by Rosa Elena Ulloa Flores, MD, PhD; Ricardo Díaz Sánchez, BS; Francisco R. de la Peña, MD, MS; Marcos F. Rosetti Sciutto, PhD; Lino Palacios Cruz, MD, PhD; and Pablo Mayer Villa, MD, MS
Dr. Ulloa Flores is with Hospital Psiquiátrico Infantil Dr. Juan N. Navarro, in México City, México. Mr. Díaz Sánchez is with Arete Proyectos in México City, México. Drs. de la Peña and Palacios Cruz are with Instituto Nacional de Psiquiatría Ramón de la Fuente Muñiz, in México City, México. Dr. Rosetti Sciutto is with Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, in México City, México. Dr. Mayer Villa is with Departamento de Ciencias de la Salud en la División de Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana Lerma in Lerma de Villada, México.
Funding: Funding was provided by a university grant from Universidad Nacional Autónoma de México (GAP-PAPIIT-IA202617).
Disclosures: The authors have no conflicts of interest relevant to the content of this article.
Innov Clin Neurosci. 2022;19(10–12):16–18.
Objective: The goal was to compare the impairment on executive functions in children and adolescents with attention deficit hyperactivity disorder (ADHD) alone and with comorbid oppositional defiant disorder (ODD), conduct disorder (CD), or both (ADHD+ODD+CD).
Design: A total of 162 patients were diagnosed with the Mini International Neuropsychiatric Interview for Children and Adolescents (MINI-KID), and the results of their performances in Behavior Rating Inventory of Executive Function (BRIEF) and the Tower of London (ToLo) were compared.
Results: Patients with only ADHD showed less impairment in the BRIEF domains and were younger than those with ADHD+CD; the latter group showed a better performance in the time-related domains of ToLo. Patients with ADHD+ODD+CD did not present a consistently worse cognitive performance.
Conclusion: The cognitive performance of patients with ADHD and externalizing disorders seems to vary according to the types of specific comorbid diagnoses, rather than the number of externalizing comorbidities.
Keywords: ADHD, externalizing disorders, BRIEF, ToLo, comorbidity
Oppositional defiant disorder (ODD) and conduct disorder (CD) are among the most common comorbid conditions in children and adolescents with attention deficit hyperactivity disorder (ADHD). ODD is present in about 1 in 2 children with ADHD, while CD can be found in 1 in every 4 to 5 children with ADHD.1,2
Some studies suggest that co-occurrence of ADHD and ODD/CD substantially worsens psychosocial outcome, compared to the presence of any of these disorders on their own.3 In terms of cognitive performance, children with ADHD+CD obtained lower scores in the Wisconsin Card Sorting Test, and adolescents with ADHD+ODD and ADHD+CD exhibited more deficits in verbal working memory, response inhibition, and other executive functions than those with ADHD alone.4–6
The introduction of the Diagnostic and Statistical Manual of Mental Disorders, 5th Edition (DSM-5) allowed clinicians to simultaneously establish the diagnoses of ODD and CD.7 This allows for the possibility to determine the independent and joint impact of an ODD and/or CD comorbidity with ADHD, which currently remains unexplored. The present study aimed to compare cognitive function across groups of children and adolescents with ADHD with and without comorbid externalizing disorders. We expected the group with ADHD+ODD+CD to show worse performance in cognitive tasks.
The protocol was approved by the internal review board of the Juan N. Navarro Children’s Psychiatric Hospital in Mexico City, Mexico (approval number 33, 2016). Written informed assent and consent were obtained from all participants and their parents.
We studied a sample of children and adolescents with a confirmed diagnosis of ADHD who had no pharmacological treatment and were attending school at the time of their evaluation; the patients were excluded if they had comorbid psychosis, a pervasive developmental disorder, or motor disability. Participants were recruited at the Hospital Psiquiátrico Infantil Dr. Juan N. Navarro in Mexico City from May 2012 to June 2018. All participants were first evaluated in the outpatient service, where ADHD was first diagnosed. Then, they were referred to a research team member to confirm ADHD diagnosis and determine the presence of comorbid disorders.
The patients were evaluated with the Mini International Neuropsychiatric Interview for Children and Adolescents (MINI-KID) to confirm ADHD diagnosis and determine presence of comorbid disorders, skipping the jump command that avoids the CD/ODD comorbidity. The MINI-KID was designed as a structured diagnostic interview to evaluate psychopathology in children and adolescents. It examines the presence of 23 psychiatric present and lifetime disorders according to the DSM-IV and the International Classification of Diseases 10th Revision (ICD-10).8 After that, they completed the Tower of London–Drexel University (ToLo), which was developed for assessing executive functioning planning deficits. It includes two identical tower structures with three wooden pegs of descending lengths mounted on a block base and three beads. The participants were asked to replicate on their own tower structure the same problem configuration presented by the examiner. The number of moves, time violations, and rule violations were scored throughout 10 problems.9
Parents of participants completed the Behavior Rating Inventory of Executive Function (BRIEF), parent version, an 86-item questionnaire that evaluates the executive functioning of the child. It includes eight clinical scales that form two indices: 1) Behavioral Regulation Index (BRI; Inhibition, Shifting, and Emotional Control) and 2) Metacognition Index (Monitor, Organization of Materials, Plan/Organize, Working Memory, and Initiate), which form a Global Executive Composite (GEC).10
Statistical analysis was carried out using the Statistical Package for Social Science (SPSS 21 for Windows). Descriptive statistics were used, followed by a one-way analysis of variance (ANOVA) to compare the scores derived from the BRIEF and ToLo among the following diagnostic groups: 1) ADHD without any externalizing disorders, 2) ADHD+ODD, 3) ADHD+CD, and 4) ADHD+ODD+CD. When significant, ANOVAs were followed by the Tukey Honestly Significant Difference test for pairwise comparisons. Significance for all tests was established as p less than 0.05.
The sample included 162 children and adolescent outpatients, 80.2 percent of whom were male. Mean age was 10.39±2.9 years (range: 6–16 years). The ADHD+ODD group was the largest group. The comparison of demographic and clinical characteristics showed that children with only ADHD, while younger, had better scores in multiple BRIEF subcategories (Inhibition, Shifting, Emotional Control, and Monitor) than the other groups. When ToLo was evaluated, the ADHD+CD group solved the problem faster than the other groups, despite no differences being observed in the number of successful trials or any other metrics indicating a successful performance. Significant differences can be seen in Table 1.
The present study compared cognitive performance among participants with ADHD with and without comorbid disruptive behavior disorders. Contrary to our expectations, the results showed that performance did not vary in accordance with the number of comorbid disorders, in that the ADHD+ODD+CD group did not have the worst performance among groups.
The ADHD+CD group had higher scores in several BRIEF scales; in particular, they had the worst performance in Inhibition. Difficulties in inhibition can be associated with poor monitoring and working memory, which have been reported in patients with this comorbid pattern.6,11,12
Comparisons also showed significant differences between the ADHD+CD and ADHD only groups, as well as between the ADHD+CD and ADHD+ODD groups, in ToLo scores, reflecting time performance. These scores are usually associated with planning; the shorter the time, the more efficient the participant is in implementing a solution. The lack of difference in scores reflecting success shows that while all groups arrived at a solution, children with ADHD or ADHD+ODD did so in a less efficient manner. Planning is related to other cognitive functions, among them set shifting, which has been reported to be impaired in children with ADHD+ODD.13 Present results could reflect difficulties in cognitive flexibility and working memory in this group of patients, which, in addition to attention problems, led to less planning efficiency.14 This should be confirmed in further studies of patients with ODD.
Our findings suggest that having ADHD paired with other behavioral disruptive disorders provides some specific differences in performance in BRIEF and ToLo evaluations. These results could have some implications in clinical settings, especially in the need to differentiate which specific disruptive behavior disorder is comorbid with ADHD.
The cognitive performance of patients with ADHD and externalizing disorders seems to vary according to the types of specific comorbid diagnoses, rather than the number of externalizing comorbidities.
The authors thank Donaldo López and José Luis Rodríguez for their assistance in preparing the manuscript.
- Burke J, Romano-Verthelyi A. Oppositional defiant disorder. In: Developmental Pathways to Disruptive, Impulse-Control and Conduct Disorders. Academic Press. 2018;21–52.
- Taurines R, Schmitt J, Renner T, et al. Developmental comorbidity in attention-deficit/hyperactivity disorder. Atten Def Hyp Disord. 2010;2(4):267–289.
- Loeber R, Green S, Lahey B, et al. Findings on disruptive behavior disorders from the first decade of the Developmental Trends Study. Clin Child Fam Psychol Rev. 2000;3(1):37–60.
- Ter-Stepanian M, Grizenko N, Cornish K, et al. Attention and executive function in children diagnosed with attention deficit hyperactivity disorder and comorbid disorders. J Can Acad. 2017;26(1):21.
- Lin YJ, Gau SS. Differential neuropsychological functioning between adolescents with attention-deficit/hyperactivity disorder with and without conduct disorder. J Formos Med Assoc. 2017;116(12):946–955.
- Shahrokhi H, Tehrani-Doost M, Shahrivar Z, et al. Deficits of executive functioning in conduct disorder and attention deficit/hyperactivity disorder. Ann Psychiatry Treatm. 2017;2(1):13–20.
- American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition. American Psychiatric Association; 2013.
- Sheehan D, Sheehan K, Shytle R, et al. Reliability and validity of the Mini International Neuropsychiatric Interview for Children and Adolescents (MINI-KID). J Clin Psychiatry. 2010;71(3):313–326.
- Culbertson W, Zillmer E. The construct validity of the Tower of London DX as a measure of the executive functioning of ADHD children. Psychol Asses. 1998;5(3):215–226.
- Mahone E, Cirino P, Cutting L, et al. Validity of the behavior rating inventory of executive function in children with ADHD and/or tourette syndrome. Arch Clin Neuropsychol. 2002;17(7):643–662.
- Danforth J, Connor D, Doerfler L. The development of comorbid conduct problems in children with ADHD: an example of an integrative developmental psychopathology perspective. J Atten Disord. 2016;20(3):214–229.
- Forslund T, Brocki C, Bohlin G, et al. The heterogeneity of attention‐deficit/hyperactivity disorder symptoms and conduct problems: cognitive inhibition, emotion regulation, emotionality, and disorganized attachment. Br J Dev Psychol. 2016;34(3):371–387.
- Van Goozen S, Cohen-Kettenis P, Snoek H, et al. Executive functioning in children: a comparison of hospitalised ODD and ODD/ADHD children and normal controls. J Child Psychol Psychiatry. 2004;45(2):284–292.
- Rodrigues C, de Almeida C, Serafim A, et al. Impairment in planning tasks of children and adolescents with anxiety disorders. Psychiatry Res. 2019;274:243–246.