Migraine history affects vestibular ocular motor screening,King-Devick,and reported symptoms in collegiate student-athletes: Findings from the concussion assessment,research,and education consortium

Abstract

Background

Migraine, a common neurological disease, can negatively impact vestibular and oculomotor functioning. Vestibular and oculomotor function and symptomology are routinely tested in collegiate athletes as part of baseline concussion assessments. The purpose of this study was to identify how migraine history influences vestibular ocular baseline assessments in collegiate student-athletes.

Methods

A total of 1775 collegiate student-athletes from de-identified data provided by the National Collegiate Athletic Association – Department of Defense Grand Alliance from 2014 to 2020. Participants self-reported migraine status, sex, age, Hospital Anxiety and Depression score, and sleep were used to predict Vestibular/Ocular Motor (VOMS) provocation scores, King-Devick times, and Sport Concussion Assessment Tool (SCAT) symptom scores.

Results

Participants with migraine history have 1.75 odds of reporting abnormal baseline VOMS symptoms (≥2) than those without migraine (p = 0.007, 95% confidence interval [CI] 1.15, 2.63). Participants with migraine also had a predicted 1.15-point higher total symptom score and a 4.1-point symptom severity increase on the SCAT. Migraine did not significantly influence King-Devick performance. Females had 1.44 odds of slower reading times on the King-Devick (p < 0.001, 95% CI: 1.15, 1.81).

Conclusions

Migraine history was the highest predictor of abnormal baseline vestibular ocular performance and symptoms in collegiate student-athletes. Female sex, concussion history, sleep, and anxiety and depression history also significantly contributed to baseline concussion performance. Identification of patient history prior to test interpretation is vital for appropriate diagnosis and care.

Graphical abstract

This is a visual representation of the abstract.

Keywords

brain injury vision headache concussion

Migraine affects ∼15% of the general population and 5.6% of collegiate student-athletes.¹ The pathophysiology of migraine may be responsible for differences in an individual's vestibular ocular assessment performance and reported symptoms. For example, activation of the trigeminovascular system, through the dura mater or large arteries with mechanical, chemical, or electrical stimulation, triggers the start of the headache phase during migraine.² This activation of sensory afferent nerves is believed to be responsible for the pulsating quality and pain distribution of migraine headaches.^3–5 The nociceptive innervation from the meninges and larger cerebral arteries primarily comes from the ophthalmic (V1) branch of the trigeminal nerve,⁶ while inflammation affecting the trigeminal nerve fibers projecting to the inner ear may explain some of the vestibular migraine symptoms.² These trigeminal system changes may be precipitated by both structural and functional anatomical brainstem changes that are present both during and after migraine attacks.^7,8 Additionally, cortical spreading depression may affect areas of the cortex involved in ocular and vestibular processing, leading to deficits in these areas during migraine.^2,9

Vestibular oculomotor and symptomatology assessments are routinely performed in collegiate student-athletes to determine baseline function status. Previous studies have identified that individuals with migraine have performed abnormally on other vestibular ocular assessments¹⁰ and report higher symptoms¹¹ than those without migraine. Subclinical dysfunction of the vestibular system has been identified in individuals with migraine between migraine attacks (i.e. interictal).¹² If a similar disruption is occurring during testing, this may influence test scores and interpretation. The purpose of the current study was to determine the risk of collegiate student-athletes with migraine performing abnormally on commonly used vestibular ocular assessments in the collegiate setting and reporting higher overall symptoms. The hypothesis was that there would be no difference in any outcomes (e.g. baseline symptoms, vestibular ocular tasks) between student athletes who reported a history of migraine and those who did not.

Methods

Participants

First-year data from collegiate student-athletes from 26 universities in all divisions of the National Collegiate Athletic Association (NCAA) from the concussion, assessment, research, and education (CARE) consortium were eligible for inclusion (n = 34,865). All institutions obtained IRB approval from their respective sites, with additional approval obtained from the Human Research Protection Office of the Department of Defense. All participants provided written informed consent prior to data collection in accordance with the Declaration of Helsinki.

Procedures

De-identified data was provided by the CARE consortium from 2014 to 2020. Participants completed pre-season concussion baseline testing at their respective institutions, consisting of demographics, medical history, symptomology, postural control, neurocognitive functioning, and optional vestibular ocular testing. The CARE consortium has been described in greater detail elsewhere.¹³ First-year participant data were identified. Individuals who did not complete the vestibular ocular motor screening (i.e. VOMS) and King-Devick (i.e. KD) tests, or were missing migraine status, were removed from the dataset. Descriptive statistics (i.e. biological sex, age, migraine status, and hours of sleep) of the remaining participants was determined.

Instrumentation

All descriptive statistics were collected by self-report in the medical history. Migraine status was determined by self-report with the question “Have you ever been diagnosed by a Physician/MD with migraine headaches?” Hours of sleep was self-reported with the question “How many hours did you sleep last night?” The Hospital Anxiety and Depression Scale (i.e. HADS) is a self-report 14-item questionnaire for how anxious or depressed the respondent has been feeling in the past week. Higher scores indicate potential and abnormal cases.¹⁴

Statistical analysis

Demographic data and frequency histograms were analyzed to adjust the overall conceptual models. Non-parametric tests were used to compare the nonmigraine and migraine groups due to the skewed distribution of the data (W = 0.277, p < 0.001). Binary categories for VOMS were defined as normal (< 2) or abnormal (≥ 2) symptoms at baseline (i.e. pre-test) or symptom provocation (i.e. sum of sub-test symptoms).¹⁵ KD categories were defined as normal and abnormal (5 s slower than the group mean).¹⁶ Two univariate logistic (i.e. VOMS and KD) and two univariate linear (i.e. SCAT) regressions were used to assess for the effects of the student-athletes age (age), sex (male and female), migraine status (no migraine history and migraine history), number of previous concussions (total concussions), reported sleep from the previous night (hours), and HADS total score (anxiety and depression subscale total) on the relationship of the baseline assessments. Reference categories were selected because they were either temporally first or the largest. Analysis was completed in R (Vienna, Austria).¹⁷

Results

Demographics

Out of the 33,090 student-athletes, 644 were removed due to a missing migraine diagnosis. Another 32,446 were excluded due to missing clinical assessments of interest, leaving a total of 1775 participants in the final analysis. Summary statistics associated with the demographic variables used in the regression models are displayed in Table 1. From the 1775 participants that were included in the study, 52.1% (n = 924/1775) identified as female, 46.4% (n = 823/1775) identified as male, and 1.6% (n = 28/1775) did not disclose. The mean age was 19.1 years (SD = 1.65). Of the student-athletes, 7.0% (n = 124/1775) self-reported a migraine diagnosis. Forty-five percent of the population with an abnormal VOMS provocation score also had migraine history (n = 56/124). Those reporting a history of migraine diagnosis had 1.75 odds of reporting abnormal (≥ 2 symptoms) at baseline VOMS testing than peers without migraine (p = 0.007, 95% confidence interval [CI]: 1.15, 2.63). Females had 1.48 odds of abnormal VOMS baseline symptoms (p = 0.001, 95% CI: 1.48, 1.86) than males. For each one-point change in total HADS score, there was a 1.14 odds of reporting abnormal symptoms on baseline VOMS (p < 0.001, 95% CI: 1.11, 1.17). For each previous concussion, there was a 1.13 odds of abnormal baseline VOMS (p = 0.05, 95% CI: 1.00, 1.29).

Table 1.

Participant demographics.

Variable	No migraine (n = 1651; 93.0%)Median (25%, 75%)	Migraine (n = 124; 7.0%)Median (25%, 75%)	p-value
Sex (female; n, %)	852 (51.6)	82 (66.1)	0.002**
Age (years)	18 (18, 20)	18 (18, 20)	0.33
Number of previous concussions	1.0 (1.0, 2.0)	1.0 (1.0, 3.0)	0.002**
HADS total score	5.0 (3.0, 9.0)	6.5 (3.0, 10.0)	<0.001***
Sleep last night (hours)	7.0 (6.0, 8.0)	7.0 (6.0, 8.0)	0.90
SCAT total symptoms	1 (0.0, 5.0)	3 (1.0, 6.8)	<0.001***
SCAT symptom severity	2.0 (0.0, 7.0)	4.5 (1.0, 18.5)	<0.001***
King-Devick (mean, SD)	44.56 (9.0)	44.34 (9.5)	0.80
Abnormal VOMS baseline (n, %)	388 (23.5)	52 (41.9)	<0.001***
VOMS symptom provocation (n, %)	511 (30.1)	65 (52.4)	0.02*

HADS: Hospital Anxiety and Depression Scale; SCAT: Sport Concussion Assessment Tool; VOMS: vestibular ocular motor screening.

*p < 0.05, **p < 0.01, ***p < 0.001.

Neither migraine history nor sex significantly predicted abnormal VOMS symptom provocation score (p = 0.53, 95% CI: 0.76, 1.68; p = 0.15, 95% CI: 0.95, 1.41). However, for each one-point change in HADS, there was a 1.12 odds (p < 0.001, 95% CI: 1.10, 1.15), and for each previous concussion reported, there was a 1.29 odds (p < 0.001, 95% CI: 1.14, 1.46) of abnormal symptom provocation score. For each year age increased, there was a 1.07 higher odds of abnormal VOMS provocation score (p = 0.019, 95% CI: 1.01, 1.14). As hours of sleep increased, odds of abnormal score decreased; however, this was not a significant predictor (B = −0.03, p > 0.05, 95% CI: −0.10, 0.04).

Migraine history did not significantly predict abnormal KD performance (B = 0.04, p = 0.86, 95% CI: −0.41, 0.47). However, females had 1.44 odds of slower times (p < 0.001, 95% CI: 1.15, 1.81), and each additional previous concussion increased odds of slower reading times by 0.70 (p < 0.001, 95% CI: 0.58, 0.82). HADS, hours of sleep, and age were not significant predictors in this model.

Linear regressions for SCAT symptoms and symptom severity were similar, with all predictors significantly contributing to the models. Age was not included in the final models. For total symptoms, those with migraine were predicted to have a 1.15 higher score (p < 0.001, 95% CI: 0.59, 1.70, η_p = 0.01) while females have a predicted 0.92-point increase (p < 0.001, 95% CI: 0.63, 1.19, η_p = 0.02). Each previous concussion was associated with a 0.23-point increase (p < 0.001, 95% CI: 0.05, 0.39, η_p = 0.00) and each point on the HADS total score was associated with a 0.35-point increase (p < 0.001, 95% CI: 0.32, 0.38, η_p = 0.23). Each hour of sleep was associated with a decrease in 0.34 points (p < 0.001, 95% CI: −0.44, −0.24, η_p = 0.03). The adjusted R2 was 31%.

For symptom severity, those with migraine had a 4.1-point increase (p < 0.001, 95% CI: 2.74, 5.41, η_p = 0.02) and females had a 1.9-point higher score (p < 0.001, 95% CI: 1.23, 2.58, η_p = 0.02). Each previous concussion was associated with a 0.62-point increase (p = 0.003, 95% CI: 0.21, 1.02, η_p = 0.01), while each point on the HADS total score was associated with a 0.84-point increase (p < 0.001, 95% CI: 0.76, 0.91, η_p = 0.23). Each hour of sleep was associated with a decrease by 0.87 points (p < 0.001, 95% CI: −1.11, −0.63, η_p = 0.03). The adjusted R2 for this model was also 31%.

Discussion

Participants with migraine history were more likely to have abnormal baseline VOMS symptoms and higher SCAT total symptoms and symptom severity. Other modifying factors included female sex, age, concussion history, anxiety and depression, and sleep. Healthcare professionals should take care to include these factors in pre-participation health history questionnaires and screen for them prior to test interpretation. The findings in this study provide important clinical considerations for clinicians working with individuals with migraine. The VOMS and KD exams are commonly used as part of the baseline sport concussion assessment and can be used to help diagnose concussion in the absence of a baseline test due to their high sensitivity.^15,16 Almost a third (32.5%; n = 576/1775) of individuals in this study had an abnormal VOMS provocation (≥ 2) score at baseline. These data highlight a need to further identify contributors to positive testing that can help in clinical decision making that may lead to better health outcomes. Prior studies have identified the dose-response effect of multiple conditions on concussion recovery. Individuals with a history of mental health diagnoses, visio-vestibular deficits, and higher emotional burdens had longer concussion recovery times.^18,19 Understanding the relationships of these pre-existing conditions, including migraine and its effects on the ocular and vestibular systems, are important for healthcare providers in tailoring treatment plans and support strategies.

Abnormalities in patients with migraine during migraine-free periods have been previously identified. “Resting state” functional magnetic resonance imaging studies within migraine patients identified subtle differences in brain structure and function in pain-processing areas and the trigeminal system, even while not currently suffering from a migraine (i.e. interictal).^20,21 A study in patients with vestibular migraine found that 42% of patients had abnormal oculomotor tests (e.g. video head impulse test, caloric test, and videonystagmography) during interictal periods.¹⁰ Individuals with migraine also performed worse on the trail making test, a visuo-motor task, than controls,²² as well as slower reactions on the Stroop III and Shape Trail Test.²³ The impaired executive control in these individuals may suggest that the neural networks are negatively affected by migraine, even during headache-free periods.

The results in the current study differ from a study by Kontos et al.²⁴ in which collegiate student-athletes diagnosed with migraine were not more likely to have VOMS scores greater than or equal to one than those without a migraine history. However, in a pediatric population, those with migraine did perform worse on many of the VOMS subtests and had worse times on KD.²⁵ The other variables, including sex,²⁶ age,²⁷ concussion history,²⁸ anxiety, and depression,²⁹ have also been previously associated with decreased vestibulo-ocular performance.

Limitations

Our study has several limitations. First, participant data was only from their first year of participation in the CARE consortium, and headache status was part of a larger health-history questionnaire. The type of migraine experienced (e.g. with/without aura, vestibular) was not assessed, and differences in pathophysiology between migraine types may affect symptomology and resultant vestibular ocular effects experienced. Self-reported migraine status may also be a limiting factor, as it is subject to several forms of bias. Participants may misremember, underreport, or overreport medical diagnoses due to recall bias, social desirability bias, or lack of clinical confirmation. The accuracy of this information can also vary based on health literacy and access to prior diagnoses. Future studies should aim to corroborate this self-reported data against medical records, including following the ICHD criteria of migraine³⁰ and documentation of symptoms with a headache diary, when possible. Additionally, headache status at the time of data collection was not known and may play a role in symptomology and performance on these assessments. From the large initial sample, many participants had to be removed due to data not being collected or missing information due to some assessments (e.g. VOMS and KD) being optional at satellite sites, leading to a potentially less representative sample of collegiate student-athletes. However, student-athletes across years from multiple institutions and 15 different sports were still included in the final analysis. Differences in assessment methodology across testing sites were not considered. For example, KD administered on a tablet versus paper cards has been associated with a 2.8-second slower testing time.³¹ Finally, additional covariates were not included in the analysis, including use of prescription and over-the-counter medications for migraine, history of motion sickness, history of vestibular/ocular disorders, history of psychiatric disorders, or history of attention-deficit disorder/attention-deficit/hyperactivity disorder or learning disorder. Future studies may consider adding these to their analysis as they have been identified as affecting some concussion baseline outcomes.

Conclusion

Though migraine is a common neurological comorbidity, its effect on the patient has not been well established. The clinician should be aware of the condition and how it may be influencing concussion baseline test results. Increased baseline VOMS symptoms and symptom severity due to migraine status may influence provider interpretation of clinical testing and recommendations. Other potential influencing variables (e.g. age, concussion history, and sex) should also be considered.

Key findings

Migraine history was the largest predictor of abnormal baseline vestibular ocular motor screen performance in collegiate student athletes, with 1.75 odds of an abnormal test than those without migraine history.

Those with migraine are predicted to report 1.2 more symptoms than those without migraine and a 4.1 higher symptom severity score.

Footnotes

Acknowledgments

The authors thank the CARE Consortium Investigators: April Hoy MS, ATC (Azusa Pacific University), Louise A. Kelly, PhD (California Lutheran University), Jessica Miles, PhD, ATC (Florida College), John DiFiori, MD (Hospital for Special Surgery), Justus Ortega, PhD (Humboldt State University), Nicholas Port, PhD (Indiana University), Michael Collins, PhD and Anthony Kontos, PhD (University of Pittsburgh), Margot Putukian, MD (Major League Soccer), Christopher D’Lauro, PhD, United States Air Force Academy), Kenneth L. Cameron, PhD, MPH, ATC and Steven J. Svoboda, MD (United States Military Academy), Adam Susmarski, DO (United States Naval Academy), Joshua Goldman, MD, MBA, (University of California at Los Angeles), Thomas W. Kaminski, PhD, ATC and Thomas Buckley, EdD, ATC (University of Delaware), James R. Clugston, MD (University of Florida), Joseph Hazzard, EdD, ATC (University of Houston – Clear Lake), Julianne Schmidt, PhD, ATC (University of Georgia), Patrick O’Donnell, MHA, MBA (University of Massachusetts), Luis Feigenbaum, PT, DPT, ATC (University of Miami), J. T. Eckner, MD (University of Michigan), Jason Mihalik, PhD, CAT(C), ATC and Kevin Guskiewicz, PhD, ATC (University of North Carolina at Chapel Hill), Kristy Arbogast, PhD (University of Pennsylvania), M. Alison Brooks, MD MPH (University of Wisconsin-Madison), Steve Rowson, PhD and Stefan M. Duma, PhD (Virginia Tech), Chris Miles, MD and Laura Lintner, DO (Wake Forest University). We would also like to extend our appreciation to Jody Harland, Janetta Matesan, and Michael Menser (Indiana University School of Medicine); Ashley Rettmann and Nicole L’Heureux (University of Michigan); Melissa McEachern (Medical College of Wisconsin); Michael Jarrett, Vibeke Brinck, and Bianca Byrne (Quesgen); Melissa Baker, Christy Collins, Will Felix, and Bethany Morath, (Datalys Center for Sports Injury Research and Prevention); and the research and medical staff at each of the CARE participation sites. The authors are grateful for the participation of the student-athletes, without whom this research would not be possible.

ORCID iDs

Karlee Burns

Jane McDevitt

Consent to participate

All participants provided written informed consent prior to data collection in accordance with the Declaration of Helsinki.

Consent for publishing

Yes.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This research was supported by the Grand Alliance Concussion Assessment, Research, and Education (CARE) Consortium, funded in part by the National Collegiate Athletic Association (NCAA) and the Department of Defense (DOD). This work was supported by the Office of the Assistant Secretary of Defense for Health Affairs, through the Combat Casualty Care Research Program, endorsed by the Department of Defense, under Award No. W81XWH1420151. Opinions, interpretations, conclusions, and recommendations are those of the author and are not necessarily endorsed by the DOD.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Data availability statement

The data that support the findings of this study are available upon reasonable request from the corresponding author.

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