Traumatic Brain Injury in Children and Adolescents: Psychiatric Disorders at Two Years JEFFREY E. MAX, M.B.B.CH ., DONALD A. ROBIN, PH.D ., SCOTf D. LINDGREN , PH.D. , WILBUR L. SMITH, JR., M .D., YUTAKA SATO, M.D. , PHILIP J. MATfHEIS, M.D., JULIE A.G. STIERWALT, M.A., AND
CARLOS S. CASTILLO, M.D.
ABSTRACT ObJective: To extend findings regarding predictive factors of psychiatric outcome from the first to the second year after traumatic brain injury (TBI) in children and adolescents. Method: Subjects were children aged 6 to 14 years at the time they were hospitalized after TBI. The study used a prospective follow-up design . Assessments of preinjury psychiatric, behavioral , adaptive functioning , family functioning and family psychiatric history status were conducted. Severity of injury was assessed by standard clinical scales and neuroimaging was analyzed. The outcome measure was the presence of a psych iatric disorder, not present before the injury ("novel"), during the second year after TBI. Results: Fifty subjects enrolled , and the analyses focused on 42 subjects followed at 24 months. Severity of injury, preinjury family function, and preinjury lifetime psych iatric history predicted the development of a "novel" psychiatric disorder present in the second year. Conclusion: These data suggest that there are children, identifiable through clinical assessment, at increased risk for "novel" psychiatric disorders in the second year after TBI. J. Am. Acad. Child Ado/esc. Psychiatry. 1997,36(9):1278--1285. KeyWords: traumatic brain injury, children, adolescents, psychiatric disorder.
Traumatic brain injury (TBI) in children and adolescents is a major public health problem in the United States, involving the annual hospitalization for acute brain trauma of about 100,000 children under 15 years of age (Kraus et al., 1987). Other than the study that is the focus of this report, there has been only one prospective childhood psychiatric study of TBI in which standardized instruments were used (Brown et al., 198 I). Subjects were studied over a 2X-year follow-up. There was a marked increase Acupud FtbruAry 4. /997. Dr. Max is with tb«Department ofPsychiatry. DN. Smith and Satoart with th~ Department ofRadiology. Dr. Lindgrm is with th~ Department ofPediatrics, and Dr.Robin and MN. Stinwalt art with th~ Department ofSpuch Pathology and Audiology, University of Iowa. Iowa City. Dr. Mattheis is with the University of Montana. Missoula. Dr. Castillo is with the Cedar Centre Psychiatric Group. CedarRapids. IA. This rrstarrh wassupported by a NARSAD Yt1ung Investigator Award to Dr. Max. Theauthor: adtno wkdg~ th« h~/pjUl comments ofRobat Robinson. M.D.; statistical adoic« from St~phan Arndt. Ph.D.; Tracy Shannon. B.A.• and Erika Gaylor, B.S.•for collection ofsome ofth« data: and Paula Swygardfor http with manuscript preparation. Correspondmce to Dr. Max. Department ofPsychiatry. Univmity of Iowa. /876 JPP. IowaCity. IA 52242. 0890-8567/97/3609-1278/$O.300/0iC 1997 by the American Academy of Child and Adolescent Psychiatry.
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in psychiatric disorders after severe TBI compared with controls (62% versus 14%). Variables predicting new psychiatric disorder in children with TBI included, most importantly, increasing severity of injury, but also the children's preinjury behavior, their early postinjury intellectual level, and their psychosocial circumstances. An additional prospective study included psychiatric assessments conducted without standardized psychiatric instruments (Black et al., 1981). The study population consisted of children consecutively admitted for TBI. Most of these children had mild TBI. Approximately 80% of the children showed no posttraumatic behavioral changes . The children with a history of an initial loss of consciousness had a higher frequency of behavioral difficulty at a I-year follow-up. We have previously reported on factors predictive of the onset of a specific psychiatric disorder never before present in the individual ("novel") in the first year after a TBI (Max et al., 1997a,c; Max et al., unpublished). The model tested involved six factors: "Severity of Injury, " "Lifetime Psychiatric Disorder," "Family Psychiatric History," "Family Function," "Socioeconomic Class and Preinjury Intellectual Function," and "Behavior/Adaptive Function." We found that "Fam ily
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Psychiatric History" and "Family Function" remained significantly predictive throughout the first year. "Severity of Injury" was significant in the first 6 months but only tended to significance in the second 6 months. However, when we used a categorical measure of severe TBI rather than a continuous measure based on the lowest postresuscitation Glasgow Coma Scale (GCS) score (Teasdale and Jennett, 1974), severity of TBI remained significant. "Lifetime Psychiatric Disorder" was significant in the first 3 months but not thereafter. This effect was accounted for mostly by children with mild to moderate TBI whose preinjury psychiatric disorder history placed them at risk transiently for new psychiatric problems. Lower "Socioeconomic Class and Preinjury Intellectual Function" was predictive of a "novel" psychiatric disorder in the intervals, injury to 3 months and 6 months to 1 year after TBI. Our aim in this study was to assess severity of injury, lifetime psychiatric disorder, behavior/adaptive function, family psychiatric history, family function, socioeconomic class, and preinjury intellectual function as predictors of psychiatric outcome in the second year after TBI in children and adolescents. METHOD This prospective follow-up study, approved by the university institutional review board, included children and adolescents who suffered a TBl. Comprehensive psychiatric, family, and adaptive functioning assessments were conducted at "baseline" (as soon as possible after the injury) to assess preinjury functioning, and psychiatric assessments were repeated 24 months after the TBl. Inclusion criteria were as follows: consecutively admitted TBI patients; aged 6 years to 14 years at time of injury; patients admitted to a large tertiary care center and three regional hospitals; computed tomography (CT) scan on admission as a threshold criterion ofTBI severity; English as the primary language spoken at home. Exclusion criteria were as follows: patients who had injuries so serious that they had not emerged from posttraumatic amnesia (PTA) 3 months after the injury; penetrating TBI; documented history of child abuse; history of previous TBI involving at least one hospital admission longer than 1 night; history of mental retardation; other acquired or congenital CNS disorder; preexisting acute or chronic serious illness.
Neurological Assessments The lowest postresuscitation score on the GCS, which is the standard measure of severity of brain injury in the acute stage of injury, was recorded from clinical nores. The scale measures motor, eye-opening, and verbal responsiveness. Scores range from 3 (unresponsive) to 15 (normal). The initial CT scans were analyzed independently by WL.S. (a pediatric radiologist) and by Y.S. (a pediatric neuroradiologist), and then a consensus was reached by discussion in the case of discrepan-
cies. For the purposes of this report, the scans were classified as either showing an intracranial traumatic lesion or not. The scans were additionally classified according to the Traumatic Coma Data Bank categorization (Marshall et al., 1991), which incorporates the degree of brain edema and focal lesions into a single rating (1 to 6) of increasing severity. Interrater agreement for the presence or absence of a lesion was 100%, and regarding the Traumatic Coma Data Bank categorization, 92%. Our first predictive statistical model, "Severity of Injury," consists of three items: (1) lowest postresuscitation GCS score, (2) Traumatic Coma Data Bank categorization, and (3) normal/abnormal initial CTscan. For descriptive purposes we have classified categories of severity of TBI as follows: severe injury was defined by a lowest postresuscitation GCS score :58, moderate injury by a lowest postresuscitarion GCS score of 9 to 12 or a score of 13 to 15 with an intracranial lesion or with a depressed skull fracture seen on the initial CT scan. Mild injury is defined by a lowest postresuscitation GCS score of 13 to 15, irrespective of any associated linear skull fracture. Another measure reflecting, but not defining, the severity ofTBI included the duration of coma. This was defined as the time from injury to the attainment of a score of 6 (ability to follow commands) on the Motor subscale of the GCS. PTA was estimated by using a combination of the Children's Orientation and Amnesia Test (Ewing-Cobbs er al., 1990), nursing notes, and parents' report.
Psychiatric Measures The Schedule for Affective Disorders and Schizophrenia for School-Age Children-Epidemiologic version (K-SADS-E) (Orvaschel er al., 1982) supplemented by a posttraumatic stress disorder (PTSD) module was used at baseline. For the follow-up assessments, the Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present Episode version (K-SADS-P) (Chambers et al., 1985) was supplemented by the K-SADS-E sections on attention-deficit hyperactivity disorder (ADHD), oppositional defiant disorder (ODD), and alcohol and substance abuse, as well as the PTSD module. DSM-III-R criteria were used. The interview was administered, in all cases, by the first author .E.M.), who is a board-certified child and adolescent psychiatrist. In addition, the Neuropsychiatric Rating Schedule (NPRS) (Max, 1992), an interview with the same format as the K-SADS, designed specifically to identify symptoms and subtypes of organic personality syndrome, was conducted at all evaluations by ].E.M. Twenty-two symptoms are rated, including summary ratings defining the five subtypes of the syndrome. Preliminary data (n = 103), assessing convergent validity with the parent-completed Children's Affective Instability Scale (Gerson er al., 1993), which was designed to assess affective instability, are available for the NPRS summary rating for affective instability. The scale means (::!::SD) were significantly different between those with NPRS clinician-rated "no affective instability" versus "affective instability" (3.89 ::!:: 5.22 versus 15.35 ::!:: 9.79; t = -5.06, df= 21.67,p < .000). Preliminary interrater reliability data yielded a 1C = .91 for the clinician's ratings of current symptoms. This was based on ratings of ].E.M. on a random selection of 10 subjects with severe TBI from a different study compared with ratings of another author, C.S.c., who watched the same interview on videotape. Almost all interviews in the 2-year prospective study were videotaped, and every 20th tape was rated by a coauthor, C.S.c., for the purpose of interrater reliability measures. C.S.c., a child psychiatrist, was blind to all other data including severity of injury. Thus
]. AM. ACAD. CHILD ADOLESC. PSYCHIATRY. 36:9. SEPTEMBER 1997
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far, 10 interviews have been assessed for inrerrarer reliability. Agreement on diagnostic classification was achieved in 8 (80%) of 10 cases. The psychiatric assessment at baseline defined our second predictive model, "Lifetime Psychiatric Disorder. " This assessment, rogerher with the 24-month follow-up which evaluated status of the 12- ro 24-month interval, defined a "novel" psychiatric disorder. The designation of a "novel" psychiatric disorder was applied in one of rwo conditions. First, this could occur in a subject with no lifetime psychiatric disorders as of the baseline assessment who then manifests a psychiatric disorder. Second, this could occur in the case of a subject with a lifetime psychiatric disorder who manifests a psychiatric disorder which was not present before the TBI, e.g.. a subject with a lifetime hisrory of major depressive disorder who develops ODD after the injury would receive the classification, but would not if only a new episode of major depression or a switch to mania or hypomania occurred. The term "novel" was used to avoid confusion when comparing our findings ro those of Brown er al. (1981), who focused on "new" psychiatric disorders corresponding only with the first condition in our definition of "novel" psychiatric disorders . Since preinjury psychiatr ic disorder may be common in children who suffer TBI , we were interested in studying, among other things, the influence ofTBI on children with existing psychiatric disorders. Two mod ifications were made to the DSM-II/-R diagnostic criteria. First, we abandoned the requirement of diagnosing an organic mental disorder if a subject met all criteria for a functional psychiatric disorder but an organ ic etiology was suspected . Second, we waived the upper age limit for the onset of ADHD.
order and has had inpatient psychiatric treatment or has been incarcerated . The fourth predictive model , "Family Psychiatric History," consisted of rwo components: the rating for first-degree relatives only and the rating for first- and second-degree relatives combined.
Family Assessment Measures Family assessment measures were collected by both interview and questionnaire methods. The McMaster Structured Interview of Family Functioning is a research interview of the family and is based on the McMaster model of family function ing (Miller er al., 1994). The interviewer uses the Clinical Rating Scale (Miller et al., 1994) to rate each of seven domains, including global family functioning, I to 7 on a Likert scale in which lower scores indicate poorer function. The interviews were initially conducted by J.E.M. and subsequently by rwo trained research assistants. J.E.M. achieved an inrerrarer reliability Pearson correlation coefficient of .83 for the global functioning rating with the team of the developers of the interview. Interrater reliability Pearson correlation coefficients for the global assessment domain of .87 and .96 , respectively, were achieved between J.E.M. and the rwo trained research assistants. The Family Assessment Device (Miller et al., 1994) questionnaire was completed by family members at least 12 years of age. It measures the same domains of family functioning including a global rating. We calculated a mean global functioning dimension score for each family. Higher scores on this instrument indicate more dysfunction. The fifth predictive model, "Family Function," consisted of rwo ratings: the global family functioning score from the interview and from the questionnaire.
Adaptive Functioning and Behavior Measures Adaptive functioning assessment was accomplished with the Vineland Adaptive Behavior Scale interview (Sparrow er al., 1984). This involved a semistructured interview conducted by a trained research assistant with the primary caretaker. The Pediatric Behavior Scale (PBS) (Lindgren and Koeppl, 1987) is a behavioral rating scale designed specifically for use with neurological and other medical disorders . It has been demonstrated to have adequate reliability and validity. A parent and school teacher completed the relevant versions of this instrument. Raw scores were added to yield a total behavior score. The Vineland Adaptive Behavior Composite and the total score on the PBS constituted our third predictive model , "Behavior/ Adaptive Function."
Socioeconomic Class and Intelligence Measures Socioeconomic class assessment was accomplished through the Four Factor Index of Social Status (Hollingshead, 1975). Other measures were from the baseline teacher's version of the PBS, which has items rating the child 's preinjury intellectual ability and academic achievement on 5-point scales from "far below average" to "far above average. " The preinjury national percentile rank for vocabulary on the Iowa Tests of Basic Skills was included here because it is highly correlated with verbal IQ (Hieronymus and Hoover, 1986). The sixth predictive model , "Socioeconomic Class and Preinjury Intellectual Function," consisted of four items: Four Factor Index rating ; PBS teacher's rating of preinjury intelligence: PBS teacher's rating of preinjury school achievement : and the Iowa Tests of Basic Skills national percentile rank for vocabulary.
Family Psychiatric History The Family History Research Diagnostic Cr iteria (Andreasen er al., 1977) interview was conducted in most cases by J.E.M . and in other cases by a trained bachelor's-level research assistant with 2 years' experience as a mental health caseworker. Criteria were modified ro conform with DSM-I/I-R criteria. Based on videotaped interviews conducted by J.E.M ., adequate interrarer reliability was achieved (K values for the diagnoses screened ranged from .79 to 1.00). At least one parent acted as the informant. Family ratings were then summarized for first-degree relatives only and for a combined grouping of first- and second-degree relatives as follows: 0 = no family psychiatric disorder; I = at least one member of the family met criteria for a psychiatric disorder but no treatment was received; 2 = a family member mel criteria for a psychiatric disorder and has received outpatient treatment or been arrested for antisocial behavior; 3 = a family member met criteria for a psychiatric dis-
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Data Analysis To assess the representativeness of the sample with respect to those eligible patients who did nor participate, we conducted t tests for continuous variables and -f analyses for categor ical variables. Logistic regression analyses were conducted on each of the six predictive models described above to account for the development of "novel" psychiatric disorders . If the model was significant, we examined the significance of each of the variables with in that model. Significant variables (p < .05) and those tend ing to significance (p < .1) from each significant model were selected for post hoc analysis using a forward stepwise logistic regression. SPSS (1995) was used for statistical analyses. Other variables of interest in predicting "novel" psychiatric disorders, includ ing age at injury, litigation status, gender, and seizure activity/anticonvulsant medication, were tested, post hoc, by logistic regression analyses.
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PSYCHOPATHO LOGY AFTER CHILDHOOD TBI
RESULTS
During the course of the recruitment period, 87 TBI patients met criteria for entry into the study. Of these, the parents of 50 patients, after a complete description of the study, provided written informed consent to participate in the study and completed at least the psychiatric assessment component of the "baseline" assessment. Assent was obtained from the children when they reached a point at which they were competent to give it. The most common reason for nonparticipation was the parents of mild TBI children feeling confident that their child was back to baseline and that the scope of the study was therefore unwarranted. The next most common reason was the child's refusal on similar grounds. Coma duration in subjects was as follows: no coma in 22, less than 15 minutes in 10, 1 to 24 hours in 6, 1 to 2 days in 2, 2 to 7 days in 6, and more than 7 days in 4. Subjects' PTA durations were as follows: no PTA in 6, less than 15 minutes in 1, 15 to 59 minutes in 8, 1 to 24 hours in 18, 1 to 2 days in 3, 2 to 7 days in 5, and more than 7 days in 9. One subject remained in a vegetative state beyond the 3-month follow-up and has therefore been dropped from subsequent analyses. By the 24-month follow-up, all other subjects were ambulatory, and gross neuromotor dysfunction was never worse than mild. Causes of injury were as follows: motor vehicle accidents, 10 (20%); bicycle-car accidents, 6 (12%); falls from bicycles, 9 (18%); other falls, 10 (20%) ; sports and recreation, 7 (14%); pedestrianmotor vehicle accidents, 2 (4%); motorcycle/all-terrain vehicle accidents, 2 (4%) ; and other, 4 (8%). At the 24 month follow-up, 44 (90%) of 49 subjects returned for reassessment. Two of the 44 children were siblings and therefore 1 of the siblings was dropped from most analyses because certain variables could not be considered independent for the sibling pair. Another subject with mild TBI who suffered an accidental gunshot (penetrating TBI) (Max et al., 1997b) during the 1- to 2-year follow-up interval was excluded, too. The five subjects who did not return consisted of four children (aged 11 to 14 at injury) with mild TBI and a 9-year-old with severeTBI. All were reportedly doing well and were not interested in participating; however, two were reluctant to be reminded of related traumatic losses. The participants had the following demographic characteristics: mean age at injury (SD) 10.00 (2.42) years; 61.9% male; 98% white; and mean social class (SO) 2.76 (1.03). Categorical classification of severity
was as follows: 20/42 (47.6%) mild TBI, 9/42 (21.4%) moderate TBI, and 13/42 (31.0%) severeTBI. Current and lifetime preinjury psychiatric disorders were evident in 15/42 (35.7%) and 22/42 (52.4%) participants, respectively. Family psychiatric history in first-degree relatives was 9/41 (22.0%), 8/41 09.5%), 13/41 (31.7%), and 11/41 (26.8%), respectively, where there was no family psychiatric history, a relative met diagnostic criteria for a disorder but had no treatment, a relative had outpatient treatment or was arrested, and a relative had inpatient treatment or was incarcerated. The mean (SO) Family Assessment Device score was 1.87 (0.30) and the mean (SO) Clinical Rating Scale score was 3.98 0.52). Fifty-one percent to 52% percent of families were in the clinical range defined by the respective measures compared with 54% with high "psychosocial adversity" in a previous study (Brown et al., 1981). The mean (SO) Vineland Adaptive Behavior Composite was 95.23 (13.55). The participating children were not significantly different from those who declined enrollment with respect to age, sex, race, socialclass, history of behavior/psychiatric disorder, or treatment, but they were significantly different regarding the distribution of mild, moderate, and severe TBI (X 2 = 8.808 , df= 2, P < .02). This was due to greater participation among severely injured subjects. The presence of a "novel" psychiatric disorder in the second year after TBI occurred in 15 of 42 subjects. Of these 15 subjects, "novel" disorders in 11 had persisted from the previous assessment 12 months after TBI. Three of these 11 subjects developed an additional "novel" disorder in this interval. Another four subjects developed their disorder during this 12-month interval. "Novel" disorders were varied and consisted of ODD in eight children (two resolved and one progressed to conduct disorder but relented to ODD again), ADHO in six children (one resolved), organic personality syndrome in four children (comorbid with "novel" AOHO in all cases), simple phobia in two children, separation anxiety disorder in two children (one resolved), mania in one child, hypomania in one child, adjustment disorder with depressed mood in one child (resolved), and marijuana dependence in one subject (resolved). The determination of the classificationof "novel" psychiatric disorder did not depend on the diagnosis of organic personality syndrome exclusively in any case. The six models we wished to test to account for the development of a "novel" psychiatric disorder in the
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second year after injury were entered into logistic regression analyses. Three of the models , "Severity of Injury," "Family Function, " and "Lifetime Psychiatric Disorder," were significant. The results are presented in Table 1. A post hoc forward stepwise logistic regression analysis to determine which of the variables within the significant models significantly contributed to the development of a "novel" psychiatric disorder was conducted. This involved entering the following three variables, in which significance levels were p < .1: global family functioning score derived from the family assessment interview (Wald X2 = 6.220, df= 1, P = .013); lowest postresuscitation GCS score (Wald X2 = 6.527, df= 1, P = .011); and Lifetime Psychiatric Disorder rating (Wald X2 = 3.888, df= 1, P = .049). The results of this analysis revealed that the first variable entered in the forward stepwise logistic regression was the global family function rating (- 2 log-likelihood X2 = 12.244 , df= l,p = .0005) which correctly predicted 76.2% of "novel" disorders. The second variable entered was the lowest postresuscitation GCS score (- 2 log-likelihood X2 = 17.072, df= 2, P = .0002) , which correctly predicted 78.6% of "novel" disorders. The third variable entered was the lifetime psychiatric disorder rating (- 2 log-likelihood X2 = 21.493, df= 3, P = .0001), which correctly predicted 81.0% of "novel" disorders. DISCUSSION
This study was designed to prospectively assess the risk factors related to the presence of a "novel" psychiatric disorder in the second year after TBI in children and adolescents aged 6 to 14 years. The major finding of this study is that the three (of six) models that significantly predicted "novel" psychiatric disorder were "Family Function," "Severity of Injury," and "Lifetime Psychiatric Disorder." Post hoc forward stepwise logistic regression analyses revealed that significant predictive variables were the global family functioning score derived from the family assessment interview, the lowest postresuscitation GCS score, and lifetime preinjury psychiatric disorder. At this point, it is worth acknowledging several important limitations in the study. The representativeness of the sample of children hospitalized for TBI is an issue. We were able to follow up at 24 months with 90% of children who completed the baseline assessment. However, only 57% of eligible children enrolled
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TABLE 1 Prediction Models of "Novel" Psychiatric Disorder in the Second Year Alter Traumatic Brain Injury Prediction Models I. 2. 3. 4. 5. 6.
Severity of Injury Lifetime Psychiatric Disorder Behavior/Adaptive Fun ction Family Psychiatric History Family Function Socioeconom ic Class and Prein jury Intellectual function
X2
df
Significance
11.552 4.233
3
.009 .040
1 2 2 2
1.478
4.257 9.259
4
4.293
Note: "I! refers to the - 2 log-likelihood X
2
.478
.119 .010
.368
•
and completed baseline assessment. The characteristics of the children who did participate in the study com pared with those who did not were similar except for the overrepresentarion of severe TBI cases in the enrolled group. Therefore, we may be overestimating "novel" psychiatric disorder. A second limitation in the study is the validity of baseline psychiatric findings. Any postinjury assessment of preinjury function is subject to inaccuracies. To minimize these distortions in recollection of the child's preinjury behavior caused by knowledge of the child's current behavior, we attempted to conduct these assessments as early as possible after the injury. The baseline assessment involving the parent occurred 14.8 ± 13.1 (mean ± SO) days after the injury. Third, a control group was not essential in this study because the question was not "how do TBI children differ from controls?" bur was rather, "who among the TBI group develops a novel psychiatric disorder?" A non-CNS trauma group would be informative in the assessment of response to trauma and stress and in the documentation of naturally emerging comorbid conditions in children with preinjury psychiatric disorders. A fourth limitation is the small sample size of our study. Replication of these findings with a larger sample size would be necessary before these findings can be generally accepted. Nevertheless, the findings are remarkably similar to those of another prospective psychiatric study ofTBI (Brown et al., 1981). A fifth limitation is that the psychiatric diagnoses were based on the psychiatric interviews alone. Data from other sources may have influenced diagnostic assessment, particularly with respect to externalizing disorders. A sixth limitation is that the psychiatric interviewer was not blind to severity of injury and was blind to only a portion of the family function and family psychiatric history data. The good
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interrater reliability for the subjects' psychiatric diagnoses that was achieved with a second rater who was blind to all other data suggests that the lack of blindness did not cause a significant problem. Figure 1 illustrates the significant predictive models for the development of a "novel" psychiatric disorder in this cohort during this 12- to 24-month interval as well as for three other intervals covering the first year of follow-up (Max et al., 1997a,c; Max et al., unpublished). Lower family functioning was a significant predictor throughout the 2 years. This finding is consistent with that of Brown et al. (1981) with respect to persistent new psychiatric disorders. They measured a construct called "psychosocial adversity." This measure overlaps with our more differentiated evaluations of family function , family psychiatric history, and social class. Our model of "Severity of Injury" was significant in the first 6 months and from the 12th to the 24th month after injury. It tended to significance in its prediction of "novel" psychiatric disorder in the second 6 months after TBI. The studies of Black et al. (1981) and Brown et al. (1981) underscored the importance of severity of injury as a predictor of psychiatric outcome, 1 and 2 years, respectively, after TBI. Lifetime psychiatric disorder significantly predicted "novel" psychiatric disorder in the first 3 months and in the second year. This finding is consistent with that of Brown et al. (1981). Children with a preinjury lifetime psychiatric disorder may be especially vulnerable to the immediate disruptiveness of TBI in the first 3 months, but then they may be able to overcome the disturbance if the TBI was not "severe." Later in the follow-up, the resurgence of lifetime psychiatric disorder as a significant predictor of "novel" psychiatric disorder may reflect emerging comorbid conditions consistent with MoDthl Aftm Inlurv Sevllrilv af'InIurv
I 0-3 I
F FamilYFuDaion SocioecoDOmic C1aIIIIntelIilZeDCe
I
6-12
I
12-24
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BMavlftr/AdaDt:w FwIctioIl
3~
the natural history of child psychiatry patients (Last al., 1996). Table 2 outlines the relationship of "novel" psychiatric disorder, severity of injury, and preinjury lifetime psychiatric status. Most interesting is that there was no child with a mild/moderate TBI who was free of a preinjury lifetime psychiatric disorder who went on to manifest a "novel" psychiatric disorder in the second year after injury. Six (38%) of the 16 children with comparable severity of injury but with a preinjury lifetime psychiatric disorder went on to exhibit a "novel" psychiatric disorder in the second year. A closer look at these six children reveals that the "novel" disorders in three of the six children had already resolved by the 2year assessment and that five of the six children had preinjury traits for the disorders they would develop (three with 000, one with ADHO, and one with separation anxiety disorder). The sixth subject, an adolescent with a preinjury overanxious disorder, developed and recovered from an adjustment disorder with depressed mood after a losing conflict with her mother regarding a request for an inappropriate degree of autonomy. Only one subject with mild TBI and one subject with moderate TBI , both with preinjury traits, had their "novel" disorders persisting from the first 6 months after injury. There is considerable controversy about the risk of behavioral or psychiatric problems after mild TBI in children. However, a controlled prospective study of mild TBI (Asarnow et al., 1995) and the authors' review of 30 studies involving mild TBI, as well as the data from our study, suggest that the evidence in support of the pathogenesis of behavior problems as a direct effect of a brain injury resulting from the accident, or as a long-term secondary effect of the accident, is weak for
et
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Fig. 1 Prediction models of "novel" psych iatric disorder in the 2 years after traumatic brain injury. Shading represents interval s in wh ich each part icular model was significant in predicting "novel" psychiatr ic disorder.
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TABLE 2 Prevalence of "Novel" Psychiatric Disorders in the Two YearsAfter TBI Severity (n) Preinjury Status Severe (n = 14) No lifetime disorder (n = 7) Lifetime disorder (n = 7) Mild + moderate (n = 35) No lifetime disorder (n = 18) Lifetime disorder (n = 17)
6 Months
12 Months
24 Months
2-Year Cumulative
5/6 4/5
5/6 2/6
4/ 7 5/6
4/7
5/7
5/6
5/6
1115 7/12
1115 2/15
1115 6116
0/14 6/16
10117
3 Months
2/16
Note: Arranged by injury severity, preinjury psychiatric status, and timing of assessment. Table includes a mild TBI sibling excluded in main analyses, and only the first year (pre-gunshot) data of a mild TBI subject who suffered a penetrating TBI. TBI = traumatic brain injury,
the group of mild cases as a whole. The more likely pathogenesis is that the behavior problem is an immediate secondary effect of the accident (e.g., an emotional response to the accident, such as PTSO) or the behavior problems are caused by factors other than head injury. These data do not rule out the possibility that even a mild injury can result in direct behavioral changes in individuals who do not have obvious preinjury predisposing factors, but this occurrence appears to be relatively infrequent. Another possible predictor of psychopathology, age at injury, was not significant in the second or the first year of follow-up. Nor was age at injury significant in other psychiatric studies of childhood TBI, which have generally excluded the 0- to 5-year age range for lack of a standardized diagnostic interview instrument. However, neurobehavioral function in children aged 0 to 5 years is more sensitive to disruption than in older children (Levin et al., 1992). Also frequently discussed is the effect of litigation status on psychopathology, which was not significant in the second year or the first year of follow-up in this study. Litigation is thought to be relevant to psychopathology because of the associated stresses as well as potential monetary incentives for the maintenance of symptoms. Other commonly discussed risk factors for psychopathology after TBI include the effect of gender and seizure activity/anticonvulsant medications. Neither of these were statistically significant in predicting "novel" psychiatric disorder in the second year or in the first year of follow-up. An important component of morbidity after TBI in children may involve not only "novel" psychiatric dis-
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orders but the recurrence and/or exacerbation of preinjury disorders. Our data indicate that four subjects experienced recurrences of mood disorders or adjustment disorders in the first 2 years of follow-up. More strikingly, however, was the tendency for disorders as diverse as anxiety disorders, 000, conduct disorder, and undifferentiated attention deficit disorder to resolve in the first months after injury. None of four subjects with preinjury ADHO (with mild/moderate TBI) experienced clear exacerbation of the disorder. Clinical Implications
We have shown that preinjury family dysfunction is related to the onset of "novel" psychiatric disorders throughout the first 2 years after childhood TBI. The importance of family function is further emphasized by findings that child outcome is significantly influenced by changes in the postinjury environment induced by the injury (Taylor et al., 1995). Furthermore, psychosocial variables, including family functioning, are significantly associated with child psychiatric outcome even after severe TBI (Brown et al., 1981). Therefore, early identification and treatment of children with family dysfunction and more serious TBI may be important from clinical and public health perspectives. Another clinical implication from this and other studies (Asarnow et al., 1995) is that the risk of mild TBI contributing to persistent new psychiatric morbidity is probably small in the absence of family dysfunction and lifetime preinjury psychiatric disorder, and very small in the absence of traits of other disorders in children with a lifetime preinjury psychiatric disorder. Reassurance about psychiatric prognosis for these children may be helpful.
AM . ACAD. CHILD ADOLE SC . PSYCHIATRY, 36:9, SEPTEMBER 1997
PSYCHOPATHOLOGY AFTER CHILDHOOD TBI
REFERENCES Andreasen NC, Endicott J. Spitzer RL. Winokur G (1977), The family history method using Research Diagnostic Criteria: reliability and validity. Arch Gen Psychiatry 34 :1229-1235 Asarnow RF. Satz P, Light R. Zaucha K. Lewis R. McCleary C (1995) . The UCLA study of mild closed head injury in children and adolescents. In: Traumatic Head Injury in Children, Broman SH. Michel ME. eds, New York: Oxford University Press. pp 117-146 Black P, Blumer D. Wellner AM, Shepard RH. Walker AE (1981). Head trauma in children: neurological. behavioral. and intellectual sequelae . In : Brain DysfUnction in Children: Etiology, Diagnosis, and Management, Black P, ed . New York: Raven . pp 171-180 Brown G, Chadwick 0, Shaffer D, Rutter M, Traub M (1981), A prospective study of children with head injuries. III: psychiattic sequelae. Psychol Med 11:63-78 Chambers W), Puig-Antich J. Hirsch M er aI. (1985), The assessment of affective disorders in children and adolescents by semistructured interview: test-retest reliability of the Schedule for Affective Disorders and Schizophrenia for School-Age Children. Present Episode Version. Arch
Gm Psychiatry 42:696-702 Ewing-Cobbs L, Levin HS . Flercher JM. Miner ME. Eisenberg HM (1990). The Children's Orientation and Amnesia Test: relationship to severity of acute head injury and to recovery of memory. N~rosurg~ 27:683-691 G erson AC , Gerring J. Freund L. Joshi P, Capozzoli J, Denckla M (1993) . Development of a children's affective instability scale . In: Scientifir
Proceedings ofth« Annual Muting ofth« AmericanAcadnny ofChild and Adolescenr Psychiatry Hieronymus AN . Hoover HD (1986) . ManualfOrSchool Administrators Iowa "Uses ofBasic Skills, Forms G/H. Chicago: Riverside Publishing Company Hollingshead AB (1975). FourFactor IndexofSocialStatus. New Haven. CT: Yale University Department of Sociology Kraus JF. Fife D, Conroy C (1987), Pediatric brain injuries: the nature. clinical course , and early outcomes in a defined United States population.
Pediatrics 79:501-507
Levin HS . Aldrich EF, Saydjari C et al. (1992) . Severe head injury in children : experience of the traumatic coma data bank. Neurosurgery 31:435-444 Lindgren SD, Koeppl GK (1987), Assessing child behavior problems in a medical setting: development of the Pediatric Behavior Scale. Adv Bebao
Assm Child Fam 3:57-90 Marshall LD. Marshall SB, Klauber MRet aI. (1991). A new classification of head injury based on computerized tomography. J Neurosurg 75 : 514-520 Max JE (1992), Neuropsychiatric RatingSch~duk. Iowa City: University of Iowa Max JE, Lindren SD, Robin DA et aI. (l997a), Traumatic brain injury in children and adolescents: psychiatric disorders in the second three months. J Nero Men: Dis 185:394-401 Max JE, Lindgren SD, Sm ith WL et al. (l997b), Surprising neurobehavioral functioning and brief major depression following penetrating brain injury in an adolescent. Neurocase 3: 127-136 Max JE, Smith WL, Sato Y et aI. (l997c). Traumatic brain injury in children and adolescents: psychiatric disorders in the first three months. J Am
Acad Child Adolesc Prychiatry 36:94-102 Miller IW, Kabacoff RI. Epstein NB er aI. (1994), The development of a clinical rating scale for the McMaster model of family functioning. Fam
Process 33:53-69 Orvaschel H. Puig-Antich J, Chamber W. Tabrizi MA. Johnson R (1982), Retrospective assessment of prepubertal major depression with the Kiddie-SADS-E. J Acad Child Prychiatry 21 :392-397 Sparrow SS. Balla D. Cicchetti D (1984), Th~ VinelandAdaptio« Behavior Scale«. Circle Pines. MN: American Guidance Services SPSS (1995), SPSS for Windows: Profmional Statistics. Release 6 .1.2 . Chicago: SPSS Inc Taylor HG, Drotar D , Wade S. Yeates K. Standn T, Klein S (1995), Recovery from traumatic brain injury in children: the importance of the family. In: Traumatic Head Injury in Children, Broman SH. Michel ME, eds. New York: Oxford University Press. pp 188-216 Teasdale G. Jennett B (1974) . Assessment of coma and impaired consciousness: a practical scale. Lancet2:81-84
Last CG, Perrin S. Hersen M, Kazdin AE (1996) , A prospective study of childhood anxiety disorders. J Am Acad Child Adolesc Psychiatry 35: 1502-1510
J. AM.
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