Journal of Pediatric Psychology, Vol. 28, No. 4, 2003, pp. 251-263
© 2003 Society of Pediatric Psychology
Long-Term Behavior Problems Following Pediatric Traumatic Brain Injury: Prevalence, Predictors, and Correlates
1 Case Western Reserve University, 2 Rainbow Babies & Children's Hospital, 3 The Ohio State University and Columbus Children's Hospital, 4 University of Cincinnati and Children's Hospital Medical Center, 5 MetroHealth Medical Center
All correspondence should be sent to Lisa Schwartz, Department of Psychology, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, Ohio 44106-7123. E-mail: lxs78{at}po.cwru.edu.
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Abstract |
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Objective To study identified rates of long-term behavior problems in children with traumatic brain injury (TBI) compared to children with only orthopedic injuries and risk factors and correlates for new behavior problems following TBI. Methods Sample included children with severe TBI (n = 42), moderate TBI (n = 41), and orthopedic injuries only (ORTHO;n = 50). The baseline assessment measured child behavior, adaptation, and neuropsychological, academic, and family functioning. Follow-ups were conducted at 6 and 12 months and at an extended follow-up a mean of 4 years after injury. Results The prevalence of caseness, defined as elevated behavior problem ratings, was higher in one or both TBI groups than in the ORTHO group at each follow-up (e.g., 36% of severe TBI group, 22% of moderate TBI group, and 10% of ORTHO group at extended follow-up). Most instances of postinjury-onset caseness at the extended follow-up were evident within the first year after TBI. Predictors were severe TBI, socioeconomic disadvantage, and preinjury behavioral concerns. Concurrent correlates included weakness in working memory and adaptive behavior skills, poorer behavior and school competence, and adverse family outcomes. Conclusions Postinjury-onset caseness is persistent, risks are multifactorial, and correlates include child dysfunction and family sequelae.
Key words: traumatic brain injury; children; behavior problems; caseness; risk factors; family functioning..
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Introduction |
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Pediatric traumatic brain injury (TBI) is a major public health problem in the United States, with an average of approximately 180 per 100,000 children hospitalized for head injury each year (Kraus, 1995
). Studies of
outcomes 1 to 3 years postinjury reveal that severe pediatric TBI leads to
psychiatric and behavioral problems, difficulties in adaptive functioning, and
deficits in academic and cognitive skills
(Brown, Chadwick, Shaffer, Rutter, &
Traub, 1981; Fay et al.,
1994; Fletcher, Ewing-Cobbs,
Miner, Levin, & Eisenberg, 1990;
Jaffe, Polissar, Fay, & Liao,
1995; Max et al.,
1997; Max, Castillo, Bokura,
et al., 1998; Max, Castillo,
Robin, et al., 1998; Max et
al., 2000). Behavioral sequelae frequently fail to resolve over
time and thus are of particular concern to pediatric psychologists (Taylor et
al., in press).
Several studies that have examined outcomes after TBI in relation to
preinjury functioning have found high rates of emergent, or postinjury-onset,
behavior problems. Based on interviewer and teacher ratings of pre- and
postinjury behavioral status, Brown et al.
(1981) identified these
problems in 52% of a sample of 21 children with severe TBI examined at 1 year
after injury. In contrast, only 14% of their control group with orthopedic
injuries met criteria for new problems. Rates of postinjury-onset problems
changed little over time.
Max et al. (1997) also
examined rates of new postinjury psychiatric problems, defined in terms of
psychiatric diagnoses not present prior to injury. By the second year
following the TBI, 15 out of 42 (36%) children met criteria for a new
psychiatric disorder, 11 of whom (26%) had a disorder that persisted beyond
the 12-month assessment. Max et al.
(2000) also examined rates of
personality change disorder, a syndrome of behavioral change resulting from
brain damage. Persistence of personality change disorder was found in about
40% of the TBI participants at an average of 2 years after injury. All of the
children with persistent personality change disorder sustained a severe
TBI.
Bloom et al. (2001)
investigated postinjury-onset problems in a manner similar to Max et al.
(1997). In this study,
psychiatric interviews conducted at least 1 year after injury revealed new
problems in 27 of 46 children in the sample (58%). Twenty-two children (48%)
had problems that arose after injury and persisted to the time of the
assessment.
Some children appear to be at greater risk than others to develop
postinjury-onset behavior problems. Brown et al.
(1981) found substantially
higher rates of these problems after severe TBI than after milder TBI.
Children with milder TBI had a rate of new problems comparable to the
orthopedic injury control group. Additionally, the children with severe TBI
who had new problems had greater family adversity and more
"subclinical" preinjury behavior problems than the children from
this group who did not have new problems. Likewise, Max and his associates
(Max et al., 1997;
Max, Castillo, Bokura, et al.,
1998) reported that children with new postinjury psychiatric
diagnoses had higher rates of preinjury psychiatric disturbance and greater
family social disadvantage than children without new problems
Children's postinjury cognitive functioning is a less consistent predictor
of new behavior problems. Some studies have found a relationship between
cognitive functioning and new psychiatric disorders
(Max et al., 1999), while
others have reported weak relationships between behavioral and cognitive
outcomes of pediatric TBI (Anderson et al.,
2001; Fletcher et al.,
1990). Brown et al.
(1981) found a relationship
between new psychiatric disorders at 4 months postinjury and concurrent IQ
scores, but not after 1.5 to 2 years.
To our knowledge, no study has examined clinically significant
postinjury-onset behavior problems beyond 3 years postinjury in relationship
to comprehensive assessments of child and family outcomes. Assessment of these
problems is important in estimating incidence rates, determining which
children are at greatest risk, and advancing knowledge regarding possible
etiologies. Investigation of concurrent correlates of these problems is
required to understand associated child and family morbidity. Previous
investigations have assessed behavioral changes after TBI in relation to
relatively narrow sets of cognitive outcomes, such as IQ and memory measures
(Brown et al., 1981;
Max et al., 1999), rather than
broader neuropsychological batteries. Assessment of family outcomes has been
similarly limited.
The purpose of this study was to investigate rates, risk factors, and correlates of long-term postinjury-onset behavior problems in a sample of children with moderate to severe TBI. Behavior problems in children with moderate to severe TBI and in a control group of children with orthopedic injuries were assessed at a long-term, or "extended", follow-up conducted a mean of 4 years after injury. One specific aim was to determine rates of significant postinjury behavior problems, or caseness, in children with TBI relative to children who had sustained orthopedic injuries only (ORTHO group). Although we focused on outcomes at the extended follow-up, we also examined the continuity of caseness across earlier follow-up assessments. A second aim was to identify risks for the development of long-term postinjury-onset caseness following TBI. To meet this objective, we compared children with TBI who satisfied criteria for a clinically significant postinjury-onset problem at the extended follow-up to children with TBI who did not satisfy these criteria. Risk factors considered included TBI severity, preinjury child behavior and family status, and neuropsychological performance at a baseline evaluation conducted soon after injury. Our third aim was to identify child and family outcomes that were concurrently associated with persisting postinjury-onset caseness.
The first hypothesis was that rates of caseness at the extended follow-up
would be higher in children with TBI than in the control group. We anticipated
that group differences would be found even when the presence/absence of
preinjury caseness and sociodemographic factors were taken into account. Based
on findings suggesting that behavior problems emerge relatively soon after TBI
and persist over time (Taylor et al.,
2002), we anticipated that most postinjury-onset caseness at the
extended follow-up would have been evident within the first year after injury.
The second hypothesis was that predictors of postinjury-onset caseness in
children with TBI would include greater TBI severity, higher levels of
reported preinjury behavior problems, greater cognitive impairment soon after
the injury, and lesser family social advantage
(Brown et al., 1981). Our
third hypothesis was that postinjury-onset caseness would be associated with
cognitive, educational, and adaptive sequelae, as well as worse family
outcomes (Anderson et al.,2001;
Barry, Taylor, Klein, &
Yeates,1996; Max, Castillo,
Robin, et al., 1998; Max et
al., 2000).
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Method |
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Sample
The follow-up sample consisted of 134 of the 189 participants recruited for a longitudinal project (Taylor et al., 1999
) who remained in the study at an extended follow-up a mean of
4.10 years after injury (SD = 0.91, range = 2.37–5.84).
Forty-two children had sustained severe TBI, 42 moderate TBI, and 50
orthopedic injuries only (ORTHO group). The participants were originally
recruited from admissions to four hospitals in north-central Ohio between 1992
and 1995. The study was approved by the institutional review board at each
institution, and informed consent was obtained prior to participation.
Criteria for inclusion were (a) at least one night's hospitalization for a
traumatic brain or orthopedic injury, (b) age at injury between 6 and 12
years, (c) the absence of evidence of child abuse or previous neurological
problem, and (d) residence in an English-speaking household. Severe TBI was
defined on the basis of a lowest postresuscitation Glasgow Coma Scale (GCS;
Teasdale & Jennett, 1974)
score < 9. Children with moderate TBI had a GCS score of 9 of 12, or a GCS
score > 12 accompanied by a skull fracture, intracranial mass lesion or
contusion, diffuse cerebral swelling, posttraumatic neurological abnormality,
or loss of consciousness longer than 15 minutes. Children in the ORTHO group
were free of symptoms suggestive of possible brain insult (e.g., concussion,
severe facial trauma).
Injury severity was further described using the Modified Injury Severity
Score (Mayer, Matlak, Johnson, &
Walker, 1980), defined as the sum of the squares of injury ratings
for the three most affected body areas, including the head. To assess the
severity of injuries not involving the head, we computed a partial Modified
Injury Severity Score, defined as the sum of the squared ratings assigned to
the three most affected body regions excluding the head.
Families were characterized in terms of single-versus two-parent
households, the Hollingshead Four-Factor Index
(Hollingshead, 1975), and the
Socioeconomic Composite Index (SCI; Yeates
et al., 1997). The SCI, which served as the primary measure of
family social status, was the average of the sample z scores for the
Duncan Socioeconomic Index (Stevens &
Featherman, 1981), annual family income as coded on the Life
Stressors and Social Resources Inventory
(Moos & Moos, 1988), and a
7-point maternal education scale. Higher SCI scores reflect greater
socioeconomic disadvantage.
Table I lists demographic and injury characteristics for the three groups of children in the follow-up sample. The groups were similar in terms of age at injury, gender, and sociodemographic characteristics. The ORTHO group had a higher proportion of minority participants than the other two groups, but this difference was not significant. Children with moderate TBI were hospitalized for fewer days than children in the severe TBI and ORTHO groups, but the latter two groups were hospitalized for similar periods. These two groups were also similar in injury severity to areas of the body other than the head. Mean GCS scores and duration of impaired consciousness for the TBI groups are presented for descriptive purposes.
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Compared to the follow-up sample, participants who dropped out of the study prior to the extended follow-up had lower socioeconomic status as measured by the SCI. Attrition was also higher in the ORTHO group than in the TBI groups. The dropouts did not differ from the follow-up sample in terms of sex distribution, age at injury, race, or preinjury behavior problems as rated by parents soon after injury.
Measures and Procedure
Overview. The extended follow-up consisted of a half-day
session with the child and parent. While the child was tested, the parent
completed interviews and ratings of the child and family. Similar assessments
had been completed on three previous occasions, including a baseline at an
average of 3 weeks postinjury and follow-ups at 6 and 12 months after the
baseline (Taylor et al., 1999,
2001;
Wade, Taylor, Drotar, Stancin, &
Yeates, 1998; Yeates et al.,
1997).
Table II lists the child and
family measures considered for this study. Child testing consisted of measures
of IQ, language skills, perceptual motor abilities, memory, attention and
executive function, and academic achievement. Other child characteristics were
assessed by administering the Child Behavior Checklist (CBCL;
Achenbach, 1991a) and Vineland
Adaptive Behavior Scales (Sparrow, Balla,
& Cichetti, 1984) to parents and the Teacher's Report Form
(TRF; Achenbach, 1991b) to
teachers. CBCL and TRF Behavior Problem scales provide ratings of a broad
spectrum of child behavior problems; CBCL competence is a composite of ratings
of participation in activities, social relations, and school performance; and
TRF academic performance is a rating of performance in academic subject areas.
The Vineland is a semistructured parent interview that assesses adaptive
functioning in the domains of communication, daily living skills, and
socialization. To assess global school outcomes, we also monitored grade
repetitions and special education placements.
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Family measures included parent self-report ratings of family functioning,
parent psychological distress, and injury-related family burden (see
Wade et al., 1998). Family
functioning was assessed by the McMaster Family Assessment Device
(Miller, Bishop, Epstein, & Keitner,
1985), a self-report measure with demonstrated reliability and
validity (Stevenson-Hinde & Akister,
1995). The 12-item Family Assessment Device–General
Functioning Scale was used as a summary measure of family functioning. The
Global Severity Index of the Brief Symptom Inventory
(Derogatis & Melisaratos,
1983) served as a summary measure of parent psychological
adjustment. Family burden was measured by the Family Burden of Injury
Interview (Burgess et al.,
1999) and the Impact on Family Scale, Version G
(Stein & Jessop, 1985).
The Family Burden of Injury Interview was developed to assess the unique
burdens and challenges of pediatric TBI for families. A summary of overall
injury-related stress was defined as the mean of subscales pertaining to (a)
concerns with the child's recovery and adjustment, (b) the reactions of
extended family and friends, and (c) spouse's reactions. The Impact on Family
Scale, Version G provided a previously validated measure of the global impact
of pediatric disability (in this case, injury) on the family. The Impact on
Family Scale, Version G Total Negative Impact score served as a summary of
family burden.
Most of the battery of measures were given at baseline and the extended
follow-up. However, testing at the extended follow-up excluded several of the
tests given previously (Test of Nonverbal Intelligence–2; Token Test:
Part V; Clinical Evaluation of Language Fundamentals–Revised, Sentence
Structure; Grooved Pegboard Test; and Woodcock–Johnson Test of
Achievement–Revised, Passage Comprehension and Dictation) due to lack of
discrimination between the groups at earlier points postinjury. In place of
these tests, we administered the Oral Expression and Figurative Language
subtests of the Test of Language Competence-Expanded Version
(Wiig & Secord, 1985) to
further assess language skills, Consonant Trigrams
(Paniak, Millar, Murphy, & Keizer,
1997) to assess memory, and Rey-Osterrieth Complex Figure
(Bernstein & Waber, 1996)
to assess executive function.
The child examiner was not directly informed of the child's group
assignment, and tests were given in counterbalanced order across children to
minimize test order effects. Teacher ratings were mailed to schools after each
assessment. Respondents completed the baseline CBCL, TRF, Vineland, and Family
Assessment Device on the basis of preinjury child or family status.
Age-adjusted standard scores were used in analysis of measures with published
norms. Raw scores for other measures were transformed to age- and
gender-corrected z scores based on the performance of the ORTHO
group. Copy and recall scores for the Rey-Osterrieth Complex Figure were
scored as described by Taylor, Klein, Minich, and Hack
(2000).
Child Behavior Problems. Clinically significant child
behavior problems, or caseness, were defined as a T score > 63 on the CBCL
Behavior Problem scale, corresponding to ratings obtained by < 10% of the
normative sample. Thus, children with a T score > 63 on the CBCL Behavior
Problem scale prior to injury had preinjury caseness. Achenbach
(1991a) recommends this cutoff
as a means for optimizing classification into clinical versus nonclinical
groups. The CBCL, a widely used behavior rating scale, has good reliability
and validity in assessing children's behavior and is normed for school-age
children and adolescents. Prior research supports the validity of the CBCL in
idenifying behavior problems (Biederman et
al., 1993; Jensen et al.,
1996). We excluded the TRF in defining caseness due to previous
demonstration of the insensitivity of teacher ratings to behavior problems
following TBI (Taylor et al.,
1995) and because different teachers rated the children at
baseline and at the extended follow-up, thereby reducing the sensitivity of
teacher ratings to change.
Analysis
Group differences in rates of caseness were examined via chiquare analysis
and logistic regression. Differences between each TBI group and the ORTHO
group were represented in logistic analysis by dummy contrasts. The
presence/absence of preinjury problem, gender, race, and the SCI were included
as covariates in logistic regression to control for the influences of these
factors. Preliminary analysis failed to reveal differences in caseness in
relation to age at injury; thus, this factor was not considered. Only 41
children from the moderate TBI group were considered in analysis due to
failure of one parent to complete the CBCL at the extended follow-up. Missing
data resulted in further reductions in the sample size for some measures. The
largest reductions were due to missing teacher ratings (5% missing TRFs at the
extended follow-up).
To identify factors associated with postinjury-onset caseness, we considered only children with TBI who did not meet criteria for preinjury caseness. We then divided these children into groups with and without postinjury-onset caseness at the extended follow-up. Predictors were identified by comparing the two groups on injury measures, preinjury behavior and academic performance, family measures obtained at baseline, and baseline neuropsychological and achievement skills. Injury measures considered were TBI group (severe vs. moderate), duration of impaired consciousness defined by days until the child could follow verbal commands, lowest GSC score, nonhead Modified Injury Severity Score, and computed tomography (CT) scan findings as classified according to the presence/absence of both focal frontal lesions and other lesions. Concurrent correlates were examined by comparing the groups on child and family outcomes at the extended follow-up. To identify predictors and correlates unrelated to TBI group, we included this factor as a covariate in analysis. Additional covariates were gender, race, and the SCI. To reduce potential Type I errors, p level was set at .05 for each of the domains listed in Table II, with Bonferroni adjustments made in evaluating multiple measures within domains.
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Results |
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Total Sample
Prevalence of Caseness. Table III presents rates of caseness prior to injury (baseline ratings) and at each of the follow-ups. The table also summarizes findings from logistic regressions that compared each TBI group with the ORTHO group, controlling for gender, race, and the SCI. Despite the absence of group differences in preinjury caseness, rates were higher in the severe TBI group relative to the ORTHO group at each follow-up, and rates were higher in the moderate TBI group relative to ORTHO group at the 6-month and extended follow-up. The pattern of rates over time suggests that there was an increase in caseness in the severe group relative to the other two groups. Higher SCI scores, reflecting greater socioeconomic disadvantage, were associated with higher rates of caseness at each follow-up (p < .01). Race failed to predict caseness independently of the SCI at any of the assessments. A gender difference was found only at the 6-month follow-up, with a higher rate of caseness in boys than girls.
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Continuity of Caseness. Few children with TBI had
postinjury-onset caseness at the extended follow-up that was not present
earlier in follow-up. Considering only participants who had data for all
follow-ups, we found that 8 of 12 (75%) children with severe TBI with
postinjury-onset caseness at the extended follow-up also satisfied the
criterion for caseness at one or both of the earlier follow-ups, compared to 2
of 3 (67%) children with moderate TBI and 0 of 2 (0%) children in the ORTHO
group, 
2 (2, N = 17) = 3.24, p = .14.
Children With TBI Who Did Not Have Preinjury Caseness
Incidence of Postinjury-Onset Caseness. Fifteen (22%) of
the 69 children with TBI without caseness met criteria for caseness at the
extended follow-up, including 12 of 38 (32%) with severe TBI and 3 of 31 (11%)
with moderate TBI, ;2 (1, N = 69) = 3.61, p
= .06. Of the 15 children with postinjury-onset caseness, 13 met criteria for
externalizing problems, 8 met criteria for internalizing problems, and 7 met
criteria for both. Only 4 of 14 children in the postinjury-onset group met the
criterion of a Behavior Problem T score > 63 on the TRF (1 TRF not
completed), suggesting a lack of agreement of the teacher and parent
ratings.
Significance of Postinjury-Onset Caseness. To determine if
postinjury-onset caseness reflected meaningful changes in behavior, we
assessed the extent to which postinjury behavior ratings differed from ratings
of preinjury behavior, as well as associations of postinjury-onset caseness
with postinjury child or family counseling. If we considered only children in
the sample without preinjury caseness, the mean change in the CBCL Behavior
Problem T score at the extended follow-up, relative to the preinjury score,
was 15.67 points (SD = 4.76), or more than 1.5 SDs, for the
children with postinjury-onset caseness. This compares to a mean change of
only –0.22 points (SD = 9.53) for the children with TBI who
failed to meet the criterion for caseness. The minimum change in the children
with postinjury-onset caseness was 10 points, or 1 SD. Rates of child
or family counseling received after injury, but not prior to it, were also
higher in the children with postinjury-onset caseness. Specifically, a history
of postinjury-only counseling was identified in 11/15 (73%) of the children
with caseness, compared to 24/54 (44%) of those without caseness,
;2 (1, N = 69) = 5.52, p < .05.
Predictors of Postinjury-Onset Caseness. Logistic regressions indicated that the rate of caseness was higher in the severe TBI group than in the moderate TBI group (odds ratio = 4.85, 95% confidence interval = 1.07–21.89, p < .05). A higher rate of caseness was also associated with greater socioeconomic disadvantage and higher preinjury CBCL Behavior Problem ratings, but not with race or gender. No injury measure besides TBI severity (severe vs. moderate) discriminated between the children with and without caseness, whether analysis was carried out with the total sample of children with TBI or with each TBI group separately. Analyses also failed to reveal differences between children with and without caseness in preinjury teacher ratings of behavior problems or school performance, adaptive behavior, neuropsychological functioning, academic achievement, or any of the preinjury or early postinjury family measures.
Concurrent Correlates of Postinjury-Onset Caseness. Table IV presents the results of comparisons of children with and without caseness on concurrent child and family outcomes. According to these results, the children with caseness had lower scores on the Vineland Adaptive Behavior Composite and Consonant Trigrams. The children with caseness also had poorer family outcomes, including higher parent distress and greater injury-related family burden, as well as poorer family functioning.
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Although children with and without caseness did not differ in rates of
postinjury grade repetitions, 10 of 15 (67%) of the children with caseness
were in special education at the extended follow-up, compared to 10 of 54
(19%) of the children without caseness, ;2 (1, N =
69) = 10.99, p < .01. Controlling for covariates, we found that
logistic regression revealed only a marginally significant group difference in
rates of special education (odds ratio = 4.19, 95% confidence interval = 0.98,
17.90, p = .05). This difference was significant when analysis was
restricted to the severe TBI group (odds ratio = 8.97, 95% confidence interval
= 1.40, 57.41, p < .05).
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Discussion |
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This study extends the knowledge of long-term behavioral sequelae of pediatric TBI by describing the prevalence of such problems and identifying risk factors and correlates of postinjury-onset caseness an average of 4 years after injury. Using an orthopedic injury control group allowed us to substantiate increased rates of caseness in children with TBI compared to children who sustained other injuries. Another strength of this study was our examination of a wide range of predictors and correlates of caseness, including injury characteristics, preinjury child status, family measures, and neuropsychological outcomes.
Consistent with study hypotheses, children with moderate to severe TBI had
higher rates of caseness at the extended follow-up than the ORTHO group, even
after controlling for presence/absence of preinjury caseness and for
sociodemographic factors. As in past studies, children with severe TBI were
most often affected, and most children with TBI with postinjury-onset caseness
had a history of caseness dating back to the first year after injury
(Max et al., 1997;
Max et al., 2000). Relative to
children without caseness either before or after TBI, those with
postinjury-onset caseness had more severe TBI, were less socially advantaged,
and had higher ratings of preinjury behavior concerns. These differences were
demonstrated with TBI severity taken into account, confirming the
multifactorial nature of influences on postinjury behavior
(Brown et al., 1981;
Gerring et al., 1998;
Max et al., 1997;
Max, Castillo, Bokura, et al.,
1998). Postinjury-onset caseness was concurrently associated with
weaknesses on a test of working memory, less optimal school and adaptive
outcomes, and greater family distress and burden.
The results accord with previous findings showing that most
postinjury-onset behavior disorders emerge soon after injury and that, once
present, these disorders become discouragingly persistent
(Bloom et al., 2001;
Brown et al., 1981; Max et
al., 1997,
2000). The findings also
implicate brain insult as the primary basis for the elevated rate of
postinjury-onset caseness in the severe TBI group. The behavior problems
present at follow-up represented marked change relative to ratings of
preinjury behavior. Moreover, differences were found in comparison to another
injury control group that was closely similar to the severe TBI group in terms
of length of hospitalization and severity of injury to nonhead body
regions.
Associations of social disadvantage with behavior problems after TBI have
been demonstrated previously (Brown et
al., 1981; Gerring et al.,
1998; Kinsella, Ong, &
Murtagh, 1999; Max et al.,
1997; Max, Castillo, Bokura,
et al., 1998; Max et al.,
2000). These associations indicate that the behavioral
consequences of TBI are not due to organic impairment alone but that
environmental factors also play a role
(Brooks, 1990;
Rutter, Chadwick, & Shaffer,
1983). Although the mechanisms responsible for these associations
are unclear, the family and professional resources needed to effectively
manage cognitive and behavioral consequences of TBI may be less available in
disadvantaged settings. Children with TBI also may be more vulnerable than
other children to the stresses in these environments
(Taylor et al., 2002).
Past studies also document relationships between preinjury child
functioning and postinjury-onset problems
(Brown et al., 1981;
Gerring et al., 1998;
Max et al., 1997;
Max, Castillo, Bokura, et al.,
1998). One explanation for these relationships is that children
with more parent-reported pre-existing behavioral concerns are more vulnerable
to neurological insults. This vulnerability may be related to greater
difficulties coping with or compensating for the adverse effects of injury on
their abilities or motivation. An alternative explanation for our findings is
that smaller changes in behavior were required to detect postinjury-onset
caseness in children with higher levels of pre-existing problems. However,
most children with postinjury-onset caseness showed substantial pre- to
postinjury changes in behavior.
With regard to concurrent correlates, several past investigations have
reported associations of post-TBI behavior problems with behavior competence
and adaptive functioning (Fletcher et al.,
1990,
1996), as well as with
substandard adaptive and school functioning
(Anderson et al., 2001;
Kinsella et al., 1995,
1997;
Max, Castillo, Bokura, et al.,
1998). These associations may reflect either the broader
influences of factors responsible for the behavior problems, or the effects of
the behavior problems themselves on other aspects of functioning.
Associations between postinjury-onset behavior problems and adverse
long-term family outcomes after TBI have also been reported
(Barry et al., 1996;
Max, Castillo, Robin, et al.,
1998; Rivara et al.,
1994). In this study, children with postinjury-onset caseness did
not differ from children without caseness in measures of preinjury or early
postinjury family status. The relationship between postinjury-onset caseness
and negative family outcomes at the extended follow-up thus appears to have
emerged after TBI. The direction of potential child-family influences is
difficult to establish. Although child behavior problems may have contributed
to postinjury parent distress and family burden, adverse family reactions to
injury may have exacerbated child behavior problems. Previous analysis of
child and family data from this study supports the possibility of such
bidirectional relationships (Taylor et
al., 2001).
Neuropsychological testing generally failed to discriminate children with
postinjury-onset caseness from those without caseness, whether given soon
after TBI or several years later. The only neuropsychological difference
observed was on Consonant Trigrams at the extended follow-up. The latter
finding suggests that children with postinjury-onset caseness may have
weaknesses in verbal working memory. Armstrong, Mangeot, Colvin, Yeates, and
Taylor (2002) found
associations between working memory using Consonant Trigrams and parent
ratings of executive functioning, a construct likely related to behavioral
self-regulation. Nevertheless, the general absence of associations between
cognitive and behavior outcomes is consistent with observations from past
studies (Brown et al., 1981;
Fletcher et al., 1990). One
explanation for the absence of associations is that many neuropsychological
tests are insensitive to the types of cognitive problems that accompany
post-TBI behavior problems, such as subtle deficits in metacognition or
pragmatic judgment (Dennis, Guger,
Roncadin, Barnes, & Schachar, 2001). Another possibility is
that brain systems that mediate behavior and self-regulation are distinct from
those that mediate cognitive functions of the sort measured by most
neuropsychological tests (Eslinger,
Biddle, & Grattan, 1997), and TBI differentially affects these
systems.
Limitations
One major limitation of this study is that attrition was highest in the
ORTHO group and in children from lower SES. Higher dropout among children in
the ORTHO group may have diminished statistical power to detect group
differences. A higher dropout rate among children with lower socieoeconomic
status may have also reduced or obscured differences between the groups of
children with and without postinjury-onset caseness. Although sociodemographic
factors were included as covariates in the analyses, caution is advised in
generalizing the findings to the broader population of children with TBI.
A further study limitation is that we relied on parent ratings to identify
caseness. Our use of the CBCL was justified by its validity in distinguishing
clinical from nonclinical samples, as well as by the fact that children with
postinjury-onset caseness had higher rates of child and family counseling than
children without caseness. Nevertheless, some investigators have reported that
the CBCL has a low sensitivity to behavioral sequelae of pediatric TBI
(Fletcher & Ewing-Cobbs,
1991; Kinsella et al.,
1995; Knights et al.,
1991). Two recent studies found that structured interviews
identified more post-TBI behavior problems than did parent ratings and that
parent ratings were least effective in identifying internalizing problems
(Bloom et al., 2001;
Green, Foster, Morris, Muir, & Morris,
1998). Our procedure of excluding children who had preinjury
caseness may also have resulted in underestimating rates of postinjury-onset
disorders, as previous studies found new forms of behavior problems among
children who met criteria for pre-existing diagnoses
(Bloom et al., 2001;
Max et al., 1997).
Other concerns are that the parent ratings were used to assess both child
and family outcomes and that ratings of preinjury child behavior were
retrospective. Reliance on parent ratings in assessing both child behavior and
family outcomes also raises the possibility that shared method variance may
have contributed to associations between these measures. With respect to the
preinjury ratings, parents' perceptions of their child's preinjury behavior
may have been affected by the injury itself. Although the parent's ratings
were collected soon after the injury and the efficacy of this method has been
demonstrated in previous studies (Rivara
et al., 1994; Rutter et al.,
1983), biases due to retrospective recall cannot be ruled out.
Our small sample size is an additional concern. Despite the relatively large sample of children with moderate to severe TBI initially recruited, some were lost to follow-up, a number of those followed had preinjury caseness, and postinjury-onset caseness was identified in only a fraction of the remaining children. Although this is the first study to comprehensively examine factors associated with long-term behavioral status, larger samples are needed to identify the predictors and correlates of postinjury-onset disorders with greater precision.
Significance and Future Directions
Findings that the majority of children with moderate to severe TBI did not
have long-term postinjury-onset caseness may provide some reassurance to many
families. Assessment of the injured child's preinjury behavior and the family
resources may assist in the identification of the children who most need
monitoring. Our data indicate that children with severe TBI, previously
identified behavior concerns, and limited family resources are most at risk
and may deserve careful follow-up and more intensive school and support
services, even if neuropsychological testing fails to reveal deficits.
Psychological interventions with the child and family within the first year
after injury may help to reduce the incidence or extent of long-term problems.
Although there is a scarcity of research demonstrating the effectiveness of
interventions for children with TBI, family-based approaches deserve
consideration in treating the behavioral sequelae of TBI
(Wade, Drotar, Taylor, & Stancin,
1995). Continued monitoring of behavior beyond the first year is
also advised to identify children with later-emerging problems.
Future research is needed to examine risk factors for postinjury-onset
behavior disorders in greater detail, including predisposing child
characteristics, type of brain insult, and environmental influences.
Additionally, we need to better understand the mechanisms responsible for both
the emergence of behavior problems after injury and behavioral resiliency
(Masten, 2001). Comprehensive
assessment of behavioral outcomes, their evolution over time postinjury, and
their cognitive correlates will also be useful
(Dennis et al., 2001). The
development and testing of clinical interventions for those at risk for or
those who have developed long-term behavioral problems following TBI are also
recommended. Advances will require large, multisite samples and study designs
that help to isolate the effects of TBI.
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Acknowledgments |
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This work was supported by NINDS grant NS36335, National Institutes of Health, grant MCJ-390611, Maternal and Child Health Bureau (Title V, Social Security Act, Health Resources and Services Administration, Department of Health and Human Services), and by National Institute of Mental Health grant 18330, research training in pediatric psychology. We acknowledge the contributions of Elizabeth Shaver, Anne Birnbaum, Nichole Wood, Sharon Armstrong, Barbara Shapero, Madeline Polonia, and Matt Diamond in data collection; Nori Minich in data management and analysis; and Anne Birnbaum for her assistance in manuscript preparation. We also acknowledge the participation of the Children's Hospital Medical Center of Akron and the collaboration of George Thompson, MD, G. Dean Timmons, MD, and Dennis Weiner, MD. Assistance with recruitment was provided by the Rainbow Pediatric Trauma Center, Rainbow Babies & Children's Hospital, Columbus Children's Hospital Trauma Program, and MetroHealth Center Trauma Registry.
Received February 11, 2002; revision received May 2, 2002; accepted May 29, 2002
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