Abstract
Objective
To investigate the association between risk factors and vestibular-oculomotor outcomes following sport-related concussion (SRC).
Study Design
Cross-sectional study of patients seen 5.7 +/− 5.4 days (range, 0–30 days) post-injury.
Setting
Specialty clinic
Participants
Eighty-five athletes (50 males, 35 females) aged 14.1 +/− 2.8 years (range, 9–24 years) seeking clinical care for SRC.
Interventions
Participants completed a clinical interview, history questionnaire, symptom inventory, and vestibular/ocular-motor screening (VOMS). Chi-square with odds ratios (OR) and diagnostic accuracy were used to examine the association between risk factors and VOMS outcomes.
Main Outcome Measures
Vestibular and ocular-motor screening (VOMS)
Results
Female sex [χ2 = 4.9, p = .03], on-field dizziness [χ2 = 7.1, p = .008], fogginess [χ2 = 10.3, p = .001], and post-traumatic migraine (PTM) symptoms including headache [χ2 = 16.7, p = .001], nausea [χ2 = 10.9, p = .001], light sensitivity [χ2 = 14.9, p = .001] and noise sensitivity [χ2 = 8.7, p = .003] were associated with presence of one or more post-concussion VOMS score above clinical cut-off. On-field dizziness [χ2 = 3.8, p = .05], fogginess [χ2 = 7.9, p = .005], and PTM-like symptoms including nausea [χ2 = 9.0, p = .003] and noise sensitivity [χ2 = 7.2, p = .007] were associated with obtaining a post-concussion near point convergence (NPC) distance cut-off ≥ 5cm. The likelihood ratios were 5.93 and 5.14 for VOMS symptoms and NPC distance, respectively.
Conclusions
Female sex, on-field dizziness, fogginess, and PTM symptoms were predictive of experiencing vestibular-oculomotor symptoms/impairment following SRC.
Keywords: Concussion, Head Injury, Vestibular, Risk Factors
A sport-related concussion (SRC) is a heterogeneous injury resulting in physical, cognitive, emotional, and sleep-related symptoms.1 Physical signs, such as vestibular-oculomotor impairment, may delay recovery if left untreated.2,3 Vestibular impairment may result in symptoms including dizziness, vertigo, blurred/unstable vision, and environmental sensitivity.4 Oculomotor impairment may result in symptoms including blurred vision, diplopia, difficulty reading, and headaches.5 These symptoms are common, with dizziness reported by 50% of concussed athletes6 and visual problems by nearly 30% one week post-injury.7 Vestibular-oculomotor screening is now being used as part of a comprehensive concussion assessment. The Vestibular/Ocular Motor Screening (VOMS) is a brief tool that evaluates vestibular-oculomotor symptoms/impairment following concussion.8 Initial findings demonstrated excellent internal consistency and indicated it was effective in distinguishing concussed from non-concussed athletes;8 however, researchers have not examined which risk factors increase the likelihood for vestibular-oculomotor symptoms/impairment following SRC. Such information could help clinicians identify patients who are at risk for vestibular-oculomotor impairment/symptoms following concussion and the cases in which vestibular screening may be essential.4,9
Within the concussion literature, certain pre/post-injury risk factors (e.g., sex, migraine history, on-field dizziness, loss of consciousness [LOC], fogginess and post-traumatic migraine-like symptoms [PTM]) have been useful in understanding recovery outcomes but their association to vestibular-oculomotor outcomes remains unknown. For example, on-field dizziness10 and PTM-like symptoms11,12 are associated with a 6.4 to 7.3 times greater risk, respectively, of protracted (>21 days) recovery following SRC. Additionally, athletes with persistent fogginess report more post-concussion symptoms than athletes without fogginess.13 LOC has not been reported to be predictive of injury severity or neuropsychological functioning following SRC.14,15 Migraine history16,17 and female sex18–20 have also been identified as risk factors for poor outcomes post-concussion. Despite research suggesting worse outcomes for individuals with a history of multiple concussions, recent studies have indicated that concussion history is less important than other injury details (e.g., rate of recovery).21 Researchers have not yet examined the role of any of the preceding risk factors on vestibular-oculomotor impairment/symptoms following SRC; however, our clinical experience suggests that certain risk factors may make an individual more likely to experience certain outcomes post-concussion resulting in specific VOMS profiles.4
The purpose of this study was to investigate the association between pre/post-injury risk factors and clinical cut-off scores on the VOMS following SRC. Based on previous literature regarding risk factors and recovery outcomes and our collective clinical experience we hypothesized that: 1) female sex, migraine history, on-field dizziness, PTM-like symptoms, and fogginess would predict obtaining at least one post-concussion VOMS clinical cut-off score; 2) on-field dizziness, PTM-like symptoms, and fogginess would predict obtaining a post-concussion near point of convergence (NPC) distance cut-off score; and 3) concussion history and brief (<1 min) LOC would not be associated with obtaining a post-concussion VOMS clinical cut-off score or NPC distance cut-off score. Given limited previous research, we also wanted to explore which risk factors would be associated with which specific VOMS components (e.g., smooth pursuits).
MATERIALS AND METHODS
Research Design
A post-test only, cross-sectional research design was used for this study.
Participants
Participants included 85 of 100 (85%) consecutively enrolled athletes aged 9–24 years (M= 14.1, SD= 2.8) seeking medical care for SRC at a specialty clinic. Participants were required to visit the clinic and be diagnosed with a SRC within 1 month of injury, though most were assessed within 1–2 weeks. Exclusion criteria included a history of brain surgery and/or substance abuse. Athletes with a self-reported history of concussion, LOC/learning disability (LD), and treatment for migraines were included to examine the effects of these risk factors on vestibular-oculomotor outcomes. Participants who experienced a complete resolution of symptoms and full return to baseline functioning (i.e., symptom free at rest/with physical activity, normal vestibular-oculomotor examination, and neurocognitive functioning within expectation) following SRC were considered recovered.
Instrumentation
The Post-Concussion Symptom Scale (PCSS) and History Questionnaire from the Immediate Post-Concussion Assessment and Cognitive Testing (ImPACT)
The PCSS is used to obtain an individual’s self-report of concussion-related symptoms in terms of presence and severity at baseline and post-concussion. The scale includes 22 self-reported items rated on a Likert scale from 0 (none) to 6 (severe). The measure allows for calculation of a total symptom score ranging from 0 to 132. In concussed athletes, reliability has been estimated at .93 (SEM = 5.3, 80% CI = 6.8 points).22 The history questionnaire is used to obtain information regarding educational, concussion, and medical history. For this study, the PCSS and history questionnaire were used to obtain and confirm information regarding the athlete’s concussion history, migraine treatment history, PTM-like symptoms, and fogginess pertaining to their current injury.
The Vestibular/Ocular Motor Screening (VOMS)
The VOMS is a brief tool that assesses vestibular-oculomotor functions through seven components: 1) smooth pursuits, 2) horizontal saccades, 3) vertical saccades, 4) horizontal vestibular ocular reflex (VOR), 5) vertical VOR, 6) visual motion sensitivity (VMS), and 7) NPC. After completing each VOMS component, the patient self-reports any changes in headache, dizziness, nausea, and fogginess on a Likert scale ranging from 0 (none) to 10 (severe). NPC is assessed through self-report of symptoms and objective measurement in centimeters (cm) averaged across three trials. According to the literature, normal NPC values are within 5 cm.23–25 Initial data for the VOMS demonstrated high internal consistency (α = .92) and inter-item correlations ranged from .44 to .88.8 Of the VOMS items, VOR, VMS, and NPC resulted in 89% accuracy for identifying patients with concussion.8 With regard to clinical cut-offs, use of the VOMS resulted in a 44% probability of correctly identifying a concussion; however, a NPC measurement ≥ 5cm resulted in an increased probability of 35% and a symptom increase of ≥ 2 on any VOMS item resulted in an additional increased probability of 50%.8 For this study, clinical cut-off scores were based on a symptom score ≥ 2 on any of the VOMS components and average NPC (across three trials) of ≥ 5cm.8
Procedures
This study was approved by a University Institutional Review Board. All participants and their parents (if under age) signed written assent (child) and consent (parent) forms prior to the study. As part of a triage program in the concussion clinic, physical therapists specialized in vestibular therapy for treatment of SRC conducted a detailed clinical interview with each athlete in collaboration with a neuropsychologist. The clinical assessment was conducted in the following order: 1) clinical intake interview with the physical therapist, 2) administration of the computerized PCSS and history questionnaire as part of a neurocognitive testing battery, 3) administration of the VOMS and 4) consultation with a neuropsychologist regarding treatment recommendations. The VOMS was administered formally by physical therapists with experience and specialized training in the assessment of vestibular and oculomotor disorders. Due to the rigorous clinical schedule, establishing inter- and intra-rater reliability for the VOMS was not possible. During the clinical intake interview, the physical therapist obtained details regarding the injury mechanism, immediate/current symptom report, and the athlete’s medical history. Additionally, athletes were asked to retrospectively recall if they experienced LOC and/or on-field dizziness immediately following injury. Information regarding other pre-injury (sex, concussion history, migraine treatment history) and post-injury (PTM-like symptoms, and fogginess) risk factors was obtained and confirmed via information endorsed by the athlete during completion of the PCSS and history questionnaire. PTM-like symptoms were defined based on the presence of certain symptoms on the PCSS (i.e., headache, nausea, and photo- or phonosensitivity), consistent with previous research.11
Data Analysis
Risk factors were dichotomously coded as yes/no, since previous research has shown the presence of risk factors is what impacts recovery, not necessarily severity.10,11 Descriptive statistics including means, standard deviations, frequencies, medians and inter-quartile ranges (IQR) were conducted to describe sample characteristics for the risk factors as well as scores on each VOMS component. Chi-square analyses with odds ratios (OR) were used to identify significant risk factors using a level of Type I significance for each statistical comparison that was adjusted within each gender/injury characteristic and symptom family of comparisons (LOC, on-field dizziness, headache, nausea, light/noise sensitivity, fogginess) against a false overall discovery rate of p < .05 using methods described by Benjamini and Hochberg.26 The accuracy for the ordinal number of significant risk factors (based on results from chi-square analyses) predictive of post-concussion VOMS findings (i.e., VOMS clinical cut-off scores, NPC distance cut-off scores) was estimated using receiver operating characteristic curves (ROC) area under the curve (AUC) analyses. The sensitivity, specificity, positive likelihood ratio, and negative likelihood ratio were described based on the cumulative number of risk factors to identify participants with post-concussion VOMS findings. All analyses were conducted on SPSS version 22.
RESULTS
Demographic Data
The sample consisted of 85 (50 males, 35 females) athletes aged 14.1 +/− 2.8 years (median 14, IQR 12–16, range 9–24 years) with SRC who were seen on average 5.7 days (median 4, IQR 2–7, range 0–30 days) post-injury. Twenty-five (29.4%) participants reported up to three prior concussions, with concussion history undetermined in 8 (9.4%) participants. Specifically, 14 (16.5%) reported one prior, 6 (7.1%) reported two prior, and 5 (5.9%) reported three prior concussions. Additionally, 12 (16.0%) participants self-reported a pre-existing history of migraine treatment; 9 (10.6%) participants experienced LOC, with LOC undetermined in 8 (9.4%) participants; 46 (54.1%) participants reported on-field dizziness; 39 (45.9%) participants reported fogginess post-concussion; and 27 (31.8%) participants reported PTM-like symptoms. Of the 27 participants reporting PTM-like symptoms, 6 (22%) reported a pre-existing history of migraine treatment.
Risk Factors Associated with at Least One VOMS Clinical Cut-off Score
Chi-square analyses with ORs demonstrated that on-field dizziness, headache, nausea, light sensitivity, noise sensitivity, fogginess, and female sex were associated with an increased likelihood of obtaining at least one post-concussion VOMS clinical cut-off score (see Table 1). Results did not support an association between LOC, concussion history, or migraine treatment history and obtaining a VOMS clinical cut-off score.
Table 1.
Risk Factors associated with at least one VOMS Clinical Cut-off Score (N= 85).
| Risk Factor | χ2 | p-value | Odds Ratio (OR) |
|---|---|---|---|
| LOC | .19 | .66 | 1.4 (.31–6.1) |
| On-Field Dizziness | 7.1 | .008 | 3.9 (1.4–10.8) |
| Headache | 16.7 | .001 | 1.7 (3.0–41.1) |
| Nausea | 10.9 | .001 | 4.3 (2.0–125.5)) |
| Light Sensitivity | 14.9 | .001 | 2.0 (2.5–20.7) |
| Noise Sensitivity | 8.7 | .003 | 3.6 (1.6–12.5) |
| Fogginess | 10.3 | .001 | 6.2 (1.9–20.2) |
| Female Sex | 4.9 | .03 | 3.4 (1.1–10.2) |
| Concussion History | .08 | .78 | 1.2 (.39–3.5) |
| Migraine Treatment History | .48 | .49 | 1.6 (.42–6.1) |
Risk Factors Associated with NPC Distance Clinical Cut-off Score
Chi-square analyses with ORs indicated that on-field dizziness, nausea, noise sensitivity, and fogginess were associated with an increased likelihood of obtaining a post-concussion NPC distance cut-off score (see Table 2). Results did not support an association between LOC, headache, light sensitivity, female sex, concussion history, or migraine treatment history and obtaining a NPC distance clinical cut-off score.
Table 2.
Risk Factors associated with NPC Distance Cut-Off Scores (N= 85).
| Risk-Factor | χ2 | p-value | Odds Ratio (OR) |
|---|---|---|---|
| LOC | .79 | .38 | 1.9 (.13–2.2) |
| On-Field Dizziness | 3.8 | .05 | 2.5 (.99–6.2) |
| Headache | .73 | .39 | 1.7 (.49–6.2) |
| Nausea | 9.0 | .003 | 4.3 (1.6–11.6) |
| Light Sensitivity | 2.0 | .16 | 2.0 (.76–5.2) |
| Noise Sensitivity | 7.2 | .007 | 3.6 (1.4–9.3) |
| Fogginess | 7.9 | .005 | 3.7 (1.5–9.2) |
| Female Sex | 1.7 | .19 | 1.8 (.75–4.5) |
| Concussion History | .03 | .87 | 1.1 (.41–2.9) |
| Migraine Treatment History | .33 | .56 | .69 (.20–2.4) |
Association of Risk Factors and Specific VOMS Component Clinical Cut-off Scores
Chi-square analyses with ORs supported significant associations (i.e., risk factor significantly increased the likelihood for obtaining a cut-off score for the VOMS component) between: 1) on-field dizziness - VOR; 2) headache - vertical saccades, VOR, VMS, and NPC; 3) nausea – pursuits, horizontal saccades, vertical saccades, VMS, NPC; 4) light sensitivity – vertical saccades, VOR, VMS, and NPC; 5) noise sensitivity – pursuits, horizontal saccades, vertical saccades, VOR, VMS, and NPC; 6) fogginess - pursuits, horizontal saccades, vertical saccades, VMS, and NPC; and 7) female sex - VOR; (see Table 3). Results did not support any associations between LOC, concussion history, or migraine treatment history and obtaining cut-off scores for a specific VOMS component.
Table 3.
Association of Risk Factors and Cut-off Scores for each VOMS Component (N= 85).
| Risk-Factor (adjusted significance level)* | VOMS Component | χ2 | p-value | Odds Ratio (OR) |
|---|---|---|---|---|
| Pursuits | .003 | .95 | .96 (.22–4.2) | |
| Horizontal Saccades | 1.2 | .27 | 2.5(.47–12.7) | |
| LOC (P ≤ .05) | Vertical Saccades | .61 | .44 | 1.9 (.37–9.9) |
| VOR | .54 | .46 | 1.7 (.42–6.8) | |
| VMS | .004 | .95 | 1.0 (.26–4.2) | |
| Convergence | .61 | .44 | 1.9 (.37–9.9) | |
| Pursuits | 3.5 | .06 | 2.5 (.94–6.6) | |
| Horizontal Saccades | 3.4 | .06 | 2.3 (.94–5.8) | |
| On-Field Dizziness (P ≤ .001) | Vertical Saccades | .73 | .39 | 1.5 (.60–3.7) |
| VOR | 11.1 | .001 | 4.6 (1.8–11.4) | |
| VMS | .75 | .39 | 1.5 (.62–3.5) | |
| Convergence | 3.2 | .08 | 2.3 (.91–6.1) | |
| Pursuits | .66 | .42 | 1.8 (.44–6.9) | |
| Horizontal Saccades | 2.1 | .14 | 2.7 (.69–10.5) | |
| Headache (P ≤ .03) | Vertical Saccades | 5.1 | .03 | 8.0 (.99–64.5) |
| VOR | 6.7 | .01 | 5.3 (1.4–20.7) | |
| VMS | 5.8 | .02 | 5.8 (1.2–28.0) | |
| Convergence | 5.1 | .03 | 8.0 (.99–64.5) | |
| Pursuits | 8.4 | .004 | 4.1 (1.5–11.1) | |
| Horizontal Saccades | 12.9 | .001 | 5.7 (2.1–15.5) | |
| Nausea (P ≤.01) | Vertical Saccades | 6.4 | .01 | 3.4 (1.3–8.9) |
| VOR | 1.6 | .21 | 1.8 (.72–4.6) | |
| VMS | 4.0 | .05 | 2.6 (1.0–6.5) | |
| Convergence | 20.4 | .001 | 9.6 (3.4–27.5) | |
| Pursuits | 2.9 | .09 | 2.5 (.86–7.0) | |
| Horizontal Saccades | 3.5 | .06 | 2.5 (.94–6.5) | |
| Light Sensitivity (P ≤ .02) | Vertical Saccades | 6.2 | .01 | 3.9 (1.3–11.6) |
| VOR | 6.0 | .02 | 3.1 (1.2–7.8) | |
| VMS | 6.2 | .01 | 3.3 (1.3–8.8) | |
| Convergence | 8.9 | .003 | 5.4 (1.7–17.6) | |
| Pursuits | 4.2 | .04 | 2.8 (1.6–7.7) | |
| Horizontal Saccades | 10.9 | .001 | 5.1 (1.9–13.8) | |
| Noise Sensitivity (P ≤ .044) | Vertical Saccades | 5.8 | .016 | 3.3 (1.2–9.1) |
| VOR | 4.0 | .044 | 2.4 (2.0–5.9) | |
| VMS | 9.8 | .002 | 4.4 (1.7–11.2) | |
| Convergence | 11.2 | .001 | 5.9 (2.0–17.7) | |
| Pursuits | 5.7 | .017 | 3.2 (1.2–8.3) | |
| Horizontal Saccades | 9.4 | .002 | 4.1 (1.6–10.4) | |
| Fogginess (P ≤ .03) | Vertical Saccades | 3.7 | .05 | 2.5 (.97–6.2) |
| VOR | 3.6 | .06 | 2.3 (.97–5.6) | |
| VMS | 4.9 | .03 | 2.7 (1.1–6.5) | |
| Convergence | 11.0 | .001 | 5.0 (1.9–13.4) | |
| Pursuits | 1.2 | .27 | 1.7 (.66–4.3) | |
| Horizontal Saccades | 1.2 | .27 | 1.6 (.67–4.0) | |
| Sex (P ≤.004) | Vertical Saccades | 2.6 | .10 | 2.1 (.85–5.4) |
| VOR | 8.2 | .004 | 3.8 (1.5–9.5) | |
| VMS | 1.5 | .22 | 1.7 (.72–4.1) | |
| Convergence | .48 | .49 | 1.4 (.55–3.4) | |
| Pursuits | .40 | .53 | 1.4 (.50–3.8) | |
| Horizontal Saccades | .001 | .97 | .98 (.37–2.6) | |
| Concussion History (P≤.05) | Vertical Saccades | .211 | .65 | 1.3 (.46–3.5) |
| VOR | .26 | .61 | 1.3 (.49–3.4) | |
| VMS | .22 | .64 | 1.3 (.48–3.3) | |
| Convergence | .55 | .46 | .68 (.24–1.9) | |
| Pursuits | .32 | .57 | 1.5 (.37–6.1) | |
| Horizontal Saccades | 1.3 | .25 | 2.3 (.56–9.1) | |
| Migraine Treatment History (P ≤ .05) |
Vertical Saccades | 3.7 | .06 | 6.3 (.77–52.2) |
| VOR | .66 | .42 | .59 (.16–2.2) | |
| VMS | .08 | .78 | 1.2 (.34–4.2 | |
| Convergence | .45 | .50 | 1.6 (.40–6.6) | |
Adjusted against overall false discovery rate = .05
Predictive Accuracy for Obtaining Post-Injury VOMS Clinical Cut-Off Scores
The cumulative effect for the number of significant pre/post-injury risk factors (i.e., female sex, headache, nausea, light and noise sensitivity, fogginess, and on-field dizziness) in obtaining at least one post-concussion VOMS clinical cut-off score was estimated. The AUC for 0–7 predictors was .85 (p < .001, 95% CI = .77-.94), with the maximum sensitivity (1.0) observed for one or more, and maximum specificity (1.00) with 6–7 risk factors. The presence of five or more risk factors maximized the odds in favor of obtaining a post-concussion VOMS clinical cut-off score (likelihood ratio = 5.93, 95% CI 1.5–22.81, Table 4).
Table 4.
Predictive accuracy (sensitivity, specificity, positive and negative likelihood ratios) for clinically important post-concussion VOMS findings by number of positive risk factors.
| VOMS Outcome | Number of Risk Factors* | Sensitivity (95% CI) |
Specificity (95% CI) |
Likelihood ratio-positive (95% CI) |
Likelihood ratio-negative (95% CI) |
|---|---|---|---|---|---|
| VOMS Cut-off Score (1 or more) | ≥ 1 | 1.0 | .27 (.02–.33) | 1.21 (1.0–1.46) | 0 |
| ≥ 2 | .95 (.89–1.0) | .48 (.27–.68) | 1.82 (1.23–2.71) | .10 (.03–.33) | |
| ≥ 3 | .82 (.73–.92) | .74 (.56–.92) | 3.15 (1.57–6.33) | .24 (.13–.43) | |
| ≥ 4 | .69 (.58–.81) | .78 (.61–.95) | 3.20 (1.44–7.05) | .39 (.25–.60) | |
| ≥ 5 | .52 (.39–.64) | .91 (.79–1.0) | 5.93 (1.54–22.83) | .53 (.40–.71) | |
| ≥ 6 | .37 (.25–.49) | 1.0 | - | .63 (.52–.76) | |
| NPC Distance Cut-off Score | ≥ 1 | .88 (.77–.99) | .27 (.15–.40) | 1.21 (.98–1.50) | .44 (.15–1.22) |
| ≥ 2 | .79 (.65–.83) | .58 (.44–.72) | 1.90 (1.31–2.78) | .35 (.17–.71) | |
| ≥ 3 | .56 (.39–.73) | .79 (.68–.91) | 2.69 (1.43–5.02) | .57 (.37–.84) | |
| 4 | .32 (.17–.48) | .94 (.89–1.0) | 5.14 (1.56–17.16) | .72 (.57–.92) | |
Total count of positive factors from female sex, light sensitivity, headache (for VOMS cut-off score only), nausea, noise sensitivity, fogginess, and on-field dizziness.
The cumulative effect for the number of significant pre/post-injury risk factors (i.e.,, fogginess, nausea, noise sensitivity and on-field dizziness) in obtaining a post-concussion NPC distance cut-off score was estimated. The AUC for 0–4 risk factors was .73 (P < .001. 95% CI .62-.85). The maximum sensitivity for obtaining a post-concussion NPC distance cut-off score (.88) was associated with one or more risk factors. The maximum specificity (.94) was seen with four risk factors. The presence of four risk factors maximized the odds in favor of obtaining a post-concussion NPC distance cut-off score (likelihood ratio = 5.14 95% CI 1.56–17.16, Table 4).
DISCUSSION
The current study was the first to examine the role of risk factors on vestibular-oculomotor impairment/symptoms. Key findings indicated that female sex, on-field dizziness, headache, nausea, light sensitivity, noise sensitivity, and fogginess were associated with one or more post-concussion VOMS clinical cut-off score. The presence of five or more risk factors was associated with increased odds for post-concussion VOMS clinical cut-off scores. Additionally, on-field dizziness, nausea, noise sensitivity, and fogginess were associated with NPC distance ≥5cm. The presence of four risk factors was associated with increased odds for post-concussion NPC distance ≥5cm. Neither concussion history nor LOC were associated with VOMS clinical cut-off scores or NPC distance. We also identified the relationship between risk factors and specific VOMS components to understand the influence of each risk factor on specific vestibular-oculomotor functions.
This study extends literature on the role of risk factors in determining outcomes following SRC by adding vestibular-oculomotor outcomes.8,10,12,27,28 Results revealed associations among PTM-like symptoms, on-field dizziness, fogginess, and female sex and vestibular-oculomotor impairment/symptoms which is not surprising, as previous research identified a relationship between dizziness, fogginess, and PTM-like symptoms within the first seven days post-injury.27 Researchers have identified associations between PTM-like symptoms and fogginess and protracted recovery times,10–12 possibly due to a previously unknown risk for development of vestibular-oculomotor impairment/symptoms. The current results also support previous research reporting worse outcomes for females, who are more at risk for headaches/migraines, greater post-concussion symptoms, and more vestibular dysfunction than males.25,29
As predicted, LOC and concussion history were not associated with increased risk for vestibular-oculomotor impairment/symptoms, which supports research suggesting that concussion history may be less important than specific injury details (e.g., rate of recovery).21 Given these results, evaluation of risk factors in conjunction with screening of the vestibular-oculomotor system is important in identifying possible vestibular-oculomotor impairment following SRC. However, the current findings may also reflect greater overall impairment as indicated by fogginess, PTM-like symptoms, and on-field dizziness as well as symptom report during the VOMS. Our findings regarding the effect of multiple risk factors may reinforce this assertion.
Clinical Implications
The identified risk factors should be used to guide clinicians’ screening of the vestibular-oculomotor system using VOMS and other similar measures. Clinicians should be aware of the increased likelihood of vestibular-oculomotor findings in females and those presenting with on-field dizziness, fogginess and/or PTM-like symptoms. Additionally, given the additive effect reported in this study, clinicians should also be aware of the increased likelihood for vestibular-oculomotor findings in those individuals presenting with two to three risk factors. Essentially, the risk of vestibular-oculomotor findings increases as the number of risk factors increases. The presence of these risk factors may also help clinicians discuss with their patients expectations for specific types of symptoms, impairment, and recovery times. Ultimately, these risk factors should be used to help guide prognosis and inform potential targeted treatments for patients. Continued research exploring the relationship between risk factors and vestibular-oculomotor impairment and symptoms following concussion is warranted.
Future Directions and Research
Identifying which risk factors are related to vestibular-oculomotor impairment further informs management for this injury and results from previous research regarding risk factors and recovery outcomes. This study highlights the utility of assessing pre/post-injury risk factors in conjunction with screening of the vestibular-oculomotor system as part of a comprehensive clinical evaluation following SRC. However, we did not assess all potential risk factors and instead relied on key risk factors for SRC reported within the literature. Future studies should examine other risk factors (e.g., motion sickness, vision impairment, altered balance, cervical examination) that may cause an individual to be more likely to experience vestibular-oculomotor impairment following SRC. Additionally, further research into the VOMS, specifically its clinical utility as a screening tool for those who need vestibular and/or vision therapy, is warranted. Future research should also explore if the presence of certain risk factors influences symptom provocation on vestibular-oculomotor assessments, or if the presence of risk factors along with the provocation of vestibular symptoms is a representation of greater impairment.
Limitations
Although the current study is the first to look at the association of risk factors to vestibular/ocular-motor symptoms/impairment following concussion, it was limited by several factors. The sample was a convenient, cross-sectional sample which may not adequately represent the overall population and thereby limit generalizability of the findings. Self-reported symptoms after administration of each VOMS component were collected subjectively, based on patient reporting, potentially leading to recall bias and an issue with accuracy of reporting. Further, clinicians administering the VOMS assessment were not blinded to the presence of the risk factors of interest and procedures were not established to ensure inter and intra-rater reliability. Due to the logistics of patient scheduling, establishing intra- and/or inter-rater reliability among VOMS administrators was not possible. Therefore, individual variability in the administration of the VOMS (e.g., instructions) may influence VOMS scores and should be considered and controlled for in future studies. Additionally, the order of administration for the measures was fixed, potentially resulting in biased scores on later measures based on exposure to earlier measures. Moreover, the selected pre-injury risk factors such as concussion and migraine history are sometimes inaccurately reported (i.e., under reported), as not all concussions and migraines were necessarily diagnosed especially among younger patients. Likewise, post-injury risk factors (i.e., dizziness, LOC, or PTA) may have been misreported due to acute disorientation or confusion. In fact, nearly 10% of the sample could not determine if they experienced a LOC. Furthermore, there is potential overlap in patients who report multiple risk factors such as PTM and fogginess, which may have confounded associations for some risk factors.
Conclusion
Overall, the current study adds to the literature regarding the role of vestibular-oculomotor impairment/symptoms following SRC. Results supported previous research suggesting that PTM-like symptoms and on-field dizziness are associated with prolonged post-concussion symptoms, possibly due to development of vestibular-oculomotor impairment/symptoms. Our findings also highlighted the higher rates of vestibular-oculomotor impairments in females consistent with previous literature. In summary, the current findings suggest that it is important not only to ask about past medical history and pre/post-injury risk factors, but also to screen the vestibular-oculomotor system, which is commonly affected by concussion. For clinicians, the current study highlights the relevance of pre/post-injury risk factors to subsequent vestibular-oculomotor impairment following SRC.
Acknowledgments
Disclosure of Funding: This research was supported in part by a grant to the University of Pittsburgh from the National Institute on Deafness and Other Communication Disorders (1K01DC012332–01A1). A poster containing this information was presented in November 2015 at the 35th annual conference of the National Academy of Neuropsychology (NAN). Dr. Collins is a cofounder and 10% shareholder of ImPACT Applications Inc. However, the ImPACT test was not used in the current study. No other authors have competing interests to report.
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