Symptom and clinical recovery outcomes for pediatric concussion following early physical activity

Benjamin M. KraininDepartment of Family Medicine, University of Colorado School of Medicine, Aurora;
Department of Emergency Medicine, University of Colorado School of Medicine, Aurora;

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Corrine N. SeehusenSports Medicine Center, Children’s Hospital Colorado, Aurora;

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Katherine L. SmulliganDepartment of Orthopedics, University of Colorado School of Medicine, Aurora; and

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Mathew J. WingersonSports Medicine Center, Children’s Hospital Colorado, Aurora;
Department of Orthopedics, University of Colorado School of Medicine, Aurora; and

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Julie C. WilsonSports Medicine Center, Children’s Hospital Colorado, Aurora;
Department of Orthopedics, University of Colorado School of Medicine, Aurora; and
Department of Pediatrics, University of Colorado School of Medicine, Aurora, Colorado

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David R. HowellSports Medicine Center, Children’s Hospital Colorado, Aurora;
Department of Orthopedics, University of Colorado School of Medicine, Aurora; and

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OBJECTIVE

Recent research supports initiating physical activity as soon as 24 to 48 hours after concussion to reduce persistent postconcussive symptoms. However, this practice has not been widely adopted. The objective of this study was to evaluate the association of early physical activity with patient-reported and functional outcomes for pediatric patients following a concussion.

METHODS

A retrospective cohort of patients who presented to a pediatric sports medicine clinic (48% female, mean age14.3 ± 2.6 years, and mean 9.8 ± 5.7 days postconcussion) were evaluated. Patients were grouped based on whether they reported engaging in physical activity prior to presenting to the clinic. Patient- and parent-reported symptom frequency (Health and Behavior Inventory), 11 different clinical outcomes (including missed school, memory recall, and balance assessments), the presence of symptoms persisting beyond 28 days, and a subgroup analysis of those patients receiving exercise versus symptom-limiting activity prescriptions were examined. Outcomes were compared between physical activity groups using the Mann-Whitney U-test and the chi-square test. To adjust for the effect of potential confounders, a logistic binary regression model was constructed.

RESULTS

In total, 211 pediatric patients were included, 35 (17%) of whom reported early physical activity. A greater proportion of the no physical activity group reported a headache (85% vs 60%, p = 0.001). The no physical activity group also reported higher patient-reported (23.1 ± 13.4 vs 15.0 ± 13.4, p < 0.001) and parent-reported (19.4 ± 12.7 vs 11.2 ± 10.3, p = 0.001) symptom frequency at the initial visit. The early physical activity group had a lower proportion of patients with persistent symptoms (44% vs 22%, p = 0.02) and a shorter time to symptom resolution (15.6 ± 12.4 days vs 27.2 ± 24.2 days, p = 0.02). After adjusting for potential confounders, early physical activity was associated with 5.8 lower odds of experiencing persistent symptoms (adjusted OR 5.83, 95% CI 2.05–16.61; p = 0.001).

CONCLUSIONS

A significant association between early physical activity and decreased symptom burden was observed. A lower proportion of those patients who engaged in early physical activity experienced persistent symptoms 28 days postinjury. However, low rates of early physical activity prior to the initial clinic visit were also observed, indicating that this approach may not be well known by acute care or primary care providers, or is not widely adopted by patients and families.

ABBREVIATIONS

ED = emergency department; HBI = Health and Behavior Inventory; mBESS = modified Balance Error Scoring System; NPC = near point of convergence; PPCS = persistent postconcussion symptoms; RTP = return to play; SCAT5 = Sport Concussion Assessment Tool, 5th Edition.

OBJECTIVE

Recent research supports initiating physical activity as soon as 24 to 48 hours after concussion to reduce persistent postconcussive symptoms. However, this practice has not been widely adopted. The objective of this study was to evaluate the association of early physical activity with patient-reported and functional outcomes for pediatric patients following a concussion.

METHODS

A retrospective cohort of patients who presented to a pediatric sports medicine clinic (48% female, mean age14.3 ± 2.6 years, and mean 9.8 ± 5.7 days postconcussion) were evaluated. Patients were grouped based on whether they reported engaging in physical activity prior to presenting to the clinic. Patient- and parent-reported symptom frequency (Health and Behavior Inventory), 11 different clinical outcomes (including missed school, memory recall, and balance assessments), the presence of symptoms persisting beyond 28 days, and a subgroup analysis of those patients receiving exercise versus symptom-limiting activity prescriptions were examined. Outcomes were compared between physical activity groups using the Mann-Whitney U-test and the chi-square test. To adjust for the effect of potential confounders, a logistic binary regression model was constructed.

RESULTS

In total, 211 pediatric patients were included, 35 (17%) of whom reported early physical activity. A greater proportion of the no physical activity group reported a headache (85% vs 60%, p = 0.001). The no physical activity group also reported higher patient-reported (23.1 ± 13.4 vs 15.0 ± 13.4, p < 0.001) and parent-reported (19.4 ± 12.7 vs 11.2 ± 10.3, p = 0.001) symptom frequency at the initial visit. The early physical activity group had a lower proportion of patients with persistent symptoms (44% vs 22%, p = 0.02) and a shorter time to symptom resolution (15.6 ± 12.4 days vs 27.2 ± 24.2 days, p = 0.02). After adjusting for potential confounders, early physical activity was associated with 5.8 lower odds of experiencing persistent symptoms (adjusted OR 5.83, 95% CI 2.05–16.61; p = 0.001).

CONCLUSIONS

A significant association between early physical activity and decreased symptom burden was observed. A lower proportion of those patients who engaged in early physical activity experienced persistent symptoms 28 days postinjury. However, low rates of early physical activity prior to the initial clinic visit were also observed, indicating that this approach may not be well known by acute care or primary care providers, or is not widely adopted by patients and families.

In Brief

Researchers examined the association between physical activity after a sport-related concussion and a set of multimodal, clinically oriented outcomes. Patients who reported engaging in early physical activity reported less symptom frequency and had a lower incidence of persistent postconcussion symptoms compared with patients who reported no early physical activity. These findings were in agreement with prior observations related to the potential benefit of activity after concussion, but further investigation is required to identify casual effects.

Concussions can affect children and adolescents in many ways, including somatic symptoms (e.g., headache and fatigue), cognitive difficulties (e.g., memory and confusion), behavioral changes (e.g., irritability and unsteadiness), or sleep difficulties.1 Concussions may present differently across various developmental stages, where adolescents may present with more symptoms than their older or younger counterparts.2 Although concussion symptoms are frequently used to measure recovery, they have limitations inherent to their self-reported nature and may not accurately reflect physiological recovery.3 As a result, objective clinical measures are often used to aid clinicians in concussion management. These measures of recovery vary across clinical environments but often include test instruments such as the Sport Concussion Assessment Tool, 5th Edition (SCAT5).4,5 Objective deficits may persist beyond symptom resolution as well, creating another challenge for measuring recovery.3 Though no clear consensus exists to define physiological concussion recovery, objective measurements can guide patients, families, and multidisciplinary teams collectively during concussion recovery.

Research over the past decade has generally supported initiation of physical activity soon after concussion to facilitate better postconcussion outcomes. Initiating physical activity after a brief 24- to 48-hour postinjury rest period has been promoted more recently in clinical practice, existing studies, and expert consensus statements.1,69 These recommendations may not be widely adopted,10 despite research showing an association between early physical activity and a reduction in persistent postconcussion symptoms (PPCS).11,12 Additionally, early assessment of exercise tolerance can help clinicians predict individuals who may develop PPCS.13 Furthermore, individuals who participated in early physical activity after sustaining a concussion were observed to have decreased presence of headache, less-frequent concussion symptoms, and better postural stability outcomes compared with those who did not.10 Evaluating a multimodal array of clinical outcomes, including subjective and objective measures, may provide a more comprehensive picture of how early physical activity after a concussion is associated with clinical presentation. Understanding the relationship between early physical activity after a concussion and objective measures such as cognitive performance and postural stability may provide useful clinical information for individualizing treatment.

The purpose of this study was to evaluate how patient-reported outcomes, clinically obtained outcomes, and clinical recovery are associated with initiating physical activity before the initial visit (early physical activity) to a pediatric sports medicine clinic. Secondarily, we sought to describe physician recommendations for physical activity and/or exercise at the initial clinic visit and whether these recommendations were associated with return-to-play (RTP) clearance timing. We hypothesized that early physical activity would be associated with less-severe symptoms, fewer days of school missed, and faster recovery. With respect to clinically obtained outcomes, we hypothesized that patients who engaged in early physical activity would have better memory task performance and postural stability performance. Finally, we hypothesized that children reporting early physical activity would achieve symptom resolution and receive RTP clearance sooner than those who did not report early physical activity.

Methods

Study Design and Patients

A retrospective study of data obtained via a clinical registry of patients seen for concussion at the Children’s Hospital Colorado Sports Medicine Center was conducted. We investigated patients who presented for care between January 1, 2019, and December 31, 2019, and were seen for an initial concussion evaluation within 21 days of injury. Based on the most recent consensus statement on concussion in sport available at the time of the study (Berlin 2016), we defined concussion as a traumatic brain injury caused by forces transmitted to the head, resulting in neurological dysfunction, presenting with a variety of signs or symptoms, with or without loss of consciousness.1 Patients aged 6 to 18 years who were diagnosed with a concussion by a board-certified pediatric sports medicine physician were included. A total of 283 patients were evaluated during the study period and met criteria for screening to be included in the current study. Patients were excluded if they were initially assessed > 21 days postconcussion (n = 36), diagnosed with a closed head injury but the injury did not meet the diagnostic criteria of a concussion as discussed above (n = 11), asymptomatic at the time of initial assessment (n = 10), seen by a non–sports medicine physician (n = 7), present for care of a second head injury prior to recovery from the initial concussion (n = 5), found to have an abnormality on neuroimaging (n = 2), and older than 18 years of age (n = 1). Therefore, 211 patients were included in this study. Information regarding the referral source, such as from a primary care provider or the emergency department (ED), was gathered from a telephone encounter at the time of scheduling the initial sports medicine clinic visit. The study was approved by the IRB prior to commencement.

Grouping Variable

Patients were grouped into those who reported engaging in physical activity after sustaining a concussion but prior to the initial sports medicine clinic visit (early physical activity group) and those who did not (no physical activity group). This designation was based on a response to a question asked on the intake form for the initial clinic visit. “Since your injury, have you done any physical activity/exercise?” If the patient answered yes, we classified their specific self-reported type and level of activity to one of the 6 corresponding stages of the graduated RTP strategy put forth by the latest Berlin consensus statement on concussion in sport.1,6 We also obtained specific recommendations provided by the treating sports medicine physician after the initial assessment was complete and classified their recommendations as either a specific exercise recommendation or guidance to perform activity that does not exacerbate symptoms.

Clinical Outcomes

Both patients and their parents completed the Health and Behavior Inventory (HBI), a 20-item symptom frequency questionnaire addressing common concussion symptoms.14 We asked patients and their parents to rate current concussion symptoms as well as retrospectively rate symptoms on the day of injury using a 4-point scale, ranging from 0 (never experiencing the symptom) to 3 (experiencing the symptom often).14 Patient and parent scores were separately calculated as the sum of all responses, with a maximum score of 60.14 We included both patient- and parent-reported HBI scores because, although the degree of correlation between parents and patients is high, both offer insightful sources of information, particularly among children 12 years of age and younger when compared with adolescents.15 As headache is the most commonly reported symptom of a concussion10,16,17 and reduced presence of headache has been associated with early physical activity,10 we also assessed the presence of current headache (yes or no) and headache severity as separate data points. During the evaluation, patients rated their headache severity on a scale of 0 (not experiencing) to 10 (most severe headache possible).

To investigate how early physical activity was associated with performance on a multimodal set of outcomes, several elements from the SCAT5 were examined.6 Specifically, we included immediate and delayed word recall (using a 10-word list, used only for patients ≥ 12 years of age), digits backward task, and the modified Balance Error Scoring System (mBESS). Elements of the SCAT5 were administered by our Sports Medicine Center athletic training staff in accordance with the standard instructions.4 During mBESS administration, patients were instructed to maintain balance for 20 seconds in double-limb, single-limb, and tandem-limb stances on a solid surface with eyes closed and hands on hips; errors were counted by the athletic training staff during each 20-second trial.18,19 Errors included hip abduction > 30°, falling out of position, being unable to reestablish the testing position for > 5 seconds, opening eyes, and taking hands off hips.5

Participants also completed timed single- and dual-task tandem gait tests as well as tasks to measure the near point of convergence (NPC), which have been used in other studies and are part of our standard-of-care clinical assessment.4,20 NPC was measured using a commercially available ruler (Gulden Ophthalmics).21 A card with a vertical line of letters, printed in Times New Roman size 6 font, was brought toward the patient’s nose at a speed of 1 cm per second. Patient-reported diplopia or noted deviation of either eye (i.e., the break point) was recorded by an athletic trainer as the distance of the NPC, and the average distance of 2 trials was calculated as the outcome of interest.22 For the tandem gait test, patients walked in a heel-toe manner down and back along a 3-m strip of fabric taped to the floor. Athletic trainers recorded the total time it took for patients to complete the test. Patients completed 3 trials under single-task conditions and 3 trials under dual-task conditions (with a simultaneous cognitive task), and the mean time for each condition was calculated for further analysis. Cognitive tasks performed during dual-task conditions included spelling five-letter words backward, performing serial subtraction (subtracting by 6 or 7 from a random two-digit number, depending on age), or reciting months in reverse order beginning with a random month.22

Recovery Outcomes

Patients returned for follow-up care as specified by their treating physician. At each visit, they completed the HBI. As noted in previous pediatric concussion studies, we designated symptom resolution as an HBI score of 0.10 If their symptoms resolved prior to the follow-up visit, we asked them to provide the last day that they experienced symptoms and calculated the time from injury to symptom resolution. PPCS were defined as those having a duration > 28 days after the concussion, which is consistent with previous definitions of persistent symptoms in this age group.11,23,24 Patients whose follow-up occurred > 28 days postconcussion who were still symptomatic were classified as having PPCS. We also obtained the time from the concussion to RTP clearance.

Statistical Analysis

Continuous variables are presented as mean (standard deviation), and categorical variables are presented as the number included and corresponding percentage. Differences in demographic and medical history characteristics between the early and no physical activity groups were assessed using the independent-samples t-test and the chi-square test or the Fisher’s exact test. We then examined the interaction between, and main effects of, group (early physical activity vs no early physical activity) and time (day of injury vs day of initial clinic visit) on patient- and parent-reported HBI scores using a 2 × 2 repeated-measures ANOVA. If there was a significant interaction (defined as p < 0.05), we assessed potential differences between groups at each time point using pairwise follow-up comparisons and defined statistical significance as p < 0.025 to adjust for multiple comparisons. Clinically obtained outcomes from the initial clinic visit were then compared between groups using the independent-samples t-test and the chi-square test.

Finally, we compared outcomes between physical activity groups and between those patients who were provided an exercise versus symptom-limited activity recommendation at the initial clinic visit, using the Mann-Whitney U-test and the chi-square test. To adjust for the effect of potential confounders, a logistic binary regression model was constructed. The outcome of interest was PPCS (yes or no), and patient characteristics that differed between groups at a level of p < 0.10 were included as covariates. Significance was determined using an alpha level of p = 0.05. All statistical analyses were two-sided and performed using Stata version 15 (StataCorp.).

Results

In total, 211 patients were included in our analysis; 35 patients (17%) reported early physical activity after a concussion and prior to the initial clinic visit, which, in this sample, occurred at a mean of 9.8 days (SD 5.7 [range 1–21 days]) postconcussion. Those patients who reported early physical activity were seen approximately 2 days later postinjury than those who did not report early physical activity, and a higher proportion of the no early physical activity group reported loss of consciousness at the time of injury (Table 1); thus, these two variables were included as covariates in multivariable analyses. Other demographic characteristics were not significantly different between the groups (Table 1).

TABLE 1.

Comparison of patient characteristics between the early physical activity group and the no early physical activity group at the initial clinic visit

VariableEarly PA Group (n = 35)No Early PA Group (n = 176)p Value
Mean age, yrs13.8 (2.9)14.4 (2.6)0.22
Female sex20 (57)81 (46)0.23
Mean time from injury to assessment, days11.9 (5.7)9.4 (5.6)0.01
Referral source0.70
 PCP20 (57)87 (49)
 Athletic trainer6 (17)35 (20)
 ED4 (11)32 (18)
 Self3 (9)17 (10)
 Other2 (6)5 (3)
Mean height, cm153.5 (22.9)158.6 (19.5)0.27
LOC at time of injury2 (6)35 (20)0.05
History of prior concussion 18 (51)79 (45)0.48
History of migraines or headaches9 (26)65 (37)0.20
Presence of preinjury learning disability1 (3)13 (7)0.47
History of anxiety2 (6)25 (14)0.27
History of depression2 (6)15 (9)0.74
Sport-related concussion27 (77)133 (76)0.84
Insurance status0.71
 Public5 (14)37 (21)
 Private30 (86)134 (76)
 Not reported0 (0)5 (3)
Race
 American Indian or Alaska Native0 (0)3 (2)>0.99
 Asian0 (0)6 (3)0.59
 Black or African American2 (6)7 (4)0.65
 Native Hawaiian or other Pacific Islander0 (0)5 (3)0.59
 White28 (80)129 (73)0.41
 Unknown or not reported3 (9)16 (9)0.40
 More than one race2 (6)10 (6)>0.99
Ethnicity0.15
 Hispanic3 (9)35 (20)
 Not Hispanic29 (83)133 (76)
 Not reported3 (9)8 (5)
PA level at initial visit*
 Stage 12 (6)NA
 Stage 211 (31)NA
 Stage 315 (43)NA
 Stage 46 (17)NA
 Stage 51 (3)NA
 Stage 60 (0)NA

LOC = loss of consciousness; NA = not applicable; PA = physical activity; PCP = primary care provider.

Values represent the number of patients (%) or mean (SD) unless indicated otherwise. Patients who reported early physical activity were seen approximately 2 days later postinjury than those who did not report early physical activity, and a higher proportion of the no early physical activity group reported loss of consciousness at the time of injury; thus, these two variables were included as covariates in multivariable analyses.

Based on the Berlin consensus statement on concussion in sport guidelines.

For patient-reported (Fig. 1A) and parent-reported (Fig. 1B) HBI symptom frequency ratings, there was a significant effect of group (p < 0.001 and p = 0.001, respectively) and time (p < 0.001 and p < 0.001, respectively), but no significant interaction effect (p = 0.42 and p = 0.88, respectively). Specifically, the early physical activity group reported significantly lower HBI scores for both the parent and patient report than the no physical activity group across both time points, and both groups had lower mean HBI scores during the initial clinic visit compared with their report of the acute postinjury symptom burden (Fig. 1). Additionally, a smaller proportion of the early physical activity group reported experiencing a headache during the initial clinic visit compared with the no physical activity group (Table 2). Clinically obtained outcomes, such as immediate or delayed memory recall, digits backward, single- and dual-task tandem gait, and postural stability were not significantly different between groups (Table 2).

FIG. 1.
FIG. 1.

Line graphs showing patient-reported (A) and parent-reported (B) HBI symptom frequency scores. At the initial clinic visit, participants were asked to rate their symptom frequency at the time of injury and currently. The circles (early physical activity group) and squares (no early physical activity group) represent the group mean, and the error bars indicate the 95% CI for the mean.

TABLE 2.

Comparison of clinical outcomes between the early physical activity group and the no early physical activity group at the initial clinic visit

VariableEarly PA GroupNo Early PA Groupp Value
Missed school due to concussion24 (69)141 (80)0.13
Currently experiencing a headache21 (60)150 (85)0.001
Mean headache severity3.3 (2.1)4.2 (2.4)0.10
Mean immediate recall outcome (words correct)6.7 (1.8)7.0 (1.9)0.38
Mean delayed recall outcome (words correct)5.3 (1.9)5.2 (2.2)0.86
Mean digits backward outcome4.5 (1.3)4.1 (1.2)0.07
Mean mBESS error6.9 (5.7)7.5 (5.0)0.56
Mean single-task tandem gait time, sec21.4 (7.0)24.6 (10.4)0.11
Mean dual-task tandem gait time, sec29.6 (8.8)33.5 (13.3)0.12
Mean dual-task cognitive accuracy (% correct)74.3 (27.7)81.1 (18.5)0.09
Mean NPC break point, cm8.6 (6.1)8.7 (6.9)0.97

Values represent the number of patients (%) or mean (SD) unless indicated otherwise.

A significantly smaller proportion of the early physical activity group experienced PPCS than the no early physical activity group, and the early physical activity group demonstrated a shorter mean time from the injury to symptom resolution (Table 3). After adjusting for the effect of age, time from injury to initial clinic visit, and loss of consciousness at the time of injury, no physical activity before the initial clinic visit was associated with 5.8 higher odds of experiencing PPCS (adjusted OR 5.83, 95% CI 2.05–16.61; p = 0.001).

TABLE 3.

Comparison of recovery outcomes between the early physical activity and no early physical activity groups

VariableEarly PA GroupNo Early PA Groupp Value
Presence of PPCS, n (%) 7/32 (22)65/149 (44)0.02
Mean symptom resolution time, days15.6 (12.4)27.2 (24.2)0.02
Mean RTP clearance time, days24.2 (15.7)36.7 (40.6)0.13

Symptom resolution and RTP clearance time were not available for 3 patients (9%) in the early physical activity group and for 27 patients (15%) in the no early physical activity group.

When comparing outcomes among patients who were provided a specific exercise recommendation (n = 117) versus a general recommendation to limit symptom-exacerbating activity at the initial visit (n = 94), no significant differences in clinical outcomes were found. Specifically, the proportion of persistent symptoms, HBI scores, and recovery time outcomes were not significantly different (Table 4).

TABLE 4.

Comparison of patients who received a recommendation for exercise at the initial sports medicine clinic visit with patients who received a recommendation for limiting physical activity that would exacerbate symptoms

VariableReceived Recommendation for Exercise (n = 117)Received Recommendation to Limit Symptom-Exacerbating Activity (n = 94)p Value
Mean time from injury to initial visit, days9.9 (5.6)9.7 (5.8)0.82
PPCS, n (%)*39 (39)33 (41)0.76
Mean time to symptom resolution, days24.7 (24.5)25.4 (20.9)0.86
Mean time to RTP clearance, days37.3 (47.2)31.3 (20.9)0.34
Mean HBI score at the time of injury28.5 (14.2)29.5 (12.4)0.59
Mean HBI score at the initial visit21.4 (14.5)22.8 (12.1)0.46

Symptom resolution time data were not available for 30 patients (16 received recommendation for exercise, 14 received recommendation to limit symptom-exacerbating activity).

Discussion

We observed that early physical activity after pediatric concussion was associated with less-frequent concussion symptoms as reported by both the patient and their parent. Additionally, those who reported early physical activity had lower odds of experiencing persistent symptoms. While interesting, our study design was not equipped to infer causality from these findings. Patients who were feeling better early during concussion recovery may have simply been more likely to initiate early physical activity, or there may have been some therapeutic effect of the early physical activity, which could have conceivably contributed to a lower symptom burden or faster symptom resolution time. Interestingly, there were no statistically significant differences between the two groups with respect to clinically obtained outcomes during their sports medicine clinic evaluation. Collectively, our results corroborate prior research that has observed that recommendations centered on early physical activity engagement after concussion, at the least, are not detrimental for pediatric patients.8,10,11,13

Similar to prior studies, we found that patients who initiated early physical activity also reported lower HBI scores during the initial visit.10,11 It is important to note, however, that both patient- and parent-reported HBI scores in the early physical activity group were significantly lower than those of the no early physical activity group based on their recall of symptom burden on the date of injury and during the initial clinic visit (Fig. 1). Thus, patients with higher HBI scores could be more inclined to limit their own activity due to a greater symptom burden.25 Ultimately, the goals of concussion management are to reduce the initial symptom burden and facilitate a safe return to academic and athletic activities.1,6 Previous research has demonstrated the safety of early physical activity, even if it did not result in statistically significant changes in recovery times.13,26–28 Consistent with previous studies, our early physical activity group had significantly lower odds of developing PPCS and a reduced time to symptom resolution compared with those who did not initiate early physical activity.8,11 Our study supports clinician-guided early physical activity for patients following a concussion, given the potential benefit to recovery, without any decrement in patient-reported or functional outcomes.

Our early physical activity group did not demonstrate better performance across a multimodal battery of common clinical assessments. Previous research has indicated that early physical activity was associated with better balance control10 and better neurocognitive function.25 However, in the current study, the early physical activity group reported variable levels of early activity, and this heterogeneity may be one reason we saw limited consistency across our testing outcomes. Given that the majority of patients in our study reported physical activity at stage 3 or lower, according to the graduated RTP strategy1 (sport-specific exercise, light aerobic exercise, or symptom-limited activity), this level of activity may not have been sufficient to elicit an effect on cognitive or postural stability outcomes. One study of adult patients who presented to the ED with a concussion and who were prescribed light exercise found no difference in recovery outcomes.29 Therefore, light physical activity may have less of an effect on recovery than a higher dose of exercise that is prescribed with specific elements to guide the patient, such as exercise intensity, volume, and frequency.30 The American Academy of Pediatrics position statement on sport-related concussion recommends limiting exertion during recovery to a subsymptom threshold, such as brisk walking, but avoiding complete inactivity while symptomatic.31 The level of activity we observed is in line with these recommendations, but further investigation is required to better understand precise dosage associated with exercise that could lead to better outcomes after a concussion. Additional studies have demonstrated that moderate exertion levels were associated with improved symptoms and objective outcomes,25 along with an expedited RTP.32 Future studies may consider prospectively evaluating the effect of prescribed early physical activity during recovery and closely measuring exercise intensity, volume, and frequency to help elucidate how to maximize the benefits of early physical activity.

Following initial assessment in the sports medicine clinic, patients were given an activity recommendation in line with current guidelines,1,6,7,10,11 either a clinician-specific exercise recommendation or a recommendation to resume physical activity that does not exacerbate symptoms. Of those patients in our cohort who received early physical activity instructions from a sports medicine physician, 94% had already begun at least light aerobic exercise, with only 1 patient reaching the equivalent of stage 5 of the Berlin recommendations at the time of their initial visit.1 Our results indicate that there is exercise recommendation variability present within a single practice of sports medicine physicians. These recommendations were likely dependent on clinical presentation of the patient and individualized decision-making by each physician.6 Despite the exercise recommendation heterogeneity, our study adds to the growing body of literature recommending a stepwise, balanced approach to increasing physical exertion and limiting strict rest early in the recovery process after a concussion.

Approximately 17% of our cohort initiated early physical activity prior to the initial clinic visit, which is a small increase from previous reports (13%).10 Those patients in the no physical activity group were seen nearly 10 days after their initial injury, suggesting that patients far exceeded the current maximum rest recommendations of 24 to 48 hours by multiple organizations.1,6,7 The relatively low frequency of patients initiating early physical activity in our cohort highlights some of the challenges the medical community may be facing with initial concussion management due, in part, to multiple entry points into the healthcare system. In their 2011 study, the Centers for Disease Control and Prevention found an increase of 57% to 200% in ED visits for recreational concussions between 2001 and 2009 in persons aged 8 to 19 years.33 Additionally, in 2016, Arbogast and colleagues found that 75% of 5- to 17-year-old patients went through their pediatricians as the point of entry for concussion management.34 With ever-increasing numbers of children and adolescents experiencing concussion, priority should be placed on expanding and sharing knowledge among clinicians in the primary care and emergency settings regarding the benefits of early physical activity, as many patients will not receive care at a specialty sports medicine clinic.

Limitations

There are several limitations to our study. First, retrospective studies inherently cannot prove causation; therefore, we cannot definitively state that early physical activity resulted in improved HBI scores and faster time to symptom resolution. This study also has a significant referral bias, as it was limited to a specialty pediatric sports medicine clinic in a single geographic area. Other parts of the country may have a higher adoption rate of early physical activity or different practice patterns. Furthermore, patients with more significant injury patterns may have been referred to our specialty clinic, making our results less applicable to clinicians treating patients in other settings. Additionally, categorizing the level of activity for early physical activity patients was limited based on the data available in the clinical registry and patient medical records. This makes it difficult to do a subgroup analysis and determine recovery trajectories of the cohort based on their level of physical activity prior to the initial clinic visit. There is also a risk of recall bias among patients with regard to reporting their symptoms on the day of injury. Those who felt better at the time of their sports medicine clinic evaluation might have downplayed the initial frequency of symptoms that they experienced a week or more prior to the visit. The dichotomization of patients into early physical activity or no physical activity groups was based on self-reporting, thereby limiting the objective nature of distinguishing the two groups. Finally, clinicians did not prescribe activity uniformly to patients during their first clinic visit, and we were unable to know whether patients adhered to the exercise recommendation.

Conclusions

Patients who engaged in early physical activity were more likely to report less-frequent concussion symptoms and had a lower incidence of PPCS compared with those who did not engage in early physical activity. Early physical activity was not associated with improved clinical outcomes. Overall, relatively low rates of early physical activity were seen in our cohort (17%) despite recent evidence and consensus statements which have recommended use of early physical activity after concussion, indicating that this approach may not be widespread in our immediate medical community. Sharing knowledge among clinicians across healthcare settings about early physical activity in order to enhance concussion counseling and recovery is recommended.

Acknowledgments

Dr. Howell has received research support from the Eunice Kennedy Shriver National Institute of Child Health and Human Development (grant no. R03HD094560), the National Institute of Neurological Disorders and Stroke (grant nos. R01NS100952 and R43NS108823), MINDSOURCE Brain Injury Network, and the Tai Foundation.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: all authors. Acquisition of data: Howell, Krainin, Seehusen, Wingerson, Wilson. Analysis and interpretation of data: Howell, Krainin, Smulligan, Wingerson, Wilson. Drafting the article: Krainin. Critically revising the article: Howell, Seehusen, Smulligan, Wingerson, Wilson. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Howell. Statistical analysis: Howell, Smulligan, Wingerson. Study supervision: Howell.

Supplemental Information

Previous Presentations

An electronic poster of the abstract was presented at the 2021 American Medical Society of Sports Medicine’s 30th Annual Meeting, April 13–18, 2021, held virtually.

References

  • 1

    McCrory P, Meeuwisse W, Dvořák J, Aubry M, Bailes J, Broglio S, et al. Consensus statement on concussion in sport–the 5th international conference on concussion in sport held in. Berlin, October 2016.Br J Sports Med. 2017;51(11):838847.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Moser RS, Davis GA, Schatz P. The age variable in childhood concussion management: a systematic review. Arch Clin Neuropsychol. 2018;33(4):417426.

  • 3

    Kamins J, Bigler E, Covassin T, Henry L, Kemp S, Leddy JJ, et al. What is the physiological time to recovery after concussion? A systematic review. Br J Sports Med. 2017;51(12):935940.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Echemendia RJ, Meeuwisse W, McCrory P, et al. The Sport Concussion Assessment Tool 5th Edition (SCAT5): Background and rationale. Br J Sports Med. 2017;51(11):848850.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Hunt TN, Ferrara MS, Bornstein RA, Baumgartner TA. The reliability of the modified Balance Error Scoring System. Clin J Sport Med. 2009;19(6):471475.

  • 6

    Harmon KG, Clugston JR, Dec K, Hainline B, Herring SA, Kane S, et al. American Medical Society for Sports Medicine position statement on concussion in sport. Clin J Sport Med. 2019;29(2):87100.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    The Management of Concussion-mild Traumatic Brain Injury Working Group. VA/DoD clinical practice guideline for the management of concussion—mild traumatic brain injury. Version 2.0. Department of Veterans Affairs. Published online February 2016. https://www.healthquality.va.gov/guidelines/rehab/mtbi/mtbicpgfullcpg50821816.pdf

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Leddy JJ, Haider MN, Ellis MJ, Mannix R, Darling SR, Freitas MS, et al. Early subthreshold aerobic exercise for sport-related concussion: a randomized clinical trial. JAMA Pediatr. 2019;173(4):319325.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Schneider KJ, Leddy JJ, Guskiewicz KM, Seifert T, McCrea M, Silverberg ND, et al. Rest and treatment/rehabilitation following sport-related concussion: a systematic review. Br J Sports Med. 2017;51(12):930934.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Wilson JC, Kirkwood MW, Potter MN, Wilson PE, Provance AJ, Howell DR. Early physical activity and clinical outcomes following pediatric sport-related concussion. J Clin Transl Res. 2020;5(4):161168.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Grool AM, Aglipay M, Momoli F, Meehan WP III, Freedman SB, Yeates KO, et al. Association between early participation in physical activity following acute concussion and persistent postconcussive symptoms in children and adolescents. JAMA. 2016;316(23):25042514.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Thomas DG, Apps JN, Hoffmann RG, McCrea M, Hammeke T. Benefits of strict rest after acute concussion: a randomized controlled trial. Pediatrics. 2015;135(2):213223.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Leddy JJ, Hinds AL, Miecznikowski J, Darling S, Matuszak J, Baker JG, et al. Safety and prognostic utility of provocative exercise testing in acutely concussed adolescents: a randomized trial. Clin J Sport Med. 2018;28(1):1320.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Ayr LK, Yeates KO, Taylor HG, Browne M. Dimensions of postconcussive symptoms in children with mild traumatic brain injuries. J Int Neuropsychol Soc. 2009;15(1):1930.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Patsimas T, Howell DR, Potter MN, Provance AJ, Kirkwood MW, Wilson JC. Concussion-symptom rating correlation between pediatric patients and their parents. J Athl Train. 2020;55(10):10201026.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Starkey NJ, Jones K, Case R, Theadom A, Barker-Collo S, Feigin V. Post-concussive symptoms after a mild traumatic brain injury during childhood and adolescence. Brain Inj. 2018;32(5):617626.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Eisenberg MA, Meehan WP III, Mannix R. Duration and course of post-concussive symptoms. Pediatrics. 2014;133(6):9991006.

  • 18

    Guskiewicz KM. Balance assessment in the management of sport-related concussion. Clin Sports Med. 2011;30(1):89102,ix.

  • 19

    Bell DR, Guskiewicz KM, Clark MA, Padua DA. Systematic review of the balance error scoring system. Sports Health. 2011;3(3):287295.

  • 20

    Davis GA, Purcell L, Schneider KJ, Yeates KO, Gioia GA, Anderson V, et al. The Child Sport Concussion Assessment Tool 5th Edition (Child SCAT5): background and rationale. Br J Sports Med. 2017;51(11):859861.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Howell DR, O'Brien MJ, Raghuram A, Shah AS, Meehan WP III. Near point of convergence and gait deficits in adolescents after sport-related concussion. Clin J Sport Med. 2018;28(3):262267.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Van Deventer KA, Seehusen CN, Walker GA, Wilson JC, Howell DR. The diagnostic and prognostic utility of the dual-task tandem gait test for pediatric concussion. J Sport Health Sci. 2021;10(2):131137.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Leddy JJ, Haider MN, Ellis M, Willer BS. Exercise is medicine for concussion. Curr Sports Med Rep. 2018;17(8):262270.

  • 24

    Zemek R, Barrowman N, Freedman SB, Gravel J, Gagnon I, McGahern C, et al. Clinical risk score for persistent postconcussion symptoms among children with acute concussion in the ED. JAMA. 2016;315(10):10141025.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Majerske CW, Mihalik JP, Ren D, Collins MW, Reddy CC, Lovell MR, et al. Concussion in sports: postconcussive activity levels, symptoms, and neurocognitive performance. J Athl Train. 2008;43(3):265274.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Leddy JJ, Willer B. Use of graded exercise testing in concussion and return-to-activity management. Curr Sports Med Rep. 2013;12(6):370376.

  • 27

    Makdissi M, Schneider KJ, Feddermann-Demont N, Guskiewicz KM, Hinds S, Leddy JJ, et al. Approach to investigation and treatment of persistent symptoms following sport-related concussion: a systematic review. Br J Sports Med. 2017;51(12):958968.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Gagnon I, Grilli L, Friedman D, Iverson GL. A pilot study of active rehabilitation for adolescents who are slow to recover from sport-related concussion. Scand J Med Sci Sports. 2016;26(3):299306.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Varner CE, Thompson C, de Wit K, Borgundvaag B, Houston R, McLeod S. A randomized trial comparing prescribed light exercise to standard management for emergency department patients with acute mild traumatic brain injury. Acad Emerg Med. 2021;28(5):493501.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Howell DR, Taylor JA, Tan CO, Orr R, Meehan WP III. The role of aerobic exercise in reducing persistent sport-related concussion symptoms. Med Sci Sports Exerc. 2019;51(4):647652.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Halstead ME, Walter KD, Moffatt K. Sport-related concussion in children and adolescents. Pediatrics. 2018;142(6):e20183074.

  • 32

    Lishchynsky JT, Rutschmann TD, Toomey CM, Palacios-Derflingher L, Yeates KO, Emery CA, et al. The association between moderate and vigorous physical activity and time to medical clearance to return to play following sport-related concussion in youth ice hockey players. Front Neurol. 2019;10:588.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Centers for Disease Control and Prevention. Nonfatal traumatic brain injuries related to sports and recreation activities among persons aged ≤19 years—United States, 2001-2009. MMWR Morb Mortal Wkly Rep. 2011;60(39):13371342.

    • Search Google Scholar
    • Export Citation
  • 34

    Arbogast KB, Curry AE, Pfeiffer MR, Zonfrillo MR, Haarbauer-Krupa J, Breiding MJ, et al. Point of health care entry for youth with concussion within a large pediatric care network. JAMA Pediatr. 2016;170(7):e160294.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand

Image from Reynolds et al (pp 703–709).

  • View in gallery
    FIG. 1.

    Line graphs showing patient-reported (A) and parent-reported (B) HBI symptom frequency scores. At the initial clinic visit, participants were asked to rate their symptom frequency at the time of injury and currently. The circles (early physical activity group) and squares (no early physical activity group) represent the group mean, and the error bars indicate the 95% CI for the mean.

  • 1

    McCrory P, Meeuwisse W, Dvořák J, Aubry M, Bailes J, Broglio S, et al. Consensus statement on concussion in sport–the 5th international conference on concussion in sport held in. Berlin, October 2016.Br J Sports Med. 2017;51(11):838847.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Moser RS, Davis GA, Schatz P. The age variable in childhood concussion management: a systematic review. Arch Clin Neuropsychol. 2018;33(4):417426.

  • 3

    Kamins J, Bigler E, Covassin T, Henry L, Kemp S, Leddy JJ, et al. What is the physiological time to recovery after concussion? A systematic review. Br J Sports Med. 2017;51(12):935940.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Echemendia RJ, Meeuwisse W, McCrory P, et al. The Sport Concussion Assessment Tool 5th Edition (SCAT5): Background and rationale. Br J Sports Med. 2017;51(11):848850.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Hunt TN, Ferrara MS, Bornstein RA, Baumgartner TA. The reliability of the modified Balance Error Scoring System. Clin J Sport Med. 2009;19(6):471475.

  • 6

    Harmon KG, Clugston JR, Dec K, Hainline B, Herring SA, Kane S, et al. American Medical Society for Sports Medicine position statement on concussion in sport. Clin J Sport Med. 2019;29(2):87100.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    The Management of Concussion-mild Traumatic Brain Injury Working Group. VA/DoD clinical practice guideline for the management of concussion—mild traumatic brain injury. Version 2.0. Department of Veterans Affairs. Published online February 2016. https://www.healthquality.va.gov/guidelines/rehab/mtbi/mtbicpgfullcpg50821816.pdf

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Leddy JJ, Haider MN, Ellis MJ, Mannix R, Darling SR, Freitas MS, et al. Early subthreshold aerobic exercise for sport-related concussion: a randomized clinical trial. JAMA Pediatr. 2019;173(4):319325.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Schneider KJ, Leddy JJ, Guskiewicz KM, Seifert T, McCrea M, Silverberg ND, et al. Rest and treatment/rehabilitation following sport-related concussion: a systematic review. Br J Sports Med. 2017;51(12):930934.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Wilson JC, Kirkwood MW, Potter MN, Wilson PE, Provance AJ, Howell DR. Early physical activity and clinical outcomes following pediatric sport-related concussion. J Clin Transl Res. 2020;5(4):161168.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Grool AM, Aglipay M, Momoli F, Meehan WP III, Freedman SB, Yeates KO, et al. Association between early participation in physical activity following acute concussion and persistent postconcussive symptoms in children and adolescents. JAMA. 2016;316(23):25042514.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Thomas DG, Apps JN, Hoffmann RG, McCrea M, Hammeke T. Benefits of strict rest after acute concussion: a randomized controlled trial. Pediatrics. 2015;135(2):213223.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Leddy JJ, Hinds AL, Miecznikowski J, Darling S, Matuszak J, Baker JG, et al. Safety and prognostic utility of provocative exercise testing in acutely concussed adolescents: a randomized trial. Clin J Sport Med. 2018;28(1):1320.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Ayr LK, Yeates KO, Taylor HG, Browne M. Dimensions of postconcussive symptoms in children with mild traumatic brain injuries. J Int Neuropsychol Soc. 2009;15(1):1930.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Patsimas T, Howell DR, Potter MN, Provance AJ, Kirkwood MW, Wilson JC. Concussion-symptom rating correlation between pediatric patients and their parents. J Athl Train. 2020;55(10):10201026.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Starkey NJ, Jones K, Case R, Theadom A, Barker-Collo S, Feigin V. Post-concussive symptoms after a mild traumatic brain injury during childhood and adolescence. Brain Inj. 2018;32(5):617626.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Eisenberg MA, Meehan WP III, Mannix R. Duration and course of post-concussive symptoms. Pediatrics. 2014;133(6):9991006.

  • 18

    Guskiewicz KM. Balance assessment in the management of sport-related concussion. Clin Sports Med. 2011;30(1):89102,ix.

  • 19

    Bell DR, Guskiewicz KM, Clark MA, Padua DA. Systematic review of the balance error scoring system. Sports Health. 2011;3(3):287295.

  • 20

    Davis GA, Purcell L, Schneider KJ, Yeates KO, Gioia GA, Anderson V, et al. The Child Sport Concussion Assessment Tool 5th Edition (Child SCAT5): background and rationale. Br J Sports Med. 2017;51(11):859861.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Howell DR, O'Brien MJ, Raghuram A, Shah AS, Meehan WP III. Near point of convergence and gait deficits in adolescents after sport-related concussion. Clin J Sport Med. 2018;28(3):262267.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Van Deventer KA, Seehusen CN, Walker GA, Wilson JC, Howell DR. The diagnostic and prognostic utility of the dual-task tandem gait test for pediatric concussion. J Sport Health Sci. 2021;10(2):131137.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Leddy JJ, Haider MN, Ellis M, Willer BS. Exercise is medicine for concussion. Curr Sports Med Rep. 2018;17(8):262270.

  • 24

    Zemek R, Barrowman N, Freedman SB, Gravel J, Gagnon I, McGahern C, et al. Clinical risk score for persistent postconcussion symptoms among children with acute concussion in the ED. JAMA. 2016;315(10):10141025.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Majerske CW, Mihalik JP, Ren D, Collins MW, Reddy CC, Lovell MR, et al. Concussion in sports: postconcussive activity levels, symptoms, and neurocognitive performance. J Athl Train. 2008;43(3):265274.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Leddy JJ, Willer B. Use of graded exercise testing in concussion and return-to-activity management. Curr Sports Med Rep. 2013;12(6):370376.

  • 27

    Makdissi M, Schneider KJ, Feddermann-Demont N, Guskiewicz KM, Hinds S, Leddy JJ, et al. Approach to investigation and treatment of persistent symptoms following sport-related concussion: a systematic review. Br J Sports Med. 2017;51(12):958968.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Gagnon I, Grilli L, Friedman D, Iverson GL. A pilot study of active rehabilitation for adolescents who are slow to recover from sport-related concussion. Scand J Med Sci Sports. 2016;26(3):299306.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Varner CE, Thompson C, de Wit K, Borgundvaag B, Houston R, McLeod S. A randomized trial comparing prescribed light exercise to standard management for emergency department patients with acute mild traumatic brain injury. Acad Emerg Med. 2021;28(5):493501.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Howell DR, Taylor JA, Tan CO, Orr R, Meehan WP III. The role of aerobic exercise in reducing persistent sport-related concussion symptoms. Med Sci Sports Exerc. 2019;51(4):647652.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Halstead ME, Walter KD, Moffatt K. Sport-related concussion in children and adolescents. Pediatrics. 2018;142(6):e20183074.

  • 32

    Lishchynsky JT, Rutschmann TD, Toomey CM, Palacios-Derflingher L, Yeates KO, Emery CA, et al. The association between moderate and vigorous physical activity and time to medical clearance to return to play following sport-related concussion in youth ice hockey players. Front Neurol. 2019;10:588.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Centers for Disease Control and Prevention. Nonfatal traumatic brain injuries related to sports and recreation activities among persons aged ≤19 years—United States, 2001-2009. MMWR Morb Mortal Wkly Rep. 2011;60(39):13371342.

    • Search Google Scholar
    • Export Citation
  • 34

    Arbogast KB, Curry AE, Pfeiffer MR, Zonfrillo MR, Haarbauer-Krupa J, Breiding MJ, et al. Point of health care entry for youth with concussion within a large pediatric care network. JAMA Pediatr. 2016;170(7):e160294.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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