Disruptive Behavior in Children With Tourette's Syndrome: Association With ADHD Comorbidity, Tic Severity, and Functional Impairment

Disruptive Behavior in Children With Tourette’s Syndrome: Association With ADHD Comorbidity, Tic Severity, and Functional Impairment DENIS G. SUKHODOLSKY, PH.D., LAWRENCE SCAHILL, M.S.N., PH.D., HEPING ZHANG, PH.D., BRADLEY S. PETERSON, M.D., ROBERT A. KING, M.D., PAUL J. LOMBROSO, M.D., LILY KATSOVICH, M.S., DIANE FINDLEY, PH.D., AND JAMES F. LECKMAN, M.D.

ABSTRACT Objective: To examine the association of disruptive behavior with social, adaptive, and family functioning in Tourette’s syndrome (TS) with and without comorbid attention-deficit/hyperactivity disorder (ADHD). Method: The sample included 207 children (144 boys and 63 girls) between the ages of 7 and 18 years. Forty-two children received a diagnosis of TSonly, 52 received a diagnosis of ADHD-only, 52 children had TS+ADHD, and there were 61 unaffected control children. Best-estimate DSM-IV diagnoses were assigned on the basis of structured interviews and clinical ratings. Dependent measures included parent and teacher ratings of disruptive behavior, parent ratings of social and family functioning, and the Vineland Adaptive Behavior Scales. Results: Children with TS-only did not differ from unaffected controls on the parent ratings of aggression and delinquent behavior or on the teacher ratings of conduct problems. By contrast, children with TS+ADHD were rated significantly above unaffected controls and similar to children with ADHD-only on these indices of disruptive behavior. Hierarchical regression analyses revealed that aggression and delinquency scores added unique contributions to impairment in social and family functioning, controlling for age, gender, and diagnostic status. Conclusions: Comorbid ADHD is highly associated with disruptive behavior and functional impairment in children with TS. When disruptive behavior problems are present, there is an additional burden on children’s social and family functioning. J. Am. Acad. Child Adolesc. Psychiatry, 2003, 42(1):98–105. Key Words: Tourette’s syndrome, attention-deficit/hyperactivity disorder, disruptive behavior, aggression, functional impairment.

Tourette’s syndrome (TS) is a developmental, neuropsychiatric disorder characterized by motor and phonic tics that vary in their number, anatomic location, frequency, intensity, and complexity over time. Although the etiology is unknown, available evidence suggests that dysregAccepted July 30, 2002. From the Child Study Center, Yale University School of Medicine, New Haven, CT. Dr. Scahill has a joint appointment with Yale School of Nursing. Dr. Peterson is now with the Department of Psychiatry, New York State Psychiatric Institute and Columbia University. This work was supported in part by grants MH49351 (Dr. Leckman), NR07637 (Dr. Scahill), MH61940 (Dr. Leckman), MH01232 (Dr. Peterson), MH59239 (Dr. Peterson), the Children’s Clinical Research Center at Yale (RR06022), the Mental Health Research Center at Yale (MH30929), and a grant from the Tourette Syndrome Association (Dr. Sukhodolsky). Reprint requests to Dr. Scahill, Yale University School of Medicine, Child Study Center, 230 South Frontage Road, New Haven, CT 06520-7900; e-mail: [email protected]. 0890-8567/03/4201–0098䉷2002 by the American Academy of Child and Adolescent Psychiatry. DOI: 10.1097/01.CHI.0000024904.60748.3A

98

ulation of cortical-subcortical circuits is responsible for the symptoms of TS (Peterson et al., 2001b, in press). According to recent community-based studies, the prevalence of TS in school-age children varies in the range of 1 to 8 per 1,000 (Costello et al., 1996; Hornsey et al., 2001). Fifty percent to 90 percent of clinically referred children and adolescents with TS also have attentiondeficit/hyperactivity disorder (ADHD), oppositional defiant disorder, or conduct disorder (Coffey and Park, 1997; King and Scahill, 2001; Spencer et al., 2001). A high frequency of disruptive behaviors such as aggression, anger outbursts, and noncompliance has been reported not only in clinical samples of children with TS (Budman et al., 2000; Rosenberg et al., 1995; Stokes et al., 1991), but also in community surveys (Stefl, 1984) and community samples (Kadesjo and Gillberg, 2000; Peterson et al., 2001a). The relationship between tic severity and behavior problems is not clear. Several clinical studies have reported significant association of tic severity and behavioral dis-

J . A M . A C A D . C H I L D A D O L E S C . P S YC H I AT RY, 4 2 : 1 , J A N U A RY 2 0 0 3

DISRUPTIVE BEHAVIOR IN TS

turbance (Comings and Comings, 1987; De Groot et al., 1995; Robertson et al., 1988; Rosenberg et al., 1984; Wilson et al., 1982), but other studies have failed to find this relationship (Edell-Fisher and Motta, 1990; Erenberg et al., 1986; Stokes et al., 1991). The findings to date are inconsistent, perhaps because of age effects, insufficient control of medication status, imprecision in measurement of tic severity, and failure to characterize comorbid conditions such as ADHD. ADHD, which is a common child psychiatric disorder, often co-occurs with oppositional defiant and conduct disorders (Pliszka et al., 1999; Scahill et al., 1999) and is frequently associated with aggressive behavior (Hinshaw, 1987). Two controlled studies involving patients from tic disorder clinics (Carter et al., 2000; Stephens and Sandor, 1999) showed that children with TS-only did not differ from unaffected controls, while the TS+ADHD group scored significantly higher than controls on measures of aggression and delinquent behavior. Another controlled study involving children recruited through a psychopharmacology clinic (Spencer at al., 1998) showed that rates of oppositional defiant and conduct disorders were indistinguishable in children with ADHD-only and those with ADHD+TS. Children with TS+ADHD also appear to be more functionally impaired (Carter et al., 2000; Dykens et al., 1990; Nolan et al., 1996; Pierre et al., 1999; Spencer et al., 2001). Although Hubka et al. (1988) and Dooley et al. (1999) indicated that having a family member with TS was associated with impairment, Carter et al. (1994) observed that family dysfunction was associated with ADHD symptoms but not with tics. The purpose of this study is to evaluate the association of TS and ADHD symptoms with other disruptive behavior and with social, adaptive, and family functioning. To this end, we studied four groups of children: TSonly, TS+ADHD, ADHD-only, and unaffected controls. We hypothesized that compared with the unaffected control and TS-only groups, children with TS+ADHD (1) would have higher indices of disruptive behavior; (2) would have greater functional impairment; and (3) would reside in families with higher levels of family dysfunction. To confirm the role of ADHD, an ADHD contrast group was also included. We also explored the association of tic severity with disruptive behavior and functional impairment. Finally, the impact of aggressive and delinquent behavior on functional impairment was evaluated, controlling for the ADHD diagnosis. J . A M . A C A D . C H I L D A D O L E S C . P S YC H I AT RY, 4 2 : 1 , J A N U A RY 2 0 0 3

METHOD Subjects Subjects were recruited to participate in one or more studies of childhood neuropsychiatric disorders conducted at the Yale Child Study Center between 1993 and 2000. The TS sample was ascertained through the Tic Disorder Clinic and through the local chapter of the Tourette Syndrome Association. Subjects with a primary diagnosis of ADHD were recruited either through the Yale outpatient clinic or through a local chapter of Children and Adults With Attention Deficit Disorder (CHADD). Unaffected control children were recruited from randomly selected names on the telemarketing list of approximately 10,000 families in the local community. These families received introductory letters, which were then followed by screening and recruitment telephone calls. Approximately 10% of families who were contacted participated and received the same diagnostic evaluation as other subjects. Control subjects were group-matched with the patients by age, gender, and socioeconomic status. Children with a history of neurological illness, past seizures or history of head trauma with loss of consciousness, mental retardation, pervasive developmental disorder, psychosis, or severe major depression were excluded. Additional exclusionary criteria for control subjects were any history of tic disorder, obsessive-compulsive disorder (OCD), ADHD, or current Axis I disorder. Written informed consent was obtained from the parents and assent was obtained from children. Families were paid $60 for participation. The study sample included 207 children (144 boys and 63 girls) between the ages of 7 and 18 years (mean = 11.1, SD = 2.4). All families were middle to upper-middle class. Forty-two children received a diagnosis of TS-only and 52 received a diagnosis of ADHD-only. Fifty-two children had TS and ADHD, and of these, 35 had TS and ADHD only and 17 had ADHD and OCD. For most analyses, these two groups were combined into a single “TS+ADHD” group. Finally, 61 unaffected control children were studied. Procedures Psychiatric diagnoses were established though clinical evaluation and administration of the Schedule for Tourette and Other Behavioral Syndromes (Pauls and Hurst, 1996). This method has been used in genetic and neuropsychological TS studies and includes the Schedule for Affective Disorders and Schizophrenia for School-Age ChildrenPresent and Lifetime Version (Kaufman et al., 1997). All subjects also completed a comprehensive battery of self-report and parent-rated measures. Research assistants administering these measures were blind to the diagnostic status of the subjects. During these evaluation procedures, medicated children were on their usual dose and type of medication. An experienced clinician interviewed each child and parent with the Yale Global Tic Severity Scale (YGTSS) (Leckman et al., 1989) and the Children’s Yale-Brown Obsessive Compulsive Scale (CY-BOCS) (Scahill et al., 1997). Following a review of all available information, two clinicians independently assigned DSM-IV diagnoses (Leckman et al., 1982). The final best-estimate diagnoses were assigned after all disagreements were resolved through additional examination of evaluation materials. Measures The Child Behavior Checklist (CBCL) (Achenbach, 1991) is a standardized parent-report measure of problem behavior and adaptive functioning. Two CBCL scales were used to reflect disruptive behavior and two scales were used to reflect social competency. The Aggressive Behavior scale consists of 20 items that measure physical aggression, argumen-

99

SUKHODOLSKY ET AL.

tativeness, and excessive anger. The scale has internal consistency of 0.92 in both referred and nonreferred children. The Delinquent Behavior scale consists of 13 items of antisocial behaviors, including lying, stealing, truancy, vandalism, and drug use. The internal consistency of the scale ranges from 0.74 to 0.83 for younger and older children, respectively. The items on all problem behavior scales of the CBCL are rated on a 3-point Likert scale. The Activities Competence scale reflects the number of sports, hobbies, and clubs in which the child participates as well as the parent’s perception of how well the child performs in these activities compared with other children. The Social Competence scale assesses the number of friends, time spent with friends, and the extent to which the child gets along with his/her peers. The Vineland Adaptive Behavior Scales-Survey Form (Sparrow et al., 1984) is a measure of social and personal competence in children from birth through age 19, which is administered in a semistructured parent interview format. This measure is standardized on a large national sample (mean = 100, SD = 15), and extensive reliability and validity information is available. Three domain indices were included in this study. The Communication domain reflects receptive, expressive, and written communication skills. The Daily Living Skills domain samples personal living habits, domestic task performance, and behavior in the community. The Socialization domain assesses interaction with others, including friendships, play, and social appropriateness. The Family Environment Scale (FES) (Moos and Moos, 1986) is a parent-rated scale that consists of 10 nine-item subscales evaluating various aspects of family functioning. Three subscales pertaining to family relations were used in this study. The Conflict subscale measures the degree to which family members openly express anger, aggression, and disagreement toward each other. The Cohesion/Caring subscale pertains to the degree of commitment, help, and support family members provide to each other. The Control subscale evaluates the number of family rules and the extent to which family rules are expected to be followed. All items are answered in a true/false response format, some items are reverse-scored to avoid response sets, and scores are reported as averages. The Conners Teacher Rating Scale (CTR) (Conners, 1989) was used to obtain teacher report of the child’s behavior. The scale consists of 28 items that are rated on a 4-point Likert scale. In this study, the eight-item Conduct scale was included to reflect the scope of conduct problems in the school environment. The YGTSS (Leckman et al., 1989) is a semistructured clinical interview developed to measure tic severity. The scale yields three summary scores: total motor score, total phonic score, and total tic score with the interrater agreement coefficients of 0.78, 0.91, and 0.84, respectively. The total tic score varies from 0 to 50 and is interpreted on a continuum from minimal to severe. The ratings of tic severity were obtained for a 1-week period preceding the in-person interview and constituted the YGTSS current scores. Additional ratings were obtained for the worst-ever tic scores. Analytic Strategy To examine the differences among the four diagnostic groups on the CBCL, the Vineland Adaptive Behavior Scales, and the FES measures, multivariate analyses of covariance (MANCOVAs) with gender as a covariate were undertaken. The multivariate tests were followed by the post hoc multiple comparisons with Bonferroni adjustment for each dependent variable. The Pearson correlation was used to examine the relationship among continuous variables and χ2 was used to test the difference between categorical variables. Hierarchical regression analyses were used to examine unique contributions of diagnostic status and disruptive behavior on the measures of social, adaptive,

100

and family functioning. Diagnostic status was coded as a categorical variable with four values (1 = TS, 2 = TS+ADHD, 3 = ADHD, and 4 = unaffected controls) for the analyses of variance and as two dichotomous variables for the TS and ADHD diagnosis (0 = absent and 1 = present) for regression analyses. SPSS was used for all data analyses and used an α level of p < .05 (two-tailed). Listwise deletion of missing values was used in MANCOVA and in regression analyses, and pairwise deletion of missing values was used in univariate comparisons, χ2 tests, and Pearson correlations. The CTR and the Vineland data were available for 135 and 118 subjects, respectively. These differences were due to unavailable teacher data during summer and the changes in the assessment batteries over the period of 8 years. The differences on demographic and clinical characteristics between the group of subjects with and without the CTR and Vineland data were examined using independent sample t tests; no differences were found (data not shown).

RESULTS

Demographic and clinical characteristics of the four diagnostic groups are reported in Table 1. There was significant difference in gender distributions across four diagnostic groups, which was controlled for statistically in the subsequent analyses. There were no significant differences among the diagnostic groups on age, race, and lifetime comorbid psychiatric diagnoses. Table 1 also presents the scores on the YGTSS current and worst-ever total scales. There were no significant differences between the TS-only and TS+ADHD groups on these or motor and phonic YGTSS scales. In the TS+ADHD group, there were no differences on any of the dependent measures between subjects who had TS and ADHD and subjects who had an additional diagnosis of OCD. To minimize the number of comparisons, three separate MANCOVAs with age and gender as covariates were performed with the four narrow-band CBCL scales, the three FES subscales, and the three Vineland domain scales. Multivariate effects of the diagnostic status were significant for the CBCL narrow-band scales of aggression, delinquency, activities, and social competencies (Pillai trace = 0.47; F3,159 = 7.32; p < .0001); the FES Conflict, Cohesion, and Control subscales (Pillai trace = 0.12; F3,168 = 2.41; p < .01); and the Vineland Communication, Daily Living, and Socialization domains (Pillai trace = 0.36; F3, 111 = 5.08; p < .0001). Post hoc univariate analyses and pairwise comparisons are reported in Table 2. Disruptive Behavior

Significant main effects of diagnostic status were observed for the two parent-rated and the teacher-rated measures of disruptive behavior. Pairwise comparisons of the two parent rating scales indicated that children with TS-only

J . A M . A C A D . C H I L D A D O L E S C . P S YC H I AT RY, 4 2 : 1 , J A N U A RY 2 0 0 3

DISRUPTIVE BEHAVIOR IN TS

TABLE 1 Demographic and Clinical Characteristics by Diagnostic Group

Mean age (SD) Gender (% male) Race (% white) Mean Full Scale IQ (SD) YGTSSb total current YGTSS total worse-ever Medication status (n, %) Medicatedc Not medicated Comorbid diagnosesd (n, %) Oppositional defiant Conduct disorder Depression Anxiety disorder (except OCD)

TS-Only (n = 42)

TS+ADHDa (n = 52)

ADHD-Only (n = 52)

10.79 (1.94) 71.4 90.5 113.6 (16.3) 19.32 (8.13) 27.08 (6.05)

11.11 (2.08) 90.4 98.1 110.5 (16.4) 20.45 (7.42) 28.29 (6.22)

11.79 (2.80) 69.2 92.3 111.5 (17.4)

Controls (n = 61) 10.76

(2.31) 50.8 93.3 115.3 (15.5)

Test

p

F3,203 = 2.19 χ23 = 20.84 χ212 = 11.63 F3,130 = .59 t85 = –.67 t85 = –.91

.091 .001 .471 .626 NS NS

18 24

42.9 57.1

36 16

69.2 30.8

32 20

61.5 38.5

— —

— —

χ22 = 6.91

.032

6 0 6 7

14.3 0 14.3 16.7

17 2 10 6

34.0 4.0 20.0 12.0

16 2 15 6

31.4 3.9 29.4 11.8

— — — —

— — — —

χ22 = 5.14 χ22 = 1.71 χ22 = 3.23 χ22 = .59

.076 .425 .199 .744

Note: TS = Tourette’s syndrome; ADHD = attention-deficit/hyperactivity disorder; YGTSS = Yale Global Tic Severity Scale; OCD = obsessivecompulsive disorder; NS = not significant. a This group consisted of 35 children who had TS and ADHD and 17 children who had TS and ADHD and OCD. b Total tic score does not include Impairment score. c Included 30 stimulants, 28 α2-agonists, 19 antipsychotics, 8 selective serotonin reuptake inhibitors, 6 tricyclic antidepressants, 2 mood stabilizers, and 1 anxiolytics (17 subjects were receiving more than one type of medication). d Lifetime diagnosis based on structured interview and available data. TABLE 2 Disruptive Behavior and Social, Adaptive, and Family Functioning Measures (Mean, SD) by Diagnostic Group TS-Only

Disruptive behavior CBCL Aggression CBCL Delinquent CTR Conduct Social and adaptive functioning CBCL Activities CBCL Social Vineland Communication Vineland Daily Living Vineland Socialization Family functioning FES Conflict FES Cohesion FES Control

TS+ADHD

ADHD-Only

Controls

Mean

SD

Mean

SD

Mean

SD

Mean

SD

Test

p

54.0b,c 52.1b,c 52.1

5.6 4.9 13.1

63.3a,d 59.0a,d 60.5d

11.4 8.5 15.6

63.7a,d 61.1a,d 59.3d

11.4 9.1 13.8

51.8b,c 52.1b,c 48.9b,c

4.0 3.9 10.5

F3,167 = 18.45 F3,160 = 16.58 F3,129 = 3.04

.0001 .0001 .03

46.4 42.9d 94.4 90.0d 93.1b,c

6.3 6.7 15.8 14.7 13.0

48.3 39.2d 83.5d 85.4d 79.3a,d

6.7 10.7 18.2 14.0 16.0

44.7d 40.8d 86.3d 81.2d 76.8a,d

7.8 7.8 16.8 13.2 20.2

49.9c 5.8 49.5a,b,c 6.2 101.1b,c 12.8 100.3a,b,c 14.1 99.9b,c 16.3

F3,160 = 6.17 F3,160 = 12.45 F3,111 = 5.94 F3,111 = 12.33 F3,111 = 12.32

.001 .0001 .001 .0001 .0001

3.3 7.2 4.9

2.1 1.7 1.8

4.5d 6.3d 5.2

2.2 2.6 1.8

3.9 6.4 5.9

2.0 2.2 1.8

F3,168 = 3.61 F3,168 = 3.56 F3,168 = 2.34

.02 .02 .07

3.0b 7.8b 5.3

2.1 1.5 1.8

Note: TS = Tourette’s syndrome; ADHD = attention-deficit/hyperactivity disorder; CBCL = Child Behavior Checklist; CTR = Conners Teacher Rating; FES = Family Environment Scale. a Different from TS-only. b Different from TS+ADHD. c Different from ADHD-only. d Different from unaffected controls.

did not differ from the unaffected controls and were rated significantly below the TS+ADHD and ADHD-only groups. At the same time, children with TS+ADHD did not differ from children with ADHD-only. Similar results J . A M . A C A D . C H I L D A D O L E S C . P S YC H I AT RY, 4 2 : 1 , J A N U A RY 2 0 0 3

were observed on the teacher rating of conduct problems. The TS+ADHD and ADHD-only groups did not differ from each other and were rated significantly higher than the control group. The scores of the TS-only group, though 101

SUKHODOLSKY ET AL.

in the lower range, did not differ significantly from those of any other group.

ables were significantly associated with the measures of motor or phonic tic severity.

Social and Adaptive Functioning

Additional Impact of Disruptive Behavior on Functional Outcome

All five measures of social and adaptive functioning yielded significant main effects of diagnostic status. On the CBCL Activities scale, the TS-only and TS+ADHD groups did not differ from each other, from the ADHDonly group, or from the unaffected control group. The ADHD-only group, however, scored significantly below the unaffected controls. On the CBCL Social Competence scale, all three groups with psychiatric diagnoses scored significantly below the controls and did not differ from each other. The TS-only group did not differ from unaffected controls in the Vineland Communication and Socialization domains and was significantly better than the TS+ADHD and ADHD-only groups in the Socialization domain. The TS+ADHD and ADHD-only groups did not differ from each other and were significantly below unaffected controls in all three domains. Family Functioning

Significant main effects of diagnostic status were also observed on the FES Conflict and Cohesion scales, but not on the Control scale. The TS+ADHD children lived in families with significantly greater levels of family dysfunction than the unaffected controls, as evidenced by higher mean scores on the Conflict and Cohesion scales. There were no significant mean score differences between the TS+ADHD and ADHD-only groups in any area of family functioning. The TS-only group did not differ from unaffected controls on any of the FES scales. Relationship With Tic Severity

Pearson correlations were used to examine the relationship among the YGTSS current motor and phonic tic severity scales and the measures of disruptive behavior and functional outcome in the subgroup of TS-only and TS+ADHD subjects. Of 22 correlations, only 2 were significant without controlling for the probability of type I error. The CBCL Aggressive Behavior scale was positively related to the YGTSS phonic tic severity (r64 = 0.31, p = .01), and the CTR Conduct scale was also positively related to the YGTSS total tic severity (r59 = 0.28, p = .03). Using a Bonferroni correction, only correlations with α value of .002 should be considered statistically significant. Given the modest size of the observed correlations, it can be concluded that few if any of these vari102

Hierarchical regression analyses were conducted using TS and ADHD diagnostic status and CBCL Aggressive Behavior and Delinquent Behavior scores to predict the measures of functional outcome. The effects of each variable were examined controlling for previously entered variables. All models were adjusted for age and gender. Table 3 presents multiple regression coefficients for each dependent variable and R 2 change, the increment in squared semipartial correlation of the criterion variable (e.g., Vineland Socialization) with the predictor variable (e.g., TS diagnosis) entered after partialing out the variance accounted for by the predictor variables entered in the previous steps. A diagnosis of TS significantly predicted impairment only on the CBCL Social Competence scale. ADHD, on the other hand, significantly predicted all seven measures of functional outcome included in regression analyses. The CBCL Aggressive Behavior and Delinquent Behavior scales, entered as one block, added a unique contribution to the CBCL Social Competence score, Vineland Socialization score, and FES Conflict and Cohesion scores. DISCUSSION

This study compared children and adolescents with TS-only, TS+ADHD, ADHD-only, and unaffected controls on the indices of disruptive behavior and functional outcome. Although similar comparisons were reported previously (Carter et al., 2000; Spencer et al., 1998; Stephens and Sandor, 1999), this study reports the results from the largest sample to date that was well-characterized with regard to diagnosis, tic severity, and functional outcome. Consistent with the study hypotheses, children with TSonly did not differ from unaffected controls on the parent ratings of aggression and delinquent behavior or on the teacher ratings of conduct problems. By contrast, children with TS+ADHD were significantly higher than normal controls on measures of disruptive behavior. In addition, the TS+ADHD group did not differ from the group of children with ADHD-only, which suggests that the risk for aggressive and delinquent behavior in children with TS is posed largely by the presence of ADHD. This finding is consistent with the literature on aggressive and disruptive behavior in children with ADHD (Hinshaw, 1987) J . A M . A C A D . C H I L D A D O L E S C . P S YC H I AT RY, 4 2 : 1 , J A N U A RY 2 0 0 3

DISRUPTIVE BEHAVIOR IN TS

TABLE 3 Summary of Hierarchical Regression Analyses for Variables Predicting Functional Outcome Any TS

CBCL Activities CBCL Social Vineland Communication Vineland Daily Living Vineland Socialization FES Conflict FES Cohesion

Any ADHD

Model R 2

ΔR 2

F

ΔR 2

0.04 0.27 0.23 0.27 0.37 0.20 0.25

0.00 0.04 0.01 0.02 0.00 0.02 0.01

0.02 7.51** 0.77 1.54 0.00 2.60 1.00

0.03 0.12 0.13 0.25 0.30 0.04 0.04

F 4.84** 23.82*** 15.84*** 33.91*** 43.30*** 6.76** 7.12**

CBCL Aggression and Delinquency ΔR 2 0.00 0.08 0.03 0.00 0.06 0.13 0.08

F .21 8.37*** 1.54 .07 4.65** 11.86*** 8.52***

Note: TS = Tourette’s syndrome; ADHD = attention-deficit/hyperactivity disorder; CBCL = Child Behavior Checklist; FES = Family Environment Scale. Model R 2 = total variance explained by the model including age, gender, TS diagnosis, ADHD diagnosis, and CBCL Aggression and Delinquency scales; ΔR 2 = increments in explained variance. ** p < .01; *** p < .001.

as well as the studies that examined disruptive behavior in children with TS-only and TS with ADHD. Beginning from the early studies of referred children (Erenberg et al., 1986; Singer and Rosenberg, 1989) as well as adults (Comings and Comings, 1985; Moldofsky et al., 1974; Robertson et al., 1988), aggressive behavior in patients with TS was described as explosive, out of proportion to provocation, and incongruent to the child’s usual personality. Oppositional behavior, which is commonly characterized by disobedience and argumentativeness, has also been described as more persistent and intense in children with TS. Because of the intensity and unpredictability in response to minimal provocation, anger outbursts in TS have been referred to as rage attacks or rage storms (Budman et al., 1998). These episodes of anger reportedly last from a few minutes to an hour and are usually followed by remorse. Data from the current study suggest that aggressive behavior in children with TS is observed primarily when comorbid ADHD is present. Children with TS, regardless of ADHD comorbidity, presented with an age-appropriate level of engagement in activities such as hobbies, clubs, and sports, as measured by the Activities Competence scale of the CBCL. However, consistent with the findings by Carter at al. (2000), children with TS+ADHD demonstrated significant impairment on the four other measures of social and adaptive functioning and were similar to the ADHD contrast group. This pattern of scores on the CBCL Social Competence scales and the Vineland Adaptive Behavior Scales is indicative of multiple deficits, such as having fewer friends, being rejected by peers, and not meeting the demands of everyday life. Children with TS-only were also more impaired J . A M . A C A D . C H I L D A D O L E S C . P S YC H I AT RY, 4 2 : 1 , J A N U A RY 2 0 0 3

than unaffected controls on measures of social competency and daily living skills, but less so than those with TS+ADHD. These findings are generally consistent with earlier reports (Bawden et al., 1998; Carter et al., 1994; Dykens et al., 1990; Stokes et al., 1991). Finally, we explored the influence of disruptive behavior on social, adaptive, and family functioning above and beyond the diagnoses of TS and ADHD. When ADHD co-occurs with aggressive behavior, additional social problems, including association with deviant peers and involvement in antisocial behavior, may become salient (Deater-Deckard, 2001). Aggressive behavior was found to have the most detrimental effect on peer relationship problems in schoolchildren (Ladd and Burgess, 1999) and in children and adolescents with ADHD (Bagwell et al., 2001). Similarly, in this study, the diagnosis of ADHD was related to impairment across all measures of functional outcome, but the scores on the CBCL aggression and delinquency scales were associated with an additional increment in socialization impairment. Aggressive and delinquent behavior may also have a negative impact on family functioning as evidenced by the measures of family conflict and cohesion. However, the direction of causality is unclear, as family dysfunction can contribute to a child’s disruptive behavior problems. Limitations

The phenomenology of disruptive behavior in TS is not well understood, and the measures used in this study might have missed the specific features of such behavior in TS. Although this study found no relationship between tic severity and disruptive behavior or functional outcome, other 103

SUKHODOLSKY ET AL.

tic characteristics, such as complexity, were not investigated. The association between tic severity and impairment could also be confounded by the child’s medication status. First, psychotropic medication could have attenuated tic severity and associated impairment. Second, we note that more than half of the children in TS-only group were not on medication, suggesting that they had a milder form of TS. Subjects with TS were ascertained from a specialty clinic, which may not reflect the full breadth of TS phenomenology. Similarly, the ADHD sample was ascertained in part from the CHADD organization. Children in families who participate in voluntary organizations may represent a biased sample. This possibility is further suggested by the observation that approximately a third of the sample was not taking medication, which is lower than expected for children with ADHD. In addition, the sample included mostly middle-class white subjects and the results may not be generalizable to other populations. Finally, the cross-sectional design makes it impossible to determine the directionality of associations between the variables. Clinical Implications

The findings of this study support the notion that clinicians should focus on the identification and treatment of target symptoms in the management of children with TS. The presence of mild tics in the absence of ADHD may not require medical intervention other than education and monitoring (Petersen and Cohen, 1998). This is especially true given the evidence that tics tend to peak in severity prior to puberty and to decline in severity by early adulthood (Leckman et al., 1998). On the other hand, because of the clear negative impact on functional outcome, the presence of ADHD warrants intervention regardless of tic severity. Current evidence suggests that stimulants may be safe and effective for treating ADHD in children with TS (Tourette’s Syndrome Study Group, 2002). Alternatively, nonstimulants such as guanfacine (Scahill et al., 2001), clonidine (Leckman et al., 1991), or desipramine (Spencer et al., 2002) may be useful. REFERENCES Achenbach TM (1991), Manual for the Child Behavior Checklist/4–18 and 1991 Profile. Burlington: University of Vermont Press Bagwell CL, Molina BSG, Pelham WE, Hoza B (2001), Attention-deficit hyperactivity disorder and problems in peer relations: predictions from childhood to adolescence. J Am Acad Child Adolesc Psychiatry 40:1285–1292 Bawden HN, Stokes A, Camfield CS, Camfield PR, Salisbury S (1998), Peer relationship problems in children with Tourette’s disorder or diabetes mellitus. J Child Psychol Psychiatry 39:663–668

104

Budman CL, Bruun RD, Park KS, Lesser M, Olson ME (2000), Explosive outbursts in children with Tourette’s disorder. J Am Acad Child Adolesc Psychiatry 39:1270–1276 Budman CL, Bruun RD, Park KS, Olson ME (1998), Rage attacks in children and adolescents with Tourette’s disorder: a pilot study. J Clin Psychiatry 59:576–580 Carter AS, O’Donnell DA, Schultz RT, Scahill L, Leckman JF, Pauls DL (2000), Social and emotional adjustment in children affected with Gilles de la Tourette’s syndrome: associations with ADHD and family functioning. J Child Psychol Psychiatry 41:215–223 Carter AS, Pauls DL, Leckman JF, Cohen DJ (1994), A prospective longitudinal study of Gilles de la Tourette’s syndrome. J Am Acad Child Adolesc Psychiatry 33:377–385 Coffey BJ, Park KS (1997), Behavioral and emotional aspects of Tourette syndrome. Neurol Clin North America 15:277–289 Comings DE, Comings BG (1985), Tourette’s syndrome: clinical and psychological aspects of 250 cases. Am J Hum Genet 35:435–450 Comings DE, Comings BG (1987), A controlled study of Tourette’s syndrome, II: conduct. Am J Hum Genet 4:742–760 Conners CK (1989), Conners’ Rating Scales Manual. North Tonawanda, NY: Multi-Health Systems Costello EJ, Angold A, Burns BJ et al. (1996), The Great Smoky Mountains Study of Youth: goals, design, methods, and the prevalence of DSM-IIIR disorders. Arch Gen Psychiatry 53:1129–1136 De Groot CM, Janus MD, Bornstein RA (1995), Clinical predictors of psychopathology in children and adolescents with Tourette syndrome. J Psychiatr Res 29:59–70 Deater-Deckard K (2001), Annotation: recent research examining the role of peer relationship in the development of psychopathology. J Child Psychol Psychiatry 42:565–579 Dooley JM, Brna PM, Gordon KE (1999), Parent perceptions of symptom severity in Tourette’s syndrome. Arch Dis Child 81:440–441 Dykens E, Leckman JF, Riddle MA, Hardin MT, Schwartz S, Cohen D (1990), Intellectual, academic, and adaptive functioning of Tourette syndrome children with and without attention deficit disorder. J Abnorm Child Psychol 18:607–615 Edell-Fisher BH, Motta RW (1990), Tourette syndrome: relation to children’s and parents’ self-concepts. Psychol Rep 66:539–545 Erenberg G, Cruse RP, Rothner AD (1986), Tourette syndrome. Cleve Clin Q 53:127–131 Hinshaw SP (1987), On the distinction between attentional deficits/ hyperactivity and conduct problems/aggression in child psychopathology. Psychol Bull 10:443–463 Hornsey H, Banerjee S, Zeitlin H, Robertson M (2001), The prevalence of Tourette syndrome in 3–14-year-olds in mainstream schools. J Child Psychol Psychiatry 42:1035–1039 Hubka GB, Fulton WA, Shady GA, Champion LM, Wand R (1988), Tourette syndrome: impact on Canadian family functioning. Neurosci Biobehav Rev 12:259–261 Kadesjo B, Gillberg C (2000), Tourette’s disorder: epidemiology and comorbidity in primary school children. J Am Acad Child Adolesc Psychiatry 39:548–555 Kaufman J, Birmaher B, Brent D et al. (1997), Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 36:980–988 King RA, Scahill L (2001), Emotional and behavioral difficulties associated with Tourette syndrome. In: Tourette Syndrome, Cohen DJ, Goetz CG, Jankovic J, eds. Philadelphia: Lippincott Williams & Wilkins, pp 79–88 Ladd G, Burgess KB (1999), Charting the relationship trajectories of aggressive, withdrawn, and aggressive/withdrawn children during early grade school. Child Dev 70:910–929 Leckman JF, Harding MT, Riddle MA, Stevenson J, Ort SI, Cohen DJ (1991), Clonidine treatment of Gilles de la Tourette’s syndrome. Arch Gen Psychiatry 48:324–328 Leckman JF, Riddle MA, Hardin MT et al. (1989), The Yale Global Tic Severity Scale: initial testing of a clinician-rated scale of tic severity. J Am Acad Child Adolesc Psychiatry 28:566–573 Leckman JF, Sholomskas D, Thompson WD, Belanger A, Weissman MM (1982), Best estimate of lifetime psychiatric diagnosis: a methodological study. Arch Gen Psychiatry 39:879–883

J . A M . A C A D . C H I L D A D O L E S C . P S YC H I AT RY, 4 2 : 1 , J A N U A RY 2 0 0 3

DISRUPTIVE BEHAVIOR IN TS

Leckman JF, Zhang H, Vitale A et al. (1998), Course of tic severity in Tourette syndrome: the first two decades. Pediatrics 102:14–19 Moldofsky H, Tullis C, Lamon R (1974), Multiple tic syndrome (Gilles de la Tourette’s syndrome). J Nerv Ment Dis 159:282–292 Moos RH, Moos BM (1986), Family Environment Scale: Manual. Palo Alto, CA: Consulting Psychologists Press Nolan E, Sverd J, Gadow KD, Sprafkin J, Ezor SN (1996), Associated psychopathology in children with both ADHD and chronic tic disorder. J Am Acad Child Adolesc Psychiatry 35:1622–1630 Pauls DL, Hurst CR (1996), Schedule for Tourette and Other Behavioral Syndromes. New Haven, CT: Yale University Child Study Center (available from L Scahill: [email protected]) Peterson BS, Cohen DJ (1998), The treatment of Tourette’s syndrome: multimodal, developmental intervention. J Clin Psychiatry 59(suppl 1):62–72 Peterson BS, Pine DS, Cohen P, Brook JS (2001a), Prospective, longitudinal study of tics, obsessive-compulsive, and attention-deficit/hyperactivity disorders in an epidemiological sample. J Am Acad Child Adolesc Psychiatry 40:685–695 Peterson BS, Staib L, Scahill L et al. (2001b), Regional brain and ventricular volumes in Tourette syndrome. Arch Gen Psychiatry 58:427–440 Peterson BS, Thomas P, Kane M et al. (in press), Basal ganglia volumes in Tourette syndrome. Arch Gen Psychiatry Pierre CB, Nolan EE, Gadow KD, Sverd J, Sprafkin J (1999), Comparison of internalizing and externalizing symptoms in children with attention-deficit hyperactivity disorder with and without comorbid tic disorder. J Dev Behav Pediatr 20:170–176 Pliszka SR, Carlson CL, Swanson JM (1999), ADHD With Comorbid Disorders: Clinical Assessment and Management. New York: Guilford Robertson MM, Trimble MR, Lees AJ (1988), The psychopathology of Gilles de la Tourette syndrome: a phenomenological analysis. Br J Psychiatry 152:383–390 Rosenberg LA, Brown J, Singer HS (1995), Behavioral problems and severity of tics. J Clin Psychol 51:760–767 Rosenberg LA, Harris JC, Singer HS (1984), Relationship of the Child Behavior Checklist to an independent measure of psychopathology. Psychol Rep 54:427–430

J . A M . A C A D . C H I L D A D O L E S C . P S YC H I AT RY, 4 2 : 1 , J A N U A RY 2 0 0 3

Scahill L, Chappell PB, Kim YS et al. (2001), A placebo-controlled study of guanfacine in the treatment of children with tic disorders and attentiondeficit/hyperactivity disorder. Am J Psychiatry 158:1067–1074 Scahill L, Riddle MA, Hardin MT et al. (1997), Children’s Yale-Brown Obsessive Compulsive Scale: reliability and validity. J Am Acad Child Adolesc Psychiatry 36:844–852 Scahill L, Schwab-Stone M, Merikangas KR, Leckman JF, Zhang H, Kasl S (1999), Psychosocial and clinical correlates of ADHD in a community sample of school-age children. J Am Acad Child Adolesc Psychiatry 38:976–984 Singer HS, Rosenberg LA (1989), Development of behavioral and emotional problems in Tourette syndrome. Pediatr Neurol 5:41–44 Sparrow SS, Balla DA, Cicchetti DV (1984), Vineland Adaptive Behavior Scales. Circle Pines, MN: American Guidance Service Spencer T, Biederman J, Coffey B et al. (2002), A double-blind comparison of desipramine and placebo in children and adolescents with chronic tic disorder and comorbid attention-deficit/hyperactivity disorder. Arch Gen Psychiatry 59:649–656 Spencer T, Biederman J, Coffey B et al. (2001), Tourette disorder and ADHD. In: Tourette Syndrome, Cohen DJ, Goetz CG, Jankovic J, eds. Philadelphia: Lippincott Williams & Wilkins, pp 57–78 Spencer T, Biederman J, Harding M et al. (1998), Disentangling the overlap between Tourette’s disorder and ADHD. J Child Psychol Psychiatry 39:1037–1044 Stefl ME (1984), Mental health needs associated with Tourette syndrome. Am J Public Health 74:1310–1313 Stephens RJ, Sandor P (1999), Aggressive behavior in children with Tourette syndrome and comorbid attention-deficit hyperactivity disorder and obsessive-compulsive disorder. Can J Psychiatry 44:1036–1042 Stokes A, Bawden HN, Camfield PR, Backman JE, Doodley JM (1991), Peer problems in Tourette’s disorder. Pediatrics 87:936–942 Tourette’s Syndrome Study Group (2002), Treatment of ADHD in children with tics: a randomized controlled trial. Neurology 58:527–536 Wilson RS, Garron DC, Tanner CM, Klawans HL (1982), Behavior disturbance in children with Tourette syndrome. In: Gilles de la Tourette Syndrome, Freidhoff AJ, Chase TN, eds. New York: Raven, pp 329–333

105