Epilepsy & Behavior 19 (2010) 483–486

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Epilepsy & Behavior

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Epileptiform abnormalities in children diagnosed with attentiondeficit/hyperactivity disorder

Dobrinko Socanski a,⁎, Anita Herigstad b, Per Hove Thomsen c, Aarsland Dag d, Tor Ketil Larsen d

a Department of Child and Adolescent Psychiatry, Division of Psychiatry, Stavanger University Hospital, Stavanger, Norwayb Department of Clinical Neurophysiology, Stavanger University Hospital, Stavanger, Norwayc Centre for Child and Adolescent Psychiatry, University of Aarhus, Denmarkd Division of Psychiatry, Stavanger University Hospital, Stavanger, Norway

⁎ Corresponding author. Division of Psychiatry, Stav1163 Hillevåg, 4095 Stavanger, Norway. Fax: +47 5151

E-mail addresses: dso@sus.no, socanski@hotmail.com

1525-5050/$ – see front matter © 2010 Elsevier Inc. Aldoi:10.1016/j.yebeh.2010.08.005

a b s t r a c t

a r t i c l e i n f o

Article history:Received 24 June 2010Revised 30 July 2010Accepted 4 August 2010

Keywords:Attention-deficit/hyperactivity disorderElectroencephalographyEpileptiform abnormalitiesRolandic spikesEpileptic seizuresChildren

The frequency of epileptiform abnormalities (EAs) and correlates of EAs in children with attention deficit/hyperactivity disorder (ADHD) was investigated in a retrospective study. The total sample consisted of 607children with ADHD from the only center diagnosing and treating ADHD in the region. EEGs were obtained in517 cases, and EAs were found in 39 (7.5%) children. Of these, 21(53.9%) showed generalized EAs, 16 (41%)had focal EAs, and 2 (5.1%) had both. Rolandic spikes were observed in 9 cases (1.7% of the total group). Aprevious history of epileptic seizures was reported in 14 (2.5%) children, and was more common in thosewith EAs than in those without. The group with ADHD and EAs had a larger proportion of girls and the ADHDinattentive subtype, independent of a history of epilepsy. Future research should focus on the clinicalconsequences of EAs in children with ADHD.

anger University Hospital, PB5549.(D. Socanski).

l rights reserved.

© 2010 Elsevier Inc. All rights reserved.

1. Introduction

Attention deficit/hyperactivity disorder (ADHD) occurs in 3–7% ofall children [1] and is one of the most common neurobehavioraldisorders. ADHD occurs approximately three times as often in boys asin girls in community samples, and five to nine times more often inclinical samples [2]. According to the American Psychiatric Associa-tion's Diagnostic and Statistical Manual of Mental Disorders, FourthEdition, Revised (DSM-IV-TR) [2], ADHD is divided into three types:predominantly hyperactivity and impulsivity, predominantly atten-tion difficulties (ADHD-I), and the combined type (ADHD-C), themostfrequent type.

There are several interrelationships between ADHD and epilepti-form activity. First, although there are relatively few studies ofunselected populations, there is some evidence that children withADHD have a higher rate of interictal epileptiform abnormalities (EAs)on EEGs compared with those without ADHD according to severalstudies [3–7]. Hemmer et al. [5] reported the highest prevalence(15.4%) of EAs on awake routine EEGs in 234 children with ADHD forwhom treatment with stimulant medications was planned. This studyshowed an association between EAs and considerable risk of eventual

epileptic seizures later in the clinical course. In another study, Richeret al. [6] examined 347 children with ADHDwith one routine EEG andfound EAs in 6.1%. They found no clear association between EAs andthe development of epileptic seizures.

Holtman et al. [7] found rolandic spikes in 5.6% of children withADHD without epilepsy, which is higher than reported in normalchildren [8]. They also found that childrenwith rolandic spikes tendedto exhibit more hyperactive–impulsive symptoms. Holtman et al. [9]replicated this finding in another study, and extended these findingsby reporting that children with ADHD with rolandic spikes manifestreduced response inhibition.

Second, children with epilepsy have a higher risk of having ADHDcomparedwith the general pediatric population [10]. In a study of 175children with epilepsy without significant developmental delays whohad at least a 6-month history of epilepsy, Dunn et al. [11] found thatchildrenwith epilepsywere at higher risk for symptoms of ADHD thanthe general population. They differed from other samples of childrenwith ADHD by having a larger proportion of children with ADHD ofpredominantly the inattentive type and by an equal incidence inmales and females.

Attention deficit/hyperactivity disorder as a risk factor for incidentunprovoked seizures and epilepsy in children was described byHersdorffer et al. [12]. They conducted a population-based case–control study of newly diagnosed unprovoked seizures amongIcelandic children younger than 16. The association was restrictedto ADHD of predominantly the inattentive type.

484 D. Socanski et al. / Epilepsy & Behavior 19 (2010) 483–486

The aim of this studywas to investigate the frequency and correlatesof EAs in a large and unselected cohort of children with ADHD.

2. Methods

2.1. Design

This studywas a retrospective chart review of childrenwith ADHD.

2.2. Material

The medical records of children aged 5–14 consecutively diag-nosed with ADHD at the Department of Child and AdolescentPsychiatry, Stavanger University Hospital, Stavanger, Norway, be-tween January 2000 and December 2005 were studied. Thisdepartment is the only child and adolescent psychiatry departmentin the area and serves a population of 240,000 inhabitants. All patientswith suspected ADHD are referred to this department.

2.3. Assessment

A structured clinical interview was used to elicit general andclinical information including seizure characteristics and drugtreatment, and a clinical neurological and child psychiatry examina-tion was conducted following a structured guide. In addition,standardized psychiatric instruments including the Child BehaviorChecklist [13], Conners’ Parent/Teacher Rating Scale [14], and theADHD Rating Scale IV [15] were administered. On the basis of theclinical interview and the diagnostic procedures, a diagnosis of ADHDand subtypes and other psychiatric diagnoses were made according toDSM-IV-TR criteria [2]. Patients with IQs b50 and those meetingcriteria for pervasive developmental disorder were excluded from thepresent study.

As part of the routine assessment program, children with ADHDwere referred for digitized routine EEGs, recorded for 20 minutes,including hyperventilation and photic stimulation with 21 electrodes(10–20 system) during wakefulness without sleep deprivation. TheEEGs were classified as either epileptiform or nonepileptiform by threeboard-licensed clinical neurophysiologists. This group was supervisedby the second author (A.H.), who also carried out a majority of theclassifications, and the first author (D.S), who is an experienced childpsychiatrist with special training in electroencephalography. Thepatients with EAs were subdivided into those with focal EAs and thosewith nonfocal EAs, and within the focal EA group, those with “rolandic”spikes were tabulated separately. Based on the clinical interview,children were classified as having experienced epileptic seizures or not.

Table 1Age at admission, sex distribution, ADHD subtype, and occurrence of epileptic seizures (N=

ADHD/EEG/no EAs(n=478)

ADHD/EEG/EAs (n

All with EAs(n=39)

Age, mean±SD 9.3±2.4 9.7±2.7Gender, female 81 (16.9%) 11 (28.1%)ADHD inattentive subtype 50 (10.5%) 16 (41%)Previous epileptic seizures 2/479 (0.4%) 12/39 (30.8%)EEG findings

Focal EAs 16 (41%)Rolandic spikes 9

Generalized EAs 21 (53.9%)Mixed EAs 2 (5.1%)

a All significant differences are between the group without EAs and the group with EAs.

2.4. Statistical analysis

Statistical analysis using SPSS Version 15 was performed tocompare demographic and clinical variables in subjects with andwithout epileptic activity using Student's t test for continuous andnormally distributed data and nonparametric tests for categorical ornon-normally distributed data. Ninety-five percent confidence inter-vals were calculated (Vassar statistics online). A P value b0.05 wasconsidered statistically significant.

The study was approved by the Norwegian Data Inspectorate andby the Regional Committee on Medical Research Ethics in Bergen.

3. Results

We identified a total of 607 children diagnosed with ADHD. EEGswere obtained in 517 cases, which constituted the study group. Ofthese, 479 patients were being diagnosed for the first time withADHD, and 38 came for reassessment. The patients without EEGs didnot differ from the participants with respect to age (9.5±2.6 years vs9.4+2.5 years), gender (83.3% male vs 82.2%male), or ADHD subtype(92.2 and 87.2% had the combined subtype, respectively).

Epileptiform abnormalities were observed in 39 (7.5%) children,although in 2 of these cases, EAs were demonstrated only withactivation procedures (one patient demonstrated EAs on hyperven-tilation, and another, on photic stimulation). The characteristics ofchildren with EAs and those without EAs are summarized in Table 1.The groups did not differ in age, but there were a greater proportion ofgirls in the group with EAs. The distribution of ADHD subtype(combined or inattentive) differed between the two groups, withADHD inattentive subtype being more common in children with EAsthan in those without EAs.

A previous history of epileptic seizures was reported in 14 (2.5%)children, and was more common in those with EAs (30.8%) than inthose without EAs (0.4%) (Pb0.000). If we eliminated patients with aprevious history of epileptic seizures (14 patients: 12 of them withEAs and 2 without EAs at ADHD assessment), the incidence of EAs inchildren with ADHD was 5.4%.

Among the 39 children with EAs, 21 (53.9%) had generalized EAs,16 (41%) had focal EAs, and 2 (5.1%) had mixed EAs. Rolandic spikeswere observed in 9 cases (1.7% of the total group).

4. Discussion

The main finding of this study was that 7.5% of the unselectedsample of children with ADHD had EAs. The children with ADHD andEAs were more often female, more often manifested the ADHD-Isubtype, and had a larger proportion with epileptic seizures than thechildren with ADHD without EAs. When we exclude patients withprevious epilepsy, the rate of EAs was 5.4%.

517).

=39) P value

ADHD/EAs(n=27)

ADHD/EAs/epileptic seizures(n=12)

10.3±2.7 8.5±2.38 (29.6%) 3 (25%) b0.001a

12 (44.4%) 4 (33.3%) b0.0001a

0 12 b0.0001a

12 47 2

14 71 1

Table 2EAs in healthy children and in children with ADHD without epilepsy.

Study Country Group Age N Number (%) of EAs

Eeg-Olofsson et al. [8] Sweden Healthy 1–15 743 18 (2.4)Cavazzuti et al. [16] Italy Healthy 6–13 3724 133 (3.5)Okubo et al. [17] Japan Healthy 6–12 1057 53 (5)Our study Norway ADHD 6–14 503 27 (5.4)Richer et al. [6] Canada ADHD 5–16 347 21 (6.1)Hemmer et al. [5] USA ADHD 3–20 234 36 (15.4)Matoth et al. [18] Israel ADHD 5–16 126 6 (4.8)

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4.1. Comparison with other studies (EAs in healthy children and inchildren with ADHD)

Previous studies reporting the frequency of EAs in healthy childrenand children with ADHD are listed in Table 2. In healthy children fromdifferent geographic regions, the proportions of children with EAsvaried from 2.4 to 5.0% [8,13,14]. The study that we regard as beingepidemiologically most similar to ours, from Sweden, reported asignificantly lower rate of EAs (2.4%); however, they included childrenyounger than 6 years and had strict selection criteria. The study fromItaly reported lower rates; however, this study did not state if photicstimulation was used as an activation procedure. The study fromJapan reported rates similar to ours. It is still unclear whether childrenwith ADHD havemore EAs than in the healthy population, and furtherresearch with matched controls is needed.

In studies on children with ADHD the prevalence of EAs variesfrom 4.8 to 15.4%. Our findings are similar to those of other studies ofEAs, reporting 6.1% [6] and 4.8% [18]. The highest rate of EAs (15.4%) inchildren with ADHD was reported by Hemmer et al. [5]. There aresome differences between their study and ours. They included abroader age group, 3–20 years, and patients being evaluated fortreatment with stimulant medications.

Holtman et al. [7] reported a higher frequency of rolandic spikes(5.6%) in 482 children with ADHD (2–16 years of age) withoutepilepsy and suggested that children with rolandic spikes more oftenhave the ADHD-C subtype than the ADHD-I subtype. This frequencywas higher than in our study and three to five times higher thanreported in the general population [16]. Of interest, two of our ninepatients with rolandic spikes had had epileptic seizures before beingdiagnosed with ADHD, suggesting an association between rolandicspikes and epileptic seizures.

4.2. ADHD subtype and EAs

We found that the ADHD-I subtype was more common in childrenwith EAs independent of a history of epilepsy. To our knowledge, sucha relationship has not previously been reported in children withoutcomorbid epilepsy, although it has been observed in patients withepilepsy [11,12,19–21]. Patients with epilepsy and ADHD may havemany factors that influence occurrence of the inattentive type ofADHD, for example, subtle epileptic seizures, transient effects offrequent epileptiform discharges, antiepileptic treatment, and under-lying neurodevelopmental vulnerability. In our study, none of thechildren with ADHD with interictal EAs but without epilepsy werebeing treated with antiepileptic drugs at ADHD assessment, suggest-ing that neurodevelopmental vulnerability and other comorbiditiesmight contribute to the variation in ADHD subtype. Although frequentepileptiform discharges were not observed on routine EEGs in ourpatients, we cannot exclude that some of our patients did not haveEAs activated by sleep as previously reported [3,4].

4.3. EEG examination, EAs, and ADHD

Cognitive dysfunction, attention difficulties, and/or behavioralproblems in ADHDmay be related to the presence of interictal EAs on

EEGs. For example, transient cognitive impairment during frequentsubclinical epileptiform discharges can affect attention and cognitivefunction even in the absence of clinical seizures [22–27]. Accordingly,Becker et al. [28] suggested that assessment of children with ADHDuntil puberty should include EEGs, regardless of the lack of a priorhistory of overt seizures or other obvious neurological conditions. Thepresence of an interictal EA helps to confirm a clinical diagnosis ofepilepsy, aids in defining the epilepsy syndrome, provides informa-tion that assists in planning drug management, and helps to assesscandidacy for epilepsy surgery [29]. On the other side, interictal EAsalso occur in children who do not have epileptic seizures. Centro-temporal spikes (rolandic spikes) are age dependent and tend todisappear during the teenage years. Generalized spike-and-wavedischarges at 3–4 Hz usually are associated with idiopathic general-ized epilepsy, but may also occur in asymptomatic relatives of patientswith epilepsy. EAs also occur in healthy children [8,16,17,29,30]. Inaddition, overreading of EEGs contributes to misdiagnosis [31]. Moreresearch is needed regarding whether EEGs should be obtained inchildren with ADHD, but caution should be used particularly withthose suspected of having ADHD-I because this group is more likelyto have EAs on routine EEGs. Diagnosis of ADHD and/or epilepsy maybe misinterpreted.

4.4. Limitations of the study

Limitations of our study include the retrospective, cross-sectionaldesign. EEGs were not obtained in all childrenwith ADHD (14.8%), butthere were no differences with respect to age, gender, or ADHDsubtype between those who had EEGs and those who did not haveEEGs. The influence of comorbid disorders was not considered, butpatients with autism spectrum disorder and IQs b50 were excludedfrom this study. Strengths include the relatively large and unselectedcohort, as all children suspected of having ADHD were referred to thecenter.

5. Conclusions

The frequency of EAs on routine EEGs in children diagnosed withADHDwas 7.5%, but when patients with a previous history of epilepsyare excluded, this frequency decreases to 5.4%.Whenwe compare thisrate with rates of EAs reported in healthy children, it is unclearwhether any differences exist. The group with ADHD and EA had alarger proportion of girls and a larger proportion of children with theADHD-I subtype independent of a history of epilepsy than did thegroup without EAs. More research is needed to identify the clinicalconsequences of EAs in children with ADHD.

Appendix A. Supplementary material

Supplementary figures associated with this article can be found, inthe online version, at doi: 10.1016/j.yebeh.2010.08.005.

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