The effect of temperament and neuropsychological functioning on behavior problems in children with new-onset seizures
Introduction
Epilepsy is one of the most common neurological disorders in childhood and is associated with an increased risk for problems with adjustment, including behavioral and cognitive deficits [1], [2]. Children with seizures are nearly five times more likely to have behavior problems than control children and they have more behavior problems than children with other chronic conditions that do not involve the central nervous system [3], [4], [5], [6]. This increased risk has been shown to precede the first recognized seizure [7], [8]. Children with epilepsy tend to have more attention and internalizing behavior problems than externalizing problems [9], [10], [11].
Temperament refers to early appearing, biologically based characteristic patterns of emotional reactivity and self-regulation [12]. Specific temperamental factors have been shown to be risk factors for internalizing and externalizing problems both in healthy children and in children with seizures [13], [14], [15], [16]. In an earlier study of the present sample of children with new-onset seizures, 72.6% of whom have epilepsy, we showed that retrospectively assessed infant temperamental characteristics, such as difficultness (negative emotionality), unadaptability (negative reaction to novelty), and resistance to control (unmanageability), were related to both total and internalizing behavior problems, whereas only difficultness and resistance to control were associated with externalizing behaviors [14]. Although temperament was shown to be predictive of behavior at the time of seizure onset, it is unclear whether it remains predictive years after seizures have developed.
Children who have a chronic illness not involving the brain have less adaptive temperaments than healthy children [17]. Recent research has described the distinctive temperament and character patterns of children with epilepsy, including higher harm avoidance and lower persistence, self-directedness, and cooperativeness than healthy age- and sex-matched controls [18]. Seizure type had the greatest influence on temperament, with children with generalized seizures having higher scores on self-directedness, cooperativeness, and self-transcendence. The existing research describing temperament in populations with chronic conditions has not addressed how the onset of a child’s chronic illness may affect the child’s temperament or the parent’s perception of the child’s temperament.
Temperament components, such as effortful control, serve as an early reactive mechanism of controlling behavior [19]. As a child ages, this more reflexive means of control is affected by cortical development and increase in cognitive control capacities. Research has explored the relationship between self-regulatory behaviors that are related to temperament, such as effortful control, and those identified through neurocognitive models, such as attention and executive abilities [20], [21]. The development of executive skills is impacted by effortful control. Dysfunction in these cognitive control and attention abilities is implicated in the development of negative behavioral outcomes such as clinically significant attention problems and delinquent behaviors [22], [23].
Although neuropsychological deficits in children with epilepsy have long been recognized [8], [24], recent research has sought to identify risk factors for neuropsychological dysfunction at the time of seizure onset. Using the sample of children from the present study, Fastenau et al. [25] identified multiple risk factors including recurring seizures, use of antiepileptic drugs (AEDs), a symptomatic/cryptogenic seizure type, and EEG abnormality. Compared with sibling controls, children with new-onset seizures performed more poorly in all areas of neuropsychological functioning [25].
Executive functioning (EF) is a neuropsychological construct that refers to attention and behavioral control, among other cognitive capacities [26]. Children with seizures, including those with recent-onset seizures, score significantly lower than controls on nearly all measures of EF [6], [27] and were rated by parents as having more EF problems [6]. Poor performance on EF tasks was related to (1) overall cognitive functioning, (2) depressive symptoms, and (3) seizure variables, including epilepsy syndrome, age at onset, and AED treatment [27]. Even after accounting for overall cognitive functioning, children with seizures still had lower EF abilities [27]. This reduced cognitive ability may be related to poor behavioral outcomes. In a study of female adolescents with conduct problems, their EF mediated the relationship between temperament and aggressive behaviors; the combination of a difficult temperament and low executive functioning was strongly related to aggressive behaviors [28], supporting a potential moderating effect of neuropsychological functioning on temperament and behavior. Development of age-appropriate cognitive abilities, especially those that serve a self-regulatory function such as EF, may lessen the behavioral risk associated with negative temperaments.
Other neuropsychological constructs, such as language, may also play a role in the development of behavioral difficulties. Children with identified language impairments have a higher rate of behavioral and attention difficulties than children without these deficits [29]. In addition, children with complex partial seizures who had poorer verbal abilities also had more behavior problems [30]. Matheny [31] argued that children with specific temperaments may be more vulnerable to language impairments, thus affecting cognitive development in the area of verbal intelligence, and ultimately behavior. In a model proposed by Austin and Caplan [32], individual deficits in cognitive and linguistic abilities, along with epilepsy and family factors, have both direct and indirect effects on behavioral outcomes.
The present study had two aims: (1) to investigate the unique contributions of retrospectively assessed infant temperament and neuropsychological functioning assessed at seizure onset, specifically executive abilities and language, on behavior problems 3 years after the onset of seizures, and (2) to investigate the potentially moderating effect of neuropsychological functioning on the infant temperament–behavior relationship. Although other neuropsychological domains may contribute to later behavior problems, previous research suggests that the two constructs of executive functioning and language are likely to be the most predictive. It is hypothesized that more negative temperaments and lower neuropsychological functioning scores will be associated with more behavior problems. It is also hypothesized that the negative impact of an early negative temperament on later behavior problems is either enhanced when a child obtains low scores on tests of language and EF or reduced when the child has high language and EF test scores.
Section snippets
Participants
Children between the ages of 6 and 14 (M = 9.5 years, SD = 2.6) with a first recognized seizure were recruited as part of a 3-year longitudinal study to identify factors that predict children’s behavioral, social, and cognitive adaptation to epilepsy. The 350 children in the larger study were recruited from child neurology clinics in Cincinnati and Indianapolis (68.9%), from private neurologists in the community (10.5%), and through referrals from school nurses (20.6%). Children were excluded if
Results
As a group, the children in the present sample did not have overtly problematic infant temperaments, as judged by inspection of the mean scores on these measures [13]. For all three temperament dimensions, the means fell between 3 and 4 on the 7-point scale, with a score of 7 indicating a more negative temperament. Their IQ scores, as estimated by the K-BIT, were average (M = 104.32, SD = 12.66). Similarly, the participants had neuropsychological factor scores that were in the average range. Child
Discussion
Results revealed that negative temperamental characteristics were significant in predicting behavior problems three years after seizure onset. Unadaptability (novelty distress, perhaps an early marker of anxiety) predicted Internalizing Problems; and Resistance to Control (unmanageability, perhaps an early marker of impulsivity) predicted Externalizing Problems, as well as Total Behavior Problems. The previous study on the present sample of children found that all three temperament
Acknowledgments
This research was supported by Grant PHS R01 NS22416 from the National Institute of Neurological Disorders and Stroke to J.K.A. We acknowledge assistance from B. Hale as well as the Epilepsy and Pediatric Neurology Clinics at Riley Hospital, Indiana University Medical Center, and the Department of Neurology at Cincinnati Children’s Hospital Medical Center.
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