Otology & Neurotology 36:746Y754 Ó 2014, Otology & Neurotology, Inc.
Comparison of the Gaze Stabilization Test and the Dynamic Visual Acuity Test in Unilateral Vestibular Loss Patients and Controls *Courtney C. J. Voelker, †Amelia Lucisano, *Dorina Kallogjeri, *Belinda C. Sinks, and *Joel A. Goebel *Dizziness and Balance Center, Department of OtolaryngologyYHead and Neck Surgery, ÞWashington University School of Medicine, St. Louis, Missouri, U.S.A.
Objective: Compare the dynamic visual acuity test (DVAT) and gaze stabilization test (GST) in patients with unilateral vestibular loss (UVL) and healthy control subjects using a novel computerized testing system prototype. Study Design: Cross-sectional study. Setting: Tertiary academic referral laboratory. Patients: Seventeen UVL patients (median age 62 yr) with bithermal caloric asymmetry (Q49%) or ablative surgery and 17 control subjects (median age 57 yr). Intervention(s): Diagnostic. Main Outcome Measure(s): Comparison of DVAT and GST results during self-generated sinusoidal head movements using transient unpredictable target presentations less than 95 milliseconds in duration. Results: UVL patients had significantly higher DVAT scores toward the lesioned side compared with controls (p = 0.001) and the non-lesioned side (p = 0.003), but the non-lesioned side was not significantly different from controls (p = 0.157). When comparing GST scores, UVL patients required a slower head velocity
to maintain visual acuity with movement toward the lesioned side compared with controls (p G 0.001) and the non-lesioned side (p = 0.004). In addition, UVL patients had significantly lower scores toward the non-lesioned side (p = 0.002) compared to controls. ROC curve analysis identified optimal thresholds for abnormal test results to discriminate the lesioned side from controls. A DVAT score greater than or equal to 0.3 $logMAR provided 65% sensitivity and 88% specificity while a GST score less than or equal to 95 degrees/s provided 71% sensitivity and 100% specificity. When GST results were normal, adding DVAT increased overall sensitivity to 88% with 88% specificity. Conclusions: Both GST and DVAT demonstrated reduced gaze stabilization toward the lesioned side in the patient group compared with normal controls. Performing GST first and utilizing DVAT when GST was normal provides optimal identification of patients with vestibular dysfunction. Key Words: Dynamic visual acuity testVGaze stabilization testVVestibular testing.
Maintenance of gaze stability during head movement is a complex interaction between the vestibulo-ocular reflex (VOR), foveal smooth pursuit, optokinetic stimulation of the peripheral retina, and the cervico-ocular reflex. At lower frequencies (G2 Hz) and peak velocities (G60Y90 degrees/s), the central oculomotor mechanisms are dominant. However, at higher frequencies and velocities, the VOR becomes the primary mechanism for maximizing visual acuity by limiting retinal slip. Standard tests of vestibular function
(e.g., caloric and rotational stimulation) are useful in documenting deficits in low-frequency, horizontal semicircular canal VOR function. However, these tests fail to assess the VOR contribution to gaze stability at higher frequencies within the range of everyday head movements (1Y4 Hz). Computerized dynamic visual acuity testing (DVAT) has been developed and studied as a method of determining gaze stability during head movements at higher frequencies (92 Hz) and peak velocities ranging from greater than 50 degrees/s (1) to greater than 120 degrees/s (2Y8). DVAT compares the relative loss of visual acuity between head-still and head-moving conditions (measured in logarithmic Minimal Angle of Resolution or logMAR). This is accomplished by measuring the change in the visual target size that a participant can accurately recognize during head rotation compared to the static visual acuity (SVA) in the resting condition. The utility
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Address correspondence and reprint requests to Joel A. Goebel, M.D., Dizziness and Balance Center, Department of OtolaryngologyYHead and Neck Surgery, Washington University School of Medicine, St Louis, MO, U.S.A.; E-mail: [email protected] The authors disclose no conflicts of interest. P30 NIH Grant pays for part of biostatistician’s time to support research in the department; the grant does not specifically relate to the project.
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GST AND DVAT IN UVL PATIENTS VS. CONTROLS of the DVAT has been well documented in patients with unilateral vestibular dysfunction or bilateral vestibular loss as well as in the elderly population (1,2,6Y11). One concern, however, is the inherent visual challenge associated with changing target size separate from the effects of the VOR. Another potential issue is the use of a short duration of target presentation (G100 ms) in participants with prolonged perception times who may fail to correctly identify the target resulting from inadequate target presentation time rather than a VOR deficiency. Furthermore, published DVAT protocols have studied both predictable active and unpredictable passive head movements to assess the possible effect of prediction for the generation of preprogrammed (covert) or refixation (overt) saccadic eye movements to maintain the target on the fovea. The authors concluded that test protocols with unpredictable target presentation resulted in reduced dynamic visual acuity in subjects with vestibular dysfunction resulting from avoidance of preprogrammed saccadic eye movements (9,11). The gaze stabilization test (GST) was first described as an alternative method to document gaze stability during head motion without changing target size (2). Current GST protocols use a fixed target at a size of 0.2 to 0.3 logMAR (2Y3 lines on a standard Snellen chart) above the participant’s static visual acuity and measures the peak head velocity achieved while continuing to maintain the capability of accurately identifying target orientation (12,13). This study was designed to investigate the relative ability of the GST and DVAT using active headshaking and unpredictable target presentation to detect unilateral vestibular dysfunction. GST and DVAT results were compared between patients with unilateral vestibular loss (UVL) (defined in this study as Q49% caloric asymmetry or a history of an ablative procedure) and normal control subjects. A prototype mirrored tunnel system was used to create a longer viewing distance and more uniform target illumination. Both DVAT and GST protocols used a continuous sinusoidal, self-generated head movements as well as unpredictable timing and head direction for target presentation to minimize the effect of covert non-vestibular predictive eye movements for gaze stabilization. Furthermore, the duration of target presentation was adjusted based on documented baseline minimal perception time (MPT) to a maximum of 95 milliseconds to minimize the ability of overt saccades to refixate and identify the optotype.
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of Medicine. All participants were 18 years of age or older. Participants were excluded from the study if they had a history of cervical dysfunction that prevented them from moving their head rapidly, severe visual impairment or blind spots in their visual field, or a history of a central nervous system disorder.
Test Protocol All participants were tested with best-corrected vision using a prototype mirrored tunnel system (NeuroCom International, Clackamas, OR). Participants were seated so that the bridge of their nose was 1.5 feet from the start of the tunnel system, and the visual target appeared on a mirror monitor display as if it were 13 feet from the participant (Fig. 1). Because of the long target distance, changes in viewing angle caused by variation in participant height were minimal and no adjustment was required. In an attempt to standardize luminescence and to minimize distraction to the participant, the room lights were turned off. The only ambient light originated from the operator’s console, which was positioned behind the participant. To monitor head direction and velocity, participants were fitted with the InertiaCube2+ precision inertial orientation sensor (InterSense, Incorporated, Billerica, MA) (Fig. 1). All participants performed static acuity and minimum perception time (MPT) tests first, and the GST and DVAT were randomly placed in the third or fourth test positions to minimize learning or fatigue effect. For both DVAT and GST, the modified PEST algorithm was used to determine threshold values by using the participant’s previous response to set the relevant stimulus parameters (visual target size with DVAT and head velocity for target presentation with GST) for each subsequent trial to determine threshold values (14). For both DVAT and GST, three separate trials were conducted and the best performance threshold values were recorded for each trial. Participants were allowed rest periods if desired making the test session last from 60 to 90 minutes. Head movement was monitored visually
SUBJECTS AND METHODS Subjects This study was approved by the Human Research Protection Office of Washington University in Saint Louis. Patients with documented unilateral vestibular dysfunction based on greater than or equal to 49% bithermal binaural caloric test asymmetry on closed loop irrigation were recruited from the clinical practice of the principal investigator (J.A.G.). This cutoff for caloric asymmetry was chosen to clearly exceed the clinical standard of greater than 30% asymmetry accepted by most laboratories using this caloric stimulus. Control subjects were recruited from the Volunteer for Health Database at Washington University School
FIG. 1. Prototype mirrored tunnel system (NeuroCom International, Clackamas, OR). Participants were fitted with a headmounted, inertial orientation sensor to monitor head direction and velocity. They were placed so that the visual target appeared on a mirror monitor display as if it were 13 feet from the participant. The room lights were turned off, and the only light in the room came from the operator’s console, which was positioned behind the participant to avoid visual distraction. Otology & Neurotology, Vol. 36, No. 4, 2015
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by the operator throughout testing, and participants were verbally reinstructed as needed.
Static Visual Acuity (SVA) Static visual acuity (SVA) was measured by displaying a single optotype (letter ‘‘E’’) in the center of the monitor starting at 0.3 logMAR, which is the Snellen equivalency of 20/40. The optotype appeared for 1 second and randomly changed orientation and size with each trial, and the participant was asked to verbally identify the target orientation (up, down, left, right) until a threshold acuity was identified. In contrast to other DVAT studies, static visual acuity (SVA) determination in this study included testing below 0.0 logMAR. The SVA for each subject was then used to set target size for the subsequent DVAT and GST trials.
Minimum Perception Time (MPT) The minimum perception time (MPT) is the shortest time (ms) an optotype can be presented on the screen so that the participant could accurately identify its orientation with the head stationary. Participants focused on a box that appeared in the center of the computer screen for 2 seconds. The box disappeared and after an interval of 250 milliseconds, an ‘‘E’’ optotype 0.25 logMAR above the participant’s SVA appeared in its place for 250 milliseconds and participants were instructed to verbally identify target orientation which was entered into the program by the operator. The computer then presented additional targets with increasingly shorter presentation times until a minimum threshold was reached (14Y19). The MPT set the optotype display time parameters for the remainder of the tests. If the MPT was less than or equal to 40 milliseconds, the optotype display time was varied randomly between 40 and 75 milliseconds. If the MPT was greater than 40 milliseconds, the optotype display time varied between the MPT and MPT + 35 milliseconds up to a maximum of 95 milliseconds to minimize the capability of refixation saccades for target identification during testing.
Gaze Stabilization Test (GST) The GST quantifies the maximum head velocity at which a patient is able to maintain visual acuity. In this study, the GST measured the maximum head velocity at which a participant could accurately identify the fixed size optotype orientation. Participants were instructed to conduct smooth sinusoidal headshakes in the yaw plane at a frequency greater than 2 Hz and less than 20-degree excursions while maintaining gaze on a blank circle centered on the monitor screen. In an attempt to identify the maximum head velocity at which the participant could accurately identify the optotype orientation, the required head velocity started at 30 degrees/s and increased in a step-wise fashion to a maximum velocity of 320 degrees/s. The maximum head velocity at which each participant maintained visual acuity was determined by the computer-generated modified PEST algorithm. The headmounted inertial orientation sensor recorded actual head velocity and correlated this value with the computer-prescribed velocity to trigger target presentation. The participant was given a visual scale at the bottom of the screen that corresponded with their actual head velocity. When the participant’s head movement met the required minimum head velocity for the trial, the visual cue changed color from red to green, and an ‘‘E’’ optotype at a size 0.25 logMAR above the participant’s SVA appeared in the center of the blank circle on computer screen oriented in one of four directions. The GST data was separated into rightward and leftward head movement for analysis, but target presentation and timing were unpredictable during data acquisition. Testing
was confined to the horizontal (yaw) plane in an effort to minimize testing time and participant fatigue.
Dynamic Visual Acuity Test (DVAT) During the GST, the optotype size was fixed, while the head velocity varied according to computer-prescribed velocity for target presentation. During the dynamic visual acuity test (DVAT), the minimal head velocity was 85 degrees/sec, whereas the optotype size varied according to performance. Therefore, the DVAT measured the minimum optotype size at which orientation was accurately assessed while moving the head more than 85 degrees/s up to 140 degrees/s. Each trial was reported as the change in logMAR ($logMAR) from the participant’s SVA. Participants were required to reach the computer prescribed velocity greater than 85 degrees/s up to 140 degrees/s before the optotype would appear on the computer screen. The method of head movement, optotype display time based on MPT, and optotype orientation reporting were the same as previously described for the GST. The DVAT data was separated into rightward and leftward head movements using unpredictable target presentation timing and head direction.
Statistical Analysis Standard descriptive statistics were used to describe the study population and the distribution of scores for each of the tests. The Wilcoxon rank sum test was used to compare each test score between the patient and control groups. Receiver operating characteristic (ROC) curves were used to assess the accuracy of the DVAT and GST tests and to identify cutoff values with the best discrimination between patients and controls. The ROC is a plot of sensitivity versus 1-specificity of the values of a test. The area under the ROC curve (AUC) ranges from 0.5 (accuracy not better than obtained by chance alone) to 1 (perfect accuracy). Each point on the ROC curve can serve as a cutoff point with its own sensitivity and specificity value. Theoretically, the optimal cutoff is the point with the best combination of sensitivity and specificity. This cutoff value was chosen for each test to dichotomize the test values into normal and abnormal. The alpha level for all tests was set at 0.05. All statistical analysis was performed using the IBM SPSS Statistics, 20.0 (IBM Corp, Armonk, NY).
RESULTS The study included 17 control subjects (median age, 57 yr; range, 39Y70 yr) and 17 UVL patients (median age, 62 yr; range, 40Y86 yr) with documented unilateral vestibular dysfunction based on greater than or equal to 49% bithermal binaural caloric test (n = 8) or a history of ablative surgery or gamma knife treatment (n = 9). There was no significant difference in the age and gender between the patient group and the control group. In the UVL patient group, 47% had left-sided hypofunction and 53% had right-sided hypofunction. Nine (53%) of the 17 UVL patients had a caloric asymmetry of 100% and the rest ranged from 49% to 87% (Table 1). Three comparisons of $logMAR values (DVAT) or maximum head velocities (GST) were made for the DVAT and GST (Table 2): (1) head velocities toward the patient’s lesioned side versus toward their non-lesioned side, (2) head velocities toward the patient’s lesioned side versus the normal control group, and (3) head velocities
Otology & Neurotology, Vol. 36, No. 4, 2015
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GST AND DVAT IN UVL PATIENTS VS. CONTROLS TABLE 1.
Characteristics of study population
Characteristics N Age (yr) Median (minYmax) Gender Male Female Side of UVL Left Right Caloric asymmetry value (%) Median (minYmax)
Unilateral vestibular loss (UVL) group n (%)
Control group n (%)
17
17
62 (40Y86)
57 (39Y70)
10 (59%) 7 (41%)
11 (65%) 6 (35%) NA
8 (47%) 9 (53%) 100 (49Y100%)
NA
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p = 0.004). There was also a reduction in head velocity required to maintain visual acuity when comparing head movement toward the lesioned side in the UVL patient group (median, 86.3 degrees/s; range, 54.0Y129.3 degrees/s) with the control group (median, 141.3 degrees/s; range, 96.8Y258.5 degrees/s; p G 0.001). Finally, UVL patients also required a slower velocity to maintain visual acuity with head movement toward the non-lesioned side (median, 105.7 degrees/s; range, 64.7Y161.7 degrees/s) compared with the control group (median, 141.3 degrees/s; range, 96.8Y258.5 degrees/s; p = 0.002).
Static Visual Acuity (SVA) and Minimal Perception Time (MPT) Table 2 summarizes the results of the entire test battery. The median logMAR for SVA in the UVL patient group was 0.01 logMAR (range, j0.16 to 0.6 logMAR) compared to the control group (median, j0.06 logMAR; range, j0.15 to 0.41 logMAR). The median MPT in the UVL patient group was 20 milliseconds (range, 20Y60 ms) and 20 milliseconds in the control group (range, 20Y40 ms). There was no significant difference in SVA (p = 0.438) or MPT (p = 0.343) between UVL patients and controls.
Dynamic Visual Acuity Test (DVAT) There was a statistically significant difference in DVAT performance toward the lesioned side of UVL patients compared to both the non-lesioned side and to controls (Table 2). UVL patients had worse visual acuity with head movement toward the lesioned side (median, 0.307 $logMAR; range, 0.140Y0.550 $logMAR) compared with head movement toward the non-lesioned side (median, 0.260 $logMAR; range, 0.067Y0.367 $logMAR; p = 0.003). UVL patients also had worse visual acuity with head movement toward the lesioned side (median, 0.307 $logMAR; range, 0.140Y0.550 $logMAR) compared with the control group (median, 0.167 $logMAR; range, 0.040Y0.352 $logMAR; p = 0.001). However, unlike with GST, UVL patients did not have reduced visual acuity during DVAT with head movement toward the nonlesioned side (median, 0.260 $logMAR; range, 0.067Y0.367 $logMAR) compared with the control group (median, 0.167 $logMAR; range, 0.040Y0.352 $logMAR; p = 0.158).
Gaze Stabilization Test (GST) There was a statistically significant difference in all three comparisons in the GST (Table 2). The UVL patient group required a slower head velocity to maintain visual acuity with head movement toward the lesioned side (median, 86.3 degrees/s; range, 54.0Y129.3 degrees/s) compared with head movement toward the non-lesioned side (median, 105.7 degrees/s; range, 64.7Y161.7 degrees/s;
Receiver Operating Characteristic (ROC) Curve Analysis for the Dynamic Visual Acuity Test (DVAT) and the Gaze Stabilization Test (GST) Receiver operating characteristic (ROC) curve analysis was performed to assess the predictive accuracy of the DVAT and GST tests in identifying the lesioned side of the UVL patient group versus the control group. As demonstrated in Figures 2 and 3, both the DVAT and
toward the patient’s non-lesioned side versus the normal control group. The mean of the head velocities toward the right and left sides was used in the control group for the above comparisons.
TABLE 2.
Distribution of test scores for unilateral vestibular loss (UVL) patients and control group UVL group
Control group
Test
Median (minYmax)
Median (minYmax)
Static visual acuity (logMAR) Minimum perception time (ms)
0.01 (j0.16Y0.60) 20 (20Y60) UVL lesioned side 0.307 (0.140Y0.550) 86.3 (54.0Y129.3) UVL lesioned side 0.307 (0.140Y0.550) 86.3 (54.0Y129.3) UVL non-lesioned side 0.260 (0.067Y0.367) 105.7 (64.7Y161.7)
j0.06 (j0.15Y0.41) 20 (20Y40) UVL non-lesioned side 0.260 (0.067Y0.367) 105.7 (64.7Y161.7) Controlsa 0.167 (0.040Y0.352) 141.3 (96.8Y258.5) Controlsa 0.167 (0.040Y0.352) 141.3 (96.8Y258.5)
Dynamic visual acuity test ($logMAR) Gaze stabilization test (degrees/s) Dynamic visual acuity test ($logMAR) Gaze stabilization test (degrees/s) Dynamic visual acuity test ($logMAR) Gaze stabilization test (degrees/s)
P value 0.438 0.343 0.003 0.004 0.001 G0.001 0.158 0.002
UVL indicates unilateral vestibular loss. a There were no significant differences between left-sided and right-sided test scores of normal controls for the DVAT or GST. Therefore, normal controls were calculated as the mean of the right and left side measurements. Otology & Neurotology, Vol. 36, No. 4, 2015
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FIG. 2. Receiver operator characteristic (ROC) curve for DVAT predicting unilateral vestibular loss (UVL). The chosen cutoff value of 0.3 $logMAR is designated by the arrow. A DVAT value of Q0.3 $logMAR represents an abnormal test result. The area under the ROC curve was 0.83.
GST tests performed well in distinguishing the lesioned side of the UVL patient group versus the control group (AUCs 0.83 for DVAT and 0.94 for GST). From the ROC analysis, a 0.3 $logMAR on DVAT and a 95 degrees/s on GST were selected as optimal cutoff values for an abnormal test result. Therefore, a result of DVAT greater than or equal to 0.3 $logMAR decline in visual acuity or a GST less than or equal to 95 degrees/s maximum head velocity was defined as abnormal (Figs. 2 and 3). Both the DVAT and GST distinguished the lesioned side of the UVL patient group from the control group. For a DVAT of greater than or equal to 0.3 $logMAR, sensitivity was 65%, specificity was 88%, and accuracy was 76%. For a GST of less than or equal to 95 degrees/s, sensitivity was 71%, specificity was 100%, and accuracy was 85%. Using these cutoff values, GST was positive in 12/17 UVL patients and 0/17 control subjects. For the five UVL patients who tested negative on GST, DVAT was positive in three patients. However, DVAT was also falsely positive in 2/17 control subjects. Therefore, GST yielded no false-positive results and the combination of DVAT when GST was negative correctly identified 15/17 UVL patients and incorrectly identified 2/17 control subjects for an overall 88% sensitivity and 88% specificity (Fig. 4A). If DVAT was considered as the initial test with GST utilized when DVAT was normal, the overall results remained the same but a higher false-positive rate (2/17 normal subjects) would be seen on the initial DVAT (Fig. 4B).
perception time (MPT) to assure appropriate target presentation time. The present data are similar to the results of Goebel et al. (2007) showing that both the DVAT and GST performed well at distinguishing the UVL patient group from the control group. The optimal cutoff values as determined by ROC analysis in the present study (DVAT of 0.3 $logMAR and GST of 95 degrees/s) were also remarkably similar to the mean values obtained by Goebel et al. (2007) (DVAT of 0.33 $logMAR [minimal head velocity 120 degrees/s] and GST of 90 degrees/s). Additionally, the values for sensitivity and specificity (65 and 88% for DVAT, 71 and 100% for GST) are similar to the values identified for sensitivity and specificity in this study (71 and 88% for DVAT, 64 and 93% for GST (2)). Moreover, the current data suggest that GST is more specific then DVAT (100 vs. 88%) for identification of abnormal gaze stability and perhaps DVAT is best used to identify dysfunction in patients with a clinical suspicion of vestibular disease and a negative GST result. The current data support the ability of both DVAT and GST to distinguish the lesioned side from the non-lesioned side in the UVL patient group. Moreover, the data also support the ability of GST to distinguish the non-lesioned side from the control group. The finding of reduced performance with head movement toward the non-lesioned side is in agreement with Halmagyi et al. who found that the eye velocity generated in response to head impulses toward the non-lesioned ear was deficient when compared with the control group (20). There are several hypotheses that could explain this finding. One possibility is central suppression of VOR function on the non-lesioned side. Another explanation is decreased neural activity from the lesioned side when moving toward the non-lesioned ear. Theoretically, there is a third possibility of upward adjustment of the baseline firing rate on the non-lesioned side which could result in increased downward modulation of neural activity in the non-lesioned ear with movement
DISCUSSION The purpose of this study was to compare the results of GST and DVAT in patients with unilateral vestibular loss versus normal control subjects using a novel computerized testing system prototype which documented minimal
FIG. 3. Receiver operator characteristic (ROC) curve for GST predicting unilateral vestibular loss (UVL). The chosen cutoff value of 95 degrees/s is designated by the arrow. A GST value of e95 degrees/s represents an abnormal test result. The area under the ROC curve was 0.94.
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FIG. 4. A, Identification of unilateral vestibular loss with GST as the initial test. B, Identification of unilateral vestibular loss with DVAT as the initial test.
toward the lesioned ear at the expense of reduced maximal excitation with movement toward the non-lesioned side. In the present study, DVAT was performed with a minimum head velocity 85 degrees/s (range, 85Y140 degrees/s) whereas previous studies on dynamic visual acuity have used a range of minimal head velocities from 50 and 75 degrees/s (1) to 120 degrees/s (2,8Y10). Human smooth pursuit has been shown to be linear with a gain near unity up to 60 degrees/s (21) with a gain of 0.82 at 90 degrees/s in normal subjects (22). Therefore, it is possible that in the present study, subjects with vestibular dysfunction and excellent smooth pursuit might have demonstrated less than 0.3 $logMAR with target presentation at the lower range of head velocities. In contrast, GST used peak head velocity with a fixed target size as the main outcome measure which avoided the issue of minimum head velocity for target presentation and may have identified additional UVL subjects with normal DVAT results because of superior smooth pursuit. Another consideration in both DVAT and GST is the possibility of target recognition by non-vestibular oculomotor mechanisms. Compensatory refixation (overt) saccades with a latency of 50 to 150 milliseconds have been described as an eye movement which may occur in vestibulopathic patients in the direction of the vestibular
slow component with attempted target fixation during head rotation (23). If the optotype display time is greater than or equal to 100 milliseconds during DVAT or GST, a patient with unilateral vestibular loss might be able to identify the correct optotype orientation using a compensatory refixation saccade. Ward et al. eliminated 13 of 86 recruits for their GST study on elderly adults because of prolonged minimal perception time which they felt could negatively affect recognition of targets with less than 95 milliseconds’ duration (13). Therefore, DVAT and GST results may not be reliable when attempting to identify a peripheral vestibular lesion in a patient with a prolonged MPT (Q65 ms leading to an optotype display time Q100 ms). In the present study, all participants had a MPT less than or equal to 60 milliseconds and the maximum optotype display time was 95 milliseconds, which in theory should have been short enough to minimize the ability of overt refixation eye movements to aid in the identification of optotype orientation. However, if MPT is not documented and less than 95 milliseconds’ target duration is used, patients with a normal VOR but prolonged MPT could potentially have abnormal DVA and GST results because of their inability to recognize targets with short presentation times. Another confounding factor in gaze stability testing is the possibility of a non-vestibular preprogrammed (covert) Otology & Neurotology, Vol. 36, No. 4, 2015
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saccade which can occur within 100 milliseconds of initiation of head movement. These saccades have been shown to occur mainly with predictable head movements (24) and can confound the results of head impulse testing (25). This is also a consideration in DVAT and GST using actively generated head movements. However, the unpredictable target timing and direction of head movement during sinusoidal headshaking should minimize the generation of covert saccades for gaze stabilization. In this study, UVL patients were defined as having a caloric weakness value greater than or equal to 49% or history of ablation. This value was chosen to clearly exceed all standard clinical cutoff values for caloric asymmetry. This study did not investigate whether there was a correlation between the severity of the caloric asymmetry in the patient group and the magnitude of the GST or DVAT abnormality which would be of interest in future studies. Furthermore, this current study used the modified PEST algorithm to establish threshold levels for the participants and may have contributed to a longer test time which perhaps could be reduced by alternate methods of threshold detection similar to audiologic threshold determination techniques. Finally, the results of this study using a prototype mirrored tunnel system were quite similar to those obtained using a standard monitor which supports the utility of the GST and DVAT using available portable systems to document deficits and perhaps track the effect of vestibular rehabilitation exercises in a clinical setting. The present study has certain limitations which should be considered when interpreting the data. This study was performed on a prototype tunnel system to optimize visual conditions and target distance, and any comparison with other computer monitorYbased studies with different viewing distances, target illumination, or optotype size should be done with caution. Active instead of passive head movements were used which theoretically may have allowed generation of predictive covert non-vestibular saccadic eye movements to aid in gaze stabilization. However, the unpredictable nature of target presentation (timing and direction of head movement) should have minimized prediction. Another potential issue is the 85 degrees/s minimal head velocity chosen for DVAT which is closer to smooth pursuit threshold than previous studies and may have allowed for some contribution of smooth pursuit for gaze stability. However, actual head velocities of 85 to 140 degrees/s during target presentation combined with the transient unpredictable nature of optotype display was likely sufficient to avoid visual pursuit for target identification. There is also the consideration of increased test duration if both GST and DVAT are administered together in the clinical setting. To minimize test time, the current data support the use of GST as the initial test and performing DVAT when GST results are normal. Moreover, if both GST and DVAT are performed, the clinical protocol could be shortened by documenting static acuity and MPT only once in the beginning of testing. Finally, this study did not exclude subjects with previous vestibular rehabilitation which may have improved the sensitivity of
DVAT and GST performance for detection of subjects with unilateral vestibular dysfunction. Based on the present study, the following recommendations are proposed when testing patients for dynamic gaze instability. Both DVAT and GST using active head rotations and unpredictable target presentation are useful tests for detecting patients with unilateral vestibular loss. Static acuity testing and MPT should first be established in all patients. If the MPT is greater than or equal to 65 milliseconds (optotype duration Q95 ms), the DVAT and GST results may not be reliable. After a practice period for either test, at least three trials should be performed and the best performance should be considered when evaluating for dysfunction. According to the ROC analysis in this study, the optimal cutoff values for the DVAT is greater than or equal to 0.3 $logMAR and for the GST is less than or equal to 95 degrees/s peak head velocity. The data also support the performance of GST first and, if abnormal, no further testing is indicated. If, however, the GST result is normal, follow-up DVAT may increase detection of VOR dysfunction. REFERENCES 1. Tian JR, Shubayev I, Demer JL. Dynamic visual acuity during passive and self-generated transient head rotation in normal and unilaterally vestibulopathic humans. Exp Brain Res 2002;142:486Y95. 2. Goebel JA, Tungsiripat N, Sinks B, et al. Gaze stabilization test: a new clinical test of unilateral vestibular dysfunction. Otol Neurotol 2007;28:68Y73. 3. Burgio DL, Blakley BW, Myers SF. The high-frequency oscillopsia test. J Vestib Res 1992;2:221Y6. 4. Longridge NS, Mallinson AI. The dynamic illegible E-test. A technique for assessing the vestibulo-ocular reflex. Acta Otolaryngol 1987;103:273Y9. 5. Tian J, Crane BT, Demer JL. Vestibular catch-up saccades in labyrinthine deficiency. Exp Brain Res 2000;131:448Y57. 6. Demer JL, Honrubia V, Baloh RW. Dynamic visual acuity: a test for oscillopsia and vestibulo-ocular reflex function. Am J Otol 1994; 15:340Y7. 7. Tian JR, Shubayev I, Demer JL. Dynamic visual acuity during transient and sinusoidal yaw rotation in normal and unilaterally vestibulopathic humans. Exp Brain Res 2001;137:12Y25. 8. Herdman SJ, Tusa RJ, Blatt P, et al. Computerized dynamic visual acuity test in the assessment of vestibular deficits. Am J Otol 1998;19:790Y6. 9. Herdman SJ, Schubert MC, Tusa RJ. Role of central preprogramming in dynamic visual acuity with vestibular loss. Arch Otolaryngol Head Neck Surg 2001;127:1205Y10. 10. Herdman SJ, Schubert MC, Das VE, et al. Recovery of dynamic visual acuity in unilateral vestibular hypofunction. Arch Otolaryngol Head Neck Surg 2003;129:819Y24. 11. Schubert MC, Migliaccio AA, Della Santina CC. Modification of compensatory saccades after aVOR gain recovery. J Vestib Res 2006; 16:285Y91. 12. Pritcher MR, Whitney SL, Marchetti GF, Furman JM. The influence of age and vestibular disorders on gaze stabilization: a pilot study. Otol Neurotol 2008;29:982Y8. 13. Ward BK, Mohammed MT, Brach JS, Studenski SA, Whitney SL, Furman JM. Physical performance and a test of gaze stability in older adults. Otol Neurotol 2009;31:168Y72. 14. Lieberman HR, Pentland AP. Microcomputer-based estimation of psychophysical thresholds: the best PEST. Behav Res Meth Instr 1982;14:21Y5. 15. Saslow MG. Effects of components of displacement-step stimuli upon latency for saccadic eye movement. J Opt Soc Am 1967;57:1024Y9.
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GST AND DVAT IN UVL PATIENTS VS. CONTROLS 16. Reulen JP. Latency of visually evoked saccadic eye movements. II. Temporal properties of the facilitation mechanism. Biol Cybern 1984;50:263Y71. 17. Reulen JP. Latency of visually evoked saccadic eye movements. I. Saccadic latency and the facilitation model. Biol Cybern 1984; 50:251Y62. 18. Kalesnykas RP, Hallett PE. The differentiation of visually guided and anticipatory saccades in gap and overlap paradigms. Exp Brain Res 1987;68:115Y21. 19. Takagi M, Frohman EM, Zee DS. Gap-overlap effects on latencies of saccades, vergence and combined vergence-saccades in humans. Vision Res 1995;35:3373Y88. 20. Stevenson SA, Elsley JK, Corneil BD. A ‘‘gap effect’’ on stop signal reaction times in a human saccadic countermanding task. J Neurophysiol 2009;101:580Y90.
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21. Halmagyi GM, Curthoys IS, Cremer PD, et al. The human horizontal vestibulo-ocular reflex in response to high-acceleration stimulation before and after unilateral vestibular neurectomy. Exp Brain Res 1990;81:479Y90. 22. Kasai T, Zee DS. Eye-head coordination in labyrinthine-defective human beings. Brain Res 1978;144:123Y41. 23. Meyer CH, Lasker AG, Robinson DA. The upper limit of human smooth pursuit velocity. Vision Res 1985;4:561Y3. 24. Bloomberg J, Jones GM, Segal B. Adaptive plasticity in the gaze stabilizing synergy of slow and saccadic eye movements. Exp Brain Res 1991;84:35Y46. 25. Lee S-H, Newman-Toker DE, Zee DS, et al. Compensatory saccade differences between outward versus inward head impulses in chronic unilateral vestibular hypofunction. J Clin Neurosci 2014;21:1744Y9.
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for Papers: for Papers: for Papers: for Papers: for Papers: for Papers: for Papers: for Papers: for Papers: for Papers: for Papers: for Papers: for Papers: for Papers: for Papers: for Papers:
American Neurotology Society. Otology & Neurotology. 2013;34:971. American Otological Society, Inc. Otology & Neurotology. 2013;34:972. American Neurotology Society. Otology & Neurotology. 2013;34:1170. American Otological Society, Inc. Otology & Neurotology. 2013;34:1171. American Neurotology Society. Otology & Neurotology. 2013;34:1365. American Otological Society, Inc. Otology & Neurotology. 2013;34:1366. American Neurotology Society. Otology & Neurotology. 2013;34:1548. American Otological Society, Inc. Otology & Neurotology. 2013;34:1549. American Neurotology Society. Otology & Neurotology. 2014;35:1118. American Otological Society, Inc. Otology & Neurotology. 2014;35:1119. American Neurotology Society. Otology & Neurotology. 2014;35:1298. American Otological Society, Inc. Otology & Neurotology. 2014;35:1299. American Neurotology Society. Otology & Neurotology. 2014;35:1492. American Otological Society, Inc. Otology & Neurotology. 2014;35:1493. American Neurotology Society. Otology & Neurotology. 2014;35:1679. American Otological Society, Inc. Otology & Neurotology. 2014;35:1680.
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Comparison of the Gaze Stabilization Test and the Dynamic Visual Acuity Test in Unilateral Vestibular Loss Patients and Controls *Courtney C. J. Voelker, †Amelia Lucisano, *Dorina Kallogjeri, *Belinda C. Sinks, and *Joel A. Goebel *Dizziness and Balance Center, Department of OtolaryngologyYHead and Neck Surgery, ÞWashington University School of Medicine, St. Louis, Missouri, U.S.A.
Objective: Compare the dynamic visual acuity test (DVAT) and gaze stabilization test (GST) in patients with unilateral vestibular loss (UVL) and healthy control subjects using a novel computerized testing system prototype. Study Design: Cross-sectional study. Setting: Tertiary academic referral laboratory. Patients: Seventeen UVL patients (median age 62 yr) with bithermal caloric asymmetry (Q49%) or ablative surgery and 17 control subjects (median age 57 yr). Intervention(s): Diagnostic. Main Outcome Measure(s): Comparison of DVAT and GST results during self-generated sinusoidal head movements using transient unpredictable target presentations less than 95 milliseconds in duration. Results: UVL patients had significantly higher DVAT scores toward the lesioned side compared with controls (p = 0.001) and the non-lesioned side (p = 0.003), but the non-lesioned side was not significantly different from controls (p = 0.157). When comparing GST scores, UVL patients required a slower head velocity
to maintain visual acuity with movement toward the lesioned side compared with controls (p G 0.001) and the non-lesioned side (p = 0.004). In addition, UVL patients had significantly lower scores toward the non-lesioned side (p = 0.002) compared to controls. ROC curve analysis identified optimal thresholds for abnormal test results to discriminate the lesioned side from controls. A DVAT score greater than or equal to 0.3 $logMAR provided 65% sensitivity and 88% specificity while a GST score less than or equal to 95 degrees/s provided 71% sensitivity and 100% specificity. When GST results were normal, adding DVAT increased overall sensitivity to 88% with 88% specificity. Conclusions: Both GST and DVAT demonstrated reduced gaze stabilization toward the lesioned side in the patient group compared with normal controls. Performing GST first and utilizing DVAT when GST was normal provides optimal identification of patients with vestibular dysfunction. Key Words: Dynamic visual acuity testVGaze stabilization testVVestibular testing.
Maintenance of gaze stability during head movement is a complex interaction between the vestibulo-ocular reflex (VOR), foveal smooth pursuit, optokinetic stimulation of the peripheral retina, and the cervico-ocular reflex. At lower frequencies (G2 Hz) and peak velocities (G60Y90 degrees/s), the central oculomotor mechanisms are dominant. However, at higher frequencies and velocities, the VOR becomes the primary mechanism for maximizing visual acuity by limiting retinal slip. Standard tests of vestibular function
(e.g., caloric and rotational stimulation) are useful in documenting deficits in low-frequency, horizontal semicircular canal VOR function. However, these tests fail to assess the VOR contribution to gaze stability at higher frequencies within the range of everyday head movements (1Y4 Hz). Computerized dynamic visual acuity testing (DVAT) has been developed and studied as a method of determining gaze stability during head movements at higher frequencies (92 Hz) and peak velocities ranging from greater than 50 degrees/s (1) to greater than 120 degrees/s (2Y8). DVAT compares the relative loss of visual acuity between head-still and head-moving conditions (measured in logarithmic Minimal Angle of Resolution or logMAR). This is accomplished by measuring the change in the visual target size that a participant can accurately recognize during head rotation compared to the static visual acuity (SVA) in the resting condition. The utility
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Address correspondence and reprint requests to Joel A. Goebel, M.D., Dizziness and Balance Center, Department of OtolaryngologyYHead and Neck Surgery, Washington University School of Medicine, St Louis, MO, U.S.A.; E-mail: [email protected] The authors disclose no conflicts of interest. P30 NIH Grant pays for part of biostatistician’s time to support research in the department; the grant does not specifically relate to the project.
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GST AND DVAT IN UVL PATIENTS VS. CONTROLS of the DVAT has been well documented in patients with unilateral vestibular dysfunction or bilateral vestibular loss as well as in the elderly population (1,2,6Y11). One concern, however, is the inherent visual challenge associated with changing target size separate from the effects of the VOR. Another potential issue is the use of a short duration of target presentation (G100 ms) in participants with prolonged perception times who may fail to correctly identify the target resulting from inadequate target presentation time rather than a VOR deficiency. Furthermore, published DVAT protocols have studied both predictable active and unpredictable passive head movements to assess the possible effect of prediction for the generation of preprogrammed (covert) or refixation (overt) saccadic eye movements to maintain the target on the fovea. The authors concluded that test protocols with unpredictable target presentation resulted in reduced dynamic visual acuity in subjects with vestibular dysfunction resulting from avoidance of preprogrammed saccadic eye movements (9,11). The gaze stabilization test (GST) was first described as an alternative method to document gaze stability during head motion without changing target size (2). Current GST protocols use a fixed target at a size of 0.2 to 0.3 logMAR (2Y3 lines on a standard Snellen chart) above the participant’s static visual acuity and measures the peak head velocity achieved while continuing to maintain the capability of accurately identifying target orientation (12,13). This study was designed to investigate the relative ability of the GST and DVAT using active headshaking and unpredictable target presentation to detect unilateral vestibular dysfunction. GST and DVAT results were compared between patients with unilateral vestibular loss (UVL) (defined in this study as Q49% caloric asymmetry or a history of an ablative procedure) and normal control subjects. A prototype mirrored tunnel system was used to create a longer viewing distance and more uniform target illumination. Both DVAT and GST protocols used a continuous sinusoidal, self-generated head movements as well as unpredictable timing and head direction for target presentation to minimize the effect of covert non-vestibular predictive eye movements for gaze stabilization. Furthermore, the duration of target presentation was adjusted based on documented baseline minimal perception time (MPT) to a maximum of 95 milliseconds to minimize the ability of overt saccades to refixate and identify the optotype.
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of Medicine. All participants were 18 years of age or older. Participants were excluded from the study if they had a history of cervical dysfunction that prevented them from moving their head rapidly, severe visual impairment or blind spots in their visual field, or a history of a central nervous system disorder.
Test Protocol All participants were tested with best-corrected vision using a prototype mirrored tunnel system (NeuroCom International, Clackamas, OR). Participants were seated so that the bridge of their nose was 1.5 feet from the start of the tunnel system, and the visual target appeared on a mirror monitor display as if it were 13 feet from the participant (Fig. 1). Because of the long target distance, changes in viewing angle caused by variation in participant height were minimal and no adjustment was required. In an attempt to standardize luminescence and to minimize distraction to the participant, the room lights were turned off. The only ambient light originated from the operator’s console, which was positioned behind the participant. To monitor head direction and velocity, participants were fitted with the InertiaCube2+ precision inertial orientation sensor (InterSense, Incorporated, Billerica, MA) (Fig. 1). All participants performed static acuity and minimum perception time (MPT) tests first, and the GST and DVAT were randomly placed in the third or fourth test positions to minimize learning or fatigue effect. For both DVAT and GST, the modified PEST algorithm was used to determine threshold values by using the participant’s previous response to set the relevant stimulus parameters (visual target size with DVAT and head velocity for target presentation with GST) for each subsequent trial to determine threshold values (14). For both DVAT and GST, three separate trials were conducted and the best performance threshold values were recorded for each trial. Participants were allowed rest periods if desired making the test session last from 60 to 90 minutes. Head movement was monitored visually
SUBJECTS AND METHODS Subjects This study was approved by the Human Research Protection Office of Washington University in Saint Louis. Patients with documented unilateral vestibular dysfunction based on greater than or equal to 49% bithermal binaural caloric test asymmetry on closed loop irrigation were recruited from the clinical practice of the principal investigator (J.A.G.). This cutoff for caloric asymmetry was chosen to clearly exceed the clinical standard of greater than 30% asymmetry accepted by most laboratories using this caloric stimulus. Control subjects were recruited from the Volunteer for Health Database at Washington University School
FIG. 1. Prototype mirrored tunnel system (NeuroCom International, Clackamas, OR). Participants were fitted with a headmounted, inertial orientation sensor to monitor head direction and velocity. They were placed so that the visual target appeared on a mirror monitor display as if it were 13 feet from the participant. The room lights were turned off, and the only light in the room came from the operator’s console, which was positioned behind the participant to avoid visual distraction. Otology & Neurotology, Vol. 36, No. 4, 2015
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by the operator throughout testing, and participants were verbally reinstructed as needed.
Static Visual Acuity (SVA) Static visual acuity (SVA) was measured by displaying a single optotype (letter ‘‘E’’) in the center of the monitor starting at 0.3 logMAR, which is the Snellen equivalency of 20/40. The optotype appeared for 1 second and randomly changed orientation and size with each trial, and the participant was asked to verbally identify the target orientation (up, down, left, right) until a threshold acuity was identified. In contrast to other DVAT studies, static visual acuity (SVA) determination in this study included testing below 0.0 logMAR. The SVA for each subject was then used to set target size for the subsequent DVAT and GST trials.
Minimum Perception Time (MPT) The minimum perception time (MPT) is the shortest time (ms) an optotype can be presented on the screen so that the participant could accurately identify its orientation with the head stationary. Participants focused on a box that appeared in the center of the computer screen for 2 seconds. The box disappeared and after an interval of 250 milliseconds, an ‘‘E’’ optotype 0.25 logMAR above the participant’s SVA appeared in its place for 250 milliseconds and participants were instructed to verbally identify target orientation which was entered into the program by the operator. The computer then presented additional targets with increasingly shorter presentation times until a minimum threshold was reached (14Y19). The MPT set the optotype display time parameters for the remainder of the tests. If the MPT was less than or equal to 40 milliseconds, the optotype display time was varied randomly between 40 and 75 milliseconds. If the MPT was greater than 40 milliseconds, the optotype display time varied between the MPT and MPT + 35 milliseconds up to a maximum of 95 milliseconds to minimize the capability of refixation saccades for target identification during testing.
Gaze Stabilization Test (GST) The GST quantifies the maximum head velocity at which a patient is able to maintain visual acuity. In this study, the GST measured the maximum head velocity at which a participant could accurately identify the fixed size optotype orientation. Participants were instructed to conduct smooth sinusoidal headshakes in the yaw plane at a frequency greater than 2 Hz and less than 20-degree excursions while maintaining gaze on a blank circle centered on the monitor screen. In an attempt to identify the maximum head velocity at which the participant could accurately identify the optotype orientation, the required head velocity started at 30 degrees/s and increased in a step-wise fashion to a maximum velocity of 320 degrees/s. The maximum head velocity at which each participant maintained visual acuity was determined by the computer-generated modified PEST algorithm. The headmounted inertial orientation sensor recorded actual head velocity and correlated this value with the computer-prescribed velocity to trigger target presentation. The participant was given a visual scale at the bottom of the screen that corresponded with their actual head velocity. When the participant’s head movement met the required minimum head velocity for the trial, the visual cue changed color from red to green, and an ‘‘E’’ optotype at a size 0.25 logMAR above the participant’s SVA appeared in the center of the blank circle on computer screen oriented in one of four directions. The GST data was separated into rightward and leftward head movement for analysis, but target presentation and timing were unpredictable during data acquisition. Testing
was confined to the horizontal (yaw) plane in an effort to minimize testing time and participant fatigue.
Dynamic Visual Acuity Test (DVAT) During the GST, the optotype size was fixed, while the head velocity varied according to computer-prescribed velocity for target presentation. During the dynamic visual acuity test (DVAT), the minimal head velocity was 85 degrees/sec, whereas the optotype size varied according to performance. Therefore, the DVAT measured the minimum optotype size at which orientation was accurately assessed while moving the head more than 85 degrees/s up to 140 degrees/s. Each trial was reported as the change in logMAR ($logMAR) from the participant’s SVA. Participants were required to reach the computer prescribed velocity greater than 85 degrees/s up to 140 degrees/s before the optotype would appear on the computer screen. The method of head movement, optotype display time based on MPT, and optotype orientation reporting were the same as previously described for the GST. The DVAT data was separated into rightward and leftward head movements using unpredictable target presentation timing and head direction.
Statistical Analysis Standard descriptive statistics were used to describe the study population and the distribution of scores for each of the tests. The Wilcoxon rank sum test was used to compare each test score between the patient and control groups. Receiver operating characteristic (ROC) curves were used to assess the accuracy of the DVAT and GST tests and to identify cutoff values with the best discrimination between patients and controls. The ROC is a plot of sensitivity versus 1-specificity of the values of a test. The area under the ROC curve (AUC) ranges from 0.5 (accuracy not better than obtained by chance alone) to 1 (perfect accuracy). Each point on the ROC curve can serve as a cutoff point with its own sensitivity and specificity value. Theoretically, the optimal cutoff is the point with the best combination of sensitivity and specificity. This cutoff value was chosen for each test to dichotomize the test values into normal and abnormal. The alpha level for all tests was set at 0.05. All statistical analysis was performed using the IBM SPSS Statistics, 20.0 (IBM Corp, Armonk, NY).
RESULTS The study included 17 control subjects (median age, 57 yr; range, 39Y70 yr) and 17 UVL patients (median age, 62 yr; range, 40Y86 yr) with documented unilateral vestibular dysfunction based on greater than or equal to 49% bithermal binaural caloric test (n = 8) or a history of ablative surgery or gamma knife treatment (n = 9). There was no significant difference in the age and gender between the patient group and the control group. In the UVL patient group, 47% had left-sided hypofunction and 53% had right-sided hypofunction. Nine (53%) of the 17 UVL patients had a caloric asymmetry of 100% and the rest ranged from 49% to 87% (Table 1). Three comparisons of $logMAR values (DVAT) or maximum head velocities (GST) were made for the DVAT and GST (Table 2): (1) head velocities toward the patient’s lesioned side versus toward their non-lesioned side, (2) head velocities toward the patient’s lesioned side versus the normal control group, and (3) head velocities
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GST AND DVAT IN UVL PATIENTS VS. CONTROLS TABLE 1.
Characteristics of study population
Characteristics N Age (yr) Median (minYmax) Gender Male Female Side of UVL Left Right Caloric asymmetry value (%) Median (minYmax)
Unilateral vestibular loss (UVL) group n (%)
Control group n (%)
17
17
62 (40Y86)
57 (39Y70)
10 (59%) 7 (41%)
11 (65%) 6 (35%) NA
8 (47%) 9 (53%) 100 (49Y100%)
NA
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p = 0.004). There was also a reduction in head velocity required to maintain visual acuity when comparing head movement toward the lesioned side in the UVL patient group (median, 86.3 degrees/s; range, 54.0Y129.3 degrees/s) with the control group (median, 141.3 degrees/s; range, 96.8Y258.5 degrees/s; p G 0.001). Finally, UVL patients also required a slower velocity to maintain visual acuity with head movement toward the non-lesioned side (median, 105.7 degrees/s; range, 64.7Y161.7 degrees/s) compared with the control group (median, 141.3 degrees/s; range, 96.8Y258.5 degrees/s; p = 0.002).
Static Visual Acuity (SVA) and Minimal Perception Time (MPT) Table 2 summarizes the results of the entire test battery. The median logMAR for SVA in the UVL patient group was 0.01 logMAR (range, j0.16 to 0.6 logMAR) compared to the control group (median, j0.06 logMAR; range, j0.15 to 0.41 logMAR). The median MPT in the UVL patient group was 20 milliseconds (range, 20Y60 ms) and 20 milliseconds in the control group (range, 20Y40 ms). There was no significant difference in SVA (p = 0.438) or MPT (p = 0.343) between UVL patients and controls.
Dynamic Visual Acuity Test (DVAT) There was a statistically significant difference in DVAT performance toward the lesioned side of UVL patients compared to both the non-lesioned side and to controls (Table 2). UVL patients had worse visual acuity with head movement toward the lesioned side (median, 0.307 $logMAR; range, 0.140Y0.550 $logMAR) compared with head movement toward the non-lesioned side (median, 0.260 $logMAR; range, 0.067Y0.367 $logMAR; p = 0.003). UVL patients also had worse visual acuity with head movement toward the lesioned side (median, 0.307 $logMAR; range, 0.140Y0.550 $logMAR) compared with the control group (median, 0.167 $logMAR; range, 0.040Y0.352 $logMAR; p = 0.001). However, unlike with GST, UVL patients did not have reduced visual acuity during DVAT with head movement toward the nonlesioned side (median, 0.260 $logMAR; range, 0.067Y0.367 $logMAR) compared with the control group (median, 0.167 $logMAR; range, 0.040Y0.352 $logMAR; p = 0.158).
Gaze Stabilization Test (GST) There was a statistically significant difference in all three comparisons in the GST (Table 2). The UVL patient group required a slower head velocity to maintain visual acuity with head movement toward the lesioned side (median, 86.3 degrees/s; range, 54.0Y129.3 degrees/s) compared with head movement toward the non-lesioned side (median, 105.7 degrees/s; range, 64.7Y161.7 degrees/s;
Receiver Operating Characteristic (ROC) Curve Analysis for the Dynamic Visual Acuity Test (DVAT) and the Gaze Stabilization Test (GST) Receiver operating characteristic (ROC) curve analysis was performed to assess the predictive accuracy of the DVAT and GST tests in identifying the lesioned side of the UVL patient group versus the control group. As demonstrated in Figures 2 and 3, both the DVAT and
toward the patient’s non-lesioned side versus the normal control group. The mean of the head velocities toward the right and left sides was used in the control group for the above comparisons.
TABLE 2.
Distribution of test scores for unilateral vestibular loss (UVL) patients and control group UVL group
Control group
Test
Median (minYmax)
Median (minYmax)
Static visual acuity (logMAR) Minimum perception time (ms)
0.01 (j0.16Y0.60) 20 (20Y60) UVL lesioned side 0.307 (0.140Y0.550) 86.3 (54.0Y129.3) UVL lesioned side 0.307 (0.140Y0.550) 86.3 (54.0Y129.3) UVL non-lesioned side 0.260 (0.067Y0.367) 105.7 (64.7Y161.7)
j0.06 (j0.15Y0.41) 20 (20Y40) UVL non-lesioned side 0.260 (0.067Y0.367) 105.7 (64.7Y161.7) Controlsa 0.167 (0.040Y0.352) 141.3 (96.8Y258.5) Controlsa 0.167 (0.040Y0.352) 141.3 (96.8Y258.5)
Dynamic visual acuity test ($logMAR) Gaze stabilization test (degrees/s) Dynamic visual acuity test ($logMAR) Gaze stabilization test (degrees/s) Dynamic visual acuity test ($logMAR) Gaze stabilization test (degrees/s)
P value 0.438 0.343 0.003 0.004 0.001 G0.001 0.158 0.002
UVL indicates unilateral vestibular loss. a There were no significant differences between left-sided and right-sided test scores of normal controls for the DVAT or GST. Therefore, normal controls were calculated as the mean of the right and left side measurements. Otology & Neurotology, Vol. 36, No. 4, 2015
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FIG. 2. Receiver operator characteristic (ROC) curve for DVAT predicting unilateral vestibular loss (UVL). The chosen cutoff value of 0.3 $logMAR is designated by the arrow. A DVAT value of Q0.3 $logMAR represents an abnormal test result. The area under the ROC curve was 0.83.
GST tests performed well in distinguishing the lesioned side of the UVL patient group versus the control group (AUCs 0.83 for DVAT and 0.94 for GST). From the ROC analysis, a 0.3 $logMAR on DVAT and a 95 degrees/s on GST were selected as optimal cutoff values for an abnormal test result. Therefore, a result of DVAT greater than or equal to 0.3 $logMAR decline in visual acuity or a GST less than or equal to 95 degrees/s maximum head velocity was defined as abnormal (Figs. 2 and 3). Both the DVAT and GST distinguished the lesioned side of the UVL patient group from the control group. For a DVAT of greater than or equal to 0.3 $logMAR, sensitivity was 65%, specificity was 88%, and accuracy was 76%. For a GST of less than or equal to 95 degrees/s, sensitivity was 71%, specificity was 100%, and accuracy was 85%. Using these cutoff values, GST was positive in 12/17 UVL patients and 0/17 control subjects. For the five UVL patients who tested negative on GST, DVAT was positive in three patients. However, DVAT was also falsely positive in 2/17 control subjects. Therefore, GST yielded no false-positive results and the combination of DVAT when GST was negative correctly identified 15/17 UVL patients and incorrectly identified 2/17 control subjects for an overall 88% sensitivity and 88% specificity (Fig. 4A). If DVAT was considered as the initial test with GST utilized when DVAT was normal, the overall results remained the same but a higher false-positive rate (2/17 normal subjects) would be seen on the initial DVAT (Fig. 4B).
perception time (MPT) to assure appropriate target presentation time. The present data are similar to the results of Goebel et al. (2007) showing that both the DVAT and GST performed well at distinguishing the UVL patient group from the control group. The optimal cutoff values as determined by ROC analysis in the present study (DVAT of 0.3 $logMAR and GST of 95 degrees/s) were also remarkably similar to the mean values obtained by Goebel et al. (2007) (DVAT of 0.33 $logMAR [minimal head velocity 120 degrees/s] and GST of 90 degrees/s). Additionally, the values for sensitivity and specificity (65 and 88% for DVAT, 71 and 100% for GST) are similar to the values identified for sensitivity and specificity in this study (71 and 88% for DVAT, 64 and 93% for GST (2)). Moreover, the current data suggest that GST is more specific then DVAT (100 vs. 88%) for identification of abnormal gaze stability and perhaps DVAT is best used to identify dysfunction in patients with a clinical suspicion of vestibular disease and a negative GST result. The current data support the ability of both DVAT and GST to distinguish the lesioned side from the non-lesioned side in the UVL patient group. Moreover, the data also support the ability of GST to distinguish the non-lesioned side from the control group. The finding of reduced performance with head movement toward the non-lesioned side is in agreement with Halmagyi et al. who found that the eye velocity generated in response to head impulses toward the non-lesioned ear was deficient when compared with the control group (20). There are several hypotheses that could explain this finding. One possibility is central suppression of VOR function on the non-lesioned side. Another explanation is decreased neural activity from the lesioned side when moving toward the non-lesioned ear. Theoretically, there is a third possibility of upward adjustment of the baseline firing rate on the non-lesioned side which could result in increased downward modulation of neural activity in the non-lesioned ear with movement
DISCUSSION The purpose of this study was to compare the results of GST and DVAT in patients with unilateral vestibular loss versus normal control subjects using a novel computerized testing system prototype which documented minimal
FIG. 3. Receiver operator characteristic (ROC) curve for GST predicting unilateral vestibular loss (UVL). The chosen cutoff value of 95 degrees/s is designated by the arrow. A GST value of e95 degrees/s represents an abnormal test result. The area under the ROC curve was 0.94.
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FIG. 4. A, Identification of unilateral vestibular loss with GST as the initial test. B, Identification of unilateral vestibular loss with DVAT as the initial test.
toward the lesioned ear at the expense of reduced maximal excitation with movement toward the non-lesioned side. In the present study, DVAT was performed with a minimum head velocity 85 degrees/s (range, 85Y140 degrees/s) whereas previous studies on dynamic visual acuity have used a range of minimal head velocities from 50 and 75 degrees/s (1) to 120 degrees/s (2,8Y10). Human smooth pursuit has been shown to be linear with a gain near unity up to 60 degrees/s (21) with a gain of 0.82 at 90 degrees/s in normal subjects (22). Therefore, it is possible that in the present study, subjects with vestibular dysfunction and excellent smooth pursuit might have demonstrated less than 0.3 $logMAR with target presentation at the lower range of head velocities. In contrast, GST used peak head velocity with a fixed target size as the main outcome measure which avoided the issue of minimum head velocity for target presentation and may have identified additional UVL subjects with normal DVAT results because of superior smooth pursuit. Another consideration in both DVAT and GST is the possibility of target recognition by non-vestibular oculomotor mechanisms. Compensatory refixation (overt) saccades with a latency of 50 to 150 milliseconds have been described as an eye movement which may occur in vestibulopathic patients in the direction of the vestibular
slow component with attempted target fixation during head rotation (23). If the optotype display time is greater than or equal to 100 milliseconds during DVAT or GST, a patient with unilateral vestibular loss might be able to identify the correct optotype orientation using a compensatory refixation saccade. Ward et al. eliminated 13 of 86 recruits for their GST study on elderly adults because of prolonged minimal perception time which they felt could negatively affect recognition of targets with less than 95 milliseconds’ duration (13). Therefore, DVAT and GST results may not be reliable when attempting to identify a peripheral vestibular lesion in a patient with a prolonged MPT (Q65 ms leading to an optotype display time Q100 ms). In the present study, all participants had a MPT less than or equal to 60 milliseconds and the maximum optotype display time was 95 milliseconds, which in theory should have been short enough to minimize the ability of overt refixation eye movements to aid in the identification of optotype orientation. However, if MPT is not documented and less than 95 milliseconds’ target duration is used, patients with a normal VOR but prolonged MPT could potentially have abnormal DVA and GST results because of their inability to recognize targets with short presentation times. Another confounding factor in gaze stability testing is the possibility of a non-vestibular preprogrammed (covert) Otology & Neurotology, Vol. 36, No. 4, 2015
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saccade which can occur within 100 milliseconds of initiation of head movement. These saccades have been shown to occur mainly with predictable head movements (24) and can confound the results of head impulse testing (25). This is also a consideration in DVAT and GST using actively generated head movements. However, the unpredictable target timing and direction of head movement during sinusoidal headshaking should minimize the generation of covert saccades for gaze stabilization. In this study, UVL patients were defined as having a caloric weakness value greater than or equal to 49% or history of ablation. This value was chosen to clearly exceed all standard clinical cutoff values for caloric asymmetry. This study did not investigate whether there was a correlation between the severity of the caloric asymmetry in the patient group and the magnitude of the GST or DVAT abnormality which would be of interest in future studies. Furthermore, this current study used the modified PEST algorithm to establish threshold levels for the participants and may have contributed to a longer test time which perhaps could be reduced by alternate methods of threshold detection similar to audiologic threshold determination techniques. Finally, the results of this study using a prototype mirrored tunnel system were quite similar to those obtained using a standard monitor which supports the utility of the GST and DVAT using available portable systems to document deficits and perhaps track the effect of vestibular rehabilitation exercises in a clinical setting. The present study has certain limitations which should be considered when interpreting the data. This study was performed on a prototype tunnel system to optimize visual conditions and target distance, and any comparison with other computer monitorYbased studies with different viewing distances, target illumination, or optotype size should be done with caution. Active instead of passive head movements were used which theoretically may have allowed generation of predictive covert non-vestibular saccadic eye movements to aid in gaze stabilization. However, the unpredictable nature of target presentation (timing and direction of head movement) should have minimized prediction. Another potential issue is the 85 degrees/s minimal head velocity chosen for DVAT which is closer to smooth pursuit threshold than previous studies and may have allowed for some contribution of smooth pursuit for gaze stability. However, actual head velocities of 85 to 140 degrees/s during target presentation combined with the transient unpredictable nature of optotype display was likely sufficient to avoid visual pursuit for target identification. There is also the consideration of increased test duration if both GST and DVAT are administered together in the clinical setting. To minimize test time, the current data support the use of GST as the initial test and performing DVAT when GST results are normal. Moreover, if both GST and DVAT are performed, the clinical protocol could be shortened by documenting static acuity and MPT only once in the beginning of testing. Finally, this study did not exclude subjects with previous vestibular rehabilitation which may have improved the sensitivity of
DVAT and GST performance for detection of subjects with unilateral vestibular dysfunction. Based on the present study, the following recommendations are proposed when testing patients for dynamic gaze instability. Both DVAT and GST using active head rotations and unpredictable target presentation are useful tests for detecting patients with unilateral vestibular loss. Static acuity testing and MPT should first be established in all patients. If the MPT is greater than or equal to 65 milliseconds (optotype duration Q95 ms), the DVAT and GST results may not be reliable. After a practice period for either test, at least three trials should be performed and the best performance should be considered when evaluating for dysfunction. According to the ROC analysis in this study, the optimal cutoff values for the DVAT is greater than or equal to 0.3 $logMAR and for the GST is less than or equal to 95 degrees/s peak head velocity. The data also support the performance of GST first and, if abnormal, no further testing is indicated. If, however, the GST result is normal, follow-up DVAT may increase detection of VOR dysfunction. REFERENCES 1. Tian JR, Shubayev I, Demer JL. Dynamic visual acuity during passive and self-generated transient head rotation in normal and unilaterally vestibulopathic humans. Exp Brain Res 2002;142:486Y95. 2. Goebel JA, Tungsiripat N, Sinks B, et al. Gaze stabilization test: a new clinical test of unilateral vestibular dysfunction. Otol Neurotol 2007;28:68Y73. 3. Burgio DL, Blakley BW, Myers SF. The high-frequency oscillopsia test. J Vestib Res 1992;2:221Y6. 4. Longridge NS, Mallinson AI. The dynamic illegible E-test. A technique for assessing the vestibulo-ocular reflex. Acta Otolaryngol 1987;103:273Y9. 5. Tian J, Crane BT, Demer JL. Vestibular catch-up saccades in labyrinthine deficiency. Exp Brain Res 2000;131:448Y57. 6. Demer JL, Honrubia V, Baloh RW. Dynamic visual acuity: a test for oscillopsia and vestibulo-ocular reflex function. Am J Otol 1994; 15:340Y7. 7. Tian JR, Shubayev I, Demer JL. Dynamic visual acuity during transient and sinusoidal yaw rotation in normal and unilaterally vestibulopathic humans. Exp Brain Res 2001;137:12Y25. 8. Herdman SJ, Tusa RJ, Blatt P, et al. Computerized dynamic visual acuity test in the assessment of vestibular deficits. Am J Otol 1998;19:790Y6. 9. Herdman SJ, Schubert MC, Tusa RJ. Role of central preprogramming in dynamic visual acuity with vestibular loss. Arch Otolaryngol Head Neck Surg 2001;127:1205Y10. 10. Herdman SJ, Schubert MC, Das VE, et al. Recovery of dynamic visual acuity in unilateral vestibular hypofunction. Arch Otolaryngol Head Neck Surg 2003;129:819Y24. 11. Schubert MC, Migliaccio AA, Della Santina CC. Modification of compensatory saccades after aVOR gain recovery. J Vestib Res 2006; 16:285Y91. 12. Pritcher MR, Whitney SL, Marchetti GF, Furman JM. The influence of age and vestibular disorders on gaze stabilization: a pilot study. Otol Neurotol 2008;29:982Y8. 13. Ward BK, Mohammed MT, Brach JS, Studenski SA, Whitney SL, Furman JM. Physical performance and a test of gaze stability in older adults. Otol Neurotol 2009;31:168Y72. 14. Lieberman HR, Pentland AP. Microcomputer-based estimation of psychophysical thresholds: the best PEST. Behav Res Meth Instr 1982;14:21Y5. 15. Saslow MG. Effects of components of displacement-step stimuli upon latency for saccadic eye movement. J Opt Soc Am 1967;57:1024Y9.
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GST AND DVAT IN UVL PATIENTS VS. CONTROLS 16. Reulen JP. Latency of visually evoked saccadic eye movements. II. Temporal properties of the facilitation mechanism. Biol Cybern 1984;50:263Y71. 17. Reulen JP. Latency of visually evoked saccadic eye movements. I. Saccadic latency and the facilitation model. Biol Cybern 1984; 50:251Y62. 18. Kalesnykas RP, Hallett PE. The differentiation of visually guided and anticipatory saccades in gap and overlap paradigms. Exp Brain Res 1987;68:115Y21. 19. Takagi M, Frohman EM, Zee DS. Gap-overlap effects on latencies of saccades, vergence and combined vergence-saccades in humans. Vision Res 1995;35:3373Y88. 20. Stevenson SA, Elsley JK, Corneil BD. A ‘‘gap effect’’ on stop signal reaction times in a human saccadic countermanding task. J Neurophysiol 2009;101:580Y90.
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Erratum Incorrect DOIs The publisher found that the following articles were published with incorrect DOIs: Volume 34, Issue 5 In the announcement, Call for Papers: American Neurotology Society (Otology & Neurotology. 2013;34:971), the DOI was incorrect and should have been 10.1097/01.mao.0000460840.77560.f1. In the announcement, Call for Papers: American Otological Society, Inc. (Otology & Neurotology. 2013;34:972), the DOI was incorrect and should have been 10.1097/01.mao.0000460844.08056.10. Volume 34, Issue 6 In the announcement, Call for Papers: American Neurotology Society (Otology & Neurotology. 2013;34:1170), the DOI was incorrect and should have been 10.1097/01.mao.0000460841.54690.7f. In the announcement, Call for Papers: American Otological Society, Inc. (Otology & Neurotology. 2013;34:1171), the DOI was incorrect and should have been 10.1097/01.mao.0000460845.92808.63. Volume 34, Issue 7 In the announcement, Call for Papers: American Neurotology Society (Otology & Neurotology. 2013;34:1365), the DOI was incorrect and should have been 10.1097/01.mao.0000460842.62313.3f. In the announcement, Call for Papers: American Otological Society, Inc. (Otology & Neurotology. 2013;34:1366), the DOI was incorrect and should have been 10.1097/01.mao.0000460846.86970.bf. Volume 34, Issue 8 In the announcement, Call for Papers: American Neurotology Society (Otology & Neurotology. 2013;34:1548), the DOI was incorrect and should have been 10.1097/01.mao.0000460843.00432.c8. In the announcement, Call for Papers: American Otological Society, Inc. (Otology & Neurotology. 2013;34:1549), the DOI was incorrect and should have been 10.1097/01.mao.0000460847.94593.fe. Volume 35, Issue 6 In the announcement, Call for Papers: American Neurotology Society (Otology & Neurotology. 2014;35:1118), the DOI was incorrect and should have been 10.1097/01.mao.0000460831.23619.79. In the announcement, Call for Papers: American Otological Society, Inc. (Otology & Neurotology. 2014;35:1119), the DOI was incorrect and should have been 10.1097/01.mao.0000460835.54113.df. Volume 35, Issue 7 In the announcement, Call for Papers: American Neurotology Society (Otology & Neurotology. 2014;35:1298), the DOI was incorrect and should have been 10.1097/01.mao.0000460832.31242.19.
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American Neurotology Society. Otology & Neurotology. 2013;34:971. American Otological Society, Inc. Otology & Neurotology. 2013;34:972. American Neurotology Society. Otology & Neurotology. 2013;34:1170. American Otological Society, Inc. Otology & Neurotology. 2013;34:1171. American Neurotology Society. Otology & Neurotology. 2013;34:1365. American Otological Society, Inc. Otology & Neurotology. 2013;34:1366. American Neurotology Society. Otology & Neurotology. 2013;34:1548. American Otological Society, Inc. Otology & Neurotology. 2013;34:1549. American Neurotology Society. Otology & Neurotology. 2014;35:1118. American Otological Society, Inc. Otology & Neurotology. 2014;35:1119. American Neurotology Society. Otology & Neurotology. 2014;35:1298. American Otological Society, Inc. Otology & Neurotology. 2014;35:1299. American Neurotology Society. Otology & Neurotology. 2014;35:1492. American Otological Society, Inc. Otology & Neurotology. 2014;35:1493. American Neurotology Society. Otology & Neurotology. 2014;35:1679. American Otological Society, Inc. Otology & Neurotology. 2014;35:1680.
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