Published online June 2, 2008
PEDIATRICS Vol. 121 No. 6 June 2008, pp. e1686-e1695 (doi:10.1542/peds.2007-2461)
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow E-mail this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My File Cabinet
Right arrow Download to citation manager
Right arrowRequest Permissions
Citing Articles
Right arrow Citing Articles via CrossRef
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Sesma, H. W.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Sesma, H. W.
Related Collections
Right arrow Emergency Medicine
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Facebook   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?

ARTICLE

Executive Functioning in the First Year After Pediatric Traumatic Brain Injury

Heather Whitney Sesma, PhDa, Beth S. Slomine, PhDb,c, Ru Ding, MSd, Melissa L. McCarthy, MS, ScDd the Children's Health After Trauma (CHAT) Study Group

a Department of Pediatrics, University of Minnesota, Minneapolis, Minnesota
b Department of Neuropsychology, Kennedy Krieger Institute, Baltimore, Maryland
c Departments of Psychiatry
d Emergency Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
BACKGROUND AND OBJECTIVE. Children with traumatic brain injuries often show impaired executive function (the ability to carry out goal-directed behavior). The Behavior Rating Inventory of Executive Function, a caregiver-report questionnaire, measures executive function in everyday activities. In this study, our goal was to use the Behavior Rating Inventory of Executive Function to document changes in children's executive function in the first year after traumatic brain injury and identify child, family, and injury variables associated with greater dysfunction. We predicted that children with traumatic brain injury would have more executive dysfunction than children hospitalized for orthopedic fractures and that more severe traumatic brain injury would predict greater dysfunction. Children's premorbid functioning and family characteristics were expected to moderate their executive function.

PATIENTS AND METHODS. Caregivers of children aged 5 to 15 years (330 mild-to-severe traumatic brain injury, 103 control orthopedic fractures) enrolled onto a longitudinal study of executive function. Caregivers completed the Behavior Rating Inventory of Executive Function by telephone at baseline (obtained retrospectively) and 3 months and 1 year after the injury.

RESULTS. Traumatic brain injury groups and controls showed no baseline differences in Behavior Rating Inventory of Executive Function scores. Three months after the injury, children with traumatic brain injury had more dysfunction than controls on the Global Executive Composite. One year after injury, all traumatic brain injury groups differed from the controls on the Behavioral Regulation Index, Metacognition Index, and Global Executive Composite. The working memory scale was the only scale to discriminate between the control group and all 3 traumatic brain injury severity groups at both 3 and 12 months after injury. Executive-function ratings remained stable from 3 to 12 months after injury. Across time points, preexisting learning/behavior problems, lower respondent education, and poor family functioning predicted greater Global Executive Composite dysfunction.

CONCLUSIONS. Between 18% and 38% of the children with traumatic brain injury had significant executive dysfunction in the first year after injury, with greater dysfunction reported for children with more severe traumatic brain injury. Our findings support previous reports that preinjury learning and behavior problems, limited family resources, and poor family functioning adversely affect executive function. These results suggest a need for more systematic screening for executive dysfunction after traumatic brain injury to increase recognition of cognitive disability and improve access to appropriate services.

Key Words: executive function/dysfunction • traumatic brain injury • cognitive function

Abbreviations: TBI—traumatic brain injury • BRIEF—Behavior Rating Inventory of Executive Function • GEE—generalized estimating equation • AIS—Abbreviated Injury Scale • NISS—New Injury Severity Scale • GEC—Global Executive Composite

Traumatic brain injury (TBI) in children represents a significant public health problem in the United States, causing an estimated 435 000 emergency department visits and 37 000 hospitalizations annually among children aged 0 to 14 years.1 As many as 29 000 children experience new disability after TBI as a result of lasting changes in their physical, cognitive, social, and behavioral functioning.2 Despite its high incidence, TBI-related disability often goes unrecognized by caregivers, educators, and physicians. In particular, children's cognitive needs after TBI are commonly unmet or unrecognized.3 TBI was established as a special education disability category in the 1990 amendments to the Individuals With Disabilities Education Act, yet many children after TBI are either misclassified in the special education system or do not receive special education services at all.4,5

Deficits in executive functioning are among the most frequently reported areas of cognitive impairment after TBI.6–9 Executive functioning refers to an individual's ability to carry out goal-directed behavior and includes skills such as planning and sequencing multistep actions, inhibiting inappropriate behavior, and sustaining effort for extended periods of time.10,11 Typical development of these skills is protracted and depends on intact frontal-striatal circuits.12,13 However, these circuits are frequently damaged from TBI because they are distributed networks that run through common lesion sites (ie, frontal and prefrontal cortex) and are particularly vulnerable to the diffuse axonal injury that can occur from severe TBI.14,15

Several studies that examined executive functioning after TBI have documented deficits on performance-based measures soon after injury but significant improvement over time.6,16 Such improvements may be related to recovery from brain injury or practice effects from repeated test administrations. Performance-based measures may mask impairments, because they are administered in a distraction-free environment, the tests are highly structured, and they provide the child with cues as to how to respond.17,18 Therefore, the test demands and setting are markedly different from the child's real-world environment, which is often considerably less structured and filled with distractions but the child is expected to concentrate on required tasks, remember what to do next, and inhibit the impulse to engage in a more desirable activity instead. As a result, performance-based measures of executive functioning may overestimate a child's level of independence with everyday tasks at home and in the classroom. The Behavior Rating Inventory of Executive Function (BRIEF) was developed to capture caregiver and teacher observations regarding how a child may exhibit executive dysfunction during daily activities such as completing homework and household chores despite showing no evidence of impairment on more structured performance-based tasks.19 Multiple studies have demonstrated that the BRIEF is a reliable and valid measure of executive functioning in both typically developing children and children with TBI.8,17,20

Previous research has demonstrated that executive functioning measured by performance-based tests after TBI is moderated by a variety of factors, including severity of injury, age at injury, time since injury, premorbid functioning, and family functioning.6,16,21–23 Children who sustain more severe injuries and who are injured at younger ages show greater evidence of long-term impairments and slower rates of acquisition for new skills.6,9,16,24 Children with preexisting difficulties with inattention and hyperactivity are at higher risk for developing attention-deficit/hyperactivity disorder after TBI.25,26 Family factors such as family functioning, parent distress, and injury-related family burden also are associated with worse cognitive and behavioral outcomes after TBI.8,23,27

Although previous studies have used the BRIEF to measure executive dysfunction after TBI, each of them has relied on relatively small samples (<100 participants) and has been limited to 1 assessment, typically ≥1 year after injury.8,28,29 In this study, we built on previous work by examining caregiver responses on the BRIEF prospectively and longitudinally in a large sample of children hospitalized with a TBI or an orthopedic fracture to document changes in executive functioning in the first year after injury. In addition, we explored the role of injury, child, and family characteristics as potential moderators of reported executive functioning on the BRIEF by using a generalized estimating equation (GEE) model, a statistical approach that allows the influence of moderating variables to change over time while controlling for the autocorrelation associated with repeated assessments. We hypothesized that children who sustained a TBI would have more reported executive dysfunction than children who were hospitalized for orthopedic fractures and that more severe TBI would be associated with greater executive dysfunction. Furthermore, we predicted that child, family, and injury characteristics would moderate reported executive functioning.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Participants
Inclusion Criteria
Study participants were children between the ages of 5 and 15 years who sustained a TBI or an orthopedic fracture with an Abbreviated Injury Scale (AIS) severity score of ≥2 and were hospitalized for at least 1 night at 1 of 4 level I pediatric trauma center hospitals.30 Participating hospitals included Johns Hopkins Hospital (Baltimore, MD), Children's Hospital of Philadelphia (Philadelphia, PA), Harborview Medical Center (Seattle, WA), and Arkansas Children's Hospital (Little Rock, AR).

Exclusion Criteria
Potential participants were excluded if the child or his or her parents did not speak English or in cases of suspected child abuse. Children also were excluded if they had a preexisting medical condition that markedly affected their premorbid physical (eg, amputation), psychological (eg, bipolar disorder), or cognitive (eg, mental retardation) functioning. However, children with premorbid learning disabilities or behavioral problems were included to increase the generalizability of the findings and evaluate the role of preinjury risk factors on postinjury executive functioning.

Injury Severity
Injury severity was determined by using AIS head scores, because the AIS is the most commonly used anatomic measure of injury severity.31 To ensure an adequate number of subjects with more severe TBI, the sample was stratified according to TBI severity. Children with AIS head scores of 2, 3, and 4 were enrolled consecutively into their respective groups until each group included ~95 children. Target enrollment for the control, mild-TBI, and moderate-TBI study groups was set at 95 per group because a power analysis indicated that would be an adequate sample size to detect group differences of 3 to 5 T-score points or more among the BRIEF scores. Because of the relative infrequency of AIS 5 head injuries, the target enrollment for this group was 50.

Procedures
Institutional review boards from all participating institutions approved the study. Between January 15, 2002, and July 31, 2003, the study coordinators approached all eligible families and invited them to participate. Of the 541 families who were eligible, 433 (80%) enrolled by consenting and completing the baseline interview. Ninety percent of the original 433 families completed the 3-month telephone interviews, and 87% completed the 12-month interviews.

Medical charts were abstracted for background information related to the child's mechanism of injury, length of hospital stay, and disposition. In addition, all injuries sustained were classified, and their severity was rated by using the AIS.30,31 Each injury's severity was rated from 1 (minor) to 6 (unsurvivable) according to AIS criteria. Within this sample, representative head injuries for each level of severity included a closed skull fracture (AIS score: 2), comminuted skull fracture or subarachnoid hemorrhage (AIS score: 3), epidural or subdural hematoma (AIS score: 4), and diffuse axonal injury (AIS score: 5). Overall injury severity was quantified by using the New Injury Severity Scale (NISS), which is calculated by summing the squares of the AIS severity scores for the 3 most severe injuries sustained.32 Values on the NISS range from 0 to 75, with 75 signifying the greatest injury severity.

A professional survey research firm conducted all interviews with 1 of the injured child's primary caregivers. Interviews took place within 3 weeks of hospitalization (baseline) and again 3 and 12 months after the injury. During the baseline interview, caregivers reported on the child's preinjury executive functioning and provided background information on the child and family. In subsequent interviews, caregivers reported on the child's behavior during the preceding month. Respondents were queried about the child's age, race, health insurance status, and any premorbid medical conditions or problems with learning and behavior. Prevalent conditions included asthma (18%), allergies (17%), problems with attention (12%), learning disabilities (11%), and behavioral problems (7%). The preinjury prevalence rates of learning and behavior problems in this sample were somewhat higher than those found in the general population but similar to rates reported in other samples of children who had sustained TBI.21,33

Respondents also provided information on their age, race, marital status, level of education, annual household income, and relationship to the child. They also rated their family's overall family functioning by completing the general functioning scale of the Family Assessment Device. This 12-item scale has a possible range of 1 to 4; scores of ≥2 are interpreted as unhealthy family functioning.34–36

To assess the children's executive functioning in the context of their everyday activities, the caregivers completed the BRIEF during each telephone interview.19 The BRIEF includes 8 clinical scales that consist of 72 behaviors that are scored on a 3-point scale depending on how frequently the behavior occurs: never, sometimes, or often. The 8 BRIEF scales aggregate into 2 dimensions of executive functioning (behavioral regulation and metacognition) and a measure of overall executive functioning (the Global Executive Composite [GEC]). The Behavioral Regulation Index includes the inhibit, shift, and emotional-control scales, which consist of items such as "interrupts others," "acts upset by a change in plans," and "overreacts to small problems," respectively.17,19 The Metacognition Index comprises the initiate, working memory, plan/organize, organization of materials, and monitor scales, which include items such as "is not a self-starter," "when given 3 things to do, remembers only the first or last," "gets caught up in details and misses the big picture," "cannot find things in room or school desk," and "does not check work for mistakes."17,19

Scores for all 8 clinical scales and the 3 summary scales of the BRIEF are provided in the form of standardized T scores with a mean of 50 and an SD of 10. Subjects who had a score that was 1 or 2 SDs above the mean (ie, score of 60 or 70) were in the 84th and 98th percentiles of the normal population, respectively. Therefore, changes of 5 T-score points or more (half an SD) are clinically important. Scores of >65 (ie, 1 SDs above normal) represent clinically significant impairment.19 The BRIEF also includes 2 validity scales to measure extreme rater negativity (negativity scale) and inconsistent responses on similar items (inconsistency scale). Because this study administered only the 72 items that comprise the core measure (ie, the 8 clinical scales and 3 composite indices), the negativity scale could not be calculated.19

The BRIEF is a reliable instrument, with good test-retest reliability documented for the caregiver-report form over a 2-week interval in a normative sample as well as a sample of 95 children with TBI.17,20 The measure has also shown evidence of good construct validity, convergent and discriminant validity, content validity, and internal consistency.17 In addition, the BRIEF seems to be a valid instrument for use with children who have sustained a TBI. In a previous analysis, we found that the BRIEF scales had good-to-excellent internal consistency (ie, 0.82–0.98) and that the BRIEF working memory scale demonstrated good construct validity by discriminating well among groups of children with varying levels of TBI severity.20

Data Analyses
Baseline group differences in injury, child, and family characteristics were assessed according to study group by using the {chi}2 test of homogeneity. To evaluate the effects of TBI severity on reported executive function, BRIEF T scores for each of the 8 domain scales and for the summary scales for the control fracture group and each of the TBI severity groups were compared by using 1-way analysis of variance. Significant differences among the groups were explored further by using pairwise comparisons. Scores for children in the TBI group with AIS ratings of 2 and 3 were combined in the univariate analyses, because no significant differences were observed between these groups on any of the BRIEF scales. In the remainder of this article, we refer to head injury AIS scores of 2 or 3 as mild TBI, head injury AIS scores of 4 as moderate TBI, and head injury AIS scores of 5 as severe TBI. For the univariate analyses, differences were considered statistically significant if the P value was <.05.

The relative influence of injury, child, and family characteristics on reported executive functioning was estimated by using a GEE model that allows for the influence of factors to change over time and accounts for the autocorrelation associated with repeated assessment of the same subjects.37 We modeled the overall BRIEF score (GEC) and the Behavioral Regulation Index and Metacognition Index summary scores. Because the results of all 3 models were similar, only the results of the GEC model are presented. The following factors were considered in the GEE models: time since injury, severity of injury, mechanism of injury, the presence of major associated injuries (AIS ≥ 2), Glasgow Coma Scale score, child characteristics (ie, age, race, gender, preexisting conditions), caregiver characteristics (ie, age, race, gender, relationship to child, education), and family characteristics (ie, total household income, health insurance status, marital status, and family functioning). Different interactions hypothesized to influence executive functioning were examined. Only factors and interactions that were statistically significant (ie, the 95% confidence interval did not include 1.0) were retained in the final model. Among family characteristics, total household income and health insurance status were both statistically significant factors in the model but strongly correlated. To minimize concerns with multicollinearity, health insurance status was retained and total household income was dropped from the model. Health insurance status was selected as the variable of interest because, from a public health perspective, children's health insurance status is more readily modifiable than families' total household income.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Participant Characteristics
The study sample comprised 433 children, including 330 children who sustained mild-to-severe TBI and 103 children with orthopedic fractures. Of the 433 families who completed the baseline interview, 391 (90%) completed the interview 3 months after injury, and 377 (87%) completed the interview 12 months after injury. Twenty subjects (5%) did not complete either follow-up interview. Those with no follow-up were significantly more likely to be younger, nonwhite, and part of a single-parent household compared with those with follow-up (P < .05) (data not shown). Child, caregiver, and family characteristics for the sample are summarized in Table 1. The mean age of all enrolled subjects was 10 years. Those in the control and TBI groups did not differ significantly on any child, caregiver, or family characteristics.


View this table:
[in this window]
[in a new window]

  		TABLE 1 Percent Distribution of Baseline Child, Caregiver, and Family Characteristics

 
The injury characteristics of the sample are presented in Table 2. Children in the TBI groups were more severely injured than those in the control group as measured by a NISS score of ≥25 and the presence of a major associated injury. Children with TBI were more frequently hospitalized for >1 week and were more likely to be discharged to a rehabilitation facility than to go directly home.


View this table:
[in this window]
[in a new window]

  		TABLE 2 Distribution of Injury Characteristics

 
BRIEF Ratings According to Study Group
The mean BRIEF scores for the summary and domain scales are displayed in Tables 3 and 4, respectively. Inconsistent caregiver responses were a concern on <1% of completed BRIEF interviews. At baseline, caregiver ratings for the control and TBI groups did not differ significantly on any of the BRIEF summary indices. However, by 3 months after injury, the caregivers of children with mild and severe TBI reported significantly greater executive dysfunction than the caregivers for controls on the GEC. The difference in scores represented 0.3 SD in the mild-TBI group and 0.7 SD in the severe-TBI group. Although the difference between the moderate-TBI group and the controls on the GEC was greater than that observed between the mild-TBI group and the controls, this difference did not reach statistical significance because of the smaller number of participants in the moderate-TBI group. Twelve months after injury, caregivers of the children with TBIs of all severities reported significantly greater executive dysfunction on the GEC and the Behavioral Regulation and Metacognition summary scores than caregivers for the children with an extremity fracture.


View this table:
[in this window]
[in a new window]

  		TABLE 3 Mean BRIEF Summary Scores According to TBI Severity

 

View this table:
[in this window]
[in a new window]

  		TABLE 4 Mean BRIEF Domain Scores According to TBI Severity

 
The BRIEF domain scores reflected a similar pattern to the summary scores (see Table 4). No significant differences were observed between any of the study groups at baseline. However, the children with a TBI did differ from the children with an extremity fracture at follow-up. The differences were largest and occurred more frequently 12 months, as opposed to 3 months, after injury. The working memory scale was the only domain that demonstrated significant differences between the control group and all 3 TBI severity groups at 3 and 12 months after injury (P < .05).

Figure 1 illustrates the proportion of each study group that had a clinically impaired score (T ≥ 65) at baseline and 3 and 12 months after injury. At baseline, groups did not differ in the percentage of children whose caregivers reported significant preinjury executive dysfunction. For the control group, the percentage with significant executive dysfunction did not change markedly during the follow-up period. In contrast, the proportion with significant executive dysfunction doubled among the children with a mild TBI and tripled among those with a moderate-to-severe TBI by 3 months after injury (P < .01). Furthermore, the postinjury rate of significant executive dysfunction among the TBI groups remained elevated 12 months after injury (P < .01).


Figure 1
View larger version (19K):
[in this window]
[in a new window]

  		FIGURE 1 Proportion of each study group (fracture, mild TBI, moderate TBI, and severe TBI) whose caregivers reported clinically significant executive dysfunction on the GEC of the BRIEF at baseline and 3 and 12 months after injury. GEC scores of ≥65 were interpreted to reflect clinically significant impairment in executive functioning.

 
Multivariate Modeling of BRIEF Scores
Because no significant differences were observed between children who sustained mild versus moderate TBI on BRIEF scores, these groups were combined in the multivariate modeling. The final results are summarized in Table 5. We found that specific child, family, and injury characteristics significantly influenced BRIEF scores, although the impact of some of these factors changed over time. For example, after adjusting for other factors, no significant differences according to study group were observed in the preinjury executive-functioning scores. However, at follow-up, children who sustained a mild-to-moderate TBI were significantly more likely to have a worse GEC score (increases of 2.5 T-score points at 3 months and 3.4 T-score points at 12 months) than children with a fracture at the same points in time. Children who sustained a severe TBI had significantly worse executive dysfunction (increase of 5.6 T-score points) than children with a fracture 12 months after injury.


View this table:
[in this window]
[in a new window]

  		TABLE 5 Change in GEC Score Associated With Each Factor

 
Similarly, although no significant differences were found in BRIEF scores according to mechanism of injury or insurance status at baseline, significant differences were present 3 and 12 months after injury. Children who sustained a traffic-related injury had worse GEC scores 3 (increase of 3.2 T-score points) and 12 (increase of 3.7 T-score points) months after injury than children whose injury was caused by a fall. Likewise, the follow-up scores of children with Medicaid insurance were significantly worse than scores for children with commercial insurance.

The presence of a preexisting learning or behavioral condition, lower educational attainment of the caregiver, and poor family functioning had a consistently negative impact on executive function over time. After controlling for other significant factors, the BRIEF GEC score was 9.6 T-score points higher among the children who had a preexisting learning or behavioral problem compared with the children who did not. The BRIEF GEC scores of the children whose caregivers reported poor family functioning were 4.3 T-score points higher than scores for the children whose caregivers reported good family functioning. Finally, children whose caregivers did not have a college degree had greater executive dysfunction on average (2.2 T-score point increase) than the children whose caregivers were college graduates.


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Few studies have documented the prevalence and examined the moderators of executive-functioning problems in everyday life of children who sustain TBI.8,18,28,38 In this study, we examined caregiver responses on the BRIEF longitudinally in a large sample of children who were hospitalized with a TBI or an orthopedic fracture to document changes in executive functioning prospectively in the first year after injury. As hypothesized, we found that the children who sustained a TBI had more reported executive dysfunction than those who were hospitalized for orthopedic fractures and that more severe TBI was associated with greater executive dysfunction. Furthermore, we found that child and family characteristics moderated reported executive functioning.

In this study, executive dysfunction was common after TBI, whereas it was relatively rare after orthopedic injury. Between 18% and 38% of the children who sustained a TBI had clinically significant levels of reported executive dysfunction during the first year after injury, with more severe TBI associated with greater executive dysfunction. In contrast, only ~8% to 10% of children with orthopedic fractures displayed executive dysfunction in the year after injury. Moreover, in all groups, the clinically elevated scores did not decrease between 3 and 12 months after injury. Twelve months after injury, children who sustained a TBI had significantly poorer executive-functioning skills in almost all domains of the BRIEF compared with children with an orthopedic fracture. These results suggest that there is considerable cognitive disability present among children who are hospitalized with a TBI.

Findings from this study are consistent with those from previous reports of executive dysfunction on the BRIEF several years after TBI.8 This study also supports previous reports of a dose-response relation between severity of injury and degree of cognitive impairment, with the greatest level of executive dysfunction reported in the severe-TBI group.6,8,16 Although Mangeot et al8 did not identify specific domain scales from the BRIEF that discriminated between TBI and control groups at extended follow-up, our study found the working-memory scale to be particularly sensitive to injury severity within the first year after TBI. Working memory represents the ability to hold information in mind long enough to manipulate it in the service of completing a task or goal. Deficits in working memory have been observed after TBI on both performance-based tests and behavior rating forms.9,29

It is important to note that caregivers did not report recovery in executive function over the first year. These results conflict with previous reports that children's scores on performance-based tests of executive function improve over time.6,16,39 As noted above, it is difficult to interpret reported improvements on performance-based measures of executive functioning, because better scores may be related to either recovery from TBI or increased practice with the tests. The executive challenge of many performance-based measures depends on requiring the individual to organize a response to a novel task, so the measures become less challenging with increasing familiarity. Thus, the current data provide support to earlier reports that suggested that the BRIEF may be sensitive to aspects of executive functioning that are not measured by performance-based tests in children who sustain moderate-to-severe TBI.8,28 Whereas 10% to 21% of children demonstrated clinically significant impairment on performance-based tests of executive function in the study by Vriezen and Pigott,28, 29% to 35% of the sample received clinically elevated ratings on the BRIEF. These findings lend support to the assertion that performance-based tests have the potential to overestimate a child's level of executive functioning as a result of the highly structured nature of standardized, individual assessment. In contrast, behavioral rating forms such as the BRIEF allow caregivers to respond on the basis of a much broader sample of their children's behavior in situations that require greater independence in organizing, initiating, and monitoring goal-directed actions. Other behavioral indicators used in previous studies also have been found to show evidence of persisting executive dysfunction. Specifically, caregiver report of attention and socialization skills and the number of children who met criteria for a diagnosis of attention-deficit/hyperactivity disorder did not improve in the period from 6 to 12 months after injury, suggesting that day-to-day behavior may not improve in the same way that improvements have been documented on performance-based tests.6,40,41

The persistence of increased executive dysfunction on the BRIEF after TBI is particularly important given that cognitive impairments often go unrecognized by caregivers and educators. Without awareness of the kinds of cognitive difficulties that may be present after TBI, caregivers and educators may attribute observed academic or behavioral difficulties to stable traits of the child and characterize him or her as lazy or oppositional rather than provide appropriate support and accommodations.3–5

Executive-functioning outcomes were moderated by the child's premorbid learning and behavioral functioning as well as family functioning and family resources. After controlling for child, family, and injury-related factors, the presence of premorbid learning or behavioral problems was strongly associated with reported executive dysfunction. Importantly, our findings suggest that children with premorbid attentional or learning problems have greater reported executive dysfunction across time points, indicating that executive dysfunction present before injury persists in the year after injury. In this study, we did not detect a significant interaction between premorbid learning/behavioral functioning and time of measurement that would suggest that executive dysfunction after injury was worse for children with preexisting attention or learning problems. However, previous reports of cognitive outcomes on both performance-based measures and caregiver and teacher rating scales after TBI have shown that children with premorbid attention problems and overactivity displayed greater postinjury executive dysfunction than children without premorbid problems.25,42

Unhealthy family functioning and limited family resources also had a negative impact on children's reported executive functioning. Increased rates of clinically significant family dysfunction have been documented in families of children with severe TBI.43,44 Moreover, a recent study suggested that family functioning worsens over time when caregivers do not have adequate social support.45 Greater family dysfunction was associated with worse performance on measures of verbal memory and math skills as well as lower teacher ratings of academic performance among children with severe TBI.23 We previously reported that poor family functioning was associated with higher rates of unrecognized need during the follow-up period.3 Greater executive dysfunction is a predictable outcome for children whose families do not recognize their cognitive impairments and consequently fail to seek appropriate health and educational support services.

Caregivers reported greater executive dysfunction for children with Medicaid insurance than for children with commercial insurance. Medicaid insurance status probably serves as a marker for limited financial resources in the family. Children with Medicaid insurance also were found to have more unmet service needs after injury.3 Socioeconomic disadvantage has been linked to declines in social functioning after TBI, a set of skills thought to depend in part on the integrity of executive functions such as inhibitory control and social problem solving.38,40 Results from this study are consistent with previous reports that socioeconomic disadvantage and poor family functioning are associated with decreased social competence and higher rates of clinically significant behavior problems after TBI.27,46

Executive dysfunction has the potential to adversely impact children's quality of life and daily functioning in multiple domains, including their academic functioning, independent living skills, and social interactions.27,47 Although quality of life was not included in the current analyses, we previously reported that children from this sample who sustained moderate-to-severe TBI experienced a decline in quality of life across multiple dimensions, including physical, cognitive, psychosocial, and overall quality of life.48 Another study documented that caregivers of children who sustained severe TBI reported lower health-related quality of life in multiple domains (eg, behavior, mental health, family impact) and lower levels of adaptive functioning several years after injury.47 Impairment on performance-based measures of executive functions also has been linked to lower levels of adaptive skills.8,16

Findings from this study should be evaluated in the context of the following limitations. First, the BRIEF is a caregiver-report measure and is subject to caregiver bias. As previously noted, we used only the 72 core items from the BRIEF, which did not permit calculation of the negativity scale, a validity scale that was intended to detect extreme rater negativity regarding the child's behavior. It is possible that some caregivers may have rated their child's behavior in an excessively negative fashion, resulting in higher scores on the BRIEF for some subjects. Also, information regarding each child's executive functioning before injury was collected retrospectively, creating potential recall bias in caregiver responding. To minimize bias, baseline interviews were completed as soon after injury as possible, with the majority completed within 2 weeks of hospitalization. BRIEF scores did not differ between the fracture and TBI groups at baseline, suggesting that if recall bias was present, it was similar across study groups. Second, family functioning was assessed only at baseline. We did not account for potential changes in family functioning that may have occurred after injury or as a result of new or exacerbated family stressors associated with the injury.23,42,49 Third, this study relied on caregiver report to determine if the child had premorbid learning or behavioral problems and to assess the child's level of executive functioning both before injury and at follow-up. Earlier studies have demonstrated that factors such as the family burden of caring for an injured child, parent psychological distress, and family functioning are related to a child's level of impairment on caregiver-reported measures.23 It will be important for future studies of executive dysfunction after TBI to collect concurrent ratings from children's caregivers and classroom teachers to document the extent to which informants' ratings are consistent across settings. In addition, future studies of executive dysfunction in children after TBI should include real-world outcome measures such as daily functioning and academic performance to further delineate the relation between reported executive dysfunction and the child's ability to meet age-appropriate environmental expectations.18 Although initial studies have not demonstrated a strong relation between informant ratings of executive dysfunction and children's scores on performance-based tests of executive functioning, future studies of executive functioning after TBI should examine the relation between performance-based tests and behavior rating measures in larger samples of children with TBI to determine if the different methods are more closely related at finer levels of analysis (ie, tests and domain scales that measure specific aspects of executive functioning such as working memory).8,29


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Caregiver report of executive dysfunction is common and persistent during the first year after injury among children who are hospitalized with TBI. Findings from our current study provide further evidence of the need for clinical follow-up after TBI to facilitate early identification of persistent cognitive deficits so that interventions and services can be provided to children that reduce the harmful effects of TBI. Standardized questionnaires such as the BRIEF represent a valuable tool for assessing executive dysfunction after TBI and provide a rich source of behavioral information for pediatricians that extends beyond the limited range of behaviors that can be observed directly during a typical clinic visit. The instrument can be administered easily in a pediatrician's office and requires no more than 10 minutes for a caregiver to complete. Children whose caregivers report clinically significant concerns may be referred for a more comprehensive neuropsychological evaluation. A more systematic approach to screening children for executive dysfunction and other cognitive sequelae after TBI will increase recognition of TBI-related disability and allow children and families better access to appropriate educational and health services.


   ACKNOWLEDGMENTS
 
This study was funded by grant R49/CCR319701 from the Centers for Disease Control and Prevention's National Center for Injury Prevention and Control.

The Children's Health After Trauma (CHAT) Study Group members were Melissa McCarthy, ScD, Ellen MacKenzie, PhD, Dennis Durbin, MD, Charles Paidas, MD, Mary Aitken, MD, MPH, Kenneth M. Jaffe, MD, Beth Slomine, PhD, Andrea Dorsch, PhD, James Christensen, MD, Ronald Berk, PhD, Eileen Houseknecht, RN, BSN, Susan Ziegfeld, MSN CRNP, Vinita Misra Knight, MPH, CSTR, Patricia Korehbandi, RN, MS, Donna Parnell, RN, MNSc, and Pat Klotz, RN, BSN.


   FOOTNOTES
 
Accepted Dec 18, 2007.

Address correspondence to Heather Whitney Sesma, PhD, University of Minnesota, Department of Pediatrics, Mayo Mail Code 486, 420 Delaware St SE, Minneapolis, MN 55455. E-mail: hwsesma{at}umn.edu

The authors have indicated they have no financial relationships relevant to this article to disclose.


What's Known on This Subject

Executive function deficits are common after TBI, with children often showing deficits on performance-based executive function measures soon after injury but significant improvement over time. The BRIEF represents an alternative executive function measure that captures caregiver observations regarding children's executive function in everyday life.

 

What This Study Adds

Previous studies that used the BRIEF to measure executive function after TBI were limited to 1 assessment with relatively small (<100) samples. This study built on previous work by measuring caregiver BRIEF responses longitudinally for a large sample of children with TBI.

 


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

  1. Langlois JA, Rutland-Brown W, Thomas KE. Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations, and Deaths. Atlanta, GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control; 2004
  2. Schutzman SA, Greenes DS. Pediatric minor head trauma. Ann Emerg Med. 2001;37 (1):65 –74[CrossRef][Web of Science][Medline]
  3. Slomine BS, McCarthy ML, Ding R, et al. Health care utilization and needs after pediatric traumatic brain injury. Pediatrics. 2006;117 (4). Available at: www.pediatrics.org/cgi/content/full/117/4/e663
  4. Glang A, Tyler J, Pearson S, Todis B, Morvant M. Improving educational services for students with TBI through statewide consulting teams. NeuroRehabilitation. 2004;19 (3):219 –231[Web of Science][Medline]
  5. Ylvisaker M, Todis B, Glang A, et al. Educating students with TBI: themes and recommendations. J Head Trauma Rehabil. 2001;16 (1):76 –93[CrossRef][Web of Science][Medline]
  6. Anderson V, Catroppa C. Recovery of executive skills following paediatric traumatic brain injury (TBI): a 2 year follow-up. Brain Inj. 2005;19 (6):459 –470[CrossRef][Web of Science][Medline]
  7. Brookshire B, Levin HS, Song JX, Zhang L. Components of executive function in typically developing and head-injured children. Dev Neuropsychol. 2004;25 (1–2):61 –83[CrossRef][Web of Science][Medline]
  8. Mangeot S, Armstrong K, Colvin AN, Yeates KO, Taylor HG. 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[Medline]
  9. Roncadin C, Guger S, Archibald J, Barnes M, Dennis M. Working memory after mild, moderate, or severe childhood closed head injury. Dev Neuropsychol. 2004;25 (1–2):21 –36[CrossRef][Web of Science][Medline]
  10. Denckla MB. Executive function, the overlap zone between attention deficit hyperactivity disorder and learning disabilities. Int Pediatr. 1989;4 (2):155 –160
  11. Lezak MD. Neuropsychological Assessment. 3rd ed. New York, NY: Oxford University Press; 1995
  12. Giedd JN, Blumenthal J, Jeffries NO, et al. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci. 1999;2 (10):861 –863[CrossRef][Web of Science][Medline]
  13. Luciana M, Nelson CA. The functional emergence of prefrontally-guided working memory systems in four- to eight-year-old children. Neuropsychologia. 1998;36 (3):273 –293[CrossRef][Web of Science][Medline]
  14. Levin HS, Culhane KA, Mendelsohn D, et al. Cognition in relation to magnetic resonance imaging in head-injured children and adolescents. Arch Neurol. 1993;50 (9):897 –905[Abstract/Free Full Text]
  15. Mendelsohn D, Levin HS, Bruce D, et al. Late MRI after head injury in children: relationship to clinical features and outcome. Childs Nerv Syst. 1992;8 (8):445 –452[CrossRef][Web of Science][Medline]
  16. Levin HS, Song J, Scheibel RS, et al. Concept formation and problem-solving following closed head injury in children. J Int Neuropsychol Soc. 1997;3 (6):598 –607[Medline]
  17. Gioia GA, Isquith PK. Ecological assessment of executive function in traumatic brain injury. Dev Neuropsychol. 2004;25 (1–2):135 –158[CrossRef][Web of Science][Medline]
  18. Silver CH. Ecological validity of neuropsychological assessment in childhood traumatic brain injury. J Head Trauma Rehabil. 2000;15 (4):973 –988[Web of Science][Medline]
  19. Gioia GA, Isquith PK, Guy SC, Kenworthy L. Behavior Rating Inventory of Executive Function. Odessa, FL: Psychological Assessment Resources; 2000
  20. McCarthy ML, MacKenzie EJ, Durbin DR, et al. The Pediatric Quality of Life Inventory: an evaluation of its reliability and validity for children with traumatic brain injury. Arch Phys Med Rehabil. 2005;86 (10):1901 –1909[CrossRef][Web of Science][Medline]
  21. Slomine BS, Gerring JP, Grados MA, et al. Performance on measures of "executive function" following pediatric traumatic brain injury. Brain Inj. 2002;16 (9):759 –772[CrossRef][Web of Science][Medline]
  22. Taylor HG. Research on outcomes of pediatric traumatic brain injury: current advances and future directions. Dev Neuropsychol. 2004;25 (1–2):199 –225[CrossRef][Web of Science][Medline]
  23. Taylor HG, Yeates KO, Wade SL, Drotar D, Klein SK, Stancin T. Influences on first-year recovery from traumatic brain injury in children. Neuropsychology. 1999;13 (1):76 –89[CrossRef][Web of Science][Medline]
  24. Ewing-Cobbs L, Barnes M, Fletcher JM, Levin HS, Swank PR, Song J. Modeling of longitudinal academic achievement scores after pediatric traumatic brain injury. Dev Neuropsychol. 2004;25 (1–2):107 –133[CrossRef][Web of Science][Medline]
  25. Schachar R, Levin HS, Max JE, Purvis K. 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[CrossRef][Web of Science][Medline]
  26. 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[CrossRef][Web of Science][Medline]
  27. Schwartz L, Taylor HG, Drotar D, Yeates KO, Wade SL, Stancin T. Long-term behavior problems following pediatric traumatic brain injury: prevalence, predictors, and correlates. J Pediatr Psychol. 2003;28 (4):251 –263[Abstract/Free Full Text]
  28. Vriezen ER, Pigott SE. The relationship between parental report on the BRIEF and performance-based measures of executive function in children with moderate to severe traumatic brain injury. Child Neuropsychol. 2002;8 (4):296 –303[Medline]
  29. Conklin H, Salorio C, Kent J, Slomine B. Performance- and rater-based measures of working memory in children and adolescents following moderate to severe traumatic brain injury. Poster presented at: the 34th annual meeting of the International Neuropsychological Society; February 1–4, 2006; Boston, MA
  30. Committee on Injury Scaling. The Abbreviated Injury Scale. 1990 Rev. Des Plaines, IL: Association for the Advancement of Automotive Medicine; 1990
  31. MacKenzie EJ. Injury severity scales: overview and directions for future research. Am J Emerg Med. 1984;2 (6):537 –549[CrossRef][Web of Science][Medline]
  32. Osler T, Baker SP, Long W. A modification of the Injury Severity Score that both improves accuracy and simplifies scoring. J Trauma. 1997;43 (6):922 –926[Web of Science][Medline]
  33. Visser SN, Lesesne CA. Mental health in the United States: prevalence of diagnosis and medication treatment for attention-deficit/hyperactivity disorder—United States, 2003. MMWR Morb Mortal Wkly Rep. 2005;54 (34):842 –847[Medline]
  34. Byles J, Byrne C, Boyle MH, Offord DR. Ontario Child Health Study: reliability and validity of the general functioning subscale of the McMaster Family Assessment Device. Fam Process. 1988;27 (1):97 –104[CrossRef][Web of Science][Medline]
  35. Epstein NB, Baldwin LM, Bishop DS. The McMaster Family Assessment Device. J Marital Fam Ther. 1983;9 (2):171 –180[CrossRef][Web of Science]
  36. Miller IW, Epstein NB, Bishop DS, Keitner GI. The McMaster Family Assessment Device: reliability and validity. J Marital Fam Ther. 1985;11 (4):345 –356[CrossRef][Web of Science]
  37. Hanley JA, Negassa A, Edwardes MD, Forrester JE. Statistical analysis of correlated data using generalized estimating equations: an orientation. Am J Epidemiol. 2003;157 (4):364 –375[Abstract/Free Full Text]
  38. Dennis M, Guger S, Roncadin C, Barnes M, Schachar R. Attentional-inhibitory control and social-behavioral regulation after childhood closed head injury: do biological, developmental, and recovery variables predict outcome? J Int Neuropsychol Soc. 2001;7 (6):683 –692[CrossRef][Web of Science][Medline]
  39. Jaffe KM, Polissar NL, Fay GC, Liao S. Recovery trends over three years following pediatric traumatic brain injury. Arch Phys Med Rehabil. 1995;76 (1):17 –26[CrossRef][Web of Science][Medline]
  40. Taylor HG, Yeates KO, Wade SL, Drotar D, Stancin T, Minich M. A prospective study of short- and long-term outcomes after traumatic brain injury in children: behavior and achievement. Neuropsychology. 2002;16 (1):15 –27[CrossRef][Web of Science][Medline]
  41. Levin H, Hanten G, Max J, et al. Symptoms of attention-deficit/hyperactivity disorder following traumatic brain injury in children. J Dev Behav Pediatr. 2007;28 (2):108 –118[CrossRef][Web of Science][Medline]
  42. Slomine BS, Salorio CF, Grados MA, Vasa RA, Christensen JR, Gerring JP. Differences in attention, executive functioning, and memory in children with and without ADHD after severe traumatic brain injury. J Int Neuropsychol Soc. 2005;11 (5):645 –653[Web of Science][Medline]
  43. Rivara JB, Fay GC, Jaffe KM, Polissar NL, Shurtleff HA, Martin KM. Predictors of family functioning one year following traumatic brain injury in children. Arch Phys Med Rehabil. 1992;73 (10):899 –910[Web of Science][Medline]
  44. Wade SL, Taylor HG, Drotar D, Stancin T, Yeates KO. Family burden and adaptation during the initial year after traumatic brain injury in children. Pediatrics. 1998;102 (1 pt 1):110 –116[Abstract/Free Full Text]
  45. 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[Abstract/Free Full Text]
  46. Yeates KO, Swift E, Taylor HG, et al. Short- and long-term social outcomes following pediatric traumatic brain injury. J Int Neuropsychol Soc. 2004;10 (3):412 –426[CrossRef][Web of Science][Medline]
  47. Stancin T, Drotar D, Taylor HG, Yeates KO, Wade SL, Minich NM. Health-related quality of life of children and adolescents after traumatic brain injury. Pediatrics. 2002;109 (2). Available at: www.pediatrics.org/cgi/content/full/109/2/e34
  48. McCarthy ML, MacKenzie EJ, Durbin DR, et al. Health-related quality of life during the first year after traumatic brain injury. Arch Pediatr Adolesc Med. 2006;160 (3):252 –260[Abstract/Free Full Text]
  49. Rivara JB, Jaffe KM, Polissar NL, et al. Family functioning and children's academic performance and behavioral problems in the year following traumatic brain injury. Arch Phys Med Rehabil. 1994;75 (4):369 –389[CrossRef][Web of Science][Medline]
PEDIATRICS (ISSN 1098-4275). ©2008 by the American Academy of Pediatrics

Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Facebook Facebook   Add to Reddit Reddit   Add to Technorati Technorati   Add to Twitter Twitter    What's this?



This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow E-mail this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My File Cabinet
Right arrow Download to citation manager
Right arrowRequest Permissions
Citing Articles
Right arrow Citing Articles via CrossRef
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Sesma, H. W.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Sesma, H. W.
Related Collections
Right arrow Emergency Medicine
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Facebook   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?