Epilepsy & Behavior 45 (2015) 105–109
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Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Socioeconomic deprivation is an independent risk factor for behavioral problems in children with epilepsy Joanna Carson a,1, Andrew Weir a,1, Richard F. Chin a,b,c,⁎,2, Ailsa McLellan c,2 a b c
The University of Edinburgh, UK Muir Maxwell Epilepsy Centre, UK Royal Hospital for Sick Children, Edinburgh, UK
a r t i c l e
i n f o
Article history: Received 29 January 2015 Revised 25 February 2015 Accepted 8 March 2015 Available online 2 April 2015 Keywords: Epilepsy Behavior Deprivation
a b s t r a c t Aim: The aim of this study was to examine whether socioeconomic deprivation in children with epilepsy (CWE) increases risk for behavioral problems independent of seizure factors. Methods: A cross-sectional study was done in which parents of children attending a specialist epilepsy clinic were invited to complete a child behavior checklist (CBCL) questionnaire about their child. Medical and sociodemographic data on CWE were obtained through their pediatric neurologists. Home postal code was used to obtain quintiles of Scottish Index of Multiple Deprivation 2012 (SIMD2012) scores for individuals. Lower (1–3) quintiles correspond to higher socioeconomic deprivation. Regression analysis was used to investigate whether a lower quintile was an independent risk factor for scores N63 (significant behavioral problem). Results: Parents of 87 children (42 male, mean age of 10.5 years) were enrolled. Fifty-nine percent had total scores N63. A higher proportion of children from quintiles 1–3 compared to those from quintiles 4–5 had externalizing (49% vs. 25%, p = 0.02) and total (54% vs. 30%, p = 0.02) scores N63. Adjusted OR of quintiles 1–3 vs. 4–5 for scores N63 = 14.8, 95% CI = 3.0, 68.0. Fewer children with scores N63 and from quintiles 1–3 were known to the child and adolescent mental health service (CAMHS) compared to those in quintiles 4–5 (p = 0.01). Interpretation: Socioeconomic deprivation was an independent risk factor for behavioral problems in CWE. Children with epilepsy and behavioral problems who lived in socioeconomically deprived areas received less help. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Epilepsy is the most common serious neurological disorder in children, with a prevalence of 1% [1]. Children with epilepsy are more likely to have behavioral problems [2] than age- and gender-matched controls, but the cause(s) for this increased likelihood is not fully understood. Antiepileptic drugs [3], type of epilepsy, early age of onset [4], longstanding epilepsy, and lack of seizure control [5,6] have all been associated with increased behavioral problems in children with epilepsy. The interaction between behavioral problems, epilepsy, and intellectual disability is also well known [7]. However, 25% of children with epilepsy, including those without learning difficulty, have preexisting behavioral problems when their epilepsy is diagnosed suggesting that there are other factors separate from seizure-related factors that independently increase risk for behavioral problems [8].
⁎ Corresponding author at: Muir Maxwell Epilepsy Centre, Child Life and Health, 20 Sylvan Place, Edinburgh EH9 1UW, UK. Tel.: +44 1315360841; fax: +44 1315360821. E-mail address: [email protected] (R.F. Chin). 1 Contributed equally to the study. 2 Joint last author.
http://dx.doi.org/10.1016/j.yebeh.2015.03.009 1525-5050/© 2015 Elsevier Inc. All rights reserved.
The increased prevalence in behavioral problems in children with epilepsy may be partly attributable to the fact that this condition is often a chronic disorder, leading to increased disruptions to development and family life due to frequent hospitalization and limited activities [9]. However, compared to other chronic illnesses viz: asthma [10,11], cardiac disorders [12], and diabetes [6], epilepsy has the strongest association with behavioral and psychiatric problems. Thus, there are factors specific to epilepsy that increase risk. Socioeconomic deprivation is associated with increased risk for epilepsy in adults [13,14], but there is an ongoing debate on whether this occurs in children with epilepsy [15–17]. Children from families from high deprivation areas are at greater risk of behavioral problems [18]. This increased prevalence of behavioral problems has been postulated to be related to poor nutrition, family stress, financial stress, low material quality of home [1], poor compliance with medication [2], and abnormal family function [7,10,19,20]. It is important to identify children with behavioral problems, so that they can receive more appropriate management. Previous studies have shown that people from high deprivation areas are less likely to have access to appropriate medical services [21]. In Scotland, such diagnosis and management is principally facilitated through the multidisciplinary child and adolescent mental health service (CAMHS). Referral to the
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CAMHS can be made by doctors, social workers, or schools and is appropriate for a child with intellectual disability, mental health problems, and/or behavioral problems. Within Edinburgh, the principal population served by the Royal Hospital for Sick Children (RHSC), Edinburgh, there are five CAMHS centers distributed throughout and located in areas of high population density. Services in these centers are free at the point of delivery and are thus available to anyone who has been referred. This study aimed to test the hypotheses that among attendees to the epilepsy clinic at the Royal Hospital for Sick Children, Edinburgh (RHSC): 1. Children with epilepsy will have a high prevalence of CBCL total Tscores N63, and a higher mean total T-score compared to the reference general population. 2. Children from the areas of higher deprivation (SIMD quintiles 1–3) are at greater risk of having T-scores N63 compared to those from lower deprivation areas (SIMD quintiles 4–5). This risk will be independent of seizure frequency, longstanding epilepsy, focal epilepsy, multiple antiepileptic drugs (AEDs), presence of abnormality on MRI scan, and those with intellectual disability. 3. Children with T-scores N63 and who reside in an area of higher deprivation will be less likely to be known to CAMHS. 2. Material and methods The study was completed in keeping with the STROBE guidelines for observational studies. All parents and/or caregivers of children attending the epilepsy clinic at the RHSC over two periods (30/10/11–15/12/11 and 6/11/12–11/12/ 12) were invited to enter the study. RHSC, being a part of the National Health Service of Scotland, provides free at the point of delivery secondary epilepsy services for the children of the City of Edinburgh and tertiary services for all child residents in the South East of Scotland. Thus, health care is determined by clinical need and not by the ability of families to pay. Volunteers were informed that the study was a health service evaluation focused on identifying the behavioral needs of children who attended the epilepsy clinic, determining factors associated with increased risk for behavioral problems, and determining how often those with identified needs were receiving appropriate support. All parents were further informed that the information received would be anonymized, that every effort would be made to protect patient confidentiality, and that lack of entry into the study would not affect the clinical care their child received. Parents were asked to complete an anonymized CBCL questionnaire about their child to aid in the evaluation. The child behavior checklist (CBCL) is a widely used validated instrument for identification of behavioral and psychiatric disorders in children with a specificity of 83% and a sensitivity of 66% [22]. Its use has been validated in children with epilepsy [23,24]. Detailed information on how the CBCL is scored is available elsewhere [25]. Questionnaires were scored using standard gender and age specific criteria to give individual total internalizing (Ti), total externalizing (Te), and total overall (Tt) scores. Ti-scores provide a measure of anxious, withdrawn, and depressed behavior and somatic complaints. Te-scores can serve as a measure of rule breaking and aggressive behavior. Tt-scores are a measure for the presence of general behavioral problems. Any type of T-score N63 (whether Ti, Te, or Tt) is accepted as being in the clinical range for behavioral problems within that respective domain [23]. Thus, a child with Ti N 63 would be considered as having clinically significant internalizing behavioral problems. A T-score of 60–63 is described as a borderline clinical score, and b60 as normal. In this study, behavioral T-scores were dichotomized into N 63 and ≤63, with scores N63 defined as indicating the presence of behavioral problems. Clinical and demographic data on children of enrolled parents were obtained using a standardized study proforma. Data were obtained from direct interview of individual children's pediatric neurologist and from
review of medical notes by two of the authors (JC and DW). Etiology of the epilepsy was determined by the children's pediatric neurologists and was subsequently categorized as “Symptomatic” for children with symptomatic or cryptogenic epilepsy, and “Nonsymptomatic” for all other types of epilepsy. Children were considered as having an intellectual disability if a previous neurological and/or psychological assessment concluded that they had. Home postal code for individual families was used to obtain a quintile from the most up-to-date Scottish Index of Multiple Deprivation (SIMD) available at the time of the study, SIMD2012. The Scottish Index of Multiple Deprivation (SIMD) is a reliable and effective method of measuring socioeconomic status. An area-based measure of deprivation, it incorporates data on seven domains (education, housing, access, crime, income, health, and employment [3]) to rank each area in Scotland, from high deprivation to low deprivation. The areas can be divided into quintiles, with the 1st quintile being the most deprived (i.e., lowest SES) and the 5th being the least deprived. This tool has been used in various research settings and by the UK government for policy formation [26]. The 1st quintile represents areas of highest deprivation, and the 5th are those with lowest deprivation. The sample size for this study necessitated that we pooled quintiles and thus compared those in quintiles 1–3 (high socioeconomic deprivation) to those in quintiles 4–5 (low socioeconomic deprivation). In addition, each SIMD domain was split into either high or low deprivation, and the percentage of children scoring N63 on the CBCL was compared within each SIMD domain. Data analysis was carried out using SPSS software Version 17 (Chicago, Illinois, USA) and Minitab software. Minitab software was used to identify exact intergroup differences in proportions, and their 95% confidence intervals, of children with CBCL T-scores N63. Binary logistic regression analysis was used to examine whether children from SIMD quintiles 1–3 were more associated with having T-scores N63 than those from quintiles 4–5 after adjusting for the other factors listed above. Fisher's exact tests were used to examine differences in proportion of children with T-scores N63 and known to CAMHS according to SIMD2012 quintiles. 2.1. Ethics Ethical approval was not required since the study was carried out as part of a health service evaluation. The study was discussed with the South East Scotland Research Ethics Committee 2 who confirmed that its approval was unnecessary. 2.2. Results Ninety-seven parents were approached for the study. Five did not agree to participate, mainly on the grounds of time limitations, and thus no data on these were collected. Five whose epilepsy was in remission were excluded. No data on those excluded were collected. Of the 87 children whose parents had agreed to participate, 42 (48.3%) were male, and 45 (51.7%) were female. The age range was 2–17 years, and the mean age was 10.5 years. The mean Tt-score in this study was 60.4 (range: 28–84) which was significantly higher than the reference CBCL mean population score of 50 (p b 0.001). Fifty-nine percent of the (95% CI 48–64%) children in this study had Tt-scores N63, a clinically significant score. A greater proportion of children (49%) who lived in SIMD2012 quintile areas 1–3 had Tt-scores N63 compared to those from quintiles 4–5 (25%) (p = 0.02). Fifty-four percent of those in quintiles 1–3 had Te N 63, compared to 30% of those in quintiles 4–5 (p = 0.02). A higher proportion of children in quintiles 1–3 (49%) had Ti-scores N63 compared to those in quintiles 4–5 (34.1%), but this was not statistically significant (p = 0.1). Children with SIMD quintiles 1–3 compared to quintiles 4–5 were associated with a greater likelihood of Tt N 63 (OR 14.8, 95% CI 3.0, 68.0) independent of seizure frequency, seizure type, number of antiepileptic drugs, presence of an MRI abnormality, whether there was a known intellectual disability, and etiology (see Table 1).
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Table 1 Regression analysis of factors associated with Tt N 63. Variable
% patients with Tt N 63 (95% CI)
Group (n)
Gender Deprivation Income Employment Health Education Housing Geographical access Crime level in area of residence Seizure frequency No. of AEDs Seizure type MRI abnormality
Intellectual disability Known to CAMHS Etiology
Male (42) Female (45) High (43) Low (44) High (40) Low (47) High (37) Low (50) High (37) Low (50) High (41) Low (46) High (55) Low (32) High (31) Low (56) High (42) Low (45) b1/month (56) N1/month (31) 1 (52) ≥2 (25) Focal (40) Generalized (44) Present (33) Not present (49) None done (5) Present (40) Not present (47) Known (21) Not known (66) Symptomatic (43) Not symptomatic (44)
38 (25–53) 44 (31–59) 54 (39–67) 30 (18–44) 55 (40–69) 30 (19–44) 51 (36–67) 34 (22–48) 57 (38–69) 30 (19–44) 51 (37–66) 33 (21–47) 47 (41–69) 31 (18–49) 39 (19–46) 43 (34–59) 52 (38–67) 31 (20–46) 38 (26–51) 48 (32–65) 42 (30–56) 36 (20–55) 43 (29–58) 41 (28–56) 42 (27–59) 41 (28–55) – 53 (38–67) 32 (20–46) 67 (45–83) 33 (23–45) 61 (46–74) 57 (42–70)
Among each constituent SIMD2012 domain, income deprivation (OR 2.7, 95% CI = 1.2,7.0), crime (OR 2.4, 95% CI = 1.0,5.8), and health deprivation (OR 2.05, 95% CI = 1.3,7.4) were significantly associated with Tt-scores N63 on univariable analysis, but no individual constituent factor was significant on multivariable analysis (Table 1). Thirty-three percent of those with Tt-scores N63 were unknown to CAMHS. Fewer children with high socioeconomic deprivation and T t -scores N63 (6/23, 26%) were known to CAMHS compared to those with low socioeconomic deprivation (8/13, 62%) (p = 0.009) (see Table 2.) 2.3. Discussion Although there have been sporadic attempts to look at associations between socioeconomic status and behavior in children with epilepsy [27–29], to our knowledge, this is the first study to focus systematically on the relationship between socioeconomic deprivation and behavioral problems in children with epilepsy. The main findings from our study are: (1) six out of every ten children with epilepsy in this clinic-based study had behavioral problems; (2) socioeconomic deprivation was an independent risk factor for behavioral problems in children with Table 2 Children with behavioral problems known to CAMHS according to socioeconomic deprivation (SED). High SED represents SIMD quintiles 1–3 and low SED represents SIMD quintiles 4–5.
High SED Low SED
CBCL score
Known to CAMHS (%)
Not known (%)
Total
≤63 N63 ≤63 N63
2 (10.0%) 6 (26.1%) 5 (16.1%) 8 (61.5%)
18 (90.0%) 17 (73.9%) 26 (83.9%) 5 (38.5%)
20 23 31 13
Fisher's exact test, p = 0.009.
Univariable analysis
Multivariable analysis
Odds ratio (95% CI)
Odds ratio (95% CI)
0.77 (0.33, 1.81)
–
2.74 (1.14, 6.63)
14.81 (3.0, 67.98)
2.74 (1.19, 6.97)
7.54 (0.49,14.33)
2.89 (0.86, 4.89)
–
2.05 (1.26, 7.44)
2.54 (0.67, 9.43)
3.06 (0.91, 5.17)
0.28 (0.02, 3.25)
2.17 (0.79, 4.93)
–
1.97 (0.34, 2.06)
–
2.44 (1.02, 5.84)
2.18 (0.65, 6.91)
0.64 (0.26, 1.56)
–
1.56 (0.57, 4.26)
5.35 (0.89, 32.38)
1.07 (0.45, 2.54)
0.44 (0.11, 1.83)
1.07 (0.44, 2.62)
0.78 (0.19, 3.22)
2.28 (0.95, 5.48)
1.80 (0.41, 8.01)
4.00 (1.41,11.34)
14.67 (2.68, 80.4)
0.86 (0.37, 2.02)
–
epilepsy; and (3) children who lived in more socioeconomically deprived areas and had behavioral problems were less frequently known to CAMHS compared with those from less socioeconomically deprived areas. Our finding that 59% children attending a specialist epilepsy clinic had CBCL Tt-scores N 63 is supportive of our hypothesis that the prevalence of behavioral problems is much higher than in the general childhood population, which has been reported as 7–9% [30]. Our results, on a clinic-based sample and thus not necessarily representative of the broader population of children with epilepsy, are comparable with the somewhat lower rate of behavioral problems reported in populationbased studies, using different assessment methods. For example, in a population-based study that used a combination of Development and Well-Being Assessments, specialist psychiatric interviews as well as parental reports of emotional and behavioral problems, 37% (95% CI 22–49%) of children with epilepsy had behavioral problems compared to 9% of controls [4]. Another population-based study that used Achenbach scales and Raven matrices found that a greater proportion (45%) of children with epilepsy had psychosocial problems when compared to age- and gender-matched controls [2]. In the general population, 20% of healthy but socioeconomically deprived children have behavioral problems [18]. Compared to this, it was striking that 54% of the children attending our specialist epilepsy clinic and who lived in high deprivation areas had behavioral problems. It is possible that our findings may at least be partly explained by the clinicbased source of our sample which by its nature may reflect a population of children with the more severe forms of epilepsy. Indeed, epilepsy factors such as seizure frequency, length of time with epilepsy, number of AEDs, and presence of abnormality on MRI scan have all been associated with behavioral problems in various other studies [3–5,7]. However, we found high deprivation was associated with Tt-scores N 63 independent of these factors. We also observed that high deprivation was associated
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with high Te-scores. These data are consistent with findings that social factors, including poverty and social stress, are part of the biosocial interactive model of externalizing behavior [31] and that in the general population, children of low socioeconomic status are more likely to have externalizing behavioral problems and academic underachievement [32]. In contrast, one study of patients with complex partial seizures showed association with internalizing behavioral problems [33]. We investigated the composite domains to identify deprivation factors that were most associated with behavioral problems. On univariable analysis, health, household income, and crime levels in the area of residence were significantly associated with increased behavioral problems in children with epilepsy, but no single factor was significant on multivariable analysis. This may be because deprivation is a complex interplay of factors. A large UK study on socioeconomic status and behavior in a general population of 6000 children found that no individual social factor could be singled out as a risk factor for behavioral problems, but together, social factors accounted for half of the variation in behavioral problems [18]. Features of deprivation that have been associated with behavioral problems in previous studies include parenting behavior, low material quality of the home, poor nutrition, as well as the effect of genetics [11,14,19,34]. Future studies on factors associated with behavioral problems in children with epilepsy should include a determination of which of these factors are important. In the current study, children with epilepsy and behavioral problems from high deprivation areas were less frequently known to CAMHS than those from low deprivation areas. On the other hand, similar proportions of those with intellectual disability and high deprivation compared to those with intellectual disability and low deprivation were known to CAMHS. These results suggest that children with epilepsy and behavioral problems are less likely to present to professional services if they do not also have overt intellectual disability. It was perhaps not surprising that a high proportion (53%) of children with intellectual disability in our cohort had clinically significantly high CBCL Tt-scores since intellectual disability is very strongly correlated with behavioral problems [35]. Thus, it can be a major confounding factor in studies of epilepsy and behavior. To address this possibility, we included the presence of intellectual disability in our regression model but still found socioeconomic status to be an independent risk factor. In the current study, there was some evidence on univariable analysis that intellectual disability itself was a predictor for high CBCL scores N 63, but not on multivariable analysis. Possible explanations for this include that our sample size was modest, and/or the study was clinic-based. The high CBCL scores for children with ID may also have been due to higher self-reporting by parents of such children where behaviors are placed under greater scrutiny than those exhibited by other siblings — diagnostic overshadowing. Recognizing behavioral problems can be challenging, even for people who spend considerable time with children. Parents who are preoccupied with concerns about family finances [36] or if they are not the primary carers may have difficulty in recognizing behavioral problems in their child. Teachers are more likely to recognize behavioral problems if the child is not meeting education goals and is aggressive or disruptive [37], suggesting that children whose behavioral problems are not disruptive may be less likely to be noticed. Findings from a clinic-based study indicate that clinicians only identified emotional or behavioral problems in a quarter of children who had a parent-rated disorder [38]. This could have been because the clinicians were not enquiring enough about behavioral problems in the children, or because parents were not reporting concerns when questioned. Up to 55% of the parents in that study would not discuss behavioral and/or emotional concerns about their child with their pediatrician [38], but it was beyond the scope of that study to identify possible reasons for this parental reluctance. Findings from another study, though, showed that when mothers were from a low deprivation group (higher socioeconomic status) they were more likely to discuss psychosocial issues with their child's clinician [39]. Lack of detection of behavioral problems may also be related
to differences between socioeconomic groups in their attitude to coping with difficulties; people from areas of high deprivation may adopt increased acceptance of difficult situations in their daily lives with resultant reduced reporting/identification of behavioral problems. Taken together, these data, in addition to our own findings, highlight the value of an objective screening tool for behavioral problems, which would be helpful in assessing children attending an epilepsy clinic. 2.4. Study limitations Our sample size was modest, and the study population was obtained from a tertiary epilepsy clinic which may raise questions about representativeness of our sample. It is possible that the used SIMD2012 scores, despite being an accurate measure of the relative deprivation in an area, may not correctly represent an individual's level of deprivation, but this is a widely accepted method for estimating socioeconomic deprivation. We had no matched controls but were able to compare our findings with data from the published literature. The child behavior checklist is primarily a screening instrument for behavioral problems, and it is possible that some of the children that scored highly in our study did not ultimately have clinically significant behavioral problems. Finally, our study has identified that socioeconomic status was independently associated with behavioral problems in children with epilepsy; however, no causal assumption can be made on the basis of the current study. 2.5. Conclusion In conclusion, this study found that children attending a specialist epilepsy clinic were more likely to have behavioral problems than the general population. Use of an objective screening tool such as the CBCL may be useful in epilepsy clinics in order to identify those at risk of behavioral problems. Socioeconomic deprivation, particularly in the health and income domains, was significantly associated with behavioral scores in the clinical range, independent of seizure factors. Of those with behavioral problems and epilepsy, children from areas of high deprivation were less likely to be known to CAMHS than those from low deprivation areas. Thus, people who share in the care of children with epilepsy should be made aware of the high prevalence of behavioral problems, especially in groups who have an increased risk, such as those from deprived areas. Further research on the relationship between socioeconomic status, epilepsy, and behavioral problems is needed to identify interventional strategies. Acknowledgments The authors would like to thank the patients and their parents for participating in the study. JC was the recipient of a University of Edinburgh Student Selected Component Bursary fund. The Muir Maxwell Epilepsy Centre receives support from the Muir Maxwell Trust. Conflicts of interest None. We confirm that we have read the journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. References [1] Reading R, Haynes R, Beach R. Deprivation and incidence of epilepsy in children. Seizure 2006;15(3):190–3. [2] Modi AC, Rausch JR, Glauser TA. Patterns of nonadherence to antiepileptic drug therapy in children with newly diagnosed epilepsy. JAMA 2011;305(16):1669–76. [3] Payne RAG. UK indices of multiple deprivation — a way to make comparisons across constituent countries easier. Health Stat Q 2012:53. [4] Hinshaw SP. Externalizing behavior problems and academic underachievement in childhood and adolescence: causal relationships and underlying mechanisms. Psychol Bull 1992;111(1):127–55.
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Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Socioeconomic deprivation is an independent risk factor for behavioral problems in children with epilepsy Joanna Carson a,1, Andrew Weir a,1, Richard F. Chin a,b,c,⁎,2, Ailsa McLellan c,2 a b c
The University of Edinburgh, UK Muir Maxwell Epilepsy Centre, UK Royal Hospital for Sick Children, Edinburgh, UK
a r t i c l e
i n f o
Article history: Received 29 January 2015 Revised 25 February 2015 Accepted 8 March 2015 Available online 2 April 2015 Keywords: Epilepsy Behavior Deprivation
a b s t r a c t Aim: The aim of this study was to examine whether socioeconomic deprivation in children with epilepsy (CWE) increases risk for behavioral problems independent of seizure factors. Methods: A cross-sectional study was done in which parents of children attending a specialist epilepsy clinic were invited to complete a child behavior checklist (CBCL) questionnaire about their child. Medical and sociodemographic data on CWE were obtained through their pediatric neurologists. Home postal code was used to obtain quintiles of Scottish Index of Multiple Deprivation 2012 (SIMD2012) scores for individuals. Lower (1–3) quintiles correspond to higher socioeconomic deprivation. Regression analysis was used to investigate whether a lower quintile was an independent risk factor for scores N63 (significant behavioral problem). Results: Parents of 87 children (42 male, mean age of 10.5 years) were enrolled. Fifty-nine percent had total scores N63. A higher proportion of children from quintiles 1–3 compared to those from quintiles 4–5 had externalizing (49% vs. 25%, p = 0.02) and total (54% vs. 30%, p = 0.02) scores N63. Adjusted OR of quintiles 1–3 vs. 4–5 for scores N63 = 14.8, 95% CI = 3.0, 68.0. Fewer children with scores N63 and from quintiles 1–3 were known to the child and adolescent mental health service (CAMHS) compared to those in quintiles 4–5 (p = 0.01). Interpretation: Socioeconomic deprivation was an independent risk factor for behavioral problems in CWE. Children with epilepsy and behavioral problems who lived in socioeconomically deprived areas received less help. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Epilepsy is the most common serious neurological disorder in children, with a prevalence of 1% [1]. Children with epilepsy are more likely to have behavioral problems [2] than age- and gender-matched controls, but the cause(s) for this increased likelihood is not fully understood. Antiepileptic drugs [3], type of epilepsy, early age of onset [4], longstanding epilepsy, and lack of seizure control [5,6] have all been associated with increased behavioral problems in children with epilepsy. The interaction between behavioral problems, epilepsy, and intellectual disability is also well known [7]. However, 25% of children with epilepsy, including those without learning difficulty, have preexisting behavioral problems when their epilepsy is diagnosed suggesting that there are other factors separate from seizure-related factors that independently increase risk for behavioral problems [8].
⁎ Corresponding author at: Muir Maxwell Epilepsy Centre, Child Life and Health, 20 Sylvan Place, Edinburgh EH9 1UW, UK. Tel.: +44 1315360841; fax: +44 1315360821. E-mail address: [email protected] (R.F. Chin). 1 Contributed equally to the study. 2 Joint last author.
http://dx.doi.org/10.1016/j.yebeh.2015.03.009 1525-5050/© 2015 Elsevier Inc. All rights reserved.
The increased prevalence in behavioral problems in children with epilepsy may be partly attributable to the fact that this condition is often a chronic disorder, leading to increased disruptions to development and family life due to frequent hospitalization and limited activities [9]. However, compared to other chronic illnesses viz: asthma [10,11], cardiac disorders [12], and diabetes [6], epilepsy has the strongest association with behavioral and psychiatric problems. Thus, there are factors specific to epilepsy that increase risk. Socioeconomic deprivation is associated with increased risk for epilepsy in adults [13,14], but there is an ongoing debate on whether this occurs in children with epilepsy [15–17]. Children from families from high deprivation areas are at greater risk of behavioral problems [18]. This increased prevalence of behavioral problems has been postulated to be related to poor nutrition, family stress, financial stress, low material quality of home [1], poor compliance with medication [2], and abnormal family function [7,10,19,20]. It is important to identify children with behavioral problems, so that they can receive more appropriate management. Previous studies have shown that people from high deprivation areas are less likely to have access to appropriate medical services [21]. In Scotland, such diagnosis and management is principally facilitated through the multidisciplinary child and adolescent mental health service (CAMHS). Referral to the
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CAMHS can be made by doctors, social workers, or schools and is appropriate for a child with intellectual disability, mental health problems, and/or behavioral problems. Within Edinburgh, the principal population served by the Royal Hospital for Sick Children (RHSC), Edinburgh, there are five CAMHS centers distributed throughout and located in areas of high population density. Services in these centers are free at the point of delivery and are thus available to anyone who has been referred. This study aimed to test the hypotheses that among attendees to the epilepsy clinic at the Royal Hospital for Sick Children, Edinburgh (RHSC): 1. Children with epilepsy will have a high prevalence of CBCL total Tscores N63, and a higher mean total T-score compared to the reference general population. 2. Children from the areas of higher deprivation (SIMD quintiles 1–3) are at greater risk of having T-scores N63 compared to those from lower deprivation areas (SIMD quintiles 4–5). This risk will be independent of seizure frequency, longstanding epilepsy, focal epilepsy, multiple antiepileptic drugs (AEDs), presence of abnormality on MRI scan, and those with intellectual disability. 3. Children with T-scores N63 and who reside in an area of higher deprivation will be less likely to be known to CAMHS. 2. Material and methods The study was completed in keeping with the STROBE guidelines for observational studies. All parents and/or caregivers of children attending the epilepsy clinic at the RHSC over two periods (30/10/11–15/12/11 and 6/11/12–11/12/ 12) were invited to enter the study. RHSC, being a part of the National Health Service of Scotland, provides free at the point of delivery secondary epilepsy services for the children of the City of Edinburgh and tertiary services for all child residents in the South East of Scotland. Thus, health care is determined by clinical need and not by the ability of families to pay. Volunteers were informed that the study was a health service evaluation focused on identifying the behavioral needs of children who attended the epilepsy clinic, determining factors associated with increased risk for behavioral problems, and determining how often those with identified needs were receiving appropriate support. All parents were further informed that the information received would be anonymized, that every effort would be made to protect patient confidentiality, and that lack of entry into the study would not affect the clinical care their child received. Parents were asked to complete an anonymized CBCL questionnaire about their child to aid in the evaluation. The child behavior checklist (CBCL) is a widely used validated instrument for identification of behavioral and psychiatric disorders in children with a specificity of 83% and a sensitivity of 66% [22]. Its use has been validated in children with epilepsy [23,24]. Detailed information on how the CBCL is scored is available elsewhere [25]. Questionnaires were scored using standard gender and age specific criteria to give individual total internalizing (Ti), total externalizing (Te), and total overall (Tt) scores. Ti-scores provide a measure of anxious, withdrawn, and depressed behavior and somatic complaints. Te-scores can serve as a measure of rule breaking and aggressive behavior. Tt-scores are a measure for the presence of general behavioral problems. Any type of T-score N63 (whether Ti, Te, or Tt) is accepted as being in the clinical range for behavioral problems within that respective domain [23]. Thus, a child with Ti N 63 would be considered as having clinically significant internalizing behavioral problems. A T-score of 60–63 is described as a borderline clinical score, and b60 as normal. In this study, behavioral T-scores were dichotomized into N 63 and ≤63, with scores N63 defined as indicating the presence of behavioral problems. Clinical and demographic data on children of enrolled parents were obtained using a standardized study proforma. Data were obtained from direct interview of individual children's pediatric neurologist and from
review of medical notes by two of the authors (JC and DW). Etiology of the epilepsy was determined by the children's pediatric neurologists and was subsequently categorized as “Symptomatic” for children with symptomatic or cryptogenic epilepsy, and “Nonsymptomatic” for all other types of epilepsy. Children were considered as having an intellectual disability if a previous neurological and/or psychological assessment concluded that they had. Home postal code for individual families was used to obtain a quintile from the most up-to-date Scottish Index of Multiple Deprivation (SIMD) available at the time of the study, SIMD2012. The Scottish Index of Multiple Deprivation (SIMD) is a reliable and effective method of measuring socioeconomic status. An area-based measure of deprivation, it incorporates data on seven domains (education, housing, access, crime, income, health, and employment [3]) to rank each area in Scotland, from high deprivation to low deprivation. The areas can be divided into quintiles, with the 1st quintile being the most deprived (i.e., lowest SES) and the 5th being the least deprived. This tool has been used in various research settings and by the UK government for policy formation [26]. The 1st quintile represents areas of highest deprivation, and the 5th are those with lowest deprivation. The sample size for this study necessitated that we pooled quintiles and thus compared those in quintiles 1–3 (high socioeconomic deprivation) to those in quintiles 4–5 (low socioeconomic deprivation). In addition, each SIMD domain was split into either high or low deprivation, and the percentage of children scoring N63 on the CBCL was compared within each SIMD domain. Data analysis was carried out using SPSS software Version 17 (Chicago, Illinois, USA) and Minitab software. Minitab software was used to identify exact intergroup differences in proportions, and their 95% confidence intervals, of children with CBCL T-scores N63. Binary logistic regression analysis was used to examine whether children from SIMD quintiles 1–3 were more associated with having T-scores N63 than those from quintiles 4–5 after adjusting for the other factors listed above. Fisher's exact tests were used to examine differences in proportion of children with T-scores N63 and known to CAMHS according to SIMD2012 quintiles. 2.1. Ethics Ethical approval was not required since the study was carried out as part of a health service evaluation. The study was discussed with the South East Scotland Research Ethics Committee 2 who confirmed that its approval was unnecessary. 2.2. Results Ninety-seven parents were approached for the study. Five did not agree to participate, mainly on the grounds of time limitations, and thus no data on these were collected. Five whose epilepsy was in remission were excluded. No data on those excluded were collected. Of the 87 children whose parents had agreed to participate, 42 (48.3%) were male, and 45 (51.7%) were female. The age range was 2–17 years, and the mean age was 10.5 years. The mean Tt-score in this study was 60.4 (range: 28–84) which was significantly higher than the reference CBCL mean population score of 50 (p b 0.001). Fifty-nine percent of the (95% CI 48–64%) children in this study had Tt-scores N63, a clinically significant score. A greater proportion of children (49%) who lived in SIMD2012 quintile areas 1–3 had Tt-scores N63 compared to those from quintiles 4–5 (25%) (p = 0.02). Fifty-four percent of those in quintiles 1–3 had Te N 63, compared to 30% of those in quintiles 4–5 (p = 0.02). A higher proportion of children in quintiles 1–3 (49%) had Ti-scores N63 compared to those in quintiles 4–5 (34.1%), but this was not statistically significant (p = 0.1). Children with SIMD quintiles 1–3 compared to quintiles 4–5 were associated with a greater likelihood of Tt N 63 (OR 14.8, 95% CI 3.0, 68.0) independent of seizure frequency, seizure type, number of antiepileptic drugs, presence of an MRI abnormality, whether there was a known intellectual disability, and etiology (see Table 1).
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Table 1 Regression analysis of factors associated with Tt N 63. Variable
% patients with Tt N 63 (95% CI)
Group (n)
Gender Deprivation Income Employment Health Education Housing Geographical access Crime level in area of residence Seizure frequency No. of AEDs Seizure type MRI abnormality
Intellectual disability Known to CAMHS Etiology
Male (42) Female (45) High (43) Low (44) High (40) Low (47) High (37) Low (50) High (37) Low (50) High (41) Low (46) High (55) Low (32) High (31) Low (56) High (42) Low (45) b1/month (56) N1/month (31) 1 (52) ≥2 (25) Focal (40) Generalized (44) Present (33) Not present (49) None done (5) Present (40) Not present (47) Known (21) Not known (66) Symptomatic (43) Not symptomatic (44)
38 (25–53) 44 (31–59) 54 (39–67) 30 (18–44) 55 (40–69) 30 (19–44) 51 (36–67) 34 (22–48) 57 (38–69) 30 (19–44) 51 (37–66) 33 (21–47) 47 (41–69) 31 (18–49) 39 (19–46) 43 (34–59) 52 (38–67) 31 (20–46) 38 (26–51) 48 (32–65) 42 (30–56) 36 (20–55) 43 (29–58) 41 (28–56) 42 (27–59) 41 (28–55) – 53 (38–67) 32 (20–46) 67 (45–83) 33 (23–45) 61 (46–74) 57 (42–70)
Among each constituent SIMD2012 domain, income deprivation (OR 2.7, 95% CI = 1.2,7.0), crime (OR 2.4, 95% CI = 1.0,5.8), and health deprivation (OR 2.05, 95% CI = 1.3,7.4) were significantly associated with Tt-scores N63 on univariable analysis, but no individual constituent factor was significant on multivariable analysis (Table 1). Thirty-three percent of those with Tt-scores N63 were unknown to CAMHS. Fewer children with high socioeconomic deprivation and T t -scores N63 (6/23, 26%) were known to CAMHS compared to those with low socioeconomic deprivation (8/13, 62%) (p = 0.009) (see Table 2.) 2.3. Discussion Although there have been sporadic attempts to look at associations between socioeconomic status and behavior in children with epilepsy [27–29], to our knowledge, this is the first study to focus systematically on the relationship between socioeconomic deprivation and behavioral problems in children with epilepsy. The main findings from our study are: (1) six out of every ten children with epilepsy in this clinic-based study had behavioral problems; (2) socioeconomic deprivation was an independent risk factor for behavioral problems in children with Table 2 Children with behavioral problems known to CAMHS according to socioeconomic deprivation (SED). High SED represents SIMD quintiles 1–3 and low SED represents SIMD quintiles 4–5.
High SED Low SED
CBCL score
Known to CAMHS (%)
Not known (%)
Total
≤63 N63 ≤63 N63
2 (10.0%) 6 (26.1%) 5 (16.1%) 8 (61.5%)
18 (90.0%) 17 (73.9%) 26 (83.9%) 5 (38.5%)
20 23 31 13
Fisher's exact test, p = 0.009.
Univariable analysis
Multivariable analysis
Odds ratio (95% CI)
Odds ratio (95% CI)
0.77 (0.33, 1.81)
–
2.74 (1.14, 6.63)
14.81 (3.0, 67.98)
2.74 (1.19, 6.97)
7.54 (0.49,14.33)
2.89 (0.86, 4.89)
–
2.05 (1.26, 7.44)
2.54 (0.67, 9.43)
3.06 (0.91, 5.17)
0.28 (0.02, 3.25)
2.17 (0.79, 4.93)
–
1.97 (0.34, 2.06)
–
2.44 (1.02, 5.84)
2.18 (0.65, 6.91)
0.64 (0.26, 1.56)
–
1.56 (0.57, 4.26)
5.35 (0.89, 32.38)
1.07 (0.45, 2.54)
0.44 (0.11, 1.83)
1.07 (0.44, 2.62)
0.78 (0.19, 3.22)
2.28 (0.95, 5.48)
1.80 (0.41, 8.01)
4.00 (1.41,11.34)
14.67 (2.68, 80.4)
0.86 (0.37, 2.02)
–
epilepsy; and (3) children who lived in more socioeconomically deprived areas and had behavioral problems were less frequently known to CAMHS compared with those from less socioeconomically deprived areas. Our finding that 59% children attending a specialist epilepsy clinic had CBCL Tt-scores N 63 is supportive of our hypothesis that the prevalence of behavioral problems is much higher than in the general childhood population, which has been reported as 7–9% [30]. Our results, on a clinic-based sample and thus not necessarily representative of the broader population of children with epilepsy, are comparable with the somewhat lower rate of behavioral problems reported in populationbased studies, using different assessment methods. For example, in a population-based study that used a combination of Development and Well-Being Assessments, specialist psychiatric interviews as well as parental reports of emotional and behavioral problems, 37% (95% CI 22–49%) of children with epilepsy had behavioral problems compared to 9% of controls [4]. Another population-based study that used Achenbach scales and Raven matrices found that a greater proportion (45%) of children with epilepsy had psychosocial problems when compared to age- and gender-matched controls [2]. In the general population, 20% of healthy but socioeconomically deprived children have behavioral problems [18]. Compared to this, it was striking that 54% of the children attending our specialist epilepsy clinic and who lived in high deprivation areas had behavioral problems. It is possible that our findings may at least be partly explained by the clinicbased source of our sample which by its nature may reflect a population of children with the more severe forms of epilepsy. Indeed, epilepsy factors such as seizure frequency, length of time with epilepsy, number of AEDs, and presence of abnormality on MRI scan have all been associated with behavioral problems in various other studies [3–5,7]. However, we found high deprivation was associated with Tt-scores N 63 independent of these factors. We also observed that high deprivation was associated
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with high Te-scores. These data are consistent with findings that social factors, including poverty and social stress, are part of the biosocial interactive model of externalizing behavior [31] and that in the general population, children of low socioeconomic status are more likely to have externalizing behavioral problems and academic underachievement [32]. In contrast, one study of patients with complex partial seizures showed association with internalizing behavioral problems [33]. We investigated the composite domains to identify deprivation factors that were most associated with behavioral problems. On univariable analysis, health, household income, and crime levels in the area of residence were significantly associated with increased behavioral problems in children with epilepsy, but no single factor was significant on multivariable analysis. This may be because deprivation is a complex interplay of factors. A large UK study on socioeconomic status and behavior in a general population of 6000 children found that no individual social factor could be singled out as a risk factor for behavioral problems, but together, social factors accounted for half of the variation in behavioral problems [18]. Features of deprivation that have been associated with behavioral problems in previous studies include parenting behavior, low material quality of the home, poor nutrition, as well as the effect of genetics [11,14,19,34]. Future studies on factors associated with behavioral problems in children with epilepsy should include a determination of which of these factors are important. In the current study, children with epilepsy and behavioral problems from high deprivation areas were less frequently known to CAMHS than those from low deprivation areas. On the other hand, similar proportions of those with intellectual disability and high deprivation compared to those with intellectual disability and low deprivation were known to CAMHS. These results suggest that children with epilepsy and behavioral problems are less likely to present to professional services if they do not also have overt intellectual disability. It was perhaps not surprising that a high proportion (53%) of children with intellectual disability in our cohort had clinically significantly high CBCL Tt-scores since intellectual disability is very strongly correlated with behavioral problems [35]. Thus, it can be a major confounding factor in studies of epilepsy and behavior. To address this possibility, we included the presence of intellectual disability in our regression model but still found socioeconomic status to be an independent risk factor. In the current study, there was some evidence on univariable analysis that intellectual disability itself was a predictor for high CBCL scores N 63, but not on multivariable analysis. Possible explanations for this include that our sample size was modest, and/or the study was clinic-based. The high CBCL scores for children with ID may also have been due to higher self-reporting by parents of such children where behaviors are placed under greater scrutiny than those exhibited by other siblings — diagnostic overshadowing. Recognizing behavioral problems can be challenging, even for people who spend considerable time with children. Parents who are preoccupied with concerns about family finances [36] or if they are not the primary carers may have difficulty in recognizing behavioral problems in their child. Teachers are more likely to recognize behavioral problems if the child is not meeting education goals and is aggressive or disruptive [37], suggesting that children whose behavioral problems are not disruptive may be less likely to be noticed. Findings from a clinic-based study indicate that clinicians only identified emotional or behavioral problems in a quarter of children who had a parent-rated disorder [38]. This could have been because the clinicians were not enquiring enough about behavioral problems in the children, or because parents were not reporting concerns when questioned. Up to 55% of the parents in that study would not discuss behavioral and/or emotional concerns about their child with their pediatrician [38], but it was beyond the scope of that study to identify possible reasons for this parental reluctance. Findings from another study, though, showed that when mothers were from a low deprivation group (higher socioeconomic status) they were more likely to discuss psychosocial issues with their child's clinician [39]. Lack of detection of behavioral problems may also be related
to differences between socioeconomic groups in their attitude to coping with difficulties; people from areas of high deprivation may adopt increased acceptance of difficult situations in their daily lives with resultant reduced reporting/identification of behavioral problems. Taken together, these data, in addition to our own findings, highlight the value of an objective screening tool for behavioral problems, which would be helpful in assessing children attending an epilepsy clinic. 2.4. Study limitations Our sample size was modest, and the study population was obtained from a tertiary epilepsy clinic which may raise questions about representativeness of our sample. It is possible that the used SIMD2012 scores, despite being an accurate measure of the relative deprivation in an area, may not correctly represent an individual's level of deprivation, but this is a widely accepted method for estimating socioeconomic deprivation. We had no matched controls but were able to compare our findings with data from the published literature. The child behavior checklist is primarily a screening instrument for behavioral problems, and it is possible that some of the children that scored highly in our study did not ultimately have clinically significant behavioral problems. Finally, our study has identified that socioeconomic status was independently associated with behavioral problems in children with epilepsy; however, no causal assumption can be made on the basis of the current study. 2.5. Conclusion In conclusion, this study found that children attending a specialist epilepsy clinic were more likely to have behavioral problems than the general population. Use of an objective screening tool such as the CBCL may be useful in epilepsy clinics in order to identify those at risk of behavioral problems. Socioeconomic deprivation, particularly in the health and income domains, was significantly associated with behavioral scores in the clinical range, independent of seizure factors. Of those with behavioral problems and epilepsy, children from areas of high deprivation were less likely to be known to CAMHS than those from low deprivation areas. Thus, people who share in the care of children with epilepsy should be made aware of the high prevalence of behavioral problems, especially in groups who have an increased risk, such as those from deprived areas. Further research on the relationship between socioeconomic status, epilepsy, and behavioral problems is needed to identify interventional strategies. Acknowledgments The authors would like to thank the patients and their parents for participating in the study. JC was the recipient of a University of Edinburgh Student Selected Component Bursary fund. The Muir Maxwell Epilepsy Centre receives support from the Muir Maxwell Trust. Conflicts of interest None. We confirm that we have read the journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. References [1] Reading R, Haynes R, Beach R. Deprivation and incidence of epilepsy in children. Seizure 2006;15(3):190–3. [2] Modi AC, Rausch JR, Glauser TA. Patterns of nonadherence to antiepileptic drug therapy in children with newly diagnosed epilepsy. JAMA 2011;305(16):1669–76. [3] Payne RAG. UK indices of multiple deprivation — a way to make comparisons across constituent countries easier. Health Stat Q 2012:53. [4] Hinshaw SP. Externalizing behavior problems and academic underachievement in childhood and adolescence: causal relationships and underlying mechanisms. Psychol Bull 1992;111(1):127–55.
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