1 Return to Play: Neurocognitive Testing and Return to Play Status in Adolescent Athletes
2 Abstract Objective: To assess the ability of neurocognitive testing in conjunction with symptom reporting to establish return to play status for adolescent athletes that have suffered a sports related concussion. Design: Systematic review of literature. Methods: Comprehensive keyword searches of Pubmed, TRIP data base, Cochrane Library, Google scholar and Dynamed using the terms concussion and neurocognitive testing, concussion and ImPACT. Pubmed was searched with limits of clinical trials, RCT, practice guidelines, case control trial, humans, and children -18 years old and adult 19+. Trip database search terms included concussion and neurocognitive testing with limits of years Results: Three cohort studies met inclusion criteria. Three articles used ImPACT in the evaluation of concussed athletes using statistical analysis to relate results to either control group or baseline testing. All three studies show statistically significant results in reference to post concussion testing and change in ImPACT results. Conclusion: Neurocognitive testing such as ImPACT can further aid clinicians to establish if an athlete has returned to pre-concussive neurocognitive status rather than using symptom reporting and on field diagnosis. Introduction Contact sports are among the most popular with adolescents competing in sports such as football, soccer, and wrestling. With increasing participation comes an escalating number of injuries, one of the most common being concussion or mild traumatic brain injury. In
3 29, 21% of all traumatic brain injuries (TBI) in children and adolescents were sports related, with over 446,788 sports related head injury visits to US emergency rooms. 1 Between 1997 and 28 there were.23 cases of TBI for every 1 high school athletic encounters, with the incidence of mild TBI or concussion in high school football at >5%. 2 Concussion is defined as a complex pathophysiological process induced by traumatic biomechanical forces 3 It typically results from direct blows to the head that may result in temporary loss of consciousness. Concussions are also typically followed by short lived symptoms that can include retro or anteriograde amnesia, confusion, difficulty concentrating, and headaches, although other symptoms may be present. In most cases, symptoms typically resolve within 5-7 days. Symptom resolution and clinical judgment are the tools used in designating return to play status post injury. However, recent studies indicate that second impact syndrome, or receiving a subsequent blow to the head following incomplete recovery to be more worrisome than previously thought. Incomplete recovery increases vulnerability to minor impacts during the post concussive period and can lead to cumulative brain injury or rarely, sudden death. 4 Adolescent athletes are notorious for under reporting or misreporting symptoms following a concussive incident. The current gold standard for concussion evaluation and determining return to play (RTP) status depend on clinical impression, on field diagnosis, and symptom reporting. Neurocognitive testing may be a valuable tool to assess cognitive symptoms and recovery that athletes may either be unaware of or not report.
4 The studies reviewed all employ a computer-based system called the ImPACT Neurocognitive Test Battery (Table1). The test is comprised of four categories: verbal memory, visual memory, reaction time and visual motor processing speed, along with a symptom reporting score, or post concussive symptom reporting score (PCS). Six different tests are administered and each is factored into these categories to give a composite score for each neurocognitive domain. The PCS score is established on a point system covering 22 common postconcussive symptoms such as headache, nausea, and difficulty concentrating. Clinical Question In adolescent athletes with concussion or mild traumatic brain injury, do neurocognitive tests aid in diagnosis and return to play status? Methods A search of PubMed was performed using the terms concussion and neurocognitive testing, and concussion and ImPACT testing. Limits included Clinical trials, RCT, metaanalysis, practice guidelines, case control trial, humans, and children -18 years old and adult 19+. Searches were limited to studies after 21 since most of the background data and reliability of ImPACT testing was completed after 21. The search yielded 78 results, with two meeting inclusion criteria (Table 2). Additional searches in TRIP Database, DynaMed, Cochrane Library, Google Scholar along with a hand search yielded another study that met inclusion criteria.
5 Van Kampen, et al 26 5 Objective: To see if the use of computer based neurocognitive testing results in an increased capacity to detect post concussive abnormalities after injury. Study Design: This was a prospective and retrospective cohort study of 122 collegiate and high school athletes from six states who underwent baseline cognitive testing using ImPACT and repeat testing within 2 days following a concussive incident from (Table 3). Their results were then compared with gold standard on field diagnosis performed by either a medical doctor or certified athletic trainer. A control group of 7 non-concussed athletes was established who underwent baseline Impact testing and retesting 1 week later. Post concussive evaluation revealed significant score differences using a Reliable Change Index (RCI) to account for practice effect and other factors that can affect test scores in repeat testing situations. RCI s were established for different aspects of ImPACT, where 56 non-concussed athletes took ImPACT twice over a two-day time period. Test results from these subjects were analyzed to evaluate for test/retest reliability and practice effect to establish a normal variability within repeat scores. 6 An individual performance was reliably different from baseline testing if the difference in score between baseline and post concussive testing was larger than the RCI score. Therefore, a change in a score that exceeds the RCI is deemed to be an abnormal for follow up testing. Statistical significance was determined using χ² analysis (χ²₁=55.4, p<.).
6 Study Results: Based on reported post concussive symptom (PCS) scores, 64% of athletes reported increased symptoms from baseline that exceeded RCI. Eighty-three percent of concussed athletes had at least 1 ImPACT score that exceeded the RCI. The addition of neurocognitive testing to symptom reporting alone increased sensitivity by 19%. If an athlete had either a symptom score or at least 1 ImPACT test abnormality, 93% of concussed subjects were correctly identified compared to the 64% that were identified by PCS and on field diagnosis. While 93% of the concussed sample had either an ImPACT or symptom score that fell within abnormal RCI scores compared to baseline, none of the concussed athletes had both an abnormal PSC score and abnormal ImPACT performance. If ImPACT was used without reported symptoms, the predictive value for having at least 1 abnormal ImPACT score was 83% with a negative predictive value of 7%. The combination of an abnormal PCS score with an abnormal ImPACT score resulted in a predictive value of 81% while the negative predictive value was 83%. The authors found there was a significant increase in diagnosis. Two days after an on field diagnosis only 64% of athletes reported increased symptoms on PCS. The addition of ImPACT increased the percentage of abnormal, or patients with a change in their ImPACT score, increased to 83%, thus showing that ImPACT increased the diagnosis rate by 19%. Study Critique: This study demonstrates that, although an athlete may report no symptoms, neurocognitive effects may be present and that RTP should be delayed. In addition, symptom reporting and on field diagnosis may not diagnose all cases. A strength of this study is matching on field diagnosis and symptom reporting compared to follow up ImPACT testing. It suggests that under reporting of symptoms may have detrimental
7 effects on RTP status. The authors address the effects of prior concussions which is an additional strength. In baseline testing, patients with a history of concussion did not show statistically significant differences in scores in all categories except the verbal memory composite (t= 2.72, p<.7). Generally, subjects with a prior concussion performed better on the test. The impact on these findings is not addressed by the authors. The use of RCI s, that may miss milder concussions, is another weakness. If the test result deviates from baseline test scores but not enough to fit into an RCI classification, a mild concussion may be missed. In addition, control groups and study groups often have different demographics in reference to specific sport participation. Contact sports, especially football, have a significantly higher representation in study groups unlike the control groups. This study follows the same bias trend, but it does not directly affect comparison to an individual s baseline testing. Timing of the testing between control and test subjects presents additional issues. Control subjects retook the test within one week of initial testing, while the timing for athletes was not established. This may allow for bias in that controls may be influenced following exposure to the test within a shorter time period although studies have looked at the test retest reliability of ImPACT in non-concussed subjects and found that there is little practice effect or improvement with multiple testing over a longer time period. 7 Finally, it is difficult to construct a study with appropriate blinding. While study results are analyzed and calculated by the ImPACT program, administrators are not blinded to
8 subjects or concussion status as only those with a concussion underwent follow up testing. Testing was administered according to ImPACT standards by a team including neuropsychologists, athletic trainers, and/or physicians, but blinding or issues of bias were not addressed. Level of evidence: 2b- Fazio 27 8 Objective: To examine the differences in neurocognitive performance between symptomatic concussed athletes, a group of asymptomatic concussed athletes, and a nonconcussed group of control athletes using ImPACT. Study Design: This cohort study was composed of 192 high school and college athletes (78 concussed symptomatic, 44 concussed asymptomatic, and 7 non-concussed athletes). All athletes in the study underwent baseline ImPACT testing prior to sport participation during athletic seasons from (Table 4). Following a concussive event diagnosed by a physician or athletic trainer, athletes took a follow up ImPACT test within 7 days. The non-concussed control group underwent follow up testing within 48 days of an initial test. Statistical analysis was performed using Multiple Analysis of Variance (MANOVA) and univariate analysis to assess the variance between the 3 subject groups in reference to neurocognitive performance on ImPACT.
9 Study Results: The study found the overall MANOVA was highly statistically significant (F=14.5, p<.1) for difference in overall test scores between the three subject groups. Statistically significant variance in verbal memory score was evident F=34.4, p<., with the symptomatic concussed group scoring lowest, followed by the asymptomatic concussed group, and the control group performing the best. The symptomatic concussed group had the lowest performance in all categories, for visual memory F=41.6, p<., processing speed F= 32.4, p<., and reaction time composite F=33.6, p<.. Study Critique: This study shows a solid correlation between symptomatic patients and decreased ImPACT scores as compared to asymptomatic and non-concussed athletes. A main strength is the comparison between asymptomatic and symptomatic patients. High school and college athletes often underreport symptoms in an effort to return to activity, this study shows that neurocognitive impairment is often still present after symptoms have resolved or reportedly resolved. The comparison between these two groups supports the validity of the study in showing that ImPACT can have a significant place in diagnosis, especially in athletes with no reported symptoms. However, there is a significant factor that should have been addressed. The inclusion criteria state that all participants in the study underwent baseline testing, however the baseline tests are never addressed in the study. There is significant population variation pertaining to type of sport participation among the groups. Contact sports are over represented in the concussed group compared to controls. This may represent a problem in comparing test score when there is no initial comparison in baseline test scores. In
10 addition, there is no exclusion criteria included in the methods. Participants in contact sports are more likely to sustain concussions, and with 68% of participants in both symptomatic and asymptomatic concussion groups participating in football, it seems reasonable that prior concussion status and baseline test score would be relevant information to include for true comparison of ImPACT s ability to diagnose concussion. Finally, as in the other studies blinding is neither considered nor addressed in this study. Level of Evidence: 2b- Mcclincy, et al 26 9 Objective: To examine the time of recovery from concussive injury for high school and collegiate athletes participating in a variety of sports using ImPACT. Study Design: This retrospective cohort study employed 14 high school and college athletes that experienced a concussive event. Participants had a pre-season baseline ImPACT evaluation, an on field diagnosed concussion injury during play, and three subsequent ImPACT tests following injury (Table 5). No control group was established due to each athlete having a baseline test done as the method for individual evaluation and comparison, thus serving as their own control. Athletes were returned to activity when they achieved their own baseline score, at which time no further testing was done. Following a concussive event, athletes had follow up ImPACT testing on days 2, 7, and 14 post injury. Testing information was gathered in the standardized method as established
11 by ImPACT and scores were automatically generated eliminating possibility of variation in administration or data collection. All results were compared to the subjects initial baseline score. In addition patients also reported on a total symptom score that is included in the ImPACT test. Prior concussion history and associated symptoms were noted but not factored into results since subjects were compared to their baseline score. The study also did not exclude subjects with a history of seizure or other neurological disorder. MANOVA was used for statistical analysis and to evaluate statistical significance of on athlete performance on ImPACT. In addition, a Bonferroni analysis was used to test for significant differences in baseline and post concussive test scores, and to adjust for experimental error and false positive tests. Study Results: Statistically significant test scores were found throughout follow up testing from baseline score in all categories, with post injury day 2 producing the greatest amount of variation. For the verbal memory composites through the entire evaluation period there was a significant difference in performance F (3,39)=37.74 (p<.1), with a large decrease in score extending into the 3 rd testing session. Full verbal memory had not recovered to baseline within the testing period. The visual memory composite showed a significant difference in test performance between baseline and initial post concussion evaluation on day 2, F (3,225)=19.5, p,.1. However by day 14, no significant difference was observed from baseline. The visual composite was
12 only applied to 76 of the sample subjects, as prior to 23 the visual composite was still in the testing phase for ImPACT and not factored into test scores. There was a significant increase for processing time in day 2 testing. However, subsequent tests showed normalized processing times with the final test at day 14 post injury actually showing a decreased processing time from baseline. There was a significant increase in reaction time score from days 2 and 7, but by day 14, no significant difference was present and in some cases, reaction test times improved from baseline. Finally in symptom reporting, significant differences in score were found from baseline to day 7 F(3,39)=72.3, p<.1. By day 14 significant differences were no longer apparent. Overall this study predicts that 8% of the sample would have returned to play prematurely based on on-field concussion symptoms and symptom reporting alone. Study Critique: This study has many strengths; most important is the use of baseline testing as the control for the study. Previous studies have established that baseline testing for control parameters eliminates the need for establishing a homogeneous control and study group for testing that is based on individual scores. It also eliminated the need for extensive exclusion criteria for learning disabilities or other disorders that may interfere with testing. Secondly, the study looks into previous concussion history and was able to show that the study group had similar trends to predicted values. Finally, this study uses a conservative method of analysis (Bonferroni), and is still able to show significant differences in test scores that support postponing RTP until ImPACT scoring has returned to baseline.
13 One major weakness of this study was the inability to follow all possible athletes that had a concussive event. Subjects were returned to play as soon as they were asymptomatic and ImPACT testing had returned to baseline. Therefore, the test does not include patients that were on the short end of the testing spectrum, and would have decreased the total variation in scores. Those athletes followed throughout the 14 day testing many have suffered more severe concussion possibly accounting for their increase in reported symptom and lower testing score which may have skewed results of the study. Sample demographics also limit this study in that very few were collegiate athletes, and the median age for the sample was the youngest of all studies (16.11 years). Studies have shown that concussions may take longer to heal in younger patients, therefore it may be difficult to expand this study s conclusions to collegiate athletes. 1 This study, unlike the other studies, fails to define diagnostic criteria for concussion prior to testing. While it looked at the reported on field symptoms it does not outline which method was used for diagnosis. It is not clear in this study what the authors used as a gold standard for comparison of their testing, as well as any attempt to blind or effects of blinding may have had on study outcomes. Level of Evidence: 2b-
14 Discussion Diagnosis of concussion has long depended on on-field diagnosis and symptom reporting, with the typical athlete returning to play seven days after initial injury. Interestingly, this is the typical time frame between football games. 9 (9) The studies in this review look at the ability of ImPACT to diagnose athletes in conjunction with the gold standard of diagnosis and measurement of post concussive symptoms to make important RTP decisions. The three studies vary significantly in study design, most importantly in establishing a control group. In Van Kampen et al and Mcclincy et al, baseline testing was used for control measurements against the test subjects. In a study that looks at baseline testing as part of the evaluation and diagnosis, this is important to establish continuity in evaluation of the study group. Since ImPACT is based on variation from baseline for diagnosis of concussion it seems that this would be an important method for evaluating the effectiveness of the test as well as control for variations in the study population; the need for an equal control group is eliminated. However, Fazio et al designates a control group for score comparison in retesting. The main problem with comparison between groups is large variation in sports participation. Many of the concussed group participates in contact sports while the control or non-concussed group participates in non contact sports. The key problem with this comparison is that the inclusion/exclusion criteria do not account for inherent differences between the groups. Another important factor addressed by Van Kampen et al and Fazio et al is the criteria for establishing if patients had suffered a concussive event. Both outline a method for on-field
15 and reporting of concussive symptoms for diagnosis and inclusion into the study population. They both make a direct reference to the current gold standard of diagnosis and how this was reached. This allows linkages between direct differences of the on-field diagnoses and the difference ImPACT. Mcclincy states only that participants diagnosed with in season concussions were included, but there are no criteria for concussion established, so inclusion criteria is vague. While the three studies all use ImPACT, they look at the testing and its utility in different ways. All authors used the same version of ImPACT except where noted in the study appraisals. Van Kampen et al, specifically evaluates the ability of ImPACT to increase the sensitivity of diagnosis from symptom reporting alone from 64%-89%. With this increase in diagnostic accuracy, RTP can then be better gauged. In contrast, Mcclincy et al and Fazio et al, use MANOVA to evaluate for statistical differences between multiple testing groups. These studies look at the effect of time on testing results and the reporting of symptoms between groups. All three studies demonstrate the value of ImPACT score reporting. Definite trends arise in the concussed groups whether control groups or baseline test results are used. While large standard deviations are present in many categories Table 8 still shows that athletes post concussion perform worse on ImPACT compared to either baseline or control scores. The most significant change is apparent in day 2 scores. All three studies showed statistically significant changes on the first day of testing regardless of symptom reporting, use of baseline testing, or use of control subject testing.
16 While Fazio et al does not give specific time intervals for testing and only notes that it was done within 7 days of injury, it shows along with Mcclincy et al, that cognitive effects may be present when symptom reporting is either resolved or very minimal. This indicates that symptom reporting alone may not be the ideal criteria to return adolescents to unrestricted activity. Conclusion With growing concern over the long term effects of multiple concussions on cognition recently reported in case series and prevalent in the news today, it is important for clinicians to find ways to prevent excessive youth athlete head injury. Adolescents can be poor reporters of symptoms and objective measures to improve diagnosis are warranted. While none of the above studies give a definitive answer as to ImPACT s use over the gold standard, they suggest that ImPACT can aid clinical decision-making following a concussive injury. Neurocognitive testing may be a practical and prudent support to the current standard of clinical presentation. Additional studies with larger, more diverse patient populations will offer greater insight into the utility of ImPACT on determining RTP status and providing additional tools to keep athletes safer following concussion.
17 References 1. Sports Related Head Injury. American Assoc of Neurological Surgeons [Internet]. Rolling Meadow (IL): -Related%2Head%2Injury.aspx. Updated July Trends in Sports Related Concussion- Incidence at the High School Level American Public Health Assoc Paul McCrory, MBBS, PhD*; Willem Meeuwisse, MD, PhD; Karen Johnston, MD, PhD et al. Consensus Statement on Concussion in Sport: The 3 rd International Conference on Concussion in Sport Held in Zurich, November 28. Journal of Athletic Training 29;44(4): Schnadower. Controversies in evaluation and management of minor blunt head trauma in children. Pediatrics. 19:258, D. Van Kampen, M. Lovell, J. Pardini, M. Collins, F.H. Fu. The Value Added of Neurocognitive Testing After Sports Related Concussion. Am J Sports Med. 26 Oct;34(1): Epub 26 Jun 3.PMID:
18 6. Iverson GL, M. Lovell, M Collins. Interpreting change on ImPACT following sport concussion. Clinical Neuropsych. 23;17: Schatz, Philip. Long-Term Test-Retest Reliability of Baseline Cognitive Assessment Using ImPACT. The American Journal of Sports Medicine. 21; V. Fazio, M. Lovell, J. Pardini, M. Collins. The relationship between post concussion symptoms and neurocognitive performance in concussed athletes. NeuroRehabilitation. 27;22(3): PMID: M. McClincy, M. Lovell, J. Pardini, M. Collins, M. Spore. Recovery from sport concussion in high school and collegiate athletes. Brain Inj. 26 Jan;2(1):33-9. PMID: Field M, Collins MW, Lovell M. Does age play a role in recovery from sports related concussion? A comparison of high school and collegiate athletes. Journal of Pediatrics. 23;142:
19 Tables Table 1: ImPACT Neurocognitive Test Battery Test Name Word Memory Design Memory X s and O s Symbol Match Color Match Three Letters Memory Symptom Scale (PCS score) Composite Score Verbal memory Visual memory Reaction time Visual motor processing speed Neurocognitive Domain Measured Verbal recognition memory (learning and retention) Spatial recognition memory (learning and retention) Visual working memory and cognitive speed Memory and visual motor speed Impulse inhibition and visual motor speed Verbal working memory and cognitive speed Rating of individual self-reported symptoms Contributing Score Averaged percentage correct scores for the Word Memory (learning and delayed), Symbol Match memory test, and Three Letters Memory test Averaged percentage correct scores for the Design Memory (learning and delayed) and the X s and O s test Mean time in milliseconds for the X s and O s (mean counted correct reaction time), Symbol Match (mean weighted reaction time for correct responses), and Color Match (mean reaction time for correct response) X s and O s (mean correct distracters), Symbol Match (mean correct responses), and Three Letters *Van Kampen et al. Table 2. Study Inclusion Criteria Adolescents- high school and/or college athletes Use of ImPACT Study conducted after 21 Cohort studies, RCT, or case control Table 3. Van Kampen et al 26. Concussed Patient Exclusion Criteria History of attention deficit disorder- with medication treatment History of psychiatric disorder- with medical treatment Seizure or other neurological disorder Table 4. Fazio 27. Inclusion Criteria Concussed Group High School or College athlete Baseline ImPACT Retest within 7 days of concussion Control Group High School or College athlete Baseline ImPACT Retest within 2 days
20 Table 5. Mcclincy 26. Inclusion Criteria Pre season baseline ImPACT On Field Diagnosed concussion Three follow up ImPACT tests Table 6. Summary of Designs and Validity Study Design and analysis Initial diagnosis criteria Van Kampen, 26 Fazio, 27 Mcclincy, 26 Case Control, Exploratory Cohort, Retrospective Reliable Change MANOVA Cohort, MANOVA, Index Scoring Bonferroni Symptom reporting, altered LOC, on filed medical professional dx Observable change in LOC at time of injury, on field exam, self reported symptoms Not specified Control group Yes Yes Yes. Subject preconcussion baseline data used as control Follow up testing schedule % patients with follow up Baseline, 2 days 2 days Baseline, 2, 7, 14 days 1% 1% Unknown-only patients with 3 test results included Level of evidence 2b- 2b- 2b-
21 Table 7. Summary of Study Demographics Total subjects High school % College % Sport % Football Soccer Basketball Swimming Track Other Average Age (years) On Field reported Symptoms % +LOC Amnesia Confusion Van Kampen, 26 Fazio, 27 Mcclincy, 26 Concussed Control Symptomatic Asymptomatic Control Concussed N/A N/A Table 8. Comparison of Statistical Values Test Fazio, 27 McClincy. 26 Van Kampen, 26* Verbal F=34.4 p<.1 F=37.74 p<.1 ImPACT ImPACT Alone & + PCS Visual F=41.6 p<. F=19.5 p<. Sensitivity 83% Sensitivity N/A Processing Speed F=32.4 p<. F=26.74 p<. PPV= 83% PPV= 81% Reaction Time F=33.6 p<. F=28.7 p<. NPV= 7% NPV= 83% *Results for Van Kampen, 26, differ due to statistical method.
22 Table 9. Summary of Results- ImPACT composite scores: testing group means and (standard deviations) ImPACT Scores Verbal Memory Composite (What is in the parentheses?) Visual Memory Composite Reaction Time Composite Processing Speed Composite Symptom Report Composite Van Kampen, 26 Fazio, 27 Mcclincy, 26 Baseline Day 2 Control Asympt. Sympt. baseline Day 2 Day 7 Day (8.9) 74. (12.8).57 (.8) 36. (6.8) 6.8 (9.6) 76 (14.4) 64.3 (13.8).64 (.13) 25.6 (8.6) 25.6 (19.1) 89.6 (7.7) 8. (11.7).53 (.6) 42.2 (6.9) 79.8 (1.6) 67.6 (13.5).58 (.8) 37. (6.5) 73.1 (15.7) 6.5 (13.8).67 (.13) 32. (8.9) (8.59) 74.4 (13.82).57 (.76) 35.5 (8.9) N/A N/A N/A 5.14 (7.87) 72. (14.87) 61.2 (12.92).667 (.151) 3.28 (9.6) (19.69) (13.79) (15.92).635 (.121) (8.1) 13.8 (15.5) (13.6) (14.31).568 (.88) (8.3) 7.18 (15.86)