The Co-Occurrence of Vestibular/Ocular Motor Provocation and State Anxiety in Adolescents and Young Adults with Concussion

Abstract

Vestibular/ocular motor provocation and state anxiety are both independently linked to poor recovery outcomes following concussion. However, the relationship between these two clinical presentations and their co-occurring effects on concussion recovery outcomes is understudied. The purpose was to examine the co-occurring effects of vestibular/ocular motor provocation and state anxiety following concussion. There were 532 participants (15–25 years) with concussions who completed the vestibular/ocular motor screening (VOMS), State-Trait Anxiety Inventory, and the Post-Concussion Symptom Scale within 30 days of injury. Participants were classified into provocation (PROV) and no provocation (NO PROV) groups based on exceeding/not exceeding VOMS cutoffs. An analysis of covariance was used to examine between-group comparisons on state anxiety scores; and logistic regressions, with adjusted odds ratios (Adj OR), were used to evaluate predictors of clinical levels of state anxiety and protracted recovery. A total of 418 participants (78.6%; age = 17.2 ± 2.6; 65% female) exceeding VOMS cutoffs were in the PROV, and 114 (21.4%; age = 16.6 ± 2.2; 53% female) participants were in the NO PROV group. The PROV group (mean [M] = 39.50, standard deviation [SD] = 12.05) exhibited significantly higher state anxiety scores than the NO PROV group (M = 32.45, SD = 10.43) (F[1, 532] = 15.36, p < 0.001, η ² = 0.03). Vestibular/ocular motor provocation (Adj OR = 3.35, p < 0.001, 95% confidence interval [CI]: 1.42–3.88) was the most robust predictor of clinical state anxiety following concussion (χ² [4, 532] = 86.78, p < 0.001). Participants exhibiting vestibular/ocular motor provocation with clinical levels of state anxiety were at 2.47 times (p < 0.001, 95% CI: 1.53–3.99) greater odds of experiencing a protracted concussion recovery than participants with vestibular/ocular motor provocation without clinical state anxiety. Vestibular/ocular motor provocation is associated with increased state anxiety following concussion, and the addition of clinical state anxiety to vestibular/ocular motor provocation increases the odds for protracted recovery. Clinicians should assess vestibular/ocular motor function and anxiety following concussion.

Introduction

Vestibular/ocular motor provocation and state anxiety are both independently linked to poor recovery outcomes following concussion. Individuals who experience post-concussion vestibular/ocular motor provocation often exhibit symptom increases (e.g., dizziness, headache, nausea, and fogginess) and/or visual dysfunction (e.g., convergence insufficiency) during a vestibular/ocular motor assessment (e.g., vestibular/ocular motor screening [VOMS])^1,2 and/or following exposure to busy environments.³ Approximately 42–68% of individuals with concussion exhibit vestibular/ocular motor provocation,^4
–6 and these impairments have been linked to significantly longer/prolonged concussion recovery trajectories,^7,8 and increased risk of developing chronic concussion symptoms.⁹ Post-concussion state anxiety symptoms include worry, sadness, fear, somatization, feelings of depression, irritability, and sleep dysregulation,¹⁰ and occur in approximately 13–39% of individuals with this injury.^11
–13 These symptoms are commonly assessed via inventories (e.g., Post-Concussion Symptom Scale [PCSS])^14,15 and/or mood assessments that measure state anxiety (e.g., State-Trait Anxiety Inventory [STAI], 7-item Generalized Anxiety Disorder Scale [GAD-7]).^11,16 Similar to post-concussion vestibular/ocular motor provocation, increased levels of state anxiety are associated with increased symptom burden,¹⁷ decreased cognitive performance,¹⁸ and delayed recovery¹⁴ following concussion. Although these findings highlight the independent effects of vestibular/ocular motor provocation and state anxiety symptoms on concussion recovery outcomes, the relationship between these two clinical presentations and their co-occurring effects on recovery outcomes is understudied.

The co-occurrence of psychological distress (e.g., generalized anxiety) is well established in patient populations with vestibular disorders^19
–21 and visual impairment,^22,23 and more recently discussed in clinical reports for concussion care.^10,24 However, there are no studies to date that specifically examine subclinical and clinical levels of state anxiety in individuals with post-concussion vestibular/ocular motor provocation. A related study by Gillie and colleagues¹² identified predictors of subclinical and clinical levels of anxiety in adolescents with concussion. Specifically, pre-injury panic symptoms, post-concussion symptoms, and headache/migraine history predicted mild levels of anxiety following concussion, while clinical levels of generalized anxiety were predicted by pre-injury panic symptoms, vestibular dysfunction (i.e., symptom provocation on horizontal vestibular–ocular reflex), and non-sport injury mechanism.¹² Despite the importance of these findings, Gillie et al.¹² included a small sample of individuals with concussion (n = 129) and a smaller, subsample of individuals with clinical levels of anxiety (13%, n = 17). Therefore, additional research examining vestibular/ocular motor provocation and post-concussion anxiety in a larger clinical cohort is needed. Moreover, there is a need to control for other established predictors of anxiety including sex (i.e., female gender),²⁵ history of anxiety,^12,26 and symptom burden,^17,26 to better determine the relationship between state anxiety and post-concussion vestibular/ocular motor provocation. There is also the opportunity to extend this work to examine the co-occurring effects of vestibular/ocular motor provocation and state anxiety on concussion recovery. A dose–response relationship between the number of risk factors and protracted concussion recovery is reported in the literature.²⁷ However, the combined effects of multiple risk factors that may be likely to co-occur (e.g., vestibular/ocular motor provocation and anxiety) on concussion recovery time are unknown.

The overall purpose of the current study was to examine the co-occurring effects of vestibular/ocular motor provocation and state anxiety following concussion. State anxiety scores were hypothesized to be higher for patients with post-concussion vestibular/ocular motor provocation than for patients without post-concussion vestibular/ocular motor provocation. A secondary purpose was to evaluate post-concussion vestibular/ocular motor provocation as a predictor of clinical levels of state anxiety. Vestibular/ocular motor provocation was hypothesized to be a significant predictor of clinical levels of state anxiety among history of anxiety, symptom burden, and sex (female). Finally, the combined effect of vestibular/ocular motor symptom provocation and clinical state anxiety on concussion recovery time was investigated. Individuals with vestibular/ocular motor provocation and clinical levels of state anxiety were hypothesized to have a higher odds for protracted recovery compared with individuals with vestibular/ocular motor provocation without clinical state anxiety.

Methods

Design and participants

A retrospective analysis of electronic medical record (EMR) data from patients aged 18 to 25 years within 30 days of a concussion at a specialty clinic in the Mid-Atlantic U.S. region between March 2017 and October 2023 was performed. Participants with sport and non-sport (e.g., assaults and falls) mechanisms of injury were included in the final sample. Any patient who sustained a concussion due to a motor vehicle accident (MVA) was excluded from participation, as this mechanism is linked to a different symptom²⁸ and emotional²⁹ clinical presentation.

Measures/instrumentation

Concussion definition

The following consensus^30,31 criteria were used to diagnose concussion at the initial clinical visit: (1) a clear mechanism of injury (sport, non-sport, and MVA) and (2) the presence of at least one or more on-field/acute signs (e.g., loss of consciousness, vomiting, disorientation, and balance difficulties), and/or the presence of at least one concussion symptom after injury (e.g., headache, nausea, and mental fogginess), and/or impairment on neurocognitive testing or VOMS. All diagnoses of concussion were confirmed at first clinical visit by a clinician trained in concussion clinical care.

Demographics and health history

Participant demographics (e.g., age, sex, and concussion history) and health history (e.g., learning disorder [LD], attention deficit hyperactivity disorder [ADHD], history of concussion, migraine, ocular dysfunction, anxiety, and depression), as well as time (days) until first clinical visit from date of injury and mechanism of injury (e.g., sport/recreation or MVA) were collected from the clinical interview.

Post-concussion symptoms

The PCSS, a 22-item self-reported symptom assessment that is scored on a 7-point Likert scale ranging from 0 (none) to 6 (severe), was used to assess concussion-related symptoms. As demonstrated in previous research,³² PCSS scores were used to identify and control for initial symptom burden (PCSS total score >13) among participant groups. The reliability (0.88–0.94) and validity (e.g., face and content validity) of the PCSS are well documented in the literature.^33,34

Vestibular/ocular motor symptoms and impairment

The VOMS, a brief clinical screening tool, was used to assess vestibular/ocular motor symptoms and impairments.^1,2 The VOMS consists of ocular motor (e.g., smooth pursuits, horizontal saccades, vertical saccades, near point of convergence [NPC] distance [cm], and symptoms) and vestibular (horizontal vestibular ocular reflex, vertical vestibular ocular reflex, and visual motion sensitivity) items. Participants rate headache, dizziness, nausea, and fogginess symptoms on an 11-point Likert scale (0 = none; 10 = severe) at pretest (i.e., baseline) and again after completing each VOMS component. NPC distance was calculated as an average of three trials. An overall total change score was used to classify vestibular/ocular motor impairment and symptoms (i.e., provocation).¹ As reported in Elbin et al.,¹ participants who exceeded a cutoff score of ≥3 for the overall VOMS change score and/or exhibited an average NPC distance of ≥3 cm were classified into a vestibular/ocular motor provocation group (PROV)¹ and participants who did not exceed these cutoffs were classified into a no provocation group (NO PROV). The VOMS has a high overall internal consistency (Cronbach α = 0.92 and 0.97), a sensitivity of 0.68–0.89, and a specificity of 0.72.^2,35

State and trait anxiety

The STAI-Y is a clinical measure of state and trait anxiety.³⁶ The STAI-Y is a 40-item assessment with 20 items for state anxiety and 20 items for trait anxiety. The current study included only the state anxiety scale of the STAI-Y, which assesses participants’ emotional state in the present moment. State items are rated on a 4-point Likert scale from 1 (not at all) to 4 (very much so). These items were summed into a total state anxiety score (range: 20–80), with higher scores indicative of higher levels of state anxiety. In addition, a clinical cutoff of ≥40 is indicative of probable levels of clinical state anxiety, as reported in previous studies.³⁷ The STAI-Y has shown internal consistency coefficients ranging from 0.86 to 0.95 in adolescent and adult samples.^36,38,39

Recovery time

Recovery time was defined as the total number of days from injury until medical clearance. Per international consensus,^30,31 all participants were required to be symptom-free at rest and following physical and cognitive exertion. In addition, all clinical data (i.e., vestibular/ocular motor and neurocognitive) were required to be within normal limits for medical clearance.

Procedures

The current study’s protocol was approved by the institutional review board under an expedited, retrospective review of EMR. All participants completed an initial clinical visit within 30 days of concussion. During the initial clinic visit, participants completed a detailed clinical interview (e.g., demographics, health history, and injury-related information) and then completed the PCSS, VOMS, and STAI clinical measures. The clinical interview and assessments were administered by a trained clinician as part of the clinical standard of care and were conducted in the order listed above for each participant.

Data analysis

Descriptive statistics (e.g., means [M], standard deviations [SDs], frequencies, and percentages) were used to describe sample demographics and scores on all measures. Vestibular/ocular motor provocation group equivalence on patient demographics (age, sex), health history (yes/no: concussion, LD, ADHD, history of concussion, migraine, ocular dysfunction, anxiety, and depression), injury details (days until first clinical visit from date of injury, and non-sport mechanism of injury), and symptom burden (yes/no: PCSS total score >13) was evaluated with a series of independent samples t-tests and chi-square tests.

To examine differences between the PROV and NO PROV groups on state anxiety scores, a one-way analysis of covariance (ANCOVA), controlling for sex, symptom burden (yes/no), history of anxiety (yes/no), and history of depression (yes/no), was performed. A chi-square analysis was used to examine differences in exhibiting clinical levels of state anxiety (≥40 on STAI) among the PROV and NO PROV groups. A logistic regression (LR) with adjusted odds ratios (Adj ORs) and 95% confidence intervals (CIs) was performed to identify the relative contribution of vestibular/ocular motor provocation for exhibiting clinical levels of state anxiety (≥40 on STAI) among other established predictors, including sex, history of anxiety (yes/no), and symptom burden (yes/no).

Participants with recovery time data were extracted from the overall sample and examined separately to explore the combined effects of vestibular/ocular motor provocation and clinical levels of state anxiety on protracted recovery from concussion. Protracted recovery was defined as a recovery time of 30 days or more from the date of injury.³¹ Means, SDs, and frequencies were used to describe the overall recovery time for this sample and the percentage of the sample exhibiting protracted recovery. Participants who exhibited provocation on the VOMS with clinical levels of state anxiety were classified into a PROV ANX group, and participants who exhibited provocation on the VOMS without clinical levels of state anxiety were classified into a PROV NO ANX group. Between-group differences were evaluated with a series of t-tests and chi-square analyses for all demographics, health history, injury details, symptom burden, and recovery time (days and protracted recovery status). A one-way ANCOVA, controlling for symptom burden (yes/no), history of anxiety (yes/no), and history of depression (yes/no), was performed to test between-group differences on recovery time (days). An LR with Adj ORs and 95% CIs was performed to examine the relative contribution of vestibular/ocular motor provocation with clinical levels of state anxiety on protracted recovery among other predictors, including history of anxiety (yes/no), history of depression (yes/no), and symptom burden (yes/no). Statistical significance was set at p ≤ 0.05, and all statistical analyses were conducted with SPSS version 29.⁴⁰

Results

Participant demographics

A total of 1014 patient EMRs met study inclusion criteria, from which 482 (48%) participants were excluded for the following reasons: 161 (16%, 161/1014) reported an MVA mechanism of injury, 261 (26%, 261/1014) were outside of the 15–25-year study inclusion criterion, and 60 (6%, 60/1014) completed their first visit more than 30 days following injury. The final sample comprised 532 (52%) patient records, of which 329 (62%) included recovery data. Forty-three percent (228/532) of cases exceeded clinical cutoffs on the STAI for clinical levels of state anxiety. There were 418 (79%) participants who exhibited provocation on the VOMS and were assigned to the PROV group, and 114 (21%) participants who did not exhibit provocation on the VOMS were assigned to the NO PROV group. Individuals in the PROV group were significantly older (17.15 vs. 16.61 years) than those in the NO PROV group (t (530) = 2.05, p = 0.04), and there was no significant difference in the distribution of females in the PROV group (65%) compared with the NO PROV group (53%) (χ² [1, 532] = 1.26, p = 0.26). Furthermore, there were no between-group differences for days from injury until first clinical visit (t (530) = 0.82, p = 0.41), history of concussion (χ² [1, 532] = 0.64, p = 0.42), migraine (χ² [1, 532] = 1.08, p = 0.30), ocular dysfunction (χ² [1, 532] = 3.57, p = 0.06), ADHD (χ² [1, 532] = 0.48, p = 0.49), LD (χ² [1, 532] = 0.34, p = 0.56), depression (χ² [1, 532] = 2.90, p = 0.09), or non-sport injury mechanism (χ² [1, 532] = 2.74, p = 0.10). However, the PROV group had significantly more participants endorsing a history of anxiety (32% vs. 22%; χ² [1, 532] = 4.58, p = 0.03) and symptom burden (83% vs. 63%; χ² [1, 532] = 22.43, p < 0.001). As a result, sex, history of anxiety, and symptom burden were used as co-variates in between-group analyses. Group means, SDs, and percentages are provided in Table 1.

Table 1.

Means, Standard Deviations, Frequencies, and Percentages for Demographic and Injury-Related Variables for the PROV (n = 418) and NO PROV Groups (n = 114)

	PROV		NO PROV
	M	SD	M	SD
Age (y)^*	17.15	2.57	16.61	2.20
Days until the first clinical visit	9.11	6.83	8.53	6.36

	%	n	%	n
Sex (% female)^*	65	273	53	60
Non-sport mechanism	23	96	16	18
History of concussion	53	223	49	56
History of migraine	22	92	18	20
History of ocular dysfunction	10	42	4	5
History of ADHD	18	76	21	24
History of LD	10	40	11	13
History of anxiety^*	32	135	22	25
History of depression	19	80	12	14
Symptom burden^*	83	349	63	72

p < 0.05.

ADHD, attention-deficit/hyperactivity disorder; LD, learning disorder; M, mean; PROV, provocation; NO PROV, no provocation; SD, standard deviation.

Post-concussion vestibular/ocular motor provocation and state anxiety

The results of a one-way (PROV, NO PROV) between-groups ANCOVA, controlling for sex, history of anxiety, and symptom burden, on total state anxiety scores revealed a significant between-subjects effect for the provocation group (F[1, 532] = 15.36, p < 0.001, η ²= 0.03). Specifically, the PROV group (M = 39.50, SD = 12.05) exhibited significantly higher state anxiety scores than the NO PROV group (M = 32.45, SD = 10.43). There was also a significantly greater percentage of participants in the PROV (48%, 201/418) group exhibiting clinical levels of state anxiety compared with the NO PROV group (24%, 27/114) (χ² [1, 532] = 21.78, p < 0.001). The LR examining predictors for clinical levels of state anxiety was significant (χ² [4, 532] = 86.78, p < 0.001). After accounting for variance associated with total symptom burden and history of anxiety, participants exhibiting vestibular/ocular motor provocation had a 3.35 times greater odds for endorsing clinical levels of state anxiety following concussion than those without vestibular/ocular motor provocation (Table 2).

Table 2.

Results of a Logistic Regression Examining Predictors for Clinical Levels of State Anxiety Following Concussion (N = 532)

Variable	Adjusted OR	p	95% CI for OR
Vestibular/Ocular motor provocation	3.35	<0.001	1.42–3.88
History of anxiety	2.17	<0.001	1.45–3.25
Symptom burden	5.55	<0.001	3.03–10.17
Sex (female)	1.06	0.78	0.72–1.55

CI, confidence interval; OR, odd ratios.

Exploring the combined effects of vestibular/ocular motor provocation and clinical state anxiety on recovery time following concussion

Recovery time was available for 62% (329/532) of the sample, yielding an average recovery time of 31.82 days (SD = 17.77, range = 6–88 days), and 48% (159/329) experiencing a protracted recovery from injury. Of the 329 participants with available recovery time, 148 (45%) participants exhibited vestibular/ocular motor provocation with clinical state anxiety (PROV ANX), and 181 (55%) participants exhibited vestibular/ocular motor provocation without clinical state anxiety (PROV NO ANX). There were no between-group differences for age (t (327) = −0.04, p = 0.97), days from injury until first clinical visit (t (327)= −0.07, p = 0.94), sex (χ² [1, 329] = 3.11, p = 0.08), non-sport mechanism (χ² [1, 329] = 0.41, p = 0.52), history of concussion (χ² [1, 329] = 1.27, p = 0.26), migraine (χ² [1, 329] = 0.59, p = 0.44), ocular motor dysfunction (χ² [1, 329] = 1.10, p = 0.29), ADHD (χ² [1, 329] = 0.07, p = 0.79), or LD (χ² [1, 329] = 0.93, p = 0.34). These groups did differ on history of anxiety (χ² [1, 329] = 13.09, p < 0.001), depression (χ² [1, 329] = 5.28, p = 0.02), and symptom burden (χ² [1, 329] = 35.05, p < 0.001) (Table 3), which were used as covariates in the ANCOVA and LR.

Table 3.

Means, Standard Deviations, Frequencies, and Percentages for Demographic and Injury-Related Variables for the PROV ANX (n = 148) and PROV NO ANX Groups (n = 181) with Documented Recovery Time

	PROV ANX		PROV NO ANX
	M	SD	M	SD
Age (y)	17.03	2.49	17.04	2.51
Days until the first clinical visit	8.75	6.04	8.80	6.96

	%	n	%	n
Sex (% female)	59	88	61	90
Non-sport mechanism	22	32	23	34
History of concussion	55	82	60	89
Migraine history	22	32	22	33
History of ocular dysfunction	8	12	14	21
History of ADHD	18	27	21	31
History of LD	11	16	8	14
History of anxiety^*	41	60	27	40
History of depression^*	24	35	17	25
Symptom burden^*	95	141	85	126

p < 0.05.

ADHD, attention-deficit/hyperactivity disorder; LD, learning disorder; M, mean; PROV, provocation; NO PROV, no provocation; SD, standard deviation.

Participants in the PROV ANX group (M = 36.36, SD = 17.58 days) took significantly longer to recover from concussion than those in the PROV NO ANX group (M = 28.12, SD = 17.10 days) (F[4, 328] = 10.52, p < 0.001, η ² = 0.03). The LR was significant (χ² [4, 329] = 28.97, p < 0.001) and revealed that vestibular/ocular motor provocation with clinical state anxiety was the only predictor of protracted recovery while accounting for symptom burden, history of depression, and history of anxiety. Specifically, participants exhibiting vestibular/ocular motor provocation with clinical levels of state anxiety were 2.47 times (p < 0.001, 95% CI: 1.53–3.99) more likely to experience a protracted concussion recovery than participants with vestibular/ocular motor provocation without clinical levels of state anxiety (Table 4).

Table 4.

Results from a Logistic Regression Examining Predictors for Protracted Recovery following Concussion (N = 329)

Variable	Adjusted OR	p	95% CI for OR
Vestibular/Ocular motor provocation and clinical state anxiety	2.47	<0.001	1.53–3.99
History of depression	1.61	0.29	0.74–3.46
History of anxiety	1.08	0.82	0.57–2.06
Symptom burden	1.70	0.10	0.90–3.20

CI, confidence interval; OR, odd ratios.

Discussion

The current study examined the co-occurring effects of vestibular/ocular motor provocation and state anxiety following concussion. Participants who exhibited post-concussion vestibular/ocular motor provocation reported significantly higher state anxiety scores and were at a 3.35 greater odds for exhibiting clinical levels of state anxiety compared with participants without vestibular/ocular motor provocation. Vestibular/ocular motor provocation was the most robust predictor of clinical state anxiety among other established predictors (e.g., sex, anxiety history). Finally, participants with vestibular/ocular motor provocation and clinical levels of state anxiety were associated with a 2.47 times greater odds of protracted concussion recovery (≥30 days) than participants with vestibular/ocular motor provocation without clinical levels of state anxiety. Altogether, this study builds on the paucity of evidence demonstrating a relationship between vestibular/ocular motor dysfunction and clinical state anxiety following concussion and provides novel findings regarding their relationship to concussion recovery outcomes.

The increased levels of state anxiety documented in participants with post-concussion vestibular/ocular motor provocation are in concordance with anxiety (i.e., psychological distress) reports from patient populations with vestibular disorders^19,20 and add to the emerging literature on this topic in patients with concussion.^12,21 Researchers have hypothesized that the relationship between these two clinical presentations may be somatopsychic, whereas post-injury vestibular symptoms are interpreted as catastrophic, resulting in an avoidance/agoraphobic response.⁴¹ This is anecdotally reported by clinicians administering vestibular/ocular motor assessments (e.g., VOMS), where patients may report fear of engaging in head movements and exhibit non-verbal cues (e.g., sighing, heavy breathing, and panic response).²⁴ Conversely, this relationship may be psychosomatic, given that anxiety (i.e., arousal and hyperventilation) alters central vestibular processing, resulting in vestibular dysfunction.^42,43 Both of these explanations suggest injury and/or dysfunction to the shared neural circuitry in the brain (e.g., locus coeruleus and parabrachial nucleus) that is responsible for vestibulo-autonomic function and emotional regulation.^20,44 These results could also be attributed to the well-documented psychosocial effects of being injured and removal from sport and/or activity (e.g., threat to athletic identity, uncertain recovery, letting others down, and lack of perceived control).^24,45,46

The combined effects of clinical levels of state anxiety and post-concussion vestibular/ocular motor provocation were associated with protracted recovery—even when accounting for a history of anxiety and depression and symptom burden. This has been documented in patients with vestibular dysfunction, where those with psychiatric comorbidity exhibit more severe impairments and worse outcomes compared with those without psychiatric disorders.^47
–49 Specific to the concussion literature, it is well documented that vestibular/ocular motor provocation^50
–52 and post-injury anxiety^53
–55 are independently associated with longer recovery times. Moreover, prior research has determined that there is a dose–response effect of modifying factors on concussion recovery, with two post-injury factors (i.e., vestibular/ocular motor symptom provocation and state anxiety) demonstrating a compounded effect on the median recovery time compared with no modifying factors.²⁷ Although determining the reason for this relationship with protracted recovery was outside the scope of this study, it is plausible that elevated levels of vestibular dysfunction with anxiety (enhanced avoidance coping style) may interfere with adherence to treatment recommendations. The greater odds of protracted recovery with vestibular/ocular motor symptom provocation and state anxiety (OR = 2.47, p < 0.001) compared with symptom burden (OR = 1.70, p = 0.10) is particularly notable, given the abundance of literature identifying acute and subacute symptom severity as the strongest predictor of slower recovery.⁵⁶ These data suggest that this combination may be linked to protracted recovery following concussion.

Strengths and limitations

There are several strengths and limitations to the current study that warrant mention. Notably, it is the first study to our knowledge to examine the combined effect of vestibular/ocular motor provocation and state anxiety on concussion recovery time. The study utilized a large sample of patients (n = 532) seeking care for concussion and controlled for pre-existing differences and confounding factors across all analyses. The only significant between-group difference that was not controlled for was age due to the similarities in the means and SDs of each group (PROV = 17.15 ± 2.57 years, NO PROV = 16.61 ± 2.20 years). The current study’s limitations also include a wide enrollment range for the sample (i.e., up to 30 days following injury). Although this wide range was chosen to maximize the sample size, between-group differences in time until the first clinical visit were evaluated and controlled for appropriately. This range may also increase generalizability to common clinical presentation timelines since not all concussions are initially evaluated within an acute (<48 h) window. However, the current sample was derived from patients seeking care at a specialty clinic for concussion, which may not be generalizable to other community-based clinical samples (i.e., management from an athletic trainer), as these patients may have a more severe injury, more resources, and/or increased treatment-seeking behaviors. Although the STAI is administered prior to the VOMS due to the standard clinical visit schedule, the directionality of the relationship between vestibular/ocular motor dysfunction and state anxiety post-concussion remains unclear (i.e., the “chicken or the egg” paradox). Increased state anxiety post-concussion could have also led to exacerbated vestibular/ocular motor dysfunction, as evidenced by studies demonstrating increased vestibular sensitivity in patients with anxiety disorders.⁵⁷ Anxiety symptoms are also linked to a variety of maladaptive behaviors,⁵⁸ which were not assessed in the current study, and may also contribute to the risk for poor recovery outcomes. Due to the retrospective nature of the study of a clinical sample, there was no baseline/pre-injury measure of anxiety. All pre-existing conditions (e.g., anxiety, migraine, and concussion histories) were collected via patient self-reports, which are subject to recall bias and possible inaccuracies.

Clinical implications and future research

These findings highlight the importance of evaluating vestibular/ocular motor dysfunction and state anxiety following concussion using a multidomain assessment approach. The shared findings between the current study and those documented in the neurological and otological literature provide additional evidence for the convergent validity of the VOMS in comparison to other established vestibular tests (e.g., positional tests, electronystagmography, and caloric responses)^59,60 that have also been used to identify vestibular dysfunction in individuals with elevated stress and/or anxiety. Future research should examine the efficacy of various treatment strategies in resolving vestibular/ocular motor dysfunction (e.g., vestibular and ocular therapy and reduction of avoidance behaviors) and post-injury anxiety (e.g., exercise, psychotherapy, and medication), including if treating one impairment may mitigate the presence of the other. Future investigations should also aim to fill the gaps in the current study, including examining trait anxiety and vestibular/ocular motor provocation, identifying predictors of co-occurring vestibular/ocular motor provocation and clinical state anxiety presentations, and determining temporal precedence of the vestibular/ocular motor–anxiety relationship post-concussion. Additional study on this topic should also explore subgroups of individuals with more severe levels of anxiety and co-occurring vestibular/ocular motor dysfunction and recovery time following concussion.

Conclusions

Vestibular/ocular motor provocation is associated with increased state anxiety following concussion and the addition of clinical levels of state anxiety to vestibular/ocular motor provocation increases the odds for protracted recovery. These findings underscore the importance of evaluating both the vestibular/ocular motor system and anxiety following concussion.

Transparency, Rigor, and Reproducibility Statement

A total of 1014 patient EMRs met study inclusion criteria, from which 482 (48%) participants were excluded for the following reasons: 161 (16%, 161/1014) reported an MVA mechanism of injury, 261 (26%, 261/1014) were outside of the 15–25-year study inclusion criterion, and 60 (6%, 60/1014) completed their first visit more than 30 days following injury. The final sample comprised 532 (52%) patient records, of which 329 (62%) included recovery data. Forty-three percent (228/532) of cases exceeded clinical cutoffs on the STAI for clinical levels of state anxiety. There were 418 (79%) participants who exhibited provocation on the VOMS and were assigned to the PROV group, and 114 (21%) participants who did not exhibit provocation on the VOMS were assigned to the NO PROV group. To examine differences between the PROV and NO PROV groups on state anxiety scores, a one-way ANCOVA, controlling for sex, symptom burden (yes/no), history of anxiety (yes/no), and history of depression (yes/no) was performed. A chi-square analysis was used to examine differences for exhibiting clinical levels of state anxiety (>40 on STAI) among the PROV and NO PROV groups. An LR with Adj ORs and 95% CIs was performed to identify the relative contribution of vestibular/ocular motor provocation for exhibiting clinical levels of state anxiety (>40 on STAI) among other established predictors, including sex, history of anxiety (yes/no), and symptom burden (yes/no). Participants with recovery time data were extracted from the overall sample and examined separately to explore the combined effects of vestibular/ocular motor provocation and clinical levels of state anxiety on protracted recovery from concussion. Participants who exhibited provocation on the VOMS with clinical levels of state anxiety were classified into a PROV ANX group, and participants who exhibited provocation on the VOMS without clinical levels of state anxiety were classified into a PROV NO ANX group. Between-group differences were evaluated with a series of t-tests and chi-square analyses for all demographics, health history, injury details, symptom burden, and recovery time (days and protracted recovery status). A one-way ANCOVA, controlling for symptom burden (yes/no), history of anxiety (yes/no), and history of depression (yes/no), was performed to test between-group differences on recovery time (days). An LR with Adj ORs and 95% CIs was performed to examine the relative contribution of vestibular/ocular motor provocation with clinical levels of state anxiety on protracted recovery among other predictors, including history of anxiety (yes/no), history of depression (yes/no), and symptom burden (yes/no).

Footnotes

Acknowledgment

The authors would like to acknowledge Ms. Christina Dollar for her assistance with data collection and regulatory oversight for this project.

Authors’ Contributions

M.W.: Conceptualization, methodology, investigation, supervision, visualization, resources, formal analysis, writing—original draft, and writing—review and editing. K.D.: Methodology, data curation, formal analysis, writing—original draft, writing—review and editing, and visualization. S.J.: Conceptualization, methodology, formal analysis, writing—original draft, and writing—review and editing. S.F.: Conceptualization, methodology, formal analysis, writing—original draft, and writing—review and editing. A.J.Z.: Conceptualization, methodology, formal analysis, writing—original draft, and writing—review and editing. P.S.: Conceptualization, methodology, formal analysis, writing—original draft, and writing—review and editing. M.W.C.: Conceptualization, methodology, formal analysis, writing—original draft, and writing—review and editing. A.P.K.: Conceptualization, methodology, formal analysis, writing—original draft, and writing—review and editing. R.J.E.: Conceptualization, methodology, data curation, formal analysis, writing—original draft, writing—review and editing, visualization, and project administration.

Author Disclosure Statement

M.W. has received payment from ImPACT Applications for providing continuing education talks. A.P.K. and M.W.C. receive book royalties from APA Books, and funding for their research through the University of Pittsburgh from the Centers for Disease Control and Prevention, Chuck Noll Foundation for Brain Injury Research, Department of Defense (CDMRP, USAMRAA, USUHS), National Football League, National Institutes of Health (NICHD, NIMH, NINDS), and private donors. P.S. has served as a scientific advisor to ImPACT Applications, Inc., and serves as a consultant to Sway Operations LLC. However, neither ImPACT nor Sway were involved in the conceptualization of the study, the collection, analysis, or interpretation of the data, or the decision to submit the article for publication.

Funding Information

There was no funding provided for this research.

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