The reporting of concussions among high school adolescents has increased markedly.1 Although historically literature has reported a concussion prevalence of 4% to 5%, more recent findings have found that nearly 20% of adolescents (patients 14 to 18 years old) have experienced at least 1 diagnosed concussion in their lifetime.2,3 Due to the fact that the developing brain has greater neural plasticity, it was previously thought that young age was protective against concussion and allowed faster postconcussion recovery.4 These thoughts have been disproven in recent years because studies have found that concussions in the immature brain result in a prolonged period of pathogenesis, leading to progressive neurodegeneration, hyperactivity, sustained cognitive impairments, and ultimately longer recovery.5,6
Team physicians must be particularly mindful when evaluating an athlete in this age group due to the short- and long-term neurocognitive implications, particularly as it pertains to return to sport (RTS). To assist in the management of concussions, neuropsychological testing is routinely implemented. Many institutions use the Immediate Post-Concussion Assessment and Cognitive Testing (ImPACT) score as their primary neuropsychological exam. ImPACT uses 6 neuropsychometric tests to generate 4 separate composite scores. These scores serve as surrogate markers for memory, attention, processing speed, and reaction time. Data from the concussed athlete are then compared with the athlete's previously obtained baseline scores or normative data matching the patient's demographics.7
Although the rates and long-term effects of concussion are extensively evaluated in the adult population, previous studies have not characterized concussions in the youth athlete or evaluated factors influencing time to RTS. The purpose of this study was to elucidate the epidemiological and RTS data of a large consecutive cohort of high school athletes presenting to sports medicine clinics who sustained 1 or more concussions, using the ImPACT scoring to quantify athlete readiness. The authors hypothesized that as patients experienced recurrent concussions, all ImPACT domains would show a predictable decline and athletes would require a longer time period prior to RTS.
Materials and Methods
After receiving institutional review board approval, the clinical records of 357 consecutive patients (14 to 18 years old) who presented to a single health care system between September 2013 and December 2016 with concussions were retrospectively reviewed. Four independent reviewers collected all data and performed extensive chart reviews. Patients with diagnosed neurological disorders were excluded.
Patient demographic and historical data, including age, sex, sport of concussion, and history of previous concussion, were collected from patient charts. Concussion-related variables such as loss of consciousness, amnesia, mechanism of injury, timing of diagnosis, timing of removal, and RTS were also obtained via retrospective chart review. History of concussion was used to denote a self-reported history of remote concussion by the patient. Previous concussion was used to denote a documented concussion that occurred during the study period. Patients were permitted to RTS after completing the 6-step pathway recommended by the Centers for Disease Control and Prevention, with each step requiring a minimum of 24 hours and the athlete to remain asymptomatic. The steps are as follows: no activity until asymptomatic at rest, light aerobic exercises, sport-specific exercise, noncontact training drills, full-contact practice, and RTS.8 Patient ImPACT scores were obtained from a separate database of ImPACT assessments collected by neuropsychologists at the authors' institution who perform and interpret Im-PACT tests on athletes.
The ImPACT metrics of verbal memory, visual memory, motor speed, reaction time, impulse control, and cognitive efficiency index and symptom scores were recorded at each round of testing, corresponding to each concussion in the study period. Athletes at the authors' institution also had baseline ImPACT testing performed prior to the season. For athletes not obtaining ImPACT testing prior to the season, a normative comparative data set was created based on baseline ImPACT testing of athletes with similar demographics who had no history of concussion. Data from the concussed athlete were then compared with either normative data matching the patient's demographics or baseline scores, for those applicable.
Verbal memory, visual memory, motor speed, and reaction time were expressed as a percentage of the normative data and/or baseline scores. Impulse control is expressed as the sum of errors committed during different phases of the test and has traditionally been used as a surrogate for test validity.9 Cognitive efficiency is expressed as an integer. It represents a measurement of percentage correct and reaction time in seconds on the symbol match test. A higher score indicates that the athlete performed well in both the speed and accuracy components of the symbol match test, and thus was more cognitively efficient.10 The symptom score is an integer representing the sum of an athlete's self-reported constitutional symptoms (eg, headache, dizziness, vomiting, and sensitivity to noise) data.9 A higher score reflects a higher symptom total.
All continuous data were described using means and standard deviations, whereas categorical data were described using counts and column percentages. Univariate 2-group comparisons were performed using independent 2-group t tests for continuous variables and chi-square tests for categorical variables. A multivariate linear model was built using predictors of RTS and results. Statistical significance was set at P<.05. All analyses were performed using SAS version 9.4 software (SAS Institute Inc, Cary, North Carolina).
A total of 357 patients with concussions presented to the authors' institution between September 2013 and December 2016. No patients were excluded from this study. The average age of injury for all athletes was 15.5 years (range, 14–18 years), and 61.9% of patients were male. Football was the most common sport of injury (27.7%), followed by hockey (21.8%) and soccer (17.0%). Of those concussed, 6.7% reported loss of consciousness and 14.3% reported amnesia. A history of concussion was reported in 33.0% of patients. Overall, 99.1% of patients were able to RTS (Table 1). When examining the 3 most common sports of injury, 30.6% of football players, 48.1% of hockey players, and 33.3% of soccer players reported a historic previous concussion. Among concussions sustained during the study time period, hockey players had the highest rate of loss of consciousness and amnesia (10.4% and 15.6%, respectively).
Demographics of All Athletes
On average, high school athletes required 30.4±23.3 days of recovery prior to RTS. There was a high incidence of history of concussion (33.1%) in high school athletes, and 32 athletes experienced a recurrent concussion. There was an increased time to RTS in athletes with a history of concussion (33.5±24.9 days vs 29.2±22.6 days, P=.12) or who sustained recurrent concussions (35.3±38.3 days, P=.77), although this was not statistically significant. Mean ImPACT verbal memory and visual memory scores increased between baseline ImPACT scores and Im-PACT scores after 1 and 2 concussion(s) for those athletes who sustained multiple concussions during the study period. Visual memory showed a significant increase in patients with a history of concussion as compared with those without a concussion (56.1%±25.5% vs 35.7%±25.9%, P=.015). Mean visual motor speed and reaction time decreased with each recurrent concussion (Figure 1).
Changes in Immediate Post-Concussion Assessment and Cognitive Testing (ImPACT) scoring with consecutive concussions (A). Changes in impulse control, symptom score, and cognitive efficiency index with each recurrent concussion (B).
A multivariable linear model controlling for possible covariates demonstrated that athletes with a history of concussion (P=.005), females (P<.001), and patients diagnosed in the clinic (P=.046) had a significantly longer RTS time (Table 2).
Multivariable Linear Model and Multivariable Poisson Model: Effect of Demographic Variables on Time to Return and Number of Visits for All Athletes
Risk factors for and outcomes of concussions in the youth athlete remain an important topic. This study found a high prevalence of high school athletes with a history of concussion, and these athletes require approximately 1 month of recovery prior to RTS. Females, athletes with a previous history of concussion, and those diagnosed in-clinic rather than in-game were found to have increased RTS times. In analyzing ImPACT scores, the authors found that as athletes sustained multiple concussions, scores related to memory increased, whereas scores related to motor speed and reaction time decreased.
Previous studies have evaluated RTS timing after a concussion. In 2000, Guskiewicz et al11 performed an epidemiological study on high school and college football players who sustained concussions. Their study demonstrated that an alarming 30.8% of concussed players returned to competition on the same day, and 20% of athletes never left the game. They attributed these findings to a historic disregard of RTS guidelines by clinicians. A recent study by Putukian et al12 suggested that high school athletes take approximately 30 days to RTS after a concussion, as compared with 3 to 5 days in professional athletes. This finding was likely due to a more contemporary approach to young athletes, emphasizing more careful and conservative treatment.12–14 The current study had similar findings, as high school athletes required approximately 30 days of recovery before RTS after a concussion. Additionally, the current study found a significant increase in RTS timing in those with a previous history of concussion. These findings suggest that there is greater compliance to contemporary RTS guidelines; however, there is no standardized RTS time because presentation and severity of concussions vary greatly.13 Furthermore, the results suggest that prior concussions may have lingering effects and that incomplete recovery may cause additive cortical and subcortical pathogenesis in a dose-response manner.15–18
Researchers have evaluated the effects of concussion on ImPACT scores. Tsushima et al19 evaluated recurrent concussions in high school athletes and found that they did not have significant changes in their ImPACT scores of verbal memory, visual memory, reaction time, processing speed, or symptom score with recurrent concussions. Conversely, Asken et al20 investigated the effect of ImPACT scoring on RTS in collegiate athletes and found that 60% of their patients exhibited a reliable decline in 1 or more ImPACT composite scores after a single concussion. However, their study found a paradoxical increase in visual memory after only 1 concussion. Similarly, the current study found that patients with a history of concussion showed a statistically significant 20% increase in visual memory after 1 concussion as compared with patients without a history of concussion. The current authors also found that patients who went on to have subsequent concussions demonstrated an increase in memory ImPACT testing. These results suggest that as patients sustain multiple concussions and undergo repeated ImPACT testing, they gain familiarity and comfort with the test and are able to perform the test's memory tasks more accurately and expeditiously, thus increasing their memory scores. When evaluating other ImPACT scores more representative of cognitive function, the current study found a reliable decline in average visual motor speed and reaction time. These ImPACT domains are not as susceptible to learning and thus show a dose-related decrease in score, reflecting previous findings that subsequent concussions have a dose-response decrease in cognitive functions among athletes.18
The analysis of athlete characteristics on outcomes following concussions has led to various findings.21–24 Berz et al25 found that females have a postconcussion symptom score nearly twice as high as those of males (30.9 vs 15.8, P<.05), and females may take longer to become symptom free after a sport-related concussion. Broshek et al24 and Covassin et al22 demonstrated that females have decreased simple and complex reaction times and processing speed as well as persistently lower visual memory composite scores after concussion. The current study found similar results, with females demonstrating significantly longer RTS times compared with males. These findings have been hypothesized to be due to worse vestibular and oculomotor impairment after concussion in females. This impairment may manifest as symptomatic headache and dizziness, delaying RTS.21 Finally, the current study found that athletes diagnosed in-clinic had a longer RTS as compared with those diagnosed in-game. These findings suggest that athletes diagnosed in-clinic had delayed diagnosis and ultimately delayed initiation of treatment as compared with those diagnosed in-game. Previous studies have found that athletes who began cognitive and physical rest immediately after injury (ie, in-game diagnosis) were more likely to recover within 30 days compared with patients who had delayed cognitive and physical rest for 1 to 7 days after their injury (the time it takes for an athlete to obtain a clinic appointment).26 These findings underscore the importance of vigilance during the game and prompt diagnosis of concussions by team physicians.
There were several limitations to this study. The authors were unable to account for athletes who were known to “sandbag” the ImPACT test, which is defined as athletes who purposely perform poorly on their baseline assessments to expedite their RTS after concussion. Previous authors have shown that sandbagging is difficult to accomplish without detection.27 At the current authors' institution, RTS can be subject to significant variability based on the physical rigors of sport. Additionally, the time between concussion and ImPACT testing was not standardized and subject to neuropsychologist availability. However, ImPACT testing was obtained in an expeditious manner and was not significantly different between athletes. Because this study was retrospective in nature, data were obtained from descriptive physician notes and an ImPACT database. Data accuracy is therefore dependent on thorough note completion. At the authors' institution, a standardized note is used that explicitly addresses all questions used in this study. Unfortunately, the methodology did not allow for differentiation of data between athletes who had prior Im-PACT testing and those measured against norms. Finally, many athletes did not have preseason ImPACT testing because it was not possible to coordinate testing and subject high school athletes participating in different seasons and school districts to a standardized protocol.
This study found a high prevalence of previous concussions in high school athletes. On average, players required 1 month of recovery before RTS. However, female athletes, players with a previous history of concussion, and those with delayed diagnosis required increased time to RTS. Impact scores for memory (visual and verbal) were found to increase with recurrent concussions, whereas visual motor speed and reaction time decreased.
- Rosenthal JA, Foraker RE, Collins CL, Com-stock RD. National high school athlete concussion rates from 2005–2006 to 2011–2012. Am J Sports Med. 2014;42(7):1710–1715. doi:10.1177/0363546514530091 [CrossRef] PMID:24739186
- Veliz P, McCabe SE, Eckner JT, Schulenberg JE. Prevalence of concussion among US adolescents and correlated factors. JAMA. 2017;318(12):1180–1182. doi:10.1001/jama.2017.9087 [CrossRef] PMID:28973604
- Centers for Disease Control and Prevention. TBI data and statistics: emergency department visits, hospitalizations and deaths, 2001–2010. https://www.cdc.gov/traumaticbraininjury/data/rates.html. Accessed December 26, 2017.
- Schneider GE. Is it really better to have your brain lesion early? A revision of the “Kennard principle”. Neuropsychologia. 1979;17(6):557–583. doi:10.1016/0028-3932(79)90033-2 [CrossRef] PMID:392335
- Huh JW, Widing AG, Raghupathi R. Midline brain injury in the immature rat induces sustained cognitive deficits, bihemispheric axonal injury and neurodegeneration. Exp Neurol. 2008;213(1):84–92. doi:10.1016/j.expneurol.2008.05.009 [CrossRef] PMID:18599043
- Pullela R, Raber J, Pfankuch T, et al. Traumatic injury to the immature brain results in progressive neuronal loss, hyperactivity and delayed cognitive impairments. Dev Neurosci. 2006;28(4–5):396–409. doi:10.1159/000094166 [CrossRef] PMID:16943663
- Lovell M. ImPACT version 2.0 Clinical User's Manual. Pittsburgh, PA: ImPACT Applications, Inc; 2004.
- Karlin AM. Concussion in the pediatric and adolescent population: “different population, different concerns”. PM R. 2011;3(10) (suppl 2):S369–S379. doi:10.1016/j.pmrj.2011.07.015 [CrossRef] PMID:22035679
- ImPACT Applications, Inc. ImPACT interpretation manual: ImPACT's online version. http://images.pcmac.org/Uploads/PortageAreaSD/PortageAreaSD/Departments/DocumentsCategories/Documents/Interpreting_the_ImPACT_Clinical_Report.pdf. Accessed December 26, 2017.
- ImPACT Applications, Inc. New study confirms the clinical usefulness of the ImPACT baseline ImPACT testing model. ImPACT Research Report. 2014;2:1–5.
- Guskiewicz KM, Weaver NL, Padua DA, Garrett WE Jr, . Epidemiology of concussion in collegiate and high school football players. Am J Sports Med. 2000;28(5):643–650. doi:10.1177/03635465000280050401 [CrossRef] PMID:11032218
- Putukian M, Aubry M, McCrory P. Return to play after sports concussion in elite and non-elite athletes?Br J Sports Med. 2009;43(suppl 1):i28–i31. doi:10.1136/bjsm.2009.058230 [CrossRef]
- Collins MW, Lovell MR, Iverson GL, Cantu RC, Maroon JC, Field M. Cumulative effects of concussion in high school athletes. Neurosurgery. 2002;51(5):1175–1179. doi:10.1097/00006123-200211000-00011 [CrossRef] PMID:12383362
- Collins MW, Field M, Lovell MR, et al. Relationship between postconcussion headache and neuropsychological test performance in high school athletes. Am J Sports Med. 2003;31(2):168–173. doi:10.1177/03635465030310020301 [CrossRef] PMID:12642248
- Barker T, Russo SA, Barker G, et al. A case matched study examining the reliability of using ImPACT to assess effects of multiple concussions. BMC Psychol. 2017;5(1):14. doi:10.1186/s40359-017-0184-1 [CrossRef] PMID:28454588
- Iverson GL, Echemendia RJ, Lamarre AK, Brooks BL, Gaetz MB. Possible lingering effects of multiple past concussions. Rehabil Res Pract. 2012;2012:316575. doi:10.1155/2012/316575 [CrossRef] PMID:22550590
- McKee AC, Cantu RC, Nowinski CJ, et al. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol. 2009;68(7):709–735. doi:10.1097/NEN.0b013e3181a9d503 [CrossRef] PMID:19535999
- Guskiewicz KM, McCrea M, Marshall SW, et al. Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA. 2003;290(19):2549–2555. doi:10.1001/jama.290.19.2549 [CrossRef] PMID:14625331
- Tsushima WT, Geling O, Arnold M, Oshiro R. Effects of two concussions on the neuropsychological functioning and symptom reporting of high school athletes. Appl Neuropsychol Child. 2016;5(1):9–13. doi:10.1080/21622965.2014.902762 [CrossRef] PMID:25397997
- Asken BM, Clugston JR, Snyder AR, Bauer RM. Baseline neurocognitive performance and clearance for athletes to return to contact. J Athl Train. 2017;52(1):51–57. doi:10.4085/1062-6050-51.12.27 [CrossRef] PMID:27905859
- Sufrinko AM, Mucha A, Covassin T, et al. Sex differences in vestibular/ocular and neurocognitive outcomes after sport-related concussion. Clin J Sport Med. 2017;27(2):133–138. doi:10.1097/JSM.0000000000000324 [CrossRef] PMID:27379660
- Covassin T, Elbin RJ, Bleecker A, Lipchik A, Kontos AP. Are there differences in neurocognitive function and symptoms between male and female soccer players after concussions?Am J Sports Med.2013;41(12):2890–2895. doi:10.1177/0363546513509962 [CrossRef] PMID:24197616
- Colvin AC, Mullen J, Lovell MR, West RV, Collins MW, Groh M. The role of concussion history and gender in recovery from soccer-related concussion. Am J Sports Med. 2009;37(9):1699–1704. doi:10.1177/0363546509332497 [CrossRef] PMID:19460813
- Broshek DK, Kaushik T, Freeman JR, Erlanger D, Webbe F, Barth JT. Sex differences in outcome following sports-related concussion. J Neurosurg. 2005;102(5):856–863. doi:10.3171/jns.2005.102.5.0856 [CrossRef] PMID:15926710
- Berz K, Divine J, Foss KB, Heyl R, Ford KR, Myer GD. Sex-specific differences in the severity of symptoms and recovery rate following sports-related concussion in young athletes. Phys Sportsmed. 2013;41(2):58–63. doi:10.3810/psm.2013.05.2015 [CrossRef] PMID:23703518
- Taubman B, Rosen F, McHugh J, Grady MF, Elci OU. The timing of cognitive and physical rest and recovery in concussion. J Child Neurol. 2016;31(14):1555–1560. doi:10.1177/0883073816664835 [CrossRef] PMID:27581848
- Schatz P, Glatts C. “Sandbagging” baseline test performance on ImPACT, without detection, is more difficult than it appears. Arch Clin Neuropsychol. 2013;28(3):236–244. doi:10.1093/arclin/act009 [CrossRef] PMID:23403552
Demographics of All Athletes
|Age, mean (SD), y||15.5 (1.3)|
| Male||221 (61.9%)|
| Female||136 (38.1%)|
| Football||98 (27.7%)|
| Hockey||77 (21.8%)|
| Soccer||60 (17.0%)|
| Basketball||32 (9.0%)|
| Cheerleading||15 (4.2%)|
| Other||72 (20.3%)|
|Loss of consciousness, No.|
| Yes||24 (6.7%)|
| No||333 (93.3%)|
| Yes||51 (14.3%)|
| No||306 (85.7%)|
|History of concussion, No.|
| Yes||118 (33.1%)|
| No||239 (66.9%)|
|Mechanism of injury, No.|
| Direct impact to head||324 (93.4%)|
| Indirect force||23 (6.6%)|
|Return to sport, No.|
| Yes||354 (99.2%)|
| No||3 (0.8%)|
|Visits to return, mean (SD), No.||1.7 (0.9)|
|Time to return, mean (SD), d||30.4 (23.3)|
|Time to return recurrent concussion, mean (SD), d||35.3 (38.3)|
Multivariable Linear Model and Multivariable Poisson Model: Effect of Demographic Variables on Time to Return and Number of Visits for All Athletes
|Variable||Effect on Time to Return, Estimate (SD)||P||Effect on Number of Visits, Estimate (SD)||P|
|Age||−0.07 (0.05)||.147||−0.01 (0.05)||.777|
|Sex, male vs female||−0.48 (0.13)||<.001||0.85 (0.10)||.169|
|Loss of consciousness, yes vs no||−0.19 (0.22)||.382||1.07 (0.23)||.750|
|Amnesia, yes vs no||0.21 (0.15)||.169||1.24 (0.18)||.131|
|Concussion, yes vs no||0.40 (0.14)||.005||1.07 (0.14)||.600|
|Hit, yes vs no||0.20 (0.24)||.422||1.03 (0.25)||.919|
|Timing, in-clinic vs in-game||0.47 (0.23)||.046||1.26 (0.29)||.304|
|Timing, in-clinic vs post-game||0.08 (0.13)||.533||1.13 (0.14)||.336|
|Timing, in-game vs post-game||−0.29 (0.22)||.083||0.89 (0.19)||.604|