Abstract
This case–control study using baseline data from the population cohort Adolescent Brain Cognitive Development (ABCD) Study® compared lifetime history of concussion between children with and without attention-deficit/hyperactivity disorder (ADHD). We hypothesized that children with ADHD would have a greater lifetime history of concussion than children without ADHD. Children were recruited from schools across the United States, sampled to provide strong generalizability to the US population. The current sample included 10,585 children (age: mean = 9.9; standard deviation = 0.6; range 9-10 years; 48.9% girls; 64.6% White), including 1085 with ADHD and 9500 without ADHD. The prevalence of prior concussion among children with ADHD was 7.2% (95% CI: 6.6-7.8%) compared with 3.2% (3.1-3.3%) among children without ADHD, meaning current ADHD status was associated with twice the odds of experiencing a prior concussion [χ2 = 44.54; p < 0.001; odds ratio = 2.34 (1.81-3.03)]. No significant differences were observed in proportion of boys and girls with ADHD who had a prior concussion history. The number of current ADHD symptoms were not meaningfully associated with prior concussion history. Lower socioeconomic status was associated with lower rates of reported concussion, but not differentially in association with ADHD. ADHD is associated with twice the lifetime prevalence of prior concussion before age 11 among children from the general U.S. population. Boys and girls with ADHD did not differ in proportions with prior concussion and concussion history was not related to the number of ADHD symptoms reported by parents.
Introduction
Children, adolescents, and young adults with attention-deficit hyperactivity disorder (ADHD) self-report greater lifetime rates of concussion than those who do not have ADHD. 1 –6 Moreover, boys with ADHD report a greater lifetime history of concussion than girls with ADHD. 4 -6 However, there are important methodological weaknesses and unanswered questions relating to the association between ADHD and lifetime history of concussion in children.
First, studies have predominantly examined samples of student-athletes rather than children from the general population and a systematic review 7 called for more diverse population sampling to evaluate the association of ADHD and concussion in children, in part because children from low socioeconomic status backgrounds have a higher prevalence of ADHD than socioeconomically advantaged children. 8 Second, researchers have relied on surveys of children, adolescents, and young adults, thus examining self-reported concussion histories and self-reported ADHD diagnoses, as opposed to parent-reported diagnoses, physician-verified diagnoses, or diagnoses based on structured diagnostic interviews. 2,4 -6,9,10 Finally, we found no prior studies relating to whether symptoms of inattention and/or hyperactivity/impulsivity convey differential risk for concussion among children with formally diagnosed ADHD. Prior studies have noted an association between hyperactive/impulsive symptoms, but not inattentive symptoms, and risk for traumatic dental injury. 11,12 However, the children in these studies were not formally diagnosed with ADHD; rather, the authors compared community samples of children with and without dental injuries on reported ADHD-like symptoms and behaviors based on a questionnaire.
It is important to clarify the association between pediatric concussion and ADHD for several reasons. Confirming that children with ADHD are at increased risk for sustaining a concussion may help to target or inform prevention efforts. It might also help focus additional research aimed at better understanding why children with ADHD are at greater risk for concussion, such as whether children with ADHD are more susceptible to injury, have a lower threshold for sustaining concussion, or whether certain behavioral factors (e.g., hyperactivity, impulsivity, risk taking) or family/social factors (e.g., parental supervision, peer group composition) contribute. Moreover, having a previous history of concussion appears to confer risk for future, subsequent concussion, 13,14 and although the evidence is mixed, 15 some large-scale studies show an association between concussion history and increased risk for prolonged recovery from a subsequent injury. 16 -18
The Adolescent Brain Cognitive Development (ABCD) Study®, the largest long-term study of brain development and child health in the U.S., 19,20 provides a unique opportunity to examine associations between ADHD and concussion in a large, diverse, representative cohort of children from the U.S. general population, and to address methodological limitations and gaps in the published literature. A recent study using the ABCD dataset reported that 4% of the children in the study had a parent-reported concussion history, boys and children from households with higher income had greater odds of having a prior concussions, and that, among the full sample of children, parent-reported symptoms on an ADHD scale were not associated with increased rate of concussion. 21 Of note, this study did not stratify and examine rates of concussion among children who did and did not meet formal diagnostic criteria for ADHD, but examined the association between ADHD-like symptoms and concussion rate among the full sample of children. We hypothesized that: 1) children with ADHD would have a greater lifetime history of concussion than children without ADHD; 2) boys with ADHD would have a greater lifetime history of concussion than girls with ADHD; and 3) among children with ADHD, a history of concussion would be associated with greater ADHD symptom severity.
Methods
Design and participants
Participants were drawn from the publicly available dataset (data release 2.0.1) from the ABCD study. 19 The ABCD Study is a comprehensive longitudinal study involving 21 research sites. Data release 2.0.1 includes 11,875 children, of which 174 were missing data on ADHD status and nine children were missing data on prior concussions. We excluded five children due to having sustained an injury with loss of consciousness lasting greater than 30 min and excluded 1107 children because they appeared to meet diagnostic criteria for ADHD in the past but did not meet current criteria. The final sample for this study included 10,585 children. The mean age of the sample was 9.9 years (standard deviation = 0.6, range: 9-10) and roughly equally split between girls (48.9%) and boys (51.1%). The sample is diverse in terms of racial and ethnic composition and socioeconomic status (Table 1). An institutional review board waiver was obtained to access this publicly available dataset.
Sample Demographics
Significance tests compare the ADHD and No ADHD groups for demographic differences. The frequencies of demographic categories do not necessarily sum to the total N for that column due to a small percentage of participants having missing data on that variable.
ADHD, attention-deficit/hyperactivity disorder; M, mean; SD, standard deviation.
Measures
The Kiddie Schedule for Affective Disorders and Schizophrenia for Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (KSADS-5) 22 is a structured interview to assess DSM-523 diagnoses, and it has been translated into a computerized assessment. 24 We used results from the self-administered parent version to identify children who met formal diagnostic criteria for current ADHD. We also calculated the number of current inattention symptoms (range: 0-9) and the number of current hyperactivity/impulsivity symptoms (range: 0-9).
The Ohio State Traumatic Brain Injury Screen-Short Modified (OTBI) 25 is a questionnaire for caregivers assessing their child's lifetime history of traumatic brain injury. Parents are asked four questions to determine the occurrence of a past head injury [i.e., 1) Has your child ever been hospitalized or treated in an emergency room following an injury to his/her head or neck?; 2) Has your child ever injured his/her head or neck in a car accident or from crashing some other moving vehicle like a bicycle, motorcycle, or ATV?; 3) Has your child ever injured his/her head or neck in a fall or from being hit by something? (For example, falling from a bike or horse, rollerblading, falling on ice, being hit by a rock); Has your child ever injured his/her head or neck playing sports or on the playground?; and 4) Has your child ever injured his/her head or neck in a fight, from being hit by something, or from being shaken violently?]. If a prior injury is indicated, the parent is asked questions to determine injury severity [i.e., 1) Was he/she knocked out or did he/she lose consciousness? If yes, how long?; 2) Was he/she dazed or did he/she have a gap in his/her memory from the injury?]. For this study, after excluding children with a reported loss of consciousness greater than 30 min, we examined i) prior head injuries defined as any positive response to the four injury occurrence questions whether or not the child had lost consciousness, been dazed, or experienced a memory gap; and ii) prior concussions defined as any positive response to the 4 injury occurrence questions with a reported loss of consciousness (lasting less than 30 min) and/or the child feeling dazed or having a memory gap.
Statistical analysis
The proportions of children with and without ADHD whose caregivers reported a history of head injury and concussion were computed and compared using χ2
tests. The proportions of girls and boys with ADHD who experienced a prior concussion were also compared using χ2
tests. To characterize the magnitude of group differences, an odds ratio (OR) was calculated for each analysis as an effect size
26
and interpreted according to widely used criteria
27
(i.e., ORs between 1.2 and 1.71 = small, ORs between 1.72 and 2.4 = medium, and ORs greater than 2.4 = large). Additionally, a 95% confidence interval (CI) was constructed around each proportion using the formula:
± 1.96 * s.e.
, where
is the proportion and s.e. is the standard error of the proportion [calculated s.e.
, where n is the cell size]. The number of inattention and hyperactivity/impulsivity symptoms were compared between children with ADHD who did and did not have a prior history of concussion using Mann-Whitney U tests. The Z values from the Mann-Whitney U test were used to calculate non-parametric effect sizes (r =
),
28
which were interpreted according to conventional guidelines, i.e., r = .1, small; r = .3, medium; r = .5, large.
29
We applied the Benjamini-Hochberg False Discovery Rate (FDR) procedure to control our Type I error rate.
30
Using this procedure, setting the FDR at 5%, for the results of our 17 primary and secondary statistical tests (15 reported in Tables 2 and 3 and two Mann-Whitney U tests described in text), p values less than 0.026 were considered statistically significant. Analyses were conducted using SPSS Version 25.
Comparing Lifetime History of Parent-Reported Head/Neck Injuries and Concussions between Children with and without ADHD
Parents responded yes to the 4 injury occurrence questions on the Ohio State Traumatic Brain Injury Screen-Short Modified (OTBI), with or without any loss of consciousness or report of feeling dazed or having a memory gap.
Parents responded yes to the 4 injury occurrence questions on the OTBI and reported either loss of consciousness or their child being dazed or experiencing a memory gap.
†Fisher's exact tests were used because there were less than 5 observations per cell.
OR values are oriented so that a higher value is indicative of greater odds of children with ADHD experiencing the injury. We applied the Benjamini-Hochberg false discovery rate (FDR) procedure to control our Type I error rate. 24 Using this procedure, setting the FDR at 5%, for the results our 17 primary and secondary statistical tests (15 reported in this table and Table 3 and two Mann-Whitney U tests described in text), p values less than 0.026 were considered statistically significant.
ADHD, attention-deficit/hyperactivity disorder; CI, confidence interval; OR, odds ratio; ATV, all-terrain vehicle.
Comparing Lifetime History of Parent-Reported Concussions between Boys and Girls with ADHD
†Fisher's exact tests were used because there were less than 5 observations per cell.
OR values are oriented so that a higher value is indicative of greater odds of boys with ADHD experiencing the injury. Parents responded yes to the 4 injury occurrence questions on the Ohio State Traumatic Brain Injury Screen-Short Modified and reported either loss of consciousness lasting less than 30 min or their child being dazed or experiencing a memory gap. We applied the Benjamini-Hochberg false discovery rate (FDR) procedure to control our Type I error rate. 24 Using this procedure, setting the FDR at 5%, for the results our 17 primary and secondary statistical tests (15 reported in Table 2 and this table and 2 Mann-Whitney U tests described in text), p values less than 0.026 were considered statistically significant.
ADHD, attention-deficit/hyperactivity disorder; OR, odds ratio; CI, confidence interval; ATV, all-terrain vehicle.
Results
Descriptive data
In the total sample, one in five children (20.9%) had a parent-reported history of head or neck injury and one in 25 children (3.6%) had a parent-reported history of concussion. Boys (4.4%) had nearly twice the rate of prior concussion than girls [2.8%; χ2 = 19.82, p < 0.001, OR = 1.68 (95% CI: 1.53-1.85)]. Concussion rates differed significantly by yearly household income (χ2 = 20.63, p < 0.001). Children with a household income > $100,000 per year had the highest rate of concussion (4.5%), double the rate of injury noted in children with a household income less than $35,000 (2.2%). A total of 1,085 children (9.1% prevalence among the full ABCD Study baseline cohort; 10.3% of the current sample) met diagnostic criteria for current ADHD. Twice as many boys (13.9%) than girls (6.5%) met criteria for ADHD [χ2 = 156.76, p < 0.001, OR = 2.32 (95% CI: 2.03-2.66)]. Rates of ADHD did not differ across levels of household income (less than $35,000: 10.9%; $35,000 to $99,999: 10.9%; > $100,000: 9.4%), χ2 = 5.90, p = 0.052. A slightly greater proportion of children without ADHD identified as Hispanic/Latinx compared with the ADHD group (4.6% difference between the groups). There were very slight differences between the ADHD and No ADHD groups in proportions of children who identified as various racial groups.
ADHD and lifetime history of head injury and concussion
The rate of prior concussion among children with ADHD [7.2% (95% CI: 6.6-7.8%)] was more than twice the rate of concussion among children without ADHD [3.2% (3.1-3.3%), χ2 = 44.54, p < 0.001, OR = 2.34 (95% CI: 1.81-3.03); Table 2]. The rate of hospitalization or treatment in an emergency room for a concussion among children with ADHD [4.7% (3.9-5.5%)] was more than twice the rate among children without ADHD [2.0% (1.9-2.1%)], χ2 = 31.17, p < 0.001, OR = 2.39 (1.74-3.28)]. Among children with a parent-reported head injury, significantly more children with ADHD [22.3% (21.2-23.4%)] experienced feeling dazed or a memory gap following their injury compared with children without ADHD [14.3% (14.0-14.6%)], χ2 = 13.41, p < 0.001, OR = 1.72 (1.28-2.31)].
Gender and concussion history in ADHD
There were no statistically significant gender differences in the rates of concussion (Table 3). The rates among girls with ADHD [6.9% (4.7-9.1)] and boys with ADHD [7.3% (6.4-8.2%)] did not differ [χ2 = 0.08, p = 0.78, OR = 1.07 (0.65-1.78)].
ADHD symptom count and concussion history
Children with ADHD and a history of concussion (hyperactivity/impulsivity symptom count: median [Mdn] = 7, range: 0-9) did not display higher levels of hyperactivity and impulsivity symptoms than those with ADHD and no prior concussions (symptom count: Mdn = 6, range: 0-9; U = 35,081, p = 0.11; r = 0.05, negligible effect). Children with ADHD and a history of concussion (inattention symptom count: Mdn = 8, range: 0-9) displayed slightly higher levels of inattention symptoms than those with ADHD and no prior concussions (inattention symptom count: Mdn = 7, range: 0-9; U = 33,367, p = 0.02), although the magnitude of this difference was negligible (r = 0.07).
ADHD, concussion history, and household income
Given that concussion rates differed significantly by yearly household income, we conducted an exploratory analysis to compare concussion rates among children with and without ADHD stratified by household income. Across the three levels of household income, the ADHD group was more likely to have a concussion history, χ2 Mantel-Haenszel = 30.98, p < 0.001, OR Mantel-Haenszel = 2.18 (95% CI: 1.65-2.87). However, odds ratios for prior concussion history between children with and without ADHD were not statistically different across levels of household income, χ2 Breslow-Day = 5.09, p = 0.08 (Table 4).
Comparing Lifetime History of Parent-Reported Concussions between Children with and without ADHD Stratified by Household Income
Parents responded yes to the 4 injury occurrence questions on the Ohio State Traumatic Brain Injury Screen-Short Modified and reported either loss of consciousness lasting less than 30 min or their child being dazed or experiencing a memory gap. The total subgroup cell sizes are as follows: < $35,000: ADHD n = 207, No ADHD n = 1733; $35,000-$99,999: ADHD n = 357, No ADHD n = 3073; > $100,000: ADHD n = 366, No ADHD n = 3595.
ADHD, attention-deficit/hyperactivity disorder; OR, odds ratio; CI, confidence interval.
Discussion
This study showed that children with ADHD from the U.S. general population have twice the rate of concussion than children without ADHD. Specifically, 7% of children with ADHD had experienced a concussion prior to age 11, compared with 3% of children without ADHD. The finding is consistent with our hypothesis, as well as with survey results from studies of middle school, 4 high school, 5,6 and collegiate student-athletes. 2 Rates of prior concussion among youth student-athletes have generally been higher than the rates we found among children from the general population. For example, among middle school student-athletes (mean age 12.6 years), 23.9% of those with ADHD reported a prior concussion history compared with 11.4% of those without ADHD, 4 and among high school student-athletes (mean age 15.5 years), 24.5% of those with ADHD reported a prior concussion history compared with 16.1% of those without ADHD. 6 Differences in concussion rates are likely due to several factors, including the student-athlete samples being older than the children in the current sample, inherent differences between the samples (i.e., student-athletes vs. children from the general population) because student-athletes might have more exposure to potential concussion through participation in sports, and very importantly, methodological differences between prior studies and the current study, namely the use of parent report and a more stringent definition of concussion in the present study, compared with relying on student-athlete self report in prior studies. Interestingly, despite these differences across the studies, the magnitude of difference in concussion rates between youth with and without ADHD in the current study (OR = 2.34) is consistent with that observed among middle school student-athletes (OR = 2.45). 4
Contrary to our hypothesis, rates of concussion among girls and boys with ADHD sampled from the general population did not differ. Prior studies of youth student-athletes have suggested that boys with ADHD report higher rates of prior concussion, albeit modestly so, compared with girls with ADHD. Among middle school student-athletes, 24.5% of boys with ADHD reported a prior concussion history compared with 22.2% of girls with ADHD, 4 and among high school student-athletes, 26.4% of boys with ADHD reported a prior concussion history compared with 20.6% of girls with ADHD. 6 In the present study, 6.9% of girls with ADHD and 7.3% of boys with ADHD had prior concussions. Interestingly, among children without ADHD, there was a significant gender difference such that 3.9% of boys had prior concussion compared with 2.5% of girls.
The present study has several important strengths. This is the largest cohort of children ever evaluated for both ADHD and concussion history in a comprehensive way and the first study to report on children from the general population. Moreover, the present study is the first to confirm ADHD status using a structured diagnostic interview. Prior studies have relied on youth self-report of ADHD diagnosis. Further, prior studies have relied on youth self-reported concussion history and the present study collected parent reported concussion history using a structured brain injury questionnaire that included questions about injury occurrence but also alterations of consciousness to more clearly define the occurrence of concussion, that is, injuries that involved a loss of consciousness, posttraumatic amnesia, or feeling dazed.
Moreover, this study is the first to examine the potential association between ADHD symptom domains (i.e., inattention and hyperactivity/impulsivity symptoms) and history of concussion. Contrary to our hypothesis, we did not find an association between history of concussion and ADHD symptoms among children with ADHD. Prior studies that have reported an association have involved community samples of children with dental injuries, who were not formally diagnosed with ADHD, and examined questionnaires that assess ADHD-like symptoms, 11,12 whereas in the current study we explicitly examined the number of ADHD symptoms, based on diagnostic criteria, that parents endorsed during structured diagnostic interviews.
Clinical considerations
There are three important broader clinical considerations regarding concussions and ADHD. First, despite higher rates of concussion among those with ADHD, based on the available evidence, ADHD does not appear to be associated with worse clinical outcome or prolonged concussion recovery. 31 With that said, there are major methodological weaknesses and limitations in the concussion outcome literature that preclude definitive conclusions and more research is needed to clarify our understanding of the role of ADHD in concussion recovery and better inform clinical practice. 31 Second, treatment with ADHD medication is associated with a lower risk for hospital admissions with brain injuries. 32 Medication for ADHD might also lower risk for concussions, though direct evidence regarding concussions, as opposed to more severe head injuries, is lacking.
Finally, the clinical evaluation of children with ADHD who have sustained a concussion can be more nuanced and complicated because children with ADHD report more concussion-like symptoms in their daily lives in the absence of injury 33 -35 and on average perform a little more poorly on some concussion assessments in the absence of concussion. 34 This can potentially complicate the interpretation of symptoms following concussion, especially as more time passes since the injury. Expecting a child with ADHD to be completely asymptomatic prior to returning to full participation in all activities, when in fact ongoing symptoms are not concussion-related per se, might unnecessarily prolong their removal from beneficial and health-promoting physical and social activities. 36
Limitations
The ABCD Study data used in the analyses was from the baseline assessment wave, meaning data were cross-sectional and concussion history was retrospective. These injuries could have occurred at variable times over the course of development. It is possible that an association between ADHD symptom burden and concussion rates might be found among more recent concussions as opposed to remote concussions, sustained years prior. Moreover, the OTBI injury incidence questions are broad and multi-faceted (e.g., combining sports injuries with falls). Ideally, we would be able to examine rates of concussion among discrete injury mechanisms. Further, the OTBI injury incidence questions are not mutually exclusive which precludes us from calculating a number of prior lifetime injuries. We thus were limited to examining whether or not children had at least one prior concussion.
Conclusion
In the U.S. general population of children between the ages of 9 and 10, lifetime history of concussion is greater in boys (4.4%) than in girls (2.8%). Boys (7.3%) and girls (6.9%) with ADHD have higher rates of concussion than children who do not have ADHD, but their rates, at this age, do not differ based on gender. We find here that although ADHD may confer greater risk for sustaining concussion during early childhood, that risk is not clearly attributable to greater ADHD symptom burden (i.e., more symptomatic children being more likely to sustain concussions). There was an association between socioeconomic status and concussion, in that parents in the highest income category reported greater rates of concussion in their children (4.5%) than parents in the lowest income category (2.2%), although the proportional comparisons of lifetime concussions in children with and without ADHD in these two income categories did not differ. It is possible that parents in the highest income category have more concussion knowledge, and concern, and greater access to health care, reflecting possible social disparities in health and healthcare, which could explain this more general association with SES.
Footnotes
Authors' Contributions
Dr. Cook helped conceptualize the study, conceptualized the statistical analyses, conducted the statistical analyses, drafted sections of the manuscript, assisted with the literature review, edited the manuscript, and approved the final manuscript.
Dr. Karr drafted sections of the manuscript, critically reviewed and edited/approved the final manuscript.
Dr. Iverson helped conceptualize the study, assisted with the literature review, drafted sections of the manuscript, edited the manuscript, and approved the final manuscript.
All authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.
Funding Information
Dr. Nathan Cook acknowledges support from the Louis V. Gerstner III Research Scholar Award from Massachusetts General Hospital. Dr. Grant Iverson acknowledges unrestricted philanthropic support from the Mooney-Reed Charitable Foundation, Heinz Family Foundation, Boston Bolts, ImPACT® Applications, Inc., National Rugby League, and the Spaulding Research Institute.
Author Disclosure Statement
Dr. Iverson has a clinical practice in forensic neuropsychology, including expert testimony, involving individuals who have sustained mild TBIs. He has received research support from the Harvard Integrated Program to Protect and Improve the Health of NFLPA Members, and a grant from the National Football League. He serves as a scientific advisor for BioDirection, Inc, Sway Medical, Inc., and Highmark, Inc.
For the other authors, no competing financial interests exist.
