- Email: [email protected]
Attention problems in children with epilepsy. How is the long-term outcome?
e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 9 ( 2 0 1 5 ) 3 8 3 e3 8 5
Official Journal of the European Paediatric Neurology Society
Letter to the Editor
Attention problems in children with epilepsy. How is the long-term outcome? abstract Introduction: Attention deficit/hyperactivity disorder (ADHD) is one of the most common childhood disorders and frequently seen in other conditions like epilepsy as well. The prevalence of ADHD in the general paediatric population is estimated at 3e6% persisting into adulthood in up to one third of persons affected. The prevalence of ADHD in epilepsy is understood to be significantly higher. Approximately one third of children with epilepsy do also have a diagnosis of ADHD. How these attention problems develop over the years is however not clear. We therefore evaluated the severity of attention problems in children with epilepsy at late childhood and assessed it again in adolescence. Data was being compared with attention problems of children with developmental ADHD.
Method: 16 boys with diagnosed combined idiopathic epilepsy/ADHD and 14 boys with developmental ADHD were investigated twice; at a mean age of 10.94 (SD ¼ 1.63) and then again at a mean age of 15.82 (SD ¼ 2.0). At the baseline examination all patients completed Raven's Progressive Matrices to assess intelligence. To measure symptom severity of ADHD, parents were asked to complete the short version of the Conner's Rating Scale for Parents at both times. Parents of children with combined epilepsy/ADHD furthermore gave information about seizure frequency and intake of anticonvulsants.
Results: Patient groups did not significantly differ in age and IQ. Results of the baseline examination revealed elevated scores in both patient groups for the Conner's Rating Scales; ADHD group: M ¼ 16.86 (SD ¼ 5.35); Epilepsy/ADHD group: M ¼ 14.77 (SD ¼ 4.76) but no differences between the groups (p ¼ .29; z ¼ .39). Qualitatively, patients with developmental ADHD showed more abnormalities in the area of hyperactivity/impulsivity while patients with epilepsy/ADHD had more problems with inattention. Results of the follow-up examination showed a significant reduction of symptoms in the ADHD group of minus 4.23 points; M ¼ 12.63 (SD ¼ 3.89) (p ¼ .02); The reduction in the epilepsy/ADHD group was even bigger with minus 6.77 points; M ¼ 8.00 (SD ¼ 6.46) (p ¼ .03). However, difference between the two groups reached no significance (p ¼ .079; z ¼ 1.19). None of the patients with epilepsy has had seizures in the meantime.
Conclusion: We found a significant reduction of ADHD symptoms in our patients from the time of late childhood to adolescence. That symptoms of ADHD, especially hyperactivity, lessen with age is known from the literature (Biedermann et al., 2010). We found the same data for patients with idiopathic epilepsy and ADHD. Over the same period of time problems of attention improved substantially. We conclude that development and brain maturation may have a similar positive effect on attention problems in children with epilepsy than in developmental ADHD. © 2015 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved.
Sir, With interest we have read the article from Jonsson et al. (2014)1 assessing psychological and social outcome of children
with well-functioning epilepsy. There, children were selected from a large population based study of epilepsy in Sweden2 as a 10-year follow-up. Using a questionnaire, results revealed that the majority of that sample was comparable to the
384
e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 9 ( 2 0 1 5 ) 3 8 3 e3 8 5
normal population in early adulthood. However, some of the individuals still showed behavioral, emotional and school problems, amongst others as a result of attention problems. In Jonsson et al. ‘s study1 attention problems were related to active epilepsy and anticonvulsive polytherapy. That attention problems are very frequent in children with epilepsy and even leading to a diagnosis of attention deficit/hyperactivity disorder (ADHD), has been reported since the 1950s.3 The prevalence of ADHD in the general pediatric population is estimated at 3e6% persisting into adulthood in up to one third of persons affected. The prevalence of ADHD in epilepsy is understood to be significantly higher. Approximately one third of children with epilepsy do also have a diagnosis of ADHD.4,5 A number of studies in different populations have indicated a potential bidirectional relationship between epilepsy and ADHD.6 How these attention problems develop over the years is however not clear. We therefore evaluated the severity of attention problems in children with epilepsy at late childhood and assessed it again in adolescence. Data was being compared with attention problems of children with developmental ADHD. In line with the study of Jonsson et al. (2014)1 we focused on children with well-functioning epilepsy. These are patients who have a normal IQ and no other neurological impairment. Our sample consisted of 16 boys with diagnosed combined well-functioning epilepsy/ADHD and 14 boys with developmental ADHD. Children were assessed twice; at a mean age of 10.94 (SD ¼ 1.63) and then again at a mean age of 15.82 (SD ¼ 2.00). Initial inclusion criteria for boys with epilepsy were: diagnosis of epilepsy based on a history of two unprovoked seizures, idiopathic or cryptogenic cause, EEG -features of hypersynchronous activity and no identifiable lesions on MRI. Further, patients had to be seizure free for at least six month and fulfil the diagnosis of ADHD/ADD according to DSM-IV criteria.7 Mean age at diagnosis of epilepsy was 7.40 (SD ¼ 2.44) years and mean duration 4.00 (SD ¼ 2.48) years. Additional patient characteristics are shown in Table 1. Patients with ADHD were included according to the same diagnostic criteria of ADHD/ADD. We included five patients with
ADD and nine with ADHD. Exclusion criteria for both patient groups were other developmental disorder, other neurological disorder, abnormal intelligence, genetic disorder and abnormal MRI. This collective was part of a study we published elsewhere.9 At the baseline examination all patients completed the Raven's Progressive Matrices to assess intelligence.10 To measure symptom severity of ADHD, parents were asked to complete the short version of the Conner's Rating Scale for Parents8 at both times. Parents of children with combined epilepsy/ADHD furthermore gave information about seizure frequency and intake of anticonvulsants. Intelligence measured with the Raven's Progressive matrices yielded the following mean percent ranks: 33.92 (SD ¼ 23.48) for the epilepsy/ADHD group and 46.23 (SD ¼ 37.04) for the ADHD only group. Differences between the groups reached no significance (p ¼ .32). At the baseline examination both patient groups revealed elevated scores in the Conner's Rating Scales; Epilepsy/ADHD group: M ¼ 14.77 (SD ¼ 4.76); ADHD only group: M ¼ 16.86 (SD ¼ 5.35) but no differences between the groups (p ¼ .29; z ¼ .39). Qualitatively, patients with epilepsy/ADHD had more problems with inattention while patients with developmental ADHD showed more abnormalities in the area of hyperactivity/impulsivity. Results of the follow-up examination showed a significant reduction of symptoms in the ADHD group of minus 4.23 points; M ¼ 12.63 (SD ¼ 3.89) (p ¼ .02); The reduction in the epilepsy/ADHD group was even bigger with minus 6.77 points; M ¼ 8.00 (SD ¼ 6.46) (p ¼ .03). However, difference between the two groups reached no significance (p ¼ .079; z ¼ 1.19). None of the patients with epilepsy has had seizures in the meantime. We found a significant reduction of ADHD symptoms in our patients from the time of late childhood to adolescence. That symptoms of ADHD e especially hyperactivity - lessen with age is known from the literature.11 We found the same data also for patients with well-functioning epilepsy and ADHD. Over the same period of time problems of attention and hyperactivity improved substantially. We conclude that development and brain maturation may have a similar
Table 1 e Characteristics of patients with combined epilepsy/ADHD at baseline examination. ID
Age
Duration of epilepsy
Diagnosis
Medication
Type of AD
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
12 9 14 11 11 12 9 11 12 11 12 14 13 8 9 13
8 years 3 years 7 years 1 year 1 year 4 years 3 years 6 years 7 years 6 years 1 year 5 years 2 years missing 2 years 8 years
Focal frontal lobe epilepsy Focal parietal lobe epilepsy Focal temporal lobe epilepsy Absence epilepsy Rolandic epilepsy Rolandic epilepsy Focal generalized epilepsy Rolandic epilepsy Complex partial epilepsy; localization undefined Focal frontal lobe epilepsy Absence epilepsy Photosensitive epilepsy Complex focal epilepsy Complex focal epilepsy Focal generalized epilepsy (frontal origin) Generalized epilepsy
Valproat Valproat Carbamazepin Valproat Sulthiam Sulthiam Carbamazepin Sulthiam Clobazam Valproat No medication No medication Carbamazepin Valproat Valproat Valproat
ADD ADHD ADD ADHD ADD ADHD ADD ADD ADHD ADD ADD ADHD ADD ADD ADHD ADD
Note. AD ¼ attention deficit; ADD ¼ attention deficit disorder; ADHD ¼ attention deficit/hyperactivity disorder.
e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 9 ( 2 0 1 5 ) 3 8 3 e3 8 5
positive effect on ADHD symptoms in children with epilepsy than in developmental ADHD. In a recent and important work of Salpekar and Mishra (2014)12 the authors made suggestions how symptoms of ADHD can be distinguished from symptoms of seizures underlining the fact that attention problems in epilepsy are not only a side-effect of anticonvulsive polytherapy or active epilepsy. The authors also encourage clinicians to give medical treatment when necessary. Due to the fact that both illnesses do have a negative impact on different areas of live like academic outcome, social life or development, it is crucial to broaden the knowledge about those disorders co-occurring to enable an optimal treatment. Yours faithfully. Nina Bechtel & Peter Weber.
Conflict of interest None of the authors has any conflicts of interest to disclose.
references
1. Jonsson P, Jonsson B, Eeg-Olofsson O. Psychological and social outcome of epilepsy in well-functioning children and adolescents. A 10-year follow-up study. Eur J Paediatr Neurol 2014;18:381e90. 2. Larsson K, Eeg-Olofsson O. A population based study of epilepsy in children from a Swedish country. Eur J Paediatr Neurol 2006;10:107e13. 3. Ounsted C. The hyperkinetic syndrome in epileptic children. Lancet 1955;269:303e11. 4. Hermann B, Jones J, Dabbs K, Allen CA, Sheth R, Fine J, McMillan A, Seidenberg M. The frequency, complications and aetiology of ADHD in new onset paediatric epilepsy. Brain 2007; 130:3135e48.
385
5. Dunn DW, Austin JK, Harezlak J, Ambrosius WT. ADHD and epilepsy in childhood. Dev Med Child Neurol 2003;45:50e4. 6. Socanski D, Aurlien D, Herigstad A, Thomsen PH, Larsen TK. Epilepsy in a large cohort of children diagnosed with attention deficit/hyperactivity disorders (ADHD). Seizure 2013;22:651e5. 7. American Psychiatric Association. DSM-IV: diagnostic and statistical manual of mental disorders. Washington (DC): American Psychiatric Association; 2000. 8. Conners CK. Conners' rating scales e revised. Technical manual. New York: MHS; 2001. € fer M, 9. Bechtel N, Kobel M, Penner IK, Specht K, Klarho Scheffler K, Opwis K, Schmitt-Mechelke T, Capone A, Weber P. Attention deficit/hyperactivity disorder in childhood epilepsy: a neuropsychological and fMRI study. Epilepsia 2012;53:325e33. 10. Raven JC, Raven J, Court JH. CPM Manual: Raven's progressive matrices and vocabulary scales (German version and norms). Frankfurt: Swets & Zeitlinger; 2002. 11. Biederman J, Petty CR, Clarke A, Lomedico A, Faraone SV. Predictors of persistent ADHD: an 11-year follow-up study. J Psych Res 2011;45:150e5. 12. Salpekar JA, Mishra G. Key issues in addressing the comorbidity of attention deficit hyperactivity disorder and pediatric epilepsy. Epilepsy Behav 2014;37:310e5.
Nina Bechtel* Peter Weber Department of Neuropediatrics and Developmental Medicine, University Children's Hospital Basel (UKBB), PB CH-4031 Basel, Switzerland *Corresponding author. Tel.: þ41 61 704 12 12; fax: þ41 61 704 12 13. E-mail address: [email protected] (N. Bechtel) 1090-3798/ © 2015 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejpn.2014.12.020
Official Journal of the European Paediatric Neurology Society
Letter to the Editor
Attention problems in children with epilepsy. How is the long-term outcome? abstract Introduction: Attention deficit/hyperactivity disorder (ADHD) is one of the most common childhood disorders and frequently seen in other conditions like epilepsy as well. The prevalence of ADHD in the general paediatric population is estimated at 3e6% persisting into adulthood in up to one third of persons affected. The prevalence of ADHD in epilepsy is understood to be significantly higher. Approximately one third of children with epilepsy do also have a diagnosis of ADHD. How these attention problems develop over the years is however not clear. We therefore evaluated the severity of attention problems in children with epilepsy at late childhood and assessed it again in adolescence. Data was being compared with attention problems of children with developmental ADHD.
Method: 16 boys with diagnosed combined idiopathic epilepsy/ADHD and 14 boys with developmental ADHD were investigated twice; at a mean age of 10.94 (SD ¼ 1.63) and then again at a mean age of 15.82 (SD ¼ 2.0). At the baseline examination all patients completed Raven's Progressive Matrices to assess intelligence. To measure symptom severity of ADHD, parents were asked to complete the short version of the Conner's Rating Scale for Parents at both times. Parents of children with combined epilepsy/ADHD furthermore gave information about seizure frequency and intake of anticonvulsants.
Results: Patient groups did not significantly differ in age and IQ. Results of the baseline examination revealed elevated scores in both patient groups for the Conner's Rating Scales; ADHD group: M ¼ 16.86 (SD ¼ 5.35); Epilepsy/ADHD group: M ¼ 14.77 (SD ¼ 4.76) but no differences between the groups (p ¼ .29; z ¼ .39). Qualitatively, patients with developmental ADHD showed more abnormalities in the area of hyperactivity/impulsivity while patients with epilepsy/ADHD had more problems with inattention. Results of the follow-up examination showed a significant reduction of symptoms in the ADHD group of minus 4.23 points; M ¼ 12.63 (SD ¼ 3.89) (p ¼ .02); The reduction in the epilepsy/ADHD group was even bigger with minus 6.77 points; M ¼ 8.00 (SD ¼ 6.46) (p ¼ .03). However, difference between the two groups reached no significance (p ¼ .079; z ¼ 1.19). None of the patients with epilepsy has had seizures in the meantime.
Conclusion: We found a significant reduction of ADHD symptoms in our patients from the time of late childhood to adolescence. That symptoms of ADHD, especially hyperactivity, lessen with age is known from the literature (Biedermann et al., 2010). We found the same data for patients with idiopathic epilepsy and ADHD. Over the same period of time problems of attention improved substantially. We conclude that development and brain maturation may have a similar positive effect on attention problems in children with epilepsy than in developmental ADHD. © 2015 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved.
Sir, With interest we have read the article from Jonsson et al. (2014)1 assessing psychological and social outcome of children
with well-functioning epilepsy. There, children were selected from a large population based study of epilepsy in Sweden2 as a 10-year follow-up. Using a questionnaire, results revealed that the majority of that sample was comparable to the
384
e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 9 ( 2 0 1 5 ) 3 8 3 e3 8 5
normal population in early adulthood. However, some of the individuals still showed behavioral, emotional and school problems, amongst others as a result of attention problems. In Jonsson et al. ‘s study1 attention problems were related to active epilepsy and anticonvulsive polytherapy. That attention problems are very frequent in children with epilepsy and even leading to a diagnosis of attention deficit/hyperactivity disorder (ADHD), has been reported since the 1950s.3 The prevalence of ADHD in the general pediatric population is estimated at 3e6% persisting into adulthood in up to one third of persons affected. The prevalence of ADHD in epilepsy is understood to be significantly higher. Approximately one third of children with epilepsy do also have a diagnosis of ADHD.4,5 A number of studies in different populations have indicated a potential bidirectional relationship between epilepsy and ADHD.6 How these attention problems develop over the years is however not clear. We therefore evaluated the severity of attention problems in children with epilepsy at late childhood and assessed it again in adolescence. Data was being compared with attention problems of children with developmental ADHD. In line with the study of Jonsson et al. (2014)1 we focused on children with well-functioning epilepsy. These are patients who have a normal IQ and no other neurological impairment. Our sample consisted of 16 boys with diagnosed combined well-functioning epilepsy/ADHD and 14 boys with developmental ADHD. Children were assessed twice; at a mean age of 10.94 (SD ¼ 1.63) and then again at a mean age of 15.82 (SD ¼ 2.00). Initial inclusion criteria for boys with epilepsy were: diagnosis of epilepsy based on a history of two unprovoked seizures, idiopathic or cryptogenic cause, EEG -features of hypersynchronous activity and no identifiable lesions on MRI. Further, patients had to be seizure free for at least six month and fulfil the diagnosis of ADHD/ADD according to DSM-IV criteria.7 Mean age at diagnosis of epilepsy was 7.40 (SD ¼ 2.44) years and mean duration 4.00 (SD ¼ 2.48) years. Additional patient characteristics are shown in Table 1. Patients with ADHD were included according to the same diagnostic criteria of ADHD/ADD. We included five patients with
ADD and nine with ADHD. Exclusion criteria for both patient groups were other developmental disorder, other neurological disorder, abnormal intelligence, genetic disorder and abnormal MRI. This collective was part of a study we published elsewhere.9 At the baseline examination all patients completed the Raven's Progressive Matrices to assess intelligence.10 To measure symptom severity of ADHD, parents were asked to complete the short version of the Conner's Rating Scale for Parents8 at both times. Parents of children with combined epilepsy/ADHD furthermore gave information about seizure frequency and intake of anticonvulsants. Intelligence measured with the Raven's Progressive matrices yielded the following mean percent ranks: 33.92 (SD ¼ 23.48) for the epilepsy/ADHD group and 46.23 (SD ¼ 37.04) for the ADHD only group. Differences between the groups reached no significance (p ¼ .32). At the baseline examination both patient groups revealed elevated scores in the Conner's Rating Scales; Epilepsy/ADHD group: M ¼ 14.77 (SD ¼ 4.76); ADHD only group: M ¼ 16.86 (SD ¼ 5.35) but no differences between the groups (p ¼ .29; z ¼ .39). Qualitatively, patients with epilepsy/ADHD had more problems with inattention while patients with developmental ADHD showed more abnormalities in the area of hyperactivity/impulsivity. Results of the follow-up examination showed a significant reduction of symptoms in the ADHD group of minus 4.23 points; M ¼ 12.63 (SD ¼ 3.89) (p ¼ .02); The reduction in the epilepsy/ADHD group was even bigger with minus 6.77 points; M ¼ 8.00 (SD ¼ 6.46) (p ¼ .03). However, difference between the two groups reached no significance (p ¼ .079; z ¼ 1.19). None of the patients with epilepsy has had seizures in the meantime. We found a significant reduction of ADHD symptoms in our patients from the time of late childhood to adolescence. That symptoms of ADHD e especially hyperactivity - lessen with age is known from the literature.11 We found the same data also for patients with well-functioning epilepsy and ADHD. Over the same period of time problems of attention and hyperactivity improved substantially. We conclude that development and brain maturation may have a similar
Table 1 e Characteristics of patients with combined epilepsy/ADHD at baseline examination. ID
Age
Duration of epilepsy
Diagnosis
Medication
Type of AD
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
12 9 14 11 11 12 9 11 12 11 12 14 13 8 9 13
8 years 3 years 7 years 1 year 1 year 4 years 3 years 6 years 7 years 6 years 1 year 5 years 2 years missing 2 years 8 years
Focal frontal lobe epilepsy Focal parietal lobe epilepsy Focal temporal lobe epilepsy Absence epilepsy Rolandic epilepsy Rolandic epilepsy Focal generalized epilepsy Rolandic epilepsy Complex partial epilepsy; localization undefined Focal frontal lobe epilepsy Absence epilepsy Photosensitive epilepsy Complex focal epilepsy Complex focal epilepsy Focal generalized epilepsy (frontal origin) Generalized epilepsy
Valproat Valproat Carbamazepin Valproat Sulthiam Sulthiam Carbamazepin Sulthiam Clobazam Valproat No medication No medication Carbamazepin Valproat Valproat Valproat
ADD ADHD ADD ADHD ADD ADHD ADD ADD ADHD ADD ADD ADHD ADD ADD ADHD ADD
Note. AD ¼ attention deficit; ADD ¼ attention deficit disorder; ADHD ¼ attention deficit/hyperactivity disorder.
e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 9 ( 2 0 1 5 ) 3 8 3 e3 8 5
positive effect on ADHD symptoms in children with epilepsy than in developmental ADHD. In a recent and important work of Salpekar and Mishra (2014)12 the authors made suggestions how symptoms of ADHD can be distinguished from symptoms of seizures underlining the fact that attention problems in epilepsy are not only a side-effect of anticonvulsive polytherapy or active epilepsy. The authors also encourage clinicians to give medical treatment when necessary. Due to the fact that both illnesses do have a negative impact on different areas of live like academic outcome, social life or development, it is crucial to broaden the knowledge about those disorders co-occurring to enable an optimal treatment. Yours faithfully. Nina Bechtel & Peter Weber.
Conflict of interest None of the authors has any conflicts of interest to disclose.
references
1. Jonsson P, Jonsson B, Eeg-Olofsson O. Psychological and social outcome of epilepsy in well-functioning children and adolescents. A 10-year follow-up study. Eur J Paediatr Neurol 2014;18:381e90. 2. Larsson K, Eeg-Olofsson O. A population based study of epilepsy in children from a Swedish country. Eur J Paediatr Neurol 2006;10:107e13. 3. Ounsted C. The hyperkinetic syndrome in epileptic children. Lancet 1955;269:303e11. 4. Hermann B, Jones J, Dabbs K, Allen CA, Sheth R, Fine J, McMillan A, Seidenberg M. The frequency, complications and aetiology of ADHD in new onset paediatric epilepsy. Brain 2007; 130:3135e48.
385
5. Dunn DW, Austin JK, Harezlak J, Ambrosius WT. ADHD and epilepsy in childhood. Dev Med Child Neurol 2003;45:50e4. 6. Socanski D, Aurlien D, Herigstad A, Thomsen PH, Larsen TK. Epilepsy in a large cohort of children diagnosed with attention deficit/hyperactivity disorders (ADHD). Seizure 2013;22:651e5. 7. American Psychiatric Association. DSM-IV: diagnostic and statistical manual of mental disorders. Washington (DC): American Psychiatric Association; 2000. 8. Conners CK. Conners' rating scales e revised. Technical manual. New York: MHS; 2001. € fer M, 9. Bechtel N, Kobel M, Penner IK, Specht K, Klarho Scheffler K, Opwis K, Schmitt-Mechelke T, Capone A, Weber P. Attention deficit/hyperactivity disorder in childhood epilepsy: a neuropsychological and fMRI study. Epilepsia 2012;53:325e33. 10. Raven JC, Raven J, Court JH. CPM Manual: Raven's progressive matrices and vocabulary scales (German version and norms). Frankfurt: Swets & Zeitlinger; 2002. 11. Biederman J, Petty CR, Clarke A, Lomedico A, Faraone SV. Predictors of persistent ADHD: an 11-year follow-up study. J Psych Res 2011;45:150e5. 12. Salpekar JA, Mishra G. Key issues in addressing the comorbidity of attention deficit hyperactivity disorder and pediatric epilepsy. Epilepsy Behav 2014;37:310e5.
Nina Bechtel* Peter Weber Department of Neuropediatrics and Developmental Medicine, University Children's Hospital Basel (UKBB), PB CH-4031 Basel, Switzerland *Corresponding author. Tel.: þ41 61 704 12 12; fax: þ41 61 704 12 13. E-mail address: [email protected] (N. Bechtel) 1090-3798/ © 2015 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejpn.2014.12.020