Abstract
OBJECTIVE:
The main objective of this study was to assess whether objective vestibular, oculomotor, and balance functions were impaired in children with a current diagnosis of concussion with vestibular and/or ocular symptoms.
SETTING:
Data was collected in a vestibular/ocular clinical lab. Patient participants were recruited from a concussion clinic in a children’s hospital.
PARTICIPANTS:
33 children ages 8-17 with a current diagnosis of concussion and vestibular and/or ocular symptoms and 30 children without concussion.
DESIGN:
Cross-sectional single visit study.
MAIN OUTCOME MEASURES:
Eye-tracking rotary chair oculomotor and vestibular measures, vestibular evoked potentials, and static posturography.
RESULTS:
There were no statistically significant differences on any clinical measure between children with concussion and children without concussion. Younger children without concussion performed significantly worse on several rotary chair and balance measures compared to older children without concussion.
CONCLUSIONS:
No vestibular, oculomotor, or balance measures were significantly different between children with concussion and children without concussion, suggesting these measures may not be useful in the evaluation of a child with concussion and vestibular and/or oculomotor symptoms. Future research should investigate age effects and other vestibular and oculomotor tests to identify objective findings that better relate to vestibular and/or ocular symptoms in children with concussion.
Keywords: Concussion, pediatric, vestibular, oculomotor, balance
Background
Vestibular and oculomotor related symptoms are common following concussion and include poor balance, dizziness, and headache during head and eye movements[1–4] A common tool used to assess the severity of these symptoms in children is the Vestibular Ocular Motor Screening Tool (VOMS).[5–9] The VOMS, by quantifying these symptoms, helps guide interventions such as vestibular rehabilitation and has been correlated with recovery time.[10–15] However, as the VOMS primarily focuses on symptom provocation it does not provide as objective an assessment of vestibular and ocular function as clinical tools such as eye-tracking videography or force-plate posturography.
Previous studies have used those more objective tools to better understand post-concussion symptoms in pediatric patients. Clinical tests and eye-tracking have been used to measure saccades, smooth pursuit, and accommodation in adolescents with and without concussion.[16 17] Benign paroxysmal positional vertigo (BPPV) has been suggested as a source of vestibular symptoms children following concussion.[18 19] Other studies suggest lack of impairment to the vestibular apparatus and the vestibular-ocular reflex (VOR) following concussion.[20–23] One group found no correlation between VOR function and balance nor VOMS, hypothesizing that changes in vestibular function following concussion may be central in origin and not recognized with typical vestibular testing.[21] A publication from this lab in college-aged athletes likewise found no differences in VOR nor cervical vestibular evoked myogenic potentials (cVEMP), but did find deficits in balance and perception of vertical post-concussion, suggesting vestibular reflexes are intact but central mechanisms are impaired.[22]
There are other potential issues with using oculomotor, vestibular, and balance tasks in children due to developmental stages. First, it has been suggested that even children without concussion may fail or not be developmentally able to complete tasks like the VOMS.[23] Secondly, there is debate around what age balance function becomes “adult-like”, with some research suggesting there is continual improvement in balance function until adulthood and some suggesting children should be adult-like by age 8, emphasizing the need to identify age-related factors affecting performance.[24–29]
A better understanding of vestibular and oculomotor function following concussion will help determine the role played by these systems in post-concussion symptoms. The purpose of this study was to conduct a robust objective vestibular and oculomotor examination on a pediatric sample with concussion and vestibular and ocular symptoms and compare those results to a pediatric sample without concussion. In addition, we sought to identify whether the age of the child impacts results on these tests.
Methods
Ethical Considerations
Institutional review board approval was obtained, and all participants and parents signed informed consent/assent forms.
Group Demographics, Concussion, and Sport History
33 athletic pediatric patients (13.1 ± 2.4 years, 19 male and 14 female) with a diagnosis of sports-related concussion and vestibular and/or oculomotor symptoms from a concussion clinic and 30 non-concussed athletic children (12.8 ± 3.0 years, 18 male and 12 female) were recruited. “Athletic” was defined as participating in organized sports in the past year. The racial demographics for the sample with concussion were 1 Asian, 3 Black/African American, 1 Mixed, and 28 White. For the sample without concussion, 6 Black/African American and 24 White. Participants were recruited if they were between 8 and 17 years of age to align with findings that SOT performance maturation occurs around age 6/7; age 8 was chosen to be past that threshold.[28]
Participants with concussion were referred by the concussion clinic physician for the study due to reporting persistent vestibular and/or ocular symptoms and demonstrating exacerbation of those symptoms on VOMS testing. A specific symptom cutoff score was not used. Non-concussed children were recruited by word of mouth and mainly consisted of children from the sports teams of participants with concussion to ensure our two samples experienced similar activity levels. Participants without concussion were required to be at least one year out from medical clearance from any previous concussion. Participants were screened for previous diagnosis of vestibular and/or ocular disease and those with previous diagnoses were not included. Participants also reported their number of previously diagnosed concussions (participants with concussion did not include their current diagnosis in the number).
Participants reported their number of seasons playing specific sports. Sports were classified as contact or non-contact. Contact sports included sports where players make frequent contact with each other (e.g.: football, soccer) while non-contact included sports where contact occurs but is infrequent (e.g.: baseball, softball) or unlikely (e.g.: tennis, golf).
Rotary Chair Testing
Participants were tested in a computerized rotary chair (Neurolign Technologies, formerly Neurokinetics I-Portal Neurotologic Test Center). The participant was immobilized in the chair, wore infrared goggles that recorded eye movements, and communicated with the examiner via headset.
The session began with tests of oculomotor function: Horizontal and Vertical saccades: participants followed a dot stimulus as it stepped randomly along the horizontal/vertical meridian. The data of interest were the primary saccade accuracy (% distance the eyes moved towards the target) and latency. Horizontal and Vertical smooth pursuit (SP): participants followed a moving target along the horizontal/vertical meridian at 0.75Hz (Vertical) and 1.0Hz (Horizontal). The data of interest were the position gain of SPs, calculated as the ratio between the participant’s eye gaze location and the target stimulus’ location (1.0 indicating perfect tracking, >1.0 indicating tracking ahead of the target and <1.0 indicating lagging behind). Optokinetic reflex (OKN): participants watched a random dot pattern projected on the enclosure that moved counterclockwise then clockwise at 20°/s or 60°/s for 20 seconds each. The data of interest included velocity gain of the optokinetic response, calculated as the ratio of the participant’s fast phase eye movement velocity and the speed of the stimulus.
The vestibular protocol included: Sinusoidal Harmonic Acceleration (SHA): The chair oscillated right and left 0.64Hz to assess horizontal canal function. The data of interest were the velocity gain of the VOR (ratio between participant slow phase eye movement velocity and the chair’s velocity). Visual Enhancement and Cancellation (vestibular/visual interaction): The chair was oscillated right and left at 0.64Hz in the presence of the stationary optokinetic pattern (enhancement) or with a single dot stimulus moving in synchrony with the chair (cancellation). The data of interest were the enhancement and cancellation %, calculated as the ratio between the velocity gain on these tasks and the participant’s 0.64Hz SHA gain. Step Test: The chair rotated to the right at a constant velocity for 60s. Following an identical deceleration, the chair was stopped and kept still for 60s. The stimuli were repeated leftwards. The phases were responsible for VOR activation, with the 60s periods at constant velocity or no motion following the progress of the VOR response until its complete decay. The data of interest was the average decay time constant (i.e., the time in seconds for nystagmus to decrease to 37% of peak velocity – calculated from a curve from the participant’s peak eye velocity after acceleration/deceleration).
Finally, the Subjective Visual Vertical (SVV) test examined the participant’s perception of vertical. A line stimulus appeared tilted up to 30° clockwise or counterclockwise. The participant pressed buttons to tilt the line to perceived vertical for 6 trials. The data of interest were the average degrees off true alignment and the variance across trials.
Balance Testing
Balance was tested with the EquiTest (Natus) Sensory Organization Test (SOT). The SOT consists of 6 balance conditions where the participant is asked to stand still: Condition 1: Eyes Open, Stable Surface & Surround; Condition 2: Eyes Closed Stable Surface; Condition 3: Eyes Open Stable Surface, Sway-Referenced Surround; Condition 4: Eyes Open, Sway-Referenced Surface, Stable Surround; Condition 5: Eyes Closed, Sway-Referenced Surface; Condition 6: Eyes Open, Sway-Referenced Surface & Surround. Three 20s trials were completed for each condition. The equilibrium score calculated by the SOT software for each condition was averaged. The equilibrium score is calculated using the equation Equilibrium Score = [12.5 − (Maximum Anterior Sway Angle − Maximum Posterior Sway Angle)] / 12.5, where 12.5 is the estimated limit of sway in degrees in the sagittal plane, and an equilibrium score of 100 indicates no sway at all and 0 indicates a fall. The data of interest were average equilibrium scores for each condition and the composite score.
As the equilibrium score calculated by the SOT only considers the maximum anterior/posterior (AP) angles with the platform, higher-order balance analyses were completed.[30] Force plate data was processed in R as described by Schubert, 2014.[31] Center-of-pressure (CoP) data at 100Hz were filtered using a fourth order Butterworth, zero-phase low-pass filter at 5Hz. Trials where the participant fell were not analyzed. The sway length, sway amplitude (furthest point from average), average sway velocity in both the AP and medial-lateral (ML) direction, and the 95% confidence sway area (the area of the ellipse containing 95% of CoP points) were calculated for each trial. These measures were averaged across trials for each condition.
Cervical Vestibular-Evoked Myogenic Potentials
To assess vestibular saccular function, cVEMPs were measured using methodology and equipment from Intelligent Hearing Systems, Inc (Miami, Florida).[32 33] Electrodes were placed over sternocleidomastoid muscles. The participant turned and raised their head to contract the muscle while 100 pure tone bursts (500Hz; 107 dB nHL; 3.1/second) were delivered via monaural earphones, 2 trials per side. The positive (p13) and negative (n23) electromyogram (EMG) waveform peaks were marked. The data of interest were the latency and amplitudes for each ear and the inter-aural asymmetry ratio (IAD), corrected for baseline EMG.
Age Groups
During data collection, it was difficult to describe tasks to individuals under the age of 13. In addition, even in our control sample, participants under the age of 13 had a harder time completing Conditions 5&6 of the SOT without falling. 9/14 controls under the age of 13 fell during at least one Condition 5 trial compared to 3/16 controls age 13 or older. For these reasons, additional analyses were planned to compare results between participants ages 8-12 and participants ages 13-17.
Statistical Analysis
Statistics were completed using SPSS v.26. Age and previous concussions were compared between participants with and without concussion with a Student’s t-test. Sex distributions were compared using a χ-square test.
All data were assessed for normality visually. Not all variables for smaller group analyses were normally distributed so, to be able to compare easily across groups, medians and interquartile ranges were calculated and non-parametric bi-variate analyses (2-tailed Mann-Whitney U-tests) were used. P-values were rounded to nearest hundredth. P-values for clinical tests were ranked from smallest to largest and adjusted based on the Benjamini-Hochberg method for multiple comparisons (the smaller of either the next higher p-value rank’s adjusted p-value or (Raw p-value * Number of Comparisons / Rank of Raw p-value)). Adjusted p-values were considered statistically significant if lower than a 0.10 false discovery rate due to the exploratory nature of this study.
Four Mann-Whitney U comparisons were performed:
Participants with vs without concussion
8-12YOs vs 13-17YOs without concussion
8-12YOs with vs 8-12YOs without concussion
13-17YOs with vs 13-17YOs without concussion
Results
Demographics and Concussion History(Table 1)
Table 1 –
Sample Demographics for Children With and Without Concussion
| Non-Concussed | Concussed | p-value | |
|---|---|---|---|
| Age | 12.8 ± 3.0 | 13.1 ± 2.4 | 0.71 |
| Sex | 60% M 40% F | 58% M 42% F | 0.85 |
| Previous Concussions | 0.2 ± 0.4 | 0.8 ± 1.5 | 0.03 |
| Seasons of Sport | 13 (9) | 9 (10) | 0.29 |
| Seasons of Contact Sport | 8 (9) | 3 (7) | 0.03 |
| Time Since Concussion | - | 60 Days (98) |
Data presented as Mean ± Standard Deviation or Median (IQR). An unrounded p<0.05 was considered statistically significant. Statistically significant p-values are bolded and underlined.
There was no significant difference in age, sex, or total seasons of sport between participants with concussion and participants without concussion. Participants with concussion reported significantly more previous concussions(p=0.03). Participants with concussion were a median of 60 days from injury. There was no difference in seasons of general sport between groups, but participants without concussion reported significantly more seasons of contact sport (p=0.03).
For subgroup analyses, there was no significant difference in sex between the younger and older children without concussion (p=0.25) nor the older group with and older group without concussion (p=0.07). There were significantly more females in the younger group with concussion when compared to the younger group without concussion (7M and 7F compared to 1M and 11F).
Participants With and Without Concussion (Table 2, Supplemental Table 1)
Table 2 –
Participants With Concussion vs Participants Without Concussion
| Participants Without Concussion (n=30) | Participants With Concussion (n=33) | Raw p-value | Adjusted p-value | |
|---|---|---|---|---|
| Sensory Organization Test | ||||
| Condition 1 | 92.5 (3.6) | 91.5 (7.5) | 0.06 | 0.44 |
| Condition 2 | 90.3 (4.7) | 89.0 (11.0) | 0.02 | 0.44 |
| Condition 3 | 89.8 (8.2) | 89.0 (9.5) | 0.41 | 0.78 |
| Condition 4 | 73.8 (17.1) | 69.3 (16.6) | 0.33 | 0.78 |
| Condition 5 | 46.1 (29.1) | 48.5 (36.8) | 0.80 | 0.90 |
| Condition 6 | 45.3 (27.3) | 55.5 (26.4) | 0.21 | 0.75 |
| Composite Score | 68.0 (17.8) | 70.0 (17.5) | 0.92 | 0.92 |
| Cervical VEMP | ||||
| Average P1 Latency (ms) | 14.1 (1.4) | 13.9 (1.2) | 0.24 | 0.75 |
| Average N1 Latency (ms) | 20.4 (2.0) | 20.7 (2.8) | 0.53 | 0.78 |
| Average Amplitude (μV) | 19.8 (14.5) | 22.2 (10.5) | 0.49 | 0.78 |
| IAD Ratio | 13.7 (24.4) | 15.2 (23.2) | 0.77 | 0.90 |
| Rotary Chair Vestibular | ||||
| 0.64Hz SHA Gain | 0.73 (0.18) | 0.69 (0.21) | 0.76 | 0.90 |
| Enhancement % | 143.5 (41.8) | 130.5 (30.0) | 0.30 | 0.78 |
| Cancellation % | 72.8 (12.4) | 70.7 (15.0) | 0.53 | 0.78 |
| Vestibular Time Constant | 11.8 (4.0) | 12.1 (4.5) | 0.52 | 0.78 |
| Subjective Vertical Average | −0.8 (2.4) | −0.2 (2.8) | 0.20 | 0.75 |
| Subjective Vertical Variance | 1.1 (2.2) | 1.9 (5.3) | 0.07 | 0.44 |
| Oculomotor Function | ||||
| Smooth Pursuit | ||||
| 1.0Hz Horizontal | 0.82 (0.19) | 0.75 (0.29) | 0.17 | 0.75 |
| 0.75Hz Vertical | 0.84 (0.28) | 0.85 (0.27) | 0.88 | 0.92 |
| Saccades | ||||
| Horizontal Accuracy | 92.0 (10.4) | 89.0 (8.5) | 0.04 | 0.44 |
| Horizontal Latency | 210 (34) | 210 (63) | 0.38 | 0.78 |
| Vertical Accuracy | 97.7 (20.1) | 98.7 (26.9) | 0.68 | 0.90 |
| Vertical Latency | 234 (49) | 224 (76) | 0.78 | 0.90 |
| Optokinetic Reflex | ||||
| 20 Deg/s Gain | 0.84 (0.18) | 0.84 (0.22) | 0.37 | 0.78 |
| 60 Deg/s Gain | 0.53 (0.26) | 0.56 (0.37) | 0.83 | 0.90 |
Data presented as Median (IQR). P-values were adjusted using the Benjamini-Hochberg method. Statistically significant Benjamini-Hochberg p-values at a false discovery rate of 0.10 are bolded and underlined.
There were no statistically significant differences on any rotary chair, VEMP, or SOT measure between participants with and without concussion.
8-12YOs vs 13-17YOs Without Concussion (Table 3, Supplemental Table 2)
Table 3 –
8-12 YO vs 13-17 YO Children Without Concussion
| 8-12 YO Without Concussion (n=13) | 13-17 YO Without Concussion (n=17) | Raw p-value | Adjusted p-value | |
|---|---|---|---|---|
| Sensory Organization Test | ||||
| Condition 1 | 91.0 (2.9) | 94.5 (3.5) | 0.01 | 0.09 |
| Condition 2 | 89.0 (7.4) | 93.0 (4.3) | 0.02 | 0.09 |
| Condition 3 | 85.5 (6.8) | 91.0 (7.3) | 0.05 | 0.14 |
| Condition 4 | 73.5 (15.0) | 77.0 (19.8) | 0.07 | 0.16 |
| Condition 5 | 34.7 (29.0) | 55.5 (25.6) | 0.03 | 0.09 |
| Condition 6 | 43.0 (23.3) | 49.5 (36.0) | 0.34 | 0.46 |
| Composite Score | 61.0 (13.5) | 70.0 (14.5) | 0.02 | 0.09 |
| Cervical VEMP | ||||
| Average P1 Latency (ms) | 13.9 (1.2) | 14.6 (1.4) | 0.06 | 0.15 |
| Average N1 Latency (ms) | 19.5 (2.3) | 20.8 (1.9) | 0.03 | 0.09 |
| Average Amplitude (μV) | 16.6 (17.2) | 21.8 (11.1) | 0.13 | 0.27 |
| IAD Ratio | 12.8 (27.7) | 16.0 (24.4) | 0.35 | 0.46 |
| Rotary Chair Vestibular | ||||
| 0.64Hz SHA Gain | 0.73 (0.18) | 0.69 (0.21) | 0.76 | 0.88 |
| Enhancement % | 135.0 (52.7) | 151.8 (36.8) | 0.32 | 0.46 |
| Cancellation % | 71.0 (12.0) | 70.7 (12.0) | 0.87 | 0.88 |
| Vestibular Time Constant | 12.0 (7.0) | 11.8 (3.6) | 0.77 | 0.88 |
| Subjective Vertical Average | −1.3 (4.1) | −0.7 (1.7) | 0.88 | 0.88 |
| Subjective Vertical Variance | 2.0 (4.7) | 0.7 (1.6) | 0.03 | 0.09 |
| Oculomotor Function | ||||
| Smooth Pursuit | ||||
| 1.0Hz Horizontal | 0.77 (0.27) | 0.83 (0.14) | 0.17 | 0.33 |
| 0.75Hz Vertical | 0.72 (0.34) | 0.89 (0.17) | 0.03 | 0.09 |
| Saccades | ||||
| Horizontal Accuracy | 91.6 (11.2) | 93.2 (9.6) | 0.50 | 0.63 |
| Horizontal Latency | 218 (17) | 190 (39) | 0.01 | 0.09 |
| Vertical Accuracy | 100.0 (20.9) | 96.5 (18.3) | 0.21 | 0.37 |
| Vertical Latency | 238 (53) | 224 (67) | 0.22 | 0.37 |
| Optokinetic Reflex | ||||
| 20 Deg/s Gain | 0.87 (0.18) | 0.81 (0.18) | 0.28 | 0.44 |
| 60 Deg/s Gain | 0.53 (0.27) | 0.44 (0.26) | 0.87 | 0.88 |
Data presented as Median (IQR). P-values were adjusted using the Benjamini-Hochberg method. Statistically significant Benjamini-Hochberg p-values at a false discovery rate of 0.10 are bolded and underlined.
Age-group analyses comparing 8-12YOs without concussion to 13-17YOs without concussion revealed the younger group had significantly lower vertical SP gain and higher horizontal saccade latency (Benjamini-Hochberg p=0.09).
There were no significant differences in VOR gains. Younger participants had a higher variance in SVV (Benjamini-Hochberg p=0.09) but no difference in average response.
On cVEMPs, the younger group showed faster N1 latencies (Benjamini-Hochberg p=0.09).
In 3/6 SOT Conditions (Condition 1, 2, and 5) and overall score, the younger group exhibited worse performance (Benjamini-Hochberg p=0.09).. No higher-order balance measures were different across age groups.
8-12YOs With vs 8-12YOs Without Concussion (Table 4, Supplemental Table 3)
Table 4 –
8-12 YOs With vs Without Concussion
| 8-12 YO Without Concussion (n=13) | 8-12 YO With Concussion (n=12) | Raw p-value | Adjusted p-value | |
|---|---|---|---|---|
| Sensory Organization Test | ||||
| Condition 1 | 91.0 (2.9) | 88.0 (5.2) | 0.12 | 0.83 |
| Condition 2 | 89.0 (7.3) | 86.3 (10.6) | 0.30 | 0.83 |
| Condition 3 | 85.5 (6.8) | 85.4 (17.0) | 0.69 | 0.96 |
| Condition 4 | 73.5 (14.8) | 68.0 (10.7) | 0.44 | 0.88 |
| Condition 5 | 34.7 (28.9) | 37.6 (25.7) | 0.98 | 0.98 |
| Condition 6 | 43.0 (23.3) | 44.3 (27.1) | 0.38 | 0.88 |
| Composite Score | 61.0 (13.5) | 61.0 (14.0) | 0.91 | 0.98 |
| Cervical VEMP | ||||
| Average P1 Latency (ms) | 13.9 (1.2) | 13.4 (0.1) | 0.21 | 0.83 |
| Average N1 Latency (ms) | 19.5 (2.3) | 19.1 (1.1) | 0.29 | 0.83 |
| Average Amplitude (μV) | 16.6 (17.2) | 20.1 (12.6) | 0.19 | 0.83 |
| IAD Ratio | 12.8 (27.8) | 15.3 (30.0) | 0.70 | 0.96 |
| Rotary Chair Vestibular | ||||
| 0.64Hz SHA Gain | 0.75 (0.23) | 0.72 (0.29) | 0.89 | 0.98 |
| Enhancement % | 135.1 (52.7) | 127.2 (22.6) | 0.45 | 0.88 |
| Cancellation % | 71.0 (12.0) | 66.0 (10.7) | 0.17 | 0.83 |
| Vestibular Time Constant | 12.0 (6.9) | 11.4 (4.5) | 0.81 | 0.97 |
| Subjective Vertical Average | −1.25 (4.0) | −0.7 (3.3) | 0.30 | 0.83 |
| Subjective Vertical Variance | 2.0 (4.7) | 2.8 (9.3) | 0.25 | 0.83 |
| Oculomotor Function | ||||
| Smooth Pursuit | ||||
| 1.0Hz Horizontal | 0.77 (0.28) | 0.79 (0.26) | 0.77 | 0.96 |
| 0.75Hz Vertical | 0.72 (0.34) | 0.92 (0.33) | 0.19 | 0.83 |
| Saccades | ||||
| Horizontal Accuracy | 91.6 (11.2) | 89.3 (13.7) | 0.61 | 0.96 |
| Horizontal Latency | 220 (16) | 209 (72) | 0.50 | 0.89 |
| Vertical Accuracy | 100.1 (21.2) | 103.5 (36.3) | 0.77 | 0.96 |
| Vertical Latency | 240 (53) | 253 (74.0) | 0.77 | 0.96 |
| Optokinetic Reflex | ||||
| 20 Deg/s Gain | 0.87 (0.18) | 0.80 (0.40) | 0.46 | 0.88 |
| 60 Deg/s Gain | 0.53 (0.27) | 0.50 (0.46) | 0.97 | 0.98 |
Data presented as Median (IQR). P-values were adjusted using the Benjamini-Hochberg method. Statistically significant Benjamini-Hochberg p-values at a false discovery rate of 0.10 are bolded and underlined.
There were no significant differences in any clinical test between younger participants with and younger participants without concussion.
Younger children with concussion showed significantly higher AP path length on Condition 2, AP mean velocity on Condition 1, and ML path length and velocity in SOT Conditions 1 and 3 in our higher-order balance analysis (Benjamini-Hochberg p=0.07).
13-17YOs With vs 13-17YOs Without Concussion (Table 5, Supplemental Table 4)
Table 5 -.
13-17 YOs With vs Without Concussion
| 13-17 YO Without Concussion (n=17) | 13-17 YO With Concussion (n=21) | Raw p-value | Adjusted p-value | |
|---|---|---|---|---|
| Sensory Organization Test | ||||
| Condition 1 | 94.5 (3.5) | 92.7 (6.0) | 0.05 | 0.25 |
| Condition 2 | 93.0 (4.3) | 89.0 (9.2) | 0.01 | 0.25 |
| Condition 3 | 91.0 (7.3) | 90.7 (7.4) | 0.37 | 0.83 |
| Condition 4 | 77.0 (19.8) | 73.0 (20.5) | 0.42 | 0.83 |
| Condition 5 | 55.5 (25.6) | 54.5 (34.1) | 0.82 | 0.98 |
| Condition 6 | 49.5 (36.0) | 59.5 (26.7) | 0.5 | 0.83 |
| Composite Score | 70.0 (14.5) | 71.0 (18.5) | 0.73 | 0.96 |
| Cervical VEMP | ||||
| Average P1 Latency (ms) | 14.6 (1.4) | 14.1 (1.9) | 0.72 | 0.96 |
| Average N1 Latency (ms) | 20.8 (1.9) | 21.9 (2.7) | 0.04 | 0.25 |
| Average Amplitude (μV) | 21.8 (11.1) | 22.5 (9.5) | 0.98 | 1.00 |
| IAD Ratio | 16.0 (24.4) | 15.1 (20.3) | 0.45 | 0.83 |
| Rotary Chair Vestibular | ||||
| 0.64Hz SHA Gain | 0.69 (0.14) | 0.69 (0.21) | 0.85 | 0.98 |
| Enhancement % | 151.8 (36.8) | 131.8 (37.0) | 0.50 | 0.83 |
| Cancellation % | 73.1 (17.0) | 74.4 (17.0) | 1.00 | 1.00 |
| Vestibular Time Constant | 11.8 (3.6) | 13.5 (6.8) | 0.16 | 0.50 |
| Subjective Vertical Average | −0.7 (1.7) | −0.2 (3.1) | 0.46 | 0.83 |
| Subjective Vertical Variance | 0.7 (1.6) | 1.3 (4.5) | 0.10 | 0.42 |
| Oculomotor Function | ||||
| Smooth Pursuit | ||||
| 1.0Hz Horizontal | 0.83 (0.14) | 0.73 (0.37) | 0.04 | 0.25 |
| 0.75Hz Vertical | 0.89 (0.17) | 0.84 (0.21) | 0.18 | 0.50 |
| Saccades | ||||
| Horizontal Accuracy | 93.2 (9.6) | 87.7 (10.2) | 0.03 | 0.25 |
| Horizontal Latency | 190 (39) | 214 (61) | 0.12 | 0.43 |
| Vertical Accuracy | 96.5 (18.3) | 97.3 (24.5) | 0.57 | 0.89 |
| Vertical Latency | 224 (67) | 222 (52) | 0.86 | 0.98 |
| Optokinetic Reflex | ||||
| 20 Deg/s Gain | 0.81 (0.18) | 0.84 (0.15) | 0.91 | 0.99 |
| 60 Deg/s Gain | 0.44 (0.26) | 0.56 (0.32) | 0.71 | 0.96 |
Data presented as Median (IQR). P-values were adjusted using the Benjamini-Hochberg method. Statistically significant Benjamini-Hochberg p-values at a false discovery rate of 0.10 are bolded and underlined.
There were no significant differences in any rotary chair, VEMP, or SOT measure between older participants with and older participants without concussion.
Discussion
This study sought to identify objective oculomotor and vestibular differences between children with concussion and vestibular and/or ocular symptoms and children without concussion, and to assess whether the applicability of these tests was different across ages.
Our data suggest these objective clinical oculomotor, vestibular, and static posturography tests may not identify objective impairments in children with prolonged symptoms after concussion. After correcting for multiple comparisons using the Benjamini-Hochberg method, there were no statistically significant differences in any of our clinical tests between children with and children without concussion. This was surprising as the group with concussion in this study consisted only of children reporting vestibular and/or ocular complaints and thus were expected to exhibit differences on these tasks. It is therefore less likely to find robust differences in the general concussed patient.
Following these results and subjective observation that younger children both with and without concussion required more coaching for several tasks, we compared the results of our younger 8-12YOs without concussion to our 13-17YOs without concussion, hypothesizing that age differences may be masking differences due to concussion status. We did find evidence that age may be a confounding variable to these tasks. For example, our non-concussed 8-12YOs performed significantly worse on SVV than our 13-17YOs, and those 13-17YOs performed worse than our lab’s healthy 18-24YO data with an identical distribution of scores as that study’s 18-24YOs with concussion.[22] The younger group without concussion performed significantly worse on some rotary chair measures and SOT conditions, consistent with previous studies suggesting continual improvement on SOT until late adolescence.[24–27]
It is possible that the differences seen in these age groups were not due to vestibular development and instead due to maturity levels / inability for the younger group to follow instructions. While identical instructions for each task were given to all participants, additional coaching during tasks was needed more commonly for the younger children (i.e., reminding them to not move / keep their eyes closed during balance testing, showing them what a “straight line” looks like on the SVV task, etc.). The younger group also showed faster cVEMP latencies with the N1 latency being significantly faster. We attribute this lower latency to the younger children have a smaller anatomy, i.e., a shorter neural travel, and thus a shorter latency.[34]
Following these differences, comparisons between children with and children without concussion were repeated in two groups; children 8-12YO and children 13-17YO. These two comparisons likewise found no statistically significant differences between children with and children without concussion on any clinical measure. Our rotary chair VOR and cVEMP results suggest that children with vestibular and/or ocular symptoms following concussion have intact peripheral vestibular function, which supports findings in our previous study of college athletes with concussion.[22] Therefore, these tests may not be needed in concussion testing protocols unless the neurologic screen points to signs of a peripheral vestibular injury (e.g. nystagmus, positional vertigo).[18] Unlike our previous study in adults, children with concussion did not differ from children without concussion on SVV or VOR Cancellation, suggesting that these tests may not be sensitive in children.[22]
Higher-order balance analyses did find some significant differences between children 8-12YOs with vs without concussion, but no other significant differences were seen on higher-order balance analyses in the other comparisons. Previous studies investigating sway ellipses have found differences between children with concussion and children without concussion with similar sample sizes but used different equipment such as the Nintendo Wii Balance Board.[35–39] Differences in equipment may be responsible for the lack of findings here, but, as the SOT is a commonly used tool, it is important to emphasize that even with a more thorough analysis of force plate data not typically done clinically, few differences were seen. Future studies should include robust analyses on posturography data from the SOT and not simply the SOT equilibrium score, ideally with the goal of moving those measures into clinical practice.
Our results do not support that VOMS symptom scores are indicative of vestibular or oculomotor dysfunction on laboratory testing. While we did not complete the VOMS in lab, the clinic where we received our participants with concussion from used positive VOMS symptom score testing to identify participants for further testing. Our children with concussion subjectively reported more headaches and dizziness during testing than our children without concussion, requiring more frequent breaks during testing, particularly during optokinetic stimulation; however, these symptoms were not representative of objective impairments in oculomotor and vestibular function—at least, not impairments these particular clinical tests identified or could identify. Other clinical tests, such as dynamic visual acuity or accomodation testing, may identify these impairments.[40 41] We believe this distinction is important to prevent additional testing that may exacerbate symptoms and not contribute to, or may even prevent, treatment recommendations. For example, a child complaining of vestibular symptoms on VOMS may benefit from vestibular rehabilitation despite the tests evaluated here suggesting no impairments.
There were several limitations of this study: sample size, time from concussion, and the single-center nature / recruitment strategy for our samples. While our use of non-parametric analysis methods due to non-normal data does somewhat address our sample size concern as well by protecting our conclusions from outliers, larger sample sizes would have allowed us to use more powerful statistical methods. We believe, however, that our non-normal findings emphasize that children should not be expected to perform uniformly on these tasks. Our adjustments for multiple comparisons help further legitimize our conclusions; several measures that were statistically significant between groups were no longer significant after adjustment.
While the time since injury was variable (median: 60 days, IQR: 98), the goal of this study was not to determine what measures may diagnose a concussion but rather identify whether children with lingering vestibular and/or ocular symptoms have objective deficits that would warrant additional testing. Each participant with concussion had a current diagnosis of concussion and was seeking additional testing due to unresolved symptoms. In addition, our group has previously reported several cases of children months from their original injury becoming acutely more symptomatic and developing objective saccadic changes.[42] As we hypothesize these changes are due to maladaptive pathway remodeling, it is our belief that time since injury is not necessarily indicative of symptom severity.
In terms of generalizability, recruiting children without concussion from the sports teams the children with concussion played on and from a single concussion clinic, while ensuring our groups were equally active and our sample with concussion was receiving similar treatment/evaluations, weakens our finding’s generalizability to non-active children and other communities (specifically, rural communities as our sample was mostly urban). In addition, we did not compare results by demographic factors such as sport type and socioeconomic status. It is possible other factors may play into performance, but we believe those comparisons are outside of the scope of this study. Finally, we did not factor in mechanism of concussion (sports-related vs. non-sports related). It is possible that different mechanisms of injury may lead to distinct deficits on these measures.
Conclusion
Children with concussion commonly report vestibular and/or ocular related symptoms. However, no objective clinical tests of vestibular, oculomotor, and balance were significantly different between children with concussion and vestibular and/or ocular related symptoms and children without concussion, suggesting that additional objective testing of vestibular and ocular functions may not be beneficial in the further work-up of a child with concussion and these symptoms. The lack of differences found were hypothesized to be attributed to age related factors such as maturity and attention, which caused variability in the scores of children without concussion; however, splitting analyses by age group did not alter our conclusions regarding the efficacy of these tasks in identifying objective deficits in children with concussion. This study did not evaluate whether vestibular/ocular clinical tests are beneficial in the early diagnosis of concussion; instead, it evaluated their use in children with known concussion and prolonged vestibular and/or ocular symptoms. Future research is needed to develop salient tests to determine the cause of vestibular and ocular symptoms in children with concussion.
Supplementary Material
Acknowledgments
Conflicts of Interest and Source of Funding: The authors have no conflicts of interest relevant to this article to disclose. Funding was obtained from two NIH grants: NIH P30 EY003039, GM008361 Medical Scientist Training Program
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