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Conduct behaviors and oppositional defiant behaviors in children and adolescents with ADHD Ahmad Ghanizadeh a 1

Research Center for Psychiatry and Behavioral Sciences, Shiraz University of Medical Sciences, Shiraz, Iran b 2

Department of Psychiatry, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran c 3

Department of Neuroscience, School of Advanced Medical Sciences and Technologies, Shiraz University of Medical Sciences, Shiraz, Iran Published online: 28 May 2015.

Click for updates To cite this article: Ahmad Ghanizadeh (2015) Conduct behaviors and oppositional defiant behaviors in children and adolescents with ADHD, Postgraduate Medicine, 127:3, 289-294 To link to this article: http://dx.doi.org/10.1080/00325481.2015.996434

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http://informahealthcare.com/pgm ISSN: 0032-5481 (print), 1941-9260 (electronic) Postgrad Med, 2015; 127(3): 289–294 DOI: 10.1080/00325481.2015.996434

CLINICAL FEATURE ORIGINAL RESEARCH

Conduct behaviors and oppositional defiant behaviors in children and adolescents with ADHD Ahmad Ghanizadeh1,2,3

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1

Research Center for Psychiatry and Behavioral Sciences, Shiraz University of Medical Sciences, Shiraz, Iran, 2Department of Psychiatry, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran, and 3Department of Neuroscience, School of Advanced Medical Sciences and Technologies, Shiraz University of Medical Sciences, Shiraz, Iran Abstract

Keywords:

There is controversy about the association among attention deficit hyperactivity disorder (ADHD), conduct disorder behaviors, and oppositional defiant behaviors. This study examines whether different subcategories of conduct behaviors co-occur in children with ADHD, and investigates the association of conduct behaviors with ADHD symptoms and oppositional defiant behavior, considering the covariant factors of parental age and educational level. A total of 441 children and adolescents with ADHD participated in this study – 342 (77.6%) boys and 99 girls (22.4%). Their mean age was 9.1 (standard deviation = 2.2) years. They came from families with 1 to 8 children. There were statistically significant correlations among different subcategories of conduct disorder (p < 0.001 for all the correlations). Oppositional behavior scores were associated with all 4 subcategories of conduct behaviors. The severity of hyperactivity/impulsivity was associated with the subcategory of “destruction of property.” The inattentiveness score was associated with “aggression to people and animals.” The current results do not suggest that conduct behaviors exclude oppositional defiant behaviors. The subcategories of conduct behaviors occur in a cluster rather than as a solitary behavior. Larger family size and lower educational level of the father increase the risk of aggression to people and animals in children with ADHD.

Aggression, attention deficit hyperactivity disorder, conduct disorder, oppositional defiant behaviors, parent, sibling

Introduction Attention deficit hyperactivity disorder (ADHD) is one of the most common psychiatric disorders in children and adolescents. The main symptoms of ADHD are inattentiveness, hyperactivity, and impulsivity. The academic success of children with ADHD is highly dependent on their ability to interact with parents, teachers, and other students. More than half of clinical samples of children with ADHD also have oppositional defiant disorder, and 13.6% of them also have conduct disorder [1]. Moreover, the comorbidity of ADHD with disruptive behaviors increases the risk of other behavioral and emotional difficulties [2]. Therefore, their interactions can be problematic.

Conduct disorder behaviors and its subcategories Conduct disorder (CD) entails repetitive and persistent violations of the basic rights of others and of major ageappropriate societal norms or rules [3]. There are four major clinical subcategories of CD: aggression to people and animals, destruction of property, deceitfulness or theft, and serious violations of rules [3].

History Received 22 May 2014 Published online 13 February 2015

Association of conduct disorder and oppositional behavior Oppositional defiant disorder (ODD) is a pattern of negativistic, hostile, and defiant behaviors. An example of an ODD criterion is that the child is often angry and resentful, or the child often loses his or her temper. Anger, bullying, and loss of temper are frequently reported in patients with ODD. There is considerable controversy about the association of ODD with CD. According to the Diagnostic and Statistical Manual of Mental Disorders, fourth edition, text revision (DSM-IV-TR), CD is an exclusion diagnostic criterion to use in making diagnoses of ODD [3]. However, this exclusion criterion for conduct disorder has been removed in the fifth edition (DSM-5). The mild to moderate intensity of oppositional behaviors is more likely to be part of ADHD [4]. However, the moderate to severe intensity of oppositional behaviors is more likely to be a component of CD [4]. Although it is suggested that ODD needs to be considered as a type of ADHD [5], others disagree with this suggestion [6,7]. The ODD behaviors have also been considered as a precursor of CD in children with ADHD [8–10]. This relationship is independent of ADHD

Correspondence: Ahmad Ghanizadeh, MD, Associate Professor of Child and Adolescent Psychiatry, Shiraz University of Medical Sciences, Department of Psychiatry, Hafez Hospital, Siraz, Iran. E-mail: [email protected]; [email protected]  2015 Informa UK, Ltd.

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severity [8]. Moreover, ODD in girls with ADHD leads to a worse outcome in their adolescence [11]. In addition, studies conducted on community samples supported the idea that ODD predicts CD [12]. However, other studies reported that the symptoms of ADHD, ODD, and CD develop in parallel, and ODD symptoms are not a precursor of CD symptoms [13]. Moreover, most children with ADHD and ODD do not progress to CD in the future [10]. Although the social and environmental antecedents of CD and ODD are very similar [14], it is emphasized that ODD and CD are two separate disorders [15].

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Why is it important to assess CD in patients with ADHD? The negative consequences of CD are not limited to the patient’s childhood and adolescence but have an impact on the patient’s adulthood and on society. Antisocial behavior can be an outcome of CD. Conduct behaviors in ADHD predict poorer outcomes. For example, ADHD comorbid with CD predicts later alcohol dependence [16]. Moreover, CD in girls with ADHD is a risk factor for academic, psychiatric, and sexual behavior problems [17]. In addition, CD in inmates of juvenile detention centers is associated with a lower educational and occupational level of the father [18].

Why is it important to study the different subcategories of conduct disorder behaviors? Conduct disorder is a heterogeneous disorder. In contrast with nonaggressive behaviors, aggressive behaviors are related to the age of onset and the subtypes of CD [16]. Therefore, in the current study, the 4 DSM-IV-TR–derived subcategories of conduct behaviors in children and adolescents with ADHD were studied [3]. All of the studies cited above considered CD as an entity. In contrast with previous studies, investigating behavior and DSM-IV criteria lead to considering subsyndromal levels of CD and ODD behaviors. This is very similar to a dimensional approach. For example, it is suggested that more serious physical aggression behaviors are associated with ADHD, whereas deceptive behaviors, such as theft without the presence of physical aggression, is associated with lower levels of ADHD [17]. It is assumed that thought is required for stealing but not for physical aggression, in that a thief needs to search the environment, prepare a plan, and wait for a suitable opportunity [18]. Nevertheless, impulsivity might be associated with theft in ADHD as well. In addition, the nature of conduct behaviors is highly heterogeneous [19]. Some types of conduct behaviors are person-oriented whereas others, such as theft, are property oriented [19]. Furthermore, emotional empathy in children with ADHD– inattentive type is greater than that in boys with ADHD– combined type [20].

Current literature and the present study The controversy about the association of ODD and CD has many factors. For example, age differences in study subjects

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are an explanation for the discrepancies in the results of different studies. The precursor role of ODD in CD may be limited to children aged < 7 years [12,21]. Therefore, a wide age range is included in the current study. Some studies included only boys [10,21] or only girls [11]. Some studies reported that the risk of ODD for the development of CD is limited to only boys [22]. Therefore, both sexes are included in the current study. Another limitation of studies derives from the high comorbidity of ADHD, ODD, and CD [1]. Hyperactive, impulsive, and attention problems are a category that is distinct from conduct problems [23]. Therefore, in order to study the subcategories of CD, ADHD symptoms as covariate factors need to be controlled. In the current study, age, sex, number of siblings, parental educational level, and inattentiveness and hyperactivity scores are considered as covariant factors. I know of no study that investigated the association of ADHD characteristics with the subcategories of CD. It is hypothesized that these subcategories co-occur. Furthermore, it is hypothesized that CD behaviors are associated with oppositional defiant behaviors after controlling for severity of ADHD, age, sex, and parental educational level. Moreover, it is hypothesized that larger family size and lower parental educational level are associated with a higher rate of aggression. No published study has examined these hypotheses.

Method This study is a data reanalysis of a previous study that addressed the association of handedness and ADHD symptoms [24]. This study is approved by ethics committee of Shiraz University of Medical Sciences. The children and adolescents who participated were patients at a child psychiatry clinic affiliated with the university. The study was conducted according to the Good Clinical Practice Guidelines, in accordance with the Declaration of Helsinki 1975, as revised in 2000. The children and their parents provided their assent and written informed consent, respectively. Their participation was voluntary. They had the opportunity to ask questions about any concerns regarding participation. They were assured that their responses would be kept confidential. Participants A total of 441 children and adolescents with ADHD participated in this study. Each participant and one or both parents were interviewed face to face by a board-certified child and adolescent psychiatrist. The DSM-IV diagnostic criteria and the Farsi version of the Kiddie Schedule for Affective Disorders and Schizophrenia for School-Age Children (which has been found to be both valid and reliable, with test–retest and interrater reliability for ADHD of 0.81 and 0.69, respectively) were used to determine if the child met the criteria for a diagnosis of ADHD [25]. Epilepsy, clinically estimated mental retardation, and serious general medical conditions such as thyroid dysfunction were among exclusion criteria.

Behavior in children and adolescents with ADHD

DOI: 10.1080/00325481.2015.996434

Table 1. Basic characteristics of the participants. Variable Number (%) of boys Mean years of age Number of children in the family Mean (SD) age of father Mean (SD) age of mother Father’s mean (SD) years of education Mother’s mean (SD) years of education

342 (77.6%) 9.1 (SD = 2.2) 1 to 8 (mode = 2) 39.3 (5.8) years 33.2 (5.2) years 11.0 (3.8) 11.2 (3.3)

Abbreviation: SD = Standard deviation.

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Symptom measures The screening ADHD, ODD, and CD checklists of Child Symptom Inventory-4 were completed by the parents [26–28]. This instrument has been translated into Farsi, and has been deemed sufficiently reliable and valid [27] to be used in many studies [1,29,30]. The ADHD checklist of this inventory consists of 18 symptoms that meet the diagnostic criteria in DSM-IV; they are categorized into two groups of inattentiveness symptoms and hyperactive/ impulsivity symptoms. Each category consisted of nine symptoms. The responses were given on a Likert scale of 0, never; 1, sometimes; 2, often; and 3, almost always. The range of scoring for each category was from 0 to 3. The internal reliability of this checklist for ADHD–inattentive type, ADHD–hyperactive impulsive type, and ADHD– combined type are 0.81, 0.85, and 0.83, respectively [26]. The ODD and CD checklists include 8 and 14 symptoms from the DSM-IV diagnostic criteria, respectively, with a similar scoring system to that of the ADHD checklist. The CD Checklist has 15 questions in four categories: aggression to people and animals, destruction of property, deceitfulness or theft, and serious violations of rules. The number of questions in each category is 7, 2, 3, and 3, respectively. The ODD checklist has eight questions. Statistical analysis The subcategories of conduct behavior scores were compared for boys and girls using t-tests. The correlation among the subcategory scores of CD and the demographic factors was examined using Pearson correlation analysis. Four linear regression analyses, using the stepwise method, were performed in order to examine the association of the scores of the subcategories of CD with the following independent variables: age, sex, total number of children in the family, father’s educational level and age, mother’s educational level and age, parent-reported inattentiveness score, parent-reported hyperactivity score, and oppositional defiant behavior score.

Results Of the 441 children and adolescents with ADHD, 342 (77.6%) were boys and 99 were girls (22.4%). Their mean age was 9.1 (standard deviation = 2.2) years. The number of children in the family, the father’s and mother’s mean age, and the father’s and mother’s mean educational level are displayed in Table 1.

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The mean and standard deviation of subcategories of conduct disorder are displayed in Table 2. There were statistically significant correlations among different subcategories of conduct disorder (Table 3). Linear regression analysis demonstrated that only ODD score, sex, and hyperactive/impulsive score were associated with the destruction of property subcategory score (Table 4). None of the other variables was statistically associated with this subcategory of score. Linear regression analysis demonstrated that only ODD score, sex, and total number of children in the family were associated with the deceitfulness or theft subcategory score (Table 5). None of the other variables was statistically associated with this subcategory score. As Table 6 demonstrates, only the ODD score was statistically associated with the serious violations of rules subcategory score. The ODD score, total number of children in the family, inattentiveness score, and sex were statistically associated with the subcategory score for aggression to people and animals (Table 7).

Discussion This study examined the association of ODD and ADHD characteristics with CD in children and adolescents with ADHD. It found that the symptoms of CD usually co-occur with oppositional behaviors in children with ADHD. But it is clear that the cause-and-effect relationship cannot be investigated in a cross-sectional study. The current results do not support the idea that conduct behaviors exclude oppositional defiant behaviors. According to DSM-IV-TR, CD is an exclusion diagnostic criterion for the diagnosis of ODD [3]. The current results support the idea that the symptoms of ADHD, ODD, and CD develop in parallel [13], and that there is an overlap between CD and ODD [31]. In addition, ODD behaviors are associated with all 4 subcategories of conduct behaviors. The subcategory of aggression to people and animals as well as the subcategory of deceitfulness and theft are associated with ODD behaviors. Moreover, in contrast with the findings of other reports, person-oriented or property-oriented conduct behaviors are not associated with the ODD score or ADHD severity [18,19]. The current results show that the hyperactivity/impulsivity score is associated with the destruction of property subcategory, whereas the inattentiveness score is associated with the aggression to people or animals subcategory.

Table 2. Mean and standard deviation of subcategories of conduct disorder. Subcategory

Sex

Mean

Standard deviation

Destruction of property

F M F M F M F M

0.2 0.6 0.2 0.6 0.5 .8 2.5 3.6

0.5 1.0 0.5 1.2 1.0 1.3 2.6 3.3

Deceitfulness or theft Serious violations of rules Aggression to people and animal

Significance p < 0.001 p < 0.001 p < 0.02 p < 0.001

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Table 3. Correlation of subcategories of conduct behaviors with demographic characteristics, ADHD severity, and oppositional behaviors.

Age Sex Rank of birth Total number of children in family Handedness Inattention score Hyperactive impulsive score Oppositional defiant behavior score Destruction of property Deceitfulness or theft Serious violations of rules Aggression to people and animal

Inattention score

Hyperactive impulsive score

Oppositional defiant behavior score

Destruction of property

Deceitfulness or theft

Serious violations of rules

Aggression to people and animal

0.151** –0.015 0.073 0.110* –0.013 1 0.294** 0.323** 0.134** 0.140** 0.171** 0.283**

–0.194** –0.088 –0.012 –0.043 –0.025 0.294** 1 0.516** 0.267** 0.220** 0.229** 0.311**

0.116* –0.045 0.017 0.092 0.019 0.323** 0.516** 1 0.317** 0.337** 0.407** 0.491**

–0.021 –0.196** 0.087 0.113* 0.011 0.134** 0.267** 0.317** 1 0.503** 0.491** 0.490**

0.071 –0.151** 0.175** 0.171** –0.034 0.140** 0.220** 0.337** 0.503** 1 0.517** 0.614**

0.083 –0.097* –0.020 0.002 –0.060 0.171** 0.229** 0.407** 0.491** 0.517** 1 0.555**

0.125** –0.140** 0.180** 0.183** 0.009 0.283** 0.311** 0.491** 0.490** 0.614** 0.555** 1

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*p < 0.05. **p < 0.001.

The findings suggest that the factors best associated with conduct behavior symptoms are ODD behaviors and sex. Moreover, age is not associated with the CD behavior score. The association of conduct problems and sex is well known [32]. All three subtypes of conduct behaviors are more likely to occur in boys than in girls. The current results support the idea that the severity of inattentiveness and hyperactivity/impulsivity in children with ADHD is associated with a higher score on some subcategories of conduct behaviors. Other studies reported that there is no direct association between ADHD and criminality [32]. Our results also support the assumption that more serious physical aggression is associated with ADHD severity. Deceptive behaviors such as theft without the presence of physical aggression is associated with lower levels of ADHD [17]. A possible explanation for the inconsistencies among different studies is that conduct behaviors are heterogeneous. For example, some conduct behaviors are highly aggressive whereas others are nonaggressive. The current study distinguished between aggressive and nonaggressive conduct behaviors. Parental educational level was not associated with conduct behaviors except for the subcategory of aggression to people and animals. Children whose father had a lower educational level showed more aggression to people and animals. The father’s and mother’s age was not associated with the conduct behaviors score. It might be assumed that older parents benefit from having more experience in rearing their children. So it might be expected that an older age of the Table 4. Association of independent variables with the subcategory of destruction of property. 95% Confidence interval for odds ratio Variable ODD score Gender Hyperactive impulsive score

Odds ratio

Significance

Lower bound

Upper bound

0.26 –0.17 0.12

0.001 0.001 0.02

0.027 –0.588 0.002

0.063 –0.180 0.035

fathers and mothers is associated with a lower rate of conduct behaviors in their children. But the current results did not support this assumption. There was a significant correlation among the four subcategories of conduct behavior scores, which might indicate that these types of conduct behaviors occur in a cluster rather than as a solitary behavior, and thus clinicians should assess other subcategories of conduct behaviors in ADHD children who are referred with any type of conduct behavior. Although there is considerable clinical and functional neural deficit overlap between CD and ADHD, there are specific functional abnormalities in individuals with CD. For example, a functional magnetic resonance imaging study found a decreased level of emotional processing in the amygdala of children who display antisocial behavior in response to distress cues in others, but not in children with ADHD [33,34]. The rate of disruptive behavior disorders in the siblings of children with ADHD is 30.9% [35]. In addition, the rate of CD in the siblings of children with ADHD is higher than Table 5. Association of independent variables with the subcategory of deceitfulness or theft. 95% Confidence interval for B Variable ODD score Total number of children in family Gender

Odds ratio

Significance

Lower bound

Upper bound

0.34 0.13

0.001 0.003

0.055 0.064

0.095 0.322

–0.12

0.008

–0.607

–0.090

Table 6. Association of independent variables with the subcategory of serious violations of rules. 95% Confidence interval for B Variable

Odds ratio

Significance

Lower bound

Upper bound

ODD score

0.41

0.001

0.077

0.118

Behavior in children and adolescents with ADHD

DOI: 10.1080/00325481.2015.996434

Table 7. Association of independent variables with the subcategory of aggression to people and animals. 95% Confidence interval for B Variable

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ODD score Total number of children in family Father’s educational level Inattention score Sex

Odds ratio

Significance

Lower bound

Upper bound

0.38 0.12

0.000 0.005

0.175 0.143

0.279 0.788

–0.12 0.12 –0.10

0.005 0.007 0.016

–0.170 0.024 –10.427

–0.030 0.145 –0.151

that of healthy children [36]. Genetic factors may be a prime factor in this association. Moreover, the parent–child relationship and sibling relationships in families of children with ADHD are more impaired than in control groups [37]. These impaired relationships may make these children more prone to aggressive behavior. However, the current results did not support this assumption. Current findings need to be considered in the light of some methodological limitations. The study used a clinical sample that cannot be generalized to the general population. Moreover, the participants had a wide age range. But age was not associated with conduct behaviors in children with ADHD. Furthermore, the rate of comorbidities in clinical samples of children with ADHD is very high [1], which may overestimate the association of ODD and CD. It is possible that other factors, such as socioeconomic level, are prime causes of the association of ODD and CD behaviors. In the current study, no formal instrument was used to assess socioeconomic level because there is not a strict relationship between educational level and income in the Iranian culture. Using a formal measure of socioeconomic level might indicate its role in the diversity of patients with conduct behaviors. Our study did make note of the parents’ educational level. Other unmeasured predictors, such as family background, genetic susceptibilities, deviant peer relationships, cognitive ability, child abuse, and family violence, might further reduce this study’s validity. Finally, the only source of information was the parents’ report. Further studies should incorporate multiple informants. Despite these limitations, this study included a large sample of boys and girls with ADHD and with a wide age range. Moreover, the ADHD diagnosis was made using face-to-face interviews by a child and adolescent psychiatrist.

Conclusion Although CD is an exclusion criterion for ODD, the current results demonstrated that there is a positive correlation between ODD and CD symptoms in ADHD. Therefore, children with either ODD or CD symptoms should also be screened for symptoms of the other disorder. This study also demonstrated that these subcategories of conduct behaviors occur concurrently. Thus, all the subcategories should be screened for in patients presenting with one of the subcategories. Finally, this screening should be conducted regardless of ADHD symptom severity.

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Declaration of interest The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending, or royalties.

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Conduct behaviors and oppositional defiant behaviors in children and adolescents with ADHD.

There is controversy about the association among attention deficit hyperactivity disorder (ADHD), conduct disorder behaviors, and oppositional defiant...
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