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Caution in Clinical Interpretation of Near Point of Convergence: Influence of Time of Day on Oculomotor Function

2019; Volume: 13; Issue: 1 Linguagem: Inglês

10.3928/19425864-20190613-01

1942-5872

Sarah Coon, Zachary W. Bevilacqua, McCarthy Ferris, Zhongxue Chen, Keisuke Kawata,

Ophthalmology and Eye Disorders

Original Research freeCaution in Clinical Interpretation of Near Point of Convergence: Influence of Time of Day on Oculomotor Function Sarah Coon, MS, ATC, , , MS, ATC Zachary W. Bevilacqua, MS, ATC, , , MS, ATC McCarthy Ferris, BS, , , BS Zhongxue Chen, PhD, , and , PhD Keisuke Kawata, PhD, ATC, , PhD, ATC Sarah Coon, MS, ATC , Zachary W. Bevilacqua, MS, ATC , McCarthy Ferris, BS , Zhongxue Chen, PhD , and Keisuke Kawata, PhD, ATC Published Online:June 13, 2019https://doi.org/10.3928/19425864-20190613-01Cited by:1AbstractPDF 308.4 KB ToolsAdd to favoritesDownload CitationsTrack CitationsCopy LTI LinkHTMLAbstractPDF ShareShare onFacebookTwitterLinkedInRedditEmail SectionsMoreAbstractPurpose:To test whether near point of convergence (NPC) is stable across morning to night.Methods:Thirty healthy adults with an average sleep duration of 7 hours or more at night were recruited. The study used time (7 AM and 7 PM) as the independent variable and NPC as the outcome variable. To objectively assess one's average sleep duration, participants wore an activity/sleep tracker (ActiGraph) for 7 days prior to the study. NPC was measured by using an accommodative ruler with a target approaching participants' eyes at a speed of 2 cm/sec. Measurements were recorded when the participant reported experiencing diplopia or malalignment of the eye was observed. The assessment was repeated twice. Mean NPC (cm) was used for analyses.Results:NPC at 7 PM (6.35 ± 2.37 cm) was significantly worse compared to 7 AM (5.27 ± 2.00 cm, P < .001). After adjusting for a significant covariate (contact lens use), an estimated difference between 7 PM and 7 AM was 0.70 ± 0.98 cm, t(29) = 3.15, P = .0039.Conclusions:Results indicate that after a period of wakeful time, oculomotor function begins to decline. Although NPC emerges as a tool for concussion assessment, the time of day needs to be considered when interpreting the data.[Athletic Training & Sports Health Care. 2021;13(1):7–10.]IntroductionConcussion is classified as a mild form of traumatic brain injury, but changes in neural function following concussions are far from benign. In pursuit of identifying quick, reliable, and objective metrics to diagnose a concussion, various resources have indicated that as many as 69% of patients with a concussion exhibit some form of visual dysfunction, including accommodative disorders, convergence insufficiency, or saccadic dysfunction.1,2 Receded binocular convergence has been proposed as a chief indicator of neuro-ophthalmologic perturbation.3–5 Binocular convergence, often referred to as near point of convergence (NPC), measures the closest point to which one can focus on an object before diplopia occurs. NPC measurement is an emerging clinical tool with which clinicians can objectively identify abnormal behavioral traits in patients with potential concussion.5 In addition, NPC measurements are advantageous because they require no baseline data, have relatively well-established normative cut-off values, and can be easily administered with the use of an accommodation ruler.6Athletes with concussions have exhibited threefold worsening in NPC as compared to control individuals, with this single clinical metric yielding 73% of diagnostic accuracy for concussion.5,7,8 In previous clinical studies, we have demonstrated that NPC assessment is also sensitive enough to detect a transient neuronal dysfunction from subconcussive head impacts (eg, soccer heading and football tackle), where NPC worsened by approximately 29% to 38% relative to baseline values.9–11 Not only do mechanical forces to the brain impair NPC, but studies have also shown that neural fatigue from sleep deprivation significantly attenuates ocular-motor function.12,13 However, there is a substantial knowledge gap in the time-of-day influence on NPC. Therefore, this study aimed to answer whether the NPC is stable between morning and night despite potential neural fatigue from daily conscious activity. We hypothesized that there would be a significant worsening (increase) in NPC at night (7 PM) compared to morning (7 AM).MethodsParticipantsThirty healthy college-aged adults volunteered to participate in this study. Our sample size was determined by a power analysis using data from previous sleep deprivation literature, and 30 participants was estimated to yield at least 90% statistical power for this study. The study consisted of 16 men and 14 women with an average age of 20.4 ± 1.0 years and body mass index of 24.79 ± 3.0 k/m2, 11 of 30 participants wore contact lenses, and 10 of 30 participants had a history of one concussion. Inclusion criteria were age 18 to 26 years and average sleep duration of 7 hours or more at night, as well as a minimum of 7 hours of sleep a night before the testing, validated by a wrist-worn ActiGraph device (ActiGraph, Pensacola, FL). Exclusion criteria were any history of head injury in the 1 year prior to the study and any neurological, ocular, or sleep disorders. Two days prior to the study and during the study, participants were instructed to refrain from substances that could affect their nervous systems (eg, caffeine, alcohol, or depressants). To control participants' baseline neural fatigue, for 1 week prior to the study, potential participants were instructed to record their sleep cycle on a sleep log and were fitted with an ActiGraph wGT3X-BT to monitor their sleeping duration. Prior to test 1 (7 AM), participants' sleep duration was screened via the data from ActiGraph, and then participants who slept less than an average of 7 hours per night were excluded from the study. All participants gave written informed consent, and Indiana University's Institutional Review Board approved the study.Sleep and Activity MonitorThe ActiGraph measures human motion and step counts using a tri-axial accelerometer while eliminating non-human motion by suppressing high acceleration data.14 ActiLife (version 6.5.3; ActiGraph) software was used for the sleep analysis, and we employed the Sadeh algorithm to score sleep duration, which has been validated with 91.4% to 96.5% minute-by-minute agreement rates in adults compared with traditional polysomnography.14 A subjective sleep log was used to visually inspect the ActiGraph data.NPC MeasureNPC was assessed at 7 AM and 7 PM based on our established protocol.9,10 Briefly, using the accommodative ruler (Gulden Ophthalmics), a target was moved toward the eyes at a rate of approximately 1 to 2 cm/s. NPC, the distance between the participant and object, was recorded when the tester observed eye malalignment or when participants verbally signaled experiencing diplopia. The assessment was repeated twice, and mean NPC was used for analyses. One trained tester (SC) assessed all participants at all time points, and an intraclass correlation coefficient (ICC) between trials 1 and 2 indicated that there was a significant agreement between trials (ICC = 0.974, 95% confidence interval [CI] = 0.948 to 0.987, P < .001).Statistical AnalysisWe first used a two-tailed paired t test to compare the means of NPC between 7 AM and 7 PM. In a linear regression model, we evaluated potential covariates that may significantly modulate NPC changes (age, sex, body mass index, contact lens use, average sleep duration from 7 days prior to the study, the time that the participant awoke during the test day, concussion history, and step counts between 7 AM and 7 PM). If significant, these factors were treated as covariates, and we estimated the changes in NPC between 7 AM and 7 PM in the regression model. Statistical analysis was conducted with SAS software (version 9.4 for Windows; SAS Institute, Inc) and significance was set at a P value of less than .05.ResultsAverage sleep duration for a week prior to the study was 7.49 ± 0.70 hours. Average step counts between 7 AM and 7 PM were 9,037.3 ± 2,577.1 steps. There was a significant time-of-day effect on the ocular-motor function, where NPC at 7 PM (6.35 ± 2.37 cm) significantly worsened compared to 7 AM (5.27 ± 2.00 cm, t(32) = 4.95, P < .001), with a mean difference of 1.08 cm, 95% CI (1.49, 0.68). In a linear regression model, after adjusting for a significant covariate (contact lens use), an estimated difference between 7 PM and 7 AM was 0.70 ± 0.98 cm, t(29) = 3.15, P = .0039 (Figure 1).Figure 1. Near point of convergence (NPC) at 7 AM and 7 PM. (A) Average NPC with standard deviation. (B) Relative change in NPC at 7 PM compared to the baseline (7 AM).DiscussionThe current brief report demonstrates that NPC values significantly worsened following a 12-hour period of routine daily neural fatigue. This finding remains consistent with previous sleep science literature in that neural fatigue induced by prolonged periods of wakefulness results in the impairment of ocular-motor functions including saccades and smooth pursuit.13 Our data indicate that NPC was able to detect a subtle but significant neural fatigue after a 12-hour wakeful period. Because patients with a concussion experience a 300% increase in NPC (Table A, available in the online version of this article),5,7,15,16 the subtle NPC difference between morning and night (13% change) would not influence an accurate concussion diagnosis. Therefore, it is important to emphasize that, although the increase in NPC scores at 7 PM was statistically significant, a 0.7 cm change is not clinically meaningful, especially in the context of acute concussion diagnosis. Instead, our data are highly relevant to the return-to-play decision-making process. As NPC distance trends to baseline over time, clinicians should consider the temporal variability of NPC and exercise a careful interpretation of whether a subtle NPC increase during a patient's recovery course is due to neurotrauma or time-of-day variability. Our data suggest that magnitude of NPC worsening depends on individuals, but participants uniformly increased their NPC distances at nighttime.Table A Previous Reports on the Utility of Near Point of Convergence on Mild Traumatic Brain InjuryAuthorSubjectsStudy DesignKey FindingsMucha et al, 201464 athletes, age 13.9 ± 2.5 yearsCross-sectionalNPC distance was significantly greater in the concussed group compared with the control group (P < .001). Mean difference between groups was 4.0 cm (95% CI: 1.9 to 6.1 cm)Anzalone et al, 2016167 subjects, age 11 to 19 yearsRetrospective chart reviewCI failed to predict delayed concussion recovery (P = 1.07)Capo-Aponte et al, 2017500 U.S. military personnelRetrospective chart reviewNPC receded in blast-induced mTBI patients relative to normative valuesCapo-Aponte et al, 201240 U.S. military personnel (20 with mTBI)Cross-sectionalBlast-induced mTBI significantly receded NPC compared to military control subjects (P = .0003)Cheever et al, 201789 athletes (31 with mTBI), age 17.8 to 25.2 yearsProspective repeated measuresNPC was significantly receded during initial visit in acute (DOI ≤ 10 days prior) and post-acute (DOI ≥ 16 days prior) mTBI athletes, and remained receded in the post-acute group during a 2-week follow-upEllis et al, 2017399 athletes, age males 13.9 years, females 15.4 yearsRetrospective reviewVestibulo-ocular dysfunction (including NPC) was significantly related to development of post-concussion syndromeEllis et al, 2015101 athletes, age 14.2 ± 2.3 yearsRetrospective reviewVestibulo-ocular dysfunction was prevalent in 28.6% and 62.5% of adolescents following sport-related concussion and post-concussion syndrome, respectivelyGallaway et al, 2017218 mTBI patients, age 6 to 72 yearsRetrospective chart reviewCI was the most prevalent (47%) oculomotor deficitHowell et al, 201764 adolescent athletes (33 with mTBI)Cross-sectionalPatients with receded NPC (55%) had significantly slower gait speed and shorter stride lengthMaster et al, 2017432 mTBI patients, age 5 to 18 yearsRetrospective cohortNPC was receded in 35% of patientsPearce et al, 201578 athletes, age 14.31 ± 2.77 yearsCross-sectionalPatients with receded NPC (42%) exhibited significantly worse neurocognitive impairment and reported higher symptom scores versus those with normal NPCStorey et al, 2017275 patients, age 5 to 18 yearsRetrospective cohortAbnormal NPC at initial visit was not correlated to the duration (P = .69, Spearman rho) or use of intervention (P = 1.00, Wilcoxon rank sum) leading to recoveryYorke et al, 2016105 adolescents, age 15.4 yearsCross-sectional descriptiveNPC demonstrated an intraclass correlation of .95 (95% CI: 0.89 to 0.98, P < .001)Kawata et al, 201629 NCAA D1 healthy football athletesProspective observationalSubconcussive head impacts resulted in a significant difference in NPC values between high impact vs low impact players across multiple time pointsKawata et al, 201620 healthy young adults, age controls = 18.9 years, heading = 20.7 yearsRepeated measures10 consecutive soccer headings significantly receded NPC values from baseline (P < .01) and was significantly different from kicking/control subjects (range: P < .01 to P < .001) at both time points post-interventionMcDevitt et al, 201672 active college student athletes (12 with mTBI), age 21.5 ± 3.4 yearsCross-sectionalNPC values were significantly correlated to participant health status (concussed vs non-concussed) (r = 0.337, P = .004)Adler et al, 200751 healthy patients, age 6 to 30 yearsCross-sectionalUse of an accommodative ruler was more effective at detecting receded NPC values versus other methods (eg, pencil tip, fingertip) (P < .001)Zonner et al, 201812 high school football players, age 16.4 ± 0.5 yearsProspective observationalSubconcussive head impacts impaired NPC by 33% up to midseason relative to head impact frequency and magnitudesDuPrey et al, 2017270 athletes, age 14.7 ± 2.0 years (range: 10 to 21 years)Retrospective cohort studyIncreased NPC at initial diagnosis was related to increased risk of prolonged concussion recoveryCI = convergence; DOI = date of injury; mTBI = mild traumatic brain injury; NPC = near point of convergence; CISS = Convergence Insufficiency Symptom SurveyTwo underlying mechanisms may explain our observation. First, as one's wakeful period prolongs, extraocular muscles experience fatigue and then become less sensitive to motor signals from ocular-motor nuclei pertaining to three cranial nerves: oculomotor (III), trochlear (IV), and abducens (VI).17 Various sleep-deprivation studies report that prolonged wakeful periods significantly reduce saccadic amplitude and velocity.18 Second, to focus one's gaze on a predictable moving target (ie, smooth pursuit, NPC), one must facilitate spatial and temporal prediction coupled with attention and anticipation. This connection between peripheral ocular-motor signaling and central neural processing in the brain, referred to as a neuro-ophthalmologic circuitry, can be attenuated due to fatigue from sleep deprivation.19,20 These underlying mechanisms may not translate into our study design with the short wakeful period. On the other hand, our data suggest that NPC is able to detect the subtle ocular-motor perturbation even from mild neural fatigue, which has an immense scientific contribution to sports medicine clinical practice, especially to the return-to-play decision-making process as mentioned.Several key limitations should be noted. The current study did not restrict cognitive activity between 7 AM and 7 PM, and thus it is plausible that cognitive fatigue might have influenced the observed NPC results at 7 PM. However, Cazzoli et al21 suggested that an individual's visual fixation ability was unaffected by cognitive fatigue; therefore, we anticipate the effect of cognitive load on NPC to be minimal. In addition, a cross-sectional study from Yorke et al22 indicated that although NPC assessments yielded a strong agreement between trials (ICC = 0.95, P < .001), a minimum detectable change with 95% confidence (MDC95) was 4 cm.22 This relatively large MDC95 value is partly due to NPC's large between-subject variability.23 Our study employed a pretest/posttest design coupled with various covariates, which enabled us to compare the nighttime NPC levels to an individual's baseline. Therefore, the MDC95 derived from a cross-sectional analysis may not be directly applicable to our findings, and thus caution is needed to contrast with normative studies if researchers employ a repeated measures study design, such as ours.Implications for Clinical PracticeThe data from this study underpin the sensitivity of NPC to neural fatigue from daily conscious activity. 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Email: [email protected]eduFrom the Departments of Kinesiology (SC, ZWB, MF, KK) and Epidemiology and Biostatistics (ZC), School of Public Health, and the Neuroscience Program, College of Arts and Sciences (KK), Indiana University, Bloomington, Indiana.Supported in part by the Indiana Spinal Cord & Brain Injury Research Fund from the Indiana State Department of Health (to Dr. Kawata: ISCBIRF 0019939) and Indiana University School of Public Health Faculty Research Grant Program (to Dr. Kawata: FRGP: 2246237).Ms. Coon and Mr. Bevilacqua contributed equally to this work and should be considered as equal first authors.