Co-Occurrence of ODD and CD in Preschool Children With Symptoms of ADHD

Abstract

Objective: Patterns of co-occurrence between ADHD, Oppositional Defiant Disorder (ODD), and Conduct Disorder (CD) were examined in a sample of non-referred preschool children. ADHD subtypes and sex differences were also explored. Method: Children aged 3.5 years (n = 1,048) with high scores on ADHD characteristics were recruited from the Norwegian Mother and Child Cohort Study and clinically assessed, including a semi-structured psychiatric interview. Results: In children with ADHD, concurrent ODD was present more often than CD (31% vs. 10%), but having ADHD gave higher increase in the odds of CD than of ODD (ODD: odds ratio [OR] = 6.7, 95% confidence interval [CI] = [4.2, 10.8]; CD: OR = 17.6, 95% CI = [5.9, 52.9]). We found a greater proportion of children having the combined ADHD subtype as well as more severe inattentiveness among children with co-occurring CD compared with ODD. Sex differences were minor. Conclusion: There are important differences in co-occurring patterns of ODD and CD in preschool children with ADHD.

Keywords

ADHD preschool children subtypes sex differences co-occurring symptoms Oppositional Defiant Disorder Conduct Disorder

ADHD is one of the most common mental disorders affecting about 5% of children and adolescents worldwide (Polanczyk, de Lima, Horta, Biederman, & Rohde, 2007). The disorder is associated with increasing rates of comorbidity over the age span (Taurines et al., 2010). Oppositional Defiant Disorder (ODD) and Conduct Disorder (CD) are the most commonly reported co-occurring disorders in school-aged children with ADHD with rates at about 50% and 20%, respectively (Pliszka, 1998). The prevalence of comorbid ODD or CD in clinical preschool samples is similar to those in school-aged children, namely, 50% to 65% with co-occurring ODD and about 20% with co-occurring CD (Kadesjo, Hagglof, Kadesjo, & Gillberg, 2003; Posner et al., 2007; Wilens et al., 2002). In community-based preschool samples the prevalence is lower, with about 20% of children with ADHD having co-occurring ODD and 14% CD (Wichstrom et al., 2011). Although comorbidity of behavior disorders, such as ODD and CD, is reported to be associated with increased severity of ADHD symptoms in school-aged children (Connor & Ford, 2012), this has not been fully investigated in preschool children.

The diagnostic system Diagnostic and Statistical Manual of Mental Disorders (4th ed., text rev.; DSM-IV-TR; American Psychiatric Association [APA], 2000) defines three ADHD subtypes: the inattentive subtype (ADHD-IA), the hyperactive–impulsive subtype (ADHD-HI), and the combined subtype (ADHD-C). In school-aged children, the most common subtypes diagnosed are ADHD-C (~60%) and ADHD-IA (~30%; Ford, Goodman, & Meltzer, 2003). In 4-year-old preschool children with ADHD, however, the most common subtypes are ADHD-HI (~60%) and ADHD-C (~30%; Byrne, Bawden, Beattie, & DeWolfe, 2000; Gadow, Sprafkin, & Nolan, 2001; Gimpel & Kuhn, 2000; Lahey et al., 1998; Wichstrom et al., 2011). In school-aged children with ADHD, the co-occurrence patterns vary between subtypes. ODD and CD show a stronger association with ADHD-HI and ADHD-C than ADHD-IA in both clinical and community samples (Eiraldi, Power, & Nezu, 1997; Willcutt, Pennington, Chhabildas, Friedman, & Alexander, 1999). Some preschool studies have reported a stronger association between ADHD-C and ODD (Kadesjo et al., 2003; Lavigne, Lebailly, Hopkins, Gouze, & Binns, 2009; Nolan, Gadow, & Sprafkin, 2001; Riley et al., 2008), whereas studies addressing relationships between ADHD subtypes and CD in preschoolers are lacking.

A diagnosis of ADHD requires attaining a symptom level above a set cut off values. However, symptoms of hyperactivity, impulsivity, and inattention are not discrete, distinct entities, and a diagnosis may be seen more or less as an entity above a certain cut-off at one extreme on a continuum of severity (Sonuga-Barke, Auerbach, Campbell, Daley, & Thompson, 2005). Thus, a dimensional approach may be an important supplement to the diagnostic categories for the understanding of early patterns of disorders.

In ADHD, there is a male predominance in older children and adolescents, and patterns of comorbidity vary between boys and girls at different ages (Monuteaux, Mick, Faraone, & Biederman, 2010). In primary-school children, boys clearly outnumber girls in ADHD-C, but there are only minor sex differences for ADHD-HI and ADHD-IA (Decker, McIntosh, Kelly, Nicholls, & Dean, 2001). In preschool, the male predominance in ADHD is less pronounced, but some studies report that boys have ADHD-C more often than girls (Egger, Kondo, & Angold, 2006; Gimpel & Kuhn, 2000), whereas some studies from preschool community samples have reported that ADHD and co-occurring behavior disorders are equally common in boys and girls (Nolan et al., 2001; Tandon, Si, & Luby, 2011), others find similar patterns to those observed in older children (Gadow et al., 2001; Wichstrom et al., 2011). This suggests some uncertainty concerning early sex-specific characteristics in the development of ADHD and co-occurring disruptive behaviors. It is plausible that boys with ADHD and co-occurring behavior problems are referred to treatment more often than girls; thus, a sex distribution toward boys in clinical samples may be influenced by referral-biases (Novik et al., 2006). Non-referred study-populations may overcome this problem and should thus be better suited to study sex distribution and differences in ADHD and comorbid disruptive behavior disorders.

The number of studies on early co-occurring patterns of ODD and CD in young children with ADHD is still limited as longitudinal studies often begin in late preschool or early school age (Keenan, Shaw, Walsh, & Delliquadri, 1997). Several preschool studies on this issue have relatively small sample sizes (Keenan et al., 1997; Pierce, Ewing, & Campbell, 1999; Tandon et al., 2011). In addition, some studies consider only co-occurring ODD and not CD, or collapse the two into one disruptive behavior disorder (Bufferd, Dougherty, Carlson, Rose, & Klein, 2012; DuPaul, McGoey, Eckert, & VanBrakle, 2001; Kadesjo et al., 2003; Lavigne et al., 2009; Posner et al., 2007). Finally, some studies have only used checklists and not diagnostic interviews for symptom measures (Gadow & Nolan, 2002; Kadesjo et al., 2003; Lavigne et al., 2009; Nolan et al., 2001). These issues indicate that studies examining preschool children with ADHD and the comorbidity patterns with ODD and CD with recommended clinical instruments are warranted.

The present study aimed to investigate the co-occurrence of ODD and CD in 3-year-old non-referred children with clinical symptoms of ADHD. More specifically, we aimed to answer the following questions:

What is the prevalence of co-occurring ODD and/or CD in children with clinical symptoms of ADHD? What is the risk of ODD or CD in children with ADHD? What are the associations between the numbers of ODD and CD symptoms to the number of ADHD symptoms and to what extent do ODD and CD predict the variance in symptoms of ADHD? Are comorbidity patterns of ODD or CD related to specific subtypes of ADHD? Is the severity of IA and HI symptoms related to certain patterns of co-occurring ODD or CD? Are there sex differences in the prevalence of ADHD, its subtypes, or in the co-occurring patterns of ODD and CD in non-referred young preschoolers?

Method

Participants

All participants were recruited from the Norwegian Mother and Child Cohort Study (MoBa), a population-based prospective birth cohort study of about 107,000 children run by the Norwegian Institute of Public Health (Magnus, Haug, Nystad, & Skjaerven, 2006). To identify a large number of preschoolers who might be at risk of developing ADHD, 3-year-old children whose sum score on 11 questions regarding hyperactivity, impulsivity, and inattention in the 36 months MoBa questionnaire, was above the 90th percentile, were invited to a clinical assessment. Six of these 11 questions were selected from the Child Behavior Checklist (Achenbach, 2000) and 5 questions were from the symptom criteria for ADHD in DSM-IV-TR (APA, 2000). Of the 2,798 invited children 1,048 (37.5%) completed the clinical assessments including diagnostic evaluation. There were no statistically significant differences between participants and invited non-participants regarding background factors and pre-and perinatal risk factors except for a higher level of maternal education in participants. Figure 1 shows enrollment into the present study.

Figure 1.

Enrollment of children into the “preschool ADHD study.”

The children, when aged 36 to 44 months, participated in a 1-day clinical assessment at Oslo University Hospital together with at least one parent. The exclusion criteria were severe medical conditions or high scores on autistic symptoms. One of the parents had to speak Norwegian language.

Measures

One of the parents, most often the mother, was interviewed with “The Preschool Age Psychiatric Assessment” (PAPA; Egger & Angold, 2004). This semi-structured interview provides information about psychiatric symptoms, including frequency, intensity, age of onset, and presence in different settings relevant for preschool children. The task of the interviewer is to ensure that the interviewee understands the questions and that she or he provides clear information concerning the symptom at hand. Interviewers continue to probe until there is enough information to decide whether the symptom is present at pre-specified levels of severity. If so, its onset date is recorded along with its frequency of occurrence and its presence at home and at day care. A 3-month primary period is used as the behavior of preschool children change rapidly in this period (Egger & Angold, 2004).

Diagnoses were generated using algorithms implementing criteria from the DSM-IV-TR (APA, 2000).

According to DSM-IV-TR diagnostic criteria a diagnosis of ADHD requires (criterion A) at least six (of nine) inattentive (ADHD-IA subtype), or six (of nine) hyperactive–impulsive symptoms (ADHD-HI subtype). If both subtypes are present, criteria for the combined subtype (ADHD-C) are met. In addition, symptoms must be maladaptive and inconsistent with developmental level and cause impairment.

At the end of each chapter in PAPA, six functional domains provide information of impairment/impact. Impairment was scored as present when symptoms caused reduced function in two or more of the following functional areas; “relationship with parents and the rest of the family,” “the ability to keep friends,” “academic performance,” “play and leisure activities,” “quality of life,” or “as a burden to the family”(Egger & Angold, 2004; Goodman, 1997). Each subscale of impairment ranged from 0 to 3 and the total impairment score from 0 to 18.

Severity of ADHD was assessed by total symptom counts of HI, IA, and total ADHD symptoms (Connor & Ford, 2012). Each symptom was scored 0 (no), 2 (yes, moderate), 3 (yes, severe). Correlations between the number of symptoms and severity scores were .97 for IA symptoms, .97 for HI symptoms, and .98 for ADHD symptoms, thus, measures of total symptom counts were used as they equated measures of symptom severity.

The DSM-IV-TR diagnostic criteria of ODD and CD include 8 and 15 diagnostic symptoms, respectively. In PAPA, symptoms of ODD are modified by cutpoints based on the top 10% of frequency for preschoolers (Egger et al., 2006). Five diagnostic symptoms for CD were excluded because they are not applicable to preschoolers (“stealing with confrontation,” “forced sexual activity,” “breaking into a house or car,” “running away from home,” and “truancy”). The modified and more age-appropriate criteria include eight symptoms, and have shown moderate validity (Keenan et al., 2007; Egger & Angold, 2004). A DSM-IV-TR diagnosis of ODD requires four or more oppositional symptoms and a diagnosis of CD three or more conduct symptoms, respectively. According to PAPA, symptoms must be present for at least 3 months and cause functional impairment.

The PAPA interviews were performed by trained psychology students and supervised by a clinically trained psychologist or child psychiatrists. An inter-rater reliability check was carried out by a second rater, blind to any knowledge about the child and family, and rescored from audiotapes of 79 randomly selected interviews. The average intraclass correlations (ICC) were .98 for total number of ADHD symptoms, .94 for total impairment score of ADHD, .98 for total number of ODD symptoms, .85 for impairment score of ODD, .91 for total number of CD symptoms, and .99 for impairment score of CD.

Covariates

Covariates included maternal and paternal educational level (socioeconomic status [SES]) obtained from the MoBa questionnaire at 17th gestational week. Information about maternal age at delivery and marital status were obtained from The Norwegian Medical Birth Registry (Magnus, Haug, Nystad, & Skjaerven, 2006). From the neuropsychological assessment performed by a trained psychologist, a short form of Stanford Binet 5th edition provided information about general intellectual functioning (Roid, 2003).

The Regional Ethics Committee and the Norwegian data inspectorate approved the study in 2007. Assessments were carried out according to ethical standards, and principles of the Helsinki declaration were followed. Parents returned a written consent prior to the clinical assessment.

Data Analysis

Maternal, paternal, and offspring characteristics for all participants were compared according to presence of ADHD (yes/no) in the child. We examined statistical differences in background characteristic by independent-sample t tests for continuous measures and Pearson chi-square tests or Fisher’s exact tests for categorical measures. Covariates significantly associated with ADHD were adjusted for in the subsequent multiple regression analyses.

We examined the odds ratios (ORs) of having co-occurring ODD and/or CD in ADHD by binary logistic regression and adjusted for possible confounding by gender, child’s age (months), IQ, maternal age (years), marital status (cohabiting/married or single parent), maternal education (years), and paternal education (years). We examined for possible confounding or interactions between independent variables (i.e., sex, ODD, and CD).

The associations between the numbers of ODD and/or CD symptoms to the numbers of ADHD symptoms were examined by Pearson product–moment correlations and by hierarchical multiple linear regression analyses. There were no statistically significant non-linear relationships of ODD and CD symptoms, nor were there significant interactions between independent variables (i.e., sex, ODD, and CD symptoms) in predicting the number of ADHD symptoms.

Comorbidity patterns of ODD and/or CD across different subtypes were compared by crosstabs and Mantel Haenzel’s ORs were reported. Furthermore, a one-way ANOVA between the groups was conducted to examine the relationship between comorbidity of ODD or CD and the severity of IA and HI symptoms. Participants were divided into four groups: ADHD only, ADHD plus ODD, ADHD plus CD, and ADHD plus ODD plus CD. Post hoc comparisons with Bonferroni correction were used.

Finally, we examined sex distribution and sex differences in ADHD, subtypes of ADHD, and in co-occurring symptom clusters by independent-sample t tests for continuous measures and Pearson chi-square tests or Fisher’s exact tests for categorical measures. All tests were two-tailed.

Results

Prevalence rate of children fulfilling the DSM-IV-TR diagnostic criteria for ADHD was 16% (n = 163). Table 1 shows sample characteristics and the number of symptoms of the 1,048 participating children.

Table 1.

Sample Characteristics of 1,048 Preschool Children in the ADHD Study.

	ADHD (n = 163)	No ADHD (n = 885)	χ²/t test
	n (%)	n (%)	χ²(df)	p
	97 (59.5)	448 (50.6)	4.4 (1)	.04
Sex (boys)	M (SD)	M (SD)	t(df)	p
Age (months)	41.6 (1.3)	41.8 (1.3)	−1.3 (1,044)	.19
IQ	99.5 (9.0)	102.2 (9.2)	−3.3 (1,033)	.001
ADHD symptoms	10.6 (2.8)	3.1 (2.7)	30.5 (1,046)	<.001
IA symptoms	3.8 (2.4)	1.0 (1.3)	14.3 (181)	<.001
HI symptoms	6.8 (1.3)	2.2 (1.9)	38.9 (322)	<.001
ODD symptoms	2.8 (1.9)	1.5 (1.4)	8.3 (198)	<.001
CD symptoms	1.3 (1.3)	0.6 (0.9)	6.8 (186)	<.001
Mothers educational level (years)	14.4 (2.5)	15.4 (2.3)	−4.4 (209)	<.001
Fathers educational level (years)	13.6 (2.9)	14.6 (2.7)	−3.9 (205)	<.001
Mothers age (years)	29.9 (4.4)	30.6 (4.2)	−2.1 (1,045)	.05
	n (%)	n (%)	χ²(df)	p
Civil status (single parent)	9 (5.5)	27 (3.1)	2.53 (1)	.16

Note. ADHD = DSM-IV-TR diagnosis of ADHD; IQ = abbreviated intellectual functioning scores; ADHD symptoms = total number of ADHD symptoms (max. 18); IA symptoms = number of inattentive symptoms (max. 9); HI symptoms = number of hyperactive–impulsive symptoms (max. 9); ODD symptoms = number of Oppositional Defiant Disorder symptoms (max. 8); CD symptoms = number of Conduct Disorder symptoms (max. 8).

Comorbidity of ODD and CD in Children With ADHD

Of children with ADHD, 31% (n = 50) had co-occurring ODD, 10% (n = 17) had co-occurring CD, of whom 3% (n = 5) had both ODD and CD (Figure 1).

Table 2 shows the prevalence, crude-, and adjusted ORs for ODD or CD in children with ADHD in a model including possible confounding of background characteristics (lower educational level of mothers was significantly associated with ADHD, whereas lower maternal age was associated with ODD) and the modifying effect of comorbidity (i.e., interactions). The effect of ADHD was modified by concurrent CD in predicting ODD and by concurrent ODD in predicting CD. Both interactions were negatively directed, which indicated that co-occurrence reduced the odds of ODD and CD, respectively (i.e., the effect of concurrent ADHD and CD was less than the combination of their separate effects in predicting ODD, and likewise, in terms of concurrent ADHD and ODD in predicting CD).

Table 2.

Comorbidity of ODD and CD in Children With ADHD.

	ODD (n = 109)
	% (n)	B	SE	Crude OR	95% CI	B	SE	Adjusted OR^a	95% CI
Sex (boys)	50.5 (55)	−0.1	0.2	0.9	[0.6, 1.4]	−0.2	0.2	0.9	[0.6, 1.3]
ADHD (n = 163)	31 (50)	1.8	0.2	6.2	[4.1, 9.5]	1.9	0.2	6.7	[4.2, 10.8]
CD (n = 30)	12 (13)	2.0	0.4	7.3	[3.5, 15.6]	3.3	0.6	27.7	[8.4, 91.2]
ADHD × Boys						−0.9	0.5	0.4	[0.2, 0.9]
ADHD × CD	4.6 (5)					−3.3	0.8	0.04	[0.01, 0.2]
	CD (n = 30)
	% (n)	B	SE	Crude OR	95% CI	B	SE	Adjusted OR^a	95% CI
Sex (boys)	50 (15)	−0.1	0.4	0.9	[0.5, 1.9]	−0.4	0.4	0.7	[0.3, 1.5]
ADHD (n = 163)	10 (17)	2.1	0.4	7.8	[3.7, 16.4]	2.9	0.6	17.6	[5.9, 52.9]
ODD (n = 109)	43.3 (13)	1.99	0.4	7.3	[3.5, 15.6]	3.4	0.6	29.6	[9.0, 96.9]
ADHD × ODD	16.7 (5)					−3.4	0.8	0.03	[0.01, 0.17]

Note. ODD = Oppositional Defiant Disorder; CD = Conduct Disorder; OR = odds ratio; CI = confidence interval. Children with ADHD + ODD/ADHD + CD (n = 5) are included in both analyses of risk for ODD and CD.

Adjusted for child’s sex, IQ, maternal age, maternal educational level, and interactions between ADHD and ODD/CD.

The Prediction of the Number of ADHD Symptoms by Symptoms of ODD- and CD

Correlations between the number of ADHD symptoms and ODD and CD symptoms, r = .34, p < .0001, and r = .32, p < .0001, respectively. Hierarchical linear regressions were used to assess the ability of ODD and CD symptoms to predict the total number of ADHD symptoms (n = 1,048) after controlling for the influence of background characteristics. In the final model, only sex, maternal age, maternal educational level, ODD, and CD symptoms were statistically significant, with ODD symptoms recoding a higher beta value (β = 0.25, p > .0001) than CD symptoms (β = 0.23, p < .0001). The total variance explained by the model was 19%, F(5, 1006) = 48.52, p < .0001, of which 4.8% was explained by background characteristics, whereas the contribution of ODD and CD symptoms was 14.6%, R² change = .15, F change (2, 1006) = 91.45, p < .0001.

Comorbidity of ODD and CD and the Associations of the ADHD Subtype

Of the 163 children with ADHD, 6% (n = 9) met criteria for ADHD-IA, 72% (n = 117) met criteria for ADHD-HI, and 23% (n = 37) met criteria for ADHD-C. Co-occurring ODD and/or CD was uncommon among children with ADHD-IA (i.e., only one child). Among children with ADHD-HI, 33% (n = 38) had co-occurring ODD: OR = 5.8, 95% confidence interval [CI] = [3.7, 9.2], p < .0001, whereas 8% (n = 9) had co-occurring CD: OR = 3.6, 95% CI = [1.6, 8.1], p = .002. Respective figures for ADHD-C were 30% (n = 11), OR = 3.9, 95% CI = [1.9, 8.2], p < .001 and 19% (n = 7), OR = 10, 95% CI = [4.0, 25.2], p < .0001 (Table 3).

Table 3.

The Association Between the Number of ODD and CD Symptoms to the Number of ADHD Symptoms.

	Number of ADHD symptoms^a
n = 1,048	B	SE	β	p
Constant	7.14	0.99		<.001
Sex (boys)	0.60	0.22	.08	.007
ODD symptoms	0.61	0.08	.25	<.001
CD symptoms	0.89	0.12	.23	<.001

Note. n = 1,048. ODD = Oppositional Defiant Disorder; CD = Conduct Disorder.

Adjusted for child’s sex, IQ, maternal age, maternal education, and symptoms of ODD/CD.

Severity of IA and HI Symptoms in ADHD and Co-Occurring ODD and/or CD

Severity of IA and HI symptoms for children with ADHD only, children with ADHD and co-occurring ODD and/or CD was further examined by one-way ANOVA between the groups (Figure 2). There were no statistical significant differences between the four groups according to the number of HI symptoms: ADHD only (M = 6.6, SD = 1.2), ADHD + ODD (M = 7.2, SD = 1.1), ADHD + CD (M = 6.7, SD = 2.2), ADHD + ODD + CD (M = 7.6, SD = 0.6). However, there was a statistically significant difference among the groups for IA symptoms, F(4, 1043) = 112, p < .0001. Post hoc comparisons showed that mean scores of IA symptoms were significantly higher in children with “ADHD and CD” (M = 5.0, SD = 2.9) compared with children with “ADHD and ODD” (M = 3.5, SD = 2.4) and “ADHD only” (M = 3.7, SD = 2.3), but there were no differences among children with ADHD alone, ADHD and ODD, or children with all three disorders.

Figure 2.

Number of IA and HI symptoms according to co-occurrence of ODD and/or CD in children with ADHD.

Sex Differences

There were no statistically significant sex differences among children with ADHD according to the number of IA symptoms, boys M = 3.8, SD = 2.4 versus girls M = 3.8, SD = 2.4, t(161) = −0.03, p = .98, nor in number of HI symptoms, boys M = 6.9, SD = 1.1 versus girls M = 6.7, SD = 1.5, t(107.5) = 1.1, p = .29. More boys than girls had ADHD, ADHD-C, and ADHD alone, but, no there were no sex differences among the diagnostic groups of ODD, CD, or among children with ADHD and co-occurring ODD and/or CD (Table 4).

Table 4.

Sex Differences in ADHD, Its Subtypes and ADHD and Co-Occurring ODD and/or CD.

	Total sample (N = 1,048)		Boys (n = 545)		Girls (n = 503)
	n	%	n	%	n	%	χ²(df)	p
ADHD	163	15.6	97	59.5	66	40.5	4.36 (1)	.04
ADHD-IA	9	0.9	2	22.2	7	77.8	3.23 (1)	.10
ADHD-HI	117	11.2	69	59	48	41	2.56 (1)	.11
ADHD-C	37	3.5	26	70	11	30	5.13 (1)	.02
ADHD only	101	9.6	67	66.3	34	33.7	9.19 (1)	.002
ADHD + ODD	45	4.3	20	44.4	25	55.6	1.08 (1)	.30
ADHD + CD	12	1.1	7	58.3	5	41.7	0.20 (1)	.78
ADHD + ODD + CD	5	0.5	3	60	2	40	0.13 (1)	1.00

Note. ODD = Oppositional Defiant Disorder; CD = Conduct Disorder; ADHD-IA = inattentive subtype; ADHD-HI = hyperactive–impulsive subtype; ADHD-C = combined subtype; ADHD only = ADHD alone; ADHD + ODD = co-occurring ADHD and ODD; ADHD + CD = co-occurring ADHD and CD; ADHD + ODD + CD = co-occurring ADHD and ODD and CD.

Discussion

In a large population-based sample of 3-year-old children with high ADHD characteristics, we found that concurrent ODD and CD shared many of the same features when examined by dimensional measures. Symptoms of ODD and CD did, to almost the same extent, predict the number of ADHD symptoms, but severity of inattentive symptoms was greatest for children with co-occurring CD. Some significant differences which supported distinctiveness also emerged in categorical analysis. Although the proportion of children with co-occurring ODD were greater than for CD, fulfilling DSM-IV diagnostic criteria for ADHD increased the odds of CD more than twice the increase of ODD. While ODD was most strongly associated with the ADHD-HI subtype, the odds of CD were greater than of ODD among children with the ADHD-C subtype. There were no sex differences in numbers of IA or HI symptoms, nor among children with co-occurring ODD or CD. However, the ratio of ADHD in boys versus girls was 1.3 to 1 and for ADHD-C 2.3 to 1.

The comorbidity rates of ODD and CD were about 40% among children fulfilling DSM-IV diagnostic criteria for ADHD in our sample, which is lower than the rates reported in school-aged children of 50% and above (Pliszka, 1998). However, most studies indicate rates of co-occurring ODD 3 times the rates of CD in school-aged children with ADHD (Biederman & Faraone, 2005), which is in line with findings from this preschool sample.

Epidemiological studies indicate that mental disorders co-occur more often than expected by chance (Kessler et al., 1994). There are a number of possible causes of increased rates of comorbidity including shared underlying liability and direct causation (Krueger & Markon, 2006). Early patterns of comorbidity may provide important etiological information. If symptoms of ADHD precede symptoms of ODD, ADHD may be regarded as a risk factor and a predecessor, but if development was simultaneous at an early age, this might point more in the direction of shared etiology or liability (Taurines et al., 2010; Thapar, Harrington, & McGuffin, 2001). In a cross-sectional study, it is not possible to clarify whether ADHD is a predecessor for developing ODD/CD, but findings of these co-occurring patterns at the age of 3.5 indicate an even earlier emergence of comorbidity.

Detecting differences in associations between ADHD and ODD versus ADHD and CD is important to understand the early developmental trajectories of ADHD and comorbidity patterns. Findings from Mannuzza, Klein, Abikoff, and Moulton (2004) indicate that early onset CD among young children with ADHD may predict a persistent pattern of later CD (Mannuzza et al., 2004), and results from genetic studies are compatible with the comorbid variant of ADHD and CD being either a genetically distinct, or a more severe subtype of ADHD (Christiansen et al., 2008; Thapar et al., 2001). We found a higher proportion of children with CD than ODD having the ADHD-C subtype, and more severe inattentiveness among children with CD. Inattentive symptoms have been found to predict a more persistent pattern of ADHD in younger children (Lahey, Pelham, Loney, Lee, & Willcutt, 2005). Following this, our data could imply that early co-occurring CD represents a more severe subtype of ADHD in these young preschoolers, and hence, be in line with reports of increased symptom severity of ADHD in co-occurring CD compared with co-occurring ODD or ADHD alone in school-aged children (Connor & Doerfler, 2008). Combining ODD and CD into one disruptive behavior category, as often is done in preschool studies, may potentially obscure important features of these conditions that could be useful for planning of prevention and early intervention strategies.

Like most large community- and clinical-based preschool studies, the ADHD-HI was the most common, whereas the ADHD-IA subtype was the least common subtype in our study (Byrne et al., 2000; Lahey et al., 1998; Ramelli, Zanda, Bianchetti, & Leoni, 2010; Wichstrom et al., 2011). Actually, ADHD-IA without hyperactivity in this age group appears to be virtually absent in several preschool studies (Byrne et al., 2000; Egger et al., 2006; Lavigne et al., 2009; Posner et al., 2007; Wichstrom et al., 2011), but the ADHD-C subtype is also less commonly observed than in school-aged children. Inattentive symptoms have been found to increase by age (Galera et al., 2011; Levy, Hay, Bennett, & McStephen, 2005) and are also more persistent than HI symptoms during childhood, whereas HI symptoms, however, are reported to decline over time during the preschool period (Lahey et al., 2005). Attention problems might be harder to spot in preschoolers because of modest demands and requests for attention capacity in this age group compared with older children. Alternatively, the capacity for focused attention gradually develops during the preschool period. Findings might point toward DSM-IV diagnostic criteria not being developmentally sensitive enough to effectively capture early significant inattentive symptoms in a manner they are present in preschool children (Chacko, Wakschlag, Hill, Danis, & Espy, 2009). As most IA symptoms focus on school-based tasks in current nosology further efforts are needed in terms of operationalization of more developmentally appropriate symptom measures or, alternatively, to lower the symptom threshold level.

The sex distribution in this non-referred population-based preschool study was less skewed than previously reported for ADHD, with a male–female ratio of 1.3:1 compared with 2:1 reported in earlier preschool studies (Egger & Angold, 2006; Gadow & Nolan, 2002; Gimpel & Kuhn, 2000). The male predominance in ADHD is most pronounced in clinical samples (Egger & Angold, 2006; Lavigne et al., 2009), which may be due to selection and referral bias (Coles, Slavec, Bernstein, & Baroni, 2012).

The bulk of evidence suggests a male predominance in all subtypes, and in co-occurring ODD and CD in preschool children with ADHD in clinical samples (Galera et al., 2011; Nolan et al., 2001), but findings in population-based preschool samples vary (Bufferd et al., 2012; Gadow et al., 2001; Wichstrom et al., 2011). In accordance with other studies (Decker et al., 2001; Gershon, 2002), we found a predominance of boys with ADHD-C, but along the lines of a few previous community-based preschool samples (Nolan et al., 2001; Tandon et al., 2011) and clinical- and community-based studies of school-aged children and adolescents (Biederman et al., 2005; Novik et al., 2006), there were no sex differences in patterns of co-occurring ODD or CD in our sample.

Like most clinical- and community-based preschool samples (Egger et al., 2006; Lahey et al., 2005; Lavigne et al., 2009), we were unable to examine sex differences in ADHD-IA because there were too few cases (in this study, only nine children).

Strengths and Limitations

The present population-based sample of non-referred preschool children with high scores on ADHD symptoms allowed for the study of a relatively large group of children with ADHD with and without comorbid ODD and/or CD. The children were examined using a validated, structured diagnostic interview including detailed information on present psychiatric symptoms. This gave the opportunity to include all ADHD subtypes, which together with the large sample size, allowed for examination of potentially moderating effects of sex, as well as co-occurring ODD/CD.

The study also has some limitations. First, the selection into this study is a two-step process, first to the MoBa, then into the present study. Even though the original cohort of 107,000 is large and recruited broadly from the population, the response rates for both samples were low (Figure 1). The MoBa sample has been shown to be biased compared with the general population with underrepresentation of young mothers, mothers living alone, mothers with more than two children, and mothers smoking during pregnancy (Nilsen et al., 2009). Despite this, no differences were found in exposure-outcome associations between participants in the MoBa and the general population (Nilsen et al., 2009). Furthermore, no differences were found between the MoBa sample and the present sample on the same variables as measured in the Nilsen et al.’s study, except that mothers had slightly higher education among participants in the present study compared with MoBa (Skogan et al., 2014).

Second, the participating children in the present study were selected based on high scores on ADHD symptoms, thus the OR for having ODD or CD in preschool children with ADHD in our study cannot be generalized to clinical or epidemiological samples. Yet, the selection procedure made it possible to study a large number of children presumably with an increased risk for ADHD. Clinical samples are often subject to biases of comorbidity (Berskson’s bias), gender, and severity, thus the present sample may be particularly pertinent for the detection of early precursors of ADHD and comorbidities.

Third, exclusion criteria do not include other major mental health conditions, and we have not excluded children with anxiety, depression, or pediatric bipolar disorder.

Fourth, considering the rapid developmental shifts of cognitive skills and self-regulation of emotions and behavior at this age, narrowly constraining ADHD phenomenology into existing nosology could lead to both over- and under-identification of disorders in these young children (Chacko et al., 2009). The predictive validity of both ADHD, ODD, and CD symptoms is found to be only moderate for preschool children (Keenan et al., 2007; Kim-Cohen et al., 2009; Willcutt et al., 2012), and a further validation of clinical constructs and appropriate criteria for ADHD, ODD, and CD is needed. Thus, our study needs replication and follow-up to confirm a diagnosis and make the distinction between children who will have a persistent symptom pattern and those who will have transient symptoms.

Finally, the symptoms scores were based solely on parents’ ratings, and may introduce parental rating biases. However, the use of a validated structural clinical interview provides information about intensity, duration, and pervasiveness of symptoms in each diagnostic domain, and parents may be the best informants on these issues in early preschool age.

Conclusion

Identification of early co-occurring patterns may increase our understanding of the age- and sex-dependent development of comorbidity in children with ADHD. In this preschool sample, we found that children with ADHD had concurrent ODD more often than CD, but having ADHD increased the odds of CD more than twice the increase of ODD. Children with co-occurring CD had a higher level of IA symptoms compared with children with co-occurring ODD. If we equate early onset CD with severity and more IA symptoms with increased risk of persistence of ADHD, findings might indicate that preschool children with co-occurring ADHD and CD have an increased risk of developing chronic and severe problems.

Clinical Implications

Early identification of ADHD, ODD, and CD in preschool children is challenging since the normal variations in behaviors are immense. However, early identification is a key for altering the developmental course of these disorders.

By using structured clinical assessments, it is possible to identify some significant symptom patterns, alone or in combination, in 3-year-old children. However, the identification of inattentiveness when hyperactive–impulsive symptoms are not present at the same time, clearly represents a major concern that should be recognized and prioritized in research on early identification. We found a significant risk for comorbidity of both ODD and CD among both boys and girls with ADHD. Presence of ADHD predicted CD more strongly than ODD even if concurrent ODD occurred more frequently. Furthermore, a higher proportion of children with CD than those with ODD had ADHD-C. ADHD-C and concurrent early CD might represent a particularly high risk for the development of chronic difficulties in these young children. The distinction between ODD and CD in preschoolers with ADHD should receive attention as these disorders are assumed to have different developmental courses that might require implementation of differentiation of early intervention programs.

Footnotes

Acknowledgements

We are most grateful to children and families in Norway who participate in these ongoing studies. We also want to thank Eili Sponheim, Astrid Aasland, and Anne-Grete Urnes for their contribution in planning this study, and all clinicians and research-assistants for collecting the data; and a special thank you to Eli Nyhus and Line Glemmestad for, in the best possible manner, organizing staff and the participation of the families.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The present study was supported by a grant, no. 39289, from the South Eastern Health Region, funding from the Norwegian Resource Centre for ADHD, Tourettes Syndrome and Narcolepsy, and Oslo University Hospital. Data were drawn from The Norwegian Longitudinal ADHD Study, which was supported by funds and grants from the Norwegian Health Directorate, the Norwegian Ministry of Health, The South Eastern Health Region, G&P Sorensen Fund for Scientific Research, and from the Norwegian Resource Centre for ADHD, Tourettes Syndrome and Narcolepsy. The Norwegian Mother and Child Cohort Study was supported by the Norwegian Ministry of Health and the Ministry of Education and Research, NIH/NIEHS (contract no. NO-ES-75558), NIH/NINDS (grant no. 1 UO1 NS 047537-01), and the Norwegian Research Council/FUGE (grant no. 151918/S10).

Author Biographies

Bothild Bendiksen, MD, is a specialist in child and adolescent psychiatry and a researcher at the Department of Psychiatric Research at Oslo University Hospital. Her research focuses on early risk factors and early identification of ADHD and behavioral disorders (e.g., ODD and CD).

Elisabeth Svensson, PhD, is an epidemiologist at the University of Aarhus, Denmark.

Heidi Aase is a psychologist with a PhD in experimental neuropsychology and ADHD. She is department director at the Norwegian Institute of Public Health, Division of Mental Health, and principal investigator for the Norwegian Longitudinal ADHD Study. Her research interests are within causal factors and developmental trajectories for neurodevelopmental disorders, in particular ADHD.

Ted Reichborn-Kjennerud, MD, PhD, is a professor of psychiatric epidemiology at the University of Oslo and department director at the Norwegian Institute of Public Health, Division of Mental Health. He was one of the founders of the Norwegian Longitudinal ADHD Cohort Study.

Svein Friis, MD, PhD, is a professor of psychiatry at the University of Oslo and researcher at Oslo University Hospital.

Anne M. Myhre, MD, PhD, is an associate professor in child and adolescent psychiatry at the University of Oslo. Her main research interest is neuropsychiatric disorders in child and adolescent psychiatry.

Pål Zeiner, MD, PhD, is a specialist in child and adolescent psychiatry, a researcher at Oslo University Hospital, and a principal investigator for the Norwegian Longitudinal ADHD Study. His main research interest is neuropsychiatric disorders, in particular ADHD.

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