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Paroxysmal nonepileptic events in pediatric patients confirmed by long-term video-EEG monitoring — Single tertiary center review of 143 patients
Epilepsy & Behavior 24 (2012) 336–340
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Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Paroxysmal nonepileptic events in pediatric patients confirmed by long-term video-EEG monitoring — Single tertiary center review of 143 patients Seung Hyo Kim a, 1, Hunmin Kim b, 1, Byung Chan Lim c, d, Jong-Hee Chae c, d, Ki Joong Kim c, d, Yong Seung Hwang c, d, Hee Hwang b,⁎ a
Department of Pediatrics, Jeju National University College of Medicine, Jeju-do, Republic of Korea Department of Pediatrics, Seoul National University Bundang Hospital, Gyeonggi-do, Republic of Korea Department of Pediatrics, Seoul National University Children's Hospital, Seoul National University College of Medicine, Seoul, Republic of Korea d Pediatric Clinical Neuroscience Center, Seoul National University Children's Hospital, Seoul, Republic of Korea b c
a r t i c l e
i n f o
Article history: Received 3 January 2012 Revised 13 March 2012 Accepted 15 March 2012 Available online 11 May 2012 Keywords: Nonepileptic Paroxysmal events Seizure Psychogenic Infants Video-EEG monitoring Children Adolescents
a b s t r a c t The purpose of the study was to evaluate the clinical characteristics of paroxysmal nonepileptic events (PNEs) in pediatric patients. Reports of 1108 patients who underwent long-term video-EEG monitoring at Seoul National University Children's Hospital were reviewed retrospectively. One hundred forty-three (12.9%) patients were diagnosed as having PNEs. The most common type of PNE was staring. Staring, tonic posturing, sleep myoclonus, and sleep-related disorders were more common in patients younger than 6 years old. Psychogenic nonepileptic seizure was the most common PNE in patients older than 6 years. Patients who were younger than 6 years old showed shorter disease duration and more varied types of PNEs when compared to older patients (6 years old or older). Presence of epilepsy was not significantly related to clinical difference in PNEs. In patients with developmental delay, staring and tonic posture were significantly more frequent than patients without developmental delay. Thirty-two patients without concurrent epilepsy were misdiagnosed with epilepsy, and AEDs were discontinued after the correct diagnosis of PNEs. Whenever the diagnosis of paroxysmal abnormal behavior is uncertain, correct diagnosis should be made using long-term video-EEG monitoring, especially in younger pediatric patients and patients with developmental delay. © 2012 Elsevier Inc. All rights reserved.
1. Introduction Paroxysmal nonepileptic events (PNEs) are episodes of paroxysmal altered movement, sensation, or experience resembling epileptic seizures. Paroxysmal nonepileptic events are not associated with abnormal electrical discharges in the brain; rather, they are caused by physiologic or psychogenic process [1,2]. The prevalence of PNEs is estimated at 5–20% of the outpatient adult epilepsy population [3], with a lower frequency reported in pediatric patients. Although the frequencies and types of PNEs have been studied extensively in the adult population [4,5], the data available for children and adolescents are more limited [6,7]. Studies addressing PNEs in pediatric patients usually include a majority of patients older than 10 years [8]. Limited information is available on the phenomenology of childhood PNEs according to developmental stage, especially in infants. Although previous studies have reported a high prevalence (5–50%) of PNEs with
⁎ Corresponding author at: Division of Pediatric Neurology, Department of Pediatrics, Seoul National University Bundang Hospital, 166 Gumi-ro, Bundang-gu, Seongnam-si, Gyeonggi-do 463-707, Republic of Korea. Fax: + 82 31 787 4054. E-mail address: [email protected] (H. Hwang). 1 Co-first authors. 1525-5050/$ – see front matter © 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2012.03.022
concurrent epilepsy, there are few data on the demographic and clinical characteristics of patients with PNEs and epilepsy in the pediatric population. Using long-term video-electroencephalography (EEG) monitoring, we report our experience with PNEs in a pediatric population consisting of various age groups. The clinical characteristics and demographic features of younger patients with PNEs and the differences of PNEs and clinical characteristics between the different age groups were evaluated and compared. The clinical characteristics of PNEs between the patients with or without epilepsy were also compared. 2. Methods This study was approved by the Institutional Review Board of the Seoul National University Hospital. The reports of 1108 patients who underwent long-term video-EEG monitoring at the Pediatric Epilepsy Monitoring Unit (PEMU) of the Seoul National University Children's Hospital between March 1995 and December 2009 were retrospectively reviewed. Paroxysmal nonepileptic events were diagnosed on the basis of clinical history and long-term video-EEG monitoring. Medical records were reviewed to collect information regarding sex, age at onset of symptoms, duration of symptoms prior to diagnosis,
S.H. Kim et al. / Epilepsy & Behavior 24 (2012) 336–340
concurrent epilepsy, developmental delay, use of antiepileptic drugs (AEDs), and brain MRI findings. Scalp electrodes were placed according to the international 10–20 system. Digital video-EEG recordings were obtained by using a Grass Technologies LTM digital EEG system. If additional electromyographic (EMG) findings were necessary, five EMG electrodes were placed on both thighs, both deltoids, and the neck. Three pediatric epileptologists (Kim KJ, Hwang YS, and Hwang H) independently reviewed interictal EEGs and video-EEGs. The monitoring was performed for a minimum of 24 h. Duration of monitoring ranged from 1 to 5 days (mean, 3.2 days and median, 2 days). An episode was not induced in all the cases, and psychogenic nonepileptic seizures were obtained spontaneously in all the cases. Each patient had at least one habitual episode recorded during the study. Patients and their families verified that the recorded episode was a typical and habitual episode. The habitual episode was considered nonepileptic if it was not associated with ictal abnormalities on the EEG. Certain types of seizures such as simple partial seizures or frontal lobe seizures without EEG correlation were excluded in this study. Diagnosis of the specific type of PNE was based on detailed descriptions from parents and on the typical feature observed during the videoEEG monitoring. Whenever possible, diagnosis was made to the level of specific etiologic entity or disease. If it was impossible to make a certain etiologic diagnosis, PNEs were classified according to the typical manifestations. Hyperkinetic movements such as chorea, dystonia, athetosis, tics, or tremors were classified as movement disorder. Sleep walking, night terrors, confusional arousals, and rhythmic movements other than sleep myoclonus were classified as a sleep disorder. The stereotypic behavior was separated from movement disorder because a large proportion of patients had developmental delays as a comorbid condition. Gastroesophageal reflux was diagnosed with 24-hour esophageal pH monitoring. Only patients with a staring event that was considered as physiologic or organic in origin were classified as ‘staring’. Dizziness, headache, or other nonspecific sensory complaints were classified as ‘sensory symptoms’. To assess the relationship between types of PNEs and clinical characteristics of patients, the patients were divided into three groups based on a threshold of 6 years of age (age at the time of monitoring). Group A included patients who were younger than 6 years old, group B included patients who were 6 years old or older but younger than 12 years old, and group C included patients who were 12 years old and older. In addition, the differences between only PNEs and PNEs with concurrent epilepsy were analyzed. Statistical analysis was performed using SPSS 18.0 for Windows. To compare patient characteristics, the Student t test and Pearson χ 2 test, and ANOVA were used. To compare the clinical characteristics between the different groups, the Pearson χ 2 test and Fisher's exact test were used, based on sample size. Statistical significance was defined as p b 0.05.
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3. Results After a review of 1108 long-term video-EEG reports, 143 (12.9%) patients (84 boys and 59 girls) diagnosed as having a specific type of PNE were identified. Ninety-one patients were classified into group A, 37 patients into group B, and 15 patients were classified into group C according to the age at diagnosis. The male:female ratio in group A was 1.68:1, 1.1:1 in group B, and 1:1.5 in group C (p = 0.246). The mean age at the onset of symptoms in group A was 1.4 years (range, 1 day to 5.8 years), 7.0 years (range, 1.2–11.8 years) for group B, and 12.7 years (range, 4.1–18.9 years) for group C. Fifty-five patients (38.4%) were younger than 1 year old, and 11 patients (7.6%) were 12 years old or older at the time of the onset of symptoms. The mean age at the time of diagnosis was 5.0 years (range, 15 days to 19.0 years). Thirty-five patients (24.5%) were younger than 1 year old, and only 15 patients (10.5%) were 12 years old or older at the time of diagnosis. The mean time difference between the onset of symptoms and diagnosis was 0.7 years in group A, 1.4 years in group B, and 1.6 years in group C (p = 0.013) (Table 1). Between one and four AEDs had been prescribed to 77 patients. Forty-six patients had concurrent epilepsy, and eight out of 46 patients (17.3%) with concurrent epilepsy were younger than 1 year old. One patient in group A was newly diagnosed as having epilepsy after monitoring. Unnecessary AEDs were prescribed to 32 of 143 patients (22.4%). Antiepileptic drugs were discontinued in 27 (84.4%) of the 32 patients who were deemed (after monitoring) to have been misdiagnosed with epilepsy. Developmental delay was present in 49 of 143 patients (34.3%) (p = 0.016). Sixty-four of 143 (44.7%) patients had concurrent epilepsy or developmental delay. Brain MRI was performed in 119 of 143 patients, and abnormal MRI results were found in 28 of 77 patients (36.4%) in group A, in 9 of 29 patients (31.0%) in group B, and 6 of 13 patients (46.2%) in group C. Stratification of PNEs according to age group showed various types of PNEs observed according to the developmental stage. The most common PNE observed was staring (22/143 patients, 15.4%). The second most common PNE was tonic posturing and sleep myoclonus (17/143 patients, 11.8%), followed by movement disorder (16/143 patients, 11.1%), and psychogenic nonepileptic seizure (15/143 patients, 10.5%) (Table 2). An analysis of patients younger than 6 years revealed that staring (16/22 patients, 72.7%), tonic posturing (16/17 patients, 94.1%), sleep myoclonus (10/17 patients, 72.7%), and sleep disorder (9/13 patients, 69.2%) were diagnosed more frequently. Psychogenic nonepileptic seizure (13/15 patients, 86.7%) was the major subgroup of PNEs in patients older than 6 years (Table 2). Based on clinical manifestations, pediatric patients with psychogenic nonepileptic seizure showed two different patterns. One was decreased responsiveness, when the patients became dialeptic with absence or decreased spontaneous movements. Another was excessive motor manifestations, when they brought out motor phenomena such as
Table 1 Demographic and clinical characteristics of patients with paroxysmal nonepileptic events by age group.
Sex (male:female) Mean age at onset of symptoms (range) Mean age at diagnosis (range) Mean latency (range) AED prescription before diagnosis (%) Concurrent epilepsy (%) Unnecessary AED (%) Developmental delay (%) Abnormal brain MRI findingsa (%)
Group A (n = 91)
Group B (n = 37)
Group C (n = 15)
p Value
57:34 1.4 y (1 d–5.8 y) 2.1 y (15 d–5.9 y) 0.7 y (6 d–5.2 y) 54 (59.3) 32 (35.2) 23 (25.3) 39 (42.9) 28 (36.4)
21:16 7.0 y (1.2–11.8 y) 8.4 y (6.0–11.9 y) 1.4 y (16 d–6.3 y) 16 (43.2) 8 (21.6) 8 (21.6) 7 (18.9) 9 (31.0)
6:9 12.7 y (4.1–18.9 y) 14.3 y (12.1–19.0 y) 1.6 y (3 d–9.0 y) 7 (46.7) 6 (40.0) 1 (6.7) 3 (20.0) 6 (46.2)
0.246
AED, antiepileptic drug. Latency, time difference from symptom onset to diagnosis. a The total number of brain MRIs performed in this study was 119 (77 patients in group A, 29 patients in group B, and 13 patients in group C).
0.013 0.213 0.261 0.274 0.016 0.639
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S.H. Kim et al. / Epilepsy & Behavior 24 (2012) 336–340
Table 2 Stratification of paroxysmal nonepileptic events into different age groups.
Staring Tonic posturing Sleep myoclonus Movement disorder PNES Sleep disorder Stereotyped behavior Sensory symptomsa Nonepileptic myoclonus Shuddering Breath holding spell Spasmus nutans GER
b 1 year
1–3 years
3–6 years
6–9 years
9–12 years
12–19 years
Total (%)
2 10 3 0 0 2 1 0 3 5 5 2 2
11 5 3 3 0 1 4 1 4 1 0 0 0
3 1 4 4 2 6 1 2 0 0 0 0 0
3 1 7 1 0 3 3 5 0 0 0 0 0
1 0 0 3 7 0 2 0 0 0 0 0 0
2 0 0 5 6 1 0 1 1 0 0 0 0
22 (15.4) 17 (11.8) 17 (11.8) 16 (11.1) 15 (10.5) 13 (9.0) 11 (7.7) 9 (6.3) 8 (5.5) 6 (4.2) 5 (3.5) 2 (1.4) 2 (1.4)
PNES, psychogenic nonepileptic seizure; GER, gastroesophageal reflux. a Sensory symptoms: dizziness, headache, or other nonspecific sensory complaints.
bizarre, irregular movements of extremities, not typical of epileptic seizures. The number of patients who showed decreased responsiveness vs. excessive motor manifestation was 1:1 in group A, 3:4 in group B, and 2:4 in group C. Various PNEs were observed in infants. The PNEs observed in infants were (in decreasing order of frequency): tonic posturing (10/35 patients, 28.6%), staring (2/35 patients, 5.7%), stereotyped behavior (1/35 patients, 2.8%), sleep myoclonus (3/35 patients, 8.6%), breath holding spell (5/35 patients, 14.3%), shuddering (5/35 patients, 14.3%), nonepileptic myoclonus (3/35 patients, 8.6%), spasmus nutans (2/35 patients, 5.7%) and gastroesophageal reflux (2/35 patients, 5.7%) (Table 2). The male:female ratio was 2:1 for patients without epilepsy and 1:1.4 for patients with epilepsy (p = 0.004). The time difference from the onset of symptoms to diagnosis was 1.1 years in patients without epilepsy and 0.7 years for patients with epilepsy (p = 0.023). Among the 46 patients with concurrent epilepsy, 34 patients (73.9%) exhibited partial seizures, and 12 patients (26.1%) had generalized seizures. Thirty-one of the 46 patients (67.4%) with epilepsy exhibited developmental delay. Brain abnormalities on MRI were detected in 14 (19.2%) of the patients with NEs alone and in 29 of the 46 (63.0%) patients with epilepsy (Table 3). When we compared the difference of specific PNE types between the groups of patients with or without developmental delay, staring,
Table 3 Demographic and clinical characteristics of patients with or without concurrent epilepsy.
Sex (M:F) Mean age at onset of symptom Mean age at monitoring Mean latency Developmental delay (%) Prescription of AED (%) Interictal spike (%) Abnormal brain MRI (%) Specific PNE type Staring (%) Tonic posturing (%) Sleep myoclonus (%) Movement disorder (%) PNES (%) Stereotyped behavior (%) Nonepileptic myoclonus (%)
Without epilepsy (n = 97)
With epilepsy (n = 46)
p Value
65:32 (2:1) 4.0 y 5.1 y 1.1 y 18 (18.6) 32 (33.0) 19 (19.6) 14a (19.2)
19:27 (1:1.4) 4.2 y 4.9 y 0.7 y 31 (67.4) 45 (98.0) 46 (100) 29 (63.0)
0.004 0.755 0.806 0.023 b 0.01 b 0.01 b 0.01 b 0.01
12 (12.3) 8 (8.2) 14 (14.4) 13 (13.4) 11 (11.3) 6 (6.1) 3 (3.0)
10 (21.7) 9 (19.5) 3 (6.5) 3 (6.5) 4 (8.6) 5 (10.8) 5 (10.8)
0.147 0.051 0.172 0.144 0.515 0.332 0.111
y, years; AED, antiepileptic drug; PNES, pyschogenic nonepileptic seizure. a Brain MRI was not performed in 24 of the 97 PNE patients without coexisting epilepsy.
tonic posturing, and nonepileptic myoclonus were observed more frequently in patients with developmental delay (p b 0.05) (Table 4). 4. Discussion The frequency of PNEs in pediatric patients admitted for monitoring at an epilepsy center ranges from 3.5% to 43% [6,9]. This wide range is probably a reflection of the population being monitored and of a referral bias [10]. In our study, 12.9% of patients monitored in PEMU were diagnosed with PNEs. Several factors can affect the prevalence of PNEs. The prevalence of PNEs is higher in patients with intractable epilepsy than in the general population [11]. In addition, abnormal behavior is common in patients with developmental delay. Our study included a substantial proportion of patients with epilepsy or developmental delay, and this could have affected the prevalence. Moreover, this study was limited to patients referred for long-term video-EEG monitoring; therefore, the results are not a true indication of the actual incidence of PNEs in the general population. In our series, the mean age of onset and mean age at diagnosis were lower than those reported in other pediatric studies, in which the mean age at the diagnosis was usually over 10 years old [6,8,9,12]. Thirty-four patients (23.7%) in this study were infants at the time of diagnosis, which led to a lower mean age of onset and a lower mean age at the time of diagnosis. The younger age population comprised a high proportion of males (1.67:1), whereas the male:female ratio was more balanced in older patients. Two pediatric studies showed a male predominance pattern in younger children, ranging in age between 2 months and 5 years [8,10]. Our results followed a similar pattern, although they did not reach statistical significance. The mean time difference from the onset of symptom to diagnosis was 1.0 year, which was similar to the results of other studies [6,8,11,13]. The mean latency was shorter in the younger age group than in the older age group. It is well known that patients with
Table 4 Comparison of paroxysmal nonepileptic events in patients with or without developmental delay. Type
Patients without DD (n = 94)
Patients with DD (n = 49)
p Value
Staring (%) Tonic posturing (%) Sleep myoclonus (%) PNES (%) Movement disorder (%) Sleep disorder (%) Stereotyped behavior (%) Nonepileptic myoclonus (%)
9 (9.5) 1 (1.0) 17 (18.0) 14 (14.9) 16 (17.0) 11 (11.7) 6 (6.3) 2 (2.1)
13 (26.5) 16 (32.6) 0 1 (2.0) 0 2 (4.0) 5 (10.2) 6 (12.2)
0.008 b0.01 b0.01 0.011 b0.01 0.219 0.511 0.020
DD, developmental delay; PNES, psychogenic nonepileptic seizure.
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developmental delay frequently show abnormal movements and unexplained behavior [6,8,10,14–16]. Higher prevalence of developmental delay in younger patients with PNEs may have led to the early detection of such abnormal movements in younger patients. The most common manifestation of PNEs was staring, followed by tonic posturing, sleep myoclonus, movement disorder and psychogenic nonepileptic seizures. This result was in line with the results of other studies, in which staring was the most common manifestations of PNEs in pediatric patients [6,9,16,17]. Our data indicate that the specific types of PNEs vary widely with age. Various types of PNEs were observed in younger patients (especially in infants) compared to older patients. In a previous study, infants presented with a wide spectrum of movement patterns that mimic epilepsy [18]. It was also found that PNEs in younger patients were different from those in older patients. Subtle motor activities, such as staring, were more frequent in younger patients, whereas older patients exhibited prominent motor activities, such as movement disorders and psychogenic nonepileptic seizures. This finding was in agreement with the results of other studies [6,9,16,17]. There are a few studies that compared PNEs with or without concurrent epilepsy in pediatric populations [19]. Epileptic seizures and PNEs often coexist in the same patient [20,21]. A high prevalence (32.1%) of concurrent epilepsy in patients with PNEs was observed in this study. In other pediatric studies, this prevalence is usually between 15% and 60% [8,10,19,22,23]. Considering the high prevalence of PNE in patients with epilepsy, especially in pediatric patients with epilepsy and cognitive impairment which is shown in this study, we stress the importance of long-term video-EEG monitoring in differentiating PNEs from habitual seizures to prevent over-medication. Patients with concurrent epilepsy exhibited a high frequency of development delay, abnormal brain MRI findings, and shorter time difference between onset of symptom and diagnosis. The high frequency of developmental delay or abnormal brain MRI findings in patients with PNE and concurrent epilepsy was reported in a previous study [19]. Regarding mean latency, patients with epilepsy showed shorter mean latency than patients without epilepsy. Concerning the seizure type in concurrent epilepsy, partial seizure was more commonly observed than generalized seizure in this study. This predominance of partial seizure is consistent with the results of other studies [6,20]. Regarding the type of PNEs, sleep myoclonus, movement disorders, psychogenic nonepileptic seizures, and staring events were common in patients without epilepsy. Staring, tonic posturing, and stereotyped behavior were common in patients with concurrent epilepsy. However, there were no significant differences in specific types of PNEs. The analysis of differences in PNEs based on the presence of developmental delay revealed that staring, tonic posturing, and nonepileptic myoclonus were significantly more frequent in patients with developmental delay, whereas sleep myoclonus, psychogenic nonepileptic seizure, and movement disorder were more common in patients without developmental delay. These findings are partly discordant with a previous study, which showed that the presence of epilepsy or developmental delay was not related to the difference in types of PNEs observed [24]. However, this difference can be used in the diagnosis of PNEs in patients with developmental delay. Thirty-one of the 97 patients (31.9%) without epilepsy had an interictal spike in the EEG or developmental delay. Twelve of these 31 patients were taking unnecessary AEDs. Frequently observed PNEs in patients with developmental delay are easily misdiagnosed as epileptic seizures in the setting of epileptiform discharges in an EEG. Long-term video-EEG monitoring should be performed in patients with abnormal behaviors, especially in patients with developmental delay and interictal epileptiform discharges. Nine of the 32 patients (28.1%) taking unnecessary AEDs, 16 of the 49 patients (32.6%) with developmental delay, and eight of the 46 patients (17.3%) with concurrent epilepsy were infants. Sixteen of the 64 (25.0%) patients with epilepsy or developmental delay were infants,
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and about 30% of infants with PNEs were taking unnecessary AEDs. To prevent misdiagnosis of epilepsy and unnecessary AED treatment, abnormal paroxysmal behaviors in infants should be diagnosed with caution. Whenever the diagnosis of PNEs or epileptic seizures is uncertain, long-term video-EEG monitoring should be performed. In conclusion, PNEs in younger pediatric patients were not different from previous studies. However, younger patients presented with shorter disease duration and more various types of PNEs compared to older patients. The presence of concurrent epilepsy was not related to the difference in clinical characteristics of PNEs. However, the presence of developmental delay was related to specific types of PNEs. Staring and tonic posturing were more frequently observed in patients with PNEs and developmental delay, and this finding was statistically significant. Misdiagnosis of epilepsy and unnecessary AED treatment were more frequent in patients with developmental delay and epileptiform discharges in an EEG. Infants were also frequently misdiagnosed with epilepsy. Pediatric neurologists must not misdiagnose PNEs as epileptic seizures, especially in patients with developmental delay or in younger patients. Whenever the diagnosis is uncertain, careful examination and verification with other tests, especially long-term video-EEG monitoring, must be done. Although the long-term video-EEG is very useful in the diagnosis of PNEs, an accurate diagnosis of PNE and the specific etiologic diagnosis of PNE may still be challenging. This is a retrospective observational analysis, so the findings in this study must be verified in prospective studies. Acknowledgments The authors are grateful to Mrs. MiSun Park for her help in preparing the manuscript. References [1] Reuber M. Psychogenic nonepileptic seizures: answers and questions. Epilepsy Behav 2008;12:622–35. [2] Brown RJ, Syed TU, Benbadis S, Lafrance Jr WC, Reuber M. Psychogenic nonepileptic seizures. Epilepsy Behav 2011;22:85–93. [3] Mari F, Di Bonaventura C, Vanacore N, et al. Video-EEG study of psychogenic nonepileptic seizures: differential characteristics in patients with and without epilepsy. Epilepsia 2006;47(Suppl. 5):64–7. [4] Abubakr A, Kablinger A, Caldito G. Psychogenic seizures: clinical features and psychological analysis. Epilepsy Behav 2003;4:241–5. [5] Benbadis SR, Allen Hauser W. An estimate of the prevalence of psychogenic nonepileptic seizures. Seizure 2000;9:280–1. [6] Patel H, Scott E, Dunn D, Garg B. Nonepileptic seizures in children. Epilepsia 2007;48:2086–92. [7] Wyllie E, Glazer JP, Benbadis S, Kotagal P, Wolgamuth B. Psychiatric features of children and adolescents with pseudoseizures. Arch Pediatr Adolesc Med 1999;153:244–8. [8] Vincentiis S, Valente KD, Thome-Souza S, Kuczinsky E, Fiore LA, Negrao N. Risk factors for psychogenic nonepileptic seizures in children and adolescents with epilepsy. Epilepsy Behav 2006;8:294–8. [9] Kutluay E, Selwa L, Minecan D, Edwards J, Beydoun A. Nonepileptic paroxysmal events in a pediatric population. Epilepsy Behav 2010;17:272–5. [10] Benbadis SR, Agrawal V, Tatum WO. How many patients with psychogenic nonepileptic seizures also have epilepsy? Neurology 2001;57:915–7. [11] Reuber M, Elger CE. Psychogenic nonepileptic seizures: review and update. Epilepsy Behav 2003;4:205–16. [12] Asano E, Pawlak C, Shah A, et al. The diagnostic value of initial video-EEG monitoring in children—review of 1000 cases. Epilepsy Res 2005;66:129–35. [13] Pierelli F, Chatrian GE, Erdly WW, Swanson PD. Long-term EEG-video-audio monitoring: detection of partial epileptic seizures and psychogenic episodes by 24hour EEG record review. Epilepsia 1989;30:513–23. [14] Wyllie E, Friedman D, Rothner AD, et al. Psychogenic seizures in children and adolescents: outcome after diagnosis by ictal video and electroencephalographic recording. Pediatrics 1990;85:480–4. [15] Reuber M, Fernandez G, Bauer J, Helmstaedter C, Elger CE. Diagnostic delay in psychogenic nonepileptic seizures. Neurology 2002;58:493–5. [16] Rosenow F, Wyllie E, Kotagal P, Mascha E, Wolgamuth BR, Hamer H. Staring spells in children: descriptive features distinguishing epileptic and nonepileptic events. J Pediatr 1998;133:660–3. [17] Shuper A, Mimouni M. Problems of differentiation between epilepsy and nonepileptic paroxysmal events in the first year of life. Arch Dis Child 1995;73:342–4. [18] Carmant L, Kramer U, Holmes GL, Mikati MA, Riviello JJ, Helmers SL. Differential diagnosis of staring spells in children: a video-EEG study. Pediatr Neurol 1996;14:199–202.
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Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Paroxysmal nonepileptic events in pediatric patients confirmed by long-term video-EEG monitoring — Single tertiary center review of 143 patients Seung Hyo Kim a, 1, Hunmin Kim b, 1, Byung Chan Lim c, d, Jong-Hee Chae c, d, Ki Joong Kim c, d, Yong Seung Hwang c, d, Hee Hwang b,⁎ a
Department of Pediatrics, Jeju National University College of Medicine, Jeju-do, Republic of Korea Department of Pediatrics, Seoul National University Bundang Hospital, Gyeonggi-do, Republic of Korea Department of Pediatrics, Seoul National University Children's Hospital, Seoul National University College of Medicine, Seoul, Republic of Korea d Pediatric Clinical Neuroscience Center, Seoul National University Children's Hospital, Seoul, Republic of Korea b c
a r t i c l e
i n f o
Article history: Received 3 January 2012 Revised 13 March 2012 Accepted 15 March 2012 Available online 11 May 2012 Keywords: Nonepileptic Paroxysmal events Seizure Psychogenic Infants Video-EEG monitoring Children Adolescents
a b s t r a c t The purpose of the study was to evaluate the clinical characteristics of paroxysmal nonepileptic events (PNEs) in pediatric patients. Reports of 1108 patients who underwent long-term video-EEG monitoring at Seoul National University Children's Hospital were reviewed retrospectively. One hundred forty-three (12.9%) patients were diagnosed as having PNEs. The most common type of PNE was staring. Staring, tonic posturing, sleep myoclonus, and sleep-related disorders were more common in patients younger than 6 years old. Psychogenic nonepileptic seizure was the most common PNE in patients older than 6 years. Patients who were younger than 6 years old showed shorter disease duration and more varied types of PNEs when compared to older patients (6 years old or older). Presence of epilepsy was not significantly related to clinical difference in PNEs. In patients with developmental delay, staring and tonic posture were significantly more frequent than patients without developmental delay. Thirty-two patients without concurrent epilepsy were misdiagnosed with epilepsy, and AEDs were discontinued after the correct diagnosis of PNEs. Whenever the diagnosis of paroxysmal abnormal behavior is uncertain, correct diagnosis should be made using long-term video-EEG monitoring, especially in younger pediatric patients and patients with developmental delay. © 2012 Elsevier Inc. All rights reserved.
1. Introduction Paroxysmal nonepileptic events (PNEs) are episodes of paroxysmal altered movement, sensation, or experience resembling epileptic seizures. Paroxysmal nonepileptic events are not associated with abnormal electrical discharges in the brain; rather, they are caused by physiologic or psychogenic process [1,2]. The prevalence of PNEs is estimated at 5–20% of the outpatient adult epilepsy population [3], with a lower frequency reported in pediatric patients. Although the frequencies and types of PNEs have been studied extensively in the adult population [4,5], the data available for children and adolescents are more limited [6,7]. Studies addressing PNEs in pediatric patients usually include a majority of patients older than 10 years [8]. Limited information is available on the phenomenology of childhood PNEs according to developmental stage, especially in infants. Although previous studies have reported a high prevalence (5–50%) of PNEs with
⁎ Corresponding author at: Division of Pediatric Neurology, Department of Pediatrics, Seoul National University Bundang Hospital, 166 Gumi-ro, Bundang-gu, Seongnam-si, Gyeonggi-do 463-707, Republic of Korea. Fax: + 82 31 787 4054. E-mail address: [email protected] (H. Hwang). 1 Co-first authors. 1525-5050/$ – see front matter © 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2012.03.022
concurrent epilepsy, there are few data on the demographic and clinical characteristics of patients with PNEs and epilepsy in the pediatric population. Using long-term video-electroencephalography (EEG) monitoring, we report our experience with PNEs in a pediatric population consisting of various age groups. The clinical characteristics and demographic features of younger patients with PNEs and the differences of PNEs and clinical characteristics between the different age groups were evaluated and compared. The clinical characteristics of PNEs between the patients with or without epilepsy were also compared. 2. Methods This study was approved by the Institutional Review Board of the Seoul National University Hospital. The reports of 1108 patients who underwent long-term video-EEG monitoring at the Pediatric Epilepsy Monitoring Unit (PEMU) of the Seoul National University Children's Hospital between March 1995 and December 2009 were retrospectively reviewed. Paroxysmal nonepileptic events were diagnosed on the basis of clinical history and long-term video-EEG monitoring. Medical records were reviewed to collect information regarding sex, age at onset of symptoms, duration of symptoms prior to diagnosis,
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concurrent epilepsy, developmental delay, use of antiepileptic drugs (AEDs), and brain MRI findings. Scalp electrodes were placed according to the international 10–20 system. Digital video-EEG recordings were obtained by using a Grass Technologies LTM digital EEG system. If additional electromyographic (EMG) findings were necessary, five EMG electrodes were placed on both thighs, both deltoids, and the neck. Three pediatric epileptologists (Kim KJ, Hwang YS, and Hwang H) independently reviewed interictal EEGs and video-EEGs. The monitoring was performed for a minimum of 24 h. Duration of monitoring ranged from 1 to 5 days (mean, 3.2 days and median, 2 days). An episode was not induced in all the cases, and psychogenic nonepileptic seizures were obtained spontaneously in all the cases. Each patient had at least one habitual episode recorded during the study. Patients and their families verified that the recorded episode was a typical and habitual episode. The habitual episode was considered nonepileptic if it was not associated with ictal abnormalities on the EEG. Certain types of seizures such as simple partial seizures or frontal lobe seizures without EEG correlation were excluded in this study. Diagnosis of the specific type of PNE was based on detailed descriptions from parents and on the typical feature observed during the videoEEG monitoring. Whenever possible, diagnosis was made to the level of specific etiologic entity or disease. If it was impossible to make a certain etiologic diagnosis, PNEs were classified according to the typical manifestations. Hyperkinetic movements such as chorea, dystonia, athetosis, tics, or tremors were classified as movement disorder. Sleep walking, night terrors, confusional arousals, and rhythmic movements other than sleep myoclonus were classified as a sleep disorder. The stereotypic behavior was separated from movement disorder because a large proportion of patients had developmental delays as a comorbid condition. Gastroesophageal reflux was diagnosed with 24-hour esophageal pH monitoring. Only patients with a staring event that was considered as physiologic or organic in origin were classified as ‘staring’. Dizziness, headache, or other nonspecific sensory complaints were classified as ‘sensory symptoms’. To assess the relationship between types of PNEs and clinical characteristics of patients, the patients were divided into three groups based on a threshold of 6 years of age (age at the time of monitoring). Group A included patients who were younger than 6 years old, group B included patients who were 6 years old or older but younger than 12 years old, and group C included patients who were 12 years old and older. In addition, the differences between only PNEs and PNEs with concurrent epilepsy were analyzed. Statistical analysis was performed using SPSS 18.0 for Windows. To compare patient characteristics, the Student t test and Pearson χ 2 test, and ANOVA were used. To compare the clinical characteristics between the different groups, the Pearson χ 2 test and Fisher's exact test were used, based on sample size. Statistical significance was defined as p b 0.05.
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3. Results After a review of 1108 long-term video-EEG reports, 143 (12.9%) patients (84 boys and 59 girls) diagnosed as having a specific type of PNE were identified. Ninety-one patients were classified into group A, 37 patients into group B, and 15 patients were classified into group C according to the age at diagnosis. The male:female ratio in group A was 1.68:1, 1.1:1 in group B, and 1:1.5 in group C (p = 0.246). The mean age at the onset of symptoms in group A was 1.4 years (range, 1 day to 5.8 years), 7.0 years (range, 1.2–11.8 years) for group B, and 12.7 years (range, 4.1–18.9 years) for group C. Fifty-five patients (38.4%) were younger than 1 year old, and 11 patients (7.6%) were 12 years old or older at the time of the onset of symptoms. The mean age at the time of diagnosis was 5.0 years (range, 15 days to 19.0 years). Thirty-five patients (24.5%) were younger than 1 year old, and only 15 patients (10.5%) were 12 years old or older at the time of diagnosis. The mean time difference between the onset of symptoms and diagnosis was 0.7 years in group A, 1.4 years in group B, and 1.6 years in group C (p = 0.013) (Table 1). Between one and four AEDs had been prescribed to 77 patients. Forty-six patients had concurrent epilepsy, and eight out of 46 patients (17.3%) with concurrent epilepsy were younger than 1 year old. One patient in group A was newly diagnosed as having epilepsy after monitoring. Unnecessary AEDs were prescribed to 32 of 143 patients (22.4%). Antiepileptic drugs were discontinued in 27 (84.4%) of the 32 patients who were deemed (after monitoring) to have been misdiagnosed with epilepsy. Developmental delay was present in 49 of 143 patients (34.3%) (p = 0.016). Sixty-four of 143 (44.7%) patients had concurrent epilepsy or developmental delay. Brain MRI was performed in 119 of 143 patients, and abnormal MRI results were found in 28 of 77 patients (36.4%) in group A, in 9 of 29 patients (31.0%) in group B, and 6 of 13 patients (46.2%) in group C. Stratification of PNEs according to age group showed various types of PNEs observed according to the developmental stage. The most common PNE observed was staring (22/143 patients, 15.4%). The second most common PNE was tonic posturing and sleep myoclonus (17/143 patients, 11.8%), followed by movement disorder (16/143 patients, 11.1%), and psychogenic nonepileptic seizure (15/143 patients, 10.5%) (Table 2). An analysis of patients younger than 6 years revealed that staring (16/22 patients, 72.7%), tonic posturing (16/17 patients, 94.1%), sleep myoclonus (10/17 patients, 72.7%), and sleep disorder (9/13 patients, 69.2%) were diagnosed more frequently. Psychogenic nonepileptic seizure (13/15 patients, 86.7%) was the major subgroup of PNEs in patients older than 6 years (Table 2). Based on clinical manifestations, pediatric patients with psychogenic nonepileptic seizure showed two different patterns. One was decreased responsiveness, when the patients became dialeptic with absence or decreased spontaneous movements. Another was excessive motor manifestations, when they brought out motor phenomena such as
Table 1 Demographic and clinical characteristics of patients with paroxysmal nonepileptic events by age group.
Sex (male:female) Mean age at onset of symptoms (range) Mean age at diagnosis (range) Mean latency (range) AED prescription before diagnosis (%) Concurrent epilepsy (%) Unnecessary AED (%) Developmental delay (%) Abnormal brain MRI findingsa (%)
Group A (n = 91)
Group B (n = 37)
Group C (n = 15)
p Value
57:34 1.4 y (1 d–5.8 y) 2.1 y (15 d–5.9 y) 0.7 y (6 d–5.2 y) 54 (59.3) 32 (35.2) 23 (25.3) 39 (42.9) 28 (36.4)
21:16 7.0 y (1.2–11.8 y) 8.4 y (6.0–11.9 y) 1.4 y (16 d–6.3 y) 16 (43.2) 8 (21.6) 8 (21.6) 7 (18.9) 9 (31.0)
6:9 12.7 y (4.1–18.9 y) 14.3 y (12.1–19.0 y) 1.6 y (3 d–9.0 y) 7 (46.7) 6 (40.0) 1 (6.7) 3 (20.0) 6 (46.2)
0.246
AED, antiepileptic drug. Latency, time difference from symptom onset to diagnosis. a The total number of brain MRIs performed in this study was 119 (77 patients in group A, 29 patients in group B, and 13 patients in group C).
0.013 0.213 0.261 0.274 0.016 0.639
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Table 2 Stratification of paroxysmal nonepileptic events into different age groups.
Staring Tonic posturing Sleep myoclonus Movement disorder PNES Sleep disorder Stereotyped behavior Sensory symptomsa Nonepileptic myoclonus Shuddering Breath holding spell Spasmus nutans GER
b 1 year
1–3 years
3–6 years
6–9 years
9–12 years
12–19 years
Total (%)
2 10 3 0 0 2 1 0 3 5 5 2 2
11 5 3 3 0 1 4 1 4 1 0 0 0
3 1 4 4 2 6 1 2 0 0 0 0 0
3 1 7 1 0 3 3 5 0 0 0 0 0
1 0 0 3 7 0 2 0 0 0 0 0 0
2 0 0 5 6 1 0 1 1 0 0 0 0
22 (15.4) 17 (11.8) 17 (11.8) 16 (11.1) 15 (10.5) 13 (9.0) 11 (7.7) 9 (6.3) 8 (5.5) 6 (4.2) 5 (3.5) 2 (1.4) 2 (1.4)
PNES, psychogenic nonepileptic seizure; GER, gastroesophageal reflux. a Sensory symptoms: dizziness, headache, or other nonspecific sensory complaints.
bizarre, irregular movements of extremities, not typical of epileptic seizures. The number of patients who showed decreased responsiveness vs. excessive motor manifestation was 1:1 in group A, 3:4 in group B, and 2:4 in group C. Various PNEs were observed in infants. The PNEs observed in infants were (in decreasing order of frequency): tonic posturing (10/35 patients, 28.6%), staring (2/35 patients, 5.7%), stereotyped behavior (1/35 patients, 2.8%), sleep myoclonus (3/35 patients, 8.6%), breath holding spell (5/35 patients, 14.3%), shuddering (5/35 patients, 14.3%), nonepileptic myoclonus (3/35 patients, 8.6%), spasmus nutans (2/35 patients, 5.7%) and gastroesophageal reflux (2/35 patients, 5.7%) (Table 2). The male:female ratio was 2:1 for patients without epilepsy and 1:1.4 for patients with epilepsy (p = 0.004). The time difference from the onset of symptoms to diagnosis was 1.1 years in patients without epilepsy and 0.7 years for patients with epilepsy (p = 0.023). Among the 46 patients with concurrent epilepsy, 34 patients (73.9%) exhibited partial seizures, and 12 patients (26.1%) had generalized seizures. Thirty-one of the 46 patients (67.4%) with epilepsy exhibited developmental delay. Brain abnormalities on MRI were detected in 14 (19.2%) of the patients with NEs alone and in 29 of the 46 (63.0%) patients with epilepsy (Table 3). When we compared the difference of specific PNE types between the groups of patients with or without developmental delay, staring,
Table 3 Demographic and clinical characteristics of patients with or without concurrent epilepsy.
Sex (M:F) Mean age at onset of symptom Mean age at monitoring Mean latency Developmental delay (%) Prescription of AED (%) Interictal spike (%) Abnormal brain MRI (%) Specific PNE type Staring (%) Tonic posturing (%) Sleep myoclonus (%) Movement disorder (%) PNES (%) Stereotyped behavior (%) Nonepileptic myoclonus (%)
Without epilepsy (n = 97)
With epilepsy (n = 46)
p Value
65:32 (2:1) 4.0 y 5.1 y 1.1 y 18 (18.6) 32 (33.0) 19 (19.6) 14a (19.2)
19:27 (1:1.4) 4.2 y 4.9 y 0.7 y 31 (67.4) 45 (98.0) 46 (100) 29 (63.0)
0.004 0.755 0.806 0.023 b 0.01 b 0.01 b 0.01 b 0.01
12 (12.3) 8 (8.2) 14 (14.4) 13 (13.4) 11 (11.3) 6 (6.1) 3 (3.0)
10 (21.7) 9 (19.5) 3 (6.5) 3 (6.5) 4 (8.6) 5 (10.8) 5 (10.8)
0.147 0.051 0.172 0.144 0.515 0.332 0.111
y, years; AED, antiepileptic drug; PNES, pyschogenic nonepileptic seizure. a Brain MRI was not performed in 24 of the 97 PNE patients without coexisting epilepsy.
tonic posturing, and nonepileptic myoclonus were observed more frequently in patients with developmental delay (p b 0.05) (Table 4). 4. Discussion The frequency of PNEs in pediatric patients admitted for monitoring at an epilepsy center ranges from 3.5% to 43% [6,9]. This wide range is probably a reflection of the population being monitored and of a referral bias [10]. In our study, 12.9% of patients monitored in PEMU were diagnosed with PNEs. Several factors can affect the prevalence of PNEs. The prevalence of PNEs is higher in patients with intractable epilepsy than in the general population [11]. In addition, abnormal behavior is common in patients with developmental delay. Our study included a substantial proportion of patients with epilepsy or developmental delay, and this could have affected the prevalence. Moreover, this study was limited to patients referred for long-term video-EEG monitoring; therefore, the results are not a true indication of the actual incidence of PNEs in the general population. In our series, the mean age of onset and mean age at diagnosis were lower than those reported in other pediatric studies, in which the mean age at the diagnosis was usually over 10 years old [6,8,9,12]. Thirty-four patients (23.7%) in this study were infants at the time of diagnosis, which led to a lower mean age of onset and a lower mean age at the time of diagnosis. The younger age population comprised a high proportion of males (1.67:1), whereas the male:female ratio was more balanced in older patients. Two pediatric studies showed a male predominance pattern in younger children, ranging in age between 2 months and 5 years [8,10]. Our results followed a similar pattern, although they did not reach statistical significance. The mean time difference from the onset of symptom to diagnosis was 1.0 year, which was similar to the results of other studies [6,8,11,13]. The mean latency was shorter in the younger age group than in the older age group. It is well known that patients with
Table 4 Comparison of paroxysmal nonepileptic events in patients with or without developmental delay. Type
Patients without DD (n = 94)
Patients with DD (n = 49)
p Value
Staring (%) Tonic posturing (%) Sleep myoclonus (%) PNES (%) Movement disorder (%) Sleep disorder (%) Stereotyped behavior (%) Nonepileptic myoclonus (%)
9 (9.5) 1 (1.0) 17 (18.0) 14 (14.9) 16 (17.0) 11 (11.7) 6 (6.3) 2 (2.1)
13 (26.5) 16 (32.6) 0 1 (2.0) 0 2 (4.0) 5 (10.2) 6 (12.2)
0.008 b0.01 b0.01 0.011 b0.01 0.219 0.511 0.020
DD, developmental delay; PNES, psychogenic nonepileptic seizure.
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developmental delay frequently show abnormal movements and unexplained behavior [6,8,10,14–16]. Higher prevalence of developmental delay in younger patients with PNEs may have led to the early detection of such abnormal movements in younger patients. The most common manifestation of PNEs was staring, followed by tonic posturing, sleep myoclonus, movement disorder and psychogenic nonepileptic seizures. This result was in line with the results of other studies, in which staring was the most common manifestations of PNEs in pediatric patients [6,9,16,17]. Our data indicate that the specific types of PNEs vary widely with age. Various types of PNEs were observed in younger patients (especially in infants) compared to older patients. In a previous study, infants presented with a wide spectrum of movement patterns that mimic epilepsy [18]. It was also found that PNEs in younger patients were different from those in older patients. Subtle motor activities, such as staring, were more frequent in younger patients, whereas older patients exhibited prominent motor activities, such as movement disorders and psychogenic nonepileptic seizures. This finding was in agreement with the results of other studies [6,9,16,17]. There are a few studies that compared PNEs with or without concurrent epilepsy in pediatric populations [19]. Epileptic seizures and PNEs often coexist in the same patient [20,21]. A high prevalence (32.1%) of concurrent epilepsy in patients with PNEs was observed in this study. In other pediatric studies, this prevalence is usually between 15% and 60% [8,10,19,22,23]. Considering the high prevalence of PNE in patients with epilepsy, especially in pediatric patients with epilepsy and cognitive impairment which is shown in this study, we stress the importance of long-term video-EEG monitoring in differentiating PNEs from habitual seizures to prevent over-medication. Patients with concurrent epilepsy exhibited a high frequency of development delay, abnormal brain MRI findings, and shorter time difference between onset of symptom and diagnosis. The high frequency of developmental delay or abnormal brain MRI findings in patients with PNE and concurrent epilepsy was reported in a previous study [19]. Regarding mean latency, patients with epilepsy showed shorter mean latency than patients without epilepsy. Concerning the seizure type in concurrent epilepsy, partial seizure was more commonly observed than generalized seizure in this study. This predominance of partial seizure is consistent with the results of other studies [6,20]. Regarding the type of PNEs, sleep myoclonus, movement disorders, psychogenic nonepileptic seizures, and staring events were common in patients without epilepsy. Staring, tonic posturing, and stereotyped behavior were common in patients with concurrent epilepsy. However, there were no significant differences in specific types of PNEs. The analysis of differences in PNEs based on the presence of developmental delay revealed that staring, tonic posturing, and nonepileptic myoclonus were significantly more frequent in patients with developmental delay, whereas sleep myoclonus, psychogenic nonepileptic seizure, and movement disorder were more common in patients without developmental delay. These findings are partly discordant with a previous study, which showed that the presence of epilepsy or developmental delay was not related to the difference in types of PNEs observed [24]. However, this difference can be used in the diagnosis of PNEs in patients with developmental delay. Thirty-one of the 97 patients (31.9%) without epilepsy had an interictal spike in the EEG or developmental delay. Twelve of these 31 patients were taking unnecessary AEDs. Frequently observed PNEs in patients with developmental delay are easily misdiagnosed as epileptic seizures in the setting of epileptiform discharges in an EEG. Long-term video-EEG monitoring should be performed in patients with abnormal behaviors, especially in patients with developmental delay and interictal epileptiform discharges. Nine of the 32 patients (28.1%) taking unnecessary AEDs, 16 of the 49 patients (32.6%) with developmental delay, and eight of the 46 patients (17.3%) with concurrent epilepsy were infants. Sixteen of the 64 (25.0%) patients with epilepsy or developmental delay were infants,
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and about 30% of infants with PNEs were taking unnecessary AEDs. To prevent misdiagnosis of epilepsy and unnecessary AED treatment, abnormal paroxysmal behaviors in infants should be diagnosed with caution. Whenever the diagnosis of PNEs or epileptic seizures is uncertain, long-term video-EEG monitoring should be performed. In conclusion, PNEs in younger pediatric patients were not different from previous studies. However, younger patients presented with shorter disease duration and more various types of PNEs compared to older patients. The presence of concurrent epilepsy was not related to the difference in clinical characteristics of PNEs. However, the presence of developmental delay was related to specific types of PNEs. Staring and tonic posturing were more frequently observed in patients with PNEs and developmental delay, and this finding was statistically significant. Misdiagnosis of epilepsy and unnecessary AED treatment were more frequent in patients with developmental delay and epileptiform discharges in an EEG. Infants were also frequently misdiagnosed with epilepsy. Pediatric neurologists must not misdiagnose PNEs as epileptic seizures, especially in patients with developmental delay or in younger patients. Whenever the diagnosis is uncertain, careful examination and verification with other tests, especially long-term video-EEG monitoring, must be done. Although the long-term video-EEG is very useful in the diagnosis of PNEs, an accurate diagnosis of PNE and the specific etiologic diagnosis of PNE may still be challenging. This is a retrospective observational analysis, so the findings in this study must be verified in prospective studies. Acknowledgments The authors are grateful to Mrs. MiSun Park for her help in preparing the manuscript. References [1] Reuber M. Psychogenic nonepileptic seizures: answers and questions. Epilepsy Behav 2008;12:622–35. [2] Brown RJ, Syed TU, Benbadis S, Lafrance Jr WC, Reuber M. Psychogenic nonepileptic seizures. Epilepsy Behav 2011;22:85–93. [3] Mari F, Di Bonaventura C, Vanacore N, et al. Video-EEG study of psychogenic nonepileptic seizures: differential characteristics in patients with and without epilepsy. Epilepsia 2006;47(Suppl. 5):64–7. [4] Abubakr A, Kablinger A, Caldito G. Psychogenic seizures: clinical features and psychological analysis. Epilepsy Behav 2003;4:241–5. [5] Benbadis SR, Allen Hauser W. An estimate of the prevalence of psychogenic nonepileptic seizures. Seizure 2000;9:280–1. [6] Patel H, Scott E, Dunn D, Garg B. Nonepileptic seizures in children. Epilepsia 2007;48:2086–92. [7] Wyllie E, Glazer JP, Benbadis S, Kotagal P, Wolgamuth B. Psychiatric features of children and adolescents with pseudoseizures. Arch Pediatr Adolesc Med 1999;153:244–8. [8] Vincentiis S, Valente KD, Thome-Souza S, Kuczinsky E, Fiore LA, Negrao N. Risk factors for psychogenic nonepileptic seizures in children and adolescents with epilepsy. Epilepsy Behav 2006;8:294–8. [9] Kutluay E, Selwa L, Minecan D, Edwards J, Beydoun A. Nonepileptic paroxysmal events in a pediatric population. Epilepsy Behav 2010;17:272–5. [10] Benbadis SR, Agrawal V, Tatum WO. How many patients with psychogenic nonepileptic seizures also have epilepsy? Neurology 2001;57:915–7. [11] Reuber M, Elger CE. Psychogenic nonepileptic seizures: review and update. Epilepsy Behav 2003;4:205–16. [12] Asano E, Pawlak C, Shah A, et al. The diagnostic value of initial video-EEG monitoring in children—review of 1000 cases. Epilepsy Res 2005;66:129–35. [13] Pierelli F, Chatrian GE, Erdly WW, Swanson PD. Long-term EEG-video-audio monitoring: detection of partial epileptic seizures and psychogenic episodes by 24hour EEG record review. Epilepsia 1989;30:513–23. [14] Wyllie E, Friedman D, Rothner AD, et al. Psychogenic seizures in children and adolescents: outcome after diagnosis by ictal video and electroencephalographic recording. Pediatrics 1990;85:480–4. [15] Reuber M, Fernandez G, Bauer J, Helmstaedter C, Elger CE. Diagnostic delay in psychogenic nonepileptic seizures. Neurology 2002;58:493–5. [16] Rosenow F, Wyllie E, Kotagal P, Mascha E, Wolgamuth BR, Hamer H. Staring spells in children: descriptive features distinguishing epileptic and nonepileptic events. J Pediatr 1998;133:660–3. [17] Shuper A, Mimouni M. Problems of differentiation between epilepsy and nonepileptic paroxysmal events in the first year of life. Arch Dis Child 1995;73:342–4. [18] Carmant L, Kramer U, Holmes GL, Mikati MA, Riviello JJ, Helmers SL. Differential diagnosis of staring spells in children: a video-EEG study. Pediatr Neurol 1996;14:199–202.
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