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The effects of sleep disturbance and chronotype on baseline vestibular/ ocular motor screening in collegiate athletes

Background: The vestibular/ocular motor screening (VOMS) is a clinically validated screening tool for concussion management. Multiple factors have been known to influence VOMS performance such as preexisting migraine and mood disorders. Poor sleep is an another important variable that warrants investigation as a modifier on the VOMS that may need to be considered during administration. Aim: This study aims to examine whether self-reported sleep difficulties significantly modify baseline VOMS symptom provocation in collegiate athletes. Methods: A total of 191 collegiate student-athletes completed a pre-season baseline VOMS and the 16-item Athlete Sleep Screening Questionnaire (ASSQ) before the start of their respective sport season. The ASSQ was used to establish sleep health variables consisting of hours of sleep per night, sleep difficulties when traveling for sport, chronotype (e.g., morning or evening person), and a sleep disturbance score (SDS) category of none, mild, and moderate + severe. Results: Those who reported sleep disturbances when traveling for sport on that respective ASSQ item had higher pre-test VOMS symptoms (P < 0.001) and symptom provocation on convergence (P = 0.015), horizontal vestibular ocular reflex (VOR) (P = 0.008), and vertical VOR (P = 0.039). There were worse pre-test symptoms (P = 0.015) and provocation on horizontal VOR (P = 0.046) in the moderate + severe SDS group than no SDS. The moderate + severe SDS group reported worse symptom provocation on the horizontal (P = 0.018) and vertical VOR (P = 0.010), and VMS (P = 0.017). No differences were found on VOMS symptom provocation for hours of sleep or chronotype. Conclusions: These results show agreement with previous symptom and neurocognitive data in that sleep difficulties among collegiate athletes may have an important role in the interpretation of baseline concussion testing. It may be beneficial to utilize sleep assessments with baseline concussion testing when using the VOMS as the clinical concussion measurement modality. Relevance for Patients: The addition of sleep assessment may aid sports medicine practitioners in properly interpreting baseline VOMS scores. Pre-season baseline testing may need to be delayed if athletes report with poor sleep in the acute period prior.


Introduction
DOI: http://dx.doi.org/10.18053/jctres.08.202206.018 recommended that early morning or late-night training schedules be avoided to allow for proper sleep and recovery [3]. Lim et al. reported that elite athletes who were an evening chronotype had worse performance compared to those who were a morning chronotype [5]. It is possible that examining chronotype could be a salient factor in determining proper concussion baseline testing methods. Mihalik et al. [6] also suggested that sleep deprived athletes should not engage in baseline concussion testing until they experience a normal night of sleep. More specifically, given the importance of proper concussion management in sport, the relationship of baseline concussion testing and sleep habits in college student-athletes is a particularly important relationship to examine.
Pre-season baseline concussion testing is considered an important aspect of concussion assessment and accurate testing is needed to improve clinical decision making following injury [7]. Baseline assessment should include a combination of subjective and objective measures, including clinical overview, self-report symptoms, neurocognitive evaluation, and balance testing [8]. Given that vestibular impairments are common following concussion [9], the vestibular/ocular motor screening (VOMS) has received growing consideration as a valid and reliable tool to assess vestibular and ocular motor impairments through patient-reported symptom provocation following concussion [8], which have been recommended for inclusion in post-concussion evaluation [10].
A major consideration of baseline and post-injury research is the effects of pre-existing factors that may modify baseline concussion assessment, such as sex [11], attention/learning problems [12,13], migraine history [14], and mental health [15]. Sleep is one such pre-existing variable that could influence baseline scores on concussion testing. McAllister-Deitrick et al. [16] found that in a large sample of college athletes, those with diagnosed sleep disorders (i.e., sleep apnea and insomnia) had higher concussive symptoms during baseline testing. Moran and Ingargiola [17] also showed that athletes who slept <8 h per night before baseline concussion testing showed greater baseline concussion symptoms. It can be surmised that sleep difficulties at baseline testing may influence how these scores can be interpreted for post-concussive assessment. The authors further mentioned a low effect size which calls into question the clinical significance of how sleep disorders may impact baseline concussion testing [17]. Riegler et al. [18] reported that college athletes with insufficient sleep may present with symptoms at baseline concussion testing that is similar to post-concussive symptoms in athletes with adequate sleep. Specific to the VOMS, Moran et al. found that athletes with a preexisting migraine diagnosis reported worse provocation change scores (i.e., change from pre-test to post-task symptoms) on the VOMS smooth pursuit, convergence, vestibular ocular reflex, and vestibular motion sensitivity tasks [14]. Furthermore, athletes with higher pre-injury anxiety, depression, and anxiety with depression revealed higher scores on baseline concussion symptom report scores [15], while those diagnosed with ADHD had worse scores on the VOMS scales of saccades, convergence, vestibular ocular reflex, and visual motion sensitivity [12].
Regarding sleep assessment, a common mode of measurement is with wearable technology (i.e., wrist actigraphy and fitness trackers). However, given the cost of these tools, they may not always be suitable for mass sleep assessment in athletics. Therefore, self-report sleep questionnaires are often utilized to gain insight into sleep quality. However, general sleep screening questionnaires have limited applicability to the athletic population [19]. The Athlete Sleep Screening Questionnaire (ASSQ) [20] was developed as one such measure to detect clinically significant sleep disturbances and dysfunction in an athletic population and has been determined to be a valid and reliable measurement with acceptable internal consistency [20]. Limited research exists on the use of a self-report sleep difficulty questionnaire with baseline VOMS performance. Therefore, the purpose of the present study was to examine whether sleep disturbance, as measured by the self-report ASSQ, significantly modify symptom provocation on baseline VOMS testing in collegiate athletes.

Participants and procedures
A total of 191 collegiate athletes between the ages of 18 and 26 (M = 19.8 ± 1.5 years) from a single academic institution in the Rocky Mountain region consented to participate in the study. Of the sample, 98 (51.3%) identified as female and 93 (48.7%) as male. Regarding academic class in school, there were 48 (25.1%) freshmen, 52 (27.2%) sophomores, 43 (22.5) juniors, 34 (17.8) seniors, and 14 (7.3%) 5 th year/graduate students. Participants completed a pre-season baseline VOMS and ASSQ in a counterbalanced manner as part of pre-season sports medicine screening at the participating university.

Measures
Sleep disturbance was measured using the ASSQ [19][20][21]. The ASSQ consists of 16 items, with five items used to determine a sleep disturbance score (SDS). In addition, there are four items used to determine a morning (e.g., early bird) or evening (e.g., night owl) chronotype score that is based on a 15-point scale, which reflects their natural inclination of their body to sleep at certain times. A classification is given to respondents as having an evening chronotype (i.e., awake late at night) if their score was ≤4 [4]. Athletes with an evening chronotype are identified as being higher risk for sleep disturbance. Further assessment is recommended for athletes who are placed in the moderate or severe SDS category, have an evening chronotype, or indicate sleep-disordered breathing. The remaining five items are used to evaluate napping frequency, intake of caffeine, use of electronic devices before bed, and travel-related sleep disturbance.
For categorizing individuals into sleep health groups for VOMS comparisons, some ASSQ item responses (Table 1) were categorized appropriately. ASSQ #1 inquiries about recent hours of sleep at night, with responses of 5 -6, 6 -7, 7 -8, 8 -9, and 9+ h. For this study, we included an additional variable titled "selfreported sleep quantity," which categorized answers into <7 h These categories include none (SDS of 0 -4), mild disturbance (SDS of 5 -7), moderate disturbance (SDS of 8 -10), and severe disturbance (SDS of 11 -17). Based on category, appropriate sleep recommendations are outlined. Since moderate and severe scoring both recommend assessment by a sleep medicine physician or qualified sleep professional, those categories were combined into one group (moderate + severe sleep problems) for data analyses. All other ASSQ items, such as snoring or sleep apnea inquiry, were not included in the analyses.
The VOMS is a brief, clinical screening tool that assesses vestibular and ocular impairment and symptom provocation following vestibular-ocular motor tasks in concussion assessment [8,12,[22][23][24]. The VOMS is comprised seven tasks: Smooth pursuits, horizontal and vertical saccades, convergence, horizontal and vertical vestibular ocular reflex (VOR), and visual motion sensitivity (VMS). Before administering the VOMS tasks, the individual is asked to rate their symptoms (pre-test) of headache, dizziness, nausea, and fogginess from 0 (none) to 10 (severe). Following each task, the individual rates their symptoms again, producing a symptom provocation score. VOMS provocation scores as calculated as a change from pre-test scores [25]. For example, if an individual reports a 1 on headache at pre-test and a 2 following smooth pursuits, a 1 symptom provocation score is present for smooth pursuits. An objective measure, near point of convergence (NPC) distance is also recorded during the convergence task [8]. The VOMS is a valid tool for detecting concussion, with a high internal overall consistency, with Cronbach alphas between 0.92 and 0.99 [22,[26][27][28].

Statistical analyses
General descriptive and inferential statistics were used to summarize all demographic information, ASSQ scores, and VOMS symptoms. A series of Shapiro-Wilk tests were conducted to test for normality. Due to non-normative data, a series of Mann-Whitney U-tests were conducted to determine differences between dichotomous (yes or no) variables of sleep disturbance reporting (ASSQ #11), daytime dysfunction reporting (ASSQ #12), chronotype category (ASSQ #9; morning vs. evening), and recent self-reported sleep quantity (<7 and ≥7 h) and VOMS symptom provocation. A Kruskal-Wallis H test was conducted to compare SDS category (none, mild, and moderate + severe) on VOMS symptom provocation. A series of Mann-Whitney U-tests were conducted between groups for post hoc comparisons of significant Kruskal-Wallis H test results. Mean scores are provided for VOMS symptom provocation for ease of clinical application and common clinical scoring. Due to non-parametric data, medians and interquartile ranges were calculated for the sample and between groups.

Sleep health demographics
Of the 191 collegiate athletes in the study, 101 (53%) did not report a sleep disturbance when traveling for sport and 90 (47%) did report a sleep disturbance. Regarding daytime dysfunction

VOMS differences on sleep health when traveling
A series of Mann-Whitney U-tests revealed significant differences between sleep disturbance group, with those who reported sleep disturbances when traveling for sport having higher pre-test VOMS symptoms (U = 3316.0, P < 0.001) and symptom provocation on convergence (U = 4125.0, P = 0.015), horizontal VOR (U = 3844.5, P = 0.008), and vertical VOR (U = 4062.0, P = 0.039) than those who did not report a sleep disturbance ( Table 2). In addition, those who self-reported daytime dysfunction when traveling for sport reported higher symptoms on pre-test (U = 2199.5, P = 0.002) and provocation on convergence (U = 2734.0, P = 0.042) as compared to those who do not ( Table 2). NPC distance also differed between groups, with worse distance in those reporting daytime dysfunction (U = 2195.0, P = 0.007).

VOMS differences on SDS category
The findings of the Kruskal-Wallis H test to compare VOMS performance between SDS category (Table 4)

Discussion
The purpose of the present study was to examine whether self-reported sleep difficulties influenced symptom provocation  In addition, daytime dysfunction was significantly related to worse pre-test concussive symptoms, symptom provocation on convergence, and NPC distance. While baseline concussion testing is unlikely to occur when traveling for sport, these results still have important implications. If baseline testing is occurring before the beginning of the academic and athletic year (i.e., before start of fall semester), many athletes may be returning to the university from out-of-state locations. It would be wise for the athletic training staff to delay baseline concussion testing until athletes have reacclimated to being back on campus. There may be acute sleep disturbances that occur from traveling back to school, which could negatively influence baseline VOMS testing. Mihalik et al. [6] found that in their sample college athletes, one night of poor sleep led to a greater number of reported baseline concussive symptoms, as well as greater severity in symptom scores. Caccese et al. [29] also found that in a sample of 30,587 participants, composed of both military cadets and college athletes, poor sleep was a salient factor in leading to higher symptom reporting in those who did not experience a recent concussion. Given this effect, sports medicine professionals need to consider both acute and chronic sleep disturbances in their athletes. Before baseline concussion testing, one strategy may be to have athletes self-report sleep in the week before testing to establish a baseline of normal sleep habits. Once a baseline is established, they can continue to selfreport and follow-up with the sports medicine for any patterns of sleep disturbance. Baseline concussion testing may need to be halted until sleep patterns have normalized. As the research has demonstrated, even a single night of poor sleep can significantly alter baseline concussion testing outcomes. This strategy may also aid in identifying athletes who have pre-existing sleep conditions and can be provided further consultation and support with a sleep health professional. In addition, this knowledge will aid the sports medicine staff in having a better interpretation of baseline concussion scores.
As it relates to chronotype, athletes who reported being an evening type had higher symptom provocation on horizontal saccades when compared to athletes who reported being morning types. Zils et al. [30] found that one night of sleep deprivation impaired peak velocity saccadic eye movement. However, peak velocity returned to normal after a night of normal sleep. This would indicate that performing baseline VOMS testing after a night of poor sleep may indicate symptoms that would otherwise not be present after a normal night of sleep. McClure et al. [31] examined baseline Immediate Post-Concussion Assessment and Cognitive Testing (ImPACT) scores among 3686 athletes after a single night of sleep. The authors stratified the athletes into three groups: <7 h of sleep, 7 -9 of sleep, and >9 h of sleep. Results revealed athletes who slept <7 h reported worse performance on ImPACT baseline testing, while also reporting more baseline symptoms. It should be noted that our present sample showed no significant differences on any baseline VOMS pre-test symptoms or symptom provocation between athletes who slept <7 h and those who slept more. Poor sleep the night before baseline concussion testing can negatively impact symptoms. However, this finding may not be consistent among all athletes. This highlights the importance of an individualized approach when conducting baseline concussion testing. Athletes who regularly get 7 h of sleep per night may experience less dysfunction when receiving <7 h of sleep compared to athletes who routinely get closer to 9 or more hours of sleep.
Results did reveal a significant relationship with SDS on pretest symptoms and symptom provocation for horizontal VOR, vertical VOR, and VMS. When athletes who reported moderate or severe sleep disturbances were combined into a single category (i.e., moderate + severe SDS), analyses indicated that they reported worse pre-test concussion symptoms compared to athletes who reported no sleep disturbances. Moreover, athletes in the moderate + severe SDS group had worse symptom provocation on the horizontal VOR when compared to athletes who reported no SDS. Athletes in the moderate + severe SDS group further showed worse scores on horizontal VOR, vertical VOR, and VMS when compared to athletes reporting mild SDS. These results further align with the previous research showing that sleep has an important role in the interpretation of baseline concussion testing.

Limitations and future research
The present study was not without limitations. Sleep was measured as a 1 time assessment and may not accurately reflect objective sleep measurements and chronic sleep quality among participants in the current study. In addition, participants were not screened or queried for the presence of sleep disorders, which may have influenced results. For example, it was not determined before data collection if athletes were suffering from or diagnosed with sleep apnea, restless leg syndrome, or narcolepsy. Concussion history was based on self-report which could introduce accuracy bias as to proper recall of concussive events. Participants were asked to recall the number of diagnosed concussions, which may not accurately reflect the number of actual diagnosed or unreported/ undocumented concussions by a medical professional. Future research should examine sleep difficulties and diagnoses between seasons, during travel periods, at night after competition, and after rest/off-days. Further, attempts should be made to determine how SDS score and chronotype may affect other baseline measures of injury assessment not only for concussion, including balance, cognition, and reaction time. In addition, as the ASSQ provides indications of further assessments by a sleep expert for those in moderate or severe SDS category, future research should examine how VOMS provocation may change following interventions.

Conclusions
These data reveal that sleep disturbances can cause deleterious effects on baseline symptom reporting and VOMS symptom provocation scores in the absence of a concussive injury. It is warranted that members of the sports medicine staff consider acute and chronic sleep disturbances in their athletes before engaging in pre-season VOMS testing for concussion screenings.