Concussion symptom presentation and clinical recovery among pediatric athletes: comparing concussions sustained during school and summer months

ABSTRACT Objective We examined post-concussion symptom presentation, exercise, and sleep among pediatric athletes who sustained concussion during the school year vs. summer months. Methods We evaluated athletes 6–18 years old within 21-days of concussion. They reported symptoms (Health and Behavior Inventory), with cognitive/somatic domain sub-scores calculated, and indicated if they had exercised or experienced sleep problems since injury. We grouped patients by injury season: summer months (June–August) vs. school year (September–May). Results 350 patients (14.4 ± 2.4 years old; 37% female; initial visit 8.8 ± 5.3 days post-concussion) were seen for care: 24% sustained a concussion during summer months, 76% during the school year. Lower cognitive (median = 7 [IQR = 1, 15] vs. 9.5 [4, 17]; p = 0.01), but not somatic (7 [2.5, 11] vs. 8 [4, 13]; p = 0.06), HBI scores were observed for patients injured during the summer. Groups were similar in proportion exercising (16% vs 17%) and endorsing sleep problems (29% vs 31%). After adjustments, sustaining a concussion during the summer predicted total (β=-3.43; 95%CI = −6.50, −0.36; p = 0.029) and cognitive (β = -2.29; 95%CI = −4.22, −0.36; p = 0.02), but not somatic (β=-1.46; 95%CI = −2.84, −0.08; p = 0.04), symptom severity. Conclusion Pediatric patients with concussion may present with greater cognitive symptoms during the school year, compared to summer months.


Introduction
Concussion, a form of mild traumatic brain injury, is complex and heterogenous in clinical presentation for pediatric patients (1,2).A variety of factors should be considered both acutely post-concussion and throughout the duration of recovery (1,2).In the acute and sub-acute post-concussion period, quality sleep and engagement in sub-symptom threshold aerobic exercise are beneficial for recovery (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12).Pediatric and young adults initiating aerobic exercise sooner post-concussion demonstrate faster time to return-to-sport than those with delayed initiation of aerobic exercise (3).Better sleep quality after concussion is similarly associated with shorter recovery time (10,11,13).Furthermore, improved sleep quality and increased levels of physical activity are correlated with lower initial post-concussion symptom burden (9,(14)(15)(16)(17).This may be particularly important given that acute and sub-acute symptom severity are among the most consistent predictors of time to symptom resolution (18)(19)(20)(21).As such, management strategies for concussion generally involve some combination of engagement with symptom-limited physical activity, improving sleep quality, and gradual reintegration of cognitive activity to reduce symptom burden and accelerate recovery.
Implementing this treatment plan while simultaneously supporting appropriate return to school among pediatric athletes can be difficult.Academic problems are common in children and adolescents returning to school after sportrelated concussion (22), and recent attention has been given to processes that facilitate a successful return to school (23)(24)(25).The relationship between school attendance and concussion symptom burden is complex and likely bidirectional.Prior work suggests that earlier return to school is associated with reduced symptom severity and faster time to symptom resolution (26,27), while other research indicates that more hours of school participation within 1-2 weeks of concussion is associated with greater post-concussion symptoms (28).Thus, it is difficult to elucidate if school participation contributes to post-concussion symptoms or if post-concussion symptom burden affects the timing of return to school participation.Independent cohorts, with patients who are and are not attending school, may address some questions regarding the relationship between school participation and initial postconcussion symptom presentation or clinical recovery.Such opportunities are afforded when comparing patients who sustained concussion during the school year, when school activities are at their peak, to patients who sustained concussion during the summertime, when participation in school activities are substantially reduced for most children.
Epidemiological studies have assessed seasonal (e.g., fall, spring, summer) concussion trends (29)(30)(31)(32), but no research has investigated differences in symptom presentation or clinical recovery among patients sustaining concussion in different seasons of the year.Thus, the purpose of this study was to compare initial symptom presentation and clinical recovery outcomes for pediatric patients who sustained a concussion during summer months vs the school year.Secondarily, we sought to examine potential differences which exist in subacute exercise engagement and sleep problems in patients injured during summer months vs the school year.Last, we aimed to understand the effect of injury season (summer vs school year) on symptom presentation after controlling for the effects of sub-acute exercise and sleep problems.
We hypothesized that patients injured during summer months would report lower concussion symptom burden than those injured during the school year.We also hypothesized that patients injured in the summer months would be more likely to report exercising after injury and less likely to report sleep problems in the sub-acute phase of recovery than patients injured during the school year.Last, we hypothesized that, after controlling for exercise and sleep problems, the season of injury would no longer be associated with initial symptom presentation.The results of this study may be important for clinicians counseling patients on return-to-school within the context of exercise and sleep behaviors during concussion recovery.Secondarily, our results may identify complex relationships which exist between school participation, exercise and sleep, and clinical outcomes after concussion.

Study design and participants
We obtained data from a clinical registry of patients seen for concussion care at a single regional sports medicine program between January 2015 and December 2019.The sports medicine program where patients were evaluated was in a single metropolitan area and part of a larger tertiary care children's hospital.Electronic medical records were reviewed retrospectively, and patients were included if they were diagnosed with concussion by a board-certified pediatric sports medicine physician, 6-18 years of age at the time of injury, and seen for initial evaluation within 21 days of concussion.Concussion diagnosis was determined in accordance with the most recent consensus statement for concussion in sport at the time of clinical evaluation (2,33).Exclusion criteria consisted of having a prior concussion within 6 months of the current injury, presence of a structural abnormality on neuroimaging (if performed), or sustaining a second head injury prior to complete recovery from the presenting concussion.Provided our population of interest was pediatric athletes, and our primary clinical outcomes include time to symptom resolution and returnto-play (RTP), patients were excluded prior to analysis if their mechanism of injury was not sport-related (e.g., fall, motor vehicle collision, etc.) or if they had incomplete recovery data (Figure 1).Prior to study commencement, an ethical review was conducted by the local institutional review board (Colorado Multiple IRB), who provided approved of the study protocol.
At the initial post-concussion evaluation, patients reported demographics (age, sex, race/ethnicity) and relevant medical history as part of their routine clinical care.Medical history included history of concussion, pre-injury diagnosis of anxiety, depression, or ADD/ADHD, and presence of pre-injury sleep problems.The patient's primary sport type was collected and dichotomized as contact or non-contact, in line with previous research (34,35).Race and ethnicity demographics were only collected on approximately half of the patient sample, due to collection errors in the retrospective review of medical records, and thus are not reported.

Primary outcomes
At the initial post-concussion evaluation, patients selfreported their current symptom burden via the Health Behavior Inventory (HBI) (36,37).This measure involves rating 20 common concussion symptoms on a 4 point scale, with responses ranging from 0 (never) to 3 (often), and has been validated for use in pediatric patients with concussion (38)(39)(40).The HBI was completed by both patients and the parent/legal guardian who accompanied them to the clinical visit.Among patients <8 years old, only the parent/legal guardian form was completed.Previous work has established high correlation between parent-reported and patient-reported scores on the HBI (38).The primary outcome for the HBI is the total score, or sum of the scores for all 20 items (range: 0-60).The HBI also contains two subscales to separately assess cognitive and somatic symptoms (40).Cognitive symptoms include attention/focus, memory, or general cognition.Somatic symptoms include items such as fatigue, headache, nausea, or dizziness.
Independent of the HBI, patients also reported the severity of their current headache, rated on a 0-10 scale (least to most severe).For analysis, any score > 0 was considered an indicator for the presence of headache at the initial evaluation, and the score reported was considered the patient's headache severity.Patients also self-reported if they had engaged in exercise in the time between concussion and their initial clinic visit, or if they had experienced sleep problems during the same timeframe.Both questions were Yes/No responses.Engaging in exercise was broadly defined as participating in any form or intensity of exercise after injury.Specific exercise type, intensity, or duration were not known to the study team.Sleep problems similarly consisted of a broad range of sleep disturbances, including sleeping too much or too little, or having difficulties falling asleep or staying asleep.

Clinical outcomes
Patients received concussion management from their treating physician in accordance with current consensus recommendations, which included general instructions for brief cognitive and physical rest, followed by reintegration to physical activity and activities of daily living (e.g., school attendance) as tolerated (1,2,33).Follow-up care occurred periodically based on clinical need until physician clearance for full return to sports and physical activity.RTP decisions were made by the treating physician or by a school-based athletic trainer operating under the direction of the treating physician in line with current concussion consensus guidelines at the time of evaluation (1,2,33).At RTP visits, patients reported the last date they experienced concussion symptoms which were not present prior to injury (i.e., a return to pre-injury status).We calculated time to symptom resolution as the number of days between injury and patient-reported return to pre-injury status.We also dichotomized patients based on their time to symptom resolution.Patients with symptoms lasting for >28 days were grouped as those with persisting post-concussion symptoms (PPCS) and those who recovered sooner were grouped as those without PPCS.We calculated RTP clearance time as the number of days between injury and physician clearance to RTP.

Grouping variable
Patients were grouped according to the date of their injury.Concussions which occurred between the months of June and August in each year of data collection were grouped as 'summer month' injuries.Concussions sustained between September and May were grouped as 'school year' injuries.We recognize the inherent limitation in grouping by month, given summer school or other breaks during the school year.However, we selected this timeframe to align with the academic calendar of the local school districts in our region to the degree possible given the retrospective design of our study.Further, while some patients who sustained a concussion during the school year have not fully returned to the classroom at the time of initial post-concussion evaluation, school participation continues for the pediatric patient through other mechanisms, including at-home/make-up work.Given that the primary scope of our study was to assess the differences between school year and summer month concussions, we considered any form of school participation (in-classroom, virtual, or at-home) as presenting a potentially different environment for concussion recovery compared to summer months.A physical presence in the classroom may not be necessary to consider a patient participating in school activities, and absence from school days during the academic year could still present a challenging environment for the patient which may include at-home or make-up schoolwork assigned to (or waiting for) the recovering patient.

Statistical methods
Data are presented as mean (standard deviation) or median [interquartile range] for continuous variables and number included (corresponding percentage) for categorical variables.We first compared demographic, medical history, and concussion injury characteristics between groups using independent samples t-tests for continuous variables, and Chi-square analyses or Fisher's exact tests (for cell sizes <5) for categorical variables.Initial symptom presentation and clinical recovery outcomes were compared between groups using independent samples t-tests or Mann-Whitney U tests, depending on normality of data, and chi-square analyses.Effect sizes were calculated for median differences between groups using correlation coefficients (r) for Mann-Whitney U tests.We also calculated r 2 values indicating the percentage of the dependent variable explained by the independent variable (41).
We then constructed three multivariable linear regression models.Each model included a primary predictor of injury season (summer vs school year), as well as covariates of exercise at initial evaluation (yes/no) and endorsing sleep problems at initial evaluation (yes/no).The outcome for each model was patient-reported 1) total symptom burden on the HBI, 2) HBI somatic symptom burden, and 3) HBI cognitive symptom burden.
All analyses were two-sided and performed using Stata Statistical Software: Version 15 (StataCorp, LLC, College Station, TX, USA), and evaluated with a significance level of α = 0.05.Symptom domain (cognitive and somatic) comparisons were evaluated at a significance level of α = 0.025 in both univariable and multivariable models to adjust for multiple comparisons using variables derived from the same scale.

Results
A total of 1,269 patients were seen for a suspected concussion between 2015 and 2019.After exclusion, our sample consisted of n = 350 individuals, n = 83 (24%) of which sustained a concussion during summer months and n = 267 (76%) during the school year.A complete list of our exclusion criteria and the number of patients excluded under each criterion can be found in Figure 1 and the percentage of initial postconcussion evaluations performed in each month of the year is included in Table 1 and Figure 2.
Summer month and school year groups were similar in demographics, including age, sex, concussion history, and preinjury history of anxiety, depression, or sleep problems (Table 1).Time from injury to initial evaluation was also similar between groups (Table 1).Patients sustaining a concussion during summer months vs the school year were similar in proportion engaging in exercise or endorsing sleep problems in the time between injury and clinical evaluation (Table 1).Patients who sustained concussion during summer months reported significantly lower total HBI scores at initial evaluation than those injured during the school year (Figure 3a; effect size: correlation coefficient r = 0.12, r 2 = 0.015).Parent/legal guardian HBI scores mirrored that of their child's (Figure 3b; effect size: correlation coefficient r = 0.14, r 2 = 0.020).When evaluating patient-reported cognitive and somatic symptom sub-scores at initial evaluation, patients injured during the summer months reported significantly lower cognitive symptom burden (Figure 3d; effect size: correlation coefficient r = 0.13, r 2 = 0.016), but not somatic symptom burden (Figure 3c; effect size: correlation coefficient r = 0.11, r 2 = 0.012), compared to patients injured during the school year.After controlling for the effects of acute exercise and sleep problems, season of injury was a significant predictor of patient-reported total HBI score and cognitive, but not somatic (non-significant after adjustment for multiple comparisons) symptoms (Table 2).
Considering clinical recovery outcomes, groups did not differ significantly in symptom resolution time (Figure 4a; effect size: correlation coefficient r = 0.08, r 2 = 0.006).However, those who sustained a concussion during the summer months received physician clearance to RTP sooner than those with concussion during the school year (Figure 4b; effect size: correlation coefficient r = 0.12, r 2 = 0.014).

Discussion
The purpose of this study was to compare initial postconcussion symptom presentation and clinical recovery outcomes for pediatric patients who sustained concussion during summer months compared to the school year.Patients injured   during the school year demonstrated higher overall symptom burden initially post-concussion, than patients injured during the summer months, primarily due to increased cognitive symptoms.Prior work suggests that early return to school post-concussion is associated with reduced symptom burden in the sub-acute phase of recovery; however, this work is limited given that all patients in the sample were participating in school at the time of injury (26).Our results build on this past work, suggesting that sustaining concussion during the school year is associated with higher cognitive symptom burden.This is unsurprising given the increased cognitive load associated with academic and other school-related activities and further supports the use of return-to-learn strategies to facilitate successful reintegration to classroom activities during the school year.Sustaining a concussion during the summer was associated with a shorter time to RTP clearance, but not overall symptom resolution.Parent, child, and clinic schedules during the summer months may facilitate the process of obtaining physician appointments, thus partially explaining faster RTP time during the summer.Despite greater initial post-concussion symptom severity during the school year, time to symptom resolution was not different between groups.This is particularly interesting given existing work that has demonstrated a high prognostic value of initial symptom severity for predicting symptom resolution time in children with concussion (18)(19)(20)(21).Prior research has also shown that initial somatic, but not cognitive, symptom burden is a predictor of symptom resolution time in pediatric aged individuals (19).While total symptom burden was different between groups in our cohort, somatic symptom burden was not, potentially explaining why similar symptom resolution times were observed.
Secondarily, we did not observe any between-group differences in the proportion of those exercising or experiencing sleep problems in the time between concussion and initial clinic evaluation based on the season of injury.All patients were seen on average 8-9 days post-concussion, with fewer than 20% having engaged in exercise and approximately 30% experiencing sleep problems at that time.Although previous research has suggested a change in sleep and exercise patterns for healthy children during the summer (42,43), our results indicate that engagement in exercise and endorsement of sleep problems may be more similar than different in the sub-acute recovery period for patients with concussion.It is possible that time of year is a relatively unimportant factor for sleep or exercise in children with concussion, given the range of other symptoms and functional deficits experienced acutely postconcussion which are likely to have a much larger impact on sleep quality or propensity for exercise.However, in later stages of recovery when exercise is better tolerated and the likelihood of experiencing sleep problems is reduced, school participation may become a more influential factor.Future research should use more objective assessments of sleep and physical activity, such as wearable devices or self-report surveys with stronger internal validity than employed in this study.
Last, we aimed to understand the effect of injury season on symptom presentation after controlling for the effects of Table 2.Each row of the below table represents the results of a separate multivariable linear regression model.Each model included a primary predictor of season of injury (summer vs school year) and covariates of exercising at initial evaluation (yes/no) and experiencing sleep problems at initial evaluation (yes/no).The outcome for each model was (1) patient-reported symptom score (2), somatic symptom score, and (3) cognitive symptom score.Beta coefficients, 95% confidence intervals of the beta coefficient, and associated p-values reflect the association between our primary predictor (season of injury) and the outcome variable listed in the table, after controlling for the effects of exercise and sleep problems.exercise engagement and sleep problems in the sub-acute recovery period.Sustaining a concussion during the school year was a significant predictor of total and cognitive symptom burden after controlling for exercise engagement and sleep problems.This potentially indicates that although cognitive symptoms, and thus total symptoms, are more prominent for patients sustaining concussion during the school year, this is not related to changes in exercise or sleep which parallel the shift from summer to school year.Rather, additional factors related to the presence or absence of school participation, such as increased cognitive load, stress, peer relations, or other life situations are potentially more influential on the cognitive symptom exacerbation observed between summer and school year concussions than sleep or exercise.

Clinical impact
Clinicians treating patients with concussion may consider the impact of injury season on post-concussion symptom presentation and RTP timing.Patients presenting for care during the school year may demonstrate higher cognitive and overall symptom burden initially post-concussion, but these elevated values are not expected to limit exercise ability or exacerbate sleep problems in the sub-acute time frame, or delay symptom resolution.However, for concussions sustained during the school year, special attention may be required for RTP clearance to prevent delays in returning to pre-injury levels of physical activity and sports participation.The results of our study advance our understanding of the role of seasonality, and by proxy school participation, in influencing initial cognitive symptoms in children with concussion and add critical information to the literature as it relates to post-concussion sleep and exercise between summer months and the school year.Prior work has emphasized the importance of early return to school (26), and the results of this study do not justify complete removal from classroom activities altogether (of which may be detrimental to recovery) (26), but rather further support the use of return-to-learn protocols to reduce the potential cognitive burden of school participation for students reintegrating to classroom activities during the school year.

Study limitations
Our results should be interpreted within the context of limitations.Foremost, our data represent a retrospective investigation conducted at a single institution with clinical sites in one geographic area.The results of this study may best generalize to other regions with similar school structures.Additionally, patients were grouped based on time of year, as this was the best data available to answer our primary research question.It is possible that school activities took place during summer months for some individuals, or that school participation was paused at times throughout the school year, such as during fall, winter, or spring breaks.Future research should more accurately measure school participation to better understand the relationships identified in this study.The retrospective nature of this study also does not allow for more granular investigation of factors with possible differences in summer vs school year months.For example, engaging in exercise or experiencing sleep problems since injury was collected dichotomously (yes/no).Thus, we are unable to investigate nuanced differences in exercise or sleep behaviors between seasons of injury, such as exercise intensity or sleep efficiency.Last, the season of injury (school year vs summer month) is likely not as influential for patient outcomes as other covariates not measured in this study, such as added cognitive load, life stress, or changes in quality of life, which may accompany the seasonal change from school year to summer months.Future research on this topic should measure such factors directly, rather than using the season of injury as a proxy, as was the case in this study.

Conclusions
Pediatric patients with concussion may present initially with greater cognitive symptoms during the school year, compared to summer months.This relationship is not explained by exercise or sleep in the sub-acute phase of recovery, as these factors were similar regardless of the time of year in which injury occurred.Return-to-learn protocols may be particularly useful to reduce cognitive symptom provocation and facilitate a successful return to school for patients during the school year.

Figure 1 .
Figure 1.Assessment of inclusion and exclusion criteria, separated as criteria assessed for inclusion in the data set and criteria assessed prior to statistical analysis.

Figure 2 .
Figure 2. Heat map describing the rates of concussion throughout the calendar year (summed across all years of data collection, 2015-2019).Darker colors represent more injuries sustained on that date (range: 0-7; median = 1).

Figure 3 .
Figure 3. Symptom rating at initial evaluation, reported by (a) the patient and (b) the parent/caregiver, as well as patient-reported symptom rating for (c) somatic and (d) cognitive domain ratings.Data are presented as median (center dot with label, with corresponding number included) and interquartile range (box around the median, number in brackets).The shaded area represents the probability density of data at each level of the scale, smoothed using a kernel density estimator.

13 *
Negative coefficients indicate fewer symptoms during the summer months, compared to the school year.**Alpha level adjust to α=0.025 to account for multiple comparisons.

Figure 4 .
Figure 4. Time from injury to (a) symptom recovery and (b) return to play clearance for patients sustained a concussion during the summer vs. school months.Data are presented as median (center dot with label, with corresponding number included) and interquartile range (box around the median, number in brackets).The shaded area represents the probability density of data at each level of the scale, smoothed using a kernel density estimator.

Table 1 .
Comparison of patient characteristics among those who sustained a concussion during the summer (June-August) vs.The school year (September-May).