Executive and behavioral functioning in pediatric frontal lobe epilepsy

Highlights

• Parents and teachers report significant executive dysfunction and behavioral problems in pediatric frontal lobe epilepsy.

• There is a strong link between executive and behavioral functioning in pediatric FLE.

• Parents as well as teachers report executive dysfunction and behavioral problems to the same extent.

• Anxiety and depression are not much reported in pediatric FLE.

Abstract

Objective

Epilepsy, as a chronic and neurological disease, is generally associated with an increased risk for social and emotional behavior problems in children. These findings are mostly derived from studies on children with different epilepsy types. However, there is limited information about the associations between frontal lobe epilepsy (FLE) and cognitive and behavioral problems. The aim of this study was to examine relationships between FLE and executive and behavioral functioning reported by parents and teachers.

Material and methods

Teachers and parents of 32 children (18 boys, 14 girls, mean age 9; 2 years ± 1;6) with a confirmed diagnosis of FLE completed the Behavioral Rating Inventory of Executive Function (BRIEF), the Child Behavior Checklist (CBCL), and Teacher Report Form (TRF).

Results

About 25 to 35% of the parents and teachers rated children in the abnormal range of the main scales of the BRIEF, CBCL, and TRF. Teachers tend to report more metacognition problems, whereas parents tend to report more behavior regulation problems. Children with left-sided FLE showed more problems than children with bilateral or right-sided FLE. The whole range of executive dysfunctioning is linked to behavioral dysfunctioning in FLE, but ratings vary across settings and informants. The epilepsy variables age of onset, lateralization, drug load, and duration of epilepsy had only a small and scattered contribution.

Conclusion

Ratings on the BRIEF, CBCL, and TRF are moderately to highly correlated, suggesting a (strong) link between executive and behavioral functioning. Subtle differences between parents and teachers ratings suggest different executive function demands in various settings.

Introduction

Epilepsy is the most common neurological condition in childhood with a prevalence of 4–10 per 1000 [1]. Research on psychiatric comorbidity is extensive, and it is well-recognized that epilepsy as a chronic and neurological disease is associated with an increased risk (up to 60%) of social and emotional behavior problems in children [2], [3]. Common comorbidities include attention-deficit/hyperactivity disorder (ADHD), autism, anxiety problems, and depression [4], [5], [6], [7], [8], [9]. These problems are often present around the time of diagnosis, diminish over time [10], and appear to be associated with neurologic dysfunction, severe seizures [2], and family dysfunction [11].

Most studies have focused on temporal lobe epilepsy (TLE) because it is the most frequent type of epilepsy [12], [13]. We question the generalizability of findings to other types of epilepsy, in particular, frontal lobe epilepsy (FLE); TLE and FLE differ with respect to localization and functionality. To date, there is evidence for association between FLE and attention and inhibition problems, social cognitive problems, and aggression [13], [14], [15], [16], [17]. Executive functions (EF) are mainly localized in the frontal lobe and is an ‘umbrella’ term for the management (regulation, control) of cognitive processes like attention, inhibition, initiation of activity, working memory, mental flexibility, planning and organization, and problem solving strategies [18]. It consists of the capacities that enable a person to engage successfully in independent, purposive, self-directed, and self-serving behavior [19]. There is growing evidence of neuroimaging studies that frontal lobe epilepsy leads to structural and functional disorders [12], [13]. Also, seizures as well as interictal epileptic discharges are increasingly recognized to interfere with physiological brain circuitry [12], which in the long term can result in chronic cognitive and behavioral comorbidity [12], [13], [20]. Frontal lobe epilepsy could therefore lead to executive function problems, which can be expressed in behavioral problems and social and academic failure [6], [13], [20], [21], [22], [23], [24]. Furthermore, TLE and FLE differ with respect to seizure characteristics. In FLE, nocturnal seizures are far more frequent than in TLE, and therefore, poor quality of sleep is common. This factor on its own may be associated with a variety of behavioral and cognitive problems [25], [26], [27].

It is therefore worthwhile exploring executive and behavioral functioning and their interaction in pediatric FLE. Since clinically used performance-based measures do not always have good sensitivity and specificity, the use of parent and/or teacher-proxy measures is generally accepted for measuring emotional and behavioral problems. The Behavioral Rating Inventory for Executive Function (BRIEF) has rarely been used in studies on children with epilepsy; however, a few authors mention inclusion of FLE [28], [29], [30], usually reporting frequent executive dysfunction. Reports from parents as well as teachers are complementary for the BRIEF [31], but have only been studied in one study [28]. The Child Behavior Checklist (CBCL) and Teacher Report Form (TRF) are questionnaires, which are used extensively in pediatric epilepsy showing elevated scores [32], [33], and considered to be a valid instrument for measuring behavioral problems in children with epilepsy [34]. This has been sparsely studied in children with FLE [34], [35], [36]. Finally, the influence of epileptic lateralization, age of onset, duration of epilepsy, and drug load are evaluated.