East Asian Arch Psychiatry 2017;27:106-14

ORIGINAL ARTICLE

Psychiatric and Behavioural Problems in Children and Adolescents with Epilepsy
KA Salayev, B Sanne, R Salayev

Dr Kamran Ali Salayev, MD, PhD, Azerbaijan Medical University, Baku, Azerbaijan.
Dr Bjarte Sanne, MD, PhD, Medina Medical Center, Baku, Azerbaijan. Dr Rustam Salayev, MD, National Psychiatry Center, Baku, Azerbaijan.

Address for correspondence: Dr Kamran Ali Salayev, Azerbaijan Medical
University, 100 Mardanov Qardaslari Street, Baku, Azerbaijan. Tel: (994-50) 4938 544; Email: ksalayev@yahoo.com

Submitted: 9 June 2016; Accepted: 25 February 2017


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Abstract

Objective: To investigate the psychiatric and behavioural symptoms in children and adolescents with epilepsy.

Methods: Patients with epilepsy and aged 4 to 16 years were recruited from a medical centre in Azerbaijan during January 2012 to December 2013. A community sample was drawn from 3 schools as the comparison group. The Strengths and Difficulties Questionnaire (SDQ) was administered to parents of both patients with epilepsy and children in the comparison group. The total difficulties score and the scores for each subscale were compared between the 2 groups. Additionally, scores between different groups of epileptic patients were compared.

Results: A total of 409 patients with epilepsy and 515 children in the comparison group were recruited. Those with epilepsy had a significantly higher mean total difficulties score and mean difficulties subscale scores (p < 0.001). In epileptic children with severe mental or physical disabilities, prosocial behaviour scores were significantly lower than those in the comparison group. The proportion of children with a total difficulties score in the abnormal range was higher in the epilepsy group than in the comparison group (53.1% vs. 15.7%; p < 0.001). Children with symptomatic epilepsy showed a higher total difficulties score than those with idiopathic epilepsy (p < 0.05).

Conclusion: Children with epilepsy have a higher rate of psychiatric and behavioural symptoms. These rates are even higher in children with symptomatic epilepsy.

Key words: Child; Child behavior disorders; Epilepsy; Surveys and questionnaires

Introduction

The risk of psychiatric and behavioural disorders is higher in children with epilepsy than in the normal paediatric population as well as in children with other chronic conditions.1-5 Children with epilepsy are more likely to experience mental health and developmental co-morbidities than the general population. The higher rate of emotional disorders, attention-deficit hyperactivity disorders (ADHD), and autistic spectrum disorders among children with epilepsy has been reported in several studies.4,6-8 Despite the high prevalence of behavioural and psychiatric problems in children with epilepsy, mental disorders often remain undiagnosed and children’s psychiatric needs are largely unmet.9-11

Screening of children with epilepsy to identify behavioural and psychiatric disorders may improve their quality of life.6,12,13 The impact of difficulties on daily life might be greater for adolescents with epilepsy than for those without.14 Patients with epilepsy, however, constitute a heterogeneous group because of different aetiologies (idiopathic or symptomatic) and manifestations (localisation- related or generalised seizures) of their disorder, and some of them might be at a higher risk than others for mental disorders. Therefore, identifying children / adolescents with epilepsy with an increased risk for psychiatric disorders is important in order to provide comprehensive care.

This study aimed to investigate the psychiatric and behavioural symptoms in children / adolescents with epilepsy. We hypothesised that psychiatric and behavioural problems would be more prevalent among children / adolescents with epilepsy than those without, and that children / adolescents with symptomatic epilepsy would have more problems than those with idiopathic epilepsy.

Methods

Participants

Children and adolescents with epilepsy were recruited during January 2012 to December 2013 from outpatients referred to Medina Medical Center in Azerbaijan, a primary care facility for children with neurological and psychiatric disorders as well as for general paediatric patients. Medina Medical Center serves children of all socio-economic status and most of the referred patients were residents of Baku city.

Individuals were eligible for the study if they were aged 4 to 16 years, and have a confirmed diagnosis of epilepsy or presented with seizure episodes and were suspected of having epilepsy but did not have a definitive diagnosis of epilepsy. Children with febrile convulsions and convulsive syncope were excluded from the study.

Epileptic syndromes were diagnosed according to the 1989 International League Against Epilepsy classification.15 Patients with epilepsy were divided into the following subgroups:

(1) Idiopathic localisation-related epilepsy (ILE);
(2) Idiopathic generalised epilepsy (IGE);
(3) Symptomatic or cryptogenic epilepsy without severe mental or physical disability (severe mental delay, cerebral palsy, neurodegenerative disorders, etc.) [SE];
(4) Symptomatic epilepsy with severe mental or physical disability (SE+); and
(5) Suspected epilepsy (e.g. patients with only one seizure and normal electroencephalography and neuroimaging) or an undetermined form of epilepsy (undetermined cause or epileptic syndrome) [S/UE].

We used a large community sample as the comparison group, which was drawn from the 1st, 5th, and 10th grades of 3 government schools in Baku city. The students in these schools represent all levels of socio-economic status. There was no indication that the epilepsy and comparison groups differed with regard to socio-economic level.

This study was approved by the Ethics Commission of Azerbaijan Psychiatric Association and written informed consent was obtained prior to the study.

Assessments and Instruments

The Strengths and Difficulties Questionnaire

The Strengths and Difficulties Questionnaire (SDQ) is a screening measure that is brief and easy to administer.16,17 Its validity and reliability have been shown in western18-25 and non-western countries.26-30 The SDQ is available online and can be downloaded free of charge from <www.sdqinfo. com>.

The SDQ consists of 25 items that are divided into 5 subscales — 4 are related to difficulties (hyperactivity / inattention, emotional symptoms, peer relationship problems, and conduct problems) and 1 to strengths (prosocial behaviour). For all the subscales except the prosocial behaviour subscale, high scores indicate difficulties. Each subscale consists of 5 items, each of which is rated on a 3-point scale (‘not true’, ‘somewhat true’, and ‘certainly true’ and these are scored 0, 1 or 2, respectively, giving a total score out of 10 for each subscale).

The SDQ total difficulties score is obtained by summing the scores of all 4 difficulties subscales with a range of 0 to 40 points. The total difficulties score and a score for each of the 5 subscales can be separately calculated.

Azeri Version of the Strengths and Difficulties Questionnaire

A group of researchers translated the original SDQ version into Azeri for respondents aged 4 to 17 years, and author of the SDQ revised the back-translation and compared it with the original questionnaire.16 The Azeri version of the SDQ discriminates well between high-risk and low-risk groups.31

It is also an effective screening instrument for psychiatric problems in children with active epilepsy.6 Another advantage of using the SDQ is that children with abnormal SDQ scores can be further assessed by the Development and Well-Being Assessment, which is a package of interviews, questionnaires, and rating techniques designed to generate psychiatric diagnoses in patients age 5 to 17 years (http://www.dawba.info).

In order to investigate the prevalence of psychiatric and behavioural problems in Azerbaijani children with epilepsy, we administered the Azeri version of the SDQ to the parents of the epilepsy and comparison groups. For the epilepsy group, the questionnaires were completed by the parents before meeting the doctor. For the comparison group, parents of the children were asked to return the completed questionnaire to the teacher. The differences in SDQ scores between the epilepsy group and the comparison group, as well as between several subgroups of epileptic patients were studied.

Statistical Analysis

We analysed the data of the total difficulties score, the 4 difficulties subscale scores (hyperactivity / inattention, emotional symptoms, peer relationship problems, and conduct problems), and the strength subscale score (prosocial behaviour). Statistical analyses were performed using SPSS (Windows version 19.0; IBM Corp, Armonk [NY], US).

We performed independent-samples t tests for the total difficulties score and the 5 subscale scores in the whole epilepsy group as well as for subgroups of epileptic patients. We also used independent-samples t test to investigate the differences between subgroups of epileptic patients (ILE and IGE vs. SE; and ILE vs. IGE).

The total difficulties score and the difficulties subscale scores were categorised as ‘normal’, ‘borderline’, or ‘abnormal’ based on normative data cut-off values.16 Since there are no available norms for the Azeri version of the SDQ, Goodman’s cut-off values16 that have already been applied in an Azeri population were used.31 The Chi-square independence (χ2) test was applied to analyse the difference in proportion of children with scores in the abnormal range for the comparison group and the epilepsy group. Then we repeated the Chi-square independence (χ2) test with the comparison group for all subgroups of patients with epilepsy. Additionally, we performed the Chi-square independence test to analyse the relationship between different subgroups of patients with epilepsy (ILE and IGE vs. SE; and ILE vs. IGE).

Results

A total of 924 questionnaires from the epilepsy (n = 409) and comparison (n = 515) groups were collected and analysed. Demographics of both groups and clinical characteristics of the epilepsy group are shown in Table 1. There was a higher proportion of boys in the epilepsy group (64.5%) than in the comparison group (57.5%) with the difference reaching statistical significance (χ2 = 6.246, degrees of freedom [df] = 2, p < 0.05).

 

Independent-samples t Tests

Table 2 summarises the results of independent-samples t test for SDQ raw scores. The mean (± standard deviation) of the total difficulties score in the epilepsy group was considerably higher than that in the comparison group (17.5 ± 6.8 vs. 10.8 ± 5.4); the mean difference was statistically significant (p < 0.001). The mean difference between the 2 groups was also statistically significant (p < 0.001) for the 4 difficulties subscales (hyperactivity / inattention, emotional symptoms, peer relationship problems, and conduct problems), but not for the strengths subscale (prosocial behaviour).

The difference between the comparison group and each of the epilepsy subgroups (ILE, IGE, SE, SE+, and S/UE) was significant for the total difficulties score and for 3 of the difficulties subscales (hyperactivity / inattention, emotional symptoms, and conduct problems). For the fourth difficulty subscale (peer relationship problems), the difference was significant for all subgroups of epileptic patients, except for the IGE group. The mean score of the prosocial behaviour subscale was significantly lower than that in the comparison group for the SE+ group only.

There were statistically significant differences between the different epilepsy subgroups. The mean difference between patients with idiopathic epilepsies (ILE + IGE) and patients with SE was statistically significant for the total difficulties score, the hyperactivity / inattention subscale, and the prosocial behaviour subscale (p < 0.05).

The difference between ILE and SE patients reached significance for the total difficulties, the hyperactivity / inattention subscale, and the prosocial behaviour subscale scores.

The difference between IGE and SE patients was significant for the total difficulties, the hyperactivity / inattention subscale, the peer relationship problems subscale, and the prosocial behaviour subscale scores (p < 0.05).

Neither the total difficulties scale score nor the 5 subscale scores of the SDQ showed any significant difference between ILE and IGE patients.

Chi-square Independence Test

Table 3 summarises the results of the Chi-square independence test for the SDQ scores categorised as ‘normal’, ‘borderline’, and ‘abnormal’. The difference between the epileptic patients (the group of all epileptic patients, as well as each epilepsy subgroup separately) and the comparison group was significant for the total difficulties score and for the 3 difficulties subscale scores (hyperactivity / inattention, conduct problems, and emotional symptoms). When comparing the group of all epileptic patients as well as the SE, SE+, and S/UE subgroups with the comparison group, the difference reached significance for the peer relationship problems subscale. For the prosocial behaviour subscale, only the difference between the SE+ group and the comparison group was significant.

The comparison of different epilepsy subgroups using the Chi-square independence test revealed several statistically significant differences. Patients with idiopathic epilepsy (ILE + IGE) and SE patients differed significantly in the hyperactivity / inattention (χ2 = 7.080, df = 2, p < 0.05) and the emotional symptoms subscales (χ2 = 8.851, df = 2, p < 0.05). The difference between the ILE and SE groups also reached significance for the hyperactivity / inattention (χ2 = 6.725, df = 2, p < 0.05) and the emotional symptoms subscales (χ2 = 6.572, df = 2, p < 0.05). However, the difference between the IGE and SE groups reached significance only for the emotional symptoms subscale (χ2 = 8.424, df = 2, p < 0.05). The difference between ILE and IGE patients was non-significant both for the total difficulties scale score and for the 5 subscale scores.

Gender and Age Differences

In the comparison group, the difference between boys (n = 296) and girls (n = 219) was significant (p < 0.05) for the hyperactivity / inattention subscale (boys vs. girls: 4.0 ± 2.4 vs. 3.1 ± 2.2) and the emotional symptoms subscale (2.3 ± 2.1 vs. 2.7 ± 2.2).

In the group of epileptic patients consisting of ILE, IGE and SE, the difference between boys (n = 164) and girls (n = 90) was significant (p < 0.05) for the total difficulties score (boys vs. girls: 17.8 ± 6.7 vs. 16.0 ± 7.0), and scores for the hyperactivity / inattention subscale (5.8 ± 2.5 vs. 4.5 ± 2.7), conduct problems subscale (3.7 ± 2.1 vs. 3.0 ± 2.1), and the prosocial behaviour subscale (7.7 ± 2.0 vs. 8.3 ± 1.8). In patients with idiopathic epilepsy (ILE and IGE), the difference between boys (n = 125) and girls (n = 77) was significant (p < 0.05) for the hyperactivity / inattention subscale (boys vs. girls: 5.6 ± 2.4 vs. 4.4 ± 2.6) and the emotional symptoms subscale (4.1 ± 2.6 vs. 5.0 ± 2.8). In patients with SE, the difference between boys (n = 39) and girls (n = 13) was significant (p < 0.05) for the hyperactivity / inattention subscale (boys vs. girls: 6.6 ± 2.1 vs. 4.6 ± 3.7). There were no significant differences between boys and girls within the group of SE+ patients. Within the group of S/UE patients, the difference between boys (n = 79) and girls (n = 36) was significant (p < 0.05) for the hyperactivity / inattention subscale (boys vs. girls: 5.8 ± 2.6 vs. 4.6 ± 2.7) and the conduct problems subscale (4.1 ± 2.2 vs. 3.2 ± 2.1).

The age of the children with epilepsy was inversely associated with the SDQ total difficulties score, but this tendency did not reach significance (p > 0.05).

Discussion

The elevated SDQ scores and higher number of children with scores in the abnormal range among children with epilepsy supported our hypothesis that they have an increased risk of psychiatric and behavioural problems. The mean total difficulties score was significantly higher in the epilepsy group than that in the comparison group. Furthermore, children with epilepsy scored higher on the 4 difficulties subscales of the SDQ (hyperactivity / inattention, emotional symptoms, peer relationship problems, and conduct problems) than the comparison group. However, the strengths subscale scores (prosocial behaviour) were similar between the epilepsy and comparison groups. Our findings correspond to the results of several previous studies. Tanabe et al5 compared the SDQ scores of children with epilepsy with Japanese-standard SDQ scores and showed that they had higher total difficulties scores and also higher scores for the 4 difficulties subscales. Their children with epilepsy did not differ significantly on the prosocial behaviour subscale, which is comparable to our study. Similar findings were also revealed in a Norwegian study, in that children with epilepsy differed significantly to a large community sample in all domains, except for prosocial behaviour.1 Lossius et al14 used the SDQ self-report version and found similar results for children with epilepsy, that is, higher scores of emotional symptoms, conduct problems, hyperactivity / inattention and peer relationship problems, but no significant difference with respect to prosocial behaviour.

When categorising the SDQ scores as ‘normal’, ‘borderline’ and ‘abnormal’, the total difficulties score was abnormal in half of the children with epilepsy, ranging from 43% in ILE patients to 70% in SE+ patients. Children with abnormal scores for the difficulties subscales were more prevalent in the epilepsy group (Table 3). Our findings suggest that children with epilepsy may be more likely to fulfil the criteria for a specific psychiatric diagnosis. This concurs with previous studies that showed higher rates of psychiatric disorders in children with epilepsy.2,32

We compared different subgroups of epileptic patients with the comparison group. Regardless of epilepsy subgroup, children with epilepsy scored significantly higher on the total difficulties score, hyperactivity / inattention, emotional symptoms, and conduct problems subscales (Tables 2 and 3). The mean score of peer relationship problems of all epilepsy subgroups was also higher than that in the comparison group, with insignificant difference for the IGE group only. Interestingly, in Tanabe et al’s study,33 children with IGE showed the lowest scores in emotional symptoms and peer relationship problem compared with the other epilepsy groups. Of note, children with ILE and IGE, despite having no brain lesion and a better course of epilepsy, also had elevated scores on total difficulties and difficulties subscale (hyperactivity / inattention, emotional symptoms, and peer relationship problems).

The SE+ group was the only epilepsy subgroup with a significantly lower mean score in prosocial behaviour than the comparison group (Chi-square test). This might be a consequence of the severe physical and mental disabilities that these children had in addition to their symptomatic epilepsy. A study reveals that children with intellectual disability had lower scores in prosocial behaviour.34

Brunklaus et al35 studied children with Dravet syndrome and learning disabilities in addition to epileptic seizures, and showed that they had a significantly lower score in prosocial behaviour than the UK norms. It is unclear whether the lower prosocial behaviour scores in the SE+ group are due to a direct influence of their disability on social skills or whether they are a result of limited opportunities to be engaged in age-appropriate social interactions. As expected, the SE+ group showed the highest scores on the total difficulties scale and some subscales, indicating that more severe brain damage is associated with more severe psychopathology. Thus, SE+ patients are the most vulnerable subgroup of epileptic patients in terms of psychiatric and behavioural problems, and special attention should also be paid to the prosocial behaviour domain in these children.

In this study, the difference between ILE and IGE patients was insignificant both for the total difficulties score and for the 5 subscales of the SDQ. In another study,36 children with focal and generalised idiopathic epilepsies did not differ in psychopathology when assessed with the Child Behavior Checklist.

Children with SE scored higher than those with idiopathic epilepsy for the total difficulties and the 4 difficulties subscale, but lower on the prosocial behaviour subscale. The difference reached statistical significance for the total difficulties score, hyperactivity / inattention, and prosocial behaviour subscales when SE was compared with the group of all idiopathic epileptic patients (ILE + IGE). In addition, the SE patients had a larger proportion of abnormal total difficulties and subscale scores compared with patients with idiopathic epilepsy (Table 3). These findings support our hypothesis that children with symptomatic epilepsy have more psychiatric and behavioural problems than those with idiopathic epilepsy. Children with epilepsy are more likely to have emotional and behavioural symptoms if they have structural abnormalities in the central nervous system.37 Cognitive impairment and history of abnormal developmental milestones are associated with the development of severe behavioural problems in children with epilepsy.38 Tanabe et al33 concluded that symptomatic aetiology should be regarded as a risk factor for behavioural and emotional problems as measured by the SDQ. The findings of Davies et al2 support this view. They used a structured psychiatric interview in children with epilepsy and reported behavioural problems in 56% of those with epilepsy as well as additional neurological problems and in 26% of those with uncomplicated epilepsy. Removal of epileptic focus during epilepsy surgery resulted in behavioural improvement.39 In children with SE, structural abnormalities may not be the only factor responsible for the high rates of psychiatric and behavioural problems. Other factors related to SE, such as multiple antiepileptic drugs or recurrent seizures,40 might also lead to a higher prevalence of psychiatric and behavioural problems in SE as opposed to IGE or ILE. A recent study, however, found only minimal syndrome-specific differences between ILE and IGE patients with new- and recent-onset childhood epilepsy.41

It is possible that psychiatric and behavioural problems evolve over the course of epilepsy in a syndrome-specific way. We plan to conduct a longitudinal study of psychiatric and behavioural problems in children with recent-onset and late-stage epilepsy to investigate such evolution.

In this study, children with SE and SE+ showed the highest hyperactivity / inattention scores (Table 2). Hyperactivity / inattention was the SDQ subscale that showed the highest score and largest proportion of subjects in the clinical range among the 4 subscales of difficulties in children with epilepsy in Tanabe et al’s study.33 The authors also showed that the SDQ hyperactivity / inattention scores were highest for symptomatic localisation-related epilepsy compared with other epilepsy syndromes in another study.5 Epilepsy in children with ADHD appears to be more severe than in those without; in particular epileptic patients with ADHD were more likely to have an abnormal neurological examination and abnormal background rhythm on electroencephalography, possibly reflecting greater underlying neurological dysfunction.42 In a sample of children with epilepsy reported from a tertiary epilepsy centre, the proportion of children meeting criteria for ADHD by far exceeded the rate reported in children at first seizure, suggesting higher rates of hyperactivity / inattention symptoms in severe epilepsy.7 The relationship between epilepsy and ADHD is complex, and it remains unclear whether ADHD symptoms are the result of seizures or whether both ADHD and epilepsy represent a result of shared aetiological factors.43 Yet we can speculate that the structural brain abnormalities that cause epilepsy in SE and SE+ might cause ADHD symptoms or make them worse.

The identified gender differences in SDQ scores in this study are in agreement with our previous findings31: boys showed higher scores on the hyperactivity / inattention subscale while girls had higher scores on the emotional symptoms and the prosocial behaviour subscales. Similar to our findings, Alfstad et al1 reported that among children with epilepsy, boys had more peer relationship problems and hyperactivity / inattention, whereas girls had more emotional symptoms. Thus, the tendency of more externalising symptoms in boys and more internalising problems in girls in the general population seems to be valid also for children with epilepsy. In patients with SE, the difference between boys and girls was significant only for the hyperactivity / inattention subscale. Possibly, the relatively small number of subjects in this group precluded the other subscales of the SDQ reaching statistical significance. Interestingly, in the group of SE+ patients, we detected no significant difference between boys and girls, which may be explained by the relatively small number of subjects, and also by severe mental and physical disabilities that surpass the influence of other factors.

This study had several limitations. The information was drawn from patient charts and lacked data on seizure severity and precise intelligence quotient level of patients with epilepsy. Tanabe et al,5 however, found no significant differences in SDQ scores between children with well- controlled seizures and those with poorly controlled

seizures. Further, the SDQ indicates level of psychiatric problems but cannot be used as a diagnostic tool. Due to the lack of Azeri SDQ normative data, we used norms produced from population-based studies in the UK. Mean scores may vary in different countries22 resulting in different cut-off values for different countries.16,20,27,28,30,44,45 Nevertheless we have shown that the Azeri version of the SDQ discriminates well between paediatric and psychiatric samples when applying British cut-off values.31 Another limitation was that the teacher-reported or self-reported versions of SDQ were not used and consequently parents were the only source of information about psychopathology of their children. In this study there was a higher proportion of males in the epilepsy group than in the community sample. This potentially may have raised the prevalence of symptoms that are more frequent among boys, such as hyperactivity and behavioural problems.

In conclusion, our findings based on a large sample of children with epilepsy confirm higher rates of psychiatric and behavioural problems among this population. The SDQ scores in epileptic patients were higher than those in the community sample for all difficulties subscales (hyperactivity / inattention, emotional symptoms, conduct problems, and peer relationship problems). The SDQ scores differed between children with idiopathic and symptomatic epilepsies, but were similar between ILE and IGE. Children with epilepsy and co-morbid severe mental or physical disability showed significantly lower scores on the prosocial behaviour subscale, suggesting that social skills are limited by their mental or physical disability.46

Acknowledgements

The authors are grateful to the personnel of Medina Medical Center for their contribution to this work. We also thank volunteers who carried out the work in the schools.

Declaration

All authors have disclosed no conflicts of interest.

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