Journal of Pediatric Psychology, Vol. 27, No. 2, 2002, pp. 203-208
© 2002 Society of Pediatric Psychology
Brief Report: Cognitive Functioning in Children With Tourette's Syndrome With and Without Comorbid ADHD
1 Utrecht University, 2 University Medical Center Utrecht
All correspondence should be sent to Nico Brand, Department of Health Psychology, Utrecht University, Heidelberglaan 1, 3584 CS Utrecht, The Netherlands. E-mail: N.Brand{at}fss.uu.nl .
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Abstract |
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Objective: To examine whether patients with Tourette's syndrome (TS) with and without comorbid attention deficit and hyperactivity disorder (ADHD) differ in cognitive functioning and whether a higher level of cognitive functioning is associated with severity of TS symptoms and psychosocial functioning.
Methods: Cognitive functioning, symptom severity, and psychosocial functioning were examined in 40 patients (33 boys, 7 girls; age range 6-18 years) with TS, of whom 17 had the comorbid diagnosis of ADHD.
Results: Patients with a comorbid ADHD diagnosis evidenced poorer performance than those with TS alone with respect to severity of TS symptoms, psychosocial functioning, verbal and performance intelligence, and word fluency, but not on tests of cognitive flexibility. Psychosocial functioning was predicted by symptom severity, but not by intelligence or fluency.
Conclusions: Results confirm prior findings that comorbid ADHD is associated with more TS symptoms and worse psychosocial and cognitive functioning, and motivate whether cognitive flexibility plays a role in moderating the deleterious psychosocial effects of Tourette's syndrome and ADHD.
Key words: Tourette's syndrome; ADHD; cognitive flexibility; executive functions; children; adolescents.
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Introduction |
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Tourette's syndrome (TS) is characterized by a chronic pattern of simple or complex motor and vocal tics occurring involuntarily. TS has a typical onset between 5 and 7 years of age. In about 50% of patients, there is comorbidity with attention-deficit hyperactivity disorder (ADHD) (Comings & Comings, 1988
;
Leckman et al., 1997).
Self-regulation and adequate coping are important for well-being in people
with TS.
Neurobiological hypotheses stress the involvement of the basal ganglia in
TS. Connections of this region with other subcortical and frontal and premotor
areas suggest that TS may be associated with deficits in executive functions
(Ozonoff, Strayer, McMahon, & Filloux,
1998). However, Pennington and Ozonoff
(1996) reported little
evidence of executive dysfunctions in TS but more consistently so in ADHD.
Cognitive disturbances have frequently been reported in children with TS.
Early studies suggested that patients with TS had subnormal IQs
(Thompson, O'Quinn, & Logue,
1979) and that performance IQ (PIQ) was lower than verbal IQ
(VIQ). Recently it was suggested that comorbidity with ADHD exacerbates the
outcome (Dykens et al., 1990;
Ozonoff et al., 1998).
Bornstein (1990) found that the
cognitive performance of patients with TS was generally normal, although there
were weaknesses in executive tasks such as concept formation and verbal
fluency. Schuerholz, Baumgardner, Singer, Reiss, and Denckla
(1996) compared patients with
TS with non-TS comparison groups and with comorbid TS and ADHD patients. They
found a poorer performance on verbal fluency in the TS-only group. Ozonoff et
al. (1998), however, found
failures to suppress unintended behavior (an executive function) only in the
comorbid or severely disturbed patients. Channon, Flynn, and Robertson,
(1992) found deficits on
attentional measures such as a serial addition task, the Trail Making Test
(TMT) and a vigilance test, in adult patients with TS compared to a comparison
group.
Deficits in executive functions may impede psychosocial performance. In
patients with TS, executive functions such as planning and attention may
permit better coping with the tic behavior and potentially embarrassing
situations. Patients with more cognitive flexibility may experience less
distress and have a better psychosocial functioning and well-being. That is,
these executive capabilities would diminish the influence of symptom severity.
This suggestion is relevant in that cognitive flexibility may be trained on a
behavioral level (Delahunty & Morice,
1996).
This study examines whether patients with TS only and patients with TS and comorbid ADHD differ in cognitive functioning, and whether cognitive flexibility moderates the effect of symptom severity on psychosocial functioning. We hypothesized that patients with a comorbid diagnosis perform worse in cognitive tests than those with TS alone and that psychosocial functioning is affected more by symptom severity in patients with low cognitive flexibility than in patients with high flexibility.
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Method |
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Participants
In this retrospective case design, archival data were obtained from 40 Dutch outpatients involved in a treatment program in the Department of Child Psychiatry of the University Medical Center Utrecht. The department is a major outpatient clinic in the Netherlands, specializing in the diagnosis and treatment of TS and ADHD. The patients were assessed voluntarily. Assessments included a developmental history and a semi-structured parent interview, a psychiatric interview, a review of prior records, and information obtained from the teacher and psychological testing. In the interview with the parent, the diagnostic criteria of all relevant Axis-I conditions according to the DSM-IV (APA, 1994
) were
systematically reviewed, particularly those of disruptive conditions, anxiety
disorders, obsessive compulsive disorders, depressive conditions, and tic
disorders. The information about TS-related symptoms and features was
organized according to a fixed format including measures of psychosocial
functioning and severity of the disorder. The diagnosis of TS was confirmed by
a psychiatrist specializing in the assessment and treatment of TS (JKB).
Seventeen patients had a comorbid ADHD (all combined subtype characterized by
attention deficit and hyperactivity). ADHD symptoms were assessed using the
Diagnostic Interview Schedule for Children
(Kasius, 1993). Ages ranged between 6 and 18 years. The children in the TS-only group had a mean age of 11.7 years (SD = 3.6); in the comorbid group, this was 10.1 years (SD = 2.5). The difference in age was not significant. There were 33 boys (17 in the TS-only group) and 7 girls (6 in the TS-only group), which approximately equals the male/female ratio in the population. Distribution of type of medication in both groups was neuroleptic (10 in TS only/4 in comorbid group), clonidine (5/3), neuroleptic and clonidine combined (2/6), and no medication (6/4). Medication was aimed at the TS symptoms. No other medication was given.
Instruments
Instruments included the Tourette's Syndrome Global Scale (TSGS;
Harcherik, Leckman, Detlor, & Cohen,
1984). The TSGS provides a global score comprised of judgment of
frequency and disruptive impact of the different types of tics and judgment of
the child's behavior, motor restlessness, and school or work problems. The
scores may range between 0 and 100. To assess general psychosocial functioning
the Dutch version of Endicott's Kiddy GAS (Children-Global Assessment Scale)
was used (Endicott, Spitzer, & Feiss, 1976). This scale yields a score
from 1 (dangerous for self and others continuously) to 9 (functioning well in
all areas). Verbal and Performance IQ were measured with the Wechsler
Intelligence Scale for Children (Pijl, De
Bruyn, Haasen, Poortinga, & Lutje Spelberg, 1982) for children
between the ages of 6 and 15 (32 children), and the Wechsler Adult
Intelligence Scale (Stinissen, Willems,
Coetsier, & Hulsman, 1970) for those older than 15 years (6
children). Three neuropsychological tests were administered. First was the
Trail Making Test (TMT; Lezak,
1995). The TMT measures the ability to shift quickly between
concepts (numbers and letters). As such, it is a measure of divided attention,
or cognitive flexibility. This applies particularly to Form B, in which
numbers and letters have to be traced alternately in ascending order. In these
executive functions, the frontal lobes are believed to be involved. Second was
the Stroop Color Word Interference Test. This test consists of three cards:
(1) reading of color names (2) naming of colors, and (3) naming of the colors
in which color names are printed. On card 3, the print color interferes with
the color name. An interference measure is calculated, which is the time for
card 3 minus the time for finishing card 2. This measure stands for the
ability to attend to the physical features of the task while inhibiting the
normal reading process, an ability also ascribed to frontal lobe mechanisms.
The third test was for verbal fluency: within 1 minute, as many exemplars of a
certain semantic category as possible must be mentioned. It is a measure of
categorical long-term memory and word production. Two categories were
included: "animals" and "professions." The task has
proven to be a sensitive indicator of brain dysfunction, especially in the
frontal lobe area (Perret,
1974) and measuring aspects of mental flexibility
(Lezak, 1995).
Statistical Analysis
Not all measures were available from each participant for unknown clinical
reasons. See Table I for the
number of participants for each variable. Analysis of variance was used to
compare scores of symptom severity and psychosocial and cognitive functioning
between patients with TS-only and patients with TS and ADHD. Regarding the
multiple testing, the level of significance was set to the conservative
Bonferroni criterion of p =.005, or the normal alpha of.05 divided by
the number of measures (11). The scores of the TMT (A and B) and the Stroop
Interference measure were combined into a measure called cognitive flexibility
using z scores (correlations were between.50 and.79; Cronbach's alpha
was.83). The z scores were added and divided by the number of
variables. The two fluency measures were averaged (correlation of.65;
alpha.79) into a single word fluency measure. Multiple regression was used to
examine the relationship between symptom severity and psychosocial functioning
and the possible moderating role of intelligence, cognitive flexibility, and
word fluency, according to the procedures proposed by Baron and Kenny
(1986) and Holmbeck
(1997). Twenty-one
participants with complete data with respect to all variables (of these
participants, 8 had the comorbid diagnosis, and 2 of the 21 were female) were
included.
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Results |
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Table I shows means and standard deviations of TSGS, Kiddy GAS, and the cognitive measures of the TS-only and the comorbid patients. The comorbid group had a significant higher mean score on the TSGS, F(1, 33) = 11.9, p =.002, and a lower score on the Kiddy GAS scale, F(1, 27) = 10.6, p =.003, than the TS-only group. The comorbid patients also had a lower verbal IQ, F(1, 36) = 14.7, p <.001, than the patients with TS alone. The same was true for performance IQ, although the difference just failed to reach the Bonferroni criterion, F(1, 36) = 8,7, p =.006. Differences between comorbid patients and patients with TS-only on the flexibility tests (Stroop and TMT) were not significant. Patients with comorbid diagnosis performed significantly worse in word fluency when compared to the patients with TS-only, F(1, 29) = 11.03, p =.002. In sum, the comorbid patients had significantly poorer scores than patients with TS-only on TSGS, Kiddy GAS, verbal IQ, and word fluency.
Table I also lists the effect sizes and associated estimation of power in each of the comparisons. The effect size is high with respect to the IQ measures and verbal fluency, but low to moderate with respect to the Stroop and TMT.
Multiple Regression
In an initial stepwise regression analysis, we examined whether the
cognitive variables were predictive of individual differences in psychosocial
functioning over and above variance explained by symptom severity. We found
that intelligence and word fluency were not predictive of psychosocial
functioning. The predictive contribution of cognitive flexibility was stronger
compared to these factors, although not statistically significant.
In a second analysis, the TSGS score (predictor) and cognitive flexibility
(possible moderator) were both entered simultaneously, after being
"centered" (Aiken & West,
1991; Holmbeck,
1997). This was followed by entering the interaction term. In this
way, we examined whether cognitive functioning affected the relationship
between symptom severity and psychosocial functioning.
Table II shows that the TSGS score was the major predictor (ß = -.77; t = -7.23, p =.000) reflecting higher symptom severity associated with worse psychosocial functioning. Cognitive flexibility was not significant in the prediction of psychosocial functioning. This was also true for the interaction between severity and flexibility. Explained variance (adj. R2) of the regression model was 80.7 %, F(1, 17) = 3.65, p =.07. Inclusion of diagnostic group (TS-only versus comorbid patients) in the regression model slightly changed the p values (.07 for flexibility and.09 for the interaction severity x flexibility), suggesting that the differentiation between TS and comorbidity did not explain much variance over and beyond that of symptom severity. Finally, analyses using interactions of symptom severity with single cognitive variables (Stroop tasks, TMT-A, TMT-B, word fluency) showed that TMT-B (concept shifting) was the leading variable in the prediction of psychosocial functioning.
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Discussion |
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Patients with TS and comorbid ADHD perform less well on cognitive tasks than patients with TS alone. Verbal and Performance IQs were normal for the patients with TS-only, as Bornstein (1990
) reported, but were lower
for the patients with a comorbid diagnosis. Dykens et al.
(1990) reported that children
with TS and ADHD had a lower IQ (especially performance IQ) than patients with
TS without the attention deficit.
Pennington and Ozonoff
(1996) concluded that
executive dysfunctions are more likely in ADHD than in TS. We hypothesized
that patients with a comorbid diagnosis would show a weaker performance on the
tests of cognitive flexibility. This was in part confirmed. Verbal fluency was
significantly impaired in the children with a comorbid diagnosis. Performance
on the executive Stroop and Trail subtasks also was weaker in the comorbid
condition in comparison to the Tourette's group, albeit not statistically
significant, possibly due to low power.
It was suggested that the impact of symptom severity on psychosocial
functioning could depend on the degree of cognitive functioning. A
nonsignificant contribution of cognitive flexibility in the regression
analysis was found. Concept shifting (as measured with Form B of the TMT) is a
measure of executive functioning (Lezak,
1995; Pennington &
Ozonoff, 1996). In combination with other executive functions such
as inhibition (Ozonoff et al.,
1998), flexibility may be necessary for self-regulation and coping
with the condition. Executive control operations are important in regulating
behavior in coping with malfunctions and states of stress. Our data did not
confirm the hypothesis that diminished cognitive flexibility may be important
to explain the influence of symptom severity on psychosocial functioning.
The power of our study is low, and replication with larger samples is needed. We were not able to confirm the hypothesis, but the data are suggestive of the importance of the comorbidity factors in Tourette's syndrome. The possible role of mental flexibility as a buffer for the psychological impact of symptom severity in TS should be further investigated.
The results are relevant clinically in that, for patients who are low on
cognitive flexibility, treatment of symptoms could be the preferred way to
psychosocial well-being. Delahunty and Morice
(1996) suggested that cognitive
flexibility may be trained. Some cognitive flexibility may thus play a role in
coping with TS, and interventions that enhance cognitive flexibility may be
helpful for children with TS.
Received November 30, 1999; revision received August 21, 2000; revision received December 5, 2000; revision received April 24, 2001; revision received June 14, 2001; accepted July 7, 2001
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