Abstract
Objective:
The study aims to examine family functionality, emotion regulation difficulties, preference for loneliness, social exclusion, internalizing and externalizing disorders, and executive functions in children with Attention Deficit Hyperactivity Disorder (ADHD) and Cognitive Disengagement Syndrome (CDS) and compare with ADHD, and ADHD+ Oppositional Defiant Disorder (ODD).
Method:
This study included 842 children aged 8–12 years. The subjects were categorized according to DSM-V as ADHD (n = 246), ADHD + ODD (n = 212), ADHD + CDS (n = 176), and Control group (n = 207). The solitude and social exclusion, difficulties in emotion dysregulation and Barkley SCT scales, Child Behavior Checklist, family assessment device, and Central Vital Signs (CNSVS) test were used.
Results:
According to the study, children with ADHD + CDS had higher rates of internalizing disorders. They also preferred being alone and experienced more difficulty communicating with their parents and solving problems within the family. Additionally, these children had difficulty recognizing and understanding the emotional reactions of others. The ADHD + ODD group presented a poorer performance on CNSVS domain tests except for the psychomotor speed test than other groups. Also, ADHD + CDS children had the lowest psychomotor speed scores and lower scores on reaction time and cognitive flexibility than pure ADHD children.
Conclusion:
This study will contribute to the etiology, treatment, and clinical discrimination of ADHD + CDS.
Introduction
ADHD is the most common neuropsychiatric disorder that includes age-inappropriate inattention, hyperactivity, and impulsivity that appears in childhood (Barkley, 2013; Brown, 2013). Most children with ADHD often have another comorbid psychiatric disorder (Brown, 2013). Common externalizing disorders comorbid with ADHD include Oppositional Defiant Disorder (ODD) and Conduct disorder (CD). ADHD and ODD are among the most common psychiatric disorders of childhood in either the community or clinical samples (Willcutt, 2012). ADHD is also comorbid with Cognitive Disengagement Syndrome (CDS), previously referred to as Sluggish Cognitive Tempo (SCT), characterized by symptoms of cognitive disengagement and hypoactivity (Becker et al., 2023; Mayes et al., 2023). The international SCT Work Group has proposed a new term, “CDS” to replace the term SCT because it does not overlap with established terms for other constructs, is not offensive, reflects the current state of the science, and involves all several symptom dimensions (Becker et al., 2023). Although not recognized as a formal diagnosis in international diagnostic manuals (APA, 2022; WHO, 2021), recent reviews suggest that CDS is on the brink of being recognized as a distinct syndrome with several potential lines of inquiry (Becker et al., 2023).
Previous studies have indicated that CDS is different from ADHD (Becker et al., 2016; Lee et al., 2017; Willcutt et al., 2014). However, it has been observed that 30% to 63% of children with ADHD inattentive type also exhibit symptoms of CDS, and up to 59% of children with CDS have symptoms of ADHD (Barkley, 2012; McBurnett et al., 2014). CDS, like many other disorders such as ADHD and ODD, are often linked to other problems. Studies demonstrated that CDS remains associated with increased anxiety and depression (Becker et al., 2020; Fredrick et al., 2022; Smith et al., 2020), social withdrawal and loneliness (Fredrick & Becker, 2023; Yung et al., 2021), and to a less clear extent, executive functions (Barkley, 2013; Bauermeister et al., 2012; Wåhlstedt & Bohlin, 2010) after controlling ADHD. Also, some studies showed that CDS is related to environmental factors (Fredrick et al., 2022; Moruzzi et al., 2014). Therefore, CDS is of clinical and research interest due to its association with other psychological issues.
ADHD, and ODD, which are the most frequent neurodevelopmental disorders in childhood, and CDS can have a significant impact on the individual and the people they interact with, as well as their family and school environments. Several studies have examined the relationship between parenting stress and ADHD symptoms in children and adolescents, looking at both the parent-to-child and child-to-parent processes (Haack et al., 2016). It has been found that there is a strong link between family dysfunction and child ADHD (Barkley, 2012; Bauermeister et al., 2010; Brown, 2013), as well as between ADHD and ODD in children (Johnston & Mash, 2001). Research suggests that the degree of dysfunction within a family can be linked to the presence and severity of ADHD-related disorders such as ODD (Bhide et al., 2024). However, no studies examine the relationship between CDS and family functionality in children. One study conducted by Fredrick et al. (2019) found that a negative emotional climate within a family strengthened the relationship between CDS and ADHD inattentive type in young adults. Additionally, the same study found that a negative emotional climate increased the co-occurrence of CDS and depressive symptoms in young adults. Research has found that being exposed to a negative emotional environment can strengthen the link between CDS and depressive symptoms. This can be because children may model ineffective social interactions. There is growing evidence that CDS is strongly associated with depression and that CDS symptoms during childhood can predict depressive symptoms during adolescence (Becker & Willcutt, 2019; Becker et al., 2018). As is known, ADHD and ODD symptoms are linked with both internalizing (anxiety and depression) and externalizing (conduct disorder) problems (Brown, 2013). Both internalizing and externalizing problems often disrupt adaptive development during middle childhood and can continue into adulthood (Costello et al., 2003). These issues may lead to lasting and significant impairments for individuals and their social environment. Therefore, it is important to identify risk factors that increase the likelihood of psychological problems during childhood.
In addition, emotion regulation difficulties were common in psychiatric disorders and were related to CDS, ADHD, ODD, depression, and social interactions (Aldao et al., 2010; Taylor et al., 2020; Zlomke & Hahn, 2010). Children who have ODD and ADHD often have difficulties regulating their negative emotions (Shaw et al., 2014; Singh et al., 2023; Steinberg & Drabick, 2015). Studies have shown that emotional dysregulation is a common feature in both ADHD (Graziano & Garcia, 2016) and ODD (Cavanagh et al., 2017; Schoorl et al., 2016; Stringaris & Goodman, 2009). It has been suggested that emotional dysregulation plays a role in the development of these disorders (Ezpeleta et al., 2016; Graziano & Garcia, 2016; Steinberg & Drabick, 2015). Research has also shown that poor emotional regulation can negatively affect children’s social, emotional, and behavioral functioning and increase the risk of maladaptive behaviors. On the other hand, good emotional regulation skills can be protective (Caspi et al., 1996; Singh et al., 2023). Since emotion regulation skills have important implications for children’s mental health (McLaughlin et al., 2011), it is crucial to determine its effect according to different diagnoses.
Spencer et al. (2011) stated that 44% of children with ADHD had difficulties in regulating their emotions. This was found to be associated with increased rates of disruptive behavior disorders and anxiety disorders, as well as problems in interpersonal functioning. Four years later, these same children were reported to have higher rates of ODD and more social problems as perceived by their parents, when compared to a control group and an ADHD group with better emotional regulation (Biederman et al., 2011). Studies have shown that difficulty regulating emotions is a pathway linking childhood disruptive behavior to social problems, specifically withdrawal, and social isolation (Willcutt et al., 2014). There was also a correlation between emotion regulation and childhood disruptive behavior (Becker et al., 2016; Becker et al., 2020). Also, Flannery et al. (2016) showed that difficulty in emotion regulation had a mediating role between social impairment and CDS symptoms. Although some studies stated that there were poor relationships between them (Araujo Jiménez et al., 2015; Becker et al., 2016), in a large-sample national study that included 1800 children and adolescents between the ages of 6 and 17, emotion regulation difficulties were most common in children and adolescents with ADHD + CDS, followed by children and adolescents with only ADHD and only CDS symptoms, respectively was found (Barkley, 2013). Camprodon Rosanas et al. (2017) stated that emotional problems increase as the severity of CDS symptoms increases. A few studies have investigated specific aspects of social impairment and CDS in community and ADHD child samples (Mayes et al., 2023). The previous results showed that CDS was associated with social withdrawal (Becker et al., 2019; Ferretti et al., 2019; Yung et al., 2021). Becker et al. (2019) stated that while children with ADHD are more likely to be excluded based on impulsivity, and peers exclude children with ADHD + ODD due to their inappropriate reactions to social stimuli, aggressive behavior, and lack of self-control, children with CDS are more introverted, are in their world and prefer loneliness. The fact that the impairments in social relations seen in CDS, ADHD, and ADHD + ODD have different clinical features indicates the importance of the distinction of dimensions of loneliness.
Cross-sectional studies indicate that poor executive functions (EF) are related to psychopathology in children and adolescents (Kavanaugh et al., 2019; Mullin et al., 2020). Also, it has been proposed that executive function might be a transdiagnostic risk factor (Snyder et al., 2015). Impaired executive functioning is related to a diversity of mental disorders, although the underlying mechanisms of this relationship may vary between disorders (Halse et al., 2022). Therefore, it is important to determine the differences in EF. It is known that EF plays a central role in ADHD. Barkley (2013) stated that the processes associated with EF are very diverse and that the tasks of EF include response prevention/inhibition, organization, planning, working memory, shift and sustaining attention, emotional regulation, cognitive flexibility, and self-regulation skills. Previous studies showed that the comorbidity of ADHD and ODD/CD has a much greater risk for further impairment and worse outcomes than a diagnosis of ADHD alone (Bendiksen et al., 2017; Connor & Doerfler, 2008; Crippa et al., 2015; Cuffe et al., 2020). In addition, few studies have examined the neuropsychological deficits associated with CDS (Bauermeister et al., 2012; Huang-Pollock et al., 2005; Skirbekk et al., 2011; Wåhlstedt & Bohlin, 2010; Willcutt et al., 2014). These studies showed that CDS was not associated with neuropsychological deficits, while numerous studies associated ADHD with neuropsychological disorders (Harvey et al., 2011; Willcutt et al., 2005). Research has consistently shown that ADHD is associated with deficits in response inhibition, working memory, and response variability. On the other hand, CDS has not been associated with any of these deficits. However, when ADHD co-occurs with CDS, there is a greater impairment in sustained attention (Bauermeister et al., 2012; Inci Izmir et al., 2023; Wåhlstedt and Bohlin, 2010; Willcutt et al., 2014).
In addition, it is also crucial to differentiate between the coexistence and clinical entity of two problem areas in developmental psychopathology (Rothenberger et al., 2010). It is known that any comorbidity accompanying a disorder may affect the severity of it and complicate the treatment procedures and process (Inci et al., 2019; Kessler et al., 1997). The fact that there are not yet enough studies on the etiology of CDS may cause it to remain hidden behind other psychopathologies. Therefore, it is important to determine the substantial points that need to be addressed during the evaluation of CDS. Although there are many studies in the literature on ADHD and ODD, which are often comorbid with each other, there have been no studies comparing ADHD + ODD to CDS. Therefore, the study aims to examine family functionality, emotion regulation difficulties, preference for loneliness/solitude, social exclusion, internalizing and externalizing disorders, and executive functions in children with ADHD + CDS and compare with ADHD, and ADHD + ODD. Hypotheses are as follows;
H1: There are differences between diagnostic groups in terms of having Internalizing and Externalizing disorders. Internalizing total scores are expected to be high in the ADHD + CDS, ADHD, ADHD + ODD, and control groups, respectively. However, externalization scores are expected to be high in the ADHD + ODD, ADHD, ADHD + CDS, and control groups, respectively.
H2: There are differences between diagnostic groups in terms of social exclusion and preference for loneliness. Total loneliness preference scores are expected to be high in the ADHD + CDS, ADHD, ADHD + ODD, and control groups, respectively. However, social exclusion total scores are expected to be high in the ADHD + ODD, ADHD, ADHD + CDS, and control groups, respectively.
H3: There are differences between diagnostic groups in terms of family dysfunction. Problem-solving, Communication, Roles, Affective Responsiveness, Affective Involvement, Behavior Control, and General Functioning scores are expected to be higher in the ADHD + ODD, ADHD, ADHD + CDS, and control groups, respectively.
H4: There are differences between diagnostic groups in terms of emotion dysregulation. Awareness and Clarity subscale scores are expected to be high in the ADHD + CDS, ADHD + ODD, ADHD, and control groups, respectively. Nonacceptance, Impulse Control, Goals, and Strategies subscale scores are expected to be higher in the ADHD + ODD, ADHD, ADHD + CDS, and control groups, respectively.
H5: There are differences between diagnostic groups in terms of CNSVS. Cognitive flexibility scores were lower in the ADHD + CDS, ADHD + ODD, ADHD, and control groups, respectively; the Complex attention scores were lower in the ADHD + ODD, ADHD, ADHD + CDS, and control groups; Psychomotor speed and Reaction time scores are expected to be low in the ADHD + ODD, ADHD, ADHD + CDS, and control groups, respectively.
Methods
Participants
This study involved 841 children and adolescents (540 boys, 301 girls) aged between 8 and 12 years (M = 10.02, SD = 1.50), assessed at a child and adolescent psychiatry clinic between June 2022 and April 2023. The clinical sample and control group participants were recruited using convenient sampling. Thousand children and adolescents were evaluated with psychiatric interviews during the study period. Eighty-two children who filled out the scales incompletely were excluded from the study. Fifty-nine children who had a different psychiatric disorder outside the inclusion criteria (e.g., Conduct Disorder, Autism Spectrum Disorder, Mood disorders) were excluded from the study. Also, three children who had only CDS and fifteen children who had only ODD were excluded from the study because an adequate sample size could not be provided. The children’s diagnoses were based on DSM-V criteria and the assessment was conducted during the first psychiatric admission using the Turkish version of the Schedule for Affective Disorders and Schizophrenia for School-Aged Children Present and Lifetime Version (K-SADS-PL) by a professor in Child and Adolescent Psychiatry. Also, both the Barkley Sluggish Cognitive Tempo Scale and 4 items (13, 17, 80, 102) in CBCL were used for the diagnosis of CDS. Consequently, to diagnose CDS, after all children were assessed in a structured psychiatric interview by a professor in Child and Adolescent Psychiatry, participants who had a minimum of twenty-three scores on the Barkley Sluggish Cognitive Tempo Scale, and eight scores on 4 items of CBCL were included in the study. The subjects were grouped according to DSM-V as ADHD (n = 246), ADHD + ODD (n = 212), ADHD + CDS (n = 176), and Control group (n = 207). The exclusion criteria for this study were prior or current diagnosis of any psychiatric disorder except ADHD, ODD, and CDS; intellectual disabilities; the presence of a neurological disorder, or any other medical condition. Additionally, 204 healthy children were recruited into the study to serve as the control group, and the exclusion criteria for this group were any psychiatric disorder and intellectual disabilities or the presence of a neurological disorder.
Assessment procedure
All parents were informed about the aim and the process of the study. After that, informed consent forms were obtained from parents. The children were then assessed for socio-demographic features, and psychiatric disorders were assessed with the Kiddie Schedule for Affective Disorders and Schizophrenia for School-Age Children Present and Lifetime version (K-SADS-PL) by a professor in Child and Adolescent Psychiatry. Children also completed the face-to-face solitude scale, social exclusion for children, and the emotion dysregulation scale. Parents filled in the Child Behavior Checklist, Turgay DSM-IV-based Child and Adolescent Behavior Disorders Screening and Rating Scale, Barkley Sluggish Cognitive Tempo Scale, and Family Assessment Device. These scales were administered to each participant under the same conditions. Determining diagnostic status after reviewing all parent scales and the KSADS-PL, children were diagnosed. Then, the participants’ Executive functions were assessed using CNS Vital Signs (CNSVS), a computerized neurocognitive test battery. The Ethics Committee of XX University approved this study. This study is part of scientific research on determining etiological characteristics of ADHD + CDS. One part of the study has been published before (Inci Izmir et al., 2023).
Measures
Socio-Demographic Form
The form prepared by the researcher consists of the child’s gender and age and questions about the parent’s educational status, and income status.
Kiddie-SADS-Lifetime Version (KSADS-PL-DSM-5-T)
KSADS-PL is a semi-structured interview for assessing psychiatric disorders in children and adolescents according to DSM-V criteria. Turkish reliability and validity study of KSADS-PL-DSM-5-T was conducted by Ünal et al. (2019).
The Solitude Scale for Children
The Solitude Scale for Children (SSC) measures the preference for solitude (Inci Izmir, 2023). The preference for solitude determines whether one can spend time alone without feeling any negative emotions. In the scale, children are expected to show their responses on a 4-point Likert scale for each item. The degrees consist of 1 “Not suitable for me at all” to 4 “Always”. Higher scores indicated a high preference for loneliness/social withdrawal. The internal consistency is 0.96.
The Social Exclusion Scale for Children
The Social Exclusion Scale for Children (SESC) measures the exclusion from social relationships (Inci Izmir, 2023). Children are expected to show their 4-point Likert-type responses for each item on the scale. The degrees are 1 “Not suitable for me at all” to 4 “Always.” Higher scores indicated that social exclusion is high. The internal consistency is 0.95.
Difficulties in Emotion Regulation Scale
DERS is a 36-item self-report measure of six facets of emotion regulation. These are nonacceptance of emotional response, difficulty engaging in goal-directed behavior, impulse control difficulties, lack of emotional awareness, limited access to emotion regulation strategies, and lack of emotional clarity. Items are rated on a scale of 1 (rarely) to 5 (almost always). Higher scores indicate more difficulty in emotion regulation (Gratz & Romer, 2004). The validity and reliability studies of the Turkish scale adaptation were made by Ruganci and Gençöz (2010). In this study, the internal consistency coefficients of the scale ranged between 0.58 and 0.90.
The Child Behavior Checklist
The Child Behavior Checklist is a 113-item parent report measure designed to assess behavioral and emotional problems in children aged 6 to 18 (Achenbach & Edelbrock, 1983). This most recent version of the original measure includes items and subscales aimed at assessing symptoms of anxiety, depression, somatic complaints, social problems, thought problems, attention problems, rule-breaking behavior, and aggressive behavior. The scale’s internal consistency was 0.82 for Internalizing, 0.81 for Externalizing, and 0.88 for total problem. In the sample of this study, the internal consistency of the scale was determined as 0.89 for Internalizing, 0.91 for Externalizing, and 0.96 for total problem.
Turgay DSM-IV-Based Child and Adolescent Behavior Disorder Screening and Rating Scale
This instrument was developed by Turgay in 1994 and adapted into Turkish by Ercan et al. (2001). It is based on DSM-IV diagnostic criteria and assesses inattention, hyperactivity-impulsivity, opposition-defiance, and conduct disorder. The items are rated on a 4-point Likert-type scale. In this sample, the internal consistency coefficient of the scale ranged between 0.83 and 0.93.
Barkley Sluggish Cognitive Tempo Scales Children and Adolescents
This scale, developed to evaluate SCT (currently referred to as CDS) cases, and each item is evaluated with a 4-point Likert-type scale by Barkley (2013), consists of 12 items. In addition, 2 items related to the age of onset of the findings and in which areas they cause impairment in function. The Turkish validity and reliability study of the scale was conducted by Fırat et al. (2018). In this study, 23 points were considered the cut-off point and only the total score was used. The internal consistency coefficient of the scale in the sample of this study was determined to be 0.86.
CNS Vital Signs Battery
The CNSVS is a computerized test that evaluates the neurocognitive features of the participant. Seven subtests are included in the battery: visual and verbal memory, finger tapping, symbol digit coding, the Stroop test, the shifting attention test, and the continuous performance test. The main scores are determined by the scores obtained from these tests (neurocognitive index, holistic memory, reaction time, holistic attention, cognitive flexibility, and psychomotor speed). As a result of the validity and reliability study conducted by Gualtieri and Johnson (2006) stated that the internal consistency coefficients of the subtests ranged from 0.67 to 0.87. Some studies test the validity of the program in children and adolescents (Durak et al., 2014; Inci Izmir et al., 2022). In the sample of this study, the internal consistency coefficient of the scale ranged from 0.46 to 0.87.
Family Assessment Device
The McMaster Family Assessment Device (Epstein et al., 1983) is designed to evaluate families according to the McMaster Model of Family Functioning (MMFF). The MMFF is a clinically oriented conceptualization of families. It describes the structural and organizational properties of the family group and the patterns of transactions among family members which have been found to distinguish between healthy and unhealthy families. The FAD is made up of seven scales that measure Problem-Solving, Communication, Roles, Affective Responsiveness, Affective Involvement, Behavior Control, and General Functioning. The average score calculated for each sub-dimension varies between 1.00 and 4.00, and it is accepted that the unhealthy in terms of family functioning increases as the mean score approaches 4.00. If more than 40% of the items in each dimension are left unanswered, the average score for that dimension is not calculated. The validity and reliability studies of the Turkish adaptation of the scale were made by Bulut (1990). In the sample of this study, the internal consistency coefficient of the scale was 0.96 for the whole scale.
Statistical Analyses
Statistical analyses were performed using Statistical Package for the Social Sciences 21 (SPSS 21). Descriptive statistical analyses were used for the demographic characteristics of participants. All continuous variables were tested for normality and homogeneity of variance. The continuous variables were normally distributed; therefore, One-way analysis of variance (ANOVA) and Chi-square analysis were performed. The reliability of the scales was examined using Cronbach’s Alpha coefficients. The condition of ≥0.70 was accepted as an acceptable criterion for the reliability of the scales (Gliem & Gliem, 2003).
Results
This study included a total of 841 participants. The subjects were grouped according to DSM-V, %29.3 of children (n = 246) were in the ADHD group, 20.9% of them (n = 176) were in the ADHD + CDS group, 25.3% of them (n = 212) were in the ADHD + ODD group, and 24.7% of them (n = 207) in the control group. There were no statistically significant differences between the mean ages of groups (F (3,840) = 1.186, p = .314). However, there were statistically significant differences between the socioeconomic levels of groups (F (3,840) = 16.906, p < .001). According to the results of Tukey’s multiple comparison tests, the ADHD + CDS group differs from ADHD, ADHD + ODD, and Control groups in terms of socioeconomic levels; the ADHD + CDS group is lower than other diagnostic groups. In addition, the gender distribution significantly favored boys in all groups (χ2(3) = 44.861, p < .001). Moreover, there were statistically significant differences in the father’s education (F (3,840) = 11.688, p < .001) and the mother’s education level (F (3,840) = 17,156, p < .001) between groups. According to the results of Tukey’s multiple comparison tests, the ADHD + CDS group differs from ADHD, ADHD + ODD, and Control groups in terms of the father and mother’s education level. It was determined that the education levels of the mothers and fathers in the ADHD + CDS group were lower. The sociodemographic characteristics of the participants are presented in Table 1.
Socio-Demographic Characteristics of Participants.
ADHD = attention deficit hyperactivity disorder; CDS = cognitive disengagement syndrome; ODD = oppositional deficit disorder.
Chi-square test.
One-way ANOVA.
When the difference between diagnostic groups in terms of the mean of the family functionality total score and the sub-dimensions total score was evaluated, the FAD total score averages (F (3,840) = 190.09, p < .001, η2 = .41); Problem-solving (F (3,840) = 124.00, p < .001, η2 = .31); Communication (F (3,840) = 93.87, p < .001, η2 = .25); Affective Responsiveness (F (3,840) = 307.93, p < .001, η2 = .39); Roles (F (3,840) = 180.04, p < .001, η2 = .13); Affective Involvement (F (3,840) = 40.40, p < .001; η2 = .53) Behavioral Control (F (3,840) = 142.96, p < .001, η2 = .34); There is a statistically significant difference between the total scores of the General Functions (F (3,840) = 86.50, p < .001, η2 = .24) subscales (Table 2). A one-way ANCOVA was conducted to compare the differences between family functionality total score and sub-dimensions total score according to the diagnosis while controlling for the gender of children, socio-economic level, and father and mother’s education levels. The difference remained significant even when covariate variables were controlled for FAD total score (F (3,833) = 181.10, p < .001, η2 = .40) and sub-dimensions total score (All p < .001; η2 ranging from .12 to .39).
Comparison of Family Assessment Scale Total and Sub-Dimension Mean Scores of Different Diagnostic Groups with One-Way Analysis of Variance.
ADHD = attention deficit hyperactivity disorder; CDS = ognitive disengagement syndrome; ODD = oppositional deficit disorder.
When the difference between diagnostic groups in terms of the mean of emotion regulation difficulty and subdimensions’ total scores was evaluated, it was found that there were statistically significant differences between diagnostic groups according to the mean of emotion regulation scale total score (F (3,840) = 188.49, p < .001, η2 = .40); Awareness (F (3,840) = 158.35, p < .001, η2 = .36); Clarity (F (3,840) = 71.13, p < .001, η2 = .20); Nonacceptance (F (3,840) = 147.88, p < .001, η2 = .53); Strategies (F (3,840) = 195.82, p < .001, η2 = .41); Impulse (F (3,840) = 344.09, p < .001, η2 = .55); and Goals subscales (F (3,840) = 208.75, p < .001, η2 = .43) (Table 3). When controlling the gender of children, socio-economic level, and father and mother’s education levels, the differences between diagnostic groups remained significant for emotion regulation difficulty (F (3,840) = 178.46, p < .001, η2 = .41) and subdimensions’ total scores (All p < .001; η2 ranging from .21 to .55).
Comparison of the Mean Scores of the Total and Sub-Dimensions of the Difficulty in Emotion Regulation Scale of Different Diagnostic Groups with One-Way Analysis of Variance.
ADHD = attention deficit hyperactivity disorder; CDS = cognitive disengagement syndrome; ODD = oppositional deficit disorder.
In terms of the preference for loneliness or solitude, social exclusion, and loneliness, there were statistically significant differences between groups according to the preference for loneliness (F (3,840) = 267.73, p < .001, η2 = .49); the social exclusion (F (3,840) = 351.33, p < .001, η2 = .56); aloneness (F (3,840) = 110.17, p < .001, η2 = .28) (Table 4). According to Tukey’s multiple comparison test analysis, the total mean scores of loneliness preference were high in the ADHD + CDS, ADHD, ADHD + ODD, and Control groups, respectively; It was determined that the ADHD + CDS group preferred loneliness more. Despite that, the total mean scores of social exclusions were high in ADHD + ODD, ADHD, ADHD + CDS, and control groups. When controlling the gender of children, socio-economic level, and father and mother’s education levels, the differences between diagnostic groups remained significant for preference for loneliness or solitude (F (3,840) = 244.55, p < .001, η2 = .47); social exclusion (F (3,840) = 317.20, p < .001, η2 = .53) and loneliness (F (3,840) = 100.96, p < .001, η2 = .27).
Comparison of the Mean Scores of the Total and Sub-Dimensions of the Loneliness Preference and Social Exclusion for Children and Loneliness for Children Scale of Different Diagnostic Groups with One-Way Analysis of Variance.
ADHD = attention deficit hyperactivity disorder; CDS = cognitive disengagement syndrome; ODD = oppositional deficit disorder.
When the difference between diagnostic groups according to the mean of the CBCL subscales was evaluated, it was determined that there was a statistically significant difference between diagnostic groups in terms of the Anxiety and Depression subscale (F (3,840) = 162.32, p < .001, η2 = .37), Withdrawn subscale (F (3,840) = 325.71, p < .001, η2 = .54); The Somatic Complaint subscale (F (3,840) = 42.56, p < .001, η2 = .13) and Internalizing Disorders (F (3,840) = 256.79, p < .001, η2 = .48) also Delinquent behaviors subscale (F (3,840) = 109.42, p < .001, η2 = .28); Aggressive behaviors subscale (F (3,840) = 223.87, p < .001, η2 = .45) and Externalizing Disorders (F (3,840) = 217.38, p < .001, η2 = .44) and Social problem (F (3,840) = 195.12, p < .001, η2 = .41) (Table 5). According to Tukey’s multiple comparison test analysis, it was determined that the Anxiety and Depression subscale and Internalizing Disorder total scores were higher in the ADHD + CDS group. When controlling the gender of children, socio-economic level, and father and mother’s education levels, the differences between diagnostic groups according to the mean of the CBCL subscales remained significant (All p < .001; η2 ranging from 0.14 to 0.52).
Comparison of Mean Scores of CBCL Scale Subdimensions of Different Diagnostic Groups with One-Way Analysis of Variance.
ADHD = attention deficit hyperactivity disorder; CDS = cognitive disengagement syndrome; ODD = oppositional deficit disorder.
When the differences between EF in different diagnostic groups were evaluated, it was determined that there were statistically significant differences in terms of Neurocognitive Index, (F (3,840) = 110.04, p < .001, η2 = .28); Memory (F (3,840) = 53.34, p < .001, η2 = .16); Psychomotor Speed (F (3,840) = 51.41; p < .001, η2 = .16); Reaction time (F (3,840) = 22.63, p < .001, η2 = .08); Complex Attention (F (3,840) = 58.19, p < .001, η2 = .17); Cognitive Flexibility (F (3,840) = 30.81, p < .001, η2 = .10); Simple Attention (F (3,840) = 29.08, p < .001, η2 = .09). In addition, there were statistically significant differences between groups according to CNS-VS Subscales (Table 6). Even if controlling the gender of children, socio-economic level, and father and mother’s education levels, the differences between EF in different diagnostic groups remained significant (All p < .001; η2 ranging from .07 to .27).
Comparisons of CNSVS Domain and Subcales Scores Between Groups with One-Way Analysis of Variance.
ADHD = attention deficit hyperactivity disorder; CDS = cognitive disengagement syndrome; ODD = oppositional deficit disorder.
Discussion
This study compared the family functionality, difficulty in emotion regulation, preference for loneliness, social exclusion, internalizing and externalizing disorders, and executive functions of children according to ADHD, ADHD + CDS, and ADHD + ODD. In general, the analysis of the results completely confirmed hypotheses 1, 2, and 3. However, hypotheses 4 and 5 are partially confirmed.
It was determined that the diagnostic groups differed from the control group and within themselves regarding family functionality. It was observed that the impairment in family functionality was highest in the ADHD + ODD, followed by the ADHD, ADHD + CDS, and control groups, respectively but the family functions of the ADHD and ADHD + CDS groups did not differ from each other. These results confirmed hypothesis 3. Interactions between parents and children are viewed as a two-way exchange, where the characteristics of each party influence the other and shape the parent-child relationship over time (Johnston & Jassy, 2007). Therefore, early child characteristics can trigger problems initially. Still, if the child’s issues persist and parenting becomes more difficult, this can create a cyclical pattern where each factor exacerbates the other. In this regard, It is assumed that ADHD features emerge early in a child’s life and can negatively affect the parent’s ability to maintain consistent and sensitive parenting and that the presence of rigid or inconsistent parenting contributes to the development of the child’s behavioral problems (Johnston & Jassy, 2007). For example, a coercive cycle typically begins with a child misbehaving, followed by the parent scolding the child, which results in the child’s exacerbation of the misbehavior. If the parent disengages to stop the child’s aversive behavior, both participants are shaped by this response. The parent has been shaped to give up when the child’s behavior becomes aversive, and the child has been shaped to become aversive again the next time the child’s parent is disciplined. The negative reinforcement of the child’s misbehavior creates a positive feedback cycle whereby parent-child interactions become more difficult to manage, leading to the escalation of aggressive behaviors over time (Patterson, 2002). Therefore, it can be expected that unhealthy family functions are higher in the ADHD + ODD group than in other groups. Frequently interacting with children’s genetic predisposition to ADHD may contribute to ADHD by affecting the parent-child relationship and parenting skills (Nigg, 2012). In this context, since it is known that the presence of comorbidity is a must in ADHD and that comorbidity can increase the severity of the existing disorder, the higher level of impairment in family functionality of children with ADHD + ODD is compatible with the literature (Barkley, 2015). Jendreizik et al. (2022) stated that there are relationships between family stress, parent’s psychopathology, and negative parenting practices of children with ADHD + ODD. Longitudinal studies consistently showed that parenting difficulties (e.g., low reactivity, low positivity, over-reactivity, inconsistency) predict the increase or maintenance of disruptive behaviors over time in children diagnosed with ADHD (Biederman et al., 2001; Chronis et al., 2007; Lifford et al., 2008). In addition, there were no significant differences between ADHD and ADHD + CDS children in terms of family dysfunctionality in this study. Although there were no studies evaluating family functionality in children in the literature, there were findings that accompanying ADHD with CDS symptoms will increase the severity of ADHD (Becker et al., 2023; Fırat et al., 2021). In this study, it was found that there were differences between ADHD and ADHD + CDS children only regarding the use of solutions to preserve family functionality and ensure effective, mutual information exchange within the family. It was determined that the families of people with ADHD + CDS stated that they had more difficulty in these matters. Considering that CDS symptoms are associated with continuous and selective attention (Inci Izmir et al., 2023; Wåhlstedt & Bohlin, 2010; Willcutt et al., 2014) and that these were necessary for the continuity of social communication and the recognition and understanding of environmental messages, it is thought that it is expected that the family functionality of people in the ADHD + CDS group will be more affected in these areas. While those in the ADHD + ODD group have difficulty in problem-solving, communication, and family functioning due to ODD symptoms such as difficulty in following the rules and stubbornness; it was thought that the ADHD + CDS group’s difficulty in only these two subscales may be related to their difficulty in following messages and responding correctly to the right stimulus. It is thought that the difference between ADHD + CDS and ADHD only in these areas may be related to CDS being more associated with problems in social functioning (Becker et al., 2023; Willcutt et al., 2014). More research is needed to better define the differences between diagnostic groups in terms of family functionality.
In this study, it was determined that children in the ADHD + ODD group had more difficulty in regulating emotions compared to the other two diagnosis groups and the control group. These results partially confirmed hypothesis 4. Bunford et al. (2015) stated that the ADHD subtype and symptom severity may contribute to the development and maintenance of emotion regulation difficulties among adolescents diagnosed with ADHD. It has been shown that there is a relationship between the increased severity of emotion regulation difficulties in children with ADHD and the risk of comorbidity, and studies have stated that ODD is the most common disorder comorbid with ADHD and emotion regulation difficulties (Rosen et al., 2015; Sobanski et al., 2010). It is known that ODD is frequently comorbid with ADHD in early childhood and that the impairment in functionality increases in the presence of any psychiatric disorder comorbid with ADHD (Booster et al., 2012; Connor et al., 2003). In this regard, the fact that the ADHD + ODD group in the current study had more difficulties in emotion regulation is consistent with the literature. At the same time, emotion regulation skills develop early in life, and individual differences in emotion regulation become particularly evident in early and middle childhood when the prevalence of ODD is high (Crespo et al., 2017). Some studies examining the relationship between ODD and emotion regulation state that emotion regulation is the core symptom of ODD (Cavanagh et al., 2017; Zhang et al., 2023), but some suggest a negative relationship between them. (Chen et al., 2022), some studies have stated that those with ODD symptoms have more emotion regulation difficulties, consistent with the current study (Shaw et al., 2014; Yu et al., 2022; Zhang et al., 2023). Assuming that emotion is a dynamic process and emotion regulation is a bidirectional interaction between emotions and actions or thoughts, emotional regulation is thought to change over time and have a bidirectional interaction with other factors (Cole et al., 2019). For this reason, it was thought that a longitudinal examination of the relationship between emotion regulation and ODD would be more useful and effective for the development of child psychopathology. In addition, consistent with the findings of previous studies, the current study showed that ADHD + CDS children had more difficulty in being aware of emotional reactions (awareness) and understanding emotional reactions (clarity) than ADHD children (Becker et al., 2020). Previous studies stated that there is a relationship between the CDS symptoms and “irregular emotional expression,” which is associated with difficulty in directing the rapid complex flow of information encountered in daily situations (Flannery et al., 2016; Inci Izmir et al., 2023; Willcutt et al., 2014). Also, Becker et al. (2019) stated that children with CDS symptoms have difficulty understanding social cues. The current results are consistent with previous findings.
The other hypothesis was related to the distinction of dimensions of loneliness, which provides an important contribution to our understanding of loneliness in children with ADHD + CDS, ADHD, and ADHD + ODD. Our findings indicated that preference for loneliness or solitude was higher in the ADHD + CDS, ADHD, ADHD + ODD, and control groups as social exclusion was higher in the ADHD + ODD, ADHD, ADHD + CDS, and control groups, respectively. Previous studies stated that children with ADHD + ODD or conduct disorder experienced higher levels of peer rejection than children with ADHD, that is, their social exclusion was higher, similar to the current study (Mrug et al., 2012). Nijmeijer et al. (2008) reported that difficulties in social relationships increase when ODD accompanies ADHD. Children with ADHD may miss social cues due to attention problems and impulsivity and may persist in their incompatible negative behaviors. When ODD is comorbid to ADHD, problems in social information processing will increase, and these interrelationships are likely to result in social exclusion. Also, the results of the study showed no difference in social exclusion between the ADHD + CDS and ADHD groups, which may be due to the similar symptom severity of the sample groups and the fact that the scales are self-report scales. The findings showed that the ADHD + CDS group prefers loneliness more than other groups. Although it is stated in the literature that CDS has a relationship with loneliness, no study examines and compares loneliness multi-dimensionally. The only study in the literature that directly examines the preference for loneliness is Sáez et al. (2019) stated that there was a moderately significant relationship between CDS symptoms and loneliness preference and a high level of correlation with aloneness. Carlson and Mann (2002) and Marshall et al. (2014) conducted a study to compare the social functioning of young people diagnosed with ADHD and different levels of CDS. The studies found that young people with ADHD and high CDS were more likely to exhibit social withdrawal than young people with low CDS levels. Also, Mikami et al. (2007) similarly found that CDS had a more significant relationship with social withdrawal. In this regard, consistent with the previous studies, the current study found that loneliness preference and social withdrawal were high in those with ADHD + CDS, meaning that these children avoid taking the first step in social relationships and may have difficulty initiating and maintaining relationships.
Also, Since comorbidity appears common in ADHD, the frequency of internalizing and externalizing disorders was evaluated to more clearly understand the differences between diagnostic groups. In the current study, internalizing total scores were high in the ADHD + CDS, ADHD + ODD, ADHD, and control groups, respectively; externalizing scores were found to be high in the ADHD + ODD, ADHD, ADHD + CDS, and control groups, respectively. That is, hypothesis 1 was confirmed. Most studies showed that there was a relationship between CDS symptoms and internalizing disorders in children and adolescents (Barkley, 2013; Becker et al., 2019; Camprodon-Rosanas et al., 2017; Capdevila-Brophy et al., 2014; Carlson & Mann, 2002; Garner et al., 2010; Lee et al., 2017; Marshall et al., 2014; Willcutt et al., 2014). Barkley (2013), in a study comparing children and adolescents with ADHD, ADHD + CDS, CDS, and no diagnosis, found that the two groups with CDS and ADHD + CDS had higher depression rates than the control group. In conclusion, there is a relationship between CDS and internalizing disorders, especially depression, but these are not completely overlapping structures. Consistent with the literature, it was determined that anxiety and depression symptoms are more common in the ADHD + CDS group than in other groups in this study. Therefore, CDS symptom severity may be a risk factor for internalizing disorder. Studies on externalizing disorders have shown that it is not associated with CDS, unlike ADHD, as in the current study (Becker & Barkley, 2018; Becker et al., 2016; Binici & Kutlu, 2018). No studies have been found that show the opposite of the relationship between CDS and externalizing disorders. The current study determined that externalizing disorders were more common in the ADHD + ODD group compared to other groups, and internalizing disorders were also observed. In a meta-analysis study, it was stated that ADHD + ODD patients have a significantly worse prognosis than people with only ADHD or ODD only, in terms of an increased risk of developing anxiety and depressive disorders, as well as conduct disorder and even antisocial personality disorder later in life (Loeber et al., 2000). Consistent with the current findings, it has been reported that those with ADHD + ODD show earlier onset, more functional disorders, and more physical aggression and criminal behavior than individuals with ADHD or ODD alone (Fredrick et al., 2022; Loeber et al., 2000).
Neurocognitive deficits are closely related to psychiatric symptoms in childhood, but far less is known regarding the neurocognitive functions in CDS and the differences from other disorders. In this regard, when we examined the diagnostic group differences in terms of neurocognitive performance, the current study showed that the ADHD + ODD group presented a poorer performance on CNSVS domain tests except for the psychomotor speed test than other diagnostic and control groups. EF has a predisposing effect on impulsive and aggressive behavior (Pennington & Bennetto, 1993). Previous studies showed that the comorbidity of ODD or CD with ADHD is a much greater risk for further impairment and worse outcomes than a diagnosis of ADHD alone (Bendiksen et al., 2017; Connor & Doerfler, 2008; Cuffe et al., 2020). Qian et al. (2010) stated that children with ADHD + ODD had lower scores than those in the ADHD group. Also, it has been stated that children with ADHD + ODD show more severe EF in daily life scenarios than those with ADHD (Qian et al., 2010). It has been reported that in the presence of internalizing or externalizing disorders comorbid with ADHD, neurocognitive index, memory, psychomotor speed, cognitive flexibility, complex attention, and reaction time scores show more impairment than the ADHD-only group (Inci Izmir et al., 2022).
In addition, the findings of this study showed that there was no difference between ADHD and ADHD + CDS in terms of neurocognitive index, memory, and complex attention. It may be explained by the similarity of symptom severities and the assessment method. In addition, previous studies showed that CDS is not associated with impairment in EF (Becker et al., 2023; Willcutt et al., 2014). Consistent with the previous study’s findings, the current study’s results showed that children with CDS had lower scores than the control group in terms of CNSVS domain tests (Yazan-Songür, 2022). Similar to previous studies (Baytunca et al., 2019; Yazan-Songür, 2022), there was no statistically significant difference in memory scores between ADHD + CDS and ADHD children. However, there were studies in the literature showed that CDS negatively affects memory scores (Hinshaw et al., 2012; Skirkbekk et al., 2011). In addition, complex attention scores were lower in ADHD + ODD, ADHD, ADHD + CDS, and control groups respectively. These findings supported that CDS isn’t an EF disorder. However, the fact that the impairment was higher than the control group is significant in terms of the impairment in social relations. In contrast to the current findings, several studies stated that there was a relationship between poor complex attention and CDS (Baytunca et al., 2018; Muelller et al., 2014; Skirbekk et al., 2011; Wåhlstedt & Bohlin, 2010; Willcutt et al., 2014).
Although previous studies on CDS have focused on psychomotor speed because the core symptom of CDS is slowness, the findings are inconsistent. In this study, it was determined that the CNS-VS test psychomotor speed subscale scores were lower in the ADHD + CDS group and that there was no difference between the ADHD and ADHD + ODD groups. In terms of reaction time, findings showed that the ADHD + ODD group had the most difficulty, followed by the ADHD + CDS and ADHD groups. Consistent with the present study, previous studies indicated that CDS symptoms are associated with slow psychomotor speed in younger children (Tamm et al., 2016). Willcutt et al. (2014) and Wåhlstedt and Bohlin (2010) showed that there was a relationship between CDS and psychomotor slowness. Creque and Willcutt (2021) also stated that children with CDS had slower psychomotor speeds. Also, Cook et al. (2019) showed that CDS and processing speed have different effects on functional abilities that are not explained by the burden of ADHD symptoms. This study determined that CDS symptoms were found to significantly predict adaptive functioning, accounting for 6% of the variance. However, they did not predict academic achievement. On the other hand, processing speed did not contribute significantly to the prediction of adaptive functioning, but it did predict academic achievement, accounting for 4% of the variance. Another study indicates that CDS ratings predicted slowed processing speed and that the association between CDS symptoms and processing speed may be stronger in younger (elementary school-age) children (Jacobson et al., 2018). Also, Tamm et al. (2024) stated that CDS symptoms were uniquely associated with slower performance across a range of cognitive domains, including verbal inhibition, rapid naming/reading, planning, divided attention, and set-shifting. However, some studies indicated that there was no relationship between CDS and slower psychomotor speeds (Bauermeister et al., 2012; Baytunca et al., 2018; Wood et al., 2017; Wu et al., 2022). In addition, several studies showed that there was no difference between ADHD + CDS and ADHD in terms of reaction time (Baytunca et al., 2018; Wåhlstedt & Bohlin, 2010; Willcutt et al., 2014). In the current study, like previous studies, reaction time was more impaired in the ADHD + ODD group (Brown, 2013; Inci izmir et al., 2022; Ter-Stepanian et al., 2017). It was thought that this may be due to the high severity of the disorder. The impairment in reaction time was also high in the ADHD + CDS group. Consistent with the current study findings, Huang-Pollock et al. (2005) determined that those with CDS symptoms had lower reaction times than those without CDS symptoms. Similarly, in a study conducted with children with only CDS symptoms in Turkey, it was stated that reaction times were lower compared to the control group (Yazan Songür, 2022). Different from the current study, Baytunca et al. (2018) stated that there was no difference in reaction time between ADHD and ADHD + CDS, but the ADHD + CDS group received lower scores than the controls. It was thought that the inconsistency in the literature may be due to the cross-sectional nature of the studies, the difference in the severity of the disorders, and the difference in sample sizes and diversity. Finally, ADHD + ODD and ADHD + CDS groups had more impairment in cognitive flexibility scores than ADHD and control groups. Consistent with current study findings, previous studies showed that there was a relationship between selective attention and CDS (Inci Izmir et al., 2023; Ünsel Bolat et al., 2020; Wåhlstedt & Bohlin, 2010; Willcutt et al., 2014; Yung et al., 2021). According to Baytunca et al. (2018), children diagnosed with ADHD + CDS performed worse in the shifting attention test, which measures cognitive flexibility and selective attention, by providing fewer correct and more incorrect answers. This showed that children with ADHD + CDS symptoms are less alert to new stimuli and may have difficulty transitioning between difficult tasks. Further work is needed to understand the neurocognitive profile associated with CDS.
In sum, the current study revealed that ADHD + CDS children display divergent neurocognitive functioning from other diagnostic and control groups. Also, the ADHD + CDS group had more internalizing disorders, a preference for loneliness, difficulty recognizing and understanding the emotional reactions of others, and difficulty communicating with family members and solving intrafamilial problems. According to the results of the study, ADHD + ODD children had more impairment than other groups about all variables.
Limitations
The present results should be viewed based on the strengths and limitations of this study. As far as is known this study is the only study to compare ADHD, ADHD + CDS, and ADHD + ODD to family functioning, emotional dysregulation, social exclusion, preference of loneliness, internalizing and externalizing disorders, and neurocognitive functioning. Regarding the limitations, the participants were recruited from a single center. Therefore, the present results highlight the need for more research in this area with multicenter sampling. Another limitation is that it is a cross-sectional study. Since this may affect the generalizability of the findings and prevent causality from being mentioned, it is recommended to conduct longitudinal studies in the future. One of the limitations is the multiple comparisons conducted in our analysis, which may related to type 1 error. However, as these outcomes are inter-correlated, it may be not appropriate to adjust p-values for multiple comparisons (Barnett et al., 2022; Feise, 2002). Another limitation is that children and adolescents showing only CDS symptoms could not be included in the sample due to the low rate of admission to the clinic. In addition, future studies could include children who had only ODD to determine the differences between groups more clearly. Also, not taking any assessments from their teachers is another limitation. It is recommended to conduct a study by multi-informant assessment. Consequently, longitudinal, multicenter, and large-sample studies are needed to determine possible risk and protective factors in children having CDS symptoms and to understand better which areas differ from other disorders.
Clinical Significance
Comorbidities are a rule and not an exception in individuals with ADHD. It is known that any comorbidity accompanying a disorder may affect the severity of it and complicate the treatment procedures and process. Although it was thought that CDS can be a different disorder from ADHD, CDS can often be comorbid with ADHD. More fact that there is needed more information regarding the etiology, clinical assessment, and treatment of CDS or its relationship with ADHD with which it frequently co-occurs because CDS remains hidden behind other psychopathologies. Therefore, it is important to determine the substantial points that need to be addressed during the evaluation of CDS and the differentials of it from ADHD and ODD, the most comorbid seen with ADHD. Also, although there are many studies in the literature on ADHD and ODD, which are often comorbid with each other, no study has been found investigating their differences with CDS. Therefore, it is thought that comparing the characteristics of ADHD + CDS with ADHD and ADHD + ODD will contribute to the clinical course, etiology, treatment, and clinical discrimination of ADHD + CDS.
Footnotes
Acknowledgements
None.
Author Contributions
All authors contribute to conceptualization, methodology, statistical analyses, writing of original draft, review, and editing of the manuscript.
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) received no financial support for the research, authorship, and/or publication of this article.
Ethical Approval
This research was performed in line with the principles of the Declaration of Helsinki. The Ethics Committee of the University approved. . . Informed consent was obtained from all individual participants included in the study.
Data Availability
The data are available upon request of the corresponding author.
