Theoretical Framework - TBI

Long-Term Behavior Problems Following Pediatric Traumatic Brain Injury: Prevalence, Predictors, and Correlates

Lisa Schwartz,1 MA, H. Gerry Taylor,1,2 PhD, Dennis Drotar,1,2 PhD, Keith Owen Yeates,3 PhD, Shari L. Wade,4 PhD, and Terry Stancin,1,5 PhD 1Case Western Reserve University, 2Rainbow Babies & Children’s Hospital, 3The Ohio State

University and Columbus Children’s Hospital, 4University of Cincinnati and Children’s Hospital

Medical Center, 5MetroHealth Medical Center

Objective To study identified rates of long-term behavior problems in children with trau- matic brain injury (TBI) compared to children with only orthopedic injuries and risk factors

and correlates for new behavior problems following TBI. Methods Sample included chil- dren 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 ex-

tended follow-up a mean of 4 years after injury. Results The prevalence of caseness, de- fined 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 in-

cluded weakness in working memory and adaptive behavior skills, poorer behavior and school

competence, and adverse family outcomes. Conclusions Postinjury-onset caseness is persis- tent, risks are multifactorial, and correlates include child dysfunction and family sequelae.

Key words traumatic brain injury; children; behavior problems; caseness; risk factors; family functioning.

Journal of Pediatric Psychology, Vol.  No. , , pp. – ©  Society of Pediatric Psychology DOI: ./jpepsy/jsg

All correspondence should be sent to Lisa Schwartz, Department of Psychology, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, Ohio 44106-7123. E-mail: [email protected].

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 cog- nitive 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). Be- havioral 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 postin- jury 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 crite- ria for a new psychiatric disorder, 11 of whom (26%) had

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a disorder that persisted beyond the 12-month assess- ment. Max et al. (2000) also examined rates of personal- ity change disorder, a syndrome of behavioral change re- sulting from brain damage. Persistence of personality change disorder was found in about 40% of the TBI par- ticipants at an average of 2 years after injury. All of the children with persistent personality change disorder sus- tained 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 af- ter injury revealed new problems in 27 of 46 children in the sample (58%). Twenty-two children (48%) had prob- lems 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 prob- lems 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 chil- dren with severe TBI who had new problems had greater family adversity and more “subclinical” preinjury behav- ior 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) re- ported that children with new postinjury psychiatric di- agnoses had higher rates of preinjury psychiatric distur- bance 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 stud- ies have found a relationship between cognitive func- tioning and new psychiatric disorders (Max et al., 1999), while others have reported weak relationships between behavioral and cognitive outcomes of pediatric TBI (An- derson et al., 2001; Fletcher et al., 1990). Brown et al. (1981) found a relationship between new psychiatric dis- orders 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 assess- ments of child and family outcomes. Assessment of these problems is important in estimating incidence rates, de- termining which children are at greatest risk, and ad- vancing knowledge regarding possible etiologies. Inves- tigation of concurrent correlates of these problems is required to understand associated child and family mor- bidity. 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 out- comes 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 moder- ate 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 signif- icant postinjury behavior problems, or caseness, in children with TBI relative to children who had sustained orthope- dic 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 assess- ments. A second aim was to identify risks for the devel- opment 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 con- sidered 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 dif- ferences would be found even when the presence/absence of preinjury caseness and sociodemographic factors were taken into account. Based on findings suggesting that be- havior problems emerge relatively soon after TBI and per- sist 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 in- jury. The second hypothesis was that predictors of postin- jury-onset caseness in children with TBI would include greater TBI severity, higher levels of reported preinjury behavior problems, greater cognitive impairment soon af- ter 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 Sample

The follow-up sample consisted of 134 of the 189 partic- ipants 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 be- tween 1992 and 1995. The study was approved by the in- stitutional review board at each institution, and informed consent was obtained prior to participation. Criteria for in- clusion were (a) at least one night’s hospitalization for a traumatic brain or orthopedic injury, (b) age at injury be- tween 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 de- fined 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, in- tracranial 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 pos- sible brain insult (e.g., concussion, severe facial trauma).

Injury severity was further described using the Mod-

ified 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 In- dex (Hollingshead, 1975), and the Socioeconomic Com- posite 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 So- cioeconomic Index (Stevens & Featherman, 1981), an- nual family income as coded on the Life Stressors and So- cial Resources Inventory (Moos & Moos, 1988), and a 7-point maternal education scale. Higher SCI scores re- flect 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 pe- riods. These two groups were also similar in injury sever- ity to areas of the body other than the head. Mean GCS

Long-Term Behavior Problems 

Table I. Characteristics of Follow-up Sample

Severe TBI Moderate TBI ORTHO (n = 42) (n = 42) (n = 50)

Age at injury in years, M (SD) 9.70 (2.07) 9.53 (1.83) 9.40 (1.88)

Years between injury andextended 3.94 (0.94) 4.20 (0.86) 4.15 (0.92)

follow-up

Males (n, %) 33 (79%) 29 (69%) 30 (60%)

Minorities (n, %) 10 (24%) 10 (24%) 22 (44%)

Single-parent households (n, %) 16 (38%) 14 (33%) 27 (54%)

Hollingshead Four Factor Index, M (SD) 38.12 (12.57) 36.80 (13.38) 37.17 (13.08)

Socioeconomic Composite Index, M (SD) – 0.32 (0.77) – 0.38 (0.83) – 0.13 (0.83)

Days hospitalized, M (SD)* 12.88 (9.31) 6.69 (7.12) 14.56 (14.06)

Glasgow Coma Scale Score, M (SD)* 4.62 (1.86) 13.98 (1.88) —

Days of impaired consciousness, M (SD) 5.41 (6.48) 0.19 (0.59) —

Modified Injury Severity Score, M (SD)* 20.19 (12.21) 12.52 (5.74) 7.06 (2.81)

Partial modified injury severity 8.71 (10.78) 2.31 (3.52) 7.06 (2.81)

score, M (SD)

Hollingshead Four Factor Index see Hollingshead, 1975; Modified Injury Severity Score see Mayer et al., 1980. TBI = Traumatic brain injury; ORTHO = orthopedic injury.

See text for definitions of modified injury severity scores and Socioeconomic Composite Index.

*p < .01.

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scores and duration of impaired consciousness for the TBI groups are presented for descriptive purposes.

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 fol- low-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 consid- ered for this study. Child testing consisted of measures of IQ, language skills, perceptual motor abilities, memory, attention and executive function, and academic achieve- ment. Other child characteristics were assessed by admin- istering 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, so- cial relations, and school performance; and TRF academic performance is a rating of performance in academic sub- ject areas. The Vineland is a semistructured parent inter- view that assesses adaptive functioning in the domains of communication, daily living skills, and socialization. To as- sess global school outcomes, we also monitored grade repetitions and special education placements.

Family measures included parent self-report ratings of family functioning, parent psychological distress, and injury-related family burden (see Wade et al., 1998). Fam- ily functioning was assessed by the McMaster Family As- sessment 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 Inven- tory (Derogatis & Melisaratos, 1983) served as a sum-

mary measure of parent psychological adjustment. Family burden was measured by the Family Burden of Injury In- terview (Burgess et al., 1999) and the Impact on Family Scale, Version G (Stein & Jessop, 1985). The Family Bur- den 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 ex- tended 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 dis- ability (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 ex- tended 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, Pas- sage Comprehension and Dictation) due to lack of dis- crimination between the groups at earlier points postinjury. In place of these tests, we administered the Oral Expres- sion and Figurative Language subtests of the Test of Lan- guage Competence-Expanded Version (Wiig & Secord, 1985) to further assess language skills, Consonant Tri- grams (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 counter- balanced order across children to minimize test order ef- fects. 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 be- havior 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 Prob- lem scale prior to injury had preinjury caseness. Achen-

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Long-Term Behavior Problems 

Table II. Child and Family Measures

Domain/Measure Reference Assessment

Child Measures

IQ

WISC-III for ages <17 years; Wechsler (1991) B, F

WAIS-III for ages > 17 years: Prorated IQ based on Vocabulary,

Similarities, Block Design, and Object Assembly

TONI-2 Brown, Sherbenou, & Johnsen (1990) B

Language

Boston Naming Test Yeates (1994) B, F

Controlled Oral Word Association Test Spreen & Strauss (1991) B, F

Token Test, Part V DiSimoni (1978) B

CELF-R: Sentence Structure, Recalling Sentences Semel, Wiig, Secord, & Sabers (1987) B, F

TLC-E: Screening Composite Wiig & Secord (1985) F

Perceptual-Motor Skills

Grooved Pegboard Test: time per peg averaged across hands Knights & Norwood (1980) B

Developmental Test of Visual-Motor Integration Beery (1989) B, F

Memory

CVLT-C: trials 1-5 total Delis, Kramer, Kaplan, & Ober (1986) B, F

Rey-Osterrieth Complex Figure, recall Bernstein & Waber (1996) F

Attention and Executive function

Continuous Performance Test -3: omissions & commissions Lindgren & Lyons (1984) B, F

Underlining Test: total for subtests 2, 4, & 9 Rourke & Orr (1977) B, F

Contingency Naming Test: efficiency score Anderson, Anderson, Northam, & Taylor (2000) B, F

Consonant Trigrams: total recall Paniak, Millar, Murphy, & Keizer (1997) F

Academic Achievement

WJ-R Woodcock & Mather (1989)

Passage Comprehension, Dictation B

Letter-Word Identification B, F

Writing Samples B, F

Calculation B, F

Behavior Problems

CBCL Behavior Problem Scale Achenbach (1991a) B,a F

TRF Behavior Problem Scale Achenbach (1991b) B,a F

School Performance

TRF School Performance Scale Achenbach (1991b) B,a F

Competence and Adaptive Behavior

CBCL Competence Achenbach (1991a) B,a F

Vineland Adaptive Behavior scales, Adaptive Behavior Sparrow, Balla, & Cicchetti (1984) B,a F

Composite

Family Measures

Family Functioning

FAD-GF Miller, Bishop, Epstein, & Keitner (1985) B,a F

Parent Distress

BSI: Global Severity Index Derogatis & Melisarator (1983) B, F

Family Burden

FBII: total score Burgess et al. (1999) B, F

Impact on Family Scale: total negative impact Stein & Jessop (1985) B, F

B = baseline assessment; F = extended follow-up. WISC-III = Wechsler Intelligence Scale for Children, 3rd ed.; WAIS-III = Wechsler Adult Intelligence Scale, 3rd ed.;

TONI-2 = Test of Nonverbal Intelligence-2; CELF-R = Clinical Evaluation of Language Fundamentals-Revised; TLC-E = Test of Language Competence-Expanded Version;

CVLT-C= California Verbal Learning Test-Children’s Version; WJ-R = Woodcock-Johnson Test of Achievement-Revised; CBCL = Child Behavior Checklist; TRF = Child

Behavior Checklist-Teacher’s Report Form; FAD-GF = Family Assessment Device, General Functioning Scale; BSI = Brief Symptom Inventory; FBII = Family Burden of

Injury Interview. aReflects preinjury child or family status.

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bach (1991a) recommends this cutoff as a means for op- timizing classification into clinical versus nonclinical groups. The CBCL, a widely used behavior rating scale, has good reliability and validity in assessing children’s behav- ior and is normed for school-age children and adolescents. Prior research supports the validity of the CBCL in iden- tifying 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 (Tay- lor 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 chi-square analysis and logistic regression. Differences be- tween each TBI group and the ORTHO group were rep- resented 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 consid- ered 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 mea- sures. 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 iden- tified by comparing the two groups on injury measures, preinjury behavior and academic performance, family measures obtained at baseline, and baseline neuropsy-

chological and achievement skills. Injury measures con- sidered 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 mea- sures within domains.

Results Total Sample

Prevalence of Caseness. Table III presents rates of case- ness prior to injury (baseline ratings) and at each of the follow-ups. The table also summarizes findings from lo- gistic 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 case- ness, 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 fol- low-up (p < .01). Race failed to predict caseness inde- pendently 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.

 Schwartz et al.

Table III. Prevalence of Caseness by Group at Each Assessment (Total Sample)

Odds Ratio (95% CI)

Severe TBI Moderate TBI Severe TBI Moderate TBI ORTHO χ2 (2) vs. ORTHO vs. ORTHO

Baseline (preinjury) 4/42 (10%) 10/41 (24%) 10/50 (20%) 3.31 0.43 (0.12, 1.62) 1.78 (0.59, 5.39)

6-month follow-up 9/39 (23%) 9/41 (22%) 5/46 (11%) 2.67 12.56 (1.64, 95.92)*10.48 (1.40, 77.64)*

12-month follow-up 12/39 (31%) 9/40 (23%) 6/46 (13%) 3.94 27.11 (3.03, 243.02)** 4.88 (0.77, 30.63)

Extended follow-up 15/42 (36%) 9/41 (22%) 5/50 (10%) 8.85* 12.12 (3.00, 49.03)** 3.96 (1.01, .55)*

TBI = traumatic brain injury; ORTHO = orthopedic injury. Odds ratios (confidence intervals) were obtained from logistic regressions that controlled for the Socioeconomic

Composite Index (SCI), gender, and race. The presence of preinjury caseness was also included as a covariate in logistic analyses of the follow-up data.

*p < .05.

**p < .01.

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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, χ2 (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 crite- ria for caseness at the extended follow-up, including 12 of 38 (32%) with severe TBI and 3 of 31 (11%) with moderate TBI, χ2 (1, N = 69) = 3.61, p = .06. Of the 15 children with postinjury-onset caseness, 13 met criteria for exter- nalizing problems, 8 met criteria for internalizing prob- lems, 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 behav- ior, 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 with- out caseness, χ2 (1, N = 69) = 5.52, p < .05. Predictors of Postinjury-Onset Caseness. Logistic re- gressions 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 prein- jury 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 perfor- mance, 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 fam- ily outcomes. According to these results, the children with caseness had lower scores on the Vineland Adaptive Be- havior Composite and Consonant Trigrams. The children with caseness also had poorer family outcomes, includ- ing higher parent distress and greater injury-related fam- ily burden, as well as poorer family functioning.

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 edu- cation at the extended follow-up, compared to 10 of 54 (19%) of the children without caseness, χ2 (1, N = 69) = 10.99, p < .01. Controlling for covariates, we found that lo- gistic 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).

Discussion

This study extends the knowledge of long-term behav- ioral sequelae of pediatric TBI by describing the preva- lence 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 ex- amination 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 mod- erate to severe TBI had higher rates of caseness at the ex- tended follow-up than the ORTHO group, even after con- trolling for presence/absence of preinjury caseness and

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for sociodemographic factors. As in past studies, children with severe TBI were most often affected, and most chil- dren 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 ad-

vantaged, 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 con- currently associated with weaknesses on a test of working

 Schwartz et al.

Table IV. Child and Family Measures Associated With Postinjury-Onset Caseness at the Extended Follow-Up: Concurrent Correlates

With Caseness W/out Caseness (n = 15) (n = 54) Group Effect

Domain/Measure M (SD) M (SD) from ANCOVA

Child Measures

IQ

WISC-III/WAIS-III 92.87 (16.95) 100.72 (20.19) F(1, 62) = 0.76

Language

Boston Naming Test – 0.30 (0.99) – 0.02 (0.95) F(1, 62) = 0.21

Controlled Oral Word Association – 0.67 (0.81) – 0.25 (1.05) F(1, 62) = 0.23

CELF-R Recalling Sentences 7.86 (3.18) 9.37 (2.75) F(1, 59) = 0.67

TLC-E Screening Composite 80.13 (14.44) 90.30 (15.69) F(1, 62) = 0.06

Perceptual Motor Skills

Developmental Test of Visual-Motor Integration 86.40 (14.08) 96.00 (16.80) F(1, 61) = 1.88

Memory

CVLT-C Trials 1-5 total – 0.48 (1.45) – 0.04 (1.10) F(1, 62) = 0.26

Rey-Osterreith Complex Figure, recall – 0.08 (1.05) – 0.04 (0.86) F(1,60) = 0.00

Attention and Executive Function

Continuous Performance Test, omissions and commisions – 0.01 (0.62) – 0.16 (0.83) F(1, 51) = 0.27

Underlining Test, total for subtests 2, 4, & 9 – 0.77 (1.15) – 0.10 (1.06) F(1,62) = 1.15

Contingency Naming Test efficiency score – 0.44 (0.94) 0.10 (1.16) F(1, 62) = 0.06

Consonant Trigrams – 0.97 (1.44) 0.08 (1.13) F(1, 62) = 7.17**

Academic Achievement

WJ-R Letter-Word Identification 96.00 (14.98) 103.06 (16.26) F(1, 62) = 0.01

WJ-R Writing Samples 88.53 (13.49) 102.92 (20.90) F(1, 62) = 0.86

WJ-R Calculations 88.60 (11.64) 98.26 (15.90) F(1, 60) = 0.40

School Performance

TRF School Performance Scale 41.23 (6.02) 48.14 (8.76) F(1, 56) = 2.61

Competence and Adaptive Behavior

CBCL Competence 35.67 (5.79) 46.81 (10.80) F(1, 63) = 3.88

Vineland Adaptive* Behavior Composite 77.87 (17.33) 93.54 (14.41) F(1,63) = 4.68*

Family Measures

Family Functioning

Family Assessment Device-General Functioning 2.17 (0.40) 1.74 (0.44) F(1, 63) = 7.07*

Parent Distress

BSI Global Severity Index 60.13 (10.38) 51.40 (8.83) F(1,62) = 8.54**

Family Burden

FBII, z score for total score 1.19 (0.83) 0.32 (0.56) F(1,63) = 11.00**

Impact on Family Scale, total negative impact 31.27 (5.42) 24.67 (5.13) F(1, 63) = 9.25**

ANCOVA = analyses of covariance; WISC-III = Wechsler Intelligence Scale for Children, 3rd ed.; WAIS-III = Wechsler Adult Intelligence Scale, 3rd ed.; CELF-R = Clinical

Evaluation of Language Fundamentals-Revised; TLC-E = Test of Language Competence-Expanded Version; WJ-R = Woodcock-Johnson Tests of Achievement-Revised;

TRF = Child Behavior Checklist-Teacher’s Report Form; CBCL = Child Behavior Checklist; FAD-GF = Family Assessment Device, General Functioning Scale; BSI = Brief

Symptom Inventory; FBII = Family Burden of Injury Interview. Only children with TBI who did not have preinjury caseness were considered in the analyses. Covariates

included in ANCOVA were TBI group (severe vs. moderate), the Socioeconomic Composite Index (SCI), race, and gender. Only significant differences are listed. Higher

scores on all family measures reflect poorer outcomes.

*p < .05, Bonferroni corrected.

**p < .01, Bonferroni corrected.

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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 be- come 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 an- other 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, & Shaf- fer, 1983). Although the mechanisms responsible for these associations are unclear, the family and professional re- sources needed to effectively manage cognitive and be- havioral consequences of TBI may be less available in dis- advantaged settings. Children with TBI also may be more vulnerable than other children to the stresses in these en- vironments (Taylor et al., 2002).

Past studies also document relationships between preinjury child functioning and postinjury-onset prob- lems (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 vul- nerable 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 mo- tivation. 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 in- vestigations have reported associations of post-TBI be- havior 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 them- selves on other aspects of functioning.

Associations between postinjury-onset behavior prob- lems 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, chil- dren 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 af- ter 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 pos- sibility of such bidirectional relationships (Taylor et al., 2001).

Neuropsychological testing generally failed to dis- criminate children with postinjury-onset caseness from those without caseness, whether given soon after TBI or several years later. The only neuropsychological differ- ence 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 be- havioral 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 neuropsycholog- ical tests are insensitive to the types of cognitive prob- lems 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 be- havior and self-regulation are distinct from those that me- diate 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

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may have diminished statistical power to detect group dif- ferences. A higher dropout rate among children with lower socieoeconomic status may have also reduced or obscured differences between the groups of children with and with- out postinjury-onset caseness. Although sociodemographic factors were included as covariates in the analyses, caution is advised in generalizing the findings to the broader pop- ulation of children with TBI.

A further study limitation is that we relied on parent ratings to identify caseness. Our use of the CBCL was jus- tified by its validity in distinguishing clinical from non- clinical 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. Nev- ertheless, 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 struc- tured interviews identified more post-TBI behavior prob- lems 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 be- havior may have been affected by the injury itself. Al- though the parent’s ratings were collected soon after the in- jury 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. De- spite 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 frac- tion 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 se- vere TBI did not have long-term postinjury-onset case- ness may provide some reassurance to many families. As- sessment 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 be- havior 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 demon- strating 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 be- havior 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, in- cluding 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). Comprehen- sive 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 re- quire large, multisite samples and study designs that help to isolate the effects of TBI.

Acknowledgments

This work was supported by NINDS grant NS36335, Na- tional Institutes of Health, grant MCJ-390611, Maternal and Child Health Bureau (Title V, Social Security Act, Health Resources and Services Administration, Depart- ment of Health and Human Services), and by National Institute of Mental Health grant 18330, research training in pediatric psychology. We acknowledge the contribu- tions 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

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assistance in manuscript preparation. We also acknowledge the participation of the Children’s Hospital Medical Cen- ter of Akron and the collaboration of George Thompson, MD, G. Dean Timmons, MD, and Dennis Weiner, MD. Assistance with recruitment was provided by the Rain- bow Pediatric Trauma Center, Rainbow Babies & Chil- dren’s Hospital, Columbus Children’s Hospital Trauma Program, and MetroHealth Center Trauma Registry.

Received February 11, 2002; revisions received May 2, 2002; accepted May 29, 2002

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