No athlete in this study reported sustaining a concussion in the past 6 months. ADHD indicates attention-deficit/hyperactivity disorder; LD, learning disability.
Iverson GL, Silverberg ND, Mannix R, Maxwell BA, Atkins JE, Zafonte R, Berkner PD. Factors Associated With Concussion-like Symptom Reporting in High School Athletes. JAMA Pediatr. 2015;169(12):1132-1140. doi:10.1001/jamapediatrics.2015.2374
Every state in the United States has passed legislation for sport-related concussion, making this health issue important for physicians and other health care professionals. Safely returning athletes to sport after concussion relies on accurately determining when their symptoms resolve.
To evaluate baseline concussion-like symptom reporting in uninjured adolescent student athletes.
Design, Setting, and Participants
In this cross-sectional, observational study, we studied 31 958 high school athletes from Maine with no concussion in the past 6 months who completed a preseason baseline testing program between 2009 and 2013.
Symptom reporting was more common in girls than boys. Most students with preexisting conditions reported one or more symptoms (60%-82% of boys and 73%-97% of girls). Nineteen percent of boys and 28% of girls reported having a symptom burden resembling an International Classification of Diseases, 10th Revision (ICD-10) diagnosis of postconcussional syndrome (PCS). Students with preexisting conditions were even more likely to endorse a symptom burden that resembled PCS (21%-47% for boys and 33%-72% for girls). Prior treatment of a psychiatric condition was the strongest independent predictor for symptom reporting in boys, followed by a history of migraines. For girls, the strongest independent predictors were prior treatment of a psychiatric condition or substance abuse and attention-deficit/hyperactivity disorder. The weakest independent predictor of symptoms for both sexes was history of prior concussions.
Conclusions and Relevance
In the absence of a recent concussion, symptom reporting is related to sex and preexisting conditions. Consideration of sex and preexisting health conditions can help prevent misinterpretation of symptoms in student athletes who sustain a concussion.
Every state in the United States has passed legislation pertaining to sport-related concussion. In general, the laws mandate that injured student athletes be evaluated by a qualified health care professional before returning to participation in sports. Decisions about return to activity are usually based on symptom reporting. Athletes who experience a concussion report numerous and diverse symptoms shortly after injury,1 and those symptoms tend to improve rapidly during the first 2 weeks.2,3 Most athletes recover symptomatically within a month, but a few have persistent symptoms.4,5 Athletes with preexisting developmental problems, migraines, psychiatric conditions, or prior concussions are believed to be at increased risk for slower recovery after concussion.6,7 Numerous factors are associated with increased concussion-like symptom reporting by athletes, such as sex (girls and young women report more symptoms),8,9 attention-deficit/hyperactivity disorder (ADHD)10,11 learning disability (LD),10,11 insufficient sleep,12 and multiple prior concussions.13 Moreover, athletes who experience bodily injuries (eg, orthopedic injuries) can experience symptoms that resemble concussion symptoms, such as fatigue, sleep problems, irritability, stress, and dysphoria.14- 16 Therefore, it can be challenging to determine the extent to which an athlete’s symptoms are due to the neurobiological effects of a concussion vs other factors, especially if the athlete reports symptoms weeks or months after injury.
The purpose of this study is to clarify factors associated with concussion-like symptoms in uninjured adolescents using a unique data set of more than 30 000 adolescent student athletes. We hypothesized that a proportion of athletes will report concussion-like symptoms, in the absence of recent injury, and that demographic factors (eg, female sex) and health conditions (eg, ADHD, history of treatment of psychiatric conditions, migraines, and multiple prior concussions) will be associated with greater baseline symptom reporting. For clinicians treating athletes after concussion, understanding factors associated with baseline symptom reporting is important when making return-to-activity decisions.
In the absence of a recent concussion, 19% of boys and 28% of girls report a constellation of symptoms similar to the postconcussional syndrome.
Preexisting psychiatric, developmental (eg, attention-deficit/hyperactivity disorder [ADHD] and learning disability), and neurological factors (eg, migraines) are associated with higher rates of reporting symptoms resembling postconcussional syndrome at preseason baseline.
Prior concussions were modestly associated with increased risk for reporting clusters of symptoms, less so than preexisting developmental and psychiatric factors.
Several preexisting factors, including a history of ADHD and prior concussion(s), were more strongly associated with reporting clusters of symptoms in girls than in boys.
Participants in this multiyear, cross-sectional, observational cohort study were 33 732 adolescent student athletes from Maine aged 13 through 18 years (mean [SD] age, 15.5 [1.3] years) who completed baseline preseason testing with the Immediate Post-Concussion Assessment and Cognitive Testing (ImPACT)17 between 2009 and 2013. There were 18 290 boys (54.2%) and 15 442 girls (45.8%). Students were excluded if (1) they reported sustaining a concussion within the past 6 months (n = 869), (2) they reported a history of treatment of epilepsy or seizures (n = 337) or meningitis (n = 150) or reported undergoing brain surgery (n = 64), or (3) the language they completed the test in was not English (n = 420). The final sample included 31 958 students (94.7% of the original sample), 17 290 (54.1%) boys and 14 668 (45.9%) girls. Participants were a mean (SD) of 15.5 (1.3) years old. They completed ImPACT before participating in their first sport for that school year. Institutional review board approval to create and use this deidentified database was obtained from Colby College (primary use) and from Spaulding Rehabilitation Hospital (secondary use).
A demographics and health history survey is embedded in the ImPACT program, a computerized neuropsychological screening battery designed for use in sport concussion programs. The health history survey asked the student whether he or she has “had problems with ADD/hyperactivity,” been diagnosed as having an LD, received special education services, or repeated a grade. These questions required a yes or no response. The health history survey also asks about the number of times the student has been diagnosed as having a concussion. The health history survey also included past treatment of headaches, migraines, epilepsy, brain surgery, meningitis, substance use, or psychiatric conditions.
The Post-Concussion Scale18,19 is a component of ImPACT. This standardized self-report inventory includes 22 symptoms (Table 1 and Table 2) that are rated from 0 to 6, with 1 to 2 being mild, 3 to 4 being moderate, and 5 to 6 being severe. The internal consistency of the scale ranges from 0.88 to 0.94 in high school and college students and 0.92 to 0.93 in concussed athletes.19 Normative data for the scale are available for 1391 young males and 355 young females in high school or university.19 Students completed the Post-Concussion Scale independently.
We dichotomized the Post-Concussion Scale total score variable based on the International Classification of Diseases, 10th Revision (ICD-10), symptom criteria for postconcussional syndrome (PCS). These criteria are widely used in adult and pediatric studies because the constellation of symptoms after concussion vary little by age.20 To meet the ICD-10 criteria, participants must endorse at least 1 symptom in at least 3 of the following categories: cognitive, somatic, emotional, and insomnia. Assignment of symptoms to categories is denoted in Table 1. We did not apply the ICD-10 criterion that pertained to head trauma history because the purpose was to examine other factors that are related to PCS-like symptom reporting in the absence of recent head trauma. Because the ICD-10 does not specify a threshold for symptom endorsement, we created more and less stringent versions. For mild PCS, ratings of mild severity (≥1 on the Likert scale) were considered as symptom endorsement. Only ratings of 3 or greater were considered as symptom endorsement toward a moderate PCS classification. In other words, a severity rating of 3 or greater for at least 1 symptom in at least 3 categories would qualify a participant as meeting criteria for moderate PCS.
Logistic regression was used to determine which covariates were associated with symptom reporting, using mild PCS as the dichotomous outcome variable to maximize the ratio of participants with each outcome category to the number of covariates. Because exploratory analyses revealed strong sex effects on the outcome of interest, sex differences on most covariates, and sex by covariate interaction effects, separate models were generated for boys and girls. All covariates and interaction terms (Table 3 and Table 4) were entered en bloc in a single step for each model. Age was not included as a covariate because symptom reporting varies little across this narrow age range of high school students.21
The percentages of student athletes who endorsed individual symptoms, stratified by sex, preexisting health conditions, and concussion history, are presented in Table 1 and Table 2. The most commonly reported symptoms in boys were fatigue (20.8%), sleeping less than usual (20.3%), trouble falling asleep (18.4%), difficulty concentrating (17.5%), and headaches (16.2%). The most commonly reported symptoms in girls were fatigue (26.8%), sleeping less than usual (25.5%), trouble falling asleep (23.0%), headaches (24.6%), sadness (22.6%), feeling more emotional (21.9%), and difficulty concentrating (21.0%). Most students reported one or more symptoms (which can be calculated from the percentages endorsing “no symptoms” in Table 1 and Table 2). Students with preexisting conditions, such as ADHD, LD, prior treatment of a psychiatric condition, or a history of multiple concussions, endorsed considerably more physical, emotional, and cognitive symptoms.
Several boys (19.3%) and girls (28.0%) endorsed a cluster of symptoms similar to ICD-10 symptom criteria for mild PCS (Figure), and 4.3% of boys and 7.2% of girls met ICD-10 symptom criteria for moderate PCS. More boys with ADHD (31.5%), LD (33.6%), 3 or more prior concussions (28.1%), a history of treatment of migraines (34.0%), or a psychiatric condition (47.4%) endorsed a cluster of symptoms consistent with mild PCS. High rates of mild PCS were similarly present in girls with a history of ADHD (52.6%), LD (50.4%), 3 or more prior concussions (41.5%), or a history of treatment of migraines (42.5%) or a psychiatric condition (55.3%). Of note, among athletes with none of the queried preexisting conditions (n = 17 777), the frequency of mild PCS was 15.0% for boys and 22.2% for girls; the frequency of moderate PCS was 2.2% for boys and 4.0% for girls.
Seven predictor variables (Table 3) and one interaction term for LD by ADHD were entered in a logistic regression, with mild PCS classification as the dichotomous outcome. The logistic regression was conducted with 14 805 boys (excluding 2485 [14.4%] with at least 1 missing data point) and 12 923 girls (excluding 1745 [11.9%] with at least 1 missing data point). We examined the sources of missing data and compared participants with complete data (and who therefore were included in the logistic regression analysis) vs incomplete data. Most excluded boys and girls did not answer multiple questions (median, 4 items), typically the treatment history variables. Boys excluded from the analysis had a similar rate of mild PCS classification (20.4% vs 19.1%, P = .13) but were somewhat more likely to report having never sustained a prior concussion (88.4% vs 81.7%, χ21 = 58.32, P < .001). Girls who were excluded were more likely to meet mild PCS criteria (30.1% vs 27.7%, P = .04) and report having never sustained a prior concussion (93.0% vs 87.7%, P < .001) than girls included in the model.
For boys, the logistic regression model was significant (χ210 = 462.30, P < .001) and well calibrated (Hosmer and Lemeshow χ24 = 1.41, P = .70). Measures of discrimination suggested modest prediction accuracy (Nagelkerke R2 = 0.049, area under the receiver operating curve = 0.60, P < .001), that is, better than chance but poor for classifying individual cases. For girls, the logistic regression model was significant (χ210 = 497.30, P < .001) and reasonably well calibrated (Hosmer and Lemeshow χ22 = 4.16, P = .13). Measures of discrimination again suggested modest prediction accuracy (Nagelkerke R2 = 0.054, area under the receiver operating curve = 0.60, P < .001).
As indicated in Table 3 for boys and Table 4 for girls, all covariates had a significant association with PCS when considered in single predictor models, but the odds ratios (ORs) were relatively small. For boys, the predictors in descending order of strength were treatment of a psychiatric condition, treatment of substance abuse, having ADHD and LD, treatment of migraines, having ADHD or LD, having other academic problems, and history of concussion. After all variables in the model were adjusted for, prior treatment of a psychiatric problem was by far the strongest predictor of PCS classification, followed by treatment of migraines. For girls, the predictors in descending order of strength were treatment of substance abuse, having ADHD and LD, treatment of a psychiatric problem, having ADHD or LD, treatment of migraines, other academic problems, and prior concussions. After adjusting for all variables in the model, prior treatment of a psychiatric condition or substance abuse were the strongest predictors, followed by ADHD. The effect of each prior concussion was relatively weak, but statistically significant, in boys and girls.
For exploratory purposes, we reran the logistic regressions excluding students with a history of 1 or 2 prior concussions so we could evaluate the effects of multiple concussions (ie, ≥3) vs no prior concussions. For boys, the adjusted OR was 1.24 (95% CI, 0.94-1.63); multiple concussions remained the weakest independent predictor of PCS classification. For girls, the adjusted OR was 1.69 (95% CI, 1.17-2.44); multiple concussions now were a greater independent predictor than LD and academic problems and similar to migraine (OR, 1.74; 95% CI, 1.48-2.05) but remained less than treatment of psychiatric or substance abuse problems.
Risk of model overfitting was evaluated. Because 2832 boys and 3583 girls who contributed data to each model had symptoms consistent with mild PCS, the sample size was more than adequate for robust estimation. A cell size count revealed that every combination of every covariate with each outcome category had at least 5 cases and all but the following had at least 100 cases: girls reporting prior treatment of substance abuse (with and without mild PCS) and girls with 3 or 4 or more prior concussions (with and without mild PCS). Finally, bootstrapping was performed and found to have little effect on the model coefficients (Table 3 and Table 4). The bootstrapped CIs for the substance abuse variable included 1.0, suggesting that the regression coefficient (and OR) for this variable does not generalize well outside the present sample, perhaps because of the small cell size.
To our knowledge, this is the largest study to date of concussion-like symptom reporting in uninjured high school athletes. Using a sample of more than 30 000 athletes evaluated before the sporting season as part of a baseline testing program, we found that most students report concussion-like symptoms, with symptom reporting greater in girls and those with a preexisting condition. Several healthy uninjured student athletes, with no preexisting conditions or prior concussions, endorsed a combination of physical, emotional, cognitive, and sleep-related symptoms that resemble an ICD-10 diagnosis of PCS (Figure). Students with preexisting conditions were more likely to endorse clusters of symptoms that resemble an ICD-10 diagnosis of PCS (Table 3, Table 4, and Figure). Understanding the normative rate of concussion-like symptoms, sex differences, and their association with preexisting athlete characteristics and health conditions is essential for guiding medical management after sport-related concussion and for making return-to-play decisions.
All the individual preexisting factors we evaluated were related to symptom clusters that resemble PCS in both boys and girls, but the magnitudes of their individual contributions varied considerably, more so for boys than for girls. When considering all preexisting conditions simultaneously with logistic regression, prior treatment of a psychiatric condition had the largest effect size in symptom reporting in boys, followed by having a history of migraines. For girls, prior treatment of a psychiatric condition or substance abuse had the largest effect size, followed by ADHD. These findings extend prior studies that have examined developmental conditions11,22 and concussion history13,23,24 in isolation by demonstrating the independent contributions of these and other preexisting conditions on baseline preseason symptom reporting. These findings also refine our earlier findings with a subset of data from this larger cross-sectional study.25 The pattern of symptoms did not necessarily align with the preexisting condition. For example, based on an analysis of individual symptom endorsement rates, it was not the case that participants with a psychiatric history merely reported more sadness and nervousness, whereas individuals who had previously received treatment of migraines merely reported more headaches. Participants with these conditions, and, to a lesser extent, even participants without these conditions, endorsed a diverse range of symptoms. Of interest, the effect size of concussion history was relatively small in both boys and girls. This finding is consistent with the generally good long-term prognosis of sport-related concussion.1- 3 Prior studies6,13 have reported an association between prior concussions and preseason baseline symptoms; the present study replicated this association but demonstrated that it is weak compared with the association between concussion-like symptom reporting and other preexisting conditions.
Four interesting sex differences were identified in this study. First, sex was associated with baseline symptom reporting. Consistent with prior studies,8,19,26 a greater proportion of girls report a cluster of concussion-like symptoms at baseline. This finding might reflect, in part, girls being more aware of their symptoms and willing to report them. It might also reflect, in part, hormonal changes associated with girls’ menstrual cycle,9 an issue rarely accounted for in this literature. Second, sex was a significant modifier of the association of preexisting conditions, such as ADHD and prior concussions and symptoms reported at baseline (ie, boys and girls differed on the effect of preexisting conditions on symptom reporting). Third, a dose-response relationship with the number of prior concussions was observed for both sexes but was more robust in girls. As seen in the Figure, the association appears fairly linear. The study by Brooks et al23 is the only prior study we are aware of that examined how sex and concussion history jointly related to symptom reporting. They found that the effect of reporting none vs any prior concussions was similar for boys and girls. Their sample, however, included very few participants with 3 (n = 6 boys, n = 1 girl) or 4 or more (n = 0) prior concussions. Finally, the most novel and interesting sex difference in the present study is that the effect of prior concussions and ADHD on meeting PCS criteria was stronger in girls than boys. The 95% CIs are almost nonoverlapping (Table 3 and Table 4), and the 90% CIs do not overlap. The finding that ADHD has a stronger effect on symptom reporting in girls than boys, to our knowledge, has not been previously reported. It may reflect, in part, sex differences in the manifestation of ADHD.27
Some studies, but not all,28 have suggested that female athletes report more29,30 and prolonged31 symptoms after concussion compared with male athletes. It remains unclear whether this sex difference is attributable to injury severity (for which collision or impact force and neck musculature may be proxies), hormonal, or other factors.30 Although girls appear at higher risk for concussions in prospective surveillance studies,32 as with other studies that asked about concussion history,22,23 fewer girls than boys self-reported at least one prior concussion in our sample.
This study has several important limitations. First, all preexisting health conditions were identified through self-report, and we had no means of verification. Second, although our models identified factors associated with baseline symptom reporting, the models are not sufficient to predict the presence or absence of meeting PCS criteria in an individual athlete based on their sex and preexisting health conditions. Third, state factors, such as recent stressors and insufficient sleep,12 were not included.
A large number of healthy student athletes with no preexisting conditions and no recent concussion report a cluster of baseline symptoms that resemble ICD-10 PCS. This study further highlights that concussion-like symptoms are nonspecific,26,33- 36 and they are reported more frequently by those with a history of psychiatric condition, ADHD,10,11 LD,10,11 a migraine history, and multiple prior concussions.13 When managing a student athlete with a concussion, it has been widely noted that the athlete should be “asymptomatic” at rest and with exercise before returning to sports,37 and sometimes athletes are kept out of school for prolonged periods while they wait for symptoms to resolve, which could have negative consequences for their academic, social, and emotional functioning and contribute to symptom reporting.38 These results reinforce that “asymptomatic” status after concussion can be difficult to define.39 To assist clinicians, the present study offers normative data that are stratified by sex and preexisting health conditions. These reference tables can help interpret symptoms in student athletes who sustain a concussion.
Accepted for Publication: July 8, 2015.
Corresponding Author: Grant L. Iverson, PhD, Center for Health and Rehabilitation, Department of Physical Medicine and Rehabilitation, Harvard Medical School, 79/96 13th St, Charlestown Navy Yard, Charlestown, MA 02129 (firstname.lastname@example.org).
Published Online: October 12, 2015. doi:10.1001/jamapediatrics.2015.2374.
Author Contributions: Drs Iverson and Silverberg had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: Iverson, Maxwell, Zafonte, Berkner.
Acquisition, analysis, or interpretation of data: Iverson, Silverberg, Mannix, Maxwell, Atkins, Berkner.
Drafting of the manuscript: Iverson, Silverberg, Mannix, Zafonte.
Critical revision of the manuscript for important intellectual content: All authors.
Statistical analysis: Iverson, Silverberg, Mannix, Maxwell.
Obtained funding: Zafonte.
Administrative, technical, or material support: Iverson, Atkins, Zafonte, Berkner.
Study supervision: Iverson, Mannix, Maxwell, Zafonte.
Conflict of Interest Disclosures: Dr Iverson reported being reimbursed by the government, professional scientific bodies, and commercial organizations for discussing or presenting research relating to mild traumatic brain injury and sport-related concussion at meetings, scientific conferences, and symposiums. He reported having a clinical practice in forensic neuropsychology that involves individuals who have sustained mild traumatic brain injuries (including athletes). He reported receiving honorariums for serving on research panels that provide scientific peer review of programs. He is a coinvestigator, collaborator, or consultant on grants relating to mild traumatic brain injury funded by several organizations. He reported receiving research support from test publishing companies in the past, including ImPACT Applications Systems (not in the past 5 years). No other disclosures were reported.
Funding/Support: This study was supported by the Goldfarb Center for Public Policy and Civic Engagement/Colby College, the Bill and Joan Alfond Foundation, the Harvard Integrated Program to Protect and Improve the Health of National Football League Players Association Members (Dr Zafonte), and the Mooney-Reed Charitable Foundation (Drs Iverson and Zafonte).
Role of the Funder/Sponsor: The funding sources had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and the decision to submit the manuscript for publication.
Previous Presentation: The results of this study were presented at the Tenth World Congress on Brain Injury; March 21, 2014; San Francisco, California.
Additional Contributions: The data were gathered as part of the Maine Concussion Management Initiative. We thank the Maine Athletic Trainers Association for their collaboration with the Maine Concussion Management Initiative.