Effect of Fatigue on Ocular Motor Assessments
2017; Volume: 9; Issue: 4 Linguagem: Inglês
10.3928/19425864-20170420-03
ISSN1942-5872
AutoresJoshua D. Lindsey, Kelly Cheever, Jamie L. Mansell, Jacqueline Phillips, Ryan Tierney,
Tópico(s)Musculoskeletal pain and rehabilitation
ResumoOriginal Research freeEffect of Fatigue on Ocular Motor Assessments Joshua Lindsey, MS, LAT, ATC, , , MS, LAT, ATC Kelly Cheever, MS, LAT, ATC, , , MS, LAT, ATC Jamie L. Mansell, PhD, LAT, ATC, , , PhD, LAT, ATC Jacqueline Phillips, PhD, ATC, , and , PhD, ATC Ryan T. Tierney, PhD, LAT, ATC, , PhD, LAT, ATC Joshua Lindsey, MS, LAT, ATC , Kelly Cheever, MS, LAT, ATC , Jamie L. Mansell, PhD, LAT, ATC , Jacqueline Phillips, PhD, ATC , and Ryan T. Tierney, PhD, LAT, ATC Athletic Training & Sports Health Care, 2017;9(4):177–183Published Online:April 20, 2017https://doi.org/10.3928/19425864-20170420-03PDFAbstract ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinkedInRedditEmail SectionsMoreAbstractPurpose:To evaluate the effect of exertional fatigue on the scores of two ocular motor tests: the King-Devick (Mayo Clinic, Oakbrook Terrace, IL) and near point of convergence tests.Methods:Twenty physically active individuals participated in two sessions (control and fatigue) via a randomized crossover design. During the control session, outcome measures were assessed before and immediately following 20 minutes of rest. The experimental session outcome measures were assessed before and immediately following a 20-minute previously established physical activity fatigue protocol.Results:Analysis of variance testing indicated no significant group × time interaction effect for near point of convergence (P = .864) and King-Devick (P = .155) testing.Conclusions:The results of this study suggest that fatigue from physical activity does not affect near point of convergence or King-Devick test scores. Therefore, there is a low risk of a false-positive concussion diagnosis due to fatigue during immediate sideline evaluation using these ocular motor assessments.[Athletic Training & Sports Health Care. 2017;9(4):177–183.]IntroductionIt is estimated that up to 65% of patients with concussion present with ocular motor dysfunction.1 Consequently, more robust ocular motor screenings are starting to be incorporated into sideline concussion assessment.2 Current concussion management recommendations include a multifaceted approach to concussion evaluation consisting of a graded signs and symptoms scale, a postural stability test (eg, balance error scoring system [BESS]), and a mental status test such as the Standardized Assessment of Concussion.3,4 During competitive athletic activity, a timely and accurate (ie, high sensitivity and specificity) sideline assessment is necessary to make appropriate return-to-play decisions.5 Ocular motor testing (eg, saccades, convergence)2,3,5 can be an important concussion assessment tool because it can be performed quickly, with some authors reporting significantly high sensitivity and specificity (100% and 94%, respectively).6Eye tracking detects disconjugate eye movements associated with structural traumatic brain injury and concussion.2,3,7,8 Moreover, impaired eye movements in patients with post-concussion syndrome have been reported to indicate suboptimal brain function beyond the influence of depression, malingering, or intellectual ability.9 Saccades are the quick movements of the eyes between fixation points. Decreases in efficiency due to abnormalities in these eye movements can influence a person's timing on the King-Devick test (Mayo Clinic, Oakbrook Terrace, IL). The validity of the King-Devick test in assessing self-paced saccades was recently examined by Asken et al.,10 who found high correlations between both horizontal and vertical saccades.The near point of convergence is the closest distance in which both eyes can focus on a single point without diplopia (double vision) or an eye diverging.11 This function can be easily measured with an accommodative ruler and target for the athlete to observe.Both the King-Devick and near point of convergence tests are emerging as beneficial tools in the concussion assessment battery2,5,12,13 because both exhibit high test–retest reliability (King-Devick: intraclass correlation coefficient [ICC] = 0.97; near point of convergence: ICC = 0.95 to 0.98).12,13 Furthermore, King-Devick scores have been shown to worsen after concussion.5,6,14–19 Similarly, the near point of convergence can significantly recede when compared to normative values in patients with mild traumatic brain injury1,20,21 and in those who have a sport-related concussion.2 However, the King-Devick and near point of convergence tests have not been properly studied under the immediate effects of exertional fatigue to date.In an athletic setting, exertional fatigue is a confounding variable in concussion diagnosis immediately following activity.21–27 Moreover, baseline scores for concussion sideline assessments are taken at rest, but may be artificially changed when comparing scores in a fatigued state. It is well documented that the BESS test is significantly affected by fatigue,21–25 and alterations have been reported for up to 20 minutes following an exercise protocol.28 When Standardized Assessment of Concussion scores in a rested state were compared to a fatigued state, there was no significant difference in mean values. However, there was a large amount of score variability, suggesting that fatigue could possibly affect the scores.27 Specifically, 26 of 56 participants scored between 1 and 6 points below their resting session.27 Although not a readily available sideline tool, the Immediate Post-Concussion Assessment and Cognitive Test (ImPACT; ImPACT Applications, Inc., San Diego, CA) has also been shown to be influenced by fatigue.26 In particular, the verbal memory composite, the first section tested, is significantly affected by fatigue following an exercise protocol.26 Additionally, fatigue may add to the complexity of relying on signs or symptoms because exertion is reported to induce headaches, which are a common symptom reported by patients with concussion.29King-Devick test scores have been investigated after workouts and games with different athletic teams and post-match with mixed martial arts.5,14,18 Researchers reported no evidence that fatigue affected performance, usually finding improvements in scores. However, previous studies neglected to report the approximate amount of time following exercise that each athlete was tested. Additionally, athletes were generally tested in a large group at the same time, making it difficult to administer the King-Devick test while fatigue was still affecting each athlete. Furthermore, little description of the level of fatigue each individual experienced at the time of testing was reported. King et al.6 investigated the effect of a modified repeat high endurance intensity test on scores, but they failed to test every player and the exercise protocol involved less than 2 minutes of sprinting. To date, near point of convergence has yet to be investigated following physical exertion.Normal visual perception requires proper function of the ocular motor systems that control the position and movement of the eye.11 This requires a great deal of coordination and symmetry between the two eyes and coordination involves adjustments in pupil size, lens refraction, and accommodation. Accommodation involves a change in the shape of the lens, diameter of the pupil, and the convergence of the two eyes when directing the image of near objects onto the fovea. The near point of convergence involves the oculomotor nerve innervating the medial rectus muscle that causes adduction of the eyes. Eye movements are also controlled to direct the eyes toward moving targets (saccades), to follow the targets as they move (smooth pursuit), and to move between visual targets at different viewing distances (vergence). Such eye movements are controlled by gaze systems that ensure the image on each eye falls on the same respective location in the binocular field.11The potential effect of fatigue on the individual gaze systems that regulate eye movement in the early stages following exercise is relatively unknown. The dorsolateral prefrontal cortex is a key component in the proper functioning of saccades.30 A decrease in oxygenation at the dorsolateral prefrontal cortex occurs during high intensity exercise that may impair its functioning.31 Perceptions of fatigue also originate from the dorsolateral prefrontal cortex, adding to the workload that may interfere with saccadic movement.32 There has not been research on the effects of fatigue on the pathways of convergence. The presence of exertional fatigue may limit the ability of sideline concussion assessments such as ocular motor tests to provide accurate information in the diagnosis of a sport-related concussion. There is a paucity of well-controlled research examining the acute effect of fatigue on emerging ocular motor sideline tests. Therefore, the purpose of this study was to determine the effect of exertional fatigue on the scores of two ocular motor tests (King-Devick and near point of convergence tests).MethodsResearch DesignA repeated measures crossover design was used. The independent variables were group (fatigue vs control) and time (pretest vs posttest), with repeated measures of both factors. The dependent variables were rate of perceived exertion, heart rate, and King-Devick (seconds; errors) and near point of convergence (cm) scores.ParticipantsTwenty volunteers recruited through flyers participated in the study (Table 1). Participants were given a questionnaire to see whether they met the requirements needed to proceed further in the study. Individuals affirmed that they exercised at least 30 minutes a day for 3 or more days a week and were between the ages of 18 and 30 years. Participants were excluded if they answered "yes" to having any diagnosed concussion within the previous 6 months prior to participation, a history of cardiovascular disease, eye dysfunction (eg, nystagmus), or other ocular motor defects. All participants eligible for the study verbally agreed to Temple University's Institutional Review Board approved consent form.Table 1 Demographics of Participants (N = 20)CharacteristicValueaAge (y)21.95 ± 1.76Sex Male10 Female10Height (cm)172.07 ± 9.05Weight (kg)73.45 ± 13.46aValues are mean ± standard deviation except for sex.Fatigue ProtocolA 20-minute circuit fatigue protocol, previously used by Wilkins et al.21 to induce a high level of exertional fatigue, was used. The protocol consisted of seven stations: 5-minute moderate jog at the participant's self-selected pace, 3 minutes of sprints up and down the length of a basketball court, 2 minutes of push-ups, 2 minutes of sit-ups, 3 minutes of 12-inch step-ups, 3 minutes of sprints, and a 2-minute run during which participants were instructed to maintain the fastest pace possible for the entirety of the run. Researchers gave verbal encouragement throughout the protocol.21Rate of Perceived Exertion and Heart RateRate of perceived exertion was assessed using the Borg 15-point rating scale. The scale is composed of a numbered scale from 6 (no exertion at all) to 20 (maximum exertion) that measures the individual's exertional fatigue. The Borg scale has been reported to be a valid tool in assessing exhaustion regardless of age, gender, and fitness level.33 A target number of 15 was set to indicate a hard level of exertion. We chose this number because a rate of perceived exertion of 15 or greater has been reported to correlate to a maximum volume of oxygen during exercise (VO2) of 75% to 90%.34 Heart rate was measured using a Polar Ft1 wrist unit with a Polar T31-coded chest strap (Polar Electro Inc., Lake Success, NY). The participant's heart rate was reported in beats per minute at the beginning and end of the 20-minute sessions.King-Devick TestThe King-Devick test is a concussion sideline assessment that takes less than 2 minutes to complete. The paper version consists of three cards with single digit numbers on them that help to assess saccades.14 The participant is asked to read each card as quickly as possible without making any errors and the total time taken is recorded as the score. Baselines are administered by performing the test twice without any errors and recording the fastest time in seconds. King et al.17 established a cut-off point at an increase of more than 3 seconds as a positive test, which was found to be sensitive to concussion diagnosis. High test–retest reliability (ICC = 0.97) has been reported.5Near Point of ConvergenceAn ACR/21 accommodation convergence ruler (Astron International, Naples, FL) was used to assess near point of convergence. The ruler has a movable card with rows of single letters ranging from 20/200 to 20/20 in font size. It aids in effectively measuring near point of convergence. During the near point of convergence test, the researcher positions the end of the accommodative ruler above the bridge of the nose. The target (letter Y at 20/80 font) is set 30 cm away and moved toward the face of the participant at a rate of 1 to 2 cm/sec. The target is stopped once the participant verbally signals he or she is experiencing double vision or when the researcher notices an eye diverge. The near point of convergence score was established by averaging the distance in centimeters of three trials. The researcher (JL) within the current study was found to have high intra-rater reliability during pilot testing and training (ICC = 0.90).ProceduresEach participant participated in two sessions that were randomly assigned. At the first session, each participant performed the pretest (baseline) for the King-Devick and near point of convergence tests. The participants were then randomly assigned to either the control or experimental session. The control session involved resting for 20 minutes, whereas the experimental session consisted of performing the 20-minute fatigue protocol. Before and immediately after the 20-minute period, the participants' heart rates were recorded and they were asked to point to the number that best represented their perceived exertional fatigue on the Borg rate of perceived exertion scale. The ocular motor tests were performed immediately (< 1 min) following the 20-minute session, and consisted of one trial of the King-Devick test and an average of two trials of the near point of convergence test. The order of administration alternated to balance the initial effects of fatigue and no order effect was observed. During the second session, participants completed the protocol that they had not previously completed in the first session. The second session was completed at least 48 hours after the first to allow ample time to recover from the fatigue protocol.Data AnalysisData were analyzed using descriptive and inferential statistics. Four 2 (group) × 2 (time) repeated measures analysis of variance tests were used to assess interaction effects between groups over time in rate of perceived exertion, heart rate, and King-Devick and near point of convergence scores. Post hoc t tests were used to evaluate each outcome measure at each time point. SPSS software (version 21.0; IBM Corporation, Somers, NY) was used to assess all statistical analysis. A P value of .05 or less was considered statistically significant.ResultsThe pretest and posttest main outcome measures are presented in Table 2. A significant group × time interaction effect was observed for heart rate (P < .001) and rate of perceived exertion (P < .001). During the experimental condition only, heart rate (180.00 ± 17.37 bpm; 95% confidence interval [CI] = 171.87 to 188.13, P < .001) and rate of perceived exertion (17.15 ± .27; 95% CI = 16.58 to 17.72, P < .001) posttest scores were significantly greater than pretest scores of heart rate (78.35 ± 8.18 bpm; 95% CI = 74.52 to 82.18, P < .001) and rate of perceived exertion (6.10 ± .31; 95% CI = 5.96 to 6.24, P < .001). No significant group × time interaction effect was observed for near point of convergence (P = .864) or King-Devick (P = .155) tests. One false-positive result occurred after the fatigue protocol when a participant completed the King-Devick test more than 3 seconds slower when compared to baseline. The overall near point of convergence average was 5.27 ± 3.70 cm (95% CI = 3.58 to 6.95), and the overall King-Devick test average was 35.82 ± 6.35 seconds (95% CI = 33.46 to 38.18; only one error was recorded).Table 2 Outcome Measures Between Groups Over TimeParameterControl Mean ± SDFatigue Mean ± SDBorg RPE pretest (6 to 20)6.10 ± 0.316.00 ± 0.0Borg RPE posttest (6 to 20)6.10 ± 0.3117.15a± 1.23HR BPM pretest75.15 ± 9.3278.35 ± 8.18HR BPM posttest76.45 ± 8.49180.00a± 17.37KD pretest (sec)36.04 ± 4.9835.99 ± 5.41KD posttest (sec)36.11 ± 5.6435.15 ± 5.89NPC pretest (cm)5.06 ± 3.765.17 ± 3.70NPC posttest (cm)5.33 ± 3.745.52 ± 3.52SD = standard deviation; RPE = rate of perceived exertion; HR = heart rate; BMP = beats per minute; KD = King-Devick test; NPC = near point of convergence testaStatistically significant (P < .05).DiscussionThis study's main finding was that the immediate effects of fatigue as a result of an exercise protocol failed to significantly negatively affect the King-Devick or near point of convergence test scores. This is concurrent with previous studies that examined the effect of fatigue on the King-Devick test after a basketball scrimmage,5 a basketball workout,18 or a short sprinting drill.6 Another finding that is also in agreement with previous research is a mean improvement of 1 second that was noted during the experimental posttest of the King-Devick test. These identified improvements in scores over multiple testing sessions exemplify practice effects.35,36 This improvement was not evident with respect to the near point of convergence test, where scores remained consistent across all testing sessions.Previous research examining the effect of fatigue on King-Devick scores had several limitations. Two studies examining the King-Devick test with collegiate basketball teams before and after a 2-hour scrimmage5 and a 2.5-hour sprint workout18 were performed as a whole team, making testing each individual while under the effects of fatigue difficult. Additionally, there were no data recording the level of fatigue each athlete was experiencing while taking the test. Moreover, details of how the scrimmage or workout was constructed are not available. Another study that used seven 70-meter shuttle runs with 30-second breaks between runs recorded a Borg rating of perceived exertion, resulting in a mean of 16.6 The study involved amateur rugby players whose fitness level was unknown and a fatigue protocol with less than 2 minutes of actual sprinting time.6 All three concluded that the King-Devick test maintains specificity based on lack of performance changes post-exertion.5,6,18 There were no previous studies on the effect of fatigue on the near point of convergence.The results of this study support the use of the King-Devick and near point of convergence tests as a valid concussion sideline assessment for athletes in a fatigued state. The King-Devick test was shown to have a high sensitivity and specificity ranging from 75% and 93%12 to 100% and 94%,6 respectively. Currently, knowledge is limited with respect to comparing the difference from baseline to post-concussion in near point of convergence testing. Previous authors have suggested a cut-off point of more than 5 cm from the tip of the nose indicating a potential concussion.2,13 A near point of convergence increase from a baseline of 3 cm was reported following sub-concussive impacts from controlled soccer heading.37 This increase in near point of convergence following sub-concussive impacts may give some indication of the degree of change expected following a concussive impact.37 In the current study, fatigue did not affect average near point of convergence scores, nor did any participant have an increase greater than 3 cm posttest. The King-Devick and near point of convergence tests are valuable sideline concussion tests due to their reliability in a fatigued state.The sensitivity and specificity of timely sideline concussion assessments has been the subject of a vast body of literature.12–18,38,39 Sensitivity is important in sideline concussion assessment to properly identify athletes suffering from a concussion. However, specificity is also important to make sure athletes are not unnecessarily withheld from play in the absence of a concussion. Although fatigue has a negative impact on the specificity of concussion tests such as the BESS and symptoms scale,23,29 our results suggest that these ocular motor tests are not influenced by fatigue. By using a cut-off point of more than 3 seconds in the current study, no false-positive results occurred in participants and only 1 of 20 fatigued participants tested over the 3-second time threshold. This would give the King-Devick test a specificity of 95% under the conditions of acute fatigue.LimitationsThis study had limitations. Mental fatigue could have influenced the testing and the researchers did not assess the amount of sleep the participants had the night before the sessions. The researchers did not record measurements of fatigue within the exercise protocol to see the amount of exertion participants were experiencing then. There is potential for test administrator error in keeping time and following along with the participants' rapid number naming in the King-Devick test. A longer exercise protocol and a different study population in physical fitness or age may influence the ocular motor system following fatigue. Finally, the testing was under a controlled environment and could not mimic the same experience as actual game play and motivation of athletes to perform well to remain in the game.Implications for Clinical PracticeSideline concussion evaluations are administered to athletes who are tired from playing their respective sport. Findings from this study demonstrate that, in a college-aged physically active population, the King-Devick and near point of convergence tests are unaffected by exertional fatigue and are appropriate tools for assessing concussion under conditions of acute physical activity. Therefore, athletic trainers may perform these ocular motor assessments immediately after a suspected concussive event with low risk of a fatigue-induced false-positive result.1.Capó-Aponte JE, Urosevich TG, Temme LA, Tarbett AK, Sanghera NK. Visual dysfunctions and symptoms during the subacute stage of blast-induced mild traumatic brain injury. Military Medicine. 2012; 177:804–813.10.7205/MILMED-D-12-00061 CrossrefGoogle Scholar2.Mucha A, Collins MW, Elbin RJ, et al.A brief vestibular/ocular motor screening (VOMS) assessment to evaluate concussions: preliminary findings. Am J Sports Med. 2014; 42:2479–2486.10.1177/0363546514543775 CrossrefGoogle Scholar3.Broglio SP, Cantu RC, Gioia GA, et al.National Athletic Trainers' Association position statement: management of sport concussion. J Athl Train. 2014; 49:245–265.10.4085/1062-6050-49.1.07 CrossrefGoogle Scholar4.McCrory P, Meeuwisse W, Aubry M, et al.Consensus statement on concussion in sport: the 4th international conference on concussion in sport held in Zurich, November 2012. Br J Sports Med. 2013; 47:250–258.10.1136/bjsports-2013-092313 CrossrefGoogle Scholar5.Galetta KM, Brandes LE, Maki K, et al.The King–Devick test and sports-related concussion: study of a rapid visual screening tool in a collegiate cohort. J Neurol Sci. 2011; 309:34–39.10.1016/j.jns.2011.07.039 CrossrefGoogle Scholar6.King D, Brughelli M, Hume P, Gissane C. Concussions in amateur rugby union identified with the use of a rapid visual screening tool. J Neurol Sci. 2013; 326:59–63.10.1016/j.jns.2013.01.012 CrossrefGoogle Scholar7.Brahm KD, Wilgenburg HM, Kirby J, Ingalla S, Chang CY, Goodrich GL. Visual impairment and dysfunction in combat-injured service members with traumatic brain injury. Optom Vis Sci. 2009; 86:817–825.10.1097/OPX.0b013e3181adff2d CrossrefGoogle Scholar8.Samadani U, Ritlop R, Reyes M, et al.Eye tracking detects disconjugate eye movements associated with structural traumatic brain injury and concussion. J Neurotrauma. 2015; 32:548–556.10.1089/neu.2014.3687 CrossrefGoogle Scholar9.Heitger MH, Jones RD, Macleod AD, Snell DL, Frampton CM, Anderson TJ. Impaired eye movements in post-concussion syndrome indicate suboptimal brain function beyond the influence of depression, malingering or intellectual ability. Brain. 2009; 132:2850–2870.10.1093/brain/awp181 CrossrefGoogle Scholar10.Asken BM, Mihalik JP, Schmidt JD, Littleton AC, Guskiewicz KM, Hopfinger JB. Visual performance measures and functional implications in healthy participants: a sports concussion perspective. Athletic Training and Sports Health Care. 2016; 8:145–153.10.3928/19425864-20160204-03 LinkGoogle Scholar11.Horn AK, Leigh RJ. The anatomy and physiology of the ocular motor system. Handb Clin Neurol. 2011; 102:21–69.10.1016/B978-0-444-52903-9.00008-X CrossrefGoogle Scholar12.Galetta KM, Morganroth J, Moehringer N, et al.Adding vision to concussion testing: a prospective study of sideline testing in youth and collegiate athletes. J Neuroophthalmol. 2015; 35:235–241.10.1097/WNO.0000000000000226 CrossrefGoogle Scholar13.Pearce KL, Sufrinko A, Lau BC, Henry L, Collins MW, Kontos AP. Near point of convergence after a sport-related concussion: measurement reliability and relationship to neurocognitive impairment and symptoms. Am J Sports Med. 2015; 43:3055–3061.10.1177/0363546515606430 CrossrefGoogle Scholar14.Galetta KM, Barrett J, Allen M, et al.The King-Devick test as a determinant of head trauma and concussion in boxers and MMA fighters. Neurology. 2011; 76:1456–1462.10.1212/WNL.0b013e31821184c9 CrossrefGoogle Scholar15.King D, Clark T, Gissane C. Use of a rapid visual screening tool for the assessment of concussion in amateur rugby league: a pilot study. J Neurol Sci. 2012; 320:16–21.10.1016/j.jns.2012.05.049 CrossrefGoogle Scholar16.King D, Hume P, Gissane C, Clark T. Use of the King-Devick test for sideline concussion screening in junior rugby league. J Neurol Sci. 2015; 357:75–79.10.1016/j.jns.2015.06.069 CrossrefGoogle Scholar17.King D, Gissane C, Hume PA, Flaws M. The King–Devick test was useful in management of concussion in amateur rugby union and rugby league in New Zealand. J Neurol Sci. 2015; 351:58–64.10.1016/j.jns.2015.02.035 CrossrefGoogle Scholar18.Leong DF, Balcer LJ, Galetta SL, Evans G, Gimre M, Watt D. The King-Devick test for sideline concussion screening in collegiate football. J Optometry. 2015; 8:131–139.10.1016/j.optom.2014.12.005 CrossrefGoogle Scholar19.Scheiman M, Gallaway M, Frantz K, et al.Nearpoint of convergence: test procedure, target selection, and normative data. Optom Vis Sci. 2003; 80:214–225.10.1097/00006324-200303000-00011 CrossrefGoogle Scholar20.Szymanowicz D, Ciuffreda KJ, Thiagarajan P, Ludlam DP, Green W, Kapoor N. Vergence in mild traumatic brain injury: a pilot study. J Rehabil Res Dev. 2012; 49:1083–1100.10.1682/JRRD.2010.07.0129 CrossrefGoogle Scholar21.Wilkins JC, Valovich McLeod TC, Perrin DH, Gansneder BM. Performance on the balance error scoring system decreases after fatigue. J Athl Train. 2004: 39:156–161. Google Scholar22.Erkmen N, Taskin H, Kaplan T, Sanioglu A. The effect of fatiguing exercise on balance performance as measured by the balance error scoring system. Isokinetics and Exercise Science. 2009; 17:121–127. Google Scholar23.Fox ZG, Mihalik JP, Blackburn JT, Battaglini CL, Guskiewicz KM. Return of postural control to baseline after anaerobic and aerobic exercise protocols. J Athl Train2008; 43:456–463.10.4085/1062-6050-43.5.456 CrossrefGoogle Scholar24.Schneiders AG, Sullivan SJ, Handcock P, Gray A, McCrory PR. Sports concussions assessment: the effect of exercise on dynamic and static balance. Scand J Med Sci Sports. 2012; 22:85–90.10.1111/j.1600-0838.2010.01141.x CrossrefGoogle Scholar25.Lepers R, Bigard AX, Diard JP, Gouteyron JF, Guezennec Cy. Posture control after prolonged exercise. Eur J Appl Physiol Occup Physiol. 1997; 76:55–61.10.1007/s004210050212 CrossrefGoogle Scholar26.Covassin T, Weiss L, Powell J, Womack C. Effects of a maximal exercise test on neurocognitive function. Br J Sports Med. 2007; 41:370–374.10.1136/bjsm.2006.032334 CrossrefGoogle Scholar27.Koscs M, Kaminski TW, Swanik CB, Edwards DG. Effects of exertional exercise on the standardized assessment of concussion (SAC) score. Athletic Training & Sports Health Care. 2009; 1:24–30.10.3928/19425864-20090101-01 LinkGoogle Scholar28.Susco TM, Valovich McLeod TC, Gansneder BM, Shultz SJ. Balance recovers within 20 minutes after exertion as measured by the balance error scoring system. J Athl Train. 2004; 39:241–246. Google Scholar29.Williams SJ, Nukada H. Sport and exercise headache: II. Diagnosis and classification. Br J Sports Med. 1994; 28:96–100.10.1136/bjsm.28.2.96 CrossrefGoogle Scholar30.Pierrot-Deseilligny C, Müri RM, Ploner CJ, Gaymard B, Demeret S, Rivaud-Pechoux S. Decisional role of the dorsolateral prefrontal cortex in ocular motor behaviour. Brain. 2003; 126:1460–1473.10.1093/brain/awg148 CrossrefGoogle Scholar31.Mekari S, Fraser S, Bosquet L, et al.The relationship between exercise intensity, cerebral oxygenation and cognitive performance in young adults. Eur J Appl Physiol. 2015; 115:2189–2197.10.1007/s00421-015-3199-4 CrossrefGoogle Scholar32.Monroe DC, Gist NH, Freese EC, O'Connor PJ, McCully KK, Dishman RK. Effects of sprint interval cycling on fatigue, energy, and cerebral oxygenation. Med Sci Sports Exerc. 2016; 48:615–624.10.1249/MSS.0000000000000809 CrossrefGoogle Scholar33.Scherr J, Wolfarth B, Christle JW, Pressler A, Wagenpfeil S, Halle M. Associations between borg's rating of perceived exertion and physiological measures of exercise intensity. Eur J Appl Physiol. 2013; 113:147–155.10.1007/s00421-012-2421-x CrossrefGoogle Scholar34.Robertson RJ, Moyna NM, Sward KL, Millich NB, Goss FL, Thompson PD. Gender comparison of RPE at absolute and relative physiological criteria. Med Sci Sports Exerc. 2000; 32:2120–2129.10.1097/00005768-200012000-00024 CrossrefGoogle Scholar35.Dhawan P, Starling A, Tapsell L, et al.King-Devick test identifies symptomatic concussion in real-time and asymptomatic concussion over time. Neurology. 2014; 82:s11.003. Google Scholar36.Silverberg ND, Luoto TM, Öhman J, Iverson GL. Assessment of mild traumatic brain injury with the King-Devick Test in an emergency department sample. Brain Inj. 2014; 28:1590–1593.10.3109/02699052.2014.943287 CrossrefGoogle Scholar37.Kawata K, Tierney R, Phillips J, Jeka JJ. Effect of repetitive sub-concussive head impacts on ocular near point of convergence. Int J Sports Med. 2016; 37:405–410.10.1055/s-0035-1569290 CrossrefGoogle Scholar38.Marinides Z, Galetta KM, Andrews CN, et al.Vision testing is additive to the sideline assessment of sports-related concussion. Neurology: Clinical Practice. 2015; 5:25–34. Google Scholar39.Alsalaheen BA, Haines J, Yorke A, Stockdale K, Broglio SP. Reliability and concurrent validity of instrumented balance error scoring system using a portable force plate system. Phys Sportsmed. 2015; 43:221–226..10.1080/00913847.2015.1040717 CrossrefGoogle Scholar Previous article Next article FiguresReferencesRelatedDetails Request Permissions InformationCopyright 2017, SLACK IncorporatedPDF downloadCorrespondence: Joshua Lindsey, MS, LAT, ATC, Temple University, 1800 N. Broad Street, Philadelphia, PA 19121. E-mail: Joshua.[email protected]eduFrom the Department of Kinesiology, Temple University, Philadelphia, PennsylvaniaThe authors have no financial or proprietary interests in the materials presented herein. Received12/16/16Accepted1/11/17
Referência(s)