Peripheral Vestibular And Balance Function In Athletes With And Without Concussion

Abstract

BACKGROUND AND PURPOSE:

According to the most recent consensus statement on management of sport-related concussion (SRC), athletes with suspected SRC should receive a comprehensive neurological examination. However, which measures to include in such an examination are not defined. Our objectives were to: 1) evaluate test-retest reliability and normative data on vestibular and balance tests in athletes without SRC; 2) compare athletes with and without SRC on the subtests; 3) identify subtests for concussion testing protocols.

METHODS:

Healthy athletes (n = 87, mean age 20.6 years; SD=1.8 years; 39 F, 48 M) and athletes with SRC (n = 28, mean age 20.7 years (SD=1.9) 11 F, 17 M) were tested using rotary chair, cervical vestibular evoked myogenic potential (c-VEMP) and the Sensory Organization Test (SOT). A subset (n=43) were tested twice. We analyzed reliability of the tests, and compared results between athletes with and without SRC.

RESULTS:

Reliability ranged from poor to strong. There was no significant difference between athletes with and without SRC for tests of peripheral vestibular function (i.e. rotary chair, c-VEMP). Athletes with SRC had significantly worse scores (p<0.05) on VOR cancellation gain, subjective visual vertical and horizontal variance, and all conditions of the SOT.

DISCUSSION AND CONCLUSION:

SRC did not affect medium frequency VOR or saccular function. SRC did affect the ability to use vestibular inputs for perception of vertical and postural control, as well as ability to cancel the VOR. Video Abstract available for more insights from the authors (See Video Abstract, Supplemental Digital Content 1).

INTRODUCTION

Sport-related concussion (SRC) is defined as a “traumatic brain injury induced by biomechanical forces.”¹ SRC is a complex neurological event which results in a range of clinical signs and symptoms lasting from a few days to several years. Following SRC, clinicians typically administer a symptom scale, e.g. the Sport Concussion Assessment Tool 5.² However, this tool loses utility 3–5 days following SRC and many athletes either under-report or do not report symptoms.³ The most commonly reported symptoms include headache, difficulty sleeping, fatigue, irritability, visual problems, and academic difficulty.^4–7 Vestibular-related symptoms of dizziness and balance problems are also commonly reported in athletes with SRC^1,7 and vestibular rehabilitation (i.e. gaze stabilization, habituation and balance exercises) is often prescribed as standard treatment.^1,8

It has been reported that vestibular-related symptoms such as on-field (at time of injury) dizziness is associated with a seven times greater risk of developing post-concussion syndrome.⁹ Patients who develop post-concussion syndrome, estimated to be about 20% of all concussion cases,¹⁰ require long-term individualized therapies which could be started earlier with more objective screening for dysfunction. The most recent consensus statement regarding the management of SRC¹ suggests that all athletes with suspected SRC should receive a comprehensive neurological examination to include, but not limited to, oculomotor, vestibular, gait and balance function, but does not define which measures to include in such an examination.

Retrospective studies^11,12 have reported vestibular dysfunction in child athletes with SRC. However, the outcome score used to support this conclusion was the Vestibular/Ocular Motor Screening Assessment (VOMS),^13,14 which asks the athlete to rate symptoms after vestibular-related and oculomotor tasks. The integrity of the peripheral vestibular system, cranial nerve VIII and of the central vestibular pathway function were not measured. One method to directly test the vestibular-ocular reflex (VOR) is with the video head impulse test (vHIT), where the examiner delivers high velocity (i.e., 150–300°/s) head impulses in the plane of each pair of semicircular canals as the participant attempts to keep the eyes stable on a target in room light. Alshehri et al.¹⁵ used the vHIT to test 56 individuals (29 youth and 27 adults) who were 4–6 months post-concussion. These investigators found no VOR abnormalities, but the test procedure significantly increased headache, dizziness and nausea. In contrast, Balaban et al.¹⁶ found that the computer controlled rotation head impulse test (crHIT), delivered by a rotary chair was sensitive and specific to detect acute concussion when combined with predictive saccade and anti-saccade tests. Therefore, conflicting data exist on the role of peripheral vestibular dysfunction in SRC and better testing methodology should be developed, standardized and validated.

To our knowledge, no study has reported test-retest reliability or normative values for oculomotor and vestibular tests included in the rotary chair protocol for athletes aged 18–24 years. This information is necessary if we are to make clinical decisions such as recommending physical therapy or return to play on the basis of these test results. The purposes of this study were to: 1) describe test-retest reliability and normative data on vestibular and balance tests in a cohort of athletes aged 18–24 years with no current diagnosis of concussion; 2) compare athletes with and without concussion on the protocol subtests; 3) identify subtests to be included in standardized clinical concussion testing protocols.

METHODS

Participants

We recruited 87 healthy athletes (mean age 20.6 years; SD=1.8; 39 F, 48 M) from The University of Alabama at Birmingham (UAB) community. Participants were included if they were aged 18–24 years and stated they currently played a sport. Of these, 41 athletes were UAB football players and 26 were UAB soccer players. The other 20 athletes reported that they were currently involved in other sports. Twenty-four of these individuals had experienced at least one concussion over their lifetime but had recovered. To determine test-retest reliability, 43 of the healthy athletes repeated the measures twice. The community athletes (n=25) were tested twice on the same day, while the UAB football and soccer players (n=18) were tested at the beginning of the 2016 and 2017 seasons. Participants were excluded if they had hearing loss, visual or oculomotor abnormalities, a known neurologic diagnosis or current symptoms of dizziness or headache. Participants were asked to refrain from use of alcohol, tobacco or vestibular suppressants (e.g. meclizine) 48 hours before testing.

We also tested n=28 athletes (average age 20.7 years; SD=1.9; 11 F, 17 M) with SRC referred from UAB athletics or from physicians at UAB Sports Medicine. Thirteen of these athletes reported having experienced a previous concussion in addition to the current concussion. UAB football and soccer players with concussion (n= 17) were tested within 72 hours following injury. Athletes referred from UAB physicians (n= 11) were seen within two weeks of SRC and were not cleared for return to play at the time of testing. Demographic data is provided in Table 1. Institutional Review Board approval was obtained from The University of Alabama at Birmingham and all participants signed an informed consent document.

Table 1:

Demographic Data

	Healthy Cohort (n=87)	Concussed Cohort (n=29)
Age	20.6 ± 1.8	20.7 ± 1.9
Sex	45% F, 55% M	38% F, 62% M
Previous Concussion	27 (28%)	13 (45%)
Race
Caucasian	45 (51%)	13 (45%)
African American	34 (39%)	8 (28%)
Other	8 (9%)	7 (24%)
Ethnicity
Hispanic	6 (7%)	0 (0%)
Not Hispanic	73 (84%)	26 (90%)
Unknown	8 (9%)	3 (10%)
Sport
Football	41 (47%)	13 (45%)
Soccer	27 (31%)	8 (28%)
Other	13 (15%)	8 (28%)

Testing Protocol

For participants with concussion, we obtained baseline dizziness and headache scores on a 0–10 scale, similar to the Vestibular/Ocular Motor Screening tool.¹⁷ While many commonly used concussion tools such as the SCAT-5² utilize a 0–6 scale, we deliberately chose a new scale to prompt the participant to reevaluate their response they may have been giving on SCAT-5 testing up until that point. Following each group of subtests, we asked again for their subjective headache and dizziness scores. If they went up more than three points and the participant stated he or she did not want to continue testing, or if the participant stated he or she did not want to continue testing regardless of a change in symptom severity, we stopped testing. This methodology was based on discussions with the team physician.

A detailed description of all tests used in the protocol are included in Appendix A (Supplemental Digital Content 2, methods description). Participants were tested in a rotary chair ((Neuro Otologic Test Center Chair, I-Portal-NOTC, Neurokinetics, Inc., Pittsburgh, PA) by an experienced, trained examiner who followed standardized instructions. In general, the rotary chair tests the integrity of the horizontal semicircular canals by measuring eye movement response to head movement in complete darkness. The participant was immobilized in the chair, wore infrared goggles that measured eye movements at 100 Hz and communicated with the examiner via a headset. The protocol included two tests of horizontal canal function: 1) Sinusoidal Harmonic Acceleration (SHA): the chair was oscillated right and left at 0.02, 0.04, 0.08, 0.32, 0.64 Hz. The data of interest were the gain and phase of the VOR at each frequency. 2) Step Test: the chair was rotated to the right (60 s), stopped (60 s), rotated to the left (60 s) then stopped (60 s). The parameter of interest was the time constant, i.e., the number of seconds for nystagmus to decrease to 37% of peak velocity, averaged over the four conditions. Two subtests examined the interaction between visual and vestibular systems: 1) Visual Enhancement: The chair was oscillated right and left at 0.64 Hz in the presence of lights, and 2) VOR Cancellation: The chair was oscillated right and left at 0.64 Hz as the participant looked at a red target moving in phase with the chair. The Subjective Visual Vertical and Horizontal (SVV and SVH) subtests examined the participant’s perception of vertical and horizontal in the absence of other visual cues, thought to be mediated by the utricle and central utricular pathways.¹⁸ A straight line stimulus appeared tilted off, up to 30° displacement clockwise or counter-clockwise. The participant pressed buttons to tilt the line to perceived vertical or horizontal for six trials (three preset clockwise and three preset counter-clockwise). The parameters of interest for SVV/SVH were the average degrees off straight alignment and the variance among trials.

To further assess the peripheral vestibular system, specifically the saccule, participants were tested using the cervical Vestibular Evoked Myogenic Potential (c-VEMP), using published methodology and equipment from Intelligent Hearing Systems, Inc (Miami, FL).^19,20 Electrodes were placed over the belly of both sternocleidomastoid muscles. The participant turned the head to contract the SCM while 100 pure tone bursts (500 Hz; 107 dB nHL; 3.1/s) were delivered via monaural earphones, two trials per side. The positive (p13) and negative (n23) EMG waveforms were marked at 13 and 23 ms, respectively. The data of interest were the latency and amplitudes for each ear and the asymmetry ratio, corrected for baseline EMG activity.

Static balance was tested with the EquiTest (Natus Medical Inc., San Carlos, CA) Sensory Organization Test (SOT). The SOT includes six conditions, combining eyes opened/closed, stable/sway referenced surface, and stable/sway referenced visual surround. Two 20 second trials of each condition were completed if the athlete scored above age-matched norms, and three trials if one of the trials had a score that was below age-matched norms. The sway score for each condition was averaged. The data of interest were sway scores at each condition and the composite sway score (0=fall to 100=no sway) as well as the effectiveness ratios, or the sway score of the condition of interest divided by the sway score of condition 1 or baseline sway: visual (4/1), somatosensory (2/1) and vestibular (5/1).

Analysis

Data analysis was performed with SPSS (IBM-SPSS statistics v23IBM Corp,Armonk, NY). Normality was assessed both visually and with Kolmogorov-Smirnov tests of normality for all variables and descriptive statistics were chosen based on normal vs. non-normal distributions. To determine if the data of athletes who completed the test-retest protocol on the same day could be pooled with athletes who completed the tests over a 7–12 month period, we compared the difference scores of test 1 and test 2 between groups for each variable using a t-test. Reliability was described with the Intraclass Correlation Coefficient (ICC) and 95% confidence intervals and described as poor (ICC ≤ 0.40); fair to good (ICC > 0.40 and < 0.75) and excellent (ICC ≥ 0.75).²¹ The magnitude of ICC depends on between subject variability.²² A low ICC could simply reflect low subject variability. For this reason, we also calculated the smallest real difference, which evaluates how much a participant is expected to vary due to chance. Using ICC and the pooled standard deviation of test 1 and test 2, a 95% confidence smallest real difference (SRD) was calculated:²³

SRD = Standard Deviation * √(1-ICC) * √2 * 1.96

The SRD was compared to the mean score to calculate the “% mean,” the SRD divided by the mean score. In a study by Chen et al.²³ a % Mean (i.e. the % of the sample mean represented by the SRD) of <30% was considered acceptable.

Healthy participants (1^st session if tested twice) were compared to participants with concussion using either two tailed unequal variance t-tests or Mann-Whitney U tests at α = 0.05, depending on the normality of the data which was determined both visually and through the use of Kolmogorov-Smirnov tests.

RESULTS

No healthy participant described any significant symptom exacerbation on the 0–10 scale nor asked to stop testing. Of the 28 concussed athletes, 4 did not tolerate any SHA frequency (i.e. they asked to stop at 0.02Hz) and 11 concussed athletes asked to stop during one of the higher frequencies. Most (9/11) were willing to continue following a brief break, but did not complete the task they asked to stop (e.g. if symptoms began during SHA at 0.04Hz, after symptoms returned to baseline we started at 0.08Hz). The 0.64Hz VOR cancellation task rarely provoked symptoms, with only two participants not completing the task at all due to unwillingness to continue following an earlier SHA or step task. We found no significant symptom exacerbation in any individual during VEMP and SOT testing.

There was no significant difference between test 1 and test 2 difference scores for athletes who completed both tests on the same day and those who completed the tests 7–12 months later (p=0.15–0.87, depending on subtest). Therefore, we pooled the data for the reliability analysis. For test-retest reliability results, see Appendix B (Supplemental Digital Content 3, test-retest reliability tables). Appendix B, Tables B1–B4 describe measures of means and standard deviation due to normal distributions of data for all subtests (Kolmogorov-Smirnov p-values all >0.05), ICC, SRD and % mean.

The results for each subtest includes 80–87 healthy athletes and 23–28 athletes with concussion. Not all athletes with concussion completed the entire testing protocol due to symptom provocation. Therefore, the numbers of participants for specific subtest comparisons vary. In addition, the distribution of some of our concussed sample’s data was non-normal based on Kolmogorov-Smirnov testing. The step time constant mean, SVV variance, and SVH variance were non-normally distributed and, therefore, median / range is presented in place of mean / standard deviation. Since at least one variable was non-normally distributed in both the SOT and cVEMP test, median / ranges for all variables were compared between groups using non-parametric analyses.

SHA gain and phase showed poor (ICC=0.40) to excellent (ICC=0.81) reliability depending on the frequency, see Appendix B, Table B1 (Supplemental Digital Content 3, test-retest reliability tables). As a general trend, both gain and phase became less reliable as frequency increased. The SRD of VOR gains varied depending on the frequency with higher frequencies having higher SRD’s. The mean STEP test time constant showed fair/good reliability (ICC= 0.50). The SRD of the STEP test was 9.8 s. There was no significant difference for any of the VOR variables between athletes with and without concussion (p ≥ 0.14, Table 2).

Table 2:

SHA and STEP test performance. Gain values: ratio of eye movement velocity/head movement velocity. Phase values are in degrees.

Sinusoidal Harmonic Acceleration & Step	Healthy (n=80–82) Mean ± SD Median (Range)	Concussed (n=16–24) Mean ± SD Median (Range)	p-value
0.02 Hz Gain	0.42 ± 0.10	0.43 ± 0.08	0.74
0.02 Hz Phase	21.7° ± 6.7	22.5° ± 6.7	0.62
0.04 Hz Gain	0.48 ± 0.11	0.50 ± 0.11	0.57
0.04 Hz Phase	12.2° ± 6.2	12.2° ± 5.2	0.95
0.08 Hz Gain	0.51 ± 0.13	0.51 ± 0.10	0.93
0.08 Hz Phase	4.4° ± 5.1	3.6° ± 4.6	0.54
0.32 Hz Gain	0.50 ± 0.15	0.53 ± 0.13	0.35
0.32 Hz Phase	−2.1° ± 7.2	−3.5° ± 9.5	0.55
0.64 Hz Gain	0.58 ± 0.15	0.61 ± 0.14	0.36
0.64 Hz Phase	−2.1° ± 9.1	−3.4° ± 8.0	0.53
Step Test Mean Time Constant (sec)	13.8 (4.9 – 26.1)	13.2 (7.0 – 18.3)	0.14

VOR cancellation had excellent reliability (ICC=0.79) while visual enhancement had poor (ICC=0.36) reliability, Appendix B, Table B2 (Supplemental Digital Content 3, test-retest reliability tables). The SRD for VOR cancellation gain was 0.08 and for visual enhancement gain was 0.24. SVV/SVH mean angle had fair/good reliability (ICC = 0.69/0.66) while SVV/SVH variance had poor reliability (ICC=0.10 and 0.40, respectively). The SRD for SVV/SVH mean angle was 2.6° and 2.7°, and for SVV/SVH variance was 0.95° and 1.16°, respectively. Concussion (Table 3) negatively affected VOR cancellation gain (p= 0.031), SVV variance (p=0.009), and SVH variance (p=0.006).

Table 3:

Visual-vestibular integration task performance. Average result and standard deviation are shown. Bolded and underlined p-values indicate significance at α=0.05.Gain values are ratio of eye movement velocity/head movement velocity. SVV/SVH values are in degrees.

Visual-Vestibular Integration Test	Healthy (n=83–87) Mean ± SD Median (Range)	Concussed (n=24–28) Mean ± SD Median (Range)	p-value
Visual Enhancement Gain	1.01 ± 0.11	1.01 ± 0.11	0.77
VOR Cancellation Gain	0.16 ± 0.06	0.19 ± 0.07	0.031
Subjective Visual Vertical Mean Error	0.49° ± 1.69	−0.12° ± 1.93	0.13
Subjective Visual Vertical Variance	0.56° (0.05 – 17.29)	1.36° (0.04 – 95.98)	0.009
Subjective Visual Horizontal Mean Error	0.51° ± 1.67	0.08° ± 2.11	0.33
Subjective Visual Horizontal Variance	0.50° (0.05 – 10.10)	1.00° (0.03 – 17.8)	0.006

All c-VEMP measures (i.e. amplitude and latency of right and left ear responses) except right ear P1 latency (ICC = 0.15) had fair/good to excellent (ICC=0.63–0.86) reliability, Appendix B, Table B3 (Supplemental Digital Content 3, test-retest reliability tables). The corrected IAD ratio was not normally distributed and the median corrected IAD ratio for the healthy participants was 15% (range 0–73%). The SRDs for corrected amplitudes were 20% for the right and 34% for the left ear. There were no significant differences in c-VEMP results between athletes with and without concussion (p ≥ 0.18, Table 4).

Table 4:

Healthy vs concussed c-VEMP results.

c-VEMP	Healthy (n=72) Median (Range)	Concussed(n=16) Median (Range)	p-value
P1 Latency Right (ms)	14.0 (12.8 – 19.6)	14.2 (12.6 – 15.4)	0.89
P1 Latency Left (ms)	13.8 (12 – 18.8)	14.0 (12.8 – 16.6)	0.67
N1 Latency Right (ms)	21.3 (17.8 – 29.4)	22.7 (18.4 – 25.4)	0.65
N1 Latency Left (ms)	20.6 (16.6 – 24.8)	21.0 (18.6 – 23.0)	0.99
P1-N1 Amp Right (μV)	138 (4 – 340)	129 (38 – 224)	0.29
P1-N1 Amp Left (μV)	135 (16 – 368)	115 (26 – 222)	0.18
Corr P1-N1 Amp Right (μV)	21 (5 – 165)	18 (6 – 38)	0.20
Corr P1-N1 Amp Left (μV)	18 (2 – 175)	17 (3 – 34)	0.55
IAD Ratio (%)	18 (1 – 69)	20 (0 – 47)	0.96
Corrected IAD Ratio (%)	15 (0 – 73)	24 (1 – 38)	0.44

SOT ICCs ranged from fair/good (ICC=0.64) to excellent (ICC=0.87) depending on the condition, Appendix B, Table B4 (Supplemental Digital Content 3, test-retest reliability tables). SRDs for sway scores ranged from 3.1 for condition 1 to 23.1 for condition 6. The composite score (ICC=0.72) had an SRD of 15.9. SOT performance was significantly worse (i.e. more sway) on all conditions in the athletes with concussion (p<0.001 to 0.049, Table 5).

Table 5:

Healthy vs Concussed SOT performance. Bolded and underlined p-values indicate a significant difference between groups at α=0.05. For all SOT conditions, a score of zero indicates a fall and a score of 100 indicates no sway.

Sensory Organization Test	Healthy (n=85) Median (Range)	Concussed (n=26) Median (Range)	p-Value
Condition 1	95.0 (89.3 – 98.0)	94.3 (81.3 – 98.0)	0.0492
Condition 2	92.5 (82.3 – 96.5)	89.8 (26.0 – 96.0)	0.0004
Condition 3	92.5 (69.7 – 97.0)	91.0 (10.3 – 96.0)	0.0024
Condition 4	79.3 (30.5 – 94.5)	74.2 (0.0 – 89.5)	0.0077
Condition 5	63.5 (28.0 – 82.5)	57.5 (0.0 – 72.5)	0.0083
Condition 6	64.5 (22.7 – 85.0)	54.7 (0.0 – 72.5)	0.0028
Total Score	75.0 (17.0 – 89.0)	70.0 (8.0 – 85.0)	0.02

DISCUSSION

Normative Data and Test-Retest Reliability

All subtests resulted in normally distributed data for our healthy cohort of 18–24-year-old athletes, indicating that the mean and standard deviations presented in Appendix B (Supplemental Digital Content 3, test-retest reliability tables) could be beneficial for contextualizing individual performance on these measures.

The ICC values for subtest parameters varied from poor to excellent. According to Weir et al.²² the magnitude of the ICC depends on variability among subjects. Therefore, a low ICC could reflect low between subject variability. For this reason, we also calculated the smallest real difference so that clinicians using these tests can know how much a measure is expected to vary due to chance. In a study by Chen et al.²³ a percent (%) mean (i.e. the % of the sample mean represented by the SRD) of <30% was considered acceptable. The tests in our protocol with a % mean < 30% included SHA 0.02 Hz gain, visual enhancement gain, c-VEMP latencies, SOT conditions 1–4 and SOT composite score. Although we used procedures recommended by the manufacturer of the equipment and published methodologies, the poor reliability of some of the measures suggest that these tests should be re-examined to determine if changes in protocol and/or measurement could give better reliability. For example, higher SHA frequencies appear to be associated with lower reliability. These tests are typically completed quicker than SHA at lower frequencies and therefore, it might be advisable to perform more than one trial. The ICC for the average of the four time constants of the VOR step tests (ICC=0.50) was higher than the ICCs of each time constants (ICC= 0.30), indicating that the average time constant is a more reliable measure. Some subtests are dependent upon participant effort and alertness. We used standardized instructions during all subtests to ensure that the participants were alert and engaged, but attentional and alertness factors may be difficult to control in individuals with concussion.

The low ICC of the c-VEMP right ear P1 latency was surprising due to fair/good to excellent reliability in all other c-VEMP measures. c-VEMP is a subcortical reflex and depends only on the participant maintaining tonic EMG activity of the sternocleidomastoid (50–250 μV), which is monitored throughout the test. The SOT had fair/good to excellent test-retest reliability. However, conditions 5 and 6 had a % mean that was > 30%. In our protocol, if the athlete scored above age-matched norms, they completed only two trials of each condition. This was adequate for conditions 1–4. However, reliability of conditions 5 and 6 can potentially be improved by always executing three trials of these conditions, which is currently the max number of trials allowed by the system.

Comparison of athletes with and without SRC

When comparing athletes with and without SRC, there was no difference in VOR gain or phase indicating that the function of the peripheral vestibular system and brainstem/cerebellar VOR pathways was unaffected. These VOR subtests tend to be symptom provoking in athletes with concussion, do not have strong test-retest reliability and may not be necessary to include in a concussion protocol. Similarly, c-VEMP showed no significant differences between athletes with and without SRC, providing further evidence that the peripheral vestibular system and brainstem/cerebellar pathways were unaffected.

In contrast, athletes with SRC had a significantly higher gain with VOR cancellation. In this subtest, the eye response should be close to zero, since the participant is asked to focus on a target that is moving in phase with the chair. This indicates an altered ability of the smooth pursuit system to generate an equal and opposite signal to overwrite, at the level of the secondary vestibular neurons, the ongoing VOR response. Smooth pursuit is a voluntary cortical response involving the frontal and supplementary eye fields.²⁴ Athletes with SRC also had a significantly larger variance of SVV/SVH, more than twice that of healthy athletes. There was no significant difference in mean SVV/SVH angle, only in variance, indicating that single trials of SVV/SVH may contain valuable information that is lost when averaging the responses. These results suggest that the neural circuitry that integrates the vestibular and visual information might be affected by SRC. Tests evaluating this integration should be further explored in concussion. In the case of SVV/SVH variance, the methodology should be reviewed to improve the repeatability of the variance measures.

Athletes with SRC had significantly more sway than healthy athletes on all conditions of the SOT, including condition 1, where the participant is required to stand still on a stable surface with the eyes open. The finding of lower SOT scores is in agreement with another study that showed that SOT was sensitive for athletes with concussion.²⁵ It would be interesting to determine whether the poor balance experienced by athletes with concussion is related to larger SVV/SVH variance, abnormal VOR cancellation and other measures of oculomotor function. In addition, it would be useful to compare the sensitivity of the SOT relative to other measures developed for the assessment of balance function impairment in concussed athletes.²⁶

Taken together, these results suggest that concussion may alter central processing of vestibular and visual information while not affecting the peripheral vestibular organs and associated brainstem- and cerebellar-level processes. These findings are in agreement with current understanding of the nature of a concussion injury. From a neurometabolic point of view, after a concussion it could be more difficult for higher-order processes to take place due to changes in ion flow whereas simple three-neuron reflexes like the VOR might not show much change.²⁷ On the other hand, it may be not a problem with visual-vestibular integration but instead a problem with attention, which is required for the VOR cancellation and SVV/SVH tests. However, this would not explain the increased sway on the SOT.

CONCLUSION

Test-retest reliability of clinical vestibular measures vary, even at different conditions of the same task: for instance, VOR testing frequencies. Larger reliability studies will better ascertain which of these tasks are reliable and therefore useful for clinicians.

SRC appears to alter central integration of vestibular function, preferentially decreasing performance in higher-order integrative tasks requiring vestibular input (balance, subjective vertical) while not affecting primary vestibular reflexes (i.e. VOR and cVEMP). Future research should specifically examine tasks of vestibular integration, their neural substrate and mechanism of injury to determine if they could inform decision making and track progress for athletes with concussion.

Supplementary Material

Supplemental Data File (.doc, .tif, pdf, etc.)_1

Supplemental Digital Content 1: Video Abstract. mp4

Supplemental Data File (.doc, .tif, pdf, etc.)_2

Supplemental Digital Content 2: Detailed Methodology. pdf

Supplemental Video File

Supplemental Digital Content 3: Test-Retest Reliability Tables. pdf