocities and SET composite score. Furthermore, there was no significant correlation observed between time since concussion and GST asymmetry score or number of previous concussions and GST asymmetry score. The GST asymmetry score demonstrated the larger AUC (AUC, 0.77; 95% CI, 0.61-0.89; P = 0.0007), concluding that the AUC under the ROC curve was significantly different from 0.5 (chance performance) and the GST asymmetry score was able to distinguish between the 2 groups. In contrast, SET composite score demonstrated an AUC closer to 0.5 (AUC, 0.61; 95% CI, 0.44-0.76; P = 0.2423). A GST criterion value of .13% yielded 47% sensitivity and 96% specificity (Figure 2). Additionally, a high likelihood ratio (LR) was shown (LR, 11.20; 95% CI, 78.9-99.9), suggesting that an asymmetry score .13% is highly associated with a history of previous concussion. Although 47% sensitivity is not optimal for screening performance, setting the GST asymmetry value to .3% would improve sensitivity (80%) but would result in reduction of test specificity (54%) and LR (1.7; 95% CI, 29.1-70.9).

DISCUSSION The results reported herein suggest the possibility of occult peripheral vestibular or vestibular–visual interaction deficits in collegiate athletes with a history of concussion. Head injury has been reported to affect vestibular structures and relays13–16; this disruption may account for debilitating symptoms, acute postural instability, and inadequate compensatory www.cjsportmed.com |

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TABLE 1. Comparison of the Number of Athletes With Abnormal Bedside Oculomotor and Vestibular Test Findings Based on the History of Concussion Groups Bedside Oculomotor and Vestibular Examination Smooth pursuit Saccades Gaze stability with fixation Gaze stability without fixation Horizontal head thrust Horizontal head shake

Previous Concussion (n = 15), n (%) 2 3 1 5 2 3

(13) (20) (7) (33) (13) (20)

No Concussion (n = 25), n (%) 4 7 1 7 2 3

(16) (28) (4) (28) (8) (12)

Only subjective determination of eye movements was indicated; bedside video eye movement recordings were not quantified.

responses to head movements. In the acute phase, errors in the vestibular–visual system can produce retinal slippage and decreased visual acuity during dynamic activities.19 The central nervous system is highly adaptable and able to compensate after loss of peripheral vestibular function resulting in normal postural control and symptom resolution.32 Even though compensation acts to recalibrate central neural activity, patients with chronic peripheral vestibular loss may have lasting VOR abnormalities, including reduced gain, abnormal timing, and asymmetry of the response during quick head movements.33 When sufficiently tested, the presence of peripheral vestibular loss becomes visible upon clinical examination. Traumatic brain injury can also result in a myriad of potentially persistent problems within the visual system that may be overlooked in the acute postinjury phase.34 The VOR requires both peripheral and central pathways of the visual–vestibular system to be intact for proper gaze stabilization. The GST, which evaluates both vestibular and visual systems, showed an asymmetry, suggesting impairment of the visual–vestibular system. Thus, further investigation of visual–vestibular interactions postconcussion is warranted. The GST was shown to better classify athletes based on history of previous concussion than a postural control measure. This is not surprising given the research showing that postural control measures may evidence abnormalities only in the acute phase of head injury and typically return to baseline levels

within 7 to 10 days after injury.11,35 Specifically, Peterson et al35 evaluated 28 collegiate athletes with concussion and a control group of 18 athletes without concussion. Measures of processing speed and composite sensory organization test (SOT) score were significantly poorer in the postconcussion athletes at days 1, 2, and 10 postinjury. However, the SOT vestibular ratio (calculated with the mean condition 5 scores over the mean condition 1 scores) was significantly different for only days 1 and 2. Thus, GST may add an important perspective at time points beyond the acute phase. One limitation of the present study is the self-reported history of concussion. The definition of concussion, including clinical sequelae and objective signs, has undergone many changes over time. Furthermore, athletes often attempt to mask signs and symptoms of head injury, may be unwilling to report such a history, or may not recognize that they have experienced a concussion.36 Participants in the current study were asked about history of head injury requiring medical attention (ie, concussion), and we confirmed the selfreported concussion history with athletic medical records. Therefore, we felt confident that athletes were placed into appropriate groups. The use of a standardized method of recording concussions is warranted for future evaluations. Another limitation is the inclusion of only male, collegiate football players, limiting generalization to other ages, sports, or gender. Additionally, the variability in time since previously reported concussion was large. Future research should aim to recruit individuals with more recent concussions in addition to a larger sample size of diverse athletes. One aim of our future work is to prospectively evaluate functional changes to the vestibular system in athletes diagnosed with concussion. In addition, there is ongoing work to gather additional objective vestibular laboratory test results (1) to correlate with the present GST findings and (2) to quantitatively confirm the abnormal bedside measures reported herein. The role of re-injury to the vestibular system due to concussion is also uncertain because this may introduce new deficits or decompensation of existing deficits leading to further vestibular symptoms (eg, dizziness and imbalance) and clinical signs (postural instability and decreased visual acuity with head movements). We are cognizant that the criterion GST asymmetry score .13% yielding sensitivity of 47% is not optimal for

TABLE 2. Comparison of GST Leftward and Rightward Velocity Values, GST Asymmetry Scores, and SET Composite Scores (Mean 6 SD and Range) for Collegiate Football Players With and Without a History of Concussion Athletes With a History of Concussion (n = 15) Mean 6 SD (Range) GST asymmetry, % GST velocity leftward, degrees per second GST velocity rightward, degrees per second SET composite score DHI score

Athletes Without a History of Concussion (n = 25) Mean 6 SD (Range)

t Test

12.40 6 9.09 (1-30) 147.00 6 34.52 (81-203)

4.92 6 4.67 (0-18) 155.38 6 27.44 (95-190)

22.955* 0.839

155.00 6 37.10 (97-211)

150.921 6 29.42 (96-190)

20.385

2.99 6 0.63 (1.70-3.90) 3.60 6 10.80 (0-42)

2.74 6 0.84 (1.40-4.10) 0.64 6 1.70 (0-8)

0.979 0.311

*P , 0.01.

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GST Asymmetry Score

a combined protocol may increase the overall sensitivity, thus reducing the possibility of missing cases. Additionally, the overall sensitivity of GST may improve if studied in acute cases. Future studies should also determine fatigue effects and potential learning effects with test–retest evaluation. Standardization of the testing method is necessary to compare results and provide more widespread use across clinics. The GST is a time-efficient and inexpensive procedure, and further research may warrant its use for sport-related concussion evaluation and monitoring. REFERENCES

FIGURE 1. Box plot comparing GST asymmetry scores shows that athletes with a history of concussion have increased mean scores as compared with athletes without a history of concussion.

clinical screening purposes given the larger number of potential athletes who would be missed for concussion identification; however, the stringent criterion with high specificity (96%) indicates that those who test negative will likely not have previous concussion.37 Ideally, GST could be used in a parallel protocol (ie, all measures administered at the same time) and any positive result on the protocol measures would be considered positive for concussion.37 Using the GST in

FIGURE 2. Receiver operating characteristic curve plotting test performance of GST. A GST asymmetry score criterion value of .13% (sensitivity 47%, specificity 96%) was identified for classifying athletes with and without a history of previous concussion. Copyright © 2014 Wolters Kluwer Health, Inc. All rights reserved.

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23. Whitney SL, Marchetti GF, Pritcher M, et al. Gaze stabilization and gait performance in vestibular dysfunction. Gait Posture. 2009;29: 194–198. 24. Jacobson GP, Newman CW. The development of the dizziness handicap inventory. Arch Otolaryngol Head Neck Surg. 1990;116:424–427. 25. Riemann BL, Guskiewicz KM. Effects of mild head injury on postural stability as measured through clinical balance testing. J Athl Train. 2000; 35:19–25. 26. NeuroCom International. VSR sport: play a smarter game. http://www. playasmartergame.com. Accessed May 13, 2013. 27. Honaker JA, Shepard NT. Age effect on the gaze stabilization test. J Vestib Res. 2010;20:357–362. 28. Cohen J, ed. Statistical Power Analysis for the Behavioral Sciences. 2nd ed. Hillsdale, NJ: Erlbaum; 1988. 29. Hanley JA, McNeil BJ. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology. 1982;143:39–36. 30. DeLong ER, DeLong DM, Clarke-Pearson DJ. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics. 1988;44:837–845.

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Gaze Stabilization Test Asymmetry Score as an Indicator of Previous Concussion in a Cohort of Collegiate Football Players.

Vestibular dysfunction may lead to decreased visual acuity with head movements, which may impede athletic performance and result in injury. The purpos...
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