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A survey of behavior problems in children with epilepsy
Epilepsy & Behavior 6 (2005) 581–586 www.elsevier.com/locate/yebeh
A survey of behavior problems in children with epilepsy Daniel L. Keene a,*, Ian Manion b, Sharon Whiting a, Edgar Belanger a, Renee Brennan a, Pierre Jacob a, Peter Humphreys a a
Division of Neurology, Department of Pediatrics, ChildrenÕs Hospital of Eastern Ontario, Ottawa, Ont., Canada b Psu Mental Health, ChildrenÕs Hospital of Eastern Ontario, Ottawa, Ont., Canada Received 14 January 2005; revised 1 March 2005; accepted 1 March 2005 Available online 26 April 2005
Abstract Over a period of 3 consecutive months, a cross-sectional, descriptive survey was made of the frequency of behavior problems and needs, as reported by their caregivers, of 6- to 18-year-old epileptic children attending two neurology clinics, using the Child Behavior Checklist. Caregivers of 175 children were approached to take part in the study; 158 (90%) completed the Child Behavior Checklist. The mean age of the children was 11.3 (range, 6–18). t scores >70 were obtained for 15.9% of the group for total behavior, 12.7% of the group for internalized behavior and 11.4% of the group for externalized behavior. Compared with those with normal scores, children with elevated t scores were more likely to have learning difficulties and to require the use of more community services. Ó 2005 Elsevier Inc. All rights reserved. Keywords: Children; Epilepsy; Behavior
1. Introduction Epilepsy is a common chronic neurological disorder of childhood. An increased frequency of behavior problems of various types has been reported in this patient group [1–6]. To develop treatment programs to help this group of children with both epilepsy and behavior problems, the prevalence of the problem and risk factors need to be known. Previous studies have suggested that these behavior problems may be related to the type and severity of epilepsy [3,7], duration of the disorder [3], intellectual ability [8], EEG findings [3,9], effects of antiepileptic medications [3,8,10], and family dynamics [4]. These conclusions have often been based on small sample sizes [3,5,11,12], with the study population being drawn from epileptic children attending specialized epilepsy clinics at a tertiary care center [3,5,11]. As well, subject recruitment has been random rather than inclu*
Corresponding author. Fax: +1 613 523 2256. E-mail address: [email protected] (D.L. Keene).
1525-5050/$ - see front matter Ó 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2005.03.004
sive and has occurred over a protracted period rather than a fixed period. Inclusive recruitment is necessary for estimating the prevalence of the problem. It also increases the ability to generalize about the results. To ascertain the prevalence and types of behavior problems in children with epilepsy and the resources caregivers felt necessary, a survey of all patients attending either the ChildrenÕs Hospital of Eastern Ontario neurological clinic or the private office of a pediatric neurologist in the same community was conducted over a 3-month period. This article reports the results of this survey.
2. Method By use of a set of standardized questionnaires, a cross-sectional descriptive study was done over a period of 3 consecutive months to evaluate the occurrence and types of behavior problems in children with epilepsy. The survey was prospective. PatientsÕ parents were
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recruited from the neurological clinics of the ChildrenÕs Hospital of Eastern Ontario and the office practice of a pediatric neurologist in the same community. Patients recruited for this study had to be between the ages of 6 and 18 and diagnosed as having epilepsy for at least 6 months prior to the onset of this study. Patients who had been diagnosed less than 6 months were excluded to decrease the possibility of parental anxiety about a recent diagnosis of epilepsy and any uncertainty in taking medications, and to allow medication dosages to be established. Exclusion criteria also included patients previously diagnosed as having brain tumor or a neurodegenerative disorder. At the time of the patientÕs clinic or office visit, the parent or legal caregiver was approached by a member of the clinic or office staff and informed of the study. An envelope containing an explanatory letter and a set of questionnaires was then given to the parent or legal caregiver. If the parent or legal caregiver did not wish to take part in the study, he or she was instructed to return the envelope at the end of the visit with the questionnaires unanswered. All envelopes were labeled with a patient study number, but without other identification marks. Patient study numbers identified the questionnaires. The questionnaires included a patient demographic/ needs survey and the Child Behavior Checklist (CBCL) [13]. The CBCL was chosen for parents/caregivers reporting of their childÕs behavior as it has been shown to have both strong reliability and validity. It has also been shown to be relevant to children with epilepsy [14]. This questionnaire consists of 118 behavior-related statements in which the parent/caregiver is asked to rate the childÕs behavior on a three-point scale, the highest score reflecting greater problem. Raw scores for each of the behavior problems were converted to a standardized t score (mean = 50, SD = 10) and normed for age and gender. t scores greater than 70 (98th percentile) were considered to be in the clinically significant range. Scores for each of the following behavior scales were calculated: total behavior problems, internalized problems, externalized problems, somatic complaints, social problems, thought problems, and attention problems. Internalized problems were further broken down into the subscales anxious/depressed and withdrawn/depressed. Externalized problems was broken down into subscales for rule-breaking and aggressive behaviors. The Demographics and Needs Survey was designed specifically for this survey and consisted of a series of questions about family demographics, such as size of family, marital status of parents, and whether the child was living at home. In addition, there were questions about the childÕs education level, medications the child was taking, other disabilities the child might have, and the childÕs present and future need for specialized services in the community (i.e., education, parent relief,
alternate living arrangements for the child, specialized medical services, emotional support for patient and family). For all persons approached to take part in this survey, regardless of whether the parent/caregiver completed the questionnaires, the childÕs treating neurologist was asked to complete a clinical profile sheet. Questions included type of epilepsy, medications prescribed, presence of neurological and physical handicaps, summary of EEG patterns, clinical impression as to the presence or absence of behavior problems, and whether the child was attending school full-time in a regular classroom setting or required teaching in a specialized setting on a part-time or full-time basis each day. The purpose of this part of the survey was to describe the total population approached to take part in the survey and to examine ascertainment bias in parents/caregivers returning completed questionnaires. Data from all questionnaires were entered into a database using the patient study number to match the three questionnaires. To ensure patient confidentiality, patient name and date of birth were not entered into the database. Statistical analysis was done using the SPSS 11 program. v2 analysis was used for proportional data. Difference in group means were examined using the Student t test. A level of significance of P < 0.05 was used.
3. Results During the 3-month survey period, 175 patients were identified as meeting the study eligibility criteria; 158 (90%) of these patientsÕ parents/caregivers completed the two parent questionnaires. Forty-two (27%) of the parents/caregivers completing the survey were seen in a hospital clinical setting, and 116 (73%) were seen in the private office setting. When the clinical variables as documented on the treating physicianÕs survey were compared between parents/caregivers completing the questionnaires and those electing not to do so, the two groups were not found to be significantly different with respect to site of visit, type of epilepsy, number of medications prescribed, EEG findings, and presence of behavior problems, physical handicaps, or cognitive deficiencies. In the group in which parents/caregivers completed all questionnaires (158 patients), there was no significant gender difference (51.5% male, 48.5% females). The mean age of patients was 11.3 years (SD 3.6 years). Diagnostic classification was as follows: primary generalized epilepsy 23.1%, partial seizures 56.1%, and secondary generalized epilepsy 20.8%. The mean number of antiepileptic medications taken per patient at the time of the survey was 1.35 ± 0.69 (range, 1–4). The various EEG patterns that occurred in the study population
D.L. Keene et al. / Epilepsy & Behavior 6 (2005) 581–586
were distributed as follows: normal 14.5%, nonspecific background irregularities 8.7%, generalized spike–wave bursts 39.3%, multifocal spikes 7.5%, and focal spikes 29.5%. Physicians reported that 39.3% of the group had significant behavior problems. Learning problems of varying degree were reported to be present in 57% of the group, and 2.8% were reported to have had a neurological physical disability. The Demographics and Needs Survey results indicated that 94.4% of the children were living with their families with the remainder were living in group home/ foster home settings. Marital status of the childrenÕs parents was as follows: 70% married, 25% separated, and 5% single parent. With respect to schooling, 41.6% of the children were reported to be able to attend an ageappropriate regular classroom education program without difficulties, 22.3% were in a regular classroom program part of the time but were withdrawn for extra help each day and 36.1% were in a specialized classroom for children with intellectual impairment. The Child Behavior Checklist mean total behavior score for the group was 57.33 ± 2.27, with 15.9% of the group having t scores greater than 70. The mean group internalized behavior score was 55.8 ± 12.19, with 12.7% of the group having t scores greater than 70. The mean externalized behavior score was 55.09 ± 11.14, with 11.4% having t scores greater than 70. When the subscales within the internalized behavior scale were examined, the group mean t score for anxious/depressed behavior was 50.08 ± 9.11, with 7.6% of the t scores greater than 70. The mean group t score for withdrawn/depressed behavior was 58.96 ± 8.46, with 7.0% of the t scores above 70. When the subscales within the externalized behavior scale were examined, the group mean t score for rulebreaking behavior was 55.96 ± 11.4, with 4.2% of the t scores greater than 70. The mean group t score for aggressive behaviors was 58.73 ± 8.89, with 11.8% of the t scores being greater than 70. The group mean t scores for the remaining subscales contributing to the total behavior score, but not part of either the internalized or externalized behavior scores, were as follows: somatic complaints 58.6 ± 8.94 (7.6% >70); social problems 61.70 ± 10.73 (16.5% >70); and attention problems 64.56 ± 12.24 (26.9% >70). There was no significant difference in frequency of t scores >70 between children seen in hospital clinics and those seen in the private office setting. Elevated t scores for total behavior, internalized behavior, externalized behavior, attention difficulties, and social behavior problems were significantly more frequent among children whose cognitive impairment was sufficient to warrant specialized classroom placement. Seizure type, age of patient, sex of patient, number and types of antiepileptic medications taken, family demographics, and
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type of EEG pattern did not significantly differ between the group of patients with significantly elevated t scores for each of the above mentioned scales and those without such scores. The number of community services per patient at the time of the survey as identified by the childÕs parent/ caregiver was 0.97 ± 1.4 (range, 0–8). 44.9% of the parents/caregivers reported that their child had not needed the support of a community service agency; 24.6% reported using one agency on a regular basis, 11.4% using two agencies, 10.2% three, and 8.9% using more than three. The types of community services used were as follows: social service agencies by 20%, child development services by 19%, parent relief services by 8%, behavior management by 7%, psychologist by 7%, and community home care by 5%. When parents/caregivers were asked about the use of specialized education facilities (either within school or in addition to) in the last 6 months, 44.9% responded affirmatively. As for the need for specialized education facilities in the future, 31.3% felt their child would need such services in the next year, 27.1% for the next 2 to 5 years, and 35.5% for greater than 5 years. When parents/caregivers were questioned about the frequency of use of parent relief services, 72.5% responded that they had not required this type of service in the last 6 months; 12.0% had used it once, 4.2% twice, and 10.9% three or more times. Within the next year, 15.1% of the parents responded that they expected to use this type of service, and within the next 2 to 5 years, 15% of parents felt that they would be requiring this type of service; 18.8% of the parents felt they would be requiring this service in about 5 years. Twenty-six and one-tenth percent of parents/caregivers of parents stated that, during the last 6 months, their child had been living out of their home in a specialized residence for a period. When asked about the need for this type of facility for their child the future, 15.1% parents projected this need in the next year, 12% for the next 2 to 5 years, and 29% in greater than 5 years. When parents/caregivers were questioned about the frequency of use of specialized medical service (need for admission to hospital or emergency ward for greater than 24 hours for seizure-related problems), 79% stated that their child had not required this service in the last 6 months; 10.2% had required this type of service once in the last 6 months, 1.2% twice, and 9.6% three or more times. When parents/caregivers were asked if they felt their child would require this type of service within the next year, 15.2% responded affirmatively. When parents/caregivers were asked to forecast their childÕs need for this service in the next 2 to 5 years and after 5 years, an affirmative answer was given by 11.5 and 15.2% respectively. When parents/caregivers were asked about the frequency of use of a mental health service for emotional support for patient and family in last 6 months, 74.9%
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stated that they had not used this type of service in the last year; 10.8% of respondents stated that they had used this type of service once in the last 6 months, 2.4% twice, and 12% three or more times. When parents/caregivers were asked about future requirement for this type of service, 18.5% felt that they would in the next year, 15.1% within the next 2 to 5 years, and 17.5% in greater than 5 years. Parents/caregivers presently requiring access to specialized community services for their child in the areas of living, education, emotional support, and/or medical services projected the continued need for services for the immediate future (within the year), midterm (next 2–5 years), and long term (greater than 5 years). Parents/ caregivers not using community services at the time of the survey did not project a future need. The only predictor of need for ongoing access to specialized community services was the presence of a cognitive disability requiring specialized education. Seizure type, number of medications used, types of medication used, elevated total behavior scores, and presence of elevated total behavior, internalized behavior, and/or externalized behavior scores as recorded by the CBCL did not correlate with present or future need for specialized community services.
4. Discussion The parent/caregiver-completed CBCL in this crosssectional descriptive survey of epileptic children demonstrated an increased frequency of elevated behavior scores for all the scales and, specifically, scales for attention and social problems. This finding is similar to frequencies of behavior problems previously reported using the CBCL [1–6,14,15]. As well, it is similar to the results of our previous study using the same set of questionnaires in the same clinical setting [6]. The consistent finding of increased frequency of behavior difficulties over time in our clinical setting, coupled with the results of other investigators, strongly supports the observation that behavior problems are common in epileptic children. The etiology of this association remains unclear, but it is most likely related to a common preexisting underlying pathology. Austin et al. [1,2], using the parent-completed CBCL, reported that behavior problems were reported to be frequently present in the 6 months prior to first seizures in newly diagnosed epileptic children. In a later study, Dunn and Austin [16], using teacher-completed CBCL confirmed the observations of Austin et al. [1,2]. Other studies have suggested that the presence or absence of behavior problems could be related to the type of epilepsy [11,16–18], types of antiepileptic medications taken [10], and family demographics [3,7,9,12]. In the present study, we were unable to confirm these associations.
Seizure intensity was not examined as a predictive variable in this study. It would seem reasonable to hypothesize that parents/caregivers of children with greater seizure intensity would report a greater frequency of significantly elevated behavior scores. It is difficult, however, to quantitatively estimate the intensity of a childÕs average seizure. Seizure frequency has been used in some studies as a surrogate variable, but was not used in this study. It was felt that it would be too difficult to determine over which period to examine the frequency of seizures, and how to compare seizure attack frequencies for convulsive epilepsy and nonconvulsive epilepsy. Bourgeois [10] suggested that difficulty with control of seizures is significantly correlated with the number of antiepileptic drugs taken. In our study the number of antiepileptic medications taken was not found to be related to increased frequency of significantly elevated behavior scores. This would suggest that seizure frequency was not predictive of behavior difficulties. Like Camfield et al. [19], we found that no one EEG pattern was more frequent among children who had significantly elevated behavior scores versus those with normal scores. As only interictal EEG patterns were used, it is still possible that a correlation with ictal EEG onset and behavior might exist. Intellectual difficulties have been reported to be more prevalent in this group of children and to be associated with increased risk of psychopathology [8,20]. In our survey, the presence of cognitive difficulties as measured by the child not being able to attend a regular classroom because of a significant cognitive impairment was the only variable that was significantly correlated with an increased frequency of elevated behavior scores. As well, children who were not in a regular classroom were significantly more likely to have been reported by their parents/caregivers to require the use of a community agency in the 6 months prior to the survey and to have an ongoing need for at least one community service in the future. Seizure type, number of antiepileptic medications taken, presence of physical handicap, EEG pattern, and family demographics did not predict present or anticipated/ projected use of specialized services. The association between increased future needs for specialized services and the presence of significant cognitive difficulties was also observed in our previous study [6]. The lack of association with seizure variables was unexpected, suggesting that epilepsy per se does not play a significant role in parent-perceived future needs for their children. Though our survey detected a significant increase in the frequency of behavior problems when compared with the general population, the majority of parents/ caregivers did not indicate an increased use of mental health services in the last 6 months nor a need to use such a service. This underusage of mental health facilities by this group had previously been reported by Otto
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et al. [4], who found that two-thirds of patients identified in need of mental health services had not used them. Our survey was not designed to answer the question why this group was not using these services. Possible reasons such as lack of parental/physician knowledge of the types of services available in the community, long waiting lists, reluctance to use the services on the part of parent or treating physicians, lack of programs, and a negative connotation associated with the use of mental health programs need to be addressed in a future study. Another possibility is that parents/caregivers prioritized the physical health concerns over the social behavioral concerns. Several reasons could account for the lack of correlation between seizure and family demographic variables and reported behavior problems in our survey in comparison with previous studies. Patient ascertainment bias plays a significant role in defining the patient population. The design of our study differed significantly from that of previous studies in that our study population was drawn from both hospital and office settings rather than mainly from a specialized pediatric epilepsy clinic setting. Previous studies excluded children who had significant cognitive difficulties, whereas ours did not. Unlike previous studies, we attempted to recruit all patients in a consecutive prospective manner rather than using the voluntary referral-to-study method. Random volunteer recruitment has the inherent difficulty of selectively biasing toward persons with a vested interest in the project. As well, the 90% participation rate further suggests that a representative sample was achieved in the present study. Though we used a well-recognized standardized measurement of behavior problems in children, which has been used by other investigators in the same population, it is possible that the parent/caregiver-completed CBCL misclassified some of the study population. Jensen and Watanabe [21] reported that when the CBCL was compared with the Diagnostic Interview Schedule for Children, a false-negative rate of 10% and false-positive rate of 20% were obtained. When Ott et al. [5] compared the CBCL and the Schedule for Affective Disorders and Schizophrenia for School-Age Children (K-SADS) in a group of epileptic children, he found that K-SADS identified more children with psychopathology than the CBCL. Therefore, it is possible that some of the persons who had significant behavior problems could have been missed, accounting for some of the differences between studies. Other limitations of this study are its design as a descriptive survey, the numbers of patients in various subgroups, and the definition of learning disability. The descriptive design provides for a ‘‘scan’’ of the prevalence of the problem, a step necessary for planning of resources. As the study was not hypothesis-driven, it does not allow for conclusions to be drawn as to the cause of the problem.
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It does supply information necessary for designing future hypothesis-driven studies. The small numbers of patients in several groups did not allow for statistical analysis of the interrelationship of the various variables. The definition of learning difficulties used in this survey—of a child requiring withdrawal from regular classroom for teaching on a routine basis, some of the time or all of the time—was an operational definition. Results of psychoeducational assessments were not requested. In summary, through use of the parent/caregivercompleted CBCL, our survey confirmed the increased frequency of behavior problems in children with epilepsy. Unlike other studies, we found that the presence of significant cognitive difficulties was the only variable that was associated with an increased risk of behavior problems. When planning resources for treatment of children with epilepsy, treatment of ongoing behavior issues needs to be included.
References [1] Austin J, Dunn D, Caffrey H, Perkins S, Harezlak J, Rose D. Recurrent seizures and behavior problems in children with first recognized seizures: a prospective study. Epilepsia 2002;53:1564–73. [2] Austin J, Harezlak J, Dunn D, Huster G, Rose D, Ambrosuis W. Behavior problems in children before first recognized seizures. Pediatrics 2001;107:115–22. [3] Hermann B, Whitman S, Hughes J, Melyn M, Dell J. Multietiological determinants of psychopathology and social competence in children with epilepsy. Epilepsy Res 1988;2:51–60. [4] Otto D, Siddarth P, Gurbani S, et al. Behavioral disorders in pediatric epilepsy: unmet psychiatric need. Epilepsia 2003;44:591–7. [5] Otto D, Caplan R, Guthrie D, et al. Measures of psychopathology in children with complex partial seizures and primary generalized epilepsy with absence. J Am Acad Child Adolesc Psychiatry 2001;40:907–14. [6] Manion I, Keene D, Champagne J. Assessing the medical and non-medical needs of children with seizures disorders and their families. Can J Neurol Sci 1992;19:306. [7] Austin J, Risinger M, Beckett L. Correlates of behavior problems in children with epilepsy. Epilepsia 1992;33:1115–20. [8] Hermann B. Neuropsychological functioning and psychopathology in children with epilepsy. Epilepsia 1982;23:545–54. [9] Hoare P, Kerley S. Psychosocial adjustment of children with chronic epilepsy and their families. Dev Med Child Neurol 1991;33:201–15. [10] Bourgeois B. Antiepileptic drugs, learning and behavior in childhood epilepsy. Epilepsia 1998;39:913–21. [11] Caplan R, Arbelle S, Guthrie D, et al. Formal thought disorder and psychopathology in pediatric primary generalized and complex partial epilepsy. J Am Acad Adolesc Psychiatry 1997;36:1286–94. [12] Matthews W, Barabas G, Ferrari M. Emotional concomitant of childhood epilepsy. Epilepsia 1982;23:671–81. [13] Achenbach TM. Manual for the ASEBA. Burlington: Univ. of Vermont Research Centre for Children, Youth and Families; 2000. [14] Dorenbaum D, Cappelli M, Keene D, McGrath P. Use of a Child Behavior Checklist in the psychosocial assessment of children with epilepsy. Clin Pediatr 1985;24:634–7.
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[15] Dunn D, Austin J, Caffrey H, Perkins S. A prospective study of teacherÕs ratings of behavior problems in children with new-onset seizures. Epilepsy Behav 2003;4:26–35. [16] Dunn D, Austin J. Behavioral issues in pediatric epilepsy Neurology 1999;53(Suppl. 2):S96–S100. [17] Mitchell W, Scheier L, Baker S. Psychosocial, behavioral and medical outcomes in children with epilepsy: a developmental risk factor model using longitudinal data. Pediatrics 1994;94:471–7. [18] Mitchell W. Social outcome of childhood epilepsy: associations and mechanisms. Semin Pediatr Neurol 1994;1:136–43.
[19] Camfield C, Camfield P, Smith B, Gordon K, Dooley J. Biologic factors as predictors of social outcome of epilepsy in intellectually normal children: a population-based study. J Pediatr 1993;122:869–73. [20] Perrine K, Kiolbassa T. Cognitive deficits in epilepsy and contribution to psychopathology. Neurology 1999;53(Suppl. 2): S39–48. [21] Jensen P, Watanabe H. Sherlock Holmes and child psychopathology assessment approaches: the case of the false-positive. J Am Acad Child Adolesc Psychiatry 1999;38:138–46.
A survey of behavior problems in children with epilepsy Daniel L. Keene a,*, Ian Manion b, Sharon Whiting a, Edgar Belanger a, Renee Brennan a, Pierre Jacob a, Peter Humphreys a a
Division of Neurology, Department of Pediatrics, ChildrenÕs Hospital of Eastern Ontario, Ottawa, Ont., Canada b Psu Mental Health, ChildrenÕs Hospital of Eastern Ontario, Ottawa, Ont., Canada Received 14 January 2005; revised 1 March 2005; accepted 1 March 2005 Available online 26 April 2005
Abstract Over a period of 3 consecutive months, a cross-sectional, descriptive survey was made of the frequency of behavior problems and needs, as reported by their caregivers, of 6- to 18-year-old epileptic children attending two neurology clinics, using the Child Behavior Checklist. Caregivers of 175 children were approached to take part in the study; 158 (90%) completed the Child Behavior Checklist. The mean age of the children was 11.3 (range, 6–18). t scores >70 were obtained for 15.9% of the group for total behavior, 12.7% of the group for internalized behavior and 11.4% of the group for externalized behavior. Compared with those with normal scores, children with elevated t scores were more likely to have learning difficulties and to require the use of more community services. Ó 2005 Elsevier Inc. All rights reserved. Keywords: Children; Epilepsy; Behavior
1. Introduction Epilepsy is a common chronic neurological disorder of childhood. An increased frequency of behavior problems of various types has been reported in this patient group [1–6]. To develop treatment programs to help this group of children with both epilepsy and behavior problems, the prevalence of the problem and risk factors need to be known. Previous studies have suggested that these behavior problems may be related to the type and severity of epilepsy [3,7], duration of the disorder [3], intellectual ability [8], EEG findings [3,9], effects of antiepileptic medications [3,8,10], and family dynamics [4]. These conclusions have often been based on small sample sizes [3,5,11,12], with the study population being drawn from epileptic children attending specialized epilepsy clinics at a tertiary care center [3,5,11]. As well, subject recruitment has been random rather than inclu*
Corresponding author. Fax: +1 613 523 2256. E-mail address: [email protected] (D.L. Keene).
1525-5050/$ - see front matter Ó 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2005.03.004
sive and has occurred over a protracted period rather than a fixed period. Inclusive recruitment is necessary for estimating the prevalence of the problem. It also increases the ability to generalize about the results. To ascertain the prevalence and types of behavior problems in children with epilepsy and the resources caregivers felt necessary, a survey of all patients attending either the ChildrenÕs Hospital of Eastern Ontario neurological clinic or the private office of a pediatric neurologist in the same community was conducted over a 3-month period. This article reports the results of this survey.
2. Method By use of a set of standardized questionnaires, a cross-sectional descriptive study was done over a period of 3 consecutive months to evaluate the occurrence and types of behavior problems in children with epilepsy. The survey was prospective. PatientsÕ parents were
582
D.L. Keene et al. / Epilepsy & Behavior 6 (2005) 581–586
recruited from the neurological clinics of the ChildrenÕs Hospital of Eastern Ontario and the office practice of a pediatric neurologist in the same community. Patients recruited for this study had to be between the ages of 6 and 18 and diagnosed as having epilepsy for at least 6 months prior to the onset of this study. Patients who had been diagnosed less than 6 months were excluded to decrease the possibility of parental anxiety about a recent diagnosis of epilepsy and any uncertainty in taking medications, and to allow medication dosages to be established. Exclusion criteria also included patients previously diagnosed as having brain tumor or a neurodegenerative disorder. At the time of the patientÕs clinic or office visit, the parent or legal caregiver was approached by a member of the clinic or office staff and informed of the study. An envelope containing an explanatory letter and a set of questionnaires was then given to the parent or legal caregiver. If the parent or legal caregiver did not wish to take part in the study, he or she was instructed to return the envelope at the end of the visit with the questionnaires unanswered. All envelopes were labeled with a patient study number, but without other identification marks. Patient study numbers identified the questionnaires. The questionnaires included a patient demographic/ needs survey and the Child Behavior Checklist (CBCL) [13]. The CBCL was chosen for parents/caregivers reporting of their childÕs behavior as it has been shown to have both strong reliability and validity. It has also been shown to be relevant to children with epilepsy [14]. This questionnaire consists of 118 behavior-related statements in which the parent/caregiver is asked to rate the childÕs behavior on a three-point scale, the highest score reflecting greater problem. Raw scores for each of the behavior problems were converted to a standardized t score (mean = 50, SD = 10) and normed for age and gender. t scores greater than 70 (98th percentile) were considered to be in the clinically significant range. Scores for each of the following behavior scales were calculated: total behavior problems, internalized problems, externalized problems, somatic complaints, social problems, thought problems, and attention problems. Internalized problems were further broken down into the subscales anxious/depressed and withdrawn/depressed. Externalized problems was broken down into subscales for rule-breaking and aggressive behaviors. The Demographics and Needs Survey was designed specifically for this survey and consisted of a series of questions about family demographics, such as size of family, marital status of parents, and whether the child was living at home. In addition, there were questions about the childÕs education level, medications the child was taking, other disabilities the child might have, and the childÕs present and future need for specialized services in the community (i.e., education, parent relief,
alternate living arrangements for the child, specialized medical services, emotional support for patient and family). For all persons approached to take part in this survey, regardless of whether the parent/caregiver completed the questionnaires, the childÕs treating neurologist was asked to complete a clinical profile sheet. Questions included type of epilepsy, medications prescribed, presence of neurological and physical handicaps, summary of EEG patterns, clinical impression as to the presence or absence of behavior problems, and whether the child was attending school full-time in a regular classroom setting or required teaching in a specialized setting on a part-time or full-time basis each day. The purpose of this part of the survey was to describe the total population approached to take part in the survey and to examine ascertainment bias in parents/caregivers returning completed questionnaires. Data from all questionnaires were entered into a database using the patient study number to match the three questionnaires. To ensure patient confidentiality, patient name and date of birth were not entered into the database. Statistical analysis was done using the SPSS 11 program. v2 analysis was used for proportional data. Difference in group means were examined using the Student t test. A level of significance of P < 0.05 was used.
3. Results During the 3-month survey period, 175 patients were identified as meeting the study eligibility criteria; 158 (90%) of these patientsÕ parents/caregivers completed the two parent questionnaires. Forty-two (27%) of the parents/caregivers completing the survey were seen in a hospital clinical setting, and 116 (73%) were seen in the private office setting. When the clinical variables as documented on the treating physicianÕs survey were compared between parents/caregivers completing the questionnaires and those electing not to do so, the two groups were not found to be significantly different with respect to site of visit, type of epilepsy, number of medications prescribed, EEG findings, and presence of behavior problems, physical handicaps, or cognitive deficiencies. In the group in which parents/caregivers completed all questionnaires (158 patients), there was no significant gender difference (51.5% male, 48.5% females). The mean age of patients was 11.3 years (SD 3.6 years). Diagnostic classification was as follows: primary generalized epilepsy 23.1%, partial seizures 56.1%, and secondary generalized epilepsy 20.8%. The mean number of antiepileptic medications taken per patient at the time of the survey was 1.35 ± 0.69 (range, 1–4). The various EEG patterns that occurred in the study population
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were distributed as follows: normal 14.5%, nonspecific background irregularities 8.7%, generalized spike–wave bursts 39.3%, multifocal spikes 7.5%, and focal spikes 29.5%. Physicians reported that 39.3% of the group had significant behavior problems. Learning problems of varying degree were reported to be present in 57% of the group, and 2.8% were reported to have had a neurological physical disability. The Demographics and Needs Survey results indicated that 94.4% of the children were living with their families with the remainder were living in group home/ foster home settings. Marital status of the childrenÕs parents was as follows: 70% married, 25% separated, and 5% single parent. With respect to schooling, 41.6% of the children were reported to be able to attend an ageappropriate regular classroom education program without difficulties, 22.3% were in a regular classroom program part of the time but were withdrawn for extra help each day and 36.1% were in a specialized classroom for children with intellectual impairment. The Child Behavior Checklist mean total behavior score for the group was 57.33 ± 2.27, with 15.9% of the group having t scores greater than 70. The mean group internalized behavior score was 55.8 ± 12.19, with 12.7% of the group having t scores greater than 70. The mean externalized behavior score was 55.09 ± 11.14, with 11.4% having t scores greater than 70. When the subscales within the internalized behavior scale were examined, the group mean t score for anxious/depressed behavior was 50.08 ± 9.11, with 7.6% of the t scores greater than 70. The mean group t score for withdrawn/depressed behavior was 58.96 ± 8.46, with 7.0% of the t scores above 70. When the subscales within the externalized behavior scale were examined, the group mean t score for rulebreaking behavior was 55.96 ± 11.4, with 4.2% of the t scores greater than 70. The mean group t score for aggressive behaviors was 58.73 ± 8.89, with 11.8% of the t scores being greater than 70. The group mean t scores for the remaining subscales contributing to the total behavior score, but not part of either the internalized or externalized behavior scores, were as follows: somatic complaints 58.6 ± 8.94 (7.6% >70); social problems 61.70 ± 10.73 (16.5% >70); and attention problems 64.56 ± 12.24 (26.9% >70). There was no significant difference in frequency of t scores >70 between children seen in hospital clinics and those seen in the private office setting. Elevated t scores for total behavior, internalized behavior, externalized behavior, attention difficulties, and social behavior problems were significantly more frequent among children whose cognitive impairment was sufficient to warrant specialized classroom placement. Seizure type, age of patient, sex of patient, number and types of antiepileptic medications taken, family demographics, and
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type of EEG pattern did not significantly differ between the group of patients with significantly elevated t scores for each of the above mentioned scales and those without such scores. The number of community services per patient at the time of the survey as identified by the childÕs parent/ caregiver was 0.97 ± 1.4 (range, 0–8). 44.9% of the parents/caregivers reported that their child had not needed the support of a community service agency; 24.6% reported using one agency on a regular basis, 11.4% using two agencies, 10.2% three, and 8.9% using more than three. The types of community services used were as follows: social service agencies by 20%, child development services by 19%, parent relief services by 8%, behavior management by 7%, psychologist by 7%, and community home care by 5%. When parents/caregivers were asked about the use of specialized education facilities (either within school or in addition to) in the last 6 months, 44.9% responded affirmatively. As for the need for specialized education facilities in the future, 31.3% felt their child would need such services in the next year, 27.1% for the next 2 to 5 years, and 35.5% for greater than 5 years. When parents/caregivers were questioned about the frequency of use of parent relief services, 72.5% responded that they had not required this type of service in the last 6 months; 12.0% had used it once, 4.2% twice, and 10.9% three or more times. Within the next year, 15.1% of the parents responded that they expected to use this type of service, and within the next 2 to 5 years, 15% of parents felt that they would be requiring this type of service; 18.8% of the parents felt they would be requiring this service in about 5 years. Twenty-six and one-tenth percent of parents/caregivers of parents stated that, during the last 6 months, their child had been living out of their home in a specialized residence for a period. When asked about the need for this type of facility for their child the future, 15.1% parents projected this need in the next year, 12% for the next 2 to 5 years, and 29% in greater than 5 years. When parents/caregivers were questioned about the frequency of use of specialized medical service (need for admission to hospital or emergency ward for greater than 24 hours for seizure-related problems), 79% stated that their child had not required this service in the last 6 months; 10.2% had required this type of service once in the last 6 months, 1.2% twice, and 9.6% three or more times. When parents/caregivers were asked if they felt their child would require this type of service within the next year, 15.2% responded affirmatively. When parents/caregivers were asked to forecast their childÕs need for this service in the next 2 to 5 years and after 5 years, an affirmative answer was given by 11.5 and 15.2% respectively. When parents/caregivers were asked about the frequency of use of a mental health service for emotional support for patient and family in last 6 months, 74.9%
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stated that they had not used this type of service in the last year; 10.8% of respondents stated that they had used this type of service once in the last 6 months, 2.4% twice, and 12% three or more times. When parents/caregivers were asked about future requirement for this type of service, 18.5% felt that they would in the next year, 15.1% within the next 2 to 5 years, and 17.5% in greater than 5 years. Parents/caregivers presently requiring access to specialized community services for their child in the areas of living, education, emotional support, and/or medical services projected the continued need for services for the immediate future (within the year), midterm (next 2–5 years), and long term (greater than 5 years). Parents/ caregivers not using community services at the time of the survey did not project a future need. The only predictor of need for ongoing access to specialized community services was the presence of a cognitive disability requiring specialized education. Seizure type, number of medications used, types of medication used, elevated total behavior scores, and presence of elevated total behavior, internalized behavior, and/or externalized behavior scores as recorded by the CBCL did not correlate with present or future need for specialized community services.
4. Discussion The parent/caregiver-completed CBCL in this crosssectional descriptive survey of epileptic children demonstrated an increased frequency of elevated behavior scores for all the scales and, specifically, scales for attention and social problems. This finding is similar to frequencies of behavior problems previously reported using the CBCL [1–6,14,15]. As well, it is similar to the results of our previous study using the same set of questionnaires in the same clinical setting [6]. The consistent finding of increased frequency of behavior difficulties over time in our clinical setting, coupled with the results of other investigators, strongly supports the observation that behavior problems are common in epileptic children. The etiology of this association remains unclear, but it is most likely related to a common preexisting underlying pathology. Austin et al. [1,2], using the parent-completed CBCL, reported that behavior problems were reported to be frequently present in the 6 months prior to first seizures in newly diagnosed epileptic children. In a later study, Dunn and Austin [16], using teacher-completed CBCL confirmed the observations of Austin et al. [1,2]. Other studies have suggested that the presence or absence of behavior problems could be related to the type of epilepsy [11,16–18], types of antiepileptic medications taken [10], and family demographics [3,7,9,12]. In the present study, we were unable to confirm these associations.
Seizure intensity was not examined as a predictive variable in this study. It would seem reasonable to hypothesize that parents/caregivers of children with greater seizure intensity would report a greater frequency of significantly elevated behavior scores. It is difficult, however, to quantitatively estimate the intensity of a childÕs average seizure. Seizure frequency has been used in some studies as a surrogate variable, but was not used in this study. It was felt that it would be too difficult to determine over which period to examine the frequency of seizures, and how to compare seizure attack frequencies for convulsive epilepsy and nonconvulsive epilepsy. Bourgeois [10] suggested that difficulty with control of seizures is significantly correlated with the number of antiepileptic drugs taken. In our study the number of antiepileptic medications taken was not found to be related to increased frequency of significantly elevated behavior scores. This would suggest that seizure frequency was not predictive of behavior difficulties. Like Camfield et al. [19], we found that no one EEG pattern was more frequent among children who had significantly elevated behavior scores versus those with normal scores. As only interictal EEG patterns were used, it is still possible that a correlation with ictal EEG onset and behavior might exist. Intellectual difficulties have been reported to be more prevalent in this group of children and to be associated with increased risk of psychopathology [8,20]. In our survey, the presence of cognitive difficulties as measured by the child not being able to attend a regular classroom because of a significant cognitive impairment was the only variable that was significantly correlated with an increased frequency of elevated behavior scores. As well, children who were not in a regular classroom were significantly more likely to have been reported by their parents/caregivers to require the use of a community agency in the 6 months prior to the survey and to have an ongoing need for at least one community service in the future. Seizure type, number of antiepileptic medications taken, presence of physical handicap, EEG pattern, and family demographics did not predict present or anticipated/ projected use of specialized services. The association between increased future needs for specialized services and the presence of significant cognitive difficulties was also observed in our previous study [6]. The lack of association with seizure variables was unexpected, suggesting that epilepsy per se does not play a significant role in parent-perceived future needs for their children. Though our survey detected a significant increase in the frequency of behavior problems when compared with the general population, the majority of parents/ caregivers did not indicate an increased use of mental health services in the last 6 months nor a need to use such a service. This underusage of mental health facilities by this group had previously been reported by Otto
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et al. [4], who found that two-thirds of patients identified in need of mental health services had not used them. Our survey was not designed to answer the question why this group was not using these services. Possible reasons such as lack of parental/physician knowledge of the types of services available in the community, long waiting lists, reluctance to use the services on the part of parent or treating physicians, lack of programs, and a negative connotation associated with the use of mental health programs need to be addressed in a future study. Another possibility is that parents/caregivers prioritized the physical health concerns over the social behavioral concerns. Several reasons could account for the lack of correlation between seizure and family demographic variables and reported behavior problems in our survey in comparison with previous studies. Patient ascertainment bias plays a significant role in defining the patient population. The design of our study differed significantly from that of previous studies in that our study population was drawn from both hospital and office settings rather than mainly from a specialized pediatric epilepsy clinic setting. Previous studies excluded children who had significant cognitive difficulties, whereas ours did not. Unlike previous studies, we attempted to recruit all patients in a consecutive prospective manner rather than using the voluntary referral-to-study method. Random volunteer recruitment has the inherent difficulty of selectively biasing toward persons with a vested interest in the project. As well, the 90% participation rate further suggests that a representative sample was achieved in the present study. Though we used a well-recognized standardized measurement of behavior problems in children, which has been used by other investigators in the same population, it is possible that the parent/caregiver-completed CBCL misclassified some of the study population. Jensen and Watanabe [21] reported that when the CBCL was compared with the Diagnostic Interview Schedule for Children, a false-negative rate of 10% and false-positive rate of 20% were obtained. When Ott et al. [5] compared the CBCL and the Schedule for Affective Disorders and Schizophrenia for School-Age Children (K-SADS) in a group of epileptic children, he found that K-SADS identified more children with psychopathology than the CBCL. Therefore, it is possible that some of the persons who had significant behavior problems could have been missed, accounting for some of the differences between studies. Other limitations of this study are its design as a descriptive survey, the numbers of patients in various subgroups, and the definition of learning disability. The descriptive design provides for a ‘‘scan’’ of the prevalence of the problem, a step necessary for planning of resources. As the study was not hypothesis-driven, it does not allow for conclusions to be drawn as to the cause of the problem.
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It does supply information necessary for designing future hypothesis-driven studies. The small numbers of patients in several groups did not allow for statistical analysis of the interrelationship of the various variables. The definition of learning difficulties used in this survey—of a child requiring withdrawal from regular classroom for teaching on a routine basis, some of the time or all of the time—was an operational definition. Results of psychoeducational assessments were not requested. In summary, through use of the parent/caregivercompleted CBCL, our survey confirmed the increased frequency of behavior problems in children with epilepsy. Unlike other studies, we found that the presence of significant cognitive difficulties was the only variable that was associated with an increased risk of behavior problems. When planning resources for treatment of children with epilepsy, treatment of ongoing behavior issues needs to be included.
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