Comorbidity of Attention-deficit Hyperactivity Disorder and Overanxious Disorder STEVEN R. PLISZKA, M.D. Abstract. One hundred seven preadolescent children who meet criteria for attention-deficit hyperactivity disorder (ADHD) were further diagnosed by structured interview with regard to oppositional defiant disorder, conduct disorder, and overanxious disorder (ANX). The ADHD population was subdivided into those with and without a comorbid ANX, and the two ADHD groups were compared with each other and a control group in terms of teacher ratings, behavioral observations during an academic task, and the Inhibition version of the Continuous Performance Test. The results suggested that ADHD/ANX children may be less impulsive and/or hyperactive than those children with ADHD alone though they remain more impaired than controls. There was also a trend for the comorbid group to show fewer conduct disorder symptoms. The implications of comorbidity for the study of both ADHD and ANX are discussed. J. Am. Acad. Child Adolesc. Psychiatry, 1992, 31, 2:197-203. Key Words: attention-deficit hyperactivity disorder, anxiety, impulsivity, comorbidity. It is well accepted that children with attention-deficit hyperactivity disorder (ADHD) show significant comorbidity with other psychiatric disorders (Biederman et al., 1991a). Two independent epidemiological studies have shown that about one-fourth of children who meet DSM-III-R criteria for attention deficit disorder (ADD) concurrently meet criteria for an overanxious (ANX) disorder (Anderson et al., 1987; Bird et al., 1988). Conversely, Strauss et al. (1988) found that over a third of the child patients at a clinic for anxiety disorders met criteria for ADD. How is such comorbidity to be interpreted? Are these simply independent disorders that happen to overlap, or are those with comorbid ADHD/ANX a separate subgroup, different clinically or biologically from those with ADHb alone? Several studies have compared children who have ADHD alone with those who have ADHD and a comorbid anxiety disorder. Pliszka (1989) compared a group of ADHD children with those who met criteria or both ADHD and ANX disorder on a number of laboratory measures of behavior and cognition. Teachers rated the comorbidgroup as less inattentive and overactive on the Iowa Conners Teacher Rating Scale (CTRS) (Loney and Milich, 1982) than the ADHD-only group. The comorbid group showed lower levels of off-task behavior during an observation room task where the child had to remain seated and do arithmetic problems for 15 minutes. Off-task behavior was defined as the child breaking eye contact with the work paper for more than 4 seconds. Fidgeting, vocalizing, playing with objects, and getting out of one's seat were also measured. It can be seen that these behaviors tap into the hyperactive and impulsive aspects of
Accepted September 20, 1991. Dr. Pliszka is Assistant Professor of Psychiatry at The University of Texas Health Science Center at San Antonio. This work was supported by Grant 1 K11 MH00731 from the National1nstitute of Mental Health. Request reprints from Dr. Pliszka, Department of Psychiatry, The University ofTexas Health Science Center at San Antonio, 7703 Floyd Curl Drive, San Antonio, Texas 78284-7792. 0890-8567/92/3102--0 197$03.0010© 1992 by the American Academy of Child and Adolescent Psychiatry. J. Am. Acad. Child Adolesc. Psychiatry, 31:2, March 1992
the ADHD syndrome. If a child simply sits quietly daydreaming and working very slowly, he is not rated as offtask unless he makes a motor movement-i.e., breaking eye contact with the paper. The groups performed a selective attention task in which the child had to memorize four letters on a computer screen and then search a series of displays to determine whether one of the letters they memorized was present. The comorbid group showed slower reaction times and greater accuracy relative to the ADHD-only group as the display became more complex. Interestingly, the ADHDonly subjects began responding faster (more impulsively) as the display become more complex. The comorbid group was able to tolerate longer searches of the display to find their target letter. Those children with comorbid ADHD and ANX were less likely to be diagnosed as conduct disorder (CD) than ADHD-only group, though there was no difference between the groups in the prevalence of oppositional defiant disorder (ODD). Children with ADHD and ANX underwent a double-blind placebo-controlled stimulant trial. Those subjects with ADHD alone had a much more robust response to stimulants than the comorbid group. This was found both in terms of teacher ratings on the Iowa CTRS and observation room ratings of ADHD behavior during an academic task. The two ADHD subgroups were not compared with control subjects in this study, and no structured interview was used to establish the diagnoses. Livingston et al. (1990) found that about 40% of clinic referred children with ADD meet concurrent criteria for an anxiety or mood disorder as assessed by the child's report on the Diagnostic Interview for Children and Adolescents (Herjanic and Reich, 1982). ADD boys with a concurrent anxiety or mood disorder had lower verbal IQs and arithmetic scores than those without a mood disorder. Parents of boys with ADD and an anxiety/mood disorder rated them as having more severe problems on both the internalizing and externalizing sections of the Child Behavior Checklist. In contrast to the results of Pliszka (1989), teachers in this study rated ADD boys with anxiety/mood disorders as more inattentive, hyperactive, and aggressive than those with ADD alone. Those with a comorbid ADD and anxiety/mood
197
PLISZKA
disorder performed poorer on the Coding subtest of Weschler Intelligence Scale for Children Revised, as well as on the Trail Making Test. The comorbid group did not differ from those ADD children without an anxiety/mood disorder on the Gordon Differential Reinforcement of Low Response Rates, a putative measure of impulsivity. The studies of Pliszka (1989) and Livingston et al. (1990) both suggest that ADHD children with internalizing diagnoses differ from those with ADHD alone, though in opposite ways. The study by Pliszka (1989) suggests that the comorbid group is less impulsive and hyperactive than those with ADHD alone, whereas the findings of Livingston et al. (1990) seem to indicate that the comorbid group may be more impaired in terms of impulsivity, inattention, and aggression than the ADHD-only group. It should be noted, however, that in the Livingston et al. (1990) study the comorbid group consisted of ADHD children with both ANX and separation anxiety, as well as those with depressive disorders. Thus, some of the differences could be attributed to the subject heterogeneity. It is likely, for instance, that children with separation anxiety who actively resisted being in the classroom would be perceived as more deviant by teachers than children with ADHD alone. The study by Pliszka (1989) did not contain any subjects with separation anxiety. Interesting information regarding the relationship of ADD and anxiety emerged from a family study of both disorders (Biederman et aI., 1991b). The authors examined the prevalence of ADD and anxiety disorders among the first degree relatives of 73 clinic children with ADD, 30% of whom concurrently met criteria for an anxiety disorder. The prevalence of ADD and anxiety was also examined in the relatives of a control population. Relatives of ADD children had an increased risk of ADD themselves, regardless of whether the ADD proband had anxiety or not. Relatives of ADD children without anxiety had an increased risk of anxiety disorders (adult or child) compared with controls, but the relatives of ADD children with anxiety showed an even higher prevalence of anxiety disorders. When the analysis was restricted to childhood anxiety disorders, only those probands with ADD and an anxiety disorder had an increased prevalence of anxiety among their relatives. The rate of anxiety among relatives of ADD-only probands was not increased over that of relatives of controls. The authors suggested their data was most consistent with one of two hypotheses: (1) ADD with anxiety and ADD are etiologically distinct, or (2) ADD and ADD with anxiety share familial etiological factors, but more are needed to manifest ADD with anxiety. Thus, three studies suggest that children with ADHD and comorbid anxiety differ from those with ADHD alone, both clinically and with regard to possible etiological factors. The results of Pliszka (1989) suggested that the ADHD-only group was more impaired on measures of impulsivity and hyperactivity. This study further explores this issue by comparing children with ADHD alone with children with ADHD and a comorbid overanxious disorder (ADHD/ANX) and a control group on a number of clinical and laboratory measures. It was hypothesized that consistent with Pliszka
198
(1989), the ADHD/ANX groups would be less impaired on laboratory measures of impulsivity and hyperactivity, and they would show fewer symptoms of conduct disorder as rated by parents and teachers. Method Subjects and Diagnostic Interviews
ADHD subjects (aged 6-12) presented to a university affiliated child mental health clinic. They were referred for inattentive, impulsive, hyperactive, or oppositional behavior at home or school. They underwent psychiatric examination using a structured interview device that covered ADHD, ODD, and CD symptoms (Swanson et aI., 1991). The author spent 2 weeks observing the use of the interview. Because the above interview does not cover internalizing diagnoses, items were added from DSM-III-R covering the areas of major depression, dysthymia, and ANX. The parent was first interviewed alone, and the diagnostic categories of ADHD, ODD, CD, major depression, and ANX were covered. Next, the child was interviewed, but the child was not questioned about externalizing symptoms, as the child interview seemed to add little in terms of these areas. After establishing rapport with the child, the interviewer questioned the child about internalizing symptoms. The type of questions asked to establish the presence or absence of the seven individual items in the DSM-III-R criteria for ANX are shown in the Appendix. For each of the seven items, a number of probes were asked. If the parent or child responded that the subject experienced at least one particular probe "a lot," then the DSMIII-R item was scored as present. The interviewer could inquire of the child his/her meaning of the term "a lot" to ascertain that the child understood that it meant frequently, that is, nearly every day. The items were constructed to tap into anxiety and not simply fear of punishment for misbehavior. The number of symptoms in the areas of ADHD, ODD, and CD on the parent interview were tallied, as were the number of overanxious disorder symptoms (0-7) reported separately on the parent and child interview. Interrater reliability data for this interview are not available as yet. Subjects were seen at the clinic from June 1989 to March 1991. The subjects were seen by the author or by psychiatric residents trained to use the interview. Generally three to lO children were evaluated each week. Subjects were entered into the data base if they met eight of the 14 DSM-III-R criteria for ADHD on the parent interview; this yielded 107 ADHD subjects. All subjects were free of medication and any concurrent medical illness at the time of assessment. The child's classroom teacher'filled out the Iowa CTRS (Loney and Milich, 1982). This is a lO-item scale on which the teacher rates the child from "not at all" to "very much" on a four-point scale for each item. The first five items comprise the inattention/overactivity factor, whereas the second five items make up the aggression factor. Each factor yields a score from 0 to 3. Each child filled out the Revised Children's Manifest Anxiety Scale (RCMAS) (Reynolds and Paget, 1983). This is a 38-item scale consisting of items to which the child answers "yes" or "no." Nine of the J. Am. Acad. Child Adolesc. Psychiatry, 31:2, March 1992
ATIENTION DEFICIT AND ANXIETY
items are "lie" items; thus, the total anxiety symptoms can range from 0 to 29. Each item was read to the child and his response was recorded by the observer. Thus, differences in reading ability should not have had any effect on the child's capacity to understand the instrument. The RCMAS was obtained independently of the structured interview. Twelve normal controls (aged 6-12) were recruited from a local private school but did not undergo the structured interview. Recruitment of controls took place during the school year, and testing of controls was done on Saturday morning. There was no staff available to do the structured interview on Saturday, and generally parents of controls did not want to take their children out of school during the week to undergo the structured interview. As a compromise, rating scales were used to ensure control subjects did not show elevated levels of disruptive behavior or anxiety. Controls could be no more than one standard deviation above the mean for his or her age on either factor of the Iowa CTRS or on the RCMAS. The parent filled out the Swanson, Nolan, and Pelham Rating Scale (SNAP-R) (Pelham et aI., 1981), a DSM-III/III-R behavior checklist, and the child was administered the RCMAS. The child was required to be no more than one standard deviation above the mean for his or her age on the Iowa CTRS or the RCMAS. The SNAP-R is a revised version of the SNAP (Pelham et aI., 1981). It contains items related to the DSM-III and DSM-III-R diagnoses of ADD, ADHD, ODD, and CD, as well as items related to cognitive tempo. The author added items from DSM-III-R pertaining to major depression and ANX. The parent rates the child on a four-point scale ranging from "not at all" to "very much" on each item. The controls could not exceed one standard deviation above the mean for those factors on which normative data are available. For the internalizing items, for which there is no normative data, a control could not have any depressive or anxiety symptom checked as occurring more often than "a little" by the parent. All controls were in regular classes and had no history of psychiatric treatment or special education. Observation Room Task The child was placed in an observation room with a oneway mirror where he performed arithmetic problems (set at his or her own grade level) for 15 minutes. The observer rated the following behaviors according to the method described by Barkley (1987): off-task, fidgeting, vocalizes, plays with objects, and out of seat. Off-task behavior was defined as breaking eye contact with the worksheet for greater than 3 seconds. A fidget was defined as a motor movement that resulted in a change in the position of the trunk or legs. Hence, simple foot tapping or leg vibration was not coded as a fidget. A vocalization was defined as any audible sound other than a cough or sneeze. The 15minute period was divided into thirty 30-second intervals; the end of each interval was signaled to the observer by means of a tape recorder. If one of the five behaviors occurred during the 30-second interval, the observer recorded it; if the behavior occurred multiple times during the interval, it was still only recorded once. A score for each behavior was obtained by summing the number of intervals in which I. Am. Acad. Child Adolesc. Psychiatry, 31:2, March 1992
TABLE 1. Correlations of Measures of Impulsivity, Hyperactivity, and Anxiety (Effect of Age Partialed Out) RCMAS
ANX (Child)
ANX Observation (Parent) INB** Room Ratings
RCMAS 1.00 ANX (child) 0.548* 1.00 ANX (parent) 0.399* 1.00 NS INB** -0.338* -0.314* -0.278* 1.00 Observation Room ratings NS NS NS 0.394*
1.00
Note: RCMAS = Revised Children's Manifest Anxiety Scale, ANX = overanxious disorder, INB = Continuous Performance Test, Inhibition Version. *p < 0.Q1. ** The number of commission errors only (see text).
the behavior occurred, dividing by 30 and expressing this number as a percentage. A total ADHD behavior score was obtained by summing the total number of intervals in which a behavior occurred in all five categories and dividing by 150; this was also expressed as a percentage. Studies have shown reasonable correlations between these scores and parent/teacher ratings of behavior (Barkley, 1991). Continuous Performance Test, Inhibition Version (INB) The version developed by Lindgren and Lyons (1983) was used. The child sits at a monitor that flashes random, differently colored shapes, and he or she must press a space bar after every shape. When a blue square appears on the screen, however, he or she must inhibit his response and not press the space bar. Thus, the task may more directly measure inhibition than the traditional Continuous Performance Test. The child performed one block of four trials. Each trial contained 100 shapes, presented at a fixed interval of 1.5 seconds apart. Twenty of the shapes in each trial were blue squares; thus, the total number of blue squares that had to be avoided was 80. There were 320 other shapes on which the bar had to be pressed; failure to do so resulted in an omission error. Results
In the first step, the relationship between anxiety and impulsivity was examined by correlating five pieces of data that had been independently obtained: (1) the total number of ANX symptoms the child reported on his interview, (2) the number of ANX symptoms reported by the child's parent, (3) the RCMAS, (4) the number of commission errors on the INB task, and (5) the total ADHD behavior during the observation room task. Pearson product moment correlations were used; age was partialed out as a covariate. This analysis was performed only in the ADHD group (N = 105). Data for the INB were lost on two ADHD subjects. The results are shown in Table 1. The number of ANX symptoms reported by the child correlated positively with the RCMAS (r = 0.548, df = 105, p < 0.01), and because these two measures were obtained independently, this suggests the interview was valid for making a diagnosis of ANX. The parent report of ANX
199
PLISZKA
symptoms correlated with the child report of ANX symptoms (r = 0.399, df = 103, p < 0.01), but the parent report of ANX symptoms did not correlate with the RCMAS. The total amount of ADHD behavior shown during the observation room correlated positively with the number of commission errors (r = 0.394, df = 103, p < 0.01). Of most interest, the number of commission errors on the INB (failure to withhold a response to the blue square) correlated negatively with both the RCMAS (r = -0.338, df = 103, p < 0.01) and the number of child reported ANX symptoms (r = -0.314, df = 103, p < 0.01). Commission errors on the INB also correlated negatively with the parent report of ANX symptoms (r = -0.278, df= 103,p < 0.01). Thus, the more anxious the child, the less impulsive he or she appeared, as measured by the INB. To compare the groups categorically, the ADHD group was divided according to the number of overanxious symptoms the child reported. Those with four or more symptoms constituted the comorbid group (ADHDI ANX), whereas those with two or fewer symptoms constituted the ADHDonly group. Those who reported three overanxious symptoms (N = 15) were excluded from the analysis as borderline cases. This resulted in three groups: ADHD (N = 58), ADHD/ANX (N = 34), and controls (CON) (N = 12). Differences between the groups for the Iowa CTRS, RCMAS, and age were analyzed with SYSTAT® using analysis of variance (ANOYA). Multiple comparisons were performed by means of the Tukey HSD test. For the observation room task and INB, age was used as covariate in the ANOYA. Because SYSTAT does not perform the Tukey test when a covariate is included in the analysis, multiple comparisons were done with pairwise T-tests. The a-level was held constant by using the Bonferroni correction. Thus, when the main effect was significant, the comparisons of ADHD versus ADHD/ANX, ADHD/ANX versus CON, and ADHD versus CON were performed. Only if p < 0.016 (0.05 divided by 3, the number of comparisons), was the individual comparison regarded as significant at the 0.05 level. The results are shown in Table 2. The proportion of females was not different in each of the groups (X 2 = 3.69, df = 2, NS). The main effect of clinical group on age was significant, F(2,101) = 5.733, p < 0.001; therefore, age was used as a covariate in the analyses of the observation room and INB data. Multiple comparisons showed that the ADHD/ANX group was older than the ADHD-only group. This older age reflected a later date of referral for the comorbid group. Both the ADHD and ADHD/ANX groups were rated higher than the controls on both the inattention/overactivity factor, F(2,88) = 70.7, P < 0.000 and the aggression factor, F(2,87) = 20.3, P < 0.000, subscales of the Iowa CTRS, but no differences between the ADHD groups emerged. The ADHD/ANX groups rated themselves as more anxious than the other two groups on the RCMAS, F(2,101) = 23.68, p < 0.000. The three groups were significantly different from each other in terms of off-task behavior during the observation room task, F(2,100) = 11.63, p < 0.000. The ADHD group was worse, being off-task an average of 43.8% of the time, whereas the ADHD/ANX group was off-task, on average, 200
about 29% of the time. For fidgeting, the main effect was significant, F(2,100) = 4.14, P < 0.02, but only the ADHD and control groups were significantly different by multiple comparison. For vocalizing, the trend was in the same direction as the finding for off-task behavior, F(2,100) = 4.55, p < 0.02; when multiple comparisons were done, only the difference between the controls and the ADHD group was significant. None of the controls played with objects; therefore, this data was analyzed nonparametrically. If a child played with objects more than twice during the IS-minute task, he was coded as "plays with objects present"; if he did not, the behavior was coded "absent." Forty-one percent of the ADHD group played with objects at least twice, whereas only about 26% of the ADHD/ANX group did so (X 2 = 8.5, df = 2, p < 0.02). As stated, none of the controls played with objects. There was a trend for the ADHD group to get out of their seats more, but the variance for this measure was very large and the difference did not reach significance. When the ADHD behaviors were totaled, all three groups were significantly different from each other, F(2,l00) = 11.95, p < 0.000, with the ADHD group showing the most behaviors, followed by the ADHD/ANX group, whereas the controls showed the least number of ADHD behaviors. The groups were not significantly different in the numbers of omission errors on the INB task; this suggests that the three groups all continued to (monotonously) press the bar equally well throughout the task. In terms of failure to inhibit, however, the ADHD group made significantly more commission errors than the other two groups, which were not different from each other, F(2,99) = 12.06, p < 0.000. The two ADHD groups were then compared with each other in terms of the number of symptoms reported on the structured interview, as shown in Table 3. The ADHD groups were not different from each other in terms of the number of ADHD or ODD symptoms reported by parents, but there was a trend for the ADHD only group to show more conduct disorder symptoms than the ADHD/ANX group, t (90) = 1.748, P = 0.084. Obviously, the groups differed in the number of ANX symptoms the child reported, t (90) = 21.4, P < 0.000, because the groups were classified using this measure. Interestingly, although the groups differed in the number of parent reported ANX symptoms, t (90) = 4.7, P < 0.000, parents tended to under report ANX symptoms relative to those reported by the child. The overlap of parent versus child generated diagnoses is shown in Table 4. Of the 34 subjects who met criteria for ANX according to their own interview, 13 (38.2%) did not meet criteria according to their parent interview, that is, parents tended to underreport their ANX symptoms. On the other hand, if the parent reported that the child did meet criteria for ANX, the child usually met criteria for ANX by their own interview. Thus, using the child interview established that more of the ADHD group (34 of 107) met criteria for ANX than if the parent interview had been used to establish a diagnosis of ANX (23 of 107). Discussion This study is consistent with others (Biederman et a!., 1991b; Livingston et aI., 1990; Pliszka, 1989) in showing J. Am. Acad. Child Adolesc. Psychiatry, 31:2, March 1992
ATIENTION DEFICIT AND ANXIETY TABLE
2. Comparison of Subjects with ADHD, ADHD/ANX, and Controls
ADHD (N Measure Age % Male RCMAS Observation room Off task' Fidgetd
Vocalizedd % Plays w/objects e Out of seat Total ADHD' INB Omissions Commissions Iowa CTRS InattentioniOveractivity Aggression
=
58)
ADHD/ANX (N
X
(SD)
X
7.8 93.1% 10.1
(1.5)
9.0 85.2% 19.2
43.8 55.9 30.7 41.4 10.0 31.1
(6.2)
(29.2) (22.3) (24.4) (17.8) (14.4) (21.2)
=
34)
(SD) (1.71 (6.1 )a
CON (N = 12)
X
(SD)
p
8.4 75% 10.2
(1.5)
0.004 NS 0.000
(7.0)
28.6 55.1 19.3 26.4 5.3 22.8
(20.9) (23.1) (28.0)
5.8 36.3 8.8
(6.1) (17.9) (16.4)
(9.1) (14.1)
0.5 10.3
(1.9) (5.7)
0.000 0.019 0.013 0.014 NS 0.001
(28.7) (15.0)
19.8 35.0
(25.2) (12.2)
NS 0.000
31.1 52.8
(14.8 )a
27.2 36.8
2.4 1.7
(0.57) (0.85)
2.3 1.2
o
(0.5) (0.78)
0.4 0.2
(0.43)b (0.35)b
0.000 0.000
Note: ADHD = attention-deficit hyperactivity disorder, ANX = overanxious disorder, CON = controls, RCMAS = Revised Children's Manifest Anxiety Scale, INB = Continuous Performance Test, Inhibitor Version, CTRS = Conners Teacher Rating Scale. a This group significantly higher than the other two groups by multiple comparison, p < 0.05. b This group significantly lower than the other two groups by multiple comparison, p < 0.05. , All three groups significantly different from each other by multiple comparison, p < 0.05. d ADHD group different from Controls only by multiple comparison, p < 0.05. e Groups different by chi-square, df = 2. f ADHD/ANX group different from ADHD group by multiple comparison, p < 0.05.
that ADHD children with a comorbid internalizing disorder differ from those with ADHD alone in significant ways. Both this study and that of Pliszka (1989) suggest that those with ADHD/ANX show lower levels of impulsivity as measured by laboratory tasks than those with ADHD alone, though the current study clearly shows that those with ADHD/ANX are impaired on these measures relative to controls. The current study did not include a group of children with ANX who did not have ADHD. It is important to bear in mind that when Werry et al. (1987) compared children with ADD with controls and those with anxiety disorders (who did not have ADD or CD), no differences were found on laboratory measures of impulsivity, though differences were found with regard to motor restlessness. Child report of ANX symptoms correlated with the independently obtained RCMAS, suggesting that the interview was valid for making the diagnosis of ANX. The RCMAS explained about 30% of the variance of child reported ANX symptoms; thus, there were some children who rated themselves high in ANX on the structured interview, but low on the RCMAS and vice versa. Fewer children met criteria for ANX by parent interview than by child interview. The implications of these findings is that child diagnostic interviews, parent interviews, and child self-report anxiety scales may yield different subgroups, and of course, different findings. At present, we do not know the different correlates of parent reported diagnosis versus child reported diagnosis. In his review of the literature regarding the diagnosis of depression in children, Angold (1988) suggested that parents often underreport depression, relative to the child's report, J. Am. Acad. Child Adolesc. Psychiatry, 31:2, March 1992
leading to a population of children who meet criteria for depression by their own report, but not by parent report. Conversely, it was rare, if a parent did report depression symptoms in their child for the child to then deny depression. A similar pattern was noted in this study for ANX. If a parent noted the presence of ANX symptoms in their child, the child usually reported the symptoms as well, but many parents were unaware of their child's anxiety. This clearly suggests that child and parent interviews have different correlates, and it may be risky to "combine" information from the two interviews to yield a "best estimate" diagnosis until the reasons for this discrepancy are better understood. In terms of presenting symptoms, the ADHD and ADHD/ ANX groups are similar in terms of parent and teacher ratings. Thus, the clinician should not expect the severity of the ADHD symptoms, as related by adults, to be a clue to the comorbidity of ANX. It is likely though, that in the office (for periods up to an hour), the ADHD/ANX child is more likely to perform well on tasks that require inhibition. This phenomena, combined with the child's report of anxiety, might lead a clinician to conclude that the child has ANX and does not have ADHD; the clinician might further conclude the child's inattentive symptoms are "secondary" to the anxiety disorder. If this formulation were correct, that is, if the comorbid group "truly" was a pure anxiety group, then one would not have expected the comorbid group to be at all different from controls on measures of impulsivity and hyperactivity. The comorbid group is, in fact, more impulsive and hyperactive than controls, as noted in Table 2, showing a level of ADHD behaviors that does impair 201
PLISZKA TABLE
Appendix
3. Comparison of Symptoms Reported on Structured Interviews by Parents and Children ADHD
ADHD/ANX (N = 34)
(N = 58)
DSM-III-R Symptoms ADHD ODD Conduct disorder ANX (parent) ANX (child)
Structured Interview Items Used to Establish a Diagnosis of Overanxious (ANX) Disorder
X
(SD)
X
(SD)
p
11.2 4.0 1.8 1.2 0.78
(1.8) (2.8) (1.9)
11.1 4.1 1.1 2.9 4.6
(1.7) (2.2)
NS NS 0.06 0.001 0.001
(1.4)
(.78)
(1.3) (2.1) (0.89)
Note: Controls are not compared here, as they did not undergo the structured interview. ADHD = attention-deficit hyperactivity disorder, ANX = overanxious disorder.
TABLE 4.
Comparison of Overlap between Parent-Generated and Child-Generated Diagnoses Diagnosis by Parent Interview
Diagnosis by child interview
Present Absent Borderline Total
Present
Absent
Borderline
Total
15 5 3 23
13 48
6 5
9 70
3 14
34 58 15 107
their performance. Thus, the clinician should guard against an "either-or" approach to the diagnosis of ADHD and anxiety. As noted in Table 1, there appears to be a modest inverse relationship between anxiety and impulsivity as defined by these laboratory measures. This should be interpreted with caution, as there were no significant correlations between the child's self-rating of anxiety and teacher's rating of inattention and overactivity. If the two ADHD groups had been similar to each other on these measures and equally impaired compared with controls, one could conclude that these diagnoses simply overlap. There appears, however, to be an interaction between anxiety and impulsivity, and the trend for the anxious subjects to have fewer conduct symptoms tends to confirm that anxiety tends to moderate impulsivity. This is an interesting phenomenon that requires further study. Does the development of an anxiety disorder lead to greater inhibition in the ADHD child? If so, how is such an effect mediated? Could the differences found here between the ADHD groups be replicated using observations of actual classroom behavior? If so, why do teachers perceive the two groups as equally inattentive? The study suggests that clinicians should "split rather than lump." Any child presenting with ADHD or ANX needs to be evaluated for the comorbidity of both disorders, and both diagnoses should be made when appropriate. Finally, it is clear that the comorbidity of ANX should be controlled for in studies involving ADHD, as the two groups may have differing etiologies, cognitive styles, life course, and response to treatment (Biederman et aI., 1991a; Pliszka, 1989). 202
1. Excessive or unrealistic worry about future events Do you worry a lot about things that are going to happen, like: a. taking a test in school or getting a report card? b. going to the doctor or dentist? c. meeting new people or going new places? d. playing in a team sport? 2. Excessive or unrealistic worry about past behavior Do you feel that: a. you hurt other people's feelings a lot? b. you let your parents, family, or friends down? c. something you did caused something really bad to happen? 3. Excessive or unrealistic concern about competence Do you think that you're: a. not very good at school work? b. not very good at sports or games? c. Do you dislike the way you look? 4. Somatic complaints Do you get stomachaches, headaches, or other pains from being scared, nervous, or worried? 5. Marked self-consciousness a. Do you get embarrassed easily if you have to do things in front of people? b. Do you feel other people are looking at you and saying bad things about you? 6. Excessive need for reassurance about a variety of concerns a. Do you worry about bad things happening to your family or friends? b. Do you worry about dying or getting sick? c. Do you worry about kidnappers or burglars? d. Do you worry that other kids don't like you? e. Are you afraid of the dark? 7. Marked feelings of tenseness or inability to relax a. Does your stomach do flip flops a lot? b. Does your heart beat fast even when you're not running or playing hard? c. Do worries or scary feelings keep you from resting or sleeping?
The child and parent were interviewed separately, each was asked to state whether each probe occurred "Not at all," "Some," or "A lot." The interviewer could explore the answer to clarify the subject's response. If at least one probe was responded as occurring "a lot," the item was scored as present. I. Am. Acad. Child Adolesc. Psychiatry, 31:2, March 1992
ATIENTION DEFICIT AND ANXIETY
References Anderson, J. C., Williams, S., McGee, R. & Silva, P. A. (1987), DSMIII-R disorders in preadolescent children: prevalence in a large sample from the general population. Arch. Gen. Psychiatry, 44:6976. Angold, A. (1988), Childhood and adolescent depression. II: Research in clinical populations. Br. J. Psychiatry, 153:476-492. Barkley, R. A. (1987), The assessment of attention deficit hyperactivity disorder. Behavioral Assessment, 9:207-233. - - (1991), The ecological validity of laboratory and analogue assessment methods of ADHD symptoms. J. Abnorm. Child Psychol., 19: 149-178. Biederman, J., Newcom, J. & Sprich, S. (199Ia), Comorbidity of attention deficit hyperactivity disorder with conduct, depressive, anxiety and other disorders. Am. J. Psychiatry, 148:564-577. - - Faraone, S. V., Keenan, K., Steingard R. & Tsuang, M. T. (199Ib), Familial association between attention deficit disorder and anxiety disorder. Am. J. Psychiatry, 148:251-256. Bird, H. R., Canino, G. & Rubio-Stipec, M. (1988), Estimates of the prevalence of childhood maladjustment in a community survey in Puerto Rico. Arch. Gen. Psychiatry, 45:1120-1126. Herjanic, B. & Reich, W. (1982), Development of a structured psychiatric interview for children: agreement between child and parent on individual symptoms. J. Abnorm. Child Psychol., 10:307-324. Lindgren, S. & Lyons, D. (1983), Pediatric assessment of cognitive efficiency (PACE). Iowa City: University of Iowa.
Livingston, R. L., Dykman, R. A. & Ackerman, P. T. (1990), The frequency and significance of additional self reported psychiatric diagnoses in children with attention deficit disorder. J. Abnorm. Child Psychol., 18:465-478. Loney, J. & Milich, R. (1982), Hyperactivity, inattention, and aggression in clinical practice. In: Advances in Behavioral Pediatrics, Vol. 2, ed. M. Wolraich & D. K. Routh. Greenwich, CT: JAI Press, pp. 113-145. Pelham, W. E., Atkins, M. S., Murphy, H. A. & White, K. S. (1981), Operationalization and validation of attention deficit disorders. Paper presented at the annual meeting of the Association for the Advancement of Behavior Therapy, Toronto, Ontario, Canada. Pliszka, S. R. (1989), Effect of anxiety on cognition, behavior, and stimulant response in ADHD. J. Am. Acad. Child Adolesc. Psychiatry, 28:882-887. Reynolds, C. R. & Paget, K. D. (1983), National normative and reliability data for the Revised Children's Manifest Anxiety Scale. School Psychological Review, 12:324-336. Strauss, C. C., Lease, C. A., Last, C. G. & Francis, G. (1988), Overanxious disorder, an examination of developmental differences. J. Abnorm. Child Psychol., 16:433-443. Swanson, J. M., Posner, M., Potkin, S. et al. (1991), Activating tasks for the study of visual spatial attention in ADHD children: a cognitive anatomic approach. J. Child Neurol. 6:S119-S127. Werry, J. S., Elkind, G. S. & Reeves, J. C. (1987), Attention deficit, conduct, oppositional, and anxiety disorders in children. III. Laboratory differences. J. Abnorm. Child Psychol., 15:409-428.
From Pediatrics Normative Sexual Behavior in Children. William N. Freidrich, Ph.D., Patricia Grambsch, Ph.D., Daniel Broughton, M.D., James Kuiper, and Robert L. Beilke, Ph.D. Abstract. A large-scale, community-based survey was done to assess the frequency of a wide variety of sexual behaviors in normal preadolescent children and to measure the relationship of those behaviors to age, gender, and socioeconomic and family variables. A sample of 8802- through 12-year-old children screened to exclude those with a history of sexual abuse were rated by their mothers using several questionnaire measures. The frequency of different behaviors varied widely, with more aggressive sexual behaviors and behaviors imitative of adults being rare. Older children (both boys and girls) were less sexual than younger children. Sexuality was found to be related to the level of general behavior problems, as measured by the Achenbach Internalizing and Externalizing T scores and to a measure of family nudity. It was not related to socieconomic variables. Pediatrics 1991;88:456-464.
J. Am. Acad. Child Adolesc. Psychiatry, 3 I: 2, March 1992
203
Accepted September 20, 1991. Dr. Pliszka is Assistant Professor of Psychiatry at The University of Texas Health Science Center at San Antonio. This work was supported by Grant 1 K11 MH00731 from the National1nstitute of Mental Health. Request reprints from Dr. Pliszka, Department of Psychiatry, The University ofTexas Health Science Center at San Antonio, 7703 Floyd Curl Drive, San Antonio, Texas 78284-7792. 0890-8567/92/3102--0 197$03.0010© 1992 by the American Academy of Child and Adolescent Psychiatry. J. Am. Acad. Child Adolesc. Psychiatry, 31:2, March 1992
the ADHD syndrome. If a child simply sits quietly daydreaming and working very slowly, he is not rated as offtask unless he makes a motor movement-i.e., breaking eye contact with the paper. The groups performed a selective attention task in which the child had to memorize four letters on a computer screen and then search a series of displays to determine whether one of the letters they memorized was present. The comorbid group showed slower reaction times and greater accuracy relative to the ADHD-only group as the display became more complex. Interestingly, the ADHDonly subjects began responding faster (more impulsively) as the display become more complex. The comorbid group was able to tolerate longer searches of the display to find their target letter. Those children with comorbid ADHD and ANX were less likely to be diagnosed as conduct disorder (CD) than ADHD-only group, though there was no difference between the groups in the prevalence of oppositional defiant disorder (ODD). Children with ADHD and ANX underwent a double-blind placebo-controlled stimulant trial. Those subjects with ADHD alone had a much more robust response to stimulants than the comorbid group. This was found both in terms of teacher ratings on the Iowa CTRS and observation room ratings of ADHD behavior during an academic task. The two ADHD subgroups were not compared with control subjects in this study, and no structured interview was used to establish the diagnoses. Livingston et al. (1990) found that about 40% of clinic referred children with ADD meet concurrent criteria for an anxiety or mood disorder as assessed by the child's report on the Diagnostic Interview for Children and Adolescents (Herjanic and Reich, 1982). ADD boys with a concurrent anxiety or mood disorder had lower verbal IQs and arithmetic scores than those without a mood disorder. Parents of boys with ADD and an anxiety/mood disorder rated them as having more severe problems on both the internalizing and externalizing sections of the Child Behavior Checklist. In contrast to the results of Pliszka (1989), teachers in this study rated ADD boys with anxiety/mood disorders as more inattentive, hyperactive, and aggressive than those with ADD alone. Those with a comorbid ADD and anxiety/mood
197
PLISZKA
disorder performed poorer on the Coding subtest of Weschler Intelligence Scale for Children Revised, as well as on the Trail Making Test. The comorbid group did not differ from those ADD children without an anxiety/mood disorder on the Gordon Differential Reinforcement of Low Response Rates, a putative measure of impulsivity. The studies of Pliszka (1989) and Livingston et al. (1990) both suggest that ADHD children with internalizing diagnoses differ from those with ADHD alone, though in opposite ways. The study by Pliszka (1989) suggests that the comorbid group is less impulsive and hyperactive than those with ADHD alone, whereas the findings of Livingston et al. (1990) seem to indicate that the comorbid group may be more impaired in terms of impulsivity, inattention, and aggression than the ADHD-only group. It should be noted, however, that in the Livingston et al. (1990) study the comorbid group consisted of ADHD children with both ANX and separation anxiety, as well as those with depressive disorders. Thus, some of the differences could be attributed to the subject heterogeneity. It is likely, for instance, that children with separation anxiety who actively resisted being in the classroom would be perceived as more deviant by teachers than children with ADHD alone. The study by Pliszka (1989) did not contain any subjects with separation anxiety. Interesting information regarding the relationship of ADD and anxiety emerged from a family study of both disorders (Biederman et aI., 1991b). The authors examined the prevalence of ADD and anxiety disorders among the first degree relatives of 73 clinic children with ADD, 30% of whom concurrently met criteria for an anxiety disorder. The prevalence of ADD and anxiety was also examined in the relatives of a control population. Relatives of ADD children had an increased risk of ADD themselves, regardless of whether the ADD proband had anxiety or not. Relatives of ADD children without anxiety had an increased risk of anxiety disorders (adult or child) compared with controls, but the relatives of ADD children with anxiety showed an even higher prevalence of anxiety disorders. When the analysis was restricted to childhood anxiety disorders, only those probands with ADD and an anxiety disorder had an increased prevalence of anxiety among their relatives. The rate of anxiety among relatives of ADD-only probands was not increased over that of relatives of controls. The authors suggested their data was most consistent with one of two hypotheses: (1) ADD with anxiety and ADD are etiologically distinct, or (2) ADD and ADD with anxiety share familial etiological factors, but more are needed to manifest ADD with anxiety. Thus, three studies suggest that children with ADHD and comorbid anxiety differ from those with ADHD alone, both clinically and with regard to possible etiological factors. The results of Pliszka (1989) suggested that the ADHD-only group was more impaired on measures of impulsivity and hyperactivity. This study further explores this issue by comparing children with ADHD alone with children with ADHD and a comorbid overanxious disorder (ADHD/ANX) and a control group on a number of clinical and laboratory measures. It was hypothesized that consistent with Pliszka
198
(1989), the ADHD/ANX groups would be less impaired on laboratory measures of impulsivity and hyperactivity, and they would show fewer symptoms of conduct disorder as rated by parents and teachers. Method Subjects and Diagnostic Interviews
ADHD subjects (aged 6-12) presented to a university affiliated child mental health clinic. They were referred for inattentive, impulsive, hyperactive, or oppositional behavior at home or school. They underwent psychiatric examination using a structured interview device that covered ADHD, ODD, and CD symptoms (Swanson et aI., 1991). The author spent 2 weeks observing the use of the interview. Because the above interview does not cover internalizing diagnoses, items were added from DSM-III-R covering the areas of major depression, dysthymia, and ANX. The parent was first interviewed alone, and the diagnostic categories of ADHD, ODD, CD, major depression, and ANX were covered. Next, the child was interviewed, but the child was not questioned about externalizing symptoms, as the child interview seemed to add little in terms of these areas. After establishing rapport with the child, the interviewer questioned the child about internalizing symptoms. The type of questions asked to establish the presence or absence of the seven individual items in the DSM-III-R criteria for ANX are shown in the Appendix. For each of the seven items, a number of probes were asked. If the parent or child responded that the subject experienced at least one particular probe "a lot," then the DSMIII-R item was scored as present. The interviewer could inquire of the child his/her meaning of the term "a lot" to ascertain that the child understood that it meant frequently, that is, nearly every day. The items were constructed to tap into anxiety and not simply fear of punishment for misbehavior. The number of symptoms in the areas of ADHD, ODD, and CD on the parent interview were tallied, as were the number of overanxious disorder symptoms (0-7) reported separately on the parent and child interview. Interrater reliability data for this interview are not available as yet. Subjects were seen at the clinic from June 1989 to March 1991. The subjects were seen by the author or by psychiatric residents trained to use the interview. Generally three to lO children were evaluated each week. Subjects were entered into the data base if they met eight of the 14 DSM-III-R criteria for ADHD on the parent interview; this yielded 107 ADHD subjects. All subjects were free of medication and any concurrent medical illness at the time of assessment. The child's classroom teacher'filled out the Iowa CTRS (Loney and Milich, 1982). This is a lO-item scale on which the teacher rates the child from "not at all" to "very much" on a four-point scale for each item. The first five items comprise the inattention/overactivity factor, whereas the second five items make up the aggression factor. Each factor yields a score from 0 to 3. Each child filled out the Revised Children's Manifest Anxiety Scale (RCMAS) (Reynolds and Paget, 1983). This is a 38-item scale consisting of items to which the child answers "yes" or "no." Nine of the J. Am. Acad. Child Adolesc. Psychiatry, 31:2, March 1992
ATIENTION DEFICIT AND ANXIETY
items are "lie" items; thus, the total anxiety symptoms can range from 0 to 29. Each item was read to the child and his response was recorded by the observer. Thus, differences in reading ability should not have had any effect on the child's capacity to understand the instrument. The RCMAS was obtained independently of the structured interview. Twelve normal controls (aged 6-12) were recruited from a local private school but did not undergo the structured interview. Recruitment of controls took place during the school year, and testing of controls was done on Saturday morning. There was no staff available to do the structured interview on Saturday, and generally parents of controls did not want to take their children out of school during the week to undergo the structured interview. As a compromise, rating scales were used to ensure control subjects did not show elevated levels of disruptive behavior or anxiety. Controls could be no more than one standard deviation above the mean for his or her age on either factor of the Iowa CTRS or on the RCMAS. The parent filled out the Swanson, Nolan, and Pelham Rating Scale (SNAP-R) (Pelham et aI., 1981), a DSM-III/III-R behavior checklist, and the child was administered the RCMAS. The child was required to be no more than one standard deviation above the mean for his or her age on the Iowa CTRS or the RCMAS. The SNAP-R is a revised version of the SNAP (Pelham et aI., 1981). It contains items related to the DSM-III and DSM-III-R diagnoses of ADD, ADHD, ODD, and CD, as well as items related to cognitive tempo. The author added items from DSM-III-R pertaining to major depression and ANX. The parent rates the child on a four-point scale ranging from "not at all" to "very much" on each item. The controls could not exceed one standard deviation above the mean for those factors on which normative data are available. For the internalizing items, for which there is no normative data, a control could not have any depressive or anxiety symptom checked as occurring more often than "a little" by the parent. All controls were in regular classes and had no history of psychiatric treatment or special education. Observation Room Task The child was placed in an observation room with a oneway mirror where he performed arithmetic problems (set at his or her own grade level) for 15 minutes. The observer rated the following behaviors according to the method described by Barkley (1987): off-task, fidgeting, vocalizes, plays with objects, and out of seat. Off-task behavior was defined as breaking eye contact with the worksheet for greater than 3 seconds. A fidget was defined as a motor movement that resulted in a change in the position of the trunk or legs. Hence, simple foot tapping or leg vibration was not coded as a fidget. A vocalization was defined as any audible sound other than a cough or sneeze. The 15minute period was divided into thirty 30-second intervals; the end of each interval was signaled to the observer by means of a tape recorder. If one of the five behaviors occurred during the 30-second interval, the observer recorded it; if the behavior occurred multiple times during the interval, it was still only recorded once. A score for each behavior was obtained by summing the number of intervals in which I. Am. Acad. Child Adolesc. Psychiatry, 31:2, March 1992
TABLE 1. Correlations of Measures of Impulsivity, Hyperactivity, and Anxiety (Effect of Age Partialed Out) RCMAS
ANX (Child)
ANX Observation (Parent) INB** Room Ratings
RCMAS 1.00 ANX (child) 0.548* 1.00 ANX (parent) 0.399* 1.00 NS INB** -0.338* -0.314* -0.278* 1.00 Observation Room ratings NS NS NS 0.394*
1.00
Note: RCMAS = Revised Children's Manifest Anxiety Scale, ANX = overanxious disorder, INB = Continuous Performance Test, Inhibition Version. *p < 0.Q1. ** The number of commission errors only (see text).
the behavior occurred, dividing by 30 and expressing this number as a percentage. A total ADHD behavior score was obtained by summing the total number of intervals in which a behavior occurred in all five categories and dividing by 150; this was also expressed as a percentage. Studies have shown reasonable correlations between these scores and parent/teacher ratings of behavior (Barkley, 1991). Continuous Performance Test, Inhibition Version (INB) The version developed by Lindgren and Lyons (1983) was used. The child sits at a monitor that flashes random, differently colored shapes, and he or she must press a space bar after every shape. When a blue square appears on the screen, however, he or she must inhibit his response and not press the space bar. Thus, the task may more directly measure inhibition than the traditional Continuous Performance Test. The child performed one block of four trials. Each trial contained 100 shapes, presented at a fixed interval of 1.5 seconds apart. Twenty of the shapes in each trial were blue squares; thus, the total number of blue squares that had to be avoided was 80. There were 320 other shapes on which the bar had to be pressed; failure to do so resulted in an omission error. Results
In the first step, the relationship between anxiety and impulsivity was examined by correlating five pieces of data that had been independently obtained: (1) the total number of ANX symptoms the child reported on his interview, (2) the number of ANX symptoms reported by the child's parent, (3) the RCMAS, (4) the number of commission errors on the INB task, and (5) the total ADHD behavior during the observation room task. Pearson product moment correlations were used; age was partialed out as a covariate. This analysis was performed only in the ADHD group (N = 105). Data for the INB were lost on two ADHD subjects. The results are shown in Table 1. The number of ANX symptoms reported by the child correlated positively with the RCMAS (r = 0.548, df = 105, p < 0.01), and because these two measures were obtained independently, this suggests the interview was valid for making a diagnosis of ANX. The parent report of ANX
199
PLISZKA
symptoms correlated with the child report of ANX symptoms (r = 0.399, df = 103, p < 0.01), but the parent report of ANX symptoms did not correlate with the RCMAS. The total amount of ADHD behavior shown during the observation room correlated positively with the number of commission errors (r = 0.394, df = 103, p < 0.01). Of most interest, the number of commission errors on the INB (failure to withhold a response to the blue square) correlated negatively with both the RCMAS (r = -0.338, df = 103, p < 0.01) and the number of child reported ANX symptoms (r = -0.314, df = 103, p < 0.01). Commission errors on the INB also correlated negatively with the parent report of ANX symptoms (r = -0.278, df= 103,p < 0.01). Thus, the more anxious the child, the less impulsive he or she appeared, as measured by the INB. To compare the groups categorically, the ADHD group was divided according to the number of overanxious symptoms the child reported. Those with four or more symptoms constituted the comorbid group (ADHDI ANX), whereas those with two or fewer symptoms constituted the ADHDonly group. Those who reported three overanxious symptoms (N = 15) were excluded from the analysis as borderline cases. This resulted in three groups: ADHD (N = 58), ADHD/ANX (N = 34), and controls (CON) (N = 12). Differences between the groups for the Iowa CTRS, RCMAS, and age were analyzed with SYSTAT® using analysis of variance (ANOYA). Multiple comparisons were performed by means of the Tukey HSD test. For the observation room task and INB, age was used as covariate in the ANOYA. Because SYSTAT does not perform the Tukey test when a covariate is included in the analysis, multiple comparisons were done with pairwise T-tests. The a-level was held constant by using the Bonferroni correction. Thus, when the main effect was significant, the comparisons of ADHD versus ADHD/ANX, ADHD/ANX versus CON, and ADHD versus CON were performed. Only if p < 0.016 (0.05 divided by 3, the number of comparisons), was the individual comparison regarded as significant at the 0.05 level. The results are shown in Table 2. The proportion of females was not different in each of the groups (X 2 = 3.69, df = 2, NS). The main effect of clinical group on age was significant, F(2,101) = 5.733, p < 0.001; therefore, age was used as a covariate in the analyses of the observation room and INB data. Multiple comparisons showed that the ADHD/ANX group was older than the ADHD-only group. This older age reflected a later date of referral for the comorbid group. Both the ADHD and ADHD/ANX groups were rated higher than the controls on both the inattention/overactivity factor, F(2,88) = 70.7, P < 0.000 and the aggression factor, F(2,87) = 20.3, P < 0.000, subscales of the Iowa CTRS, but no differences between the ADHD groups emerged. The ADHD/ANX groups rated themselves as more anxious than the other two groups on the RCMAS, F(2,101) = 23.68, p < 0.000. The three groups were significantly different from each other in terms of off-task behavior during the observation room task, F(2,100) = 11.63, p < 0.000. The ADHD group was worse, being off-task an average of 43.8% of the time, whereas the ADHD/ANX group was off-task, on average, 200
about 29% of the time. For fidgeting, the main effect was significant, F(2,100) = 4.14, P < 0.02, but only the ADHD and control groups were significantly different by multiple comparison. For vocalizing, the trend was in the same direction as the finding for off-task behavior, F(2,100) = 4.55, p < 0.02; when multiple comparisons were done, only the difference between the controls and the ADHD group was significant. None of the controls played with objects; therefore, this data was analyzed nonparametrically. If a child played with objects more than twice during the IS-minute task, he was coded as "plays with objects present"; if he did not, the behavior was coded "absent." Forty-one percent of the ADHD group played with objects at least twice, whereas only about 26% of the ADHD/ANX group did so (X 2 = 8.5, df = 2, p < 0.02). As stated, none of the controls played with objects. There was a trend for the ADHD group to get out of their seats more, but the variance for this measure was very large and the difference did not reach significance. When the ADHD behaviors were totaled, all three groups were significantly different from each other, F(2,l00) = 11.95, p < 0.000, with the ADHD group showing the most behaviors, followed by the ADHD/ANX group, whereas the controls showed the least number of ADHD behaviors. The groups were not significantly different in the numbers of omission errors on the INB task; this suggests that the three groups all continued to (monotonously) press the bar equally well throughout the task. In terms of failure to inhibit, however, the ADHD group made significantly more commission errors than the other two groups, which were not different from each other, F(2,99) = 12.06, p < 0.000. The two ADHD groups were then compared with each other in terms of the number of symptoms reported on the structured interview, as shown in Table 3. The ADHD groups were not different from each other in terms of the number of ADHD or ODD symptoms reported by parents, but there was a trend for the ADHD only group to show more conduct disorder symptoms than the ADHD/ANX group, t (90) = 1.748, P = 0.084. Obviously, the groups differed in the number of ANX symptoms the child reported, t (90) = 21.4, P < 0.000, because the groups were classified using this measure. Interestingly, although the groups differed in the number of parent reported ANX symptoms, t (90) = 4.7, P < 0.000, parents tended to under report ANX symptoms relative to those reported by the child. The overlap of parent versus child generated diagnoses is shown in Table 4. Of the 34 subjects who met criteria for ANX according to their own interview, 13 (38.2%) did not meet criteria according to their parent interview, that is, parents tended to underreport their ANX symptoms. On the other hand, if the parent reported that the child did meet criteria for ANX, the child usually met criteria for ANX by their own interview. Thus, using the child interview established that more of the ADHD group (34 of 107) met criteria for ANX than if the parent interview had been used to establish a diagnosis of ANX (23 of 107). Discussion This study is consistent with others (Biederman et a!., 1991b; Livingston et aI., 1990; Pliszka, 1989) in showing J. Am. Acad. Child Adolesc. Psychiatry, 31:2, March 1992
ATIENTION DEFICIT AND ANXIETY TABLE
2. Comparison of Subjects with ADHD, ADHD/ANX, and Controls
ADHD (N Measure Age % Male RCMAS Observation room Off task' Fidgetd
Vocalizedd % Plays w/objects e Out of seat Total ADHD' INB Omissions Commissions Iowa CTRS InattentioniOveractivity Aggression
=
58)
ADHD/ANX (N
X
(SD)
X
7.8 93.1% 10.1
(1.5)
9.0 85.2% 19.2
43.8 55.9 30.7 41.4 10.0 31.1
(6.2)
(29.2) (22.3) (24.4) (17.8) (14.4) (21.2)
=
34)
(SD) (1.71 (6.1 )a
CON (N = 12)
X
(SD)
p
8.4 75% 10.2
(1.5)
0.004 NS 0.000
(7.0)
28.6 55.1 19.3 26.4 5.3 22.8
(20.9) (23.1) (28.0)
5.8 36.3 8.8
(6.1) (17.9) (16.4)
(9.1) (14.1)
0.5 10.3
(1.9) (5.7)
0.000 0.019 0.013 0.014 NS 0.001
(28.7) (15.0)
19.8 35.0
(25.2) (12.2)
NS 0.000
31.1 52.8
(14.8 )a
27.2 36.8
2.4 1.7
(0.57) (0.85)
2.3 1.2
o
(0.5) (0.78)
0.4 0.2
(0.43)b (0.35)b
0.000 0.000
Note: ADHD = attention-deficit hyperactivity disorder, ANX = overanxious disorder, CON = controls, RCMAS = Revised Children's Manifest Anxiety Scale, INB = Continuous Performance Test, Inhibitor Version, CTRS = Conners Teacher Rating Scale. a This group significantly higher than the other two groups by multiple comparison, p < 0.05. b This group significantly lower than the other two groups by multiple comparison, p < 0.05. , All three groups significantly different from each other by multiple comparison, p < 0.05. d ADHD group different from Controls only by multiple comparison, p < 0.05. e Groups different by chi-square, df = 2. f ADHD/ANX group different from ADHD group by multiple comparison, p < 0.05.
that ADHD children with a comorbid internalizing disorder differ from those with ADHD alone in significant ways. Both this study and that of Pliszka (1989) suggest that those with ADHD/ANX show lower levels of impulsivity as measured by laboratory tasks than those with ADHD alone, though the current study clearly shows that those with ADHD/ANX are impaired on these measures relative to controls. The current study did not include a group of children with ANX who did not have ADHD. It is important to bear in mind that when Werry et al. (1987) compared children with ADD with controls and those with anxiety disorders (who did not have ADD or CD), no differences were found on laboratory measures of impulsivity, though differences were found with regard to motor restlessness. Child report of ANX symptoms correlated with the independently obtained RCMAS, suggesting that the interview was valid for making the diagnosis of ANX. The RCMAS explained about 30% of the variance of child reported ANX symptoms; thus, there were some children who rated themselves high in ANX on the structured interview, but low on the RCMAS and vice versa. Fewer children met criteria for ANX by parent interview than by child interview. The implications of these findings is that child diagnostic interviews, parent interviews, and child self-report anxiety scales may yield different subgroups, and of course, different findings. At present, we do not know the different correlates of parent reported diagnosis versus child reported diagnosis. In his review of the literature regarding the diagnosis of depression in children, Angold (1988) suggested that parents often underreport depression, relative to the child's report, J. Am. Acad. Child Adolesc. Psychiatry, 31:2, March 1992
leading to a population of children who meet criteria for depression by their own report, but not by parent report. Conversely, it was rare, if a parent did report depression symptoms in their child for the child to then deny depression. A similar pattern was noted in this study for ANX. If a parent noted the presence of ANX symptoms in their child, the child usually reported the symptoms as well, but many parents were unaware of their child's anxiety. This clearly suggests that child and parent interviews have different correlates, and it may be risky to "combine" information from the two interviews to yield a "best estimate" diagnosis until the reasons for this discrepancy are better understood. In terms of presenting symptoms, the ADHD and ADHD/ ANX groups are similar in terms of parent and teacher ratings. Thus, the clinician should not expect the severity of the ADHD symptoms, as related by adults, to be a clue to the comorbidity of ANX. It is likely though, that in the office (for periods up to an hour), the ADHD/ANX child is more likely to perform well on tasks that require inhibition. This phenomena, combined with the child's report of anxiety, might lead a clinician to conclude that the child has ANX and does not have ADHD; the clinician might further conclude the child's inattentive symptoms are "secondary" to the anxiety disorder. If this formulation were correct, that is, if the comorbid group "truly" was a pure anxiety group, then one would not have expected the comorbid group to be at all different from controls on measures of impulsivity and hyperactivity. The comorbid group is, in fact, more impulsive and hyperactive than controls, as noted in Table 2, showing a level of ADHD behaviors that does impair 201
PLISZKA TABLE
Appendix
3. Comparison of Symptoms Reported on Structured Interviews by Parents and Children ADHD
ADHD/ANX (N = 34)
(N = 58)
DSM-III-R Symptoms ADHD ODD Conduct disorder ANX (parent) ANX (child)
Structured Interview Items Used to Establish a Diagnosis of Overanxious (ANX) Disorder
X
(SD)
X
(SD)
p
11.2 4.0 1.8 1.2 0.78
(1.8) (2.8) (1.9)
11.1 4.1 1.1 2.9 4.6
(1.7) (2.2)
NS NS 0.06 0.001 0.001
(1.4)
(.78)
(1.3) (2.1) (0.89)
Note: Controls are not compared here, as they did not undergo the structured interview. ADHD = attention-deficit hyperactivity disorder, ANX = overanxious disorder.
TABLE 4.
Comparison of Overlap between Parent-Generated and Child-Generated Diagnoses Diagnosis by Parent Interview
Diagnosis by child interview
Present Absent Borderline Total
Present
Absent
Borderline
Total
15 5 3 23
13 48
6 5
9 70
3 14
34 58 15 107
their performance. Thus, the clinician should guard against an "either-or" approach to the diagnosis of ADHD and anxiety. As noted in Table 1, there appears to be a modest inverse relationship between anxiety and impulsivity as defined by these laboratory measures. This should be interpreted with caution, as there were no significant correlations between the child's self-rating of anxiety and teacher's rating of inattention and overactivity. If the two ADHD groups had been similar to each other on these measures and equally impaired compared with controls, one could conclude that these diagnoses simply overlap. There appears, however, to be an interaction between anxiety and impulsivity, and the trend for the anxious subjects to have fewer conduct symptoms tends to confirm that anxiety tends to moderate impulsivity. This is an interesting phenomenon that requires further study. Does the development of an anxiety disorder lead to greater inhibition in the ADHD child? If so, how is such an effect mediated? Could the differences found here between the ADHD groups be replicated using observations of actual classroom behavior? If so, why do teachers perceive the two groups as equally inattentive? The study suggests that clinicians should "split rather than lump." Any child presenting with ADHD or ANX needs to be evaluated for the comorbidity of both disorders, and both diagnoses should be made when appropriate. Finally, it is clear that the comorbidity of ANX should be controlled for in studies involving ADHD, as the two groups may have differing etiologies, cognitive styles, life course, and response to treatment (Biederman et aI., 1991a; Pliszka, 1989). 202
1. Excessive or unrealistic worry about future events Do you worry a lot about things that are going to happen, like: a. taking a test in school or getting a report card? b. going to the doctor or dentist? c. meeting new people or going new places? d. playing in a team sport? 2. Excessive or unrealistic worry about past behavior Do you feel that: a. you hurt other people's feelings a lot? b. you let your parents, family, or friends down? c. something you did caused something really bad to happen? 3. Excessive or unrealistic concern about competence Do you think that you're: a. not very good at school work? b. not very good at sports or games? c. Do you dislike the way you look? 4. Somatic complaints Do you get stomachaches, headaches, or other pains from being scared, nervous, or worried? 5. Marked self-consciousness a. Do you get embarrassed easily if you have to do things in front of people? b. Do you feel other people are looking at you and saying bad things about you? 6. Excessive need for reassurance about a variety of concerns a. Do you worry about bad things happening to your family or friends? b. Do you worry about dying or getting sick? c. Do you worry about kidnappers or burglars? d. Do you worry that other kids don't like you? e. Are you afraid of the dark? 7. Marked feelings of tenseness or inability to relax a. Does your stomach do flip flops a lot? b. Does your heart beat fast even when you're not running or playing hard? c. Do worries or scary feelings keep you from resting or sleeping?
The child and parent were interviewed separately, each was asked to state whether each probe occurred "Not at all," "Some," or "A lot." The interviewer could explore the answer to clarify the subject's response. If at least one probe was responded as occurring "a lot," the item was scored as present. I. Am. Acad. Child Adolesc. Psychiatry, 31:2, March 1992
ATIENTION DEFICIT AND ANXIETY
References Anderson, J. C., Williams, S., McGee, R. & Silva, P. A. (1987), DSMIII-R disorders in preadolescent children: prevalence in a large sample from the general population. Arch. Gen. Psychiatry, 44:6976. Angold, A. (1988), Childhood and adolescent depression. II: Research in clinical populations. Br. J. Psychiatry, 153:476-492. Barkley, R. A. (1987), The assessment of attention deficit hyperactivity disorder. Behavioral Assessment, 9:207-233. - - (1991), The ecological validity of laboratory and analogue assessment methods of ADHD symptoms. J. Abnorm. Child Psychol., 19: 149-178. Biederman, J., Newcom, J. & Sprich, S. (199Ia), Comorbidity of attention deficit hyperactivity disorder with conduct, depressive, anxiety and other disorders. Am. J. Psychiatry, 148:564-577. - - Faraone, S. V., Keenan, K., Steingard R. & Tsuang, M. T. (199Ib), Familial association between attention deficit disorder and anxiety disorder. Am. J. Psychiatry, 148:251-256. Bird, H. R., Canino, G. & Rubio-Stipec, M. (1988), Estimates of the prevalence of childhood maladjustment in a community survey in Puerto Rico. Arch. Gen. Psychiatry, 45:1120-1126. Herjanic, B. & Reich, W. (1982), Development of a structured psychiatric interview for children: agreement between child and parent on individual symptoms. J. Abnorm. Child Psychol., 10:307-324. Lindgren, S. & Lyons, D. (1983), Pediatric assessment of cognitive efficiency (PACE). Iowa City: University of Iowa.
Livingston, R. L., Dykman, R. A. & Ackerman, P. T. (1990), The frequency and significance of additional self reported psychiatric diagnoses in children with attention deficit disorder. J. Abnorm. Child Psychol., 18:465-478. Loney, J. & Milich, R. (1982), Hyperactivity, inattention, and aggression in clinical practice. In: Advances in Behavioral Pediatrics, Vol. 2, ed. M. Wolraich & D. K. Routh. Greenwich, CT: JAI Press, pp. 113-145. Pelham, W. E., Atkins, M. S., Murphy, H. A. & White, K. S. (1981), Operationalization and validation of attention deficit disorders. Paper presented at the annual meeting of the Association for the Advancement of Behavior Therapy, Toronto, Ontario, Canada. Pliszka, S. R. (1989), Effect of anxiety on cognition, behavior, and stimulant response in ADHD. J. Am. Acad. Child Adolesc. Psychiatry, 28:882-887. Reynolds, C. R. & Paget, K. D. (1983), National normative and reliability data for the Revised Children's Manifest Anxiety Scale. School Psychological Review, 12:324-336. Strauss, C. C., Lease, C. A., Last, C. G. & Francis, G. (1988), Overanxious disorder, an examination of developmental differences. J. Abnorm. Child Psychol., 16:433-443. Swanson, J. M., Posner, M., Potkin, S. et al. (1991), Activating tasks for the study of visual spatial attention in ADHD children: a cognitive anatomic approach. J. Child Neurol. 6:S119-S127. Werry, J. S., Elkind, G. S. & Reeves, J. C. (1987), Attention deficit, conduct, oppositional, and anxiety disorders in children. III. Laboratory differences. J. Abnorm. Child Psychol., 15:409-428.
From Pediatrics Normative Sexual Behavior in Children. William N. Freidrich, Ph.D., Patricia Grambsch, Ph.D., Daniel Broughton, M.D., James Kuiper, and Robert L. Beilke, Ph.D. Abstract. A large-scale, community-based survey was done to assess the frequency of a wide variety of sexual behaviors in normal preadolescent children and to measure the relationship of those behaviors to age, gender, and socioeconomic and family variables. A sample of 8802- through 12-year-old children screened to exclude those with a history of sexual abuse were rated by their mothers using several questionnaire measures. The frequency of different behaviors varied widely, with more aggressive sexual behaviors and behaviors imitative of adults being rare. Older children (both boys and girls) were less sexual than younger children. Sexuality was found to be related to the level of general behavior problems, as measured by the Achenbach Internalizing and Externalizing T scores and to a measure of family nudity. It was not related to socieconomic variables. Pediatrics 1991;88:456-464.
J. Am. Acad. Child Adolesc. Psychiatry, 3 I: 2, March 1992
203
