Brain & Development xxx (2014) xxx–xxx www.elsevier.com/locate/braindev
Original article
Seizure occurrence during pediatric short-term EEG Eli Heyman a,c, Eli Lahat a,c, Revital Gandelman-Marton b,c,⇑ b
a Department of Pediatric Neurology, Israel Electroencephalography Laboratory, Assaf Harofeh Medical Center, Zerifin, Israel c Sackler School of Medicine, Tel Aviv University, Israel
Received 12 November 2013; received in revised form 28 April 2014; accepted 1 May 2014
Abstract Aim: To identify the patients who are more likely to experience a seizure during short-term EEG recording. Methods: We retrospectively reviewed the EEG recordings and medical records of 294 patients, who were admitted to the Pediatric Departments in Assaf Harofeh Medical Center, and referred for a short-term EEG during a 5-years period following a seizure. Results: Fifteen (5.1%) patients had seizures during short-term EEG. The likelihood of seizure occurrence was increased by history of seizures (odds ratio 11.86, 95% confidence interval 2.54–55.37), abnormal neurological examination (odds ratio 3.33, 95% confidence interval 1.05–10.55), and the presence of interictal epileptiform discharges (odds ratio 10.07, 95% confidence interval 1.26–80.42). Treatment with antiepileptic drugs and mental retardation were significantly more common among patients with seizures. Conclusions: Children with a higher likelihood of a seizure during short-term EEG can be identified using data mainly obtained by history and neurological examination. Ó 2014 The Japanese Society of Child Neurology. Published by Elsevier B.V. All rights reserved.
Keywords: Seizure; Epilepsy; EEG; Pediatric
1. Introduction Accurate classification of the seizure type and the epilepsy syndrome is crucial for appropriate selection of treatment. Determination of seizure type usually relies on clinical observation and interictal EEG. However, seizure reports by parents are inaccurate especially in young children, and certain seizure types such as absence seizures and infantile spasms can be missed altogether [1]. Interictal epileptiform discharges are highly specific for the diagnosis of epilepsy but can be ⇑ Corresponding author at: Department of Neurology, Assaf Harofeh Medical Center, Zerifin 70300, Israel. Tel.: +972 8 9778134; fax: +972 8 9779758. E-mail address: [email protected] (R. Gandelman-Marton).
occasionally misleading and cannot be demonstrated despite repeated EEG recordings in 10% of patients with epilepsy [2]. The ictal EEG can reveal previously unreported seizures and correct seizure classification and misdiagnosis of epileptic and nonepileptic seizures [3,4]. Routine EEGs are usually interictal, except in certain epilepsy syndromes such as absence epilepsies and in epilepsy with electrical status epilepticus during slow-wave sleep. Prolonged video-EEG recording can substantially increase the diagnostic yield of seizures, but this test is less accessible than routine EEG due to prolonged waiting periods and its high cost [5,6]. The evaluation of patients for epilepsy surgery requires the recording of sufficient seizures to permit correlation of clinical and EEG data. However, a single seizure recorded during short-term EEG obtained in the context
http://dx.doi.org/10.1016/j.braindev.2014.05.001 0387-7604/Ó 2014 The Japanese Society of Child Neurology. Published by Elsevier B.V. All rights reserved.
Please cite this article in press as: Heyman E et al. Seizure occurrence during pediatric short-term EEG. Brain Dev (2014), http://dx.doi.org/ 10.1016/j.braindev.2014.05.001
2
E. Heyman et al. / Brain & Development xxx (2014) xxx–xxx
of seizure type classification or in the differential diagnosis between seizure and non-seizure events can provide an accurate diagnosis at an earlier stage during the clinical course of the disease, thus decreasing mistreatment, patient inconvenience and the cost of diagnostic evaluation and treatment. The aim of our study was to identify the patients who are more likely to have a seizure during short-term EEG. 2. Subjects and methods We retrospectively reviewed the EEG recordings and medical records of patients admitted to the Pediatric Departments in Assaf Harofeh Medical Center and consecutively referred to the EEG lab due to seizures or suspected seizures between October 2006 and October 2011. Exclusion criteria included status epilepticus, and current admissions in the pediatric or neonatal intensive care units, and in the epilepsy monitoring unit. In patients with more than one EEG recording, only the first short-term EEG during the study period, either a 30-min routine EEG or a 60-min sleep-deprived EEG, was included in the study. The digital EEGs were recorded from 21 electrodes placed according to the international 10–20 system. Clinical variables were recorded from the admission files and included age, gender, the reason for admission, history of seizures, abnormal labor or pre-maturity, the use of antiepileptic drugs, the presence of fever on admission, abnormalities on the neurological examination, mental retardation, and a family history of epilepsy, results of imaging studies, and the admission – EEG recoding interval. State of consciousness was determined according to the notes of the EEG technicians in each EEG file. Intractable epilepsy was defined as continuously active epilepsy for at least 2 years in spite of adequate treatment with three antiepileptic drugs or more. Statistical analysis was done by SPSS version 15.0, Chicago, IL. Categorical variables were tested by Pearson Chi-Square and Fisher’s exact test, and continuous variables were analyzed by t-test. Multivariate analysis of the likelihood of seizure occurrence during routine EEG was tested by logistic regression. Statistical significance was determined at p < 0.05. The study was approved by the Ethics Committee at Assaf Harofeh Medical Center. 3. Results The study group included 294 children – 173 (59%) boys and 121 (41%) girls. The mean age was 7.6 ± 5.2 (range – 1 month to 17 years). Demographic and EEG data are summarized in Table 1. Hyperventilation was performed in 141 (48%) and intermittent photic
stimulation in 278 (95%) of the EEG recordings. Habitual events were captured in 9 (0.03%) of all the recordings and in 10% of the patients with a previous suspected seizure. Ninety-one (31%) patients had epilepsy, generalized in 58 (64%) and localization-related in 33 (36%) patients. Thirty (33%) patients had intractable epilepsy. Fifteen (5.1%) patients had a seizure during shortterm EEG, including the following seizures type: absence (n = 2), myoclonic (n = 5), tonic (n = 1), simple partial (n = 2) and complex partial seizures (n = 5). None of the seizures occurred during hyperventilation. Fourteen seizures occurred while the patients were awake, and one seizure occurred during intermittent photic stimulation. Logistic regression showed that the likelihood of seizure occurrence during short-term EEG was increased by history of seizures (OR 11.86, 95% CI 2.54–55.37) (p = 0.002), abnormal neurological examination (OR 3.33, 95% CI 1.05–10.55) (p = 0.041), and the presence of interictal epileptiform discharges (OR 10.07, 95% CI 1.26–80.42) (p = 0.029). A separate analysis according to EEG type revealed that seizure occurrence among patients who had a 30-min routine EEG was affected by history of seizures (OR 24.49, 95% CI 3.04–197.37) (p = 0.0001), intractable epilepsy (OR 14.71, 95% CI 3.84–56.3) (p = 0.0001), mental retardation (OR 13.66, 95% CI 3.24– 57.61) (p = 0.0001), use of antiepileptic drugs (OR 12.12, 95% CI 3.20–45.90) (p = 0.0001), presence of interictal epileptiform discharges (OR 10.46, 95% CI 1.30–83.90) (p = 0.008), and abnormal neurological examination (OR 10.28, 95% CI 2.55–41.40) (p = 0.001). No risk factors were identified among patients who had a sleep-deprived EEG because of the small sample size. 4. Discussion The diagnostic yield of EEG is influenced by the length of sampling and characteristics of the patients. In mixed populations of adults and children, recording of habitual events range between 8% and 77% during 20-min video-EEG or 1–7 days of inpatient video-EEG monitoring, respectively [5–7]. In children aged 1 month to 17 years, clinical episodes, either seizures or nonepileptic seizures, were recorded in 59–83% of patients during 24–48 h ambulatory EEG, 24–48 h inpatient video-EEG monitoring and a 2–3 h outpatient videoEEG monitoring [8–10]. Seizures are most likely to be recorded in patients with intractable epilepsy, symptomatic generalized epilepsy, or in those with frequent seizures [9,10]. In our study, seizures occurred in 15 (5.1%) of 294 patients who underwent a 30–60 min EEG. The lower yield can be attributed to the small proportion of patients with epilepsy, who consisted 14% of our study population. In addition, these patients
Please cite this article in press as: Heyman E et al. Seizure occurrence during pediatric short-term EEG. Brain Dev (2014), http://dx.doi.org/ 10.1016/j.braindev.2014.05.001
E. Heyman et al. / Brain & Development xxx (2014) xxx–xxx
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Table 1 Demographic and clinical data of patients with a seizure during short-term EEG.
Age (n = 294) Gender – male/female (n = 294) History of pre-maturity (n = 288) History of abnormal labor (n = 288) Family history of epilepsy (n = 292) History of seizures (n = 294) Intractable epilepsy (n = 294) Reason for admission (n = 294)a A seizure Increased seizure frequency Non-seizure related Fever (n = 294) Mental retardation (n = 293) Abnormal neurological examination (n = 294) Treatment with antiepileptic drugs (n = 294) Abnormal imaging (n = 112) Day of EEG recording (n = 294) EEG type – routine/sleep deprived (n = 294) Abnormal state of consciousness (n = 293) EEG background slowing (n = 294) Presence of interictal epileptiform discharges on EEG (n = 294)
Patients with seizure
Patients without seizure
p Value
6 ± 4.1 12 (80)/3 (20) 1 (6.7) 4 (26.7) 6 (40) 13 (86.7) 7 (46.7)
7.7 ± 5.2 161 (57.7)/118 (42.3) 33 (12.1) 52 (19) 58 (20.9) 78 (28) 23 (8.2)
0.214 0.109 1.0 0.502 0.106
Original article
Seizure occurrence during pediatric short-term EEG Eli Heyman a,c, Eli Lahat a,c, Revital Gandelman-Marton b,c,⇑ b
a Department of Pediatric Neurology, Israel Electroencephalography Laboratory, Assaf Harofeh Medical Center, Zerifin, Israel c Sackler School of Medicine, Tel Aviv University, Israel
Received 12 November 2013; received in revised form 28 April 2014; accepted 1 May 2014
Abstract Aim: To identify the patients who are more likely to experience a seizure during short-term EEG recording. Methods: We retrospectively reviewed the EEG recordings and medical records of 294 patients, who were admitted to the Pediatric Departments in Assaf Harofeh Medical Center, and referred for a short-term EEG during a 5-years period following a seizure. Results: Fifteen (5.1%) patients had seizures during short-term EEG. The likelihood of seizure occurrence was increased by history of seizures (odds ratio 11.86, 95% confidence interval 2.54–55.37), abnormal neurological examination (odds ratio 3.33, 95% confidence interval 1.05–10.55), and the presence of interictal epileptiform discharges (odds ratio 10.07, 95% confidence interval 1.26–80.42). Treatment with antiepileptic drugs and mental retardation were significantly more common among patients with seizures. Conclusions: Children with a higher likelihood of a seizure during short-term EEG can be identified using data mainly obtained by history and neurological examination. Ó 2014 The Japanese Society of Child Neurology. Published by Elsevier B.V. All rights reserved.
Keywords: Seizure; Epilepsy; EEG; Pediatric
1. Introduction Accurate classification of the seizure type and the epilepsy syndrome is crucial for appropriate selection of treatment. Determination of seizure type usually relies on clinical observation and interictal EEG. However, seizure reports by parents are inaccurate especially in young children, and certain seizure types such as absence seizures and infantile spasms can be missed altogether [1]. Interictal epileptiform discharges are highly specific for the diagnosis of epilepsy but can be ⇑ Corresponding author at: Department of Neurology, Assaf Harofeh Medical Center, Zerifin 70300, Israel. Tel.: +972 8 9778134; fax: +972 8 9779758. E-mail address: [email protected] (R. Gandelman-Marton).
occasionally misleading and cannot be demonstrated despite repeated EEG recordings in 10% of patients with epilepsy [2]. The ictal EEG can reveal previously unreported seizures and correct seizure classification and misdiagnosis of epileptic and nonepileptic seizures [3,4]. Routine EEGs are usually interictal, except in certain epilepsy syndromes such as absence epilepsies and in epilepsy with electrical status epilepticus during slow-wave sleep. Prolonged video-EEG recording can substantially increase the diagnostic yield of seizures, but this test is less accessible than routine EEG due to prolonged waiting periods and its high cost [5,6]. The evaluation of patients for epilepsy surgery requires the recording of sufficient seizures to permit correlation of clinical and EEG data. However, a single seizure recorded during short-term EEG obtained in the context
http://dx.doi.org/10.1016/j.braindev.2014.05.001 0387-7604/Ó 2014 The Japanese Society of Child Neurology. Published by Elsevier B.V. All rights reserved.
Please cite this article in press as: Heyman E et al. Seizure occurrence during pediatric short-term EEG. Brain Dev (2014), http://dx.doi.org/ 10.1016/j.braindev.2014.05.001
2
E. Heyman et al. / Brain & Development xxx (2014) xxx–xxx
of seizure type classification or in the differential diagnosis between seizure and non-seizure events can provide an accurate diagnosis at an earlier stage during the clinical course of the disease, thus decreasing mistreatment, patient inconvenience and the cost of diagnostic evaluation and treatment. The aim of our study was to identify the patients who are more likely to have a seizure during short-term EEG. 2. Subjects and methods We retrospectively reviewed the EEG recordings and medical records of patients admitted to the Pediatric Departments in Assaf Harofeh Medical Center and consecutively referred to the EEG lab due to seizures or suspected seizures between October 2006 and October 2011. Exclusion criteria included status epilepticus, and current admissions in the pediatric or neonatal intensive care units, and in the epilepsy monitoring unit. In patients with more than one EEG recording, only the first short-term EEG during the study period, either a 30-min routine EEG or a 60-min sleep-deprived EEG, was included in the study. The digital EEGs were recorded from 21 electrodes placed according to the international 10–20 system. Clinical variables were recorded from the admission files and included age, gender, the reason for admission, history of seizures, abnormal labor or pre-maturity, the use of antiepileptic drugs, the presence of fever on admission, abnormalities on the neurological examination, mental retardation, and a family history of epilepsy, results of imaging studies, and the admission – EEG recoding interval. State of consciousness was determined according to the notes of the EEG technicians in each EEG file. Intractable epilepsy was defined as continuously active epilepsy for at least 2 years in spite of adequate treatment with three antiepileptic drugs or more. Statistical analysis was done by SPSS version 15.0, Chicago, IL. Categorical variables were tested by Pearson Chi-Square and Fisher’s exact test, and continuous variables were analyzed by t-test. Multivariate analysis of the likelihood of seizure occurrence during routine EEG was tested by logistic regression. Statistical significance was determined at p < 0.05. The study was approved by the Ethics Committee at Assaf Harofeh Medical Center. 3. Results The study group included 294 children – 173 (59%) boys and 121 (41%) girls. The mean age was 7.6 ± 5.2 (range – 1 month to 17 years). Demographic and EEG data are summarized in Table 1. Hyperventilation was performed in 141 (48%) and intermittent photic
stimulation in 278 (95%) of the EEG recordings. Habitual events were captured in 9 (0.03%) of all the recordings and in 10% of the patients with a previous suspected seizure. Ninety-one (31%) patients had epilepsy, generalized in 58 (64%) and localization-related in 33 (36%) patients. Thirty (33%) patients had intractable epilepsy. Fifteen (5.1%) patients had a seizure during shortterm EEG, including the following seizures type: absence (n = 2), myoclonic (n = 5), tonic (n = 1), simple partial (n = 2) and complex partial seizures (n = 5). None of the seizures occurred during hyperventilation. Fourteen seizures occurred while the patients were awake, and one seizure occurred during intermittent photic stimulation. Logistic regression showed that the likelihood of seizure occurrence during short-term EEG was increased by history of seizures (OR 11.86, 95% CI 2.54–55.37) (p = 0.002), abnormal neurological examination (OR 3.33, 95% CI 1.05–10.55) (p = 0.041), and the presence of interictal epileptiform discharges (OR 10.07, 95% CI 1.26–80.42) (p = 0.029). A separate analysis according to EEG type revealed that seizure occurrence among patients who had a 30-min routine EEG was affected by history of seizures (OR 24.49, 95% CI 3.04–197.37) (p = 0.0001), intractable epilepsy (OR 14.71, 95% CI 3.84–56.3) (p = 0.0001), mental retardation (OR 13.66, 95% CI 3.24– 57.61) (p = 0.0001), use of antiepileptic drugs (OR 12.12, 95% CI 3.20–45.90) (p = 0.0001), presence of interictal epileptiform discharges (OR 10.46, 95% CI 1.30–83.90) (p = 0.008), and abnormal neurological examination (OR 10.28, 95% CI 2.55–41.40) (p = 0.001). No risk factors were identified among patients who had a sleep-deprived EEG because of the small sample size. 4. Discussion The diagnostic yield of EEG is influenced by the length of sampling and characteristics of the patients. In mixed populations of adults and children, recording of habitual events range between 8% and 77% during 20-min video-EEG or 1–7 days of inpatient video-EEG monitoring, respectively [5–7]. In children aged 1 month to 17 years, clinical episodes, either seizures or nonepileptic seizures, were recorded in 59–83% of patients during 24–48 h ambulatory EEG, 24–48 h inpatient video-EEG monitoring and a 2–3 h outpatient videoEEG monitoring [8–10]. Seizures are most likely to be recorded in patients with intractable epilepsy, symptomatic generalized epilepsy, or in those with frequent seizures [9,10]. In our study, seizures occurred in 15 (5.1%) of 294 patients who underwent a 30–60 min EEG. The lower yield can be attributed to the small proportion of patients with epilepsy, who consisted 14% of our study population. In addition, these patients
Please cite this article in press as: Heyman E et al. Seizure occurrence during pediatric short-term EEG. Brain Dev (2014), http://dx.doi.org/ 10.1016/j.braindev.2014.05.001
E. Heyman et al. / Brain & Development xxx (2014) xxx–xxx
3
Table 1 Demographic and clinical data of patients with a seizure during short-term EEG.
Age (n = 294) Gender – male/female (n = 294) History of pre-maturity (n = 288) History of abnormal labor (n = 288) Family history of epilepsy (n = 292) History of seizures (n = 294) Intractable epilepsy (n = 294) Reason for admission (n = 294)a A seizure Increased seizure frequency Non-seizure related Fever (n = 294) Mental retardation (n = 293) Abnormal neurological examination (n = 294) Treatment with antiepileptic drugs (n = 294) Abnormal imaging (n = 112) Day of EEG recording (n = 294) EEG type – routine/sleep deprived (n = 294) Abnormal state of consciousness (n = 293) EEG background slowing (n = 294) Presence of interictal epileptiform discharges on EEG (n = 294)
Patients with seizure
Patients without seizure
p Value
6 ± 4.1 12 (80)/3 (20) 1 (6.7) 4 (26.7) 6 (40) 13 (86.7) 7 (46.7)
7.7 ± 5.2 161 (57.7)/118 (42.3) 33 (12.1) 52 (19) 58 (20.9) 78 (28) 23 (8.2)
0.214 0.109 1.0 0.502 0.106
