ORIGINAL RESEARCH

Evaluation of a Simple Test of Reaction Time for Baseline Concussion Testing in a Population of High School Athletes James MacDonald, MD, MPH,* Julie Wilson, MD,† Julie Young, MA,* Drew Duerson, MD,* Gail Swisher, BS,* Christy L. Collins, MA,‡ and William P. Meehan III, MD§¶

Objective: A common sequela of concussions is impaired reaction time. Computerized neurocognitive tests commonly measure reaction time. A simple clinical test for reaction time has been studied previously in college athletes; whether this test is valid and reliable when assessing younger athletes remains unknown. Our study examines the reliability and validity of this test in a population of high school athletes.

Design: Cross-sectional study. Setting: Two American High Schools. Participants: High school athletes (N = 448) participating in American football or soccer during the academic years 2011 to 2012 and 2012 to 2013.

Interventions: All study participants completed a computerized baseline neurocognitive assessment that included a measure of reaction time (RTcomp), in addition to a clinical measure of reaction time that assessed how far a standard measuring device would fall prior to the athlete catching it (RTclin). Main Outcome Measures: Validity was assessed by determining the correlation between RTclin and RTcomp. Reliability was assessed by measuring the intraclass correlation coefficients (ICCs) between the repeated measures of RTclin and RTcomp taken 1 year apart. Results: In the first year of study, RTclin and RTcomp were positively but weakly correlated (rs = 0.229, P , 0.001). In the second year, there was no significant correlation between RTclin and RTcomp (rs = 0.084, P = 0.084). Both RTclin [ICC = 0.608; 95% confidence Submitted for publication September 9, 2013; accepted December 26, 2013. From the *Department of Pediatrics, Division of Sports Medicine, Nationwide Children’s Hospital, Columbus, Ohio; †Department of Orthopaedics, Children’s Hospital Colorado, Aurora, Colorado; ‡Center for Injury Research Policy, Nationwide Children’s Hospital, Columbus, Ohio; §The Micheli Center for Sports Injury Prevention, Waltham, Massachusetts; and ¶Department of Orthopaedics, Division of Sports Medicine, Boston Children’s Hospital, Boston, Massachusetts. J. MacDonald is supported in this research by an internal grant from the Research Institute of Nationwide Children’s Hospital and an American Medical Society of Sports Medicine (AMSSM) Young Investigator’s Grant. The authors report no conflicts of interest. Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.cjsportmed.com). Corresponding Author: James MacDonald, MD, MPH, Department of Pediatrics, Division of Sports Medicine, Nationwide Children’s Hospital, 5680 Venture Dr, Dublin, OH 43017 (james.macdonald@ nationwidechildrens.org). Copyright © 2014 Wolters Kluwer Health, Inc. All rights reserved

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interval (CI), 0.434-0.728] and RTcomp (ICC = 0.691; 95% CI, 0.554-0.786) had marginal reliability.

Conclusions: In a population of high school athletes, RTclin had poor validity when compared with RTcomp as a standard. Both RTclin and RTcomp had marginal test-retest reliability. Before considering the clinical use of RTclin in the assessment of sport-related concussions sustained by high school athletes, the factors affecting reliability and validity should be investigated further. Clinical Relevance: Reaction time impairment commonly results from concussion and is among the most clinically important measures of the condition. The device evaluated in this study has previously been investigated as a reaction time measure in college athletes. This study investigates the clinical generalizability of the device in a younger population. Video Abstract: A video abstract showing how the RTclin device is used in practice is available as Supplemetal Digital Content 1, http://links.lww.com/JSM/A43. Key Words: computerized neurocognitive testing, traumatic brain injury, reaction time, reliability, validity, youth athletes (Clin J Sport Med 2015;25:43–48)

INTRODUCTION Concussion is the most common form of traumatic brain injury sustained by athletes. According to the 2012 Zurich Consensus Statement on Concussion in Sport, concussion is a functional disturbance of the brain induced by biomechanical forces.1 From 2001 to 2005, there were an estimated 502 000 emergency department (ED) visits for concussions, with about half identified as sport-related concussions.2 Sports are a frequent cause of concussion especially in youth; among individuals aged 15-24 years, sports are second only to motor vehicle accidents as the leading cause of concussions.3 Each year, approximately 30 million children and adolescents participate in sports in the United States,4 a figure that suggests a large number of youth athletes at risk for concussion. Bakhos et al report that between 1997 and 2007, approximately 3 of every 1000 US children of high school age (14-19 years) had an ED visit for concussion sustained from organized team sports, representing a rate of increase .200% over the previous decade. Several domains are affected when a person is concussed. These include a recognized symptom complex, postural alterations, and changes in neurocognitive function, www.cjsportmed.com |

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including reaction time.5 Unfortunately, there can be significant underreporting of concussions, with 1 study demonstrating that fully one-third of athletes have suffered previously undiagnosed concussions,6 and another reporting that only 47.3% of high school football players reported their concussions to a clinician or coach.7 There is significant short-term morbidity associated with concussions and an increasingly recognized potential for long-term morbidity as well. Although there is still controversy over the precise relation of acute concussion and entities such as postconcussion syndrome and chronic traumatic encephalopathy, there is increasing concern regarding the consequences of poorly managed concussions, especially those sustained by youth athletes. Younger age may be a risk factor specifically for postconcussion syndrome.8,9 An important aspect of managing sport-related concussions involves removing the athlete from risk until completely recovered.10 Several instruments have been developed to assess a patient’s cognitive function and postural stability using objective measurable findings, so that clinicians are not forced to rely solely on a patient’s subjective reporting. These instruments include the Standardized Concussion Assessment Tool,11 the Balance Error Scoring System,12 and several proprietary computerized neurocognitive tests. Computerized neurocognitive tests assess a variety of domains affected by concussion, including memory, attention, and reaction time. All the instruments require time to administer and proper training to interpret the results. For some, a substantial investment of money is required. These tools are frequently used in baseline testing of athletes before a sporting season, so that scores measured before injury can be compared with baseline values. The exact role and impact

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of such testing, as well as the ideal time interval between tests, is debated.5 Reaction time impairment commonly results from concussion and is among the most clinically important measures of the condition.13 Changes in reaction time have been found to have prognostic value in managing high school athletes recovering from a concussion.14 Indeed, some studies have shown that measures of reaction time have the strongest prognostic utility of all domains assessed by computerized neurocognitive assessments.15 Individuals who have sustained multiple concussions tend to recover more slowly after suffering a new injury, and this has been correlated with slow recovery of reaction time to baseline.16,17 Reaction times may not recover to baseline levels until after the athlete reports symptom resolution, so measuring reaction times can help a clinician determine whether an athlete who reports symptom resolution is incompletely recovered.18 Finally, from a functional point of view, impaired reaction time may predispose an athlete to further injury.19 A novel clinical test of reaction time using a device similar to one used in high school physics experiments was developed by Eckner et al20 at the University of Michigan. This standardized device is made of an 83-cm long measuring stick coated in high-friction tape, marked in 0.5-cm increments, and embedded in a hockey puck. Materials are easily obtainable, inexpensive, and assembly is straightforward. The device is simple to administer (Figure 1) and used to efficiently obtain a clinical measurement of reaction time (RTclin). The test-retest reliability, validity, and other characteristics of RTclin have been studied previously in adult athletes, principally Division I college football players.20–23 We set out to assess the reliability and validity of RTclin in an adolescent population of high school athletes.

FIGURE 1. Administration of the RTclin measurement. The participants have consented to the publication of this figure.

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Reaction Time in Baseline Concussion Evaluations

FIGURE 2. Inclusion and exclusion of eligible participants.

METHODS

RTclin Protocol

Study Subjects Inclusion criteria were as follows: students participating in American football, boys’ soccer, and girls’ soccer at 2 high schools in central Ohio, whose athletes are cared for by the Division of Sports Medicine at Nationwide Children’s Hospital were enrolled in the study. Athletes who were only able to complete 1 of the measures (RTclin or RTcomp) or who finished the testing session with an invalid AxonSports baseline despite repeated attempts were excluded from statistical analyses.

Assessments Baseline assessments for these athletes included a computerized neurocognitive assessment (AxonSports, Wausau, Wisconsin) and were performed during the summer as per routine practice. Computerized neurocognitive testing was performed collectively in a large public space at the school, typically the school library. The output generated by AxonSports reports test results in several domains, including “processing speed.” Processing speed is derived from an algorithm that incorporates the raw simple reaction time data from all of an athlete’s nonanticipatory trials. RTcomp was defined as the mean reaction time of all nonanticipatory trials, using the same method as Eckner et al20 in the collegiate population.

The RTclin device itself has been described previously. Our study protocol followed that described in the literature.20 In brief, each subject was given an information sheet to read while waiting his/her turn for testing. Each athlete’s dominant hand, gender, date of birth, and sport were recorded. The athlete’s dominant hand was defined as the hand he or she would write with. Participants were seated so that their dominant hand rested on a table. The test administrator instructed the athlete in the method of catching and would drop the device at a random time interval, such that the stick portion of the device would fall between the participant’s thumb and fingers (Figure 1). One unrecorded practice attempt was given followed by 8 data acquisition attempts. The test administrator measured the distance the device fell before being caught using the 0.5-cm incremental markings on the stick. This distance was converted to time by a simple equation qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi ffi RTclin ms ¼ 1000 · ð2 · distance in cmÞ=ð980 cm=s2 Þ, and an average RTclin measure was calculated from the 8 drops completed. Occasionally, the study participant would attempt to catch the stick but, instead, dropped it. Up to 3 such drops were allowed, and no measurements were recorded for analysis on these “dropped” attempts. In the singular instance that 1 study participant dropped the stick 4 times, an additional administration was performed to have a minimum of 5 successful catches used to calculate the average RTclin measure.

TABLE 1. Characteristics of Study Participants Cohort 2011 test subjects 2012 test subjects Subjects enrolled in both years of study

Participants (Male/Female) 222 (168/54) 226 (169/57) 116 (84/32)

Handedness (Right/Left) 199/23 203/23 107/9

Age Mean 6 SD (Range), y

Football Players

Boys’ Soccer

Girls’ Soccer

15.5 6 1.2 (13-18) 15.5 6 1.2 (13-18) 16.1 6 1.0* (14-18)

91 96 37

77 73 47

54 57 32

*Age calculated as of 2012 testing date.

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TABLE 2. RTclin Attempts Dropped Number of Attempts Dropped 2011 participants (N) 2012 participants (N) Total (N)

0

1

2

3

4

Total

173 133 306

43 68 111

6 22 28

0 2 2

0 1 1

222 226 448

The number of attempts dropped recorded for all study participants. There were 447 study participants had 8 data acquisition attempts (1 individual had 9 attempts, as explained in “Methods”). Some individuals “dropped” the RTclin device accidentally, rather than catching it.

Statistical Analysis Validity was assessed by determining the correlation between RTclin and RTcomp. The 2011 and 2012 study cohorts were analyzed separately to determine the correlations for RTclin and RTcomp for each test year. Correlations for any normally distributed data were assessed using the Pearson product-moment correlation coefficient (r); for data that were not normally distributed, Spearman rho (rs) was used. A paired t test was used to compare the mean values of RTclin and RTcomp between the 2 academic years. Cohen’s d was calculated to determine the effect size of the differences from year to year of these 2 measures. Independent samples t tests were used to compare the mean values of RTclin and RTcomp for male and female athletes in 2011 and 2012. One-way analysis of variance testing and independent samples t tests were used to compare the mean values of RTclin and RTcomp among the 3 sports in 2011 and 2012. Measures taken from participants who participated in the study during both academic years were used to assess test-retest reliability by intraclass correlation coefficients (ICCs). IBM SPSS statistics version 19.0 (Chicago, Illinois) was used for all statistical analysis except for calculation of Cohen’s d, for which an online calculator was used.24 Significance was set at a = 0.05.

Ethical Considerations Informed consent (parents and subjects: 18 years of age and older) and assent (subjects ,18 years) were obtained in all cases. Permission for performance of this testing was obtained from administrators at the schools. The study was approved by the Institutional Review Board of Nationwide Children’s Hospital.

RESULTS A total of 493 athletes were eligible for participation in the study, but 45 were excluded for invalid baselines or only completing 1 of the assessments (Figure 2). No student-

athletes opted out of the study at any point by refusing consent/assent. We enrolled 222 athletes in 2011 and 226 in 2012 (total, N = 448), with 116 of the athletes repeating the assessments each year of study (Table 1). The majority of participants were male (75%). A plurality played football, and most were right-hand dominant. Mean age was 15.5 years (SD, 1.2). The number of data acquisition attempts dropped during RTclin administration is reported in Table 2. Mean RTclin was significantly faster than mean RTcomp for all participants in both study years (Table 3). Comparative mean RTclin and RTcomp data for the 2 genders and for the 3 sports tested are reported in Table 4.

Correlation

During the first year of study, RTclin and RTcomp were weakly but significantly correlated (rs = 0.229; P , 0.001) (Figure 3A). During the second year of study, RTclin and RTcomp had no significant correlation (rs = 0.084; P = 0.206) (Figure 3B).

Test-Retest Reliability The 116 study participants included in both sets of data were used to assess test-retest reliability. Between the 2 years of study, there was marginal reliability for both RTcomp [mean: 2011, 313.8 6 48.8 ms vs 2012, 336.1 6 56.1 ms; ICC, 0.691, 95% confidence interval (CI), 0.554-0.786] and RTclin (mean: 2011, 230.0 6 25.7 ms vs 2012, 218.8 6 25.5 ms; ICC, 0.608, 95% CI, 0.434-0.728).

DISCUSSION Reliability and validity are fundamental characteristics that should be established for any clinical measure such as reaction time. Our study assessed the RTclin device in a large group of high school athletes. We found that the RTclin device overall produced different results in our study than have been reported in college-age athletes. We did find, as did Eckner et al, that RTclin produces “faster” measures of reaction time on average than RTcomp. We also found similar measures of

TABLE 3. 2011 and 2012 Measures for Mean RTclin and RTcomp Study Year 2011 2012

RTclin Mean (95% CI)

RTcomp Mean (95% CI)

RTcomp Mean—RTclin Mean (95% CI)

P

230.2 (226.8-233.7) 227.4 (223.9-231.0)

317.2 (310.0-324.5) 340.1 (332.3-347.9)

87.0 (79.5-94.5) 112.6 (104.4-120.9)

,0.0001 ,0.001

For RTclin changes from 2011 to 2012 Cohen’s d = 0.11; for RTcomp changes from 2011 to 2012 Cohen’s d = 0.4.

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TABLE 4. Mean RTclin and RTcomp for Various Subgroups Studied, Compared by Gender and by Sport Gender Male Female Sport Football Boys’ Soccer Girls’ Soccer

Mean RTclin 2011

Mean RTclin 2012

Mean RTcomp 2011

Mean RTcomp 2012

225.7 6 24.5 244.3 6 25.2*

224.6 6 26.1 235.7 6 28.1†

316.1 6 52.2 320.9 6 62.7

340.2 6 60.4 339.8 6 56.7

226.7 6 27.3 224.6 6 20.8 244.3 6 25.2‡

228.5 6 25.3 219.5 6 26.3 235.7 6 28.1

317.1 6 50.3 314.9 6 54.7 320.9 6 62.7

336.1 6 60.8 345.5 6 59.9 339.8 6 56.7

Reaction time is represented in milliseconds. Gender subgroups were compared with each other. Sports subgroups were compared with each other. Significant differences are labeled. *Slower than male athletes in 2011; P , 0.001. †Slower than male athletes in 2012; P = 0.007. ‡Slower than football and boys’ soccer players in 2011; P , 0.001.

reliability: the ICC for between-seasons test-retest reliability in the Eckner study was 0.645 for RTclin and 0.512 for RTcomp, whereas our group found for the high school athletes the ICCs to be 0.608 for RTclin and 0.691 for RTcomp. Testretest ICCs at or greater than 0.90 are ideal and preferable for clinical decision making, whereas measures of 0.60-0.69 are considered “marginal” and 0.59 or lower are considered “low.”25 We studied a gender- and sport-diverse population. For the subgroup pairings, there were mostly no statistically significant differences in mean RTclin or RTcomp. The exceptions were the female soccer players, who had significantly slower baseline RTclin than their male peers in some of the subgroup analyses. Gender differences have been found previously on baseline neuropsychological testing26 and should be investigated in more depth in future studies of the RTclin device. We found minimal correlation between RTclin and RTcomp. This result differs from the study by Eckner et al,20 which assessed collegiate athletes and found that RTclin and RTcomp were significantly and more strongly correlated (r =

0.445). This discrepancy of findings may reflect the differences in the age of study participants, suggesting that correlation between RTclin and RTcomp may be poor for high school–aged athletes when compared with collegiate athletes. Furthermore, as with many high school athletes, our participants were tested as a group, in 1 large room, such as a high school library. Such environments may affect RTclin and RTcomp differently. RTclin may be intrinsically motivating, with student-athletes getting immediate feedback on performance and with other athletes able to observe their performance.27 Participants may be incentivized to “compete” or best their colleague’s performance. RTcomp testing may be more sensitive to the distractions in such a setting,28 and there is no immediate feedback on performance and no “shared experience” resulting in competition between athletes. Indeed, these characteristics may explain why mean RTclin measures in our study were faster than RTcomp and showed less variability from season to season. Our results should be considered in light of several limitations. Some of the athletes presented for baseline testing

FIGURE 3. Scatterplots demonstrating correlation between RTclin and RTcomp for each study year. Copyright  2014 Wolters Kluwer Health, Inc. All rights reserved.

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before a workout, and some would present after a workout. Some studies in the literature have found a differential effect of exercise on reaction time,29,30 although a recent study by Reddy et al31 showed that RTclin itself was not affected by recent exercise. In addition, there were some student-athletes in both years who were not baseline tested simply because they did not show up on test day. This may have introduced some selection bias. The test and retest administration were 1 year apart. Observed changes in RTclin may reflect maturation and development in this adolescent-aged population as opposed to test characteristics of RTclin. If so, our findings would suggest that repeat RTclin assessments should be performed throughout adolescence, if they are considered for clinical use in this age group. Finally, there was a preponderance of male athletes (75%) in our study. Future studies should include more female athletes to verify the generalizability of these findings in that subgroup.

CONCLUSIONS With increasing public awareness regarding the potential sequelae of sport-related concussions, better screening for identifying and managing concussions sustained by high school and youth athletes is desirable. Screening often necessitates further investments in time, manpower, and money, all of which are in tight supply in many jurisdictions and school districts. An inexpensive device such as RTclin would be welcomed, if proven reliable and valid. Based on our results, further validation of RTclin as a measure of reaction time for adolescent athletes is warranted before incorporating it into clinical practice. ACKNOWLEDGMENTS The authors would like to acknowledge the generous assistance provided by J. T. Eckner (University of Michigan), Jason Cromer (AxonSports), and Tina Lepley, Leslie McCann, and Susi Miller (Nationwide Children’s Hospital). REFERENCES 1. 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. Clin J Sport Med. 2013;23:89–117. 2. Bakhos LL, Lockhart GR, Myers R, et al. Emergency department visits for concussion in young child athletes. Pediatrics. 2010;126:e550–e556. 3. Marar M, McIlvain N, Fields S, et al. Epidemiology of concussions among United States high school athletes in 20 sports. Am J Sports Med. 2012;40:747–755. 4. Cassas KJ, Cassettari-Wayhs A. Childhood and adolescent sports-related overuse injuries. Am Fam Physician. 2006;73:1014–1022. 5. Harmon KG, Drezner J, Gammons M, et al. American Medical Society for Sports Medicine position statement: concussion in sport. Clin J Sport Med. 2013;23:1–18. 6. Meehan WP, Mannix RC, O’Brien MJ, et al. The prevalence of undiagnosed concussions in athletes. Clin J Sport Med. 2013;23:339–342. 7. McCrea M, Hammeke T, Olsen G, et al. Unreported concussion in high school football players: implications for prevention. Clin J Sport Med. 2004;14:13–17.

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Evaluation of a simple test of reaction time for baseline concussion testing in a population of high school athletes.

A common sequela of concussions is impaired reaction time. Computerized neurocognitive tests commonly measure reaction time. A simple clinical test fo...
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