Skip to main content
NCBI home page
NIHPA Author Manuscripts logoLink to NIHPA Author Manuscripts
. Author manuscript; available in PMC: 2023 Aug 1.
Published in final edited form as: J Dev Behav Pediatr. 2022 Feb 15;43(6):e361–e369. doi: 10.1097/DBP.0000000000001067

The Impact of Pre-Injury and Secondary Attention Deficit Hyperactivity Disorder on Outcomes after Pediatric Traumatic Brain Injury

Megan E Narad a,b, Eloise E Kaizar c, Nanhua Zhang d, H Gerry Taylor e,f, Keith Owen Yeates g,h,i, Brad G Kurowski j,k, Shari L Wade j,b
PMCID: PMC9329149  NIHMSID: NIHMS1768906  PMID: 35170571

Abstract

Objective:

Examine the impact of pre-injury attention deficit hyperactivity disorder (PADHD) and secondary ADHD (SADHD) on outcomes following pediatric traumatic brain injury (TBI).

Method:

284 individuals ages 11–18, hospitalized overnight for a moderate-severe TBI were included. Parents completed measures of child behavior and functioning and their own functioning. Linear models examined the effect of ADHD status (PADHD vs. SADHD vs no ADHD) on child executive functioning (EF), social competence, and functional impairment, and parental depression and distress.

Results:

ADHD status had a significant effect on EF (F(2,269) = 9.19, p = .0001), social competence (F(2,263) = 32.28, p < .0001), functional impairment (F(2,269) = 16.82, p < .0001), parental depression (F(2,263) = 5.53, p = .005), and parental distress (F(2,259) = 3.57, p = .03). PADHD and SADHD groups had greater EF deficits, poorer social competence, and greater functional impairment than the no ADHD group. SADHD group had greater levels of parental depression than the no ADHD and PADHD groups, and SADHD had higher parental distress than the no ADHD group.

Conclusion:

Results highlight the importance of early identification and management of ADHD symptoms after injury to mitigate downstream functional problems. Supporting parents managing new-onset ADHD symptoms may also be important.

Keywords: Pediatric brain injury, Secondary attention deficit hyperactivity disorder, behavioral outcomes, parental distress

Traumatic brain injury (TBI) is the leading cause of acquired disability in children, affecting more than half a million children each year in the United States,1 often resulting in significant deficits in cognition, behavior, and social development.2 Children who sustain TBI are more likely to demonstrate greater behavioral impairment prior to their injury compared to their non-injured peers,3,4 and the incidence of children with behavioral disorders, including attention deficit hyperactivity disorder (ADHD), is greater among injured children than otherwise expected.3 Further, attention problems are among the most common long-term outcomes of childhood TBI5 with rates of secondary ADHD (SADHD), the development of ADHD after injury, ranging from 20%−50%,3,4,6,7 with highest rates among children with severe TBI.7

ADHD is characterized by developmentally inappropriate levels of inattention, hyperactivity, and/or impulsivity across multiple settings,8 and both pre-injury (PADHD) and SADHD have a significant impact on functioning post TBI. Previous studies have linked pre-morbid attention problems with poorer recovery after TBI.5,7 Yeates and colleagues5 noted that vulnerability to the effects of TBI depends in part on the child’s pre-morbid functioning. Specifically, the greater the premorbid difficulties, the more pronounced differences in long-term behavioral problems between children with TBI and those with orthopedic injuries. Interestingly, pre-morbid attention problems are not associated with universally poor outcomes after injury, as they do not appear to be consistently related to cognitive functioning and recovery.9 Further, clinically significant attention problems after TBI have been associated with a variety of negative psychosocial sequelae,4 with children with severe TBI and attention problems at particular risk for significant functional impairments.5

Beyond child/adolescent functioning, pediatric TBI has a significant impact on caregivers and families,10 with elevated levels of caregiver psychological distress even years after injury.11 Further, more than 1/3 of parents of children with TBI reporting clinically elevated levels of anxiety or depression.12 However, families of individuals with TBI are not universally distressed,13 highlighting the need to identify factors associated with greater levels of distress, and ADHD may be one such factor. Parents of children with more severe behavioral consequences following TBI report greater levels of distress.14 Parental distress and depression are not unique to families of children with TBI, and are also commonly reported by family members of uninjured children with ADHD.15 Moreover, parental and family environment have a significant impact on outcomes of TBI,3,16 and caregivers of children with SADHD after TBI report higher levels of family dysfunction than those of children without SADHD.4

Extant studies exploring the impact of ADHD (either PADHD or SADHD) on child and/or parental functioning after pediatric TBI have failed to directly compare these samples across outcomes. While there is a body of research documenting that a subgroup of individuals develop SADHD after pediatric TBI, most existing literature focuses on factors associated with development of SADHD or symptom presentation, with little known about the broader impact of the condition. To extend our knowledge regarding the impact of attention problems on outcomes following pediatric TBI, we examined the impact of both PADHD and SADHD on adolescent and parent outcomes following pediatric TBI. Finally, while SADHD and PADHD share apparent similarities in symptom presentation, there is some evidence that SADHD is not merely an acquired phenocopy of PADHD, and a broader understanding of the functioning of those with SADHD in relation to other subgroups of pediatric TBI survivors is required. We hypothesized that children with SADHD and children with PADHD would demonstrate greater executive functioning difficulties, impaired social functioning, and greater parental psychosocial distress following pediatric TBI compared to those with no ADHD. Additionally, due to their longer history of problems in attention, coupled with previous findings demonstrating greater post injury deficits among those with pre-injury behavioral difficulties, we hypothesized that children with PADHD would have greater deficits in executive functioning and social functioning and worse parent outcomes compared to those with SADHD.

METHOD

Participants

The dataset used in the present study was created by combining existing datasets from two previously completed, multi-center, randomized controlled trials of an online family-based problem-solving intervention for adolescents with a history of moderate to severe TBI (total n = 284). Only data from the baseline (pre-treatment) visit from both studies were included. It is worth noting that this sample is made up of TBI survivors and their parents who are interested/willing to participate in a behavioral intervention trial. While this group may differ from the broader adolescent TBI survivors it provides the detailed behavioral and family functioning measurements required to test our hypotheses. Study 1 included 132 participants, ages of 12–17 years, who had been hospitalized for a moderate to severe TBI (defined below) within the previous 6 months. Additional eligibility criteria included English as the primary language, and family residence within a 3-hour drive of site. Because the sample was recruited to participate in an intervention, teens were excluded if they were insufficiently recovered to actively participate, the parent or child had been psychiatrically hospitalized the year prior to the injury, the child resided outside the home, the child had premorbid intellectual disability (based on parent report), or lived in an area without broadband internet availability. Study 2 included 152 participants, ages 11–18 years, hospitalized for a moderate to severe TBI within the previous 18 months. Other eligibility criteria were identical to Study 1. Institutional Review Board approval was obtained for all procedures.

Procedures

Written informed consent/assent was completed by all participants and caregivers prior to the collection of any data. For both studies, baseline assessments were completed in the family’s home and included caregiver reports of the adolescent’s level of functioning and behavior, and parent self-reports of depression, psychological distress, and family functioning.

Measures

Injury Severity.

Injury severity was characterized using the lowest post resuscitation Glasgow Coma Scale (GCS) score assigned at the time of injury. Severe TBI was defined as a GCS score ≤ 8. Moderate TBI was defined as a GCS score of 9–12, or >12 with abnormal findings on clinical neuroimaging.

ADHD Behaviors/symptoms.

Child Behavior Checklist (CBCL)17.

The CBCL is a validated parent-report measure of child behavior problems and possesses high test-retest reliability and criterion validity. The Attention Deficit Hyperactivity DSM-Oriented scale was used to identify clinically significant attention problems as described below.

Identification of pre-morbid ADHD.

Families completed a Background Questionnaire (developed for this study) regarding their child’s functioning, mental health diagnoses and learning disorders prior to their injury. Teens whose parents reported a pre-injury diagnosis of ADHD or treatment with stimulant medication were included in the PADHD group.

Identification of SADHD.

Teens with SADHD could not have PADHD and had to meet one of the following criteria: 1) stimulant medication initiated after the injury, 2) parent report of new diagnosis of ADHD since the injury, or 3) a T-score ≥ 65 on the CBCL Attention Deficit Hyperactivity DSM-oriented scale.

Adolescent Adjustment.

Behavior Rating Inventory of Executive Function (BRIEF).18

The BRIEF is a parent-report measure assessing daily behaviors associated with EF. The BRIEF has strong psychometric properties and high ecological validity.18 The Metacognition Index (MI), Behavior Regulation Index (BRI), and General Executive Composite Scale (GEC) T-scores were used to assess the multiple dimensions of EF. Higher scores indicative of worse EF, and T-scores of 60–65 are considered mildly elevated and scores ≥ 65 are in the clinical range.

Home and Community Social Behavior Scales (HCSBS).19

The HCSBS is a 32-item parent-report measure of the teen’s social competence. The HCSBS has strong psychometric properties, and validity.20 Social competence composite T-score was used as the dependent variable, with higher scores indicating greater social competence.

Child and Adolescent Functional Assessment Scale (CAFAS).21

The CAFAS is a structured interview administered to parents that yields standardized ratings across multiple domains of everyday functioning, with good validity and excellent interrater reliability.21,22 For these studies, 10% of interviews were rated for reliability, yielding an overall interrater reliability of 95%. The CAFAS yields eight domain scores as well as a total score. Functioning in each domain is rated on an ordinal scale ranging from 0 (unimpaired) to 30 (severe impairment) in 10-point increments, and total score is created by summing domain scores (range: 0–240), with higher scores reflecting more impairment.

Parental Adjustment.

Center for Epidemiologic Studies Depression Scale (CES-D).23

The CES-D is a 20-item self-report measure of parental depressive symptomatology with well-established psychometric properties.23 The CES-D total score was used as a summary of parental depressive symptoms. Total scores range from 0–60 with higher scores indicative of greater symptomatology, and scores greater than 15 indicate potential clinical level of depressive symptoms.

Symptom Checklist-90-R (SCL-90).24

The SCL-90 is a 90-item self-report measure assessing global parental psychiatric symptoms and distress. The General Severity Index (GSI) T-score (M = 50, SD = 10) served as the measure of overall parental distress. The GSI combines the number of symptoms endorsed with the intensity of distress and is the most consistent, valid, and reliable score from the SCL-90-R.25

Data Analysis

Linear models were used to examine the effect of injury severity (moderate vs. severe), ADHD status (PADHD vs. SADHD vs. no ADHD), time since injury, parental education (proxy for SES, defined as > high school (HS) education, HS diploma, or < HS education of primary caregiver), and injury severity by ADHD interaction on each outcome. Study (study 1 vs. study 2) was included as a covariate to control for any study-specific differences. Participant sex and age at enrollment were originally included in the models, but ultimately trimmed from the models as they were not significant in any model. Dependent variables included BRIEF, HCSBS-Social Competence, and CAFAS-Total, and parent ratings on CESD Total and SCL-90-R-GSI.

Our null hypotheses of no effect of ADHD status on functioning and family distress were tested via F-tests of the main effect of ADHD status and its interaction with TBI severity. If this hypothesis is rejected, we use t-tests of differences of least squares means with Tukey corrections to examine pairwise comparisons within these significant effects and draw conclusions regarding our second hypothesis that PADHD has worse outcomes than SADHD. No additional multiple comparisons correction is needed for the tests of the first hypothesis, since the second hypotheses are nested within it. Rather than formally correcting for testing the five outcomes variables, we consider this factor in drawing conclusions from the whole study.

Beyond testing our primary hypotheses, we further explored possible interactions between time since injury and ADHD status for parental outcomes, and also report modeling results related to demographic and clinical variables. In cases where a continuous variable is of interest, using a median split to create classes within and across which we can compare scores allowed us to report interpretable patterns of mean score differences (as compared to reporting regression slopes). We assessed model assumptions via residual plots. Analyses were conducted using SAS version 9.4 (SAS Institute, Inc, Cary, NC).

RESULTS

Participants

Demographic information for the total sample (N = 284) and for each study are presented in Table 1. Consistent with eligibility criteria discussed above, time since injury was significantly greater in study 2 compared to study 1. The study samples did not statistically differ on other demographic characteristics. Means and standard deviations for each dependent variable by ADHD group are reported in Table 2. Throughout, visual inspection of model fit diagnostics revealed no model violations other than some residual distributions right-skewed due to boundary effects. We expect our results to be robust to this well-studied model property26.

Table 1.

Demographic information by study.

Variable Study 1 (n = 132) Study 2 (n = 152) Total (n = 284)
Severe TBI, n (%) 51 (38.6%) 67 (44.1%) 118 (41.5%)
Male, n (%) 86 (65.2%) 107 (70.4%) 193 (68.0%)
Caucasian, n (%) 106 (80.3%) 122 (80.3%) 228 (80.3%)
Parent education, n (%) > high school 71 (53.8%) 90 (59.2%) 161 (56.7%)
Age at injury (years) 14.55 (1.72) 14.39 (2.08) 14.46 (1.92)
Age at baseline (years) 14.85 (1.72) 14.87 (2.04) 14.86 (1.90)
Time since injury (months) 3.6 (1.80) 5.76 (4.08) 4.8 (3.36)
PADHD, n (%) 19 (14.4%) 22 (14.5%) 41 (14.4%)
SADHD, n (%) 22 (16.7%) 21 (13.8%) 43 (15.1%)
Open in a new tab

Note: TBI = traumatic brain injury, PADHD = Pre-injury Attention Deficit Hyperactivity Disorder, SADHD = Secondary Attention Deficit Hyperactivity Disorder.

Study 1 had significantly less time since injury at baseline than study 2.

Table 2.

Mean (SD) of each dependent variable, by ADHD group.

No ADHD SADHD PADHD Total
Mean (SD) Mean (SD) Mean (SD) Mean (SD)
BRIEF-MI 54.77 (9.00) 70.05 (9.15) 66.51 (9.27) 58.78 (10.99)
BRIEF-BRI 54.04 (11.08) 67.76 (11.45) 66.34 (12.39) 57.91 (12.77)
BRIEF GEC 54.79 (9.56) 70.40 (8.97) 67.85 (9.99) 59.06 (11.58)
HCSBS-SC 51.26 (8.23) 42.65 (8.16) 41.45 (8.11) 48.56 (9.20)
CAFAS 35.05 (32.38) 58.14 (35.00) 66.32 (36.04 42.87 (35.44)
CESD 11.73 (8.70) 17.34 (10.82) 12.26 (8.85) 12.65 (9.25)
SCL-90 52.99 (10.71) 58.08 (13.17) 56.20 (11.44) 54.22 (11.33)
Open in a new tab

Note: ADHD = Attention Deficit Hyperactivity Disorder, SADHD = Secondary Attention Deficit Hyperactivity Disorder, PADHD = Pre-injury Attention Deficit Hyperactivity Disorder; BRIEF-MI = Behavior Rating Inventory of Executive Functioning-Metacognitive Index; BRIEF-BRI = Behavior Rating Inventory of Executive Functioning-Behavior Regulation Index; BRIEF-GEC = Behavior Rating Inventory of Executive Functioning-Global Executive Functioning, HCSBS-SC = Home and Community Social Behavior Scale – Social Competence, CAFAS = Child and Adolescent Functional Assessment Scale, CESD = Center for Epidemiological Studies of Depression Scale; SCL-90 = Symptom Checklist-90

Adolescent outcomes

BRIEF-Scales

Metaconition Index (MI).

A main effect of ADHD status was observed (F(2,268) = 59.75, p < .0001). Those with no ADHD (M = 55.88, SE = .89) had significantly lower MI scores than those with SADHD (M = 70.34, SE = 1.48; t(268) = 9.44, p < .0001) and those with PADHD (M = 66.66, SE = 1.56, t(268) = 6.93, p < .0001). The difference between the SADHD and PADHD groups approached significance (t(268) = 1.84, p = .07). Neither injury severity, nor its interaction with ADHD status were significant. In examining the role of demographic and clinical covariates, a significant main effect of parent education was noted (F(2,268) = 4.82, p = .009), with parents who had more than a high school education (M = 62.42, SE = .87) reporting lower levels of MI dysfunction than those with a high school diploma (M = 65.92, SE = .98; t(268) = 3.09, p = .002).

Behavior Regulation Index (BRI).

ADHD status was significantly associated with BRI scores (F(2,267) = 37.04, p < .0001). Specifically, similar BRI scores were noted in the SADHD (M = 69.62, SE = 1.82) and PADHD (M = 66.70, SE = 1.92) groups, and both ADHD groups had significantly greater BRI scores than the no ADHD group (M = 55.86, SE = 1.10, all p’s > .0001). No effect of injury severity or its interaction with ADHD status were noted. Parent education had a significant effect on BRI scores (F(2,267) = 10.96, p < .0001). Parents with more than a high school education (M = 59.42, SE = 1.07) reported their child as having lower levels of BRI dysfunction than parents with less than a high school education (M = 67.49, SE = 2.63; t(267) = 2.95, p = .003) and parents with a high school diploma (M = 65.27, SE = 1.20; t(267) = 4.19, p < .001).

General Executive Composite (GEC).

ADHD status is significantly associated with GEC scores (main effect: F(2,269) = 63.24, p < .0001, TBI severity interaction: F (2,269) = 3.64, p = .03). Figure 1 illustrates the least squares mean GEC for each cross-classification of TBI severity and ADHD status. Within TBI severity group, we see no significant divergence between the PADHD and SADHD groups (all p’s > .05), although each is significantly different from the no ADHD group (all p < 0.001). Exploratory analysis of demographic and clinical covariates only found a significant main effect for parent education, F(2,269) = 9.19, p =.0001. On average, lower GEC scores, reflecting better EF, were reported by parents with more than a high school education, M= 61.99, SE = .89, than by parents with a high school diploma, M= 66.83, SE = 1.00; t(269) = 4.11, p = .0002.

Figure 1.

Figure 1.

Open in a new tab

Visual representation of ADHD status by TBI severity interaction on BRIEF – GEC

Note: Moderate = Moderate Traumatic Brain Injury; Severe = Severe Traumatic Brain Injury; No ADHD = No Attention Deficit Hyperactivity Disorder; SADHD = Secondary Attention Deficit Hyperactivity Disorder; PADHD = Pre-injury Attention Deficit Hyperactivity Disorder

Social Competence.

Results indicated a main effect of ADHD status, F(2,263) = 32.28, p < .0001, but no significant interaction with TBI severity. Children with no ADHD had higher average scores than those with SADHD, t(263) = 5.85, p < .0001, or PADHD, t(263) = 6.423, p < .0001, but we saw little evidence for a difference between the two ADHD groups (t(263) = .51, p = .67). Among the other variables, we only saw evidence for a significant effect of parental education, F(2,263) = 7.01, p = .001. Children of parents with more than a high school education had higher social competence scores, M = 46.97 (SE = .79), than children of parents with a HS diploma, M = 43.23 (SE = .88), t(263) = 3.59, p = .0012.

CAFAS Total.

Main effect of ADHD status on the CAFAS Total score was significant, F(2,269) = 16.821, p < .0001, but the interaction with TBI severity was not. Children with no ADHD averaged lower CAFAS scores than those with SADHD, t(269) = 3.96, p = .0003, and PADHD, t(269) = 4.84, p < .0001, but we saw no significant difference between SADHD and PADHD (t(269) = .96, p < .60). Additional significant main effects were time since injury, F(1,269) = 7.40, p = .007 and parental education, F(2,269) = 6.18, p = .002. Children with time since injury less than 0.32 years had higher CAFAS scores (poorer overall functioning) M = 64.85 (SE = 4.03), as compared with children with greater time since injury, M = 51.31 (SE = 3.79). Children of parents with more than a high school education had less functional impairment, M = 46.92 (SE = 3.12) than children of parents with a high school diploma, M = 59.60 (SE = 3.55); t(269) = 3.06, p = .007, or less than a high school education, M = 66.25, (SE = 8.03), t(269) = 2.34, p = .05.

Parental outcomes

Parental Depression (CES-D).

A significant main effect was found for ADHD status, F(2,263) = 5.53, p = .005, such that mean scores were smallest for parents of children with no ADHD (M = 11.95, SE = .89) followed by PADHD (M = 12.20, SE = 1.61) and SADHD (M = 17.13, SE = 1.53). The data contained no evidence that the lowest two groups differ significantly and strong evidence that the lowest (no ADHD) and highest (SADHD) means are significantly different (t(263) = 3.31, p = .003). Our multiple testing procedure leaves us with the difficult-to-interpret statistical result of borderline evidence (t(263) = 2.34; p = 0.05) for a difference between the SADHD and PADHD groups.

Exploratory follow-up analysis regarding whether time since injury had a differential effect on parental depression based on ADHD status revealed a significant interaction (F(2,261) = 5.79, p = .004). Figure 2a highlights the uniquely high depression score of the group of parents whose children had SADHD and were injured more than 0.32 years. Specifically, this group had significantly greater depression scores than all other groups(all p-values < 0.05). Among the remaining groups, no pairwise comparisons reached statistical significance (p-values > 0.4). However, we note a possible but not statistically significant trend of decreasing estimated average scores with increased time since injury among the no ADHD and PADHD groups.

Figure 2a.

Figure 2a.

Open in a new tab

Visual representation of time since injury by ADHD group interaction on parental depression (CES-D).).

Note: CES-D = Center for Epidemiological Studies of Depression Scale; SCL-90 = Symptom Checklist-90-R ADHD = attention deficit hyperactivity disorder; SADHD = secondary attention deficit hyperactivity disorder; PADHD = primary attention deficit hyperactivity disorder.

* = p≤ .05 before multiple testing correction

Parental Distress (SCL-90).

Analysis of the SCL-90 revealed a main effect for ADHD status, F(2,259) = 3.57, p = .03. Exhibiting an anomaly of multiple testing procedures, none of the ADHD groups statistically significantly differed, but the larger average reported levels of distress among parents of children with SADHD as compared to parents of children without ADHD nearly met our threshold (t(259) = 2.35, p = .05). In follow-up exploration of whether time since injury had a differential effect on parental distress based on ADHD status, we found a significant interaction (F(2,257) = 3.45, p = .03). Figure 2b shows that parental distress exhibits a similar pattern to parental depression, though slightly less extreme. The only pairwise difference that reached statistical significance is that the SADHD group exhibited more distress than the no ADHD group among families whose child was injured more than 0.32 years ago. Again, though comparisons did not retain statistical significance after multiple testing corrections, parents in the No ADHD and PADHD groups whose child was injured more than 0.32 years ago reported lower distress than their counterparts whose child was injured more recently.

Figure 2b.

Figure 2b.

Open in a new tab

Visual representation of time since injury by ADHD group interaction on levels of parental distress (SCL-90).

Note: CES-D = Center for Epidemiological Studies of Depression Scale; SCL-90 = Symptom Checklist-90-R ADHD = attention deficit hyperactivity disorder; SADHD = secondary attention deficit hyperactivity disorder; PADHD = primary attention deficit hyperactivity disorder.

* = p≤ .05 before multiple testing correction

DISCUSSION

Our findings show that adolescents with TBI and either PADHD or SADHD have worse adolescent adjustment, with more deficits in EF, social competence, and behavioral functioning than injured adolescents without ADHD. Although we expected to see differences across ADHD status, adolescents with PADHD and SADHD were rated as having similar levels of impairment in these outcomes. Supporting our hypotheses, parents of children with SADHD had greater levels of depression and distress that met or approached statistical significance than parents of children without ADHD. However, counter to expectations that depression and distress would be greatest in the PADHD group, parents of children with PADHD and those without ADHD reported less depression and distress than did parents of children with SADHD. These parental group differences are particularly interesting given the surprisingly limited effects of TBI severity on the outcomes examined, as severe TBI was only associated with poorer EF outcomes in the absence of ADHD.

The finding of greater parental depression and distress in the SADHD group relative to both the PADHD and no ADHD groups was unexpected. Further, the absence of elevated distress in parents of children with PADHD is in direct contrast to adolescent outcomes with SADHD and PADHD groups displaying similar levels of executive, social, and behavioral functioning. There is an extensive literature documenting the impact having a child with ADHD has on a family. Specifically, parents of children with ADHD report greater levels of distress than do parents of typically developing children,27 as well as clinic-referred children without ADHD.28 Interestingly, ADHD symptom severity is one of the most consistently reported predictors of parenting distress;27 however, this is does not seem to be the case in the current study as both ADHD groups have similar levels of behavioral functioning.

We hypothesized that the parents of children with PADHD would have greater levels of distress and burden due to their children having a longer history of behavioral difficulties compared to parents of children with novel symptoms of ADHD after their injury (SADHD); however, this was not the case. Rather, parents of children with SADHD reported the greatest level of distress after their child’s injury. This may be the first time that parents of children with SADHD are faced with managing challenging behaviors in their child, while parents of children with PADHD have a history of dealing with their child’s symptoms, and have likely developed some strategies for managing their child’s behaviors prior to the TBI. Notably, parental self-efficacy or their perceived control of the child’s behavior is a significant predictor of parental distress in families of uninjured children with ADHD.27 Therefore the experience parents of children with PADHD have in managing their child’s behavior prior to their TBI may be associated with greater self-efficacy in managing challenging behavior post injury. As a result, when faced with similar levels of behavioral functioning as those with SADHD, they may feel more equipped to manage behaviors, and therefore experience less stress than parents of children with SADHD who have not faced this challenge in the past.

We also explored the role of time since injury on parental outcomes, and interestingly, longer time since injury had unique negative impact on parents of children with SADHD. While parents of children with no ADHD reported similar or lower levels of depression and distress at longer, rather than shorter, time since injury, among parents of children with SADHD longer time since injury was associated with greater levels of parental depression and distress. Previous studies have noted that parent/family distress and burden that persist many years after TBI,11 and are influenced by injury severity,29 poorer neuropsychological functioning,30 greater functional impairment,29 and greater child behavioral difficulties.16,29 Indeed, Max and colleagues31 noted that one of the factors that most influenced family functioning after TBI was the child’s development of a novel psychiatric disorder after injury, and findings from the present study suggest that new onset attention problems (SADHD) may be a factor associated with prolonged parent/family distress after injury.

Importantly these findings suggest that SADHD may pose a unique injury-related burden for families following adolescent TBI, and have important clinical implications. The association of parental depression with childhood dysfunction, coupled with the notion of a transactional/bidirectional relationship between parental distress and child behavior following pediatric TBI,16 highlights the importance of identifying this at risk group. The goal should be to intervene early and provide parents with strategies for managing difficult behaviors, to prevent the cycle of new onset behavior problems, increased parental distress, increased negative parenting strategies, and worsening of child behavior.

The one significant difference in outcomes as a function of injury severity involved greater executive dysfunction in those with severe versus moderate TBI among children with no ADHD. Injury severity was not associated with outcomes for adolescents with either PADHD or SADHD, suggesting that ADHD may have obscured injury-related effects. Aside from the EF, the limited effect of injury severity was somewhat surprising. Although many studies have reported a dose-response relationship between TBI severity and outcomes across domains,32–35 neurobehavioral outcomes following pediatric TBI are multiply determined. Notably, we relied on GCS to define injury severity, and while this is the most common method for defining injury severity, it may not be the most accurate predictor of functional outcome. Additionally, all participants were enrolled within the first 18 months post-injury, and while recovery may be most pronounced during this period, children may also experience emerging deficits throughout development.36 Examples of late effects are provided by reports of neurocognitive stall,37 chronic/persistent impairments beyond this 1–2 year mark,38 and a widening performance gap with increasing time since injury between those with severe TBI and those with less severe injuries.39 The lack of evidence for effects of injury severity in this study may be related to the acute stage of recovery, when differences in outcomes for adolescents with severe vs. more moderate TBI may be less apparent. A second potential reason may be related to the limited range of severity. Because the assessment was a baseline assessment as part of an intervention trial, and while the participants were required to have recovered sufficiently in order to actively engage in a therapeutic intervention prior to enrollment, it is possible that it is possible that the moderate TBI group may be a bit biased towards those with greater impairment and in need of intervention.

Beyond EF, the similarity in functioning between the ADHD groups was surprising. Previous research has shown that children/adolescents with pre-injury attention problems experience greater impairment following TBI,4,5 and the development of SADHD following injury is also associated with more functional impairment,3,4,9 but few studies have directly compared the functional outcomes of these two groups. The current findings suggest that ADHD-related impairments develop early in recovery (within the first 18 months) and may not be the result of chronic exposure to the negative academic and social consequences of attentional impairment.

Findings should be considered within the context of limitations. First, ADHD status was identified based only on parent report, with no information regarding symptoms or impairment in other settings or objective measures of attentional or executive functioning. This is especially relevant for the PADHD group which relied exclusively on parent report of diagnosis or treatment prior to their injury. While this method is less than ideal due to concerns related to accuracy of parental retrospective reporting, it has been demonstrated that maternal retrospective report of psychopathology is both reliable and accurate, with excellent reliability and accuracy for retrospective report of a previous ADHD diagnosis.40 Ideally, future studies would take a prospective approach or seek documentation to support previous diagnoses or treatment for ADHD prior to their injury. Further, the SADHD cutoff, while consistent with other studies, was in the ‘borderline-clinical range’. While the CBCL Attention Problems score has been shown to be highly convergent with a diagnosis of ADHD on a diagnostic interview and has been shown to be sensitive to ADHD after TBI,3 it is not consistent with the gold standard diagnostic process. Future studies would benefit from a more rigorous diagnostic process including administration of structured diagnostic interview and obtaining teacher symptom ratings to better document ADHD symptoms and impairments across settings, allow for more fine-grained analysis of the association of symptom domain and areas of impairment, and potentially include objective assessment measures of functioning. Similarly, the BRIEF is also often used for evaluation of ADHD, and there are some items that may overlap with items on the CBCL. While the BRIEF does not specifically contain symptoms of ADHD or provide diagnostic findings, the overlap in symptoms is worth noting. Further, heritability of developmental ADHD is quite high; however, we do not have information regarding family history of ADHD in this sample. Future studies should include examination of family history of ADHD to further investigate whether family history of PADHD influences development of SADHD after TBI.

While the provision of a computer or internet services to families who did not have these technologies in their home aimed to improve access to the study and intervention delivered in the trial, those who resided in areas without broadband internet services were excluded from the study which likely excluded families in more rural areas as well as those with greater health disparities. The sample consisted of children with moderate-severe TBI, limiting our ability to determine how findings compare to a non-injured ADHD sample or a healthy non-injured sample, and findings cannot be extended to ADHD-associated outcomes in children with milder injuries. As discussed, our exclusive use of GCS to define injury severity may have limited our ability to detect injury severity related effects. While GCS is the most commonly used means of determining severity to predict outcome, recent research suggests that inclusion of additional medical variables such as prehospitalization loss of consciousness, intubation and seizures can improve the prediction of outcomes.41 In addition, the cross-sectional nature of our study does not allow for determination of directionality or causation of our effects. For example, while our results suggest that parents of children with SADHD have greater levels of distress with greater passage of time since injury, we are not able to determine if this difference represents increase in distress over time. Similarly, we are unable to determine if parents develop increased distress because of their child’s symptoms of ADHD or if parents with greater levels of distress have a lower level of tolerance towards their child’s attentional or behavioral impairments. Along these lines, time since injury was confounded by study, and while this was controlled for within the models, it should be considered when interpreting time since injury findings. Future studies would benefit from prospective designs, gathering information about both parent and child functioning, to help better understand the nature of this relationship.

Of note, participants included children and caregivers agreeing to participate in an intervention trial, who may not be representative of the broader population of adolescents with TBI; however, it should be noted that only 5% of participants were excluded due to level of functioning. Notably, there was no impairment threshold required for enrollment in the parent trials, and adolescent and parental functioning as measured in the current study are largely in the normal range, indicating our sample was not overly pathological/symptomatic. Finally, the use of parent report on all outcome measures should also be considered. While the CAFAS is a structured interview scored by trained coders unaware of the child’s diagnostic status (ADHD versus no ADHD), responses are still gathered from the parent. In order to limit issues with common method variance, future studies would benefit from collecting data via a variety of methods including adolescent report, teacher report, objective measures, and physiological methods when possible.

Despite these limitations, the results are consistent with previous research showing that children with PADHD demonstrate more impairment across behavioral domains following injury than those without ADHD. Impairment in adolescents with new-onset ADHD symptoms following moderate-to-severe TBI is also greater than in adolescents without ADHD but similar to levels observed in adolescents with PADHD. The results highlight the importance of identifying children with elevated ADHD symptoms soon after injury to manage symptoms early in recovery and mitigate downstream functional problems. Providing support to parents working to manage new-onset symptoms of ADHD, in addition to other sequelae of TBI, may potentially prevent or minimize post-injury parental distress.

Conflicts of Interest and Source of Funding:

This project was supported by the National Institute of Child Health and Human Development (1R21HD089076-01 1F32HD088011-1). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Data from the following clinical trials were used in this study: NCT01042899 and NCT 00409448. No conflicts of interest declared

References

  • 1.Thurman DJ. The Epidemiology of Traumatic Brain Injury in Children and Youths: A Review of Research Since 1990. J Child Neurol. 2016;31(1):20–27. [DOI] [PubMed] [Google Scholar]
  • 2.Anderson V, Brown S, Newitt H, et al. Long-term outcome from childhood traumatic brain injury: intellectual ability, personality, and quality of life. Neuropsychology. 2011;25(2):176–184. [DOI] [PubMed] [Google Scholar]
  • 3.Gerring J, Brady KD, Chen A, et al. Premorbid prevalence of ADHD and development of secondary ADHD after closed head injury J Am Acad Child Adolesc Psy. 1998;37(6):647–654. [DOI] [PubMed] [Google Scholar]
  • 4.Max JE, Lansing AE, Koele SL, et al. Attention deficit hyperactivity disorder in children and adolescents following traumatic brain injury. Dev Neuropsychol. 2004;25(1–2):159–177. [DOI] [PubMed] [Google Scholar]
  • 5.Yeates KO, Armstrong K, Janusz J, et al. Long-term attention problems in children with traumatic brain injury. J Am Acad Child Adolesc Psy. 2005;44(6):574–584. [DOI] [PubMed] [Google Scholar]
  • 6.Max JE, Arndt S, Castillo CS, et al. Attention-deficit hyperactivity symptomatology after traumatic brain injury: a prospective study. J Am Acad Child Adolesc Psy. 1998;37(8):841–847. [DOI] [PubMed] [Google Scholar]
  • 7.Schachar R, Levin HS, Max JE, et al. Attention deficit hyperactivity disorder symptoms and response inhibition after closed head injury in children: do preinjury behavior and injury severity predict outcome? Dev Neuropsychol. 2004;25(1–2):179–198. [DOI] [PubMed] [Google Scholar]
  • 8.American Psychiatric Association D-TF. Diagnostic and Statistical Manual of Mental Disorders: DSM-5. 5th ed. Arlington, VA: Amerincan Psychiatric Publishing, Inc.; 2013. [Google Scholar]
  • 9.Ornstein TJ, Sagar S, Schachar RJ, et al. Neuropsychological performance of youth with secondary attention-deficit/hyperactivity disorder 6- and 12-months after traumatic brain injury. J Int Neuropsychol Soc. 2014;20(10):971–981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Aitken ME, McCarthy ML, Slomine BS, et al. Family burden after traumatic brain injury in children. Pediatrics. 2009;123(1):199–206. [DOI] [PubMed] [Google Scholar]
  • 11.Wade SL, Taylor HG, Yeates KO, et al. Long-term parental and family adaptation following pediatric brain injury. J Pediatr Psychol. 2006;31(10):1072–1083. [DOI] [PubMed] [Google Scholar]
  • 12.Wade SL, Taylor HG, Drotar D, et al. Family burden and adaptation during the initial year after traumatic brain injury in children. Pediatrics. 1998;102(1 Pt 1):110–116. [DOI] [PubMed] [Google Scholar]
  • 13.Perlesz A, O’Loughlan M. Changes in stress and burden in families seeking therapy following traumatic brain injury: a follow-up study. Int J Rehabil Res. 1998;21(4):339–354. [DOI] [PubMed] [Google Scholar]
  • 14.Lax Pericall MT, Taylor E. Family function and its relationship to injury severity and psychiatric outcome in children with acquired brain injury: a systematized review. Dev Med Child Neurol. 2014;56(1):19–30. [DOI] [PubMed] [Google Scholar]
  • 15.Johnston C, Mash EJ. Families of children with attention-deficit/hyperactivity disorder: review and recommendations for future research. Clin Child Fam Psych. 2001;4(3):183–207. [DOI] [PubMed] [Google Scholar]
  • 16.Taylor HG, Yeates KO, Wade SL, et al. Bidirectional child-family influences on outcomes of traumatic brain injury in children. J Int Neuropsychol Soc. 2001;7(6):755–767. [DOI] [PubMed] [Google Scholar]
  • 17.Achenbach TM. Manual for the Child Behavior Checklist/4–18 and 1991 Profile. Burlington, VT: University of Vermot, Department of Psychiatry.; 1991. [Google Scholar]
  • 18.Gioia G, Isquith PK, Guy SC, et al. BRIEF: Behavior Rating Inventory of Executive Function. Lutz, FL: Psychological Assessment Resources, Inc.; 2000. [Google Scholar]
  • 19.Merrell K School Social Behavior Scales User’s Guide (2nd ed). Eugene, OR: Assesment-Intervention Resources; 2002. [Google Scholar]
  • 20.Merrell KW, Caldarella P. Social-behavioral assessment of at-risk early adolescent students: Psychometric characteristics and validity of a parent report for of the School Social Behavior Scales. J Psychoeduc Assess. 1999;17(1):36–49. [Google Scholar]
  • 21.Hodges K The Child and Adolescent Fucntional Assessment Scale Self-Training Manual. Ypsilanti, MI: Eastern Michigan University, Department of Psychology; 1994. [Google Scholar]
  • 22.Hodges K, Wong MM. Psychometric Characteristics of a Multidimensional Measure to Assess Impairment: The Child and Adolescent Functional Assessment Scale. J Child Fam Stud. 1996;5(4):445–467. [Google Scholar]
  • 23.Radloff LS. The CES-D Scale: A Self-Report Depression Scale for Research in the General Population. Appl Psych Meas. 1977;1(3):385–401. [Google Scholar]
  • 24.Derogatis LR. The Brief Symptom Inventory (BSI) administration, scoring, and procedures manual. Minneapolis, MN: National Computer Systems; 1993. [Google Scholar]
  • 25.Bonynge ER. Unidimensionality of SCL-90-R scales in adult and adolescent crisis samples. J Clin Psych. 1993;49(2):212–215. [DOI] [PubMed] [Google Scholar]
  • 26.Schmidt AF, Finan C. Linear regression and the normality assumption. J Clin Epidemiol. 2018;98:146–151. [DOI] [PubMed] [Google Scholar]
  • 27.Theule J, Wiener J, Tannock R, et al. Parenting stress in families of children with ADHD: A meta-analysis. J Emot Behav Disord. 2013;21:3–17. [Google Scholar]
  • 28.Craig F, Operto FF, De Giacomo A, et al. Parenting stress among parents of children with Neurodevelopmental Disorders. Psychiat Res. 2016;242:121–129. [DOI] [PubMed] [Google Scholar]
  • 29.Anderson VA, Catroppa C, Haritou F, et al. Predictors of acute child and family outcome following traumatic brain injury in children. Pediatr Neurosurg. 2001;34(3):138–148. [DOI] [PubMed] [Google Scholar]
  • 30.Barry CT, Taylor HG, Klein S, et al. Validity of neurobehavioral symptoms reported in children with traumatic brain injury. Child Neuropsychol. 1996;2:213–226. [Google Scholar]
  • 31.Max JE, Castillo CS, Robin DA, et al. Predictors of family functioning after traumatic brain injury in children and adolescents. J Am Acad Child Psychiat. 1998;37(1):83–90. [DOI] [PubMed] [Google Scholar]
  • 32.Catroppa C, Anderson V. A prospective study of the recovery of attention from acute to 2 years following pediatric traumatic brain injury. J Int Neuropsychol Soc. 2005;11(1):84–98. [DOI] [PubMed] [Google Scholar]
  • 33.Wade SL, Taylor HG, Drotar D, et al. A prospective study of long-term caregiver and family adaptation following brain injury in children. J Head Trauma Rehabil. 2002;17(2):96–111. [DOI] [PubMed] [Google Scholar]
  • 34.Catroppa C, Godfrey C, Rosenfeld JV, et al. Functional recovery ten years after pediatric traumatic brain injury: outcomes and predictors. J Neurotrauma. 2012;29(16):2539–2547. [DOI] [PubMed] [Google Scholar]
  • 35.Yeates KO, Gerhardt CA, Bigler ED, et al. Peer relationships of children with traumatic brain injury. J Int Neuropsychol Soc. 2013;19(5):518–527. [DOI] [PubMed] [Google Scholar]
  • 36.Babikian T, Asarnow R. Neurocognitive outcomes and recovery after pediatric TBI: meta-analytic review of the literature. Neuropsychology. 2009;23(3):283–296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Chapman SB. Neurocognitive stall, a paradox in long term recovery from pediatric brain injury. Brain Injury Professional. 2006;3(4):10–13. [Google Scholar]
  • 38.Mangeot S, Armstrong K, Colvin AN, et al. Long-term executive function deficits in children with traumatic brain injuries: assessment using the Behavior Rating Inventory of Executive Function (BRIEF). Child Neuropsychol. 2002;8(4):271–284. [DOI] [PubMed] [Google Scholar]
  • 39.Beauchamp M, Catroppa C, Godfrey C, et al. Selective changes in executive functioning ten years after severe childhood traumatic brain injury. Dev Neuropsychol. 2011;36(5):578–595. [DOI] [PubMed] [Google Scholar]
  • 40.Faraone SV, Biederman J, Milberger S. How reliable are maternal reports of their children’s psychopathology? One-year recall of psychiatric diagnoses of ADHD children. J Am Acad Child Adolesc Psychiatry. 1995;34(8):1001–1008. [DOI] [PubMed] [Google Scholar]
  • 41.Keenan HT, Clark AE, Holubkov R, et al. Latent Class Analysis to Classify Injury Severity in Pediatric Traumatic Brain Injury. Journal of Neurotrauma. 2020. [DOI] [PMC free article] [PubMed] [Google Scholar]

RESOURCES