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Purpose: This study examined the severity and range of linguistic impairments in young, intermediate, and adolescent youth with epilepsy and how these deficits were associated with illness effects, nonverbal intelligence, psychopathology, and reading.
Methods: Tests of language, intelligence, achievement, and structured psychiatric interviews were administered to 182 epilepsy youth, aged 6.3–8.1, 9.1–11.7, and 13.0–15.2 years, as well as to 102 age- and gender-matched normal children. Parents provided demographic, seizure-related, and behavioral information on their children.
Results: Significantly more epilepsy subjects had language scores 1 standard deviation (SD) below average than the age-matched control groups did. The intermediate and adolescent epilepsy groups also had significantly lower mean language scores compared to their matched controls. The older compared to the younger epilepsy groups had more language impairment and a wider range of linguistic deficits. Longer duration of illness, childhood absence epilepsy, psychiatric diagnosis, and socioeconomic status were associated with linguistic deficits in the young group. Prolonged seizures, lower Performance IQ, and minority status predicted low language scores in the intermediate epilepsy group. In the adolescent group, language impairment was associated with poor seizure control, decreased Performance IQ, and lower socioeconomic status. Linguistic and reading deficits were significantly related in each epilepsy group.
Conclusions: The age-related increase in linguistic impairment, different profiles of predictors in each age group, and the relationship of linguistic deficits with poor reading skills have important clinical, developmental, theoretical, and academic implications.
Despite the importance of language in children’s academic performance [See review in (Schuele, 2004)] and social functioning (Beitchman et al., 1996; Conti-Ramsden & Botting, 2004; van Daal et al., 2007), this topic is understudied in children with epilepsy with normal intelligence. Although language measures, such as naming, verbal fluency, vocabulary, reading, and writing have been included in studies of the neuropsychological functioning and academic achievement of children with epilepsy (Fastenau et al., 2004; Aldenkamp et al., 2005; Hermann et al., 2006, 2007; Guimarães et al., 2007; Hermann et al., 2008), few have examined a wider range of basic linguistic skills. Moreover, most of the extant studies have been conducted on children with benign rolandic epilepsy (Staden et al., 1998; Gunduz et al., 1999; Lindgren et al., 2004; Monjauze et al., 2005; Northcott et al., 2005; Papavasiliou et al., 2005; Wolff et al., 2005; Northcott et al., 2006; Riva et al., 2007; Volkl-Kernstock et al., 2009), with only few studies on children with absence epilepsy (Henkin et al., 2003; Caplan et al., 2008), generalized epilepsy (Henkin et al., 2003), temporal lobe epilepsy (Schoenfeld et al., 1999; Caplan et al., 2004; Guimarães et al., 2007), and recent-onset epilepsy (Hermann et al., 2007). These studies demonstrate linguistic difficulties including impaired phonologic processing, verbal memory, auditory processing, verbal learning, and discourse skills.
Filling in the gap in our knowledge about language in pediatric epilepsy and its correlates is important for clinical, academic, and theoretical reasons. From the clinical perspective, this topic deserves attention because children with poor academic achievement and cognitive problems frequently have undiagnosed language difficulties (Im-Bolter & Cohen, 2007) as well as behavioral and emotional problems (Cohen et al., 1993; Handwerk & Marshall, 1998; Vallance et al., 1999; Fujiki et al., 2002; Gilmour et al., 2004; Corapci et al., 2006). In fact, children presenting to psychiatric clinics for both internalizing and externalizing behavior problems (Cohen et al., 1993; Vallance et al., 1999) and conduct disorders (Gilmour et al., 2004) often have undiagnosed language and social pragmatic problems. In addition, there is a high rate of behavioral and emotional problems (Cantwell & Baker, 1987; Beitchman et al., 1996; van Daal et al., 2007; Conti-Ramsden & Botting, 2008), as well as poor literacy (Conti-Ramsden & Durkin, 2007) in children with language disorders. Given frequent learning, behavior, and social problems in children with epilepsy [See reviews in (Austin & Caplan, 2007; Drewel & Caplan, 2007; Plioplys et al., 2007)], the diagnosis and treatment of associated language problems is essential for the clinical care of these children.
The lack of studies on language in pediatric epilepsy is also striking from the theoretical perspective in view of interest in how epilepsy is related to the lateralization of linguistic functions. Therefore, recent functional (Berl et al., 2005; Yuan et al., 2006) and structural imaging studies (Gaillard et al., 2007) indicate asymmetry of cortical activity during linguistic tasks and atypical lateralization of language in individuals with epilepsy, including children.
In addition, little information is available on the developmental impact of ongoing seizures, particularly age of onset, chronological age, and duration of illness, on the development of children’s language. Whereas some studies found a relationship of linguistic deficits with seizure variables (Schoenfeld et al., 1999; Caplan et al., 2004; Lindgren et al., 2004; Monjauze et al., 2005; Wolff et al., 2005), others have not confirmed these relationships (Northcott et al., 2005).
However, the interrelationship among seizure variables, cognition, and behavior [See review in (Austin & Caplan, 2007)] and relatively small sample sizes in prior studies preclude conclusions on how epilepsy might affect language development in children with epilepsy. Moreover, the protracted development of children’s linguistic skills from the toddler period through adolescence [See review in (Caplan, 1996)] and parallel ongoing maturation of language-related brain regions (Sowell et al., 2003; Gogtay et al., 2004) further underscore the importance of this developmental question.
To determine if linguistic deficits in children with epilepsy who have normal intelligence are associated with age or developmental stage, the study presented in this report compared language measures in a large sample of young, intermediate, and adolescent epilepsy subjects to those of age- and gender-matched children without epilepsy. In addition to age, it examined the role played by cognitive, psychopathology, seizure, and demographic variables in the linguistic skills of the epilepsy subjects in each age group. It also investigated the relationship between linguistic and reading deficits in the epilepsy subjects.
We hypothesized that children with epilepsy would have significantly impaired linguistic skills compared to children without epilepsy in the young, intermediate, and older age groups, controlling for Performance IQ differences. On the basis of the assumption that the brains of younger children with active developmental processes (Ben-Ari & Holmes, 2006), such as language, are more vulnerable to the effects of ongoing seizures than are those of older children, we predicted that the young epilepsy subjects would have significantly more linguistic impairments than the intermediate group, who in turn, would have more deficits than the older group. Because chronologic age, age of onset, and duration of illness are related developmental variables, we also examined which of these three variables were related to linguistic deficits within each age group.
In each epilepsy age group, we hypothesized that children with more severe illness would have significantly more linguistic deficits than those with less severe illness. Given the previously reviewed inconsistent relationship among illness severity, cognition, behavior, and language, we explored if, above and beyond effects of seizure variables, Performance IQ, psychopathology, and demographic variables (i.e., ethnicity, socioeconomic status) would be associated with language impairment. Finally, we posited an association of poor reading with impaired linguistic skills in each epilepsy age group.
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The study’s findings highlight the clinical, theoretical, developmental, and academic importance of studying language in youth with epilepsy, aged 6–15 years, who have average IQ scores. The significantly higher rate of language scores 1 SD below average in the three epilepsy groups should alert clinicians to the need for language evaluations in epilepsy youth with normal intelligence. In contrast to our developmental predictions, we found an increase in the rate of language impairment from about one-fourth in the young group to one-third in the intermediate group, and then to more than one-half of the adolescent epilepsy subjects. In addition, there was a wider range of linguistic deficits in the older epilepsy subjects, and the predictors of language impairment differed in the three age groups.
These findings imply an age-related rise in vulnerabilities to linguistic deficits as well as differential effects of seizure variables during the long protracted course of language development. Two lines of evidence help clarify our unpredicted developmental findings. First, despite intact syntactic and semantic skills by age 5, these skills continue to develop and undergo acceleration during adolescence with an increase in syntactic complexity, advanced use of grammar and vocabulary, as well as abstraction (Nippold et al., 2005, Ravid, 2006; Berman & Nir-Sagiv, 2007). Maturation of these skills is attributed to the parallel complex growth in thought, cognitive flexibility, and integration of knowledge (Nippold et al., 2005; Ravid, 2006; Berman & Nir-Sagiv, 2007).
The association of Performance IQ with language deficits in the intermediate and adolescent epilepsy groups also implies that skills tapped by Performance IQ subtests might play a role in the accelerated integration of language and thought in the older children. Although Performance IQ and its associated functions did not independently contribute to impaired language in the young epilepsy group, TOLD-P and WISC Performance IQ subtests might not tap the same skills.
Second, corresponding development, first of the frontal and then the temporal lobe during adolescence and young adulthood, involves language-related regions (inferior frontal and superior temporal gyri) (Sowell et al., 2003; Gogtay et al., 2004). Given the role of the frontal lobe in executive function (Alvarez & Emory, 2006) and both the frontal and temporal lobes in basic and higher level linguistic functions (Poldrack et al., 1999; Bookheimer, 2002), these brain regions participate in the previously described integration of language and cognition (i.e., thought processes) (Hagoort et al., 2004).
Therefore, our findings suggesting increased rather than decreased vulnerability of linguistic functions to the ongoing effects of seizures with age, might reflect the continued, active development of these brain regions. However, prospective language and imaging studies that replicate our cross-sectional findings are warranted to confirm this explanation. Furthermore, different subtests in the TOLD-P, TOLD-I, and TOAL probably contributed to the wider and different range of linguistic deficits and predictors in the three epilepsy age groups.
Yet, the different profile of the correlates of impaired language in the three epilepsy age groups, as found for the higher level linguistic deficits of children with CPS and CAE (Caplan et al., 2006), suggest changing vulnerability during the prolonged parallel development of language and language-related brain-related structures (Gogtay et al., 2004). In the current study, the association of increased duration of epilepsy with five of the six linguistic measures (e.g., Spoken Language, Listening, Semantics, Syntax, and Phonology) in the young group implies that continued illness impacts all aspects of ongoing language development in young children. In addition, significantly more young children with CAE than CPS with listening deficits might represent the attentional impairment (Levav et al., 2002) and predominant dorsolateral prefrontal involvement (Holmes et al., 2004) found in CAE.
Although the intermediate epilepsy group did not have a higher rate of prolonged seizures than the other epilepsy groups (Table 2), this seizure variable was significantly related to lower Spoken Language, Listening, Speaking, Semantics, and Syntax quotients in this age group. The association of linguistic deficits with a history of prolonged seizures might be similar to the evolving, long-term effect of prolonged seizures on cognitive and learning deficits in animals [See reviews in (Ben-Ari & Holmes, 2006) and (Sankar & Rho, 2007)].
In the adolescent epilepsy group, the relationship of lower language scores with poor seizure control is analogous to increased higher-level linguistic deficits in older children with CPS who had worse seizure control (Caplan et al., 2006). Poor expressive language in adolescents with longer duration of illness and increased deficits in overall language, writing, vocabulary, and grammar in those with poor seizure control further highlight the linguistic vulnerability of adolescents with epilepsy.
Independent of the reported relationship between illness severity and IQ in children with epilepsy (Caplan et al., 2004, 2008; Pulsipher et al., 2009), the association of both Performance IQ and demographic variables (i.e., ethnicity, SES) with language deficits is reported in children without epilepsy who have language impairment (Im-Bolter & Cohen, 2007; Beitchman et al., 2008). Clinically, these findings underscore the importance of language testing in youth with epilepsy with lower IQ scores and who come from minority and economically disadvantaged families.
Unlike our psychopathology predictions, the presence of a psychiatric diagnosis was significantly related to linguistic deficits only in the young group. The relationship between poor phonology skills and the presence of an affective/anxiety disorder in the young group is interesting for several reasons. First, phonologic processing is an important first-stage process in language learning in young children (Bishop, 1997). Second, phonologic difficulties are associated with reading deficits in children without epilepsy [See review in (Schuele, 2004)] and in children with epilepsy (Chaix et al., 2006; Northcott et al., 2007). Third, young children without epilepsy with phonologic difficulties are rated by their parents on the Child Behavior Checklist (Achenbach, 1991) as anxious and withdrawn (van Daal et al., 2007). These findings further emphasize the clinical importance of testing language and reading in young children with epilepsy, particularly if they have affective/anxiety disorders.
From the academic perspective, the association of impaired language with poor literacy is described in cross-sectional (Conti-Ramsden & Durkin, 2007) and prospective data [See review in (Schuele, 2004)] of children without epilepsy who have language impairment and in a large sample of 173 children with epilepsy who had both low reading and writing achievement scores (Fastenau et al., 2004). As children go from elementary to middle and then to high school, there is greater demand on their language-based learning skills (i.e., reading, writing). Undiagnosed and untreated linguistic deficits might, therefore, play an important role in the poor long-term educational outcome of pediatric epilepsy (Sillanpaa et al., 1998; Wirrell, 2003).
Study limitations include language test construction, sample size, illness variables, cohort effects, and cross-sectional study design. Different subscales and subscale definitions in the TOLD-P, TOLD-I, and TOAL, together with the small sample size of the adolescent epilepsy group, limit generalization of the study’s developmental findings. Few adolescent CAE subjects (Table 2) also preclude reaching conclusions on the lack of an association of language impairment with type of epilepsy in adolescence.
In addition, parents’ report on seizure variables, including prolonged seizures could be subject to memory loss, particularly in the parents of the older children. No evidence for a relationship of language scores with lateralization and localization of epileptic activity in the EEG of the CPS subjects should be confirmed with concurrent EEG data. Significantly higher language scores in the new versus old normal intermediate and adolescent cohorts might have contributed to the between-group language score differences (i.e., epilepsy < normal). Finally, although our findings suggest age-related differences in the severity, range, and predictors of linguistic deficits in children with epilepsy, they need to be replicated using the same language instrument across ages by a prospective rather than a cross-sectional study.
Notwithstanding these limitations, the age-related higher rate of language impairment, wider range of linguistic deficits, and different association with seizure and Performance IQ variables together with the relationship with poor reading have important clinical, developmental, theoretical, and academic implications. Most importantly, these findings underscore the need for language assessment and intervention for a wide age range of children with epilepsy with average intelligence.