Long-Term Attention Problems in Children With Traumatic Brain Injury

Long-Term Attention Problems in Children With Traumatic Brain Injury KEITH OWEN YEATES, PH.D., KIRA ARMSTRONG, PH.D., JENNIFER JANUSZ, PH.D., H. GERRY TAYLOR, PH.D., SHARI WADE, PH.D., TERRY STANCIN, PH.D., AND DENNIS DROTAR, PH.D

ABSTRACT Objective: To examine long-term attention problems and their cognitive correlates after childhood traumatic brain injury (TBI). Method: Data were drawn from a prospective, longitudinal study conducted between 1992 and 2002. Participants included 41 children with severe TBI, 41 with moderate TBI, and 50 with orthopedic injury (OI), who were all between 6 and 12 years of age at the time of injury. Parent ratings of attention problems were obtained at a long-term follow-up on average 4 years post-injury and compared with ratings of premorbid attention problems obtained shortly after injury. At the long-term follow-up, children also completed several cognitive tests of attention and executive functions. Results: Hierarchical linear and logistic regression analyses indicated that the severe TBI group displayed significantly more attention problems than the OI group at 4 years post-injury, both behaviorally and cognitively, after controlling for race, socioeconomic status, and premorbid attention problems. At long-term follow-up, 46% of the severe TBI group displayed significant attention problems on the Child Behavior Checklist, as opposed to 26% of the OI group (odds ratio = 3.38; 95% confidence interval, 1.15–9.94). On the Attention-Deficit/Hyperactivity Disorder Rating Scale, 20% of the severe TBI group displayed clinically significant attention problems compared with 4% in the OI group (odds ratio = 9.59; 95% confidence interval, 1.24–73.99). However, group differences in behavioral symptoms were significantly larger for children with more premorbid symptoms than for children with fewer premorbid problems. Measures of executive functions were significantly related to behavioral attention problems, after controlling for group membership, race, and socioeconomic status. Conclusions: Childhood TBI exacerbates premorbid attention problems. Long-term behavioral symptoms of attention problems are related to the cognitive deficits in attention and executive functions that often occur in association with childhood TBI. J. Am. Acad. Child Adolesc. Psychiatry, 2005;44(6):574–584. Key Words: traumatic brain injury, attention, outcomes children.

Accepted January 11, 2005. From the Department of Pediatrics, The Ohio State University and Columbus Children’s Research Institute, Columbus, OH (Drs. Yeates, Armstrong, and Janusz); Department of Pediatrics, Case Western Reserve University and Rainbow Babies and Children’s Hospital, Cleveland (Drs. Taylor and Drotar); College of Medicine, University of Cincinnati and Department of Physical Medicine and Rehabilitation, Children’s Hospital Medical Center, Cincinnati (Dr. Wade); and Department of Pediatrics, Case Western Reserve University and MetroHealth Medical Center, Cleveland (Dr. Stancin). A preliminary version of the paper was presented at the annual meeting of the International Neuropsychological Society in Chicago, February 2001. The research presented here was supported by grant MCJ 390611 from the Maternal and Child Health Research Bureau, Health Resources and Services Administration, Department of Health and Human Services, and by grant 5 RO1 NS36335 from the National Institute of Neurological Disorders and Stroke. The authors acknowledge the contributions of Matt Diamond, Marla Kemmerer, Madeline Polonia, Barbara Shapero, Elizabeth Shaver, and Nichole Wood. Special thanks also are due to the Rainbow Pediatric Trauma Center at Rainbow Babies and Children’s Hospital, the Trauma Program at Children’s Hospital of Columbus, and the Trauma Center at MetroHealth Medical Center. They also acknowledge the participation of the Children’s Hospital Medical Center of Akron.

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Traumatic brain injury (TBI) is a leading cause of death and disability among children and adolescents, with an annual incidence estimated at 180 cases per 100,000 in children aged 1–15 in the United States (Kraus, 1995). Among survivors, childhood TBI results in a variety of deleterious outcomes, including cognitive deficits, behavioral problems, poor school performance, and declines in adaptive behavior, especially after more severe injuries (Yeates, 2000). The negative sequelae of TBI often persist well beyond the acute stages of recovery (Taylor et al., 2002; Yeates et al., 2002). Correspondence to Dr. Keith Owen Yeates, Department of Psychology, Children’s Hospital, 700 Children’s Drive, Columbus, OH 432205; e-mail: yeatesk@ chi.osu.edu. 0890-8567/05/4406–0574 2005 by the American Academy of Child and Adolescent Psychiatry. DOI: 10.1097/01.chi.0000159947.50523.b4

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Attention problems are a common long-term outcome of childhood TBI. Existing research on attention problems in childhood TBI reflects two distinct foci: behavioral symptoms (e.g., inattention, impulsivity, hyperactivity) and cognitive functioning (e.g., sustained, focused, and divided attention as well as related aspects of executive functions). These two aspects of attention have been clearly distinguished in the study of attentional disorders (Barkley, 1994; Fletcher et al., 1994), and research indicates that children with TBI display attention problems in both domains (Anderson et al., 1998; Bloom et al., 2001; Catroppa and Anderson, 1999; Catroppa et al., 1999; Dennis et al., 1995, 2001; Ewing-Cobbs et al., 1998; Fenwick and Anderson, 1999; Gerring et al., 1998; Kaufmann et al., 1993; Konrad et al., 2000; Max et al., 1997, 1998, 2004; Schachar et al., 2004; Vriezen and Pigott, 2000; Wassenberg et al., 2004b). Studies of behavioral symptoms typically take either a categorical or dimensional approach to assessing attention problems. The former approach is illustrated by research examining the occurrence of symptoms of attention-deficit/hyperactivity disorder (ADHD) after childhood TBI. Secondary or acquired ADHD has been found to occur at significantly higher rates in children with TBI than in children without injuries or those with injuries not involving the head as well as compared with normative expectations, with prevalence rates ranging from approximately 20% to 50% (Bloom et al., 2001; Gerring et al., 1998; Konrad et al., 2000; Max et al., 1997, 2004; Schachar et al., 2004; Wassenberg et al., 2004b). Rates of secondary ADHD are usually higher among children with more severe TBI (but see Schachar et al., 2004). Studies using a dimensional approach typically have used standardized rating scales (e.g., Child Behavior Checklist) (Achenbach, 1991) and also have found higher scores in children with TBI than in comparison groups or as compared with normative expectations, with more pronounced attention problems again associated with more severe TBI (Anderson et al., 1998; Dennis et al., 2001; Fenwick and Anderson, 1999; Gerring et al., 1998; Max et al., 1998; but see Vriezen and Pigott, 2000). Children with TBI display an elevated level of behavioral symptoms premorbidly compared with noninjured controls or normative expectations (Bloom et al., 2001; Gerring et al., 1998; Max et al., 1997, 2004; but see Schachar et al., 2004). However, many studies have

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not obtained any information about premorbid attention problems or have done so long after the TBI actually occurred, increasing the likelihood of retrospective bias (Anderson et al., 1998; Fenwick and Anderson, 1999; Konrad et al., 2000; Max et al., 1997; Schachar et al., 2004; Vriezen and Pigott, 2000). A related problem is that studies often include comparison groups that do not adequately control for preexisting differences in attention problems or for other factors that may be related to the occurrence of postinjury attention problems (Bloom et al., 2001; Gerring et al., 1998; Max et al., 1997; Wassenberg et al., 2004b). For instance, many studies have used noninjured children for comparison purposes. Yet noninjured children likely differ from children who sustain traumatic injuries in their premorbid level of attention problems (Asarnow et al., 1995). Children who sustain traumatic injuries not involving the head (e.g., orthopedic injuries [OI]) constitute a more appropriate comparison group because they are likely to be similar to children with severe TBI in terms of both premorbid functioning and the severity of injuries not involving the brain. Nevertheless, children with OI have been used as a comparison group in very few studies of attention problems in childhood TBI (Max et al., 2004; Schachar et al., 2004). No published study has directly examined the potential moderating influence of premorbid behavioral symptoms on later attention problems. Research suggests that the outcomes of acquired brain impairment in childhood depend in part on premorbid functioning (Dennis, 2000). Premorbid attention problems may reflect a reduction in reserve capacity (Satz, 1993; Stern, 2002), lowering the threshold for significant postinjury attention problems after TBI. Studies of ADHD have provided evidence of morphological differences in frontostriatal and cerebellar brain regions (Berquin et al., 1998; Casey et al., 1997; Castellanos et al., 1996; Mostofsky et al., 1998). Those regions also are frequently damaged in childhood TBI (Levin et al., 1989). The effect of damage to regions that already display subtle structural differences—as may be the case for children with premorbid attention problems—may be multiplicative rather than additive, resulting in significant postinjury increases in attention problems. Several studies have suggested that children with TBI who display premorbid attention problems are more likely than those without premorbid attention problems

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to display secondary ADHD (Bloom et al., 2001; Gerring et al., 1998; Max et al., 1997, 2004; Schachar et al., 2004), but none of these studies determined whether this was more often the case for children with TBI than for children with injuries not involving the head. A true test of whether premorbid behavioral symptoms moderate the expression of attention problems after childhood TBI requires a statistical analysis that examines the interaction between premorbid functioning and injury status (TBI versus non-TBI). Although categorical and dimensional measures of behavioral symptoms of ADHD are often in close accord (Biederman et al., 1993; Boyle et al., 1997; Wassenberg et al., 2004a), a dimensional approach lends itself more readily to examining the moderating influence of premorbid status because of the increased statistical power afforded by a continuous measure of attention problems (McClelland and Judd, 1993). Research on the cognitive aspects of attention in TBI has focused largely on inhibitory control, using measures such as continuous performance tests and stop signal tasks (Anderson et al., 1998; Catroppa and Anderson, 1999; Catroppa et al. 1999; Dennis et al., 1995, 2001; Fenwick and Anderson, 1999; Kaufmann et al., 1993; Konrad et al., 2000; Schachar et al., 2004; Vriezen and Pigott, 2000; Wassenberg et al., 2004b). Most studies have found deficits in inhibitory control that are related to injury severity. A few studies have examined a broader range of cognitive measures of attention (Anderson et al., 1998; Ewing-Cobbs et al., 1998; Fenwick and Anderson, 1999; Vriezen and Pigott, 2000). The latter studies have largely found more marked impairment among children with severe TBI than among children with mild TBI or noninjured children, although the studies varied in the tasks used, their assignment to particular domains of attention, and their underlying models of attention, hampering generalizations in terms of which aspects of attention were most affected. Few studies have measured the cognitive and behavioral dimensions of attention simultaneously in children with TBI, much less examined the relationship between those dimensions. Deficits in inhibitory control have been found to be inconsistently associated with secondary ADHD and parent ratings of inattention in children with TBI (Dennis et al., 2001; Konrad et al., 2000; Wassenberg et al., 2004b). A failure to find strong relationships between cognitive and behavioral dimen-

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sions of attention in children with TBI would not be surprising. In children with ADHD, inhibitory control and other aspects of attention and executive functions are associated with behavioral symptoms, but the relationship is often modest (Doyle et al., 2000; Grodzinsky and Barkley, 1999). More generally, the cognitive sequelae of childhood TBI are not strongly related to behavioral functioning (Fletcher et al., 1990). The current study was designed to examine longterm attention problems of children with TBI. We relied on data collected as part of a prospective longitudinal study of children injured between the ages of 6 and 12 (Taylor et al., 1995). Participants included children with moderate to severe TBI and a comparison group of children with orthopedic injuries not involving the head. Parents completed standardized ratings of attention problems retrospectively soon after the child’s injury, to assess premorbid functioning, and again during a long-term follow-up assessment that occurred on average 4 years post-injury. Additionally, the children were administered neuropsychological tests at the long-term follow-up assessment that included several measures of attention and executive functions. The first goal of the study was to examine the impact of childhood TBI on cognitive and behavioral aspects of attention and specifically to assess the moderating influence of premorbid behavioral symptoms on long-term attention problems after TBI. We hypothesized that children with moderate to severe TBI would display long-term behavioral symptoms of attention problems, as well as deficits in cognitive aspects of attention. However, based on the assumption that premorbid attention problems lower the threshold for significant attention problems post-injury, children with premorbid behavioral symptoms before their TBI were expected to demonstrate more significant postinjury attention problems relative to children with orthopedic injury. The study’s second goal was to examine the concurrent relationship between cognitive and behavioral aspects of attention. Based on recent theoretical models of ADHD that posit core deficits in executive functions (Barkley, 1997) and on research showing significant relationships between cognitive and behavioral aspects of attention among children with ADHD (Doyle et al., 2000; Grodzinsky and Barkley, 1999), we anticipated that children’s performance on measures of attention and executive functions would be significantly related to parent ratings of attention problems.

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Consistent with previous reports (Taylor et al., 2002; Yeates et al., 2002), severe TBI was defined by a lowest post-resuscitation Glasgow Coma Scale (GCS) (Teasdale and Jennett, 1974) score of £8. Moderate TBI was defined by a GCS score of 9–12 or by a score of 13–15 accompanied by skull fracture; intracranial mass, lesion, or contusion; diffuse cerebral swelling; posttraumatic neurological abnormality; or loss of consciousness greater than 15 minutes. All children in the TBI groups had a GCS of £12, intracranial abnormalities on neuroimaging, or a sustained loss of consciousness. Children with brain injuries resulting from causes other than blunt head trauma were excluded. Many children with TBI also had orthopedic injuries, but children were excluded from the OI group if they demonstrated any evidence of possible brain injury (e.g., symptoms of concussion, severe facial trauma). The current study was based only on children who completed the extended follow-up evaluation approximately 4 years post-injury and had all data needed for the analyses described below. The available sample consisted of 132 children, including 41 with severe TBI, 41 with moderate TBI, and 50 with OI. Attrition occurred primarily because of family relocation, unwillingness to continue participation, and multiple missed appointments. Attrition did not vary significantly across groups but was highest in the OI group (37%) and lowest in the severe TBI group (23%). Children participating in the extended follow-up did not differ from nonparticipants in age at injury, sex, race, or measures of premorbid child and family functioning obtained shortly after recruitment. Dropouts in all groups had significantly lower family socioeconomic status than children remaining in the study. The groups did not differ significantly in gender, age at injury, age at testing, or time post-injury (Table 1). The groups also did not differ on the Socioeconomic Composite Index (Yeates and Taylor, 1997), which combined measures of parent education, family income, and parent occupational status. The groups did differ significantly in race, with proportionally more white children in the TBI groups than in the OI group, x 22 = 6.35, p < .05. The racial imbalance likely reflects differences in emergency transport patterns at the hospitals involved in the study.

METHOD Study Design and Overview of Procedures The study relied on data collected during a multisite project that used a concurrent cohort, prospective design (Taylor et al., 1995). Children with moderate to severe TBI or OI without brain insult were recruited shortly after being hospitalized for their injuries. Children and their families were invited to participate after children were medically stable. Before participating, parents or guardians of all children provided written informed consent and children provided written assent. The informed consent protocol was approved by the institutional review boards at all sites. The OI group was included to compare the consequences of TBI with those of traumatic injuries more generally and to control for factors related to the likelihood of accidental injury and the experience of hospitalization. Children and parents were assessed on multiple occasions. The data for this study were gathered at a baseline assessment that occurred on average 1 week after injury (range 0–42 days; SD = 6.89 days) and again at an extended follow-up that occurred on average 4.11 years post-injury (range 2.37–5.84 years; SD = 0.91 years). Participants The original sample included 189 children recruited from four hospitals in northern and central Ohio, 53 with severe TBI, 56 with moderate TBI, and 80 with OI only. Children met several inclusion criteria: (1) hospitalization for at least one night for moderate to severe TBI, with or without OI, or for OI only; (2) age at injury between 6 and 12 years; (3) no evidence of child abuse or previous brain disease or injury; and (4) English as the family’s primary language at home. Children were not excluded for premorbid learning disabilities, attention problems, or behavior disorders because a major goal of the research was to examine how noninjury-related factors, including children’s preinjury functioning, affect the outcomes of TBI.

TABLE 1 Participant Characteristics Group Variable Age at injury, yr mean (Standard deviation) Time post-injury, yr mean (Standard deviation) Age at long-term follow-up, yr mean (Standard deviation) Male participants, no. (%) White participants, no. (%) Socioeconomic Composite Index, mean (Standard deviation) Glasgow Coma Scale score,* mean (Standard deviation) Days of impaired consciousness,* mean (Standard deviation)

Severe TBI (n = 41)

Moderate TBI (n = 41)

OI (n = 50)

9.7 (2.1) 4.0 (0.9)

9.5 (1.8) 4.2 (0.9)

9.4 (1.9) 4.1 (0.9)

13.7 (2.2) 32 (78) 31 (76)

13.7 (1.7) 28 (68) 32 (78)

13.6 (1.8) 30 (60) 28 (56)

0.04 (0.80)

0.13 (0.85)

–0.14 (0.85)

4.6 (1.9)

14.0 (1.9)

NA

5.1 (6.2)

0.2 (0.6)

NA

Note: Duration of impaired consciousness was defined as the number of days from injury until the child was able to follow a simple verbal command. TBI = traumatic brain injury; OI = orthopedic injury; NA = not applicable. *p < .05.

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Procedures and Measures Parent ratings of children’s premorbid attention problems were obtained at the baseline assessment using the Child Behavior Checklist (CBCL) (Achenbach, 1991). At the long-term follow-up assessment, parents rated children’s postinjury attention problems using the CBCL and the ADHD Rating Scale (DuPaul et al., 1998). Children were also administered a neuropsychological test battery that included measures of overall cognitive ability as well as attention and executive functions. Tests were administered in clusters, and the clusters were counterbalanced across children. Parent Ratings. The CBCL is a well-known standardized rating scale that assesses emotional and behavioral problems, social competence, and academic performance. It has demonstrated satisfactory reliability and validity (Achenbach, 1991). For the current study, analyses were based on T scores for the Attention Problems Scale. The scale has shown acceptable agreement with diagnoses of ADHD based on structured psychiatric interviews (Biederman et al., 1993; Wassenberg et al., 2004a). The ADHD Rating Scale is a standardized rating scale that assesses the severity of the 18 symptoms that serve as diagnostic criteria for ADHD in the DSM-IV (American Psychiatric Association, 1994). It has demonstrated acceptable reliability and validity (DuPaul, 1991; Faries et al., 2001). In the current study, analyses were based on the total score for symptoms of both inattention and impulsivity-hyperactivity. Child Cognitive Tests. To assess overall cognitive ability, children were administered a short form of the WISC-III (Wechsler, 1991) or the WAIS-III (Wechsler, 1997). The short form included the Vocabulary, Similarities, Block Design, and Object Assembly subtests, which generate an estimated Full Scale IQ with a high-validity coefficient (Sattler, 2001). Children also were administered four standardized tests to assess various aspects of attention and executive functions. The Consonant Trigrams Test (Connor et al., 2000; Paniak et al., 1997) assesses complex auditory working memory by asking children to recall sets of three consonants immediately and after counting backward for varying lengths of time (i.e., 3, 9, or 18 seconds). The measure used in this study was the total number of consonants out of 54 possible correctly recalled across all 18 delay trials. The Word Fluency Test (Spreen and Strauss, 1998) assesses speeded word retrieval by asking children to name words as quickly as possible that start with a particular letter (i.e., F, A, and S). The measure used in this study was the total number of words recalled across the three trials. The Contingency Naming Test is a speeded naming task that assesses verbal rule learning, working memory, inhibitory control, and cognitive flexibility. Children are asked to name the colors or shapes of objects depending on increasingly complex rules. Performance was assessed using a measure of efficiency that reflects the ratio of speed to accuracy of performance (Anderson et al., 2000; Anderson et al., 2004). The Underlining Test (Rourke and Orr, 1977) is a cancellation task that assesses focused attention and response speed. Children are asked to underline specific letters, numbers, or objects found within larger arrays in 30- or 60-second time periods. The measure used in this study was the total correct averaged across subtests 2, 4, and 9.

Data Analyses The TBI and OI groups were compared on behavioral and cognitive aspects of attention using hierarchical linear regression analyses. Dependent variables included ratings of long-term postinjury attention problems on the CBCL and ADHD Rating Scale and the

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scores from the four tests of attention and executive functions. For each dependent variable, race, socioeconomic status (i.e., Socioeconomic Composite Index), and the rating of premorbid attention problems on the CBCL were entered as independent variables first to control for demographic variation and premorbid functioning. Two dummy variables representing group membership were entered next to test for group differences. We tested the change in R 2 associated with the dummy variables to determine whether the groups differed overall and also examined tests of the individual dummy variables to compare each TBI group with the OI group. On the third step, the moderating effects of premorbid attention problems were tested by entering interaction terms constructed by multiplying the dummy variables for group membership by the rating of premorbid attention problems. We tested the change in R 2 associated with the interaction terms to determine whether group differences were moderated by premorbid attention problems. We also examined the tests of the individual interaction terms to determine which of the TBI groups displayed evidence of moderation. A parallel set of hierarchical logistic regression analyses was conducted to determine whether the groups differed in the prevalence of clinically significant attention problems. Clinically significant attention problems were defined solely for behavioral outcomes, based on a T score ‡60 on the CBCL (Biederman et al., 1993; Wassenberg et al., 2004a) and ratings of ‘‘pretty much’’ or ‘‘very much’’ for six of nine symptoms of both inattention and impulsivity-hyperactivity on the ADHD Rating Scale (DuPaul et al., 1998). Independent variables were entered in the same steps outlined above. Likelihood ratio tests were used to examine the overall contribution of the two dummy variables representing group membership and the two interaction terms constructed to determine whether premorbid attention problems moderated the effects of TBI. Each TBI group was compared with the OI group using Wald statistics. The four cognitive tests were added to the linear and logistic regression analyses to examine whether cognitive measures of attention and executive functions were associated with postinjury behavioral symptoms. The cognitive measures were added after all other independent variables already mentioned were entered. Finally, to determine whether any relationship found between cognitive and behavioral outcomes was attributable to general intellectual functioning, Full Scale IQ was added as an independent variable in the last step of the analyses.

RESULTS Group Comparisons on Behavioral Symptoms

The groups differed significantly on both the CBCL Attention Problems Scale and the ADHD Rating Scale at the long-term follow-up assessment after controlling for race, socioeconomic status, and premorbid attention problems. As shown in Table 2, group membership accounted for an additional 6% of the variance in the CBCL Attention Problems scale (F 2,126 = 7.10, p < .001) and 4% of the variance in the ADHD Rating Scale (F 2,126 = 7.10, p < .05). For both dependent variables, the specific comparison of the severe TBI and OI groups

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was significant: t = 3.58 for the CBCL, p < .001, and t = 2.00 for the ADHD Rating Scale, p < .05. In contrast, neither contrast of the moderate TBI and OI groups was significant. Premorbid attention problems acted as a significant moderator of long-term attention problems (see Table 2). The interaction between group membership and premorbid attention problems accounted for an additional 5% of the variance in both the CBCL Attention Problems Scale (F 2,124 = 7.06, p < .001) and the ADHD Rating Scale (F 2,124 = 4.58, p < .05). For both dependent variables, the specific test of interaction for the severe TBI and OI groups was significant: t = 3.71 for the CBCL, p < .001, and t = 2.68 for the ADHD Rating Scale, p < .05. On the contrary, neither contrast of the moderate TBI and OI groups was significant. To il-

TABLE 2 Hierarchical Linear Regression Analysis for Long-Term Attention Problems CBCL Attention ADHD Rating Problems Scale Step 1:b Race SCI Premorbid attention problems (CBCL Attention Problems Scale) Total R 2 for step 1 Step 2:b Moderate TBI vs. OI Severe TBI vs. OI DR 2 for step 2 Step 3:b Moderate TBI vs. OI 3 Premorbid attention problems Severe TBI vs. OI 3 prmorbid attention problems DR 2 for step 3 Step 4:b Word Fluency Test Consonant Trigrams Test Underlining Test Contingency Naming Test DR 2 for step 4

–0.03 –0.18*

0.05 –0.13

0.57* .41*

0.50* .29*

0.05 0.27* .06

–0.05 0.17* .04*

0.88

0.17

2.38* .05*

1.98* .05*

–0.03 –0.06 –0.02 –0.20* .05*

–0.11 0.04 0.08 –0.23* .05†

Note: CBCL = Child Behavior Checklist; ADHD = attentiondeficit/hyperactivity disorder; SCI = Socioeconomic Composite Index; TBI = traumatic brain injury, OI = orthopedic injury. *p < .05; †p < .06.

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lustrate the moderating influence of premorbid attention problems, we graphed the linear regression lines predicting postinjury from preinjury attention problems separately for each group for the CBCL and the ADHD Rating Scale (Fig. 1). In both cases, higher levels of premorbid attention problems amplified the risk of longterm attention problems in children with severe TBI compared with children with OI, whereas lower levels mitigated that risk. TBI was associated with a substantial increase in the risk of clinically significant attention problems on both the CBCL (x 22 = 8.23, p < .05) and the ADHD Rating Scale (x 22 = 13.16, p < .001) (Table 3). The odds of a clinically significant attention problem were significantly higher for children with severe TBI than those with OI on both the CBCL (odds ratio [OR] = 3.38; 95% CI: 1.15–9.94) and the ADHD Rating Scale (OR = 9.59; 95% CI: 1.24–73.99); 46% of the severe TBI group displayed a significant attention problems on the CBCL as opposed to 26% of the OI group, and 20% of the severe TBI group displayed clinically significant attention problems on the ADHD Rating Scale as compared with 4% in the OI group. In contrast, the odds did not differ significantly for the moderate TBI and OI groups. The two measures of clinically significant attention problems displayed an asymmetric relationship: All children who met criteria on the ADHD Rating Scale also did on the CBCL, but only 31% of those who met criteria on the CBCL also did on the ADHD Rating Scale. No child who failed to meet criteria on the CBCL met criteria for the ADHD Rating Scale. Premorbid attention problems approached significance as a moderator of clinically significant elevations on the CBCL Attention Problems Scale (x 22 = 4.64, p < .10) but were not a significant moderator of clinically significant reports on the ADHD Rating Scale (x 22 = 1.10, p > .10). For the CBCL Attention Problems Scale, the test of the interaction involving the severe TBI and OI groups approached significance (p < .06) but that involving the moderate TBI and OI groups was not significant. Among children with few premorbid attention problems (i.e., baseline CBCL T scores <60), clinically significant long-term attention problems occurred in 32% of the severe TBI group compared with 21% of the OI group. In contrast, among children with more premorbid attention problems (i.e., baseline CBCL T scores ‡60), clinically significant long-term attention

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TABLE 3 Hierarchical Logistic Regression Analysis for Clinically Significant Long-Term Attention Problems CBCL ADHD Attention Rating Problems Scale Step 1:Wald statistics Race SCI Premorbid attention problems (CBCL Attention Problems Scale) Likelihood ratio test for step 1 (x2) Step 2:Wald statistics Moderate TBI vs. OI Severe TBI vs. OI Likelihood ratio test for variables added in step 2 (x 2) Step 3:Wald statistics Moderate TBI vs. OI 3 Premorbid attention problems Severe TBI vs. OI 3 premorbid attention problems Likelihood ratio test for variables added in step 3 (x 2) Step 4:Wald statistics Word Fluency Test Consonant Trigrams Test Underlining Test Contingency Naming Test Likelihood ratio test for variables added in step 4 (x 2)

0.40 7.76* 16.59*

0.02 0.06 11.48*

37.32*

14.09*

0.20 4.92* 8.23*

1.00 4.70* 13.16*

0.08 3.64†

0.85 0.39

4.64†

1.10

0.58 1.36 2.02 3.61† 13.47*

0.50 0.97 0.22 0.07 3.59

Note: SCI = Socioeconomic Composite Index; CBCL = Child Behavior Checklist; ADHD = attention-deficit/hyperactivity disorder; TBI = traumatic brain injury, OI = orthopedic injury. *p < .05; †p < .10.

Fig. 1 Linear regression plots show relationship between premorbid Child Behavior Checklist (CBCL) Attention Problems Scale T score and postinjury CBCL Attention Problems Scale T score (a) and Attention-Deficit/Hyperactivity Disorder Rating Scale total score (b). Severe traumatic brain injury (TBI), moderate TBI, and orthopedic injury (OI) groups are plotted separately. The plots show an increase in group differences for postinjury attention problems as a function of higher premorbid ratings.

problems occurred in 82% of the severe TBI group and 42% of the OI group. Group Comparisons on Cognitive Functioning

The groups differed significantly on the four cognitive tests at the long-term follow-up assessment. Group membership explained an additional 6% of the variance

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in the Underlining Test (F 2,127 = 3.91, p < .05) and 3% of the variance in the Contingency Naming Test (F 2,127 = 3.14, p < .05). For both tests, the comparison of the severe TBI and OI groups was significant (t = –2.28 for the Underlining Test, p < .05, and t = –2.55 for the Contingency Naming Test, p < .05), whereas neither contrast of the moderate TBI and OI groups was significant. For the Word Fluency Test and the Consonant Trigrams Test, the overall tests for group differences approached significance (F 2,127 = 2.48, p < .10, and F 2,127 = 2.46, p < .10, respectively). The specific comparisons of the severe TBI and OI groups were significant for both tests (t = –2.04 and t = –1.99, respectively, both p < .05), whereas those involving the moderate TBI

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and OI groups were not. Premorbid behavioral symptoms of attention problems did not moderate long-term cognitive test performance.

Scale IQ was not associated with clinically significant attention problems on either scale, and its inclusion in the model did not affect other model estimates.

Association of Behavioral Symptoms and Cognitive Tests

DISCUSSION

The four cognitive tests were related significantly to long-term attention problems, accounting for an additional 5% of the variance in both the CBCL Attention Problems scale (F 4,120 = 3.65, p < .01) and the ADHD Rating Scale (F 4,120 = 2.34, p < .06) (see Table 2). All four cognitive tests were significantly related to the CBCL Attention Problems Scale based on their partial correlations before entry into the regression; however, because the tests were correlated, only the Contingency Naming Test explained unique variance after all four tests were added (t = –2.42, p < .05). The Word Fluency Test and the Contingency Naming Test were related significantly to the ADHD Rating Scale before entry, but again only the Contingency Naming Test accounted for unique variance when all tests were added (t 1 = –2.92, p < .01). Full Scale IQ did not contribute significant additional variance to either the CBCL or ADHD Rating Scale after the four other cognitive measures were considered nor did its inclusion alter the relationship between the other cognitive measures and long-term attention problems. The regression analysis reflects the assumption that the association between behavioral symptoms and cognitive measures does not vary across groups. To test this assumption, we entered interaction terms constructed by multiplying the dummy variables for group membership by each of the cognitive tests. We tested the change in R 2 associated with the interaction terms as well as the unique contribution of the two interactions specific to each test. None of the interaction terms were significant. Thus, the relationship between cognitive and behavioral aspects of attention held across groups. In the logistic regression analyses (see Table 3), the four cognitive measures were significantly related to clinically significant attention problems on the CBCL but not on the ADHD Rating Scale (x24 = 13.47, p < .01, and x 24 = 3.59, p > .10, respectively). None of the four cognitive tests explained unique variance in the CBCL Attention Problems scale, presumably because they were correlated, although the Contingency Naming Test approached significance (p < .06). Full

As expected, children with severe TBI displayed deficits in both cognitive and behavioral aspects of attention compared with those with OI. Additionally, they were substantially more likely than children with OI to display clinically significant attention problems within the behavioral domain. Approximately 20% of the severe TBI group displayed symptoms consistent with a diagnosis of the combined subtype of ADHD, whereas only 4% of the OI group did so. These findings confirm previous research showing both cognitive deficits in attention and executive functions and increased behavioral symptoms of attention problems and ADHD after childhood TBI (Anderson et al., 1998; Bloom et al., 2001; Catroppa and Anderson, 1999; Catroppa et al., 1999; Dennis et al., 1995, 2001; Ewing-Cobbs et al., 1998; Fenwick and Anderson, 1999; Gerring et al., 1998; Kaufmann et al., 1993; Konrad et al., 2000; Max et al., 1997, 1998, 2004; Schachar et al., 2004; Vriezen and Pigott, 2000; Wassenberg et al., 2004b). The current study extends previous research by showing that premorbid attention problems act as a potent moderator of long-term attention problems after childhood TBI. The greater the premorbid difficulties, the more pronounced the differences in long-term behavioral symptoms were between the TBI and OI groups. This finding presumably reflects an example of reserve capacity, whereby vulnerability to the effects of TBI depends on premorbid functioning (Dennis, 2000; Satz, 1993; Stern, 2002). Interestingly, premorbid attention problems did not moderate group differences on longterm cognitive outcomes. In previous studies with this sample, we have found that behavioral and adaptive outcomes are more likely than cognitive outcomes to be affected by moderators extrinsic to the child, such as family functioning or parental perceived burden (Taylor et al., 2002; Yeates et al., 2002). The current findings suggest that the same may be true for moderators intrinsic to the child, such as premorbid attentional functioning. The dissociation may occur because cognitive functioning and recovery in children with TBI are more directly a reflection of injury severity, whereas behavioral outcomes are influenced jointly by injury severity and

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both child and family factors distinct from the injury itself (Schwartz et al., 2003). Although deficits in cognitive and behavioral aspects of attention are known to occur commonly after childhood TBI, few studies have examined whether the two types of deficits are related. In the current study, cognitive measures of attention and executive functions accounted for significant, albeit modest, variance in ratings of long-term behavioral symptoms of attention problems, irrespective of general intellectual functioning. The results therefore suggest that cognitive aspects of attention and executive functions have a relatively specific link to behavioral symptoms. In this respect, the findings are consistent with recent theories of ADHD that posit core deficits in executive functions as underlying the behavioral symptoms that define the disorder (Barkley, 1997). The findings also are consistent with research showing modest but significant relationships between cognitive and behavioral aspects of attention among children with ADHD (Doyle et al., 2000; Grodzinsky and Barkley, 1999). Notably, the relationship between cognitive and behavioral aspects of attention was consistent across groups, holding true for the TBI and OI groups. To the extent that cognitive measures reflect underlying brain structure or function, this finding may suggest that the underlying neuroanatomical substrates for attention problems or secondary ADHD in childhood TBI are similar to those for primary ADHD (Gerring et al., 2000; Herskovits et al., 1999; Max et al., 1998). Frontal-subcortical and cerebellar brain systems have been implicated in ADHD (Berquin et al., 1998; Casey et al., 1997; Castellanos et al., 1996; Mostofsky et al., 1998), and are also known to be especially likely to be damaged in children with TBI (Levin et al., 1989; Mendelsohn et al., 1992). Thus, phenotypic similarities between attention problems for children with TBI and those with ADHD may be more than skin deep. Limitations

Many children dropped out of the study before the long-term follow-up assessment, with disproportional attrition of children of lower socioeconomic status and those from the OI group. Attrition bias can complicate the interpretation of results from longitudinal studies (Cicchetti and Nelson, 1994; Francis et al., 1994). Attrition bias does not seem likely to have

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yielded spurious findings in this instance, but the findings may not generalize to all children with traumatic injuries or accurately reflect the effects of childhood TBI on attention for the most disadvantaged families. The measures used to assess cognitive aspects of attention were not selected on the basis of a specific theory of attention or executive functions (Cooley and Morris, 1990; Mirsky et al., 1991) and likely do not represent all relevant dimensions within that domain. A notable omission is the absence of a test of inhibitory control. Continuous performance tests have consistently proven to be more strongly related to behavioral symptoms of ADHD than other cognitive measures (Doyle et al., 2000; Grodzinsky and Barkley, 1999). Although a continuous performance test was included in the larger study, technical difficulties often precluded its administration, resulting in substantial missing data, so we elected not to include it in the current analyses. Nevertheless, the measures that we included do require inhibitory control. On the Contingency Naming Test, for instance, children must name the colors or shapes of objects based on complex rules that change over trials; when the rules change, children must suppress the tendency to respond based on previous rules. The significant relationships found between cognitive measures and behavioral ratings suggest that our measures captured dimensions of attention and executive functions that are involved in the behavioral regulation of attention. The measurement of behavioral attention problems was limited to rating scales that were completed only by parents, and no preinjury ratings were available on the ADHD Rating Scale. The study may have been strengthened by the inclusion of a structured psychiatric interview and by the inclusion of ratings by classroom teachers. However, a standard score >60 on the CBCL Attention Problems Scale has demonstrated good sensitivity and specificity for ADHD among children with TBI when the diagnosis is made using a structured psychiatric interview (Wassenberg et al., 2004a). Based on positive and negative predictive values derived from Wassenberg et al. (2004a), 35% of the severe TBI group and 23% of the OI group in the current sample would be expected to meet diagnostic criteria for ADHD at the long-term follow-up. These rates exceed those based on the ADHD Rating Scale (i.e., 20% versus 4%), but the latter estimates required symptoms of both inattention and impulsivity-hyperactivity, consistent with the combined subtype of ADHD, whereas all ADHD subtypes

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A TTENTION PROBL EMS I N TRA UMATIC BRA IN INJUR Y

were included by Wassenberg et al. (2004a). The rates of ‘‘clinically significant attention problems’’ on the ADHD Rating Scale increase to 26% for the severe TBI group and 18% of the OI group when the definition is expanded to include symptoms of either inattention or impulsivity-hyperactivity and are thus very consistent with Wassenberg et al. (2004a). Clinical Implications

The findings indicate that premorbid attention problems are a significant risk factor in children with TBI. Thus, children’s premorbid status should be assessed soon after their injuries to help identify those children who are most likely to require intervention. The results also demonstrate that childhood TBI leads to persistent attention problems both cognitively and behaviorally and that deficits in the two domains are related. Because clinically significant attention problems have been associated with a variety of negative psychosocial sequelae (Barkley et al., 2004; Wilens et al., 2002), the findings suggest that children with severe TBI who display significant attention problems are especially at risk of adaptive failures. The findings underscore the need for effective interventions to manage attention problems arising after childhood TBI. Unfortunately, few studies have examined psychopharmacologic or psychosocial interventions designed to ameliorate attention problems after childhood TBI (Hornyak et al., 1997; Mahalick et al., 1998). Future research in this regard could improve the clinical management of children with TBI. Disclosure: The authors have no financial relationships to disclose.

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