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ORIGINAL ARTICLE |
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| Ahead of print
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A study on behavioral disorders, academic difficulties, and parental handling patterns in children with epilepsy
Rashmi Singh1, Neena Sawant2, Rajwanti Vaswani3
1 Department of Psychiatry, BYL & Topiwala Nair Hospital, Mumbai Central, Mumbai, Maharashtra, India
2 Department of Psychiatry, Seth GSMC and KEM Hospital, Mumbai, Maharashtra, India
3 Department of Pediatrics, Seth GSMC and KEM Hospital, Mumbai, Maharashtra, India
| Date of Submission | 18-Nov-2021 |
| Date of Acceptance | 26-Dec-2021 |
| Date of Web Publication | 12-Jul-2022 |
Correspondence Address:
Neena Sawant,
Department of Psychiatry, Seth GSMC and KEM Hospital, Parel, Mumbai, Maharashtra
India
 Source of Support: None, Conflict of Interest: None DOI: 10.4103/jpn.JPN_210_21
 Abstract | | |
Background: Various psychiatric comorbidities have been reported in children with epilepsy (CWE), but Indian data on the same are lacking. Aim: This study was undertaken with the aim to find the prevalence and type of behavioral problems in CWE, academic difficulties, and parental handling patterns. Materials and Methods: Sixty-five patients of CWE and 65 controls were recruited after ethics approval and parent consent. All children were interviewed and diagnosed for psychopathology as per ICD-10 criteria, along with Strength and Difficulties Questionnaire. Parental handling questionnaire was used to assess the patterns of care or control among parents. Academic difficulties were assessed using open- and closed-ended questions. Results: Behavioral disorders were seen in 44.6% of CWE when compared with 12% of the control group. Hyperkinetic disorders were significant in CWE. Conduct and oppositional defiant disorders were not so prevalent. On Strength and Difficulties Questionnaire, a significant difference was seen on domains of hyperactivity and prosocial behavior in CWE when compared with controls, whereas emotional, conduct, peer problems, and total difficulty scores revealed no significant differences in both the groups. Academic difficulties were more in CWE, although absenteeism was not seen in both the groups. Parents of CWE had significant scores on care and control domains and were more overprotective and rigid in their behaviors when compared with the control group parents. Conclusion: Significant behavioral disorders are seen in CWE, which entails the need to have a multidisciplinary approach for early diagnosis and better control of symptoms. Parental awareness and appropriate parenting need to be emphasized for better prognosis in CWE.
Keywords: Academic difficulties, behavioral problems, children with epilepsy, parental handling patterns
| Introduction | |  |
Epilepsy is the most prevalent, chronic neurological disorder affecting children and their families with an estimated prevalence of 5.5 cases per 1000 children.[1] The prevalence of associated psychopathology in children with epilepsy (CWE) is 16–77%. Reasons for psychopathology are multifactorial arising from a complex interplay of multiple etiological variables.[2]
The neurological variables include frequent, severe seizures, early age of onset, symptomatic epilepsy, and polytherapy.[3],[4],[5] Various psychiatric comorbidities seen in CWE are depression, anxiety, attention deficit/hyperactivity disorder (ADHD), conduct disorders, oppositional defiant disorder (ODD), for enuresis,[6] sleep disturbances,[7] increased tantrums, tic disorders,[6] and somatic complaints. The increase in behavioral problems can be attributed to chemical and structural changes in the neurocircuit, parental overprotection, low self-esteem, social stigma, and others.
Epilepsy frequently begins in childhood, and children’s awareness of what is happening to them is largely a function of their parents’ explanations and behavior. Children may feel ashamed and apprehensive about their epilepsy; parental overprotection may lead to anger and resentment among children.
There are very few Indian studies which have looked at parental understanding and handling of a chronic illness such as epilepsy. It has been established that children with long-standing epilepsy have behavioral problems at rates almost 5 times higher than general population children and 2½ times higher than children with other chronic medical conditions.[8] In general, CWE display more attention problems and internalizing problems (withdrawal, somatic complaints, anxiety, and depression symptoms) than they do externalizing problems such as acting out and conduct problems.[9]
As there is a dearth of Indian studies in CWE, we undertook the present study to determine the prevalence and type of behavioral disorders in CWE, academic difficulties, and parental handling patterns on the family. We also studied the correlation of behavioral problems with the parental handling patterns in CWE.
| Materials and Methods | | |
This was a cross-sectional observational study initiated after Institutional Ethics Committee permission and written informed consent of the parent and assent from the children having epilepsy (patient group) and those without epilepsy (control group) in the Outpatient Department of Pediatrics of a tertiary care hospital after satisfying the inclusion and exclusion criteria. Sample size was 65 in each group with inclusion criteria of children being diagnosed with epilepsy as per ILAE criteria, having epilepsy for more than 6 months for the patient group, and children without epilepsy but having minor ailments such as cough, cold, fever, etc. for the control group. Children in the age group of 5–12 years and those whose parents consented were included in the study. Children having epilepsy due to medical causes such as fever, metabolic changes, meningitis/encephalitis, cerebral palsy or those already diagnosed and/or under treatment for any psychiatric illness such as hyperactivity or behavioral disturbances, autism spectrum disorders, and intellectual disabilities were excluded from the study.
All parents were interviewed with a semi-structured proforma, which enquired about the socio-demographic details of the children, birth and developmental details, neurological details of epilepsy such as age of onset, its duration, type, frequency, etiology, medications, etc. Academic details of learning problems, grade retention, school attendance, irregularity, and dropouts were noted. All children were assessed clinically for the presence of behavioral problems, hyperactivity, and habit disorders as per the structured history-taking proforma, and the children were clinically diagnosed for psychopathology as per ICD-10 diagnostic guidelines and the following scales were applied.
Strength and Difficulties Questionnaire
Strength and Difficulties Questionnaire (SDQ) is a well-standardized behavioral screening questionnaire, designed to assess the behavior, emotions, and relationships in children aged 4–16 years. It is available in Indian languages and its parent’s version was administered. It yields scores on five domains, namely, emotional symptoms, conduct problems, inattention-hyperactivity, peer problems and prosocial behavior, and total impact and total difficulties score. A total difficulty score of 0–13 was normal, 14–16 was considered borderline, and 17–40 was taken as abnormal. The five impact scores were then summed to generate a total impact score ranging from 0 to 10. A score of 0 was taken as normal, 1 as borderline, and ≥2 as abnormal.[10],[11]
Parent Handling Questionnaire
Parent Handling Questionnaire (PHQ) is a 14-item questionnaire measuring two parental handling variables, viz., care consisting of 10 items (1–10) and control consisting of 4 items (11–14) with a 3-point Likert rating. Items are worded in a manner in which higher scores depict lower levels of care as well as control.[12]
| Results | | |
The mean age of the CWE was 9.69 ± 2.35 years, whereas the mean age of controls was 9.26 ± 2.35 years with age ranging from 5 to 12 years. There was no significant difference between ages of cases and controls as both were matched. In our study population, CWE included 37 (57%) males and 28 (43%) females, whereas controls had 47 (72%) males and 18 (28%) females. Majority were Hindus with 81.54% (n = 53) in CWE, and 93.85% (n = 61) of the control group staying in nuclear families. The mean duration of epilepsy was 4.52 years with a standard deviation of 1.55. Abnormal EEG was seen in only 50.77% of the cases and magnetic resonance imaging also showed no structural abnormality and was normal in majority of the cases. It showed abnormality in only 24.62% (n = 16) of the cases. Majority of CWE were controlled on one drug (86%), whereas only six patients were refractory and had uncontrolled seizures.
As per ICD-10 criteria, we found behavioral disorders in around 44.62% (n = 29) of the CWE when compared with 12.31% (n = 8) of the normal controls, which was extremely significant. Hyperkinetic disorders were reported as the most common disorder in pre-schoolers and school-aged CWE. Around 34% (n = 22) of the CWE had disturbance of activity and attention, and 3% (n = 2) fulfilled all the criteria of hyperkinetic disorders as well as conduct disorder in CWE when compared with 1.54% (n = 1) of the control group. Around 7.69% (n = 5) were diagnosed with unsocialized conduct disorder [Table 1].
When we compared both groups on various domains of SDQ with the domain total score, then a significant difference was seen on domains of hyperactivity and peer problems with CWE having a higher mean than normal controls. Prosocial behavior was extremely significant in the control group than CWE. On other domains such as emotional and conduct problems and total difficulty score, no significant differences were seen. Comparison of internalizing and externalizing problems in both the groups showed significant externalizing behaviors in CWE [Table 2].
Approximately 41% (n = 27) of CWE had scholastic backwardness when compared with 24% (16) of the controls, with only 4.61% (n = 3) of CWE reporting frequent failures. No group satisfied criteria for absenteeism, and there was more than 75% attendance in school.
When PHQ items were compared, on care items 2, 4, and 5 and on control items 11 and 12, a statistically significant difference was seen between the two groups. The total care score, total control score, and the total PHQ scores were highly significant with CWE having higher mean scores when compared with the controls [Table 3].
| Correlation of Behavioral Problems (SDQ) and Parental Handling Pattern (PHQ) | | |
When we studied for correlation between the behavioral problems as per SDQ and parental handling pattern as per PHQ, no statistically significant difference was seen on most of the domains, except for a negative association of conduct problems with low care. There was no association between the total SDQ score and the total PHQ score in our sample [Table 4].
| Discussion | | |
Nearly 45% of our sample of CWE had ICD-10 diagnosis of behavioral disorders. Similar findings have been found in several epidemiological studies with prevalence rates of psychopathology between 35% and 50% in CWE.[13] Studies have documented a lifelong psychiatric disorder diagnosis in 35% of the PWE[14] and between 20% and 50% in both adults and children.[15],[16],[17],[18] Austin et al.[19] reported that around 41.1% of CWE were at risk for both internalizing and externalizing behavioral problems.
Seizure variables related to behavioral problems include early age of onset, poor seizure control, long duration of epilepsy, high seizure frequency, and multiple seizure types. Poor child and family response to the condition, side effects of antiepileptic medications, and the underlying neurological dysfunction are also identified as causes for behavioral problems.
When CWE were assessed for the types of behavioral problems, we found a significant difference with CWE having more hyperkinetic disorders of activity and attention when compared with the controls. The symptoms most commonly reported among these children were frequently forgetting their things at school, breaking off from tasks, leaving activities unfinished, excessive restlessness, excessive talkativeness, frequent changes from one activity to another, and fidgeting. Thome-Souza et al.,[20] Dunn and Kronenberger,[21] and Besag et al.[22] found a prevalence of ADHD to be 30–40% in CWE, which is much higher than that in general population and goes with our findings. Jones et al.[23] reported that 26.4% of CWE without developmental and other neurological conditions had hyperactivity. Hermann and co-workers[24] reported that 31.5% of clinic-referred CWE had ADHD when compared with 6.4% in cousin controls of the CWE. In a population of children with “severe” epilepsy, Sherman et al.[25] reported a high prevalence with 70% of CWE meeting clinical cut-offs on the ADHD Rating Scale.
The possible causes of hyperkinetic disorders in CWE could be the underlying mechanism causing both conditions, co-occurrence of other psychiatric disorders, associated underlying brain dysfunction, frequent subclinical epileptiform discharges, postictal elevated mood, interictal manic psychosis, and adverse effects of antiepileptics.[13] Conduct disorder was less prevalent in both our groups contrary to those of other researchers.[26] The symptoms which were frequently reported by parents for conduct were lying, stealing, bullying, disobedience, and back answering. Cumulative effects of multiple risks (i.e., susceptibility genes for aggression and violence, heritable risk factors, parental psychopathology, low socio-economic status, adverse life events, poor parenting practices, history of abuse and neglect, poor executive cognitive functioning) can cause conduct problems in young children.
About 11% of the CWE (n = 7) fulfilled the criteria for ODD when compared with 6% (n = 4) of the controls. It was found that the symptoms of ODD were seen to exist as a comorbid condition in hyperkinetic disorders. Commonly reported symptoms in our patients were hostility, being defiant, negativistic, provocative, losing temper, and being disruptive. Prevalence of ODD between 10% and 17%[23] and 11%[12] in generalized seizures has been reported, which is in keeping with our findings. Behavioral problems could be due to the structural damage in the brain resulting in epilepsy, or sometimes the side effects of the antiepileptic medications or the environmental and genetic causes. Children may find it difficult to cope with the illness, and aggression could be a reaction to it.
We did not see significant differences in both the groups on all the domains of SDQ, as reported by some researchers.[27] CWE had significant hyperactivity and peer problems. In contrast, the controls had significant prosocial behaviors. Children who scored abnormally on emotional symptoms had headaches/stomach aches, were worrisome, often unhappy and disheartened, fearful, scared, and nervous in new situations. CWE were more short-tempered, disobedient, had lying, cheating, and stealing behaviors when compared with those without epilepsy. The emotional and conduct domains did not show any significant differences. Our findings were in keeping with Alfstad et al.,[28] who found significant difference on domains of hyperactivity, peer problems, and total impact score. We found significant externalizing behaviors on SDQ in CWE, which is similar to the findings of Mishra et al.[29]
Approximately 41% (n = 27) of CWE had been facing academic problems when compared with 16 (24.62%) children in the control group. Failures were comparatively less in our sample, and school absenteeism (child having less than 75% attendance at school) was not seen in both groups. Several researchers have reported an academic decline in CWE.[27],[30] More than 50% of the parents agreed that their child had to miss the school at some point of time because of epilepsy. The reasons given by parents were seizures just before or a day prior going to school, appointments with doctors, and going for various investigations. Studies have reported that 88% missed at least one school day due to various reasons attributable to epilepsy.[31] Modage et al.[27] in their study reported a significant irregular school attendance in epileptic children when compared with non-epileptics, and they also had a significant number of school drop-outs. We also had children who missed about 20–30 days in school in a year, but there was no long absenteeism more than 75% per semester. This does reflect that children were probably better controlled on medication.
Low care and control were the handling patterns of parents of CWE. They had higher means on care items no. 2, 4, and 5, which were statistically significant. Most of the parents of CWE agreed that they did not praise their child often or spend enough talk time with their child and often failed to make their child feel better when they are upset. On the contrary, parents of the control group were high on caring for their children, which also included being there for the child when their child needed help. They would also make the child feel happy whenever he/she was upset and would often fulfill their demands.
On control items 11 and 12, which were statistically significant, parents of CWE felt that their child could not take care of himself in their absence and that their spouse was more lenient/strict toward the child. They would often console or overprotect the child whenever he/she was reprimanded by the other parent. Some of them would get very angry on the child if he/she did not behave well. This depicts lower child–parent relationship quality, overparenting, and a rigid parental attitude toward the child. This further affects child’s adjustment with peers and environment, his/her behavior, and overall quality of life. Researchers have found that children who perceived their parents as overprotective or restrictive were more depressed and had more behavioral problems.[32] They became overdependent on their family, lacked confidence, were anxious, lacked social skills, and found it difficult to make friends.[33],[34],[35]
A correlation between behavioral problems and parental handling revealed a negative association with conduct problems and parents showing low care. Other behaviors like hyperactivity, emotional symptoms, peer problems, and prosocial behaviors were not associated with increased or decreased care or control in the parents. Studies have shown that scores in CWE depicted high care and high control which may be pathological and may contribute to cause of high externalizing behaviors such as conduct problems or delinquency in these children.[12]
| Conclusions | | |
Our study highlights the prevalence of behavioral disorders in CWE and the need to create awareness among physicians, pediatricians, and parents about the same. Early referral and treatment of the comorbid psychiatric disorders would improve the coping, school-related difficulties, overall quality of life of CWE, and also the parental handling behaviors.
Limitations and future directions
There were certain limitations such as selection bias in recruiting cases for the study group as only patients seeking medical help at a tertiary care center were included. We did not consider the confounding factors of type of epilepsy and behavioral side effects of antiepileptics. A larger sample size with longer follow-up period would offer a better picture of the longitudinal outcome of behavioral problems after epilepsy is well controlled. Liaison with the pediatric and neurology departments to create awareness about the psychopathology in children is also essential.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | Udani V. Pediatric epilepsy—An Indian perspective. Indian J Pediatr 2005;72:309-13.  |
| 2. | Kraemer HC, Stice E, Kazdin A, Offord D, Kupfer D. How do risk factors work together? Mediators, moderators, and independent, overlapping, and proxy risk factors. Am J Psychiatry 2001;158:848-56. |
| 3. | Høie B, Sommerfelt K, Waaler PE, Alsaker FD, Skeidsvoll H, Mykletun A. Psychosocial problems and seizure-related factors in children with epilepsy. Dev Med Child Neurol 2006;48:213-9. |
| 4. | Berg AT, Smith SN, Frobish D, Beckerman B, Levy SR, Testa FM, et al. Longitudinal assessment of adaptive behavior in infants and young children with newly diagnosed epilepsy: Influences of etiology, syndrome, and seizure control. Pediatrics 2004;114:645-50. |
| 5. | Besag FM. Behavioral aspects of pediatric epilepsy syndromes. Epilepsy Behav 2004;5(Suppl. 1):S3-13. |
| 6. | Gonzalez-Heydrich J, Dodds A, Whitney J, MacMillan C, Waber D, Faraone SV, et al. Psychiatric disorders and behavioral characteristics of pediatric patients with both epilepsy and attention-deficit hyperactivity disorder. Epilepsy Behav 2007;10:384-8. |
| 7. | Bazil CW. Epilepsy and sleep disturbance. Epilepsy Behav 2003;4(Suppl. 2):S39-45. |
| 8. | Davies S, Heyman I, Goodman R. A population survey of mental health problems in children with epilepsy. Dev Med Child Neurol 2003;45:292-5. |
| 9. | Austin JK, Caplan R. Behavioral and psychiatric comorbidities in pediatric epilepsy: Toward an integrative model. Epilepsia 2007;48:1639-51. |
| 10. | Goodman R. The strengths and difficulties questionnaire: A research note. J Child Psychol Psychiatry 1997;38:581-6. |
| 11. | Goodman R. Psychometric properties of the strengths and difficulties questionnaire. J Am Acad Child Adolesc Psychiatry 2001;40:1337-45. |
| 12. | Malhotra S. A parental handling questionnaire. Indian J Psychiatry 1990;32:265-72. [ PUBMED] [Full text] |
| 13. | Dunn DW, Besag F, Caplan R, Aldenkamp A, Gobbi G, Sillanpaa M. Psychiatric and behavioural disorders in children with epilepsy (ILAE Task Force Report): Epidemiology of psychiatric/behavioural disorder in children with epilepsy. Epileptic Disord 2016;18:S2-7. |
| 14. | Tellez-Zenteno JF, Patten SB, Jetté N, Williams J, Wiebe S. Psychiatric comorbidity in epilepsy: A population-based analysis. Epilepsia 2007;48:2336-44. |
| 15. | Bijl RV, Ravelli A, van Zessen G. Prevalence of psychiatric disorder in the general population: Results of the Netherlands Mental Health Survey and Incidence Study (Nemesis). Soc Psychiatry Psychiatr Epidemiol 1998;33:587-95. |
| 16. | Hackett R, Hackett L, Bhakta P. Psychiatric disorder and cognitive function in children with epilepsy in Kerala, South India. Seizure 1998;7:321-4. |
| 17. | Mensah SA, Beavis JM, Thapar AK, Kerr M. The presence and clinical implications of depression in a community population of adults with epilepsy. Epilepsy Behav 2006;8:213-9. |
| 18. | Datta SS, Premkumar TS, Chandy S, Kumar S, Kirubakaran C, Gnanamuthu C, et al. Behaviour problems in children and adolescents with seizure disorder: Associations and risk factors. Seizure 2005;14:190-7. |
| 19. | Austin JK, Perkins SM, Johnson CS, Fastenau PS, Byars AW, deGrauw TJ, et al. Behavior problems in children at time of first recognized seizure and changes over the following 3 years. Epilepsy Behav 2011;21:373-81. |
| 20. | Thome-Souza S, Kuczynski E, Assumpção F Jr, Rzezak P, Fuentes D, Fiore L, et al. Which factors may play a pivotal role on determining the type of psychiatric disorder in children and adolescents with epilepsy? Epilepsy Behav 2004;5:988-94. |
| 21. | Dunn DW, Kronenberger WG. Childhood epilepsy, attention problems, and ADHD: Review and practical considerations. Semin Pediatr Neurol 2005;12:222-8. |
| 22. | Besag F, Gobbi G, Caplan R, Sillanpaa M, Aldenkamp A, Dunn DW. Psychiatric and behavioural disorders in children with epilepsy (ILAE Task Force Report): Epilepsy and ADHD. Epileptic Disord 2016;18:S8-15. |
| 23. | Jones JE, Watson R, Sheth R, Caplan R, Koehn M, Seidenberg M, et al. Psychiatric comorbidity in children with new onset epilepsy. Dev Med Child Neurol 2007;49:493-7. |
| 24. | Lin JJ, Mula M, Hermann BP. Uncovering the neurobehavioural comorbidities of epilepsy over the lifespan. Lancet 2012;380:1180-92. |
| 25. | Sherman EM, Slick DJ, Connolly MB, Eyrl KL. ADHD, neurological correlates and health-related quality of life in severe pediatric epilepsy. Epilepsia 2007;48:1083-91. |
| 26. | McLellan A, Davies S, Heyman I, Harding B, Harkness W, Taylor D, et al. Psychopathology in children with epilepsy before and after temporal lobe resection. Dev Med Child Neurol 2005;47:666-72. |
| 27. | Modage A, Gajre MP, Setia M. Neurobehavioral comorbidities in children with epilepsy. J Neurol Neurophysiol 2016;7:371. |
| 28. | Alfstad KA, Clench-Aas J, Van Roy B, Mowinckel P, Gjerstad L, Lossius MI. Psychiatric symptoms in Norwegian children with epilepsy aged 8–13 years: Effects of age and gender? Epilepsia 2011;52:1231-8. |
| 29. | Mishra OP, Upadhyay A, Prasad R, Upadhyay SK, Piplani SK. Behavioral problems in Indian children with epilepsy. Indian Pediatr 2016;54:116-20. |
| 30. | Oostrom KJ, van Teeseling H, Smeets-Schouten A, Peters ACB, Jennekens-Schinkel A. Three to four years after diagnosis: Cognition and behavior in children with “epilepsy only.” A prospective, controlled study. Brain 2005;128:1546-55. |
| 31. | Aguiar BV, Guerreiro MM, McBrian D, Montenegro MA. Seizure impact on the school attendance in children with epilepsy. Seizure 2007;16:698-702. |
| 32. | Heaney DC, MacDonald BK, Everitt A, Stevenson S, Leonardi GS, Wilkinson P, et al. Socioeconomic variation in incidence of epilepsy: Prospective community based study in South East England. Br Med J 2002;325:1013-6. |
| 33. | Johnson EK, Jones JE, Seidenberg M, Hermann BP. The relative impact of anxiety, depression, and clinical seizure features on health-related quality of life in epilepsy. Epilepsia 2004;45:544-50. |
| 34. | Oguz A, Kurul S, Dirik E. Relationship of epilepsy-related factors to anxiety and depression scores in epileptic children. J Child Neurol 2002;17:37-40. |
| 35. | Boylan LS, Flint LA, Labovitz DL, Jackson SC, Starner K, Devinsky O. Depression but not seizure frequency predicts quality of life in treatment-resistant epilepsy. Neurology 2004;62:258-61. |
[Table 1], [Table 2], [Table 3], [Table 4]
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