Executive functioning and social skills in children with epileptic seizures and non-epileptic seizures

Highlights

• No significant differences were observed on measures of executive functioning between children with ES and children with NES.

• Parent reports of poorer behavioral regulation correlated to parent reports of poorer social skills in both groups (ES and NES).

• Parent and child ratings of executive functioning did not correlate with child-reported social skills.

Abstract

Children experiencing epileptic seizures (ES) and children experiencing non-epileptic seizures (NES) may experience deficits in both executive functioning and in social skills, but little research has examined differences in executive functioning between the two groups and no studies have examined the relationship between executive functioning and social skills in pediatric ES and NES groups. The purposes of this study were to determine if ES/NES group differences exist for executive functioning and to determine if executive functioning was related to social skills in these groups. Children (N = 43) were recruited from epilepsy monitoring units (EMU) at Primary Children’s Medical Center and Phoenix Children’s Hospital. The NES group consisted of 15 participants (67 % female, M age at test = 12.62, SD = 3.33), and the ES group consisted of 28 participants (50 % female, M age at testing = 11.79, SD = 3.12). Parents and children completed the Social Skills Improvement System (SSIS) Rating Scales, and the Behavior Rating Inventory of Executive Function (BRIEF). No significant differences on measures of executive functioning were observed between ES and NES groups. Parent reports of poorer behavioral regulation correlated to parent reports of poorer social skills in both groups, but neither parent nor child ratings of executive functioning correlated with child-reported social skills. This finding suggests there may be differences between parent and child self-observations of executive functioning and social skills in both NES and ES groups. Limitations to this study and directions for future research are discussed.

Introduction

Epileptic seizures are a brain disease characterized by two reflex seizures occurring more than 24 h apart, by one reflex seizure and a probability (60 % of higher) of future seizures in the next ten years after two unprovoked seizures, or by the diagnosis of an epilepsy syndrome (Fisher et al., 2014). Studies have found the prevalence of epilepsy in children in the United States to be about 0.6 %, with the rate being higher in older, male children, and in lower-income families (Russ et al., 2012, Centers for Disease Control, 2016). Children with non-epileptic seizures do not present with epileptiform activity but do present with semiology features like children with epileptic seizures (Szabó et al., 2012; Perez and LaFrance, 2016; Reilly et al., 2013). One study found the incidence of PNES to be 4.90/100,000/year across all ages (Duncan et al., 2011). There is some evidence that among NES patients, between 10 % and 73 % experience comorbid NES and ES (Benbadis et al., 2001, Bowman, 1998), with a recent meta-analysis illustrating that the frequency of epilepsy among those of mixed adult-child populations with PNES was 22 %, while the frequency of PNES among those with epilepsy was 12 % (Kutlubaev et al., 2018).

There is evidence to suggest that children with epilepsy and children with non-epileptic seizures experience deficits on global measures of executive functioning when compared to typically developing peers (Zhang et al., 2018, Modi et al., 2019, Cragar et al., 2002, MacAllister et al., 2012, Campiglia et al., 2014, LaFrance, 2008, Strutt et al., 2011, Karaaslan and Hamamcı, 2020). Research in adults has suggested that there are no significant differences between epilepsy and NES groups on measures of executive functioning, attention, memory, or verbal or visuospatial abilities (Cragar et al., 2002, Turner et al., 2011). Only one study has examined differences in neuropsychological functioning in children with epilepsy and children with NES, reporting that children in the epilepsy group performed significantly worse on measures of orientation, delayed recall, and executive functioning than children with NES (Karaaslan and Hamamcı, 2020). While this suggests that differences in executive functioning may exist between ES and NES groups, significantly more research is needed to better understand executive functioning deficits in both groups.

There is evidence to suggest that children and adults with epilepsy experience poor long-term social outcomes (Wirrell et al., 1997, Jalava et al., 1997, Camfield et al., 1993), with less than a third of children and adults with epilepsy attending school or work regularly (Reuber et al., 2003, Sri et al., 2008). For children with epilepsy that do attend school, studies have shown that they have higher rates of behavioral problems when compared to their typically developing peers (Gebauer-Bukurov et al., 2015; Stewart et al., 2019; Lew et al., 2015; Zhao et al., 2014; Raud et al., 2015). However, other studies have shown that while children with epilepsy experience more difficulty understanding sarcasm, intentional lying, and false belief, their overall social skills are not significantly different than those of their typically developing peers (Tse et al., 2007). Some have proposed that verbal intelligence, parental anxiety, learning disability, and family function are better predictors of social skills in children with epilepsy than their epilepsy diagnosis (Tse et al., 2007, Carson and Chapieski, 2016). Only one study has examined psychosocial differences between children with ES and children with NES, and it found that children with NES had more relational problems, had suffered more trauma and abuse, had lower self-esteem, and had higher psychiatric comorbidity rates than children with ES (Say et al., 2014). It is important to understand the relationship between ES, NES, and social skills because diminished social skills may lead to impaired interpersonal functioning and decreased quality of life (Nickels et al., 2016, Caplan, 2019).

Modi et al. (2019) found that children with epilepsy experiencing global executive functioning deficits also experienced worse psychosocial functioning. A similar study found that children with epilepsy performed worse than typically developing peers on measures of executive functioning, attention, and verbal and fine motor tasks; these children also experienced more problems with memory tasks and understanding sarcasm (Raud et al., 2015). It has been suggested that some measures typically believed to measure executive functioning may instead be indicating general impairment, including social skills impairment (McAuley et al., 2010). Children with epilepsy experience both executive functioning and social skills deficits, but there is less evidence of these deficits in children with NES. The reasons linking impaired executive functioning to impaired social skills in children with epilepsy and children with non-epileptic seizures have not been adequately detailed in existing literature.

There is limited research examining executive functioning and social skills deficits in children with ES and NES. Existing research has focused on outcome measures like IQ and achievement, and has failed to address contributing factors (i.e., executive functioning) that may influence the development of appropriate social skills. The first aim of this study was to identify group differences between children with ES and NES on measures of executive functioning. It was hypothesized that children with ES would demonstrate lower executive functioning than children with NES, consistent with the existing research showing children with ES exhibit worse neuropsychological functioning than children with PNES (Karaaslan and Hamamcı, 2020). The second aim of this study was to determine if executive functioning was related to social skills. It was hypothesized that executive functioning would be negatively correlated with social skills scores on the SSIS Social Skills Scale; in other words, it was hypothesized that better executive functioning would be associated with better social skills.