Parent-rated emotional–behavioral and executive functioning in childhood epilepsy
Introduction
Childhood epilepsy is often associated with psychiatric disorders such as attention deficit hyperactivity disorder (ADHD), depressive disorders, and anxiety disorders [1]. Based on diagnostic interviews in clinically referred samples, studies have identified comorbidity rates of 26–40% for ADHD, 27–36% for anxiety disorders, 13–23% for depressive disorders, and 13% for oppositional defiant disorder [2], [3], [4]. Within a community sample of children and adolescents with epilepsy [5], the comorbidity rate was 21% for ADHD, 13% for depressive disorders, 5% for anxiety disorders, and 5% for oppositional defiant disorder/conduct disorder (ODD/CD). Initial research hypothesized that such neurobehavioral comorbidities of epilepsy were primarily due to consequences of stigmatization, life obstacles, and other psychosocial stressors. However, the more recent theory in the field is that the shared underlying neurobiologic pathogenic mechanisms responsible for the manifestations of seizures play a large role in neurobehavioral comorbidities [6], [7], [8], [9]. Neurobehavioral comorbidities appear to be the rule rather than the exception in epilepsy, with challenges frequently identified in emotional, cognitive, and social functioning [7], [10]. Given the identified shared genetic pathways with other neurodevelopmental disorders as well as the frequency of these neurobehavioral comorbidities, epilepsy has more recently been classified as a neurodevelopmental disorder, as have autism spectrum disorders, intellectual disability, and schizophrenia [6], [11].
Neuropsychological evaluation can be an effective clinical tool in the delineation of difficulties in emotional–behavioral and executive functioning, two neuropsychological domains frequently involved in a range of psychiatric conditions [12], [13], [14]. One method of assessing emotional–behavioral and executive functioning is parent-rating forms, which have proven effective in the assessment of childhood conditions such as ADHD, depressive disorders, and anxiety disorders [12]. Because of their clinical effectiveness, as well as brevity and cost-efficiency, rating forms have been frequently used in children with epilepsy to identify psychiatric comorbidities [15]. While a complete review of studies using rating forms in childhood epilepsy is beyond the scope of this article, Rodenburg and colleagues [16] conducted a meta-analysis on the use of rating forms (parent, teacher, and self) to assess emotional–behavioral functioning in childhood epilepsy. Results indicated medium to large effect sizes across symptoms of psychopathology, most notably in attention problems, thought problems, and social problems.
A few studies to date have used the Behavior Assessment System for Children—Second Edition—Parent Report Scales (BASC-2-PRS) [17] to assess emotional–behavioral functioning in childhood epilepsy [15], [18], [19], [20]. While each research group uniquely studied emotional–behavioral functioning in their respective samples, the studies generally identified elevated symptoms across the domains of internalizing problems, externalizing problems, and behavioral symptoms. For example, within a mixed clinical sample, Clary and colleagues [20] identified the most frequently occurring clinical elevations in the subdomains of atypicality (45%), withdrawal (37%), and depressive symptoms (29%). In another study, Bender and colleagues [15] identified clinical elevations in the domains of externalizing problems in 7%, behavioral symptoms in 10%, and internalizing symptoms in 19% of their mixed clinical sample. Within a sample of childhood absence epilepsy, Vega and colleagues [18] identified clinical elevations in the subdomains of anxiety (11%) and depression (24%). Additionally, at least three studies have used the Behavioral Rating Inventory of Executive Function (BRIEF) [21] parent-report form to assess the everyday or behavioral components of executive functioning in a mixed clinical sample of children with epilepsy, in a sample of children with intractable epilepsy, and in a group with idiopathic epilepsy (generalized and location-related) [22], [23], [24]. Broadly, these studies identified significantly elevated symptoms in their samples with epilepsy across BRIEF domains and subdomains, reflecting significant executive functioning difficulties in the everyday behaviors of these children and adolescents.
The majority of research studies have not found epilepsy-related variables to be significantly associated with emotional–behavioral functioning in children and adolescents with epilepsy [1], [4], [25], [26], [27], [28]. However, while the sum of the research is inconclusive, a few studies have identified some specific relationships between epilepsy variables and select outcomes. For example, younger age at seizure onset and longer duration of epilepsy have been associated with the presence of anxiety disorders as well as anxiety and depressive symptoms [4], [19], [27]. Seizure frequency/severity and medication status (polytherapy versus monotherapy) have been associated with the presence of internalizing disorders as well as anxiety and depressive symptoms [5], [27], [29]. Further, temporal lobe seizure foci have been associated with increased behavioral problems and diagnosis of depression [2], localization-related seizures have been associated with tic disorders and depressive disorders, generalized seizures have been associated with conduct disorder, and childhood absence epilepsy has been associated with anxiety disorders [3], [4]. Associations have also been examined between epilepsy-related variables and executive functioning using both performance-based and parent-report measures [23]. MacAllister and colleagues identified significant associations between epilepsy-related variables (seizure frequency, number of antiepileptic drugs [AEDs], and age at epilepsy onset) and performance-based executive functions (impulsivity and total time of problem solving). In contrast, they found no associations between epilepsy-related variables and parent-rated executive functioning (i.e., BRIEF) [23]. In sum, more information is needed regarding the variables or factors that are responsible for such neurobehavioral comorbidities [4] in order to provide clinicians with appropriate information on how to accurately identify and treat those patients who are at increased risk for such comorbidities.
This study aimed to provide clarity to prior inconsistent research findings by examining clinical and demographic risk factors associated with parent-rated emotional–behavioral and executive functioning in children and adolescents with epilepsy within a large clinically referred mixed sample. The present study sought to examine the potential influence of demographic, family history, and epilepsy-related variables on emotional–behavioral functioning (internalizing and externalizing problems and behavioral symptoms) and executive functioning (metacognition and behavior regulation) as measured by parent-rating scales. While the BASC-2 and BRIEF have previously been studied in childhood epilepsy, the current study simultaneously assessed the factors associated with both scales within a large mixed clinical sample to provide a more cohesive understanding of emotional–behavioral and executive functioning in childhood epilepsy.
Section snippets
Participants
Institutional Review Board approval was obtained through the Johns Hopkins University School of Medicine. Three hundred forty-one children, adolescents, and young adults with epilepsy consecutively referred for neuropsychological evaluation at the Kennedy Krieger Institute (KKI) between 2009 and 2014 were considered for inclusion in the present study. Participants were generally referred for neuropsychological evaluation to characterize cognitive functioning and guide treatment planning.
The
Results
All domain scores on the BASC-2 and BRIEF were significantly higher in the group with epilepsy than published normative data, including BRIEF GEC (p < .001), BRIEF MCI (p < .001), BRIEF BRI (p < .001), BASC-2 Externalizing Problems (p < .01), BASC-2 Internalizing Problems (p < .001), and BASC-2 BSI (p < .001). Percentages of participants scoring in the clinical range extended from 8.9% (BASC-2 Externalizing Problems) to 46.9% (BRIEF MCI). Almost a quarter of the sample had at least one clinical elevation
Discussion
Given prior inconsistent research findings, the present study examined clinical and demographic risk factors associated with parent-rated emotional–behavioral and executive functioning in children and adolescents with epilepsy. This is the first study to our knowledge that has examined and successfully identified such risk factors for emotional–behavioral and executive functioning dysfunction within a large outpatient sample of patients with childhood epilepsy. The following can summarize the
Conclusions
In conclusion, childhood epilepsy is often characterized by emotional–behavioral and executive functioning difficulties, yet the mental health needs of these young people continue to go underserved. The present study identified seizure-related and demographic variables associated with parent ratings of emotional–behavioral and executive functioning, specifically seizure status, age at evaluation, and family psychiatric history. Assessing these variables in the clinical treatment of childhood
Conflict of interest
We wish to confirm that there are no known conflicts of interest associated with this publication.
References (39)
- et al.
Psychiatric and neurodevelopmental disorders in childhood-onset epilepsy
Epilepsy Behav
(2011) - et al.
Heredity in epilepsy: neurodevelopment, comorbidity, and the neurological trait
Epilepsy Behav
(2011) - et al.
Uncovering the neurobehavioural comorbidities of epilepsy over the lifespan
Lancet
(2012) - et al.
Depression and epilepsy: epidemiologic and neurobiologic perspectives that may explain their high comorbid occurrence
Epilepsy Behav
(2012) - et al.
The neurobehavioural comorbidities of epilepsy: can a natural history be developed?
Lancet Neurol
(2008) - et al.
Early screening and identification of psychological comorbidities in pediatric epilepsy is necessary
Epilepsy Behav
(2012) - et al.
Examining health-related quality of life, adaptive skills, and psychological functioning in children and adolescents with epilepsy presenting for a neuropsychological evaluation
Epilepsy Behav
(2010) - et al.
Anxiety and depression in children with epilepsy and their mothers
Epilepsy Behav
(2004) - et al.
Symptoms of depression in adolescents with epilepsy
J Am Acad Child Adolesc Psychiatry
(1999) - et al.
Psychopathology in children and adolescents with epilepsy: an investigation of predictive variables
Epilepsy Behav
(2008)