Evaluation of the Zurich Guidelines and Exercise Testing for Return to Play in Adolescents Following Concussion

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1 ORIGINAL RESEARCH Evaluation of the Zurich Guidelines and Exercise Testing for Return to Play in Adolescents Following Concussion Scott R. Darling, MD,* John J. Leddy, MD,* John G. Baker, PhD,* Amy J. Williams, MA, Anthony Surace, MEd,* Jeffrey C. Miecznikowski, PhD, and Barry Willer, PhD Objective: To evaluate return to play (RTP) and return to classroom outcomes when the Zurich guidelines are combined with a standardized exercise treadmill test [Buffalo Concussion Treadmill Test (BCTT)] and computerized neuropsychological (cnp) testing in adolescent athletes after concussion. Design: Retrospective chart review and follow-up. Setting: University Sports Medicine Concussion Clinic. Participants: One hundred seventeen athletes (75% male) with sport concussion ages 13 to 19 years and telephone follow-up of 91 (77.8%) athletes and their parents. Interventions: Concussed athletes who were asymptomatic at rest completed Automated Neuropsychological Assessment Metrics or Immediate Post-concussion Assessment and Cognitive Test cnp testing followed by the BCTT on the same day. Athletes then followed the Zurich consensus guidelines for RTP. Main Outcome Measures: The primary outcome measure was the degree of success in RTP, that is, RTP with or without return of concussive symptoms. Secondary outcome measure was return to school with or without symptoms. Results: All athletes returned to sport without exacerbation of symptoms. Telephone follow-up revealed that 38.5% experienced new issues upon return to the classroom. Forty-eight percent of athletes had 1 or more cnp subtests below average (,ninth percentile) when asymptomatic. Ultimately, performance on cnp was not predictive of return to school issues. Conclusions: The BCTT in combination with the Zurich consensus guidelines seems to be safe and successful for RTP. There is evidence to suggest that cnp testing performed in athletes who do not have a preinjury baseline test was not related to RTP or problems upon return to school. Submitted for publication October 22, 2012; accepted September 10, From the *Departments of Orthopaedics; Nuclear Medicine; Biostatistics; and Psychiatry, University at Buffalo, Buffalo, New York. The authors wish to thank the following organizations for financial support of the project described in this article: The Robert Rich Family Foundation, Program for Understanding Childhood Concussion and Stroke, Buffalo Bills (Ralph Wilson) Team Physician Fund and the Buffalo Sabres Foundation. The authors report no conflicts of interest. Corresponding Author: Scott R. Darling, MD, Department of Orthopaedics and Sports Medicine, University at Buffalo, 160 Farber Hall, Buffalo, NY Copyright 2013 by Lippincott Williams & Wilkins Key Words: concussion, computerized neuropsychological testing, return to play, return to sport, exercise, treadmill (Clin J Sport Med 2014;24: ) INTRODUCTION Athletes in the United States sustain 1.6 to 3.8 million sport-related concussions yearly. 1 The return to play (RTP) decision is challenging for clinicians because symptom reports are complicated by their subjective nature and poor specificity. Establishing asymptomatic at-rest status may also be difficult given the prevalence of daily symptoms reported by healthy people. 2 Several testing methods have been developed to try to quantify the degree of concussion injury, with computerized neuropsychological (cnp) testing gaining the most attention. 3,4 Automated Neuropsychological Assessment Metrics () and the Immediate Post-concussion Assessment and Cognitive Test () cnp batteries are among the most widely used programs. 5,6 Test interpretation may be enhanced if baseline testing has been performed. 7 For many organizations, however, cnp testing is either unavailable or limited by a lack of staff to reliably administer and interpret test results. 8 Computerized neuropsychological testing has been shown to be affected by age, 9 sex, 10 symptoms, 11 and concussion history. 12 The RTP decision becomes even more challenging when symptom reports and cnp test performance do not coincide. 13 Furthermore, despite its growing popularity, the reliability and utility of cnp testing for concussion assessment has been questioned. 8,14,15 The Zurich Consensus Conference Concussion Guidelines recommend physical and cognitive rest for recovery from concussion in the early stages and provide clinicians with a structured RTP plan that is widely used but has never been evaluated for outcome. 16 The guidelines state that cnp testing can be useful but that RTP decisions should not be based solely on cnp test results. The guidelines also imply that athletes should not RTP until they have demonstrated the ability to perform to the maximum level of their sport without recurrent symptoms. Additionally, they specifically ask whether provocative exercise testing is useful in the RTP decision. A standardized exercise treadmill test [the Buffalo Concussion Treadmill Test (BCTT)] has been shown to be safe and reliable for the evaluation of concussion in athletes with persistent symptoms. 17 Furthermore, using the BCTT, exercise below symptom threshold is safe and effective in returning these athletes to sport. 18, Clin J Sport Med Volume 24, Number 2, March 2014

2 Clin J Sport Med Volume 24, Number 2, March 2014 Evaluation of Zurich Guidelines It is not known whether the ability to exercise to exhaustion without symptom provocation is a valid method to determine readiness to RTP. Therefore, the primary purpose of this study was to evaluate the outcome of RTP decisions for adolescents when based on a combination of the BCTT and the Zurich guidelines. We hypothesized that athletes who pass the BCTT will have little or no difficulty with symptom exacerbation when they RTP. A second purpose of the study was to quantify if any impairment existed on cnp test performance once athletes were deemed asymptomatic, and, if so, did this impairment predict problems in return to school or sport. There is growing concern for the problems children and adolescents have with return to school following a concussion. 20,21 We hypothesized that poor performance on cnp tests would relate to symptoms and/or complications upon return to school in adolescents after concussion. Ethical Considerations All participants were patients of the University at Buffalo Sports Medicine Concussion Management Clinic. Retrospective review of medical records does not require consent. However, verbal consent (and assent in the case of those under the age of 18 years) was obtained from all who participated in the telephone follow-up. Confidentiality of all participants was respected and maintained. Research ethics approval was granted through the University at Buffalo Institutional Review Board. METHODS Study Participants To be included in the study, subjects had to be adolescent athletes (aged years) who sustained a concussion during a sporting event as observed by a team trainer and as assessed by a sports medicine physician experienced in concussion management. All athletes seen at 1 concussion clinic during a 3-year period ( ) were included as long as there were at least 2 months from the time of RTP to follow-up. Table 1 provides additional information on the athletes in the study. A structured telephone follow-up of the athletes (and a parent in instances where the athlete was still a minor) was performed asking whether the athlete had any problems with RTP or return to school. If an athlete (or their parent) indicated there was a problem with return to school, we asked whether the problem existed before the concussion, and, if so, we asked if the problem was worse after the concussion. We successfully interviewed 91 of the 117 subjects (77.8%). The number of males in the total sample was 88 (75.2%) and the number of males in the follow-up sample was 70 (76.9%). The median age of the total sample was 15 years and the median age of the follow-up sample was 15 years. Assessment and Instruments The initial clinic assessment included cnp testing and the Sport Concussion Assessment Tool-2 (SCAT-2), which provides a symptom checklist and balance testing. Athletes did not have a preinjury baseline cnp test. Status of asymptomatic was defined as no (all 0s ) or minimal (ie, a few 1s or 2s out of 6 points on the severity scale) symptoms on the SCAT This is consistent with the level of symptoms reported by healthy people. 2 Once an athlete reported being asymptomatic, he/she underwent final cnp testing and the BCTT. 17 Athletes who were able to exercise to voluntary exhaustion on the BCTT without exacerbation of symptoms were allowed to RTP following the stepwise progression recommended by the Zurich Consensus Conference. 16 Following the RTP decision, any athlete with symptom recurrence was instructed to notify the concussion clinic immediately. For all subjects teams, the clinic provided certified athletic trainers (ATCs) capable of recognizing any recurrent concussion issues. The ATCs were advised to ensure that anyone who developed symptoms upon RTP would immediately withdraw from the sport and return to the clinic for reassessment. During the period of the study, the clinic switched from using to ; thus, the first 65 athletes were assessed using and the next 52 were assessed using. Automated Neuropsychological Assessment Metrics 23 and 24 are both norm-based measures that TABLE 1. Time (in Days) From Concussion to Initial Evaluation, Symptom Recovery, and Physiologic Recovery; Age and History of Prior Concussions for all Males and Females in the Study Population (N = 117) Age Prior Concussions Days From Concussion to Initial Evaluation Days From Concussion to Asymptomatic Days From Concussion to Pass BCTT Male (n = 88) Mean = 15.4 Yes = 29 Mean = 9.0 Mean = 14.0 Mean = 22.0 Median = 15.0 No = 59 Median = 6.0 Median = 11.0 Median = 17.0 SD = 1.6 SD = 8.0 SD = 13.0 SD = 17.0 Range = 0-41 Range = 0-81 Range = Female (n = 29) Mean = 15.4 Yes = 8 Mean = 11.0 Mean = 22.0 Mean = 33.0 Median = 15.0 No = 21 Median = 8.0 Median = 20.0 Median = 22.0 SD = 1.5 SD = 11.0 SD = 18.0 SD = 22.0 Range = 0-56 Range = 0-61 Range = Total (N = 117) Mean = 15.5 Yes = 37 Mean = 10.0 Mean = 16.0 Mean = 24.0 Median = 15 No = 80 Median = 6.0 Median = 12.0 Median = 18.0 SD = 1.6 SD = 9.0 SD = 15.0 SD = 19.0 Range = 0-56 Range = 0-61 Range = Ó 2013 Lippincott Williams & Wilkins 129

3 Darling et al Clin J Sport Med Volume 24, Number 2, March 2014 provide percentile rank standing. The Sports Medicine Battery of subtests include: Simple Reaction Time 1, Procedural Reaction Time, Code Substitution Learning, Code Substitution Delayed, Matching to Sample, Mathematical Processing, and Simple Reaction Time 2. The throughput score, which is based on the number of correct responses per unit of time, was calculated for each subtest. For, we used the 4 norm-referenced composite scores contained in the clinical report (Verbal Memory, Visual Memory, Visual Motor Speed, and Reaction Time). Automated Neuropsychological Assessment Metrics or was administered to individual athletes by a trained ATC using a designated computer in a quiet room. The cnp test was always administered before the BCTT to avoid any possibility that exercise might influence results (see McGrath et al 25 ). The BCTT is described by Leddy et al 17 and consists of an incremental treadmill exercise test following a standard Balke protocol until symptom exacerbation or voluntary exhaustion. In addition to frequent heart rate readings and close observation by a therapist, athletes are asked every minute while on the treadmill whether they are experiencing any worsening symptoms. Exercise testing is terminated if symptom exacerbation occurs or the athlete reaches exhaustion (defined by a rate of perceived exertion.18). Athletes who exercise to voluntary exhaustion without symptom exacerbation are considered ready for RTP. Statistical Analysis Statistical analysis was performed using the R programming language. 26 For the purposes of analysis of cnp data, we used normalized scores for subtests and percentiles for subtests (see Results). Logistic regression analysis and equivalence testing were used to determine whether performance on cnp tests in a cohort of adolescent athletes after concussion was predictive of return to learn difficulties. RESULTS The sample of adolescents assessed for concussion and eventually returned to play at this concussion clinic was threefourths male (75.2%). The sports most commonly represented among concussed males were football (n = 37, 42.1%), ice hockey (n = 22, 25.0%), and wrestling (n = 11, 12.5%). The most common sport for concussed females was soccer (n = 10, 34.5%). Table 1 provides information on the days since the concussion event until first visit at the clinic, days until the patient was asymptomatic, and days until successfully passing the BCTT. Females took substantially longer to achieve a state of asymptomatic, whereas days to completion of the BCTT was only slightly longer for females versus males. As noted in Table 1, this population of adolescents represents a substantial range in severity of concussion when severity is indicated by the number of days from injury to physiologic recovery (ability to exercise to exhaustion without exacerbation of symptoms on the BCTT). There was also a substantial difference in the number of days between injury and the initial physician assessment. The physician saw some athletes on the day of the injury and others were not seen for weeks after the injury. The latter cases were generally seen first by their primary care physician and referred to the concussion clinic for RTP and/or treatment for persistent symptoms. All the athletes were returned to sport in the week following successful completion of the BCTT. They were then progressed through the Zurich guidelines stages of RTP. 16 None of the athletes experienced a setback during the RTP process. Furthermore, none of the athletes experienced exacerbation of symptoms in sport during the 2 months following RTP. Follow-up phone contact with 91 athletes or their parents validated this finding. A number of the athletes in the follow-up portion of the study (n = 39, 42.9%) had at least some difficulty in readjusting to the classroom following concussion, with the most common complaint being difficulty concentrating. Although some of these athletes said they had trouble in school before the injury, the majority reported new problems in the classroom or increased problems (n = 35, 38.5%). The distribution of gender for those who reported a new problem in the classroom (males = 27, 77.1%) was essentially the same as the gender distribution for the sample as a whole. As presented in Table 1, 37 (31.7%) athletes had 1 or more previous concussions. Twenty-four (20.5%) had 1 previous concussion, 10 (8.6%) had 2 previous concussions and 3 (2.6%) had 3 or more. For the follow-up sample, the number of athletes with previous concussions was 31 (34.1%). A logistic regression analysis with a single independent variable (number of previous concussions) and a single dependent variable (new or increased difficulties in the classroom) showed that the number of previous concussions did not significantly predict school adjustment issues. Computerized Neuropsychological Testing More than half of the adolescent athletes (n = 28, 53.9%) had at least 1 subtest and close to half (n = 16, 41.0%) had 1 composite score in the borderline range on the day they passed the BCTT. Borderline was defined as less than the ninth percentile 27 and is referred to in the manual as below average. This study included 2 cohorts of patients for cnp testing. One cohort was given the test and the other cohort was given the test. The test, consisting of memory testing, motor skills testing, and reaction time testing, resulted in 4 variables included in this study (see Table 2 for the list of variables). The data for each of the 4 variables were the percentiles of the scores of each student relative to their national age group standards. The subtests primarily measured attention and working memory, information processing speed, associative learning, and recognition memory and resulted in 7 variables included in this study (see Table 2 for the list of variables). The raw scores from these variables were transformed to z scores by subtracting the raw score from the normative mean score and dividing by the normative standard deviation. The normative scores were obtained from the high school athlete normative sample from the 4 Users Manual. 28 The 2 outcomes were binary in measure. The first outcome (outcome 1) assessed new difficulty in school as Ó 2013 Lippincott Williams & Wilkins

4 Clin J Sport Med Volume 24, Number 2, March 2014 Evaluation of Zurich Guidelines TABLE 2. P-value Results for s and Subtests With Return to Learn Outcomes cnp Test Variable 1. Memory Verbal 2. Memory Visual 3. Visual Motor Speed 4. Reaction Time 1. Simple Reaction Time 2. Code Substitution Learning 3. Procedural Reaction Time 4. Mathematical Processing 5. Matching to Sample 6. Code Substitution Delayed 7. Simple Reaction Time Unadjusted P (Logistic Regression) With Outcome 1/2 Unadjusted P (Equivalence: Two 1-Sided Tests) With Outcome 1/ / / / / / / / / /0.9477,0.0001/, /0.9505,0.0001/, /0.5654,0.0001/, /0.4265,0.0001/, / / /0.8972,0.0001/, / / reported by either the adolescent or the parent and the second outcome (outcome 2) assessed difficulty in school as reported by either the adolescent or parent regardless of previous history in school. Assessment of correlation of and variables with outcomes was via logistic regression. The logistic regression P-value results for and variables are shown in Table 2 as determined by the glm function in R. Note that none of the variables are significant at level 0.05, suggesting that none of these variables are significantly correlated with either outcome. Equivalence testing was also performed to conclude whether the 2 classes of adolescents in each outcome scored similarly on cnp tests (with statistical significance). Equivalence testing was performed using the equivalence package in R package version (Ross Ihaka and Robert Gentleman, Auckland, New Zealand). Specifically, two 1-sided tests were performed with a bound of 2 for the variables and a bound of 30 for the variables with the (unadjusted) P values given in Table Significance for the equivalence tests was assessed using a Bonferroni corrected alpha level that required a P value less than 0.05/4 = , whereas the significance of the equivalence tests required a P value less than 0.05/7 = For the tests with outcome 1, we see that variables 1, 3, and 4 are significantly equivalent; that is, there is sufficient evidence to conclude that adolescents with new difficulties in returning to school scored similarly on those variables with adolescents who did not report any new difficulties in returning to school. For outcome 2, variables 1, 2, and 3 are significantly equivalent; that is, there is sufficient evidence to conclude that adolescents with difficulty in returning to school scored similarly on those variables to adolescents who did not report difficulty in returning to school. For equivalence testing, variable 5 (matching to sample score) is the only variable not significant with either outcome, suggesting that most variables do not vary significantly according to outcome. DISCUSSION The Zurich Consensus Conference Guidelines have been very helpful to sports medicine providers by encouraging a systematic approach to RTP following concussion. In this study, we allowed adolescent athletes to begin the Zurich stepwise RTP only after they were asymptomatic and able to pass the BCTT. The fact that 100% of these athletes returned to sport successfully is a testament to the value of following the Zurich guidelines. It also underscores the value of the BCTT as a preliminary test of physiologic recovery following concussion. This combination of treadmill testing and Zurich guidelines is clinically conservative, especially as the average adolescent in this sample returned to sport 1 month postinjury. It should be noted that there was a great deal of variability in the length of time to RTP in this population, presumably reflecting the variability in concussion severity. However, safe return to sport was achieved regardless of severity of injury. The BCTT closely simulates activity performed during sport and closely matches the Zurich guidelines with respect to attention paid to exacerbation of symptoms. The BCTT has good interrater and retest reliability for identifying symptom exacerbation in patients with concussion. 17 There is growing concern that some athletes do not truthfully report symptoms because of either self-imposed demands or external pressures from parents, teammates, or coaches. 30 We think this tendency to understate symptoms partially explains why the male athletes reached asymptomatic stage nearly a week earlier on average than females. However, males were only a few days ahead of females in passing the BCTT. An advantage of provocative exercise testing is that with increasing exercise intensity there is a fairly rapid and visible onset of signs of symptom exacerbation, such as vertigo, headache, or difficulty maintaining attention in those who have not fully recovered. 17 A potential benefit for athletes who successfully complete the BCTT without symptom recurrence is that they could bypass stage 2 of the Zurich graduated RTP protocol 16 (light aerobic exercise) and move directly into stage 3 (sportspecific exercise), hastening RTP for those who are physiologically recovered. This is an area of potential future study. A secondary purpose of our study was to quantify if any cognitive impairment existed on cnp test performance once Ó 2013 Lippincott Williams & Wilkins 131

5 Darling et al Clin J Sport Med Volume 24, Number 2, March 2014 athletes reported being asymptomatic. Almost half of these athletes had 1 or more cnp subtest or composite (either or ) score in the borderline range on the same day that they successfully completed the BCTT. In this study we did not have access to cnp baseline test results, but the athletes were compared with the normative data for both and. Comparison of cnp results with ageadjusted norms is recommended by some as the most effective approach. 7,31 In our clinic, cnp test performance was consulted but not used to determine the RTP decision; and as it turned out, cnp test performance did not relate to RTP success. In other words, poor performance on an subtest or an composite score did not have any bearing on successful RTP. Perhaps this is not surprising, given that success in RTP was defined as RTP without symptom exacerbation. The observation that 38.5% of adolescent athletes experienced problems adjusting to the classroom following a concussion was unexpected and concerning. Unfortunately, we did not ask how long these problems existed or the seriousness of the problems. Athletes with a history of concussions had no greater likelihood of having new school problems or exacerbation of earlier school problems. We were further surprised that cnp performance had essentially no relationship with the presence of school adjustment issues, especially since the most common complaint from the adolescents was difficulty concentrating. It was coincidence that the clinic switched from using to using halfway through the study, but it did allow us to comment on the predictive nature of both batteries. In this case, neither battery predicted school-related issues. However, it is important to point out that the test results used were from the final cnp test before return to sport. This was 3 weeks postinjury on average and school problems may have already resolved. One possible explanation for the high rate of borderline test results on either cnp test used is that the athletes did not put forth a full effort. Although the athlete is observed by an ATC during the testing process, it is difficult to determine if the athlete is struggling with the test or simply bored or unmotivated. A minority of athletes ask why they have to do this test again, a question heard regardless of whether we were using or. Test-taking behavior and a negative attitude of the athlete may explain why some think cnp tests do not meet minimum standards for reliability. Randoph et al 15 found that cnp test performance may lack utility in individual decision making for RTP, noting that additional research is clearly necessary before cnp testing can be considered a component of the routine standard of care for management of sport-related concussion. There are a number of limitations to the present study. All athletes passed the BCTT before being progressed back to sport using the Zurich guidelines. It is possible that return to sport would have been as successful if only the BCTT was used or if only the Zurich guidelines were used. The predictive nature of cnp testing might have been enhanced if baseline data were available. The telephone follow-up period in our study was variable and memory of school adjustment issues may have been forgotten with time; additionally, we did not assess for possible differences in academic accommodations among participants. The primary outcome measure of safe and successful RTP may not capture subtle cognitive issues represented by cnp testing. Future studies ideally would include preinjury baseline data, more cnp testing protocols, and cnp tests conducted sooner after the concussion to evaluate how cognitive issues relate to an athlete s performance on the field and in the classroom once returned to sport and to school. In conclusion, this study suggests that the BCTT in combination with the Zurich guidelines predicts a successful and safe return to sport. Programs may therefore want to consider using standardized exercise testing to help in the concussion RTP decision-making process. This study highlights the possibility that adolescents may have problems with the return to learn process even though they have successfully returned to sport. The study also raises questions about the degree to which successful return to the classroom can be predicted. Our evidence suggests that performance on cnp tests in a cohort of adolescent athletes with a concussion has no relationship with return to learn difficulties. Thus far, cnp testing performed once the athlete is asymptomatic does not relate to RTP and does not predict return to school issues. REFERENCES 1. Langlois JA, Rutland-Brown W, Wald MM. The epidemiology and impact of traumatic brain injury: a brief overview. J Head Trauma Rehabil. 2006;21: Lovell MR, Iverson GL, Collins MW, et al. Measurement of symptoms following sports-related concussion: reliability and normative data for the post-concussion scale. Appl Neuropsychol. 2006;13: Meehan WP III, d Hemecourt P, Collins CL, et al. Computerized neurocognitive testing for the management of sport-related concussions. Pediatrics. 2012;129: Coppel DB. Use of neuropsychological evaluations. Phys Med Rehabil Clin N Am. 2011;22: , viii. 5. Broglio SP, Ferrara MS, Macciocchi SN, et al. Test-retest reliability of computerized concussion assessment programs. J Athl Train. 2007;42: Segalowitz SJ, Mahaney P, Santesso DL, et al. Retest reliability in adolescents of a computerized neuropsychological battery used to assess recovery from concussion. Neurorehabilitation. 2007;22: Schmidt JD, Register-Mihalik JK, Mihalik JP, et al. Identifying impairments after concussion: normative data versus individualized baselines. Med Sci Sports Exerc. 2012;44: Shrier I. Neuropsychological testing and concussions: a reasoned approach. Clin J Sport Med. 2012;22: Field M, Collins MW, Lovell MR, et al. Does age play a role in recovery from sports-related concussion? A comparison of high school and collegiate athletes. J Pediatr. 2003;142: Covassin T, Schatz P, Swanik CB. Sex differences in neuropsychological function and post-concussion symptoms of concussed collegiate athletes. Neurosurgery. 2007;61: ; discussion, Broglio SP, Macciocchi SN, Ferrara MS. Sensitivity of the concussion assessment battery. Neurosurgery. 2007;60: ; discussion, Covassin T, Elbin R, Kontos A, et al. 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6 Clin J Sport Med Volume 24, Number 2, March 2014 Evaluation of Zurich Guidelines 16. 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 Clin J Sport Med. 2013;23: Leddy JJ, Baker JG, Kozlowski K, et al. Reliability of a graded exercise test for assessing recovery from concussion. Clin J Sport Med. 2011;21: Leddy JJ, Kozlowski K, Donnelly JP, et al. A preliminary study of subsymptom threshold exercise training for refractory post-concussion syndrome. Clin J Sport Med. 2010;20: Baker JG, Freitas MS, Leddy JJ, et al. Return to full functioning after graded exercise assessment and progressive exercise treatment of postconcussion syndrome [published online ahead of print January 16, 2012]. Rehabil Res Pract. doi: /2012/ McAvoy K. REAP the Benefits of Good Concussion Management. Centennial, CO: Rocky Mountain Sports Medicine Institute Center for Concussion; Accessed June Master CL, Gioia GA, Leddy JJ, et al. Importance of return-tolearn in pediatric and adolescent concussion. Pediatr Ann. 2012; 41: McCrory P. Sport concussion assessment tool 2. Scand J Med Sci Sports. 2009;19: Cernich A, Reeves D, Sun W, et al. Automated neuropsychological assessment metrics sports medicine battery. Arch Clin Neuropsychol. 2007;22:S101 S Iverson GL, Brooks BL, Collins MW, et al. Tracking neuropsychological recovery following concussion in sport. Brain Inj. 2006;20: McGrath N, Dinn WM, Collins MW, et al. Post-exertion neurocognitive test failure among student-athletes following concussion. Brain Inj. 2013; 27: Team RC. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation Statistical Computing; Lezak MD. Neuropsychological Assessment. 4th ed. New York, NY: Oxford University Press; Performance CftSoHO. 4 Users Manual. Version 4:[Sport High School Norms, Section A3, 73 76] com/anam-intro.html. Accessed March Wellek S. Testing Statistical Hypotheses of Equivalence and Noninferiority. Boca Raton, FL: Chapman and Hall/CRC; Lovell MR. Is neuropsychological testing useful in the management of sportrelated concussion? J Athl Train. 2006;41: ; author reply, Echemendia RJ, Iverson GL, McCrea M, et al. Advances in neuropsychological assessment of sport-related concussion. Br J Sports Med. 2013;47: Ó 2013 Lippincott Williams & Wilkins 133

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