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Oculomotor Function in Collegiate Student–Athletes With a Previous History of Sport-Related Concussion

2013; Volume: 5; Issue: 6 Linguagem: Inglês

10.3928/19425864-20131108-01

1942-5872

Peter A. Braun, Thomas W. Kaminski, C. Buz Swanik, Christopher A. Knight,

Vestibular and auditory disorders

Original Research freeOculomotor Function in Collegiate Student–Athletes With a Previous History of Sport-Related Concussion Peter A. Braun, MS, ATC, LAT, , , MS, ATC, LAT Thomas W. Kaminski, PhD, ATC, FNATA, FACSM, , , PhD, ATC, FNATA, FACSM Charles B. Swanik, PhD, ATC, FNATA, , and , PhD, ATC, FNATA Christopher A. Knight, PhD, , PhD Peter A. Braun, MS, ATC, LAT , Thomas W. Kaminski, PhD, ATC, FNATA, FACSM , Charles B. Swanik, PhD, ATC, FNATA , and Christopher A. Knight, PhD Published Online:November 08, 2013https://doi.org/10.3928/19425864-20131108-01Cited by:1PDFAbstract ToolsAdd to favoritesDownload CitationsTrack CitationsCopy LTI LinkHTMLAbstractPDF ShareShare onFacebookTwitterLinkedInRedditEmail SectionsMoreAbstractThis study aimed to determine whether sport-related concussion creates lasting deficits in oculomotor function and learning, as measured by the King-Devick (K-D) Test. One hundred seventy collegiate student–athletes participated. Concussion history determined group delineation. Objective measurements were obtained through the K-D Test. Total time (seconds) to complete the K-D Test and the improvement time (seconds) between trials was compared using separate analysis of variance. No significant differences existed between groups for oculomotor function (F1,168 = 0.870, P = .352) or improvement time (F1,166 = 0.253, P = .615). Results suggest that no long-term deficits in oculomotor function or learning exist in this collegiate student–athlete population with previous concussion. Additional research of athletes with acute concussion along a continuum of recovery is warranted. Due to the essentiality of oculomotor function in physical and cognitive tasks, the absence of long-term deficits supports current recommended guidelines regarding concussion assessment and management. [Athletic Training & Sports Health Care. 2013;5(6):282–288.]IntroductionOver the past few years, clinicians and researchers have developed an increasing interest in the field of concussion assessment and management. This attention has improved the knowledge regarding the physiological effects, as well as the proper evaluation and recovery protocol, associated with brain injury. Results from recent research have changed medical practices in all areas of athletics. The National Football League altered previous guidelines for concussion management by expanding the list of symptoms that could prohibit an athlete from returning to play. Similar adjustments, such as improving and mandating certain protective equipment, have been made in field hockey and lacrosse to ensure player safety. Even with these heightened precautions, incidence rates of concussion have increased considerably, classifying concussion as an epidemic.1 Approximately 1.6 to 3.8 million sport-related concussions occur annually in the United States, with an estimated $60 billion associated with the direct and indirect costs of emergency room visits.2 The highest risk of concussion exists in contact team sports, such as ice hockey, rugby, and American football, and individual sports, such as boxing, taekwondo, and karate.3 Furthermore, many athletes experience concussions that go undiagnosed or their injuries fail to be properly assessed by medical providers who categorize concussive blows as "dings." This misinterpretation could result in further injury, irreversible damage, and even death.4Concussion is defined as a complex pathophysiological process affecting the brain, induced by traumatic biomechanical forces that result in transient neurologic signs or symptoms and reflect a functional disturbance of the brain, rather than a structural injury.4 The most common mechanism for sport-related concussion is head-to-head contact with another individual.5 This causes linear, rotational, or angular movement of the brain inside the cerebral cavity, forcing the brain to strike the cranial wall. This impact leads to tissue damage of the brain and brain stem, thus creating a variety of neurological symptoms. These symptoms are often indicators of the extent of the injury and the recommended management process.4Controversy currently exists among medical providers regarding the most reliable, practical, and effective tool for clinically diagnosing and assessing sport-related concussion. In 2004, the National Athletic Trainers' Association released a position statement regarding the management of sport-related concussions in an attempt to increase the consistency of care given to athletes experiencing such injuries.6 One of these recommendations includes the use of a variety of instruments and apparatuses to comprehensively evaluate the concussed athlete, including clinical examination, symptoms checklists, the Standardized Assessment of Concussion, the Balance Error Scoring System, and computerized neuropsychological testing.6 Despite the utility of these tools, only a detailed clinical evaluation, which assesses cranial nerve function and visual tracking ability, may identify the considerable deficits in oculomotor function that are often affected by brain trauma.7 Mechanisms, such as linear, rotational, and angular forces, associated with concussion cause trauma not only to the brain but also to the cranial nerves, which control eye movement. More precise and objective measurements of oculomotor function are seldom included in head injury evaluations, and many clinicians are reluctant to test this skill because, until recently, there was no way to practically evaluate it. A comprehensive evaluation of head injury needs to include a component that can detect subtle deficits in eye movement. Although no research has explicitly shown that oculomotor deficits can exist in the absence of all other symptoms, a detailed and thorough assessment is necessary to ensure that the proper care and management strategies may be implemented in each individual case.To improve current protocol, clinicians must first recognize that these deficits may be present in a concussed population. Sparse literature exists on the objective measurement of oculomotor function; however, recent research has shown promising results. Researchers in optometry have recorded eye movement deficits in study participants with a history of acquired brain injury due to stroke.8 However, these results do not necessarily extrapolate to the collegiate athletic population, nor do they include mild traumatic brain injuries, such as sport-related concussion. The most revealing data on oculomotor function in concussed athletes may be seen in recent studies that utilize a new concussion screening tool known as the King-Devick (K-D) Test.9,10 This test challenges individuals to read a series of numbers as quickly as possible without making errors. Proper execution requires the individual to perform quick, controlled movements of the eye, known as saccades. Examining saccadic eye movement reveals motor control and conduction velocity of several cranial nerves, including II, III, IV, and VI. These nerves originate in the diencephalon and midbrain, which has been shown to be the most affected portion of the central nervous system during rotational forces that are associated with concussion.11 Currently, 2 studies exist that implement the K-D Test on concussed athletes.9,10 Results reveal that concussion causes acute deficits in oculomotor function when comparing preinjury to postinjury scores within participants.9 However, these deficits have not been examined at various times after injury to rule out the possible long-term oculomotor deficits related to concussion.The method of this current study requires student–athletes to complete the K-D Test twice, examining each participant's ability to improve performance between trials. This protocol allows researchers to observe a learning effect, which will provide insight into the possible long-term effects that concussion has on learning. Generally, the ability of an individual to learn a task is the result of chemical and anatomical modifications to the neurons and neural synapses in the brain.12 These changes create a more efficient and effective neural pathway, allowing the same individual to complete the same demand more quickly.Therefore, the purpose of the current study was to determine whether sport-related concussion creates lasting deficits in oculomotor function and learning. We hypothesized that a previous history of concussion will hinder oculomotor function and result in higher overall test times and suppress the learning effect, revealing lower improvement times from trial 1 to trial 2.MethodOculomotor function was evaluated in 170 collegiate student–athletes. All participants were selected from a single, Delaware-based university and ranged in age from 18 to 24 years. Seventy-three participants had a previous history of sport-related concussion (experimental group). Concussion history was determined based on a self-reported, formal diagnosis from an appropriate medical provider (ie, MD or DO). No other inclusion criteria were necessary. The control group included 97 individuals with no prior history of head injury. Both groups were closely related in mean age, sex, height, and mass (Table 1). The researchers excluded potential participants from the study if a prior diagnosis of oculomotor dysfunction or reading disability was reported. All participants signed institutionally approved documents of informed consent.Table 1 Demographics of Study ParticipantsDEMOGRAPHICCONTROL GROUPEXPERIMENTAL GROUPParticipants9773Mean (SD) age (y)19.7 (1.3)19.7 (1.3)Sex (M/F)45/5240/33Mean (SD) height (cm)175.6 (10.2)177.4 (10.6)Mean (SD) mass (kg)77.1 (16.3)79.0 (17.2)Mean (SD) concussionsN/A1.5 (1.3)Mean (SD) time since most recent concussion (mo)N/A28.7 (28.0)Mean (SD) recovery time (d)N/A8.6 (12.9)Abbreviation: N/A, not applicable.The K-D Test was used to assess oculomotor function (Figure 1). This test required the participant to rapidly name numbers out loud from an index card. Three test cards were included; the test from each card was timed using a stop watch, and the total completion time for all 3 cards was the measured variable.Figure 1. The King-Devick Test. The upper left portion of the figure displays the demonstration card. This card does not serve as practice but to help the participant visualize the task. The upper right, lower left, and lower right cards are used for testing. Each card has a different format but the objective remains to read the numbers aloud as quickly as possible without making a mistake. Reprinted with permission from Wolters Kluwer Health.9The study protocol involved a quasi-experimental, ex post facto design. Testing took place in a laboratory environment, which provided a quiet area that was free from distractions. All participants were first asked to complete a questionnaire that had questions pertaining to general medical information and specific details regarding prior concussive incident(s). If the participant was part of the control group (no previous history of concussion), that portion of the questionnaire was left blank. This allowed researchers to collect a variety of data pertaining to factors that may affect oculomotor function, including the number of concussions experienced, as well as their severity, and time since injury. After the questionnaire was completed, participants were briefed on the K-D Test, using a set of standardized instructions.The K-D Test was introduced to the participants, and instructions were given using the demonstration card as a visual example. The researcher ensured that the test card was held at a comfortable reading distance. Participants were able to use reading glasses or contacts if necessary. The researcher explained the directions of the K-D Test, making certain to iterate to the participants that they could not use their hands or fingers to assist themselves in reading. The test required the participant to read aloud a series of numbers from an index card from left to right, as quickly as possible without making any errors. The participant read the numbers on each of the 3 test cards while being timed. Recorded times were documented only if the participant read the entire card without making a mistake. If an error was made, the participant was stopped and the card was repeated from the beginning. The time it took to complete each card and the number of errors made was recorded, and the entire test was repeated. After the third and final test card of the second trial was completed, the participant was free to leave the testing area. Total testing time was approximately 10 minutes.A pilot subgroup analysis was also undertaken in this study. Five participants completed the K-D Test 5 times, with minimal rest between trials. The purpose of this experiment was to examine the learning effect across multiple trials to determine when the greatest improvements in test time were seen. From this pilot study, it was determined that 2 test trials would be sufficient to document the maximal learning effect if present (Figure 2). This supports current research involving the K-D Test, which recommends 2 trials to establish an appropriate baseline score for each athlete.9,10Figure 2. Pilot test data of subgroup learning effect. Trial 1 represents the change in mean King-Devick Test completion time from trial 1 to trial 2. Trial 2 represents the change from trial 2 to trial 3 and so on. The greatest improvement in time completed was between trials 1 and 2.The independent variable evaluated in this study was the participant's history of concussion. This separated the participants into 2 groups—the control group, which had no history of concussion, and the experimental group, which had a previous history of concussion. Two dependent variables were examined. The main variable was the total time (seconds) to complete the K-D Test, and the secondary dependent variable is the improvement time (seconds) from trial 1 to trial 2, which was used to examine the learning effect, if any, present. Improvement time was recorded in positive and negative values. If the participant completed the K-D Test more quickly on the second trial, then the improvement time was positive; conversely, if the participant's second trial took longer, then the improvement time was negative. All data were analyzed with an alpha level set a priori at P < .05. Separate, between-participant, one-way analysis of variances were used to compare the means between the 2 groups for both total time and improvement time. Scores were removed from analysis if they were deemed as outliers. This was determined by first standardizing all outcome measurements into z scores and then removing any scores higher than 3.29. Eliminating scores above 3.29 removed all values that fell in the outer 0.1% of the data set. Only 2 improvement time scores in the control group were labeled as outliers and were removed from analysis. All other z scores were lower than 3.29.ResultsAll participant demographics (n = 170) are shown in Table 1. Individuals in the experimental group displayed a mean of 1.5 concussions sustained during their lifespan, with more than a 2-year time period since their most recent concussion. Mean recovery time from concussion was approximately 9 days.The times to complete the K-D Test ranged from 25.69 to 55.68 seconds in the control group and 25.77 to 55.01 seconds in the experimental group (Table 2). Median test times of the control and experimental groups were 37.73 and 38.29 seconds, respectively (Table 2). The mean total test time of the control group was 38.21 ± 6.17 seconds, which was slightly lower than the experimental group, which was 39.12 ± 6.48 seconds. The analysis of variance of total test time resulted in no significant difference (F1,168 = 0.870, P = .352) between groups. Results of improvement time ranged from −4.93 to 12.04 seconds in the control group, compared with −1.24 to 9.12 seconds in the experimental group (Table 2). Mean improvement time in the control group (2.48 ± 2.87 seconds) revealed no significant difference (F1,166 = 0.253, P = .615) compared with the experimental group (2.68 ± 2.12 seconds).Table 2 Descriptive Statistics of Total Test Time and Improvement Time Between GroupsTEST TIME BY GROUPRANGE (s)MEAN ± SD (s)MEDIAN (s)95% CIControl group Total test time25.69 to 55.6838.21 ± 6.1737.7336.97–39.45 Improvement time−4.93 to 12.042.48 ± 2.872.431.90–3.07Experimental group Total test time25.77 to 55.0139.12 ± 6.4838.2937.6–40.63 Improvement time−1.24 to 9.122.68 ± 2.122.532.19–3.18Abbreviation: Cl, confidence interval.DiscussionResults indicate that there are no significant deficits in oculomotor function in the collegiate athlete population with a previous history of concussion, as examined by the K-D Test. Certain commonly used tools, such as the Immediate Post-Concussion Assessment and Cognitive Test or the Standardized Assessment of Concussion test, have been utilized to measure cognitive function at a variety of time points after injury. Much of this research suggests that brain function is typically restored within a few days after the initial event and that the athlete may begin return-to-play protocol when full function is achieved.13–15 These tools contain aspects that analyze numerous functional properties of the brain; however, there is little emphasis on movement of the eye. The assumption that motor function of the eye improves in relation with other skills, such as balance, memory, coordination, or concentration, has been commonplace in clinical practice. Although oculomotor deficits did not exist with respect to the control group, more research is needed to determine when full function of the eye is restored after sustaining a head injury.Another assessment of neurologic ability that often goes untested with regard to concussion is learning effect. During a head injury, neurons in the brain undergo physical, chemical, and metabolic changes.12 These changes affect the functional integrity of the involved neurons and manifest as symptoms.16 Brain plasticity, or the ability to learn, is very difficult to recognize without proper testing. By examining learning effect, researchers can gain a glimpse into the brain's ability to recognize the demand of a task and then it uses an efficient and effective means to accomplish that task. Learning has been a topic that is often investigated with variables such as sleep, mental disorders, teaching styles, and other scientific fields, but it has rarely been associated with concussion.17–19 Although conclusions cannot yet be made, initial results indicate that college-aged student–athletes retain normal neuroplasticity after recovery from concussion.Limitations exist in the design of our study. A retrospective methodology does not allow for standardization of the diagnostic criteria for concussion. Different examiners, assessment tools, and knowledge on the topic introduce uncertainty regarding the accuracy of the diagnosis. Future studies need to implement a prospective design to eliminate controllable factors that could affect group placement. Second, the K-D Test is intended to be used as a within-participant tool, which compares postinjury scores with baseline scores. The recommended methodology eliminates the wide variability of the results and produces more comparable values. However, in this study, the K-D Test was used to compare scores among participants, which produced inconsistent results and substantially reduced the ability to detect an effect. If a difference did exist between groups, a substantial number of participants would need to be recruited to create a significant and powerful study with a large effect size. Also, the sex distribution differences between groups could contribute to inaccurate data. Men and women exhibit differing anatomical and functional characteristics of the brain.20 Men exhibit cortical networks that are less economical than women,21 inferring that women display a larger overall connectivity of neurons in the brain. Women have also been shown to have a larger corpus callosum, which functions as the bridge between the left and right hemispheres of the brain.20 However, conclusions cannot yet be made regarding whether these differences affect K-D Test times; however, a distinction between the cognitive function of men and women must be noted.The number of errors during testing was another variable recorded by the researchers in this experiment. Poststudy analysis revealed trending data, which indicated that student–athletes with a previous history of multiple concussions (2 or more) generated more errors during testing than those student–athletes with less than 2 past concussions. These results produce an interesting topic for future research, which could impact current knowledge and practice concerning multiple concussion management and return-to-play guidelines. In addition to the number of errors committed by each individual, other information, such as number of concussions, time since last concussion, and mean concussion recovery time, were also documented to determine whether these variables affected K-D Test scores. During data collection, it became apparent that the participants were providing arbitrary answers to these questions; therefore, the detailed information necessary to statistically analyze these variables was inadequate. The researchers decided to continue collecting the information for demographic purposes but agreed against using it for statistical analysis.ConclusionThe K-D Test is a screening tool for concussion that is quick, easy, and accurate. Further research involving this test should include variables such as sex, age, and, as discussed previously, errors committed during testing. Clinicians should recognize the usefulness of the K-D Test and consider incorporating it into concussion assessment protocols. Even without the application of this tool, more focus should be placed on areas of cognitive function, such as oculomotor function and learning, so that head injury examinations can be more comprehensive and athletes can receive the highest quality of care.Implications for Clinical PracticeResults from this study strengthen current management practices for concussion. The basis for returning an athlete to play is largely dependent on the individual's symptoms. The 2 variables examined in this study—oculomotor function, as measured by total time to complete the K-D Test, and learning effect, as represented by improvement time—expand the possible objective components that may be used to monitor concussion recovery. 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J Neurosci. 2009; 29(50):15684–15693.10.1523/JNEUROSCI.2308-09.2009 Crossref, Google Scholar Previous article FiguresReferencesRelatedDetailsCited byHeick J, Bay C, Dompier T and Valovich McLeod T (2016) The Psychometric Properties of the King–Devick Test and the Influence of Age and Sex in Healthy Individuals Aged 14 to 24 Years, Athletic Training & Sports Health Care, 8:5, (222-229), Online publication date: 1-Sep-2016. Request Permissions InformationCopyright 2013, SLACK IncorporatedPDF downloadAddress correspondence to Peter A. Braun, MS, ATC, LAT, ATI Physical Therapy, 73 Old Dublin Pike, Suite 6, Doylestown, PA 18902; e-mail: [email protected]com.The authors are from the Department of Kinesiology & Applied Physiology, University of Delaware, Newark, Delaware.Dr Kaminski was not involved in the peer review or decision-making process for this manuscript.The authors have no financial or proprietary interest in the materials presented herein.