Abstract
Objective:
To assess the Empathizing Quotient (EQ) of patients diagnosed with attention-deficit/hyperactivity disorder (ADHD) only or comorbid with oppositional defiant disorder (ODD) and compare the two groups' responses to methylphenidate (MPH) treatment.
Methods:
Fifty-two children (8–18 years) diagnosed with ADHD, 26 of whom were also diagnosed with comorbid ODD (ADHD/ODD), were treated with MPH for 12 weeks. The level of EQ was assessed with the Children's version of the Empathizing Quotient (EQ-C) and the severity of ADHD symptoms with the ADHD Rating Scale (ADHD-RS). Assessments were done at baseline and at end point.
Results:
A significant increase in EQ scores was obtained in both groups following MPH treatment (p = 0.003 for ADHD/ODD; p = 0.002 for ADHD). Significant correlation was found in the ADHD group between the changes in ADHD-RS and those in EQ, following MPH treatment (p = 0.015), but not in the ADHD/ODD group (p = 0.48).
Conclusions:
A correlation exists between MPH-related improvement in ADHD symptoms and between more empathy in children with ADHD not comorbid with ODD.
Introduction
A
Some attention impairments or executive deficits in children with ADHD can be associated with theory of mind (ToM) dysfunction (Mary et al. 2016). Impairments in executive functioning, associated with impaired attention, impulsivity, and distractibility, may affect the ability of a child to perceive the perspective of others. Thus, it is likely that stimulants have a beneficial effect on social responsiveness in children with ADHD. In addition, the lateral prefrontal cortex is an important node in the social brain, involved not only in inhibiting prepotent responses (e.g., activation of the amygdala in response to threatening social stimuli) but also in reflecting on the meaning of a salient social stimulus (Rubia et al. 2009). ADHD can result in inappropriate social behavior, which may be related to poorer social skills and failure to comprehend the impact on others of one's actions.
Along with EF deficits, socioemotional impairments are frequently reported in ADHD (Nijmeijer et al. 2008; Uekermann et al. 2010). Charman et al. (2001) found that children with ADHD had lower social competencies, as assessed by parental questionnaires, and made more errors in an executive inhibition task, yet performed at the same level as normatively developing children in an executive planning task and in an advanced ToM paradigm. Comorbidities, such as oppositional defiant disorder (ODD), pervasive developmental disorder (PDD), or conduct disorder (CD) can be considered additional risk factors for socioemotional dysfunction in ADHD, including deficiency in empathy (Nijmeijer et al. 2008).
Methylphenidate (MPH) possesses agonistic dopamine and norepinephrine activity and is the treatment of choice in ADHD, affecting impulsivity and aggression positively in ADHD pediatric populations. While there are numerous reports on the influence of MPH treatment on emotional regulation (Williams et al. 2008), little is known about its effect on empathy. Maoz et al. (2014) found that administration of MPH was associated with improvement in cognitive and ToM performance.
There is a scarcity of studies on this difficult to manage phenomenon in pediatric ADHD and on the impact of MPH treatment on empathy levels. In the present study baseline scores in the Empathizing Quotient—Children's Version (EQ-C) questionnaire (Auyeung et al. 2009) of children diagnosed with ADHD only (ADHD) were compared with those of children diagnosed with ADHD comorbid with ODD (ADHD/ODD). In addition, changes in Empathizing Quotient (EQ) levels were monitored for the 3 months following MPH treatment. The authors hypothesized that the level of EQ would be higher in ADHD than in ADHD/ODD and that MPH treatment would improve EQ in ADHD patients, but not in ADHD/ODD ones.
Methods
Subjects
Fifty-two children aged 8–18 years of whom 26 were diagnosed with ADHD and the other 26 with ADHD/ODD were recruited at a Maccabi Children's Psychiatric Clinic in Rishon Lezion, Israel during the period from January 2012 to December 2013. All participants were recruited from the same child psychiatry clinic.
All the children met criteria for ADHD, according to the Diagnostic and Statistical Manual of Mental Disorders, 4th ed., Text Revision (DSM-IV-TR) (American Psychiatric Association 2000) as was established by semistructured clinical interviews with the children and their parent(s) using the Kiddie-Schedule for Affective Disorders and Schizophrenia—Present and Lifetime Version (K-SADS-PL), and the ADHD Rating Scale (ADHD-RS) (DuPaul et al. 1998a, 1998b) that was completed by the parents. The diagnosis of the 26 children who also met DSM-IV-TR criteria for ODD was established by the K-SADS-PL combined with the parent and teacher reports. All the children attended regular school during the study period and all came from similar socioeconomic background. All the children were psychostimulant-medication naive and were referred for assessment at the clinic by a pediatrician, a school consultant, or by the parents.
The study was approved by the Maccabi Health Services Review Board for Human Clinical Studies. All participants and their parents gave written informed consent for participation in the study.
Exclusion criteria
History of organic brain syndrome, substance use, mental retardation, CDs, bipolar disorder, schizophrenia, delusional disorder or suicidal ideation, and autistic spectrum disorder.
Procedure
Diagnosis
The diagnoses of DSM-IV-TR ADHD and ODD were established through interviews conducted by board-certified senior child and adolescent psychiatrists, who followed the guidelines of K-SADS-PL (Kaufman et al. 2000).
The severity of ADHD was assessed by the clinician using the ADHD-RS (DuPaul et al. 1998a, 1998b). The severity of ODD was assessed using the K-SADS-PL (Kaufman et al. 2000).
Measures
Rating scales
ADHD-RS for ADHD
ADHD-RS is a clinician-rated, 18-item scale with one item for each of the 18 DSM-IV symptom criteria for ADHD, each rated on a severity scale of 0 (not present) to 3 (severe). The questionnaire's overall minimal score = 0 and maximal score = 54 (DuPaul et al. 1998a, 1998b). A larger score indicates higher severity of ADHD. The scale was administered by a clinician as a semistructured interview with the children and their parents at the first visit and again at the last one 3 months later, to monitor changes in ADHD symptom severity.
K-SADS-PL for ODD
Psychiatric diagnosis of ODD was established through semistructured clinical interviews of the children and their parents that followed the guidelines of the K-SADS-PL (Kaufman et al. 2000). None of the participants met the DSM-IV-TR criteria for CD.
EQ-C scale for empathy
EQ-C scale (27 Empathy items)—parent version, was derived from the combined EQ-C/Children's Systemizing Quotient (SQ-C) (Auyeung et al. 2009). This Likert-format questionnaire contains a list of statements about real-life situations, experiences, and interests that require empathizing abilities. Measures showed good test–retest reliability and high internal consistency. Responses that score 1 or 2 points are recorded, while other responses score 0. For total score, sum of all items was calculated. The higher the score on this scale the more empathic the person (Chapman et al. 2006). The EQ-C was completed by the parents.
MPH treatment procedure
All participants received daily doses of 0.5–1.0 mg/kg of MPH treatment. The daily doses did not exceed 60 mg/day. The trial was conducted for 12 weeks. At baseline (baseline, time point 0) and at endpoint (time point 12 weeks), the patients were assessed by both the ADHD-RS and the EQ-C scales. They did not receive any other treatment during the course of this trial.
Safety and tolerability
The safety and tolerability of the treatment were evaluated at baseline and at end point and also through spontaneous self-reports of adverse effects throughout the study period. Participants were able to report side effects by telephone at any time during the study.
Statistical analysis
Two-tailed, paired Student's t-test and Spearman's correlation test were used as appropriate. All results are expressed as mean ± standard deviation.
Results
ADHD-RS scores in the ADHD/ODD and ADHD groups
No significant pretreatment differences in ADHD severity, as assessed by the ADHD-RS, were found between the ADHD/ODD group (N = 26) and the ADHD group (N = 26), 17.8 ± 11.5 versus 21.8 ± 11; unpaired t = 1.30, df = 50, p = 0.22.
A significant reduction in the ADHD-RS scores was detected following MPH treatment in both the ADHD/ODD group (before and after: 17.8 ± 11.5 vs. 14.1. ± 8.6; paired t = 3.9, df = 25, p < 0.001) and the ADHD group (before and after: 21.8 ± 11 vs. 16.6 ± 8.5; paired t = 5.64, df = 25, p < 0.0001).
Baseline EQ-C scores in ADHD/ODD versus ADHD group
Significantly lower baseline EQ-C scores were observed in the ADHD/ODD (N = 26) group compared with the ADHD group (N = 26) (32.3 ± 8.4 vs. 38.3 ± 6.2, respectively; unpaired t-test, t = 2.9, df = 50, p = 0.005).
The impact of MPH treatment on EQ-C scores in the ADHD/ODD and ADHD groups
Attention-deficit/hyperactivity disorder
A modest, but statistically significant increase in the EQ-C scores was obtained in the ADHD group (N = 26) following MPH treatment (before vs. after: 38.3 ± 6.2 vs. 40.5 ± 5.9 paired t-test = 3.5, df = 25, p = 0.002).
Attention-deficit/hyperactivity disorder/ODD
A similar significant increase in the EQ scores was detected in the ADHD/ODD group (N = 26) following MPH treatment (before and after: 32.3 ± 8.2 vs. 36.2 ± 9.8; paired t = 3.25, df = 25, p = 0.003). The improvements in EQ levels (Δ) were similar in both groups (ADHD alone vs. ADHD/ODD 2.0 ± 3.0 vs. 3.9 ± 5.0; t = 1.66, df = 50, p = 0.10), thus it is unlikely that the existence of ODD moderated the response of EQ-C to MPH treatment.
Correlations
Significant correlation was found between the changes in ADHD-RS and EQ scores after MPH treatment in the ADHD group (Spearman's r = 0.47, p = 0.015), but not in the ADHD/ODD group (Spearman's r = 0.14, p = 0.48).
Discussion
The aim of the present study was to compare the baseline levels of EQ, as well as the changes in EQ levels following 3 months MPH treatment, in children diagnosed with ADHD to those with ADHD/ODD. The authors hypothesized that at baseline, the level of empathy as assessed by EQ-C would be larger in ADHD children than in ADHD/ODD children. Furthermore, it was assumed that EQ-C would be enhanced in the ADHD population by the MPH treatment, while no such finding was expected in the ADHD/ODD group.
The findings indeed showed the hypothesis to be true, as baseline EQ-C was found to be significantly lower in ADHD/ODD children in comparison to ADHD children.
In addition, the MPH treatment led to significant improvement in EQ in both the ADHD (p < 0.002) and ADHD/ODD (p < 0.003) groups. Thus it seems that ODD without comorbid CD does not interfere with the beneficial effect of MPH on EQ.
Improvement of empathy level in ADHD children without ODD was shown recently by Maoz et al. (2014). In that study, administration of MPH to children diagnosed with ADHD, but not ODD, was associated with improvement in cognitive and affective ToM, as well as in empathy functioning. Thus it appears that MPH has a beneficial effect on empathy irrespective of the absence or presence of ODD.
Strengths of the study
The strength of this study is in its examination of an understudied component of empathy in youngsters with ADHD, which may contribute to the social impairments that are commonly associated with ADHD. In addition, including a relevant comorbid condition (i.e., ODD) and comparing children with and without this comorbidity contribute to clarification of the relationship among ADHD, treatment with stimulants, and empathy.
Limitations
The main limitations of the current study are the open label design, the small sample size, the relatively short treatment duration (12 weeks), and the lack of long-term follow-up.
The ODD patients were diagnosed according to DSM-IV-TR criteria, but no additional assessment tools were used to evaluate subdimensional differences in this population, such as neurocognitive battery or specific questionnaires. It should be noted that the semistructured interview used in the current study, namely the K-SADS, provides a categorical diagnosis of ODD and is not a good indicator of its severity. In addition, both main outcome measures were parent-based (ADHD-RS and EQ-C) and may be biased by expectancy effects. Furthermore, the primary outcome of interest, namely empathy, was measured by the Empathy Quotient-Parent report. Thus, the results may reflect the parents' perception of their child's empathy. In addition, EQ-C has been validated in 4- to 11-year olds while the present study included adolescents. There is, however, a marked similarity between the EQ-C and the adolescent EQ scale that was developed later (Auyeung et al. 2012). Another limitation consists of the relatively low ADHD-RS scores at baseline and modest changes in ADHD symptoms (4–5 points on ADHD-RS) found in both groups. Those could be accounted for by time, as well as expectancy effects. These methodological weaknesses limit the ability to generalize the findings of the present study.
It is suggested that a future study with a similar design, investigating the impact of MPH treatment on empathy, should include children diagnosed with ADHD and CD with callous-emotional traits.
Conclusions
MPH treatment may bring a modest improvement in empathy of patients diagnosed with ADHD, whether comorbid or not with ODD. It is possible that empathy deficiency in ODD patients relates to multiple factors, including anxiety and callous-emotional traits. Unfortunately we did not measure real-life empathy functioning, thus it is unclear whether the modest improvement in EQ-C scores is clinically significant in youths diagnosed with ADHD with or without ODD.
Clinical Significance
In addition to the expected beneficial effect of MPH treatment on the core ADHD symptomatology in children and adolescents diagnosed with ADHD, but not with ODD, the treatment may also improve the level of empathy in this population.
Footnotes
Disclosures
No competing financial interests exist.