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Research on Child and Adolescent Psychopathology https://doi.org/10.1007/s10802-020-00713-9

Inhibitory Control Deficits in Children with Oppositional Defiant Disorder and Conduct Disorder Compared to Attention Deficit/ Hyperactivity Disorder: A Systematic Review and Meta‑analysis

Mikaela D. Bonham1  · Dianne C. Shanley1 · Allison M. Waters1 · Olivia M. Elvin1

Accepted: 24 September 2020 © Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Inhibitory control decits are known to be characteristic of Oppositional Deant Disorder (ODD), Conduct Disorder (CD), and Attention-Decit/Hyperactivity Disorder (ADHD); but it is unclear whether children with ODD/CD have inhibitory control problems independent of ADHD comorbidity. Previous reviews of inhibitory control and ODD/CD have only focused on one type of measure of inhibitory control or used non-clinical samples. The current meta-analysis explored inhibitory control problems of children with ODD/CD by systematically reviewing studies where children have a diagnosis of ODD and/or CD. Comparisons were made across 25 studies between children with ODD/CD, ODD/CD + ADHD, ADHD, and healthy controls (HC) on various measures of inhibitory control and ADHD symptomatology to explore impacts of ADHD comorbidity. A small signicant eect (g = -0.58, p < .001) suggested children with ODD/CD are likely to have more diculties with inhibitory control than healthy children. However, comparisons between clinical groups suggested this eect may be due to ADHD symptomatology present in each group. As diculties with inhibitory control are similar, across clinical groups, a dimensional approach to understanding ODD/CD and ADHD may be more useful to consider in future diagnostic criteria. Similarities across clinical groups highlight that therapeutic approaches that assist children with disruptive behaviours could benet from teaching children and their families how to cope with inhibitory control decits.

Keywords Inhibitory control · Conduct disorder · Oppositional deant disorder · Executive function · Disruptive behaviour

Introduction

Children with disruptive behaviour disorders have diculty regulating emotions and inhibiting undesirable behaviours. Executive function plays an important role in the regulation of thoughts, emotions, and behaviours (Diamond 2013). Recently, empirical studies have highlighted the unique role that executive function decits can play in the aetiology of disruptive behaviours (Ezpeleta and Granero 2014; Hobson et al. 2011). Historically, these neurobiological factors have often been overlooked in favour of psychological and social factors that cause disruptive behaviour. According to the Diagnostic and Statistical Manual (DSM-5), disruptive

behaviour disorders are classied as Disruptive, Impulse- Control, and Conduct Disorders (DICCD); including conduct disorder (CD), oppositional deant disorder (ODD), kleptomania, intermittent explosive disorder, pyromania, and other or unspecied disruptive, impulse-control and conduct disorders (American Psychological Association 2013). In the past, Attention Decit/Hyperactivity Disorder (ADHD) was classied as a disruptive behaviour disorder, and as such, much of the research on the relationship between executive function deficits and disruptive behaviours has focussed on children with ADHD. However, with the introduction of the DSM-5, ADHD has been reclassified. It is now a Neurodevelopmental Disorder due to empirical evidence that neurobiological deficits (e.g., executive dysfunction) are core characteristics of ADHD (Oosterlaan et al. 1998; Thorell and Wahlstedt 2006; Senderecka et al. 2012).

Interestingly, similar deficits are present in early childhood for children with ODD/CD (Schoemaker et al. 2012), but these disorders have remained in the DICCD chapter. This systematic review uses a meta-analytic

* Mikaela D. Bonham mikaela.bonham@grithuni.edu.au

1 School of Applied Psychology, Menzies Health Institute of Queensland, Grith University, Mt Gravatt, Quensland 4122, Australia

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approach to examine the role of inhibition control, one of the three key components of executive function, in ODD/ CD. It compares the following groups on measures of inhibitory control as well as ADHD symptomatology: ODD/ CD, ODD/CD + ADHD, ADHD, and healthy controls (HC). Systematically reviewing the available empirical evidence will help us to consider whether ODD and CD are better captured within diagnostic manuals as a neurodevelopmental disorder.

Aetiology of ODD and CD

Psychopathology across the l i fespan typical ly develops from the interaction between individual and environmental factors over time (Matthys and Lochman 2017). When considering the aetiology and treatment of disruptive behaviours, learned behaviour and parenting style have received much attention. Children are exposed to disruptive models of behaviour and learn this behaviour from their environment, which in turn develops into a disruptive behavioural disorder over time (Tremblay 2010). This has been demonstrated in children who model behaviour after coercive parents or associate with delinquent peers when there is an absence of positive parenting (Matthys et al. 2012). When disruptive behaviour disorders are explained by coercive parenting or peer inf luences, interventions naturally follow a “learning-based” approach (Matthys et  al., 2012, p. 235). Interventions focussed on parenting and behaviour modification for antisocial youths have demonstrated small to moderate effect sizes; with a mean effect size of 0.47 (range -0.06 to 1.68) and 0.35 (range -1.04 to 1.87), respectively (McCart et al. 2006). Similarly, parenting group interventions for externalising behaviours have also demonstrated small to moderate effect sizes; with a mean effect size of -0.38 favouring intervention (range -0.56 to -0.19; Buchanan-Pascall, Gray, Gordon & Melvin, 2018). Matthy and Lochman (2017) argue that although there is demonstrated effectiveness for behavioural parent training, the effect sizes remain small to moderate, which may be due to many studies being conducted in highly controlled environments which may not be representative of real-world practice. Further, there may also be an impact on children’s ability to learn and problem solve due to neurocognitve impairments in areas such as executive function (Matthys and Lochman, 2017; Matthys et al., 2012). Matthys and colleagues (2012) highlighted that the neurocognitive basis of skill deficits in children with ODD and CD is understudied and understanding its role in the development and maintenance of these disorders has important implications for intervention, with investigation into the role of executive function in ODD/CD as being an important next step. Understanding

children’s neurocognitive challenges would be useful to inform more individualised treatment for children and their families (Matthys and Lochman, 2017). This review will be the first to meta-analyse inhibitory control deficits across childhood, in a clinical sample of children with ODD/CD relative to healthy and clinical controls.

Inhibitory Control. Executive function deficits are a key characteristic of ADHD. Inhibitory control is one of the three established domains of executive function (Miyake et  al. 2000). Broadly, inhibitory control refers to the ability to withhold an emotional or behavioural response in order to achieve a goal (Best and Miller 2010; Nigg 2000; van Goozen et al. 2004). When there is a skill deficit in this area, children have more difficulty stopping unwanted behaviour. While this is the definition used in the present review, across the literature, there are several ways of conceptualising inhibitory control; definitions tend to differ based on the function of inhibitory control. For example, some have conceptualised inhibitory control as executive, motivational, and attentional inhibitory control (Nigg 2000) or prepotent response inhibition, resistance to distractor interference, and resistance to proactive interference (Friedman and Miyake 2004).

The current review will examine cool and hot inhibitory control separately because inhibitory control may operate differently based on the emotional salience of the task at hand (Zelazo and Carlson 2012; Zelazo et al. 2010). Therefore, inhibitory control may operate as a ‘hot’ function when a person is in affective contexts, where cues for reward or punishment are present; for example, a delayed snack task employing delayed gratification (Zelazo et al. 2010). On the other hand, ‘cool’ inhibitory control is utilised when presented with abstract problems (Zelazo et al. 2010); for example, a go/ no-go behavioural task, assessing a person’s ability to not respond to a stimulus. Fundamentally, hot and cool executive function require different cognitive processes to be executed (Zelazo and Carlson 2012), which suggests that tasks assessing hot and cool inhibitory control should be analysed separately.

Measuring Inhibitory Control. Performance measures and rating scales will be examined separately throughout the review. Accurate measurement of executive function, including inhibitory control is difficult due to the overlapping nature of brain functions. It is impossible to obtain a pure measure of one cognitive process, such as inhibitory control, as all behaviours require more than one cognitive process (Anderson 2002). This issue is known as task impurity, where an outcome from a task or measurement does not solely reect a single ability, because completing the task requires more than one brain function to be executed (Miyake and Friedman 2012). For example,

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the Stroop task is a measure to assess inhibitory control however the task requires reading and comprehension to be completed. If an individual is impaired in either of these areas, it may aect their performance on the task overall. Performance measures of inhibitory control are standardised or experimental tasks that capture a child’s ability to inhibit a response when completing a task. Results of performance measures of executive function are often confounded by noise, as other executive and non-executive functions are contributing to performance (Miyake et al. 2000; Miyake and Friedman 2012). Ratng scales oer an ecological way to assess inhibitory control by documenting informant- or self- report of inhibitory control behaviours. They too continue to be aected by task impurity. Further complicating the measurement of inhibitory control, performance tasks and rating scales have been demonstrated by some researchers to not reect the same construct (Bodnar et al. 2007; Toplak et al. 2013).

Meta-analysis may allow for a way to assess overall inhibitory control performance at a group level, through a pooled eect size across all measures, providing a more global picture of inhibitory control in children with ODD/ CD. Analysing each task within inhibitory control separately makes it dicult to ascertain an overall eect of inhibitory control. However, understanding differences between performance on each task of inhibitory control is important. Prior meta-analyses of children with ADHD and ODD/CD have only reviewed the Stop Task (Lipszyc and Schachar 2010; Oosterlaan et al. 1998). As such, the analyses in the current review will pool all measures (i.e., according to cool vs. hot, and performance measures vs. rating scales) to understand inhibitory control in children with ODD/CD more globally, as well as subgroup analyses by task.

The Relationship Between ODD/CD, ADHD, and Inhibitory Control

This review will explore the similarities and dierences between children with ODD/CD, ADHD, ODD/ CD + ADHD, and healthy controls on measures of inhibitory control and ADHD symptomatology. When compared to their typically developing peers, pre-schoolers with ADHD, hard to manage behaviours, and aggressive behaviours have been found to have more diculties with inhibitory control (Schoemaker et al. 2013). However, there were too few studies to conduct ADHD and disruptive behaviour analyses separately. Oosterlaan and colleagues (1998) identied that children with CD (and no ADHD) had more diculties with inhibitory control compared to typically developing children; however, the review was limited to one measure of inhibitory control (i.e., stop signal task). Similarly, Lipszyc and Schachar (2010) meta-analysed performance on the stop signal task, revealing children with ODD/CD, ADHD,

and ADHD + ODD/CD had worse performance on the stop signal task compared to healthy controls. Greatest eects were found in children with ADHD, followed by ODD/CD and ADHD + ODD/CD respectively. Similarly, others have identied inhibitory control decits for children with ADHD compared to healthy controls (e.g., Wright, Lipszyc, Dupuis, Thayapararajah, Sathees, and Schachar 2014). There is an absence of reviews where performance on measures of hot inhibitory control has been assessed or reported for children with ODD/CD.

Often, behavioural/response inhibition (i.e., cool inhibitory control) is investigated in relation to externalising behaviours such as ODD/CD. Poor response inhibition is thought to be one factor that contributes to externalising behaviour diculties; including conduct problems (Miyake and Friedman 2012). As a result, children with diculties in response inhibition would be expected to have more diculty stopping unwanted behaviours (Hwang et al. 2016). Others have identied more diculties with hot inhibitory control, due to dysfunctional brain circuitry (cortico-striato- thalamo-corticial neurocircuitry) responsible for emotional executive function (Zhu et al. 2018). A review of imaging studies indicated abnormalities in brain regions associated with hot executive functions were more common in children with ODD/CD compared to those with ADHD (Rubia 2011). Further, diculties with emotional responding have been observed in children aged 10 to 18 years, based on fMRI data on an aective stop signal task (Hwang et al. 2016). Despite the inhibitory control decit hypothesis for children with ODD/CD, with a dearth of meta-analytic reviews, the literature lacks consensus as to whether these decits are characteristic of children with ODD/CD. Taken together, our current understanding of inhibitory control deficits in children with ODD/CD is limited; and this is further complicated by the relationship between ODD/CD and ADHD.

ADHD has often been found to be comorbid in girls with CD (OR > 40) and ODD (OR = 79), and boys with CD (OR = 3.7) and ODD (OR = 8.7; Costello et al. 2003). Other studies have also identied high comorbidity between CD and ADHD comorbidity in a community sample of children (OR = 10.7Angold et  al. 1999). As ODD/CD and ADHD are often comorbid, it is dicult to ascertain whether decits in inhibitory control are due to the severity of disruptive behaviour in ODD/CD, or whether they may simply be due to sub-clinical levels of ADHD symptoms (Blair et al. 2018). For example, youths aged 10 to 18 years with conduct disorder were found to have more diculties with hot inhibitory control, however this was attributed to the presence of ADHD symptoms, rather than the severity of conduct problems (Hwang et al. 2016). Understanding whether inhibitory control decits are indeed characteristic of children with ODD/CD or if they are simply a result

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of ADHD symptomatology may help us understand if ODD/CD and ADHD are categorically dierent or similar psychopathology within the same dimension.

Aims

The aim of this review was to comprehensively assess whether children and adolescents (3–17  years) with a clinical diagnosis of ODD and/or CD demonstrate inhibitory control decits more than healthy peers, independent of ADHD comorbidity. ODD/CD and ADHD are signicantly comorbid, hence there is a need to examine whether inhibitory control is similar or dierent for these diagnostic categories. Therefore, this paper aims to determine whether children with ODD/CD have greater or lesser inhibitory control decits when compared to children with ADHD or healthy controls (HC). We sought to answer these questions by making comparisons between ODD/CD, ADHD, ODD/ CD + ADHD, and HC groups on measures of inhibitory control and ADHD symptomatology. Additionally, we explored whether there were differences between the aforementioned groups on measures of cool and hot inhibitory control, rating scales, and the implications of measuring inhibitory control. All measures of inhibitory control and ADHD symptomatology were included in the review. Determining if inhibitory control decits are characteristic of children with disruptive disorders will contribute to a more comprehensive aetiological framework, which in turn will inform more focussed intervention strategies.

Methods

Inclusion and Exclusion Criteria

Studies were included if: (1) they were written in English, (2) sample participants were 3-17 years old, (3) sample participants had a clinical diagnosis of ODD, CD, and/or comorbid ADHD based on ICD-10, DSM-IV, DSM-IV-TR, or DSM-5 criteria using either clinical interviewing or diagnostic measures, (4) outcome measures specically tested for inhibitory control using a performance or rating scale, and (5) they had a healthy control (HC) or ADHD group as a comparison. Studies were excluded if sample participants had intellectual impairment, Autism Spectrum Disorder, or other cognitive impairments as comorbid disorders.

Search Strategy and Study Selection

The meta-analysis followed the recommendations and standards set by the Preferred Reporting Items for Systematic

Reviews and Meta-Analyses (PRISMA; Moher et al. 2009). A review protocol was registered with PROSPERO prior to completion of title and abstract screening. The initial protocol was amended, and all changes were reected on the published PROSPERO protocol (CRD42019121527). To obtain relevant literature, the following electronic databases were accessed in February 2020: PsycINFO, PubMed, Embase, CINAHL and Scopus. The nal title and abstract searches were conducted using the strings:

(executive function OR cognitive function OR executive dysfunction OR dysexecutive syndrome OR cognitive dysfunction OR executive control OR executive impairment OR inhibition OR inhibitory control OR attentional control OR emotional control OR cognitive control OR effortful control) AND (externalising behaviour OR externalizing behavior OR oppositional defiant disorder OR disruptive behaviour OR disruptive behavior OR problem behaviour OR problem behaviour OR conduct problems OR conduct disorder OR ADHD OR AD/HD OR attention decit hyperactivity disorder OR hyperkinetic) AND (child OR children OR adolescent OR kid OR school OR preschool OR pre-school OR pediatric OR paediatric OR teen OR teenager OR youth OR boy OR girl).

Key words and MESH terms were determined to be ineective in this search, as many records that were found explored executive function as a secondary construct of interest. Therefore, only title and abstract searches were used. Searches did not employ a restriction of year of publication. Reference list checks of review articles (Lipszyc and Schachar 2010; Oosterlaan et al. 1998; Schoemaker et al. 2013) and articles included in the current review were hand-checked to ensure all possible eligible studies were included.

Data Extraction

A total of 10,622 articles were retrieved through database and reference list searches. Following deduplication and assessment for eligibility, a total of 25 studies remained for nal review. Screening and appraisal were completed by two independent reviewers (MB and OE). Data extraction was completed by MB and with cross checks completed by another reviewer (OE). The following variables were extracted from the data: sample size, age, gender composition, country, IQ, primary diagnosis, comorbid diagnoses, medication status, details of diagnostic assessment, measures of inhibitory control, definition of inhibitory control, dependent variable as a measure of inhibitory control, measures of ADHD symptoms, eect size, and confounding variables. Where a consensus could not be reached, a third reviewer was consulted (DS). The

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PRISMA ow diagram outlines assessment of studies in Fig. 1.

Results

Studies Included

The following meta-analysis and synthesis will address differences between a healthy control (HC) group and children with a diagnosis of ODD/CD, ODD/CD + ADHD, or ADHD. In total, 25 studies were considered for meta- analysis (see Table 1), with the total included population

ranging from 3 to 14 years of age. Across the included studies, eight dierent task paradigms were employed to assess cool inhibitory, one hot inhibitory control measure was used, and one type of rating scale. When reporting ADHD symptoms, papers utilised standardised measures, symptom scales, and symptom counts from diagnostic interview schedules. Rating scales were either reported as a T-score, subscale raw score, or an average item score.

Publication Bias and Quality Appraisal

Publication bias was assessed through visual inspection of the funnel plot of standard error in Hedges G, revealing

Records idenfied through database

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Full-text arcles excluded (n=74) Not in English (n=5) Outside 3-17yrs (n=3) No appropriate comparison (n=13) Non-clinical sample ODD/CD (n = 14) DSM-III (n= 10) ASD/II/TBI (n= 1) Did not assess inhibitory control (n=7) Conference paper/dissertaon (n=15) Duplicate sample/paper (n=2) Unable to source data from authors (n=4)

Studies included in qualitave synthesis

(n=25)

Studies included in quantave synthesis

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Fig. 1 PRISMA ow chart of studies included in the review

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