Comparison of semiologic characteristics of psychogenic nonepileptic seizures and frontal and temporal lobe seizures

Kubra Isik; Gulin Morkavuk; Burak Mete; Guray Koc

doi:10.4103/nsn.nsn_4_22

ORIGINAL ARTICLE

Year : 2022 | Volume : 39 | Issue : 3 | Page : 126-131

Comparison of semiologic characteristics of psychogenic nonepileptic seizures and frontal and temporal lobe seizures

Kubra Isik¹, Gulin Morkavuk¹, Burak Mete², Guray Koc³
¹ Department of Neurology, Faculty of Medicine, Ufuk University, Ankara, Turkey
² Department of Public Health, Faculty of Medicine, Cukurova University, Adana, Turkey
³ Department of Neurology, Ankara City Hospital, Ankara, Turkey

Date of Submission	10-Jan-2022
Date of Decision	06-May-2022
Date of Acceptance	08-May-2022
Date of Web Publication	30-Sep-2022

Correspondence Address:
Kubra Isik
Department of Neurology, Ufuk University Faculty of Medicine, Boulevard Mevlana (Konya Rd) 86-88 Balgat, Ankara 06520
Turkey

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/nsn.nsn_4_22

Abstract

Introduction: Video electroencephalography monitoring (VEM) is the gold standard for differentiating epileptic seizures and psychogenic nonepileptic seizures (PNES). This study aimed to compare the semiologic characteristics of PNES and frontal and temporal seizures. Materials and Methods: This study was conducted retrospectively on the records of patients aged over 18 years with PNES and frontal and temporal lobe seizures, who were followed up as inpatients in the Ufuk University Neurology Clinic VEM unit between 2016 and 2020. Seventy-two patients who met the study criteria and were hospitalized during this period were included in the study. The preictal, ictal, and postictal semiologic characteristics of the patients were examined and compared in terms of the seizure type. Results: Of the 72 patients included in the study, 29.2% had PNES, 15.3% had frontal lobe epilepsy, and 41.7% had temporal lobe epilepsy. The mean age of the patients was 32.74 ± 9.84 years. In patients with PNES, frequent semiologic changes, frequent medical visits, ability to execute commands, remembering test words, forced eye closure, subjective sensory symptoms, ictal crying, tremor in extremities, gradual onset, fluctuating course, postictal pseudo-sleep, pelvic thrusting movement, and arrhythmic synchronous extremity movement manifestations were determined to be significantly higher compared with frontal and temporal lobe epilepsies. Conclusion: Seizure semiology is important in the differential diagnosis of epileptic seizures and PNES. VEM remains the gold standard for differentiating PNES and epileptic seizures.

Keywords: Epilepsy, focal, psychogenic nonepileptic seizures, semiology, video electroencephalography monitoring

How to cite this article:
Isik K, Morkavuk G, Mete B, Koc G. Comparison of semiologic characteristics of psychogenic nonepileptic seizures and frontal and temporal lobe seizures. Neurol Sci Neurophysiol 2022;39:126-31

How to cite this URL:
Isik K, Morkavuk G, Mete B, Koc G. Comparison of semiologic characteristics of psychogenic nonepileptic seizures and frontal and temporal lobe seizures. Neurol Sci Neurophysiol [serial online] 2022 [cited 2023 May 29];39:126-31. Available from: http://www.nsnjournal.org/text.asp?2022/39/3/126/357502

Introduction

In the seizure classification, epileptic seizures are divided into three main categories: focal, generalized, and unclassifiable, and the incidence is slightly higher in favor of focal epilepsies.^[1],[2],[3] Psychogenic nonepileptic seizures (PNES) are a condition in which movements, sensory symptoms, and experiences, which resemble epilepsy and are not caused by abnormal neuronal discharges, occur in the brain.^[4] Nonepileptic seizures can have many different physiologic causes. These include syncope, transient ischemic attack, sleep disturbance, hypoglycemia, hyponatremia, and cardiac arrhythmia. The prevalence of PNES is estimated to be 2–33/100,000 in the general population.^[5] PNES seizures can also occur in patients with epilepsy, and this is a diagnostic problem. Epileptic seizures can be observed in 5%–40% of patients with PNES.^[6],[7] Patients with PNES are followed up for years with a misdiagnosis and receive antiepileptic medications, and it takes an average of 7–8 years to diagnose these patients.^[8] Considering these, it is vital to make a differential diagnosis of epileptic seizure and PNES. Video electroencephalography monitoring (VEM) is the gold standard for detailed semiologic identification of PNES and epileptic seizures.^[9] This study aimed to retrospectively examine patients hospitalized in the VEM unit and compare the semiologic characteristics of PNES and epileptic seizures (frontal and temporal).

Materials and Methods

This study was conducted retrospectively through the files and VEM records of patients aged over 18 years with PNES and frontal and temporal lobe seizures, who were hospitalized in the VEM unit of Ufuk University Neurology Clinic between 2016 and 2020. Patients aged between 18 and 60 years who were hospitalized in the VEM unit with PNES and frontal and temporal lobe seizures during this period were included in the study. Preictal, ictal, and postictal semiologic characteristics of the patients were examined and compared in terms of the seizure type. Patients aged under 18 or over 60 years, who had focal epileptic seizures or generalized epileptic seizures, except in the frontal and temporal regions, were excluded from the study.

Information sheets

Sociodemographic characteristics and disease history, including age, sex, marital status, presence of comorbid psychiatric illness, age at first seizure, witnessed a seizure, seizure characteristics (2-min long seizure, frequent semiologic change, sleep seizure), frequent physician visits, and the number of monthly seizures, were obtained from the patient files.

The VEM evaluations and records of the patients and hospitalization files were retrospectively reviewed, and seizure characteristics and vital signs were recorded. The investigated characteristics included duration of VEM hospitalization, number of seizures in VEM admission (PNES seizure number and number of epileptic seizures), mean seizure duration, seizures during sleep, and interictal electroencephalography (EEG) abnormality. Moreover, while monitoring heart rate video EEGs, simultaneous ECG recordings were also examined, and the ictal heart rate of the subjects was computed. The ictal respiratory rate was obtained retrospectively from the observation notes recorded at the time of the seizure.

Seizure typing is divided into four main groups: PNES, temporal seizures, frontal seizures, and PNES + epileptic seizures.

Cranial MRI findings were obtained from the hospital monitoring system or patient files. They were grouped based on the presence of abnormal findings

Regarding EEG findings, VEM records were reviewed retrospectively

Regarding semiologic characteristics, preictal, ictal, and postictal periods were reviewed from separate records, and existing findings were recorded in the predetermined semiologic manifestation form.

Statistical analysis

The Statistical Package for the Social Sciences for Windows, version 22.0 (IBM Corporation, Armonk, NY, USA) was used to perform the statistical analysis of the data. Nonparametric tests were used in the analysis of qualitative data, and parametric tests were used in the analysis of quantitative data. The Shapiro–Wilk test was used to determine whether variables conformed to normal distribution. The Chi-square test, binary logistic regression analysis, one-way analysis of variance, and Kruskal–Wallis test were used in the analysis. The results were considered significant at P < 0.05.

Results

Of the 72 patients included in the study, 29.2% had PNES, 15.3% had frontal seizures, and 41.7% had temporal lobe seizures. Forty-two (58.3%) of the patients were female and thirty (30.2%) were male. The mean age was 32.74 ± 9.84 (min: 18-max: 60) years. It was determined that there was no significant difference between females and males in terms of seizure types. In the interictal EEG, abnormal findings were found to be significantly higher in the temporal and frontal groups compared with the PNES group, and the presence of abnormal MR was more frequent among the temporal group compared with the PNES and frontal groups. In the PNES + epileptic group, the presence of abnormal MRI was found to be significantly more frequent than in the PNES group [Table 1].

Table 1: Comparison of patient characteristics by seizure type

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It was found that disease duration was significantly longer among those with frontal and temporal seizures compared with those with PNES, and the number of monthly seizures was significantly higher in the PNES group compared with the temporal group. It was determined that the number of PNES seizures during VEM hospitalization was significantly higher in the PNES group compared with the frontal and temporal groups [Table 2]. In post hoc analyses, disease duration was found to be 10.5 years longer in frontal seizures and 7.8 years in temporal seizures compared to PNES. In post hoc analyses, it was found that the number of monthly seizures was 11.3 times lower in the temporal group compared with PNES, the number of PNES seizures was 7.3 times higher in the PNES group compared with the temporal group, and 7.2 times higher than in the frontal group, whereas the number of epileptic seizures was 6.6 times lower in PNES compared with frontal seizures and 4.8 times lower compared with temporal seizures.

Table 2: Comparison of seizure characteristics by seizure type

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It was found that the findings of the ability to execute commands, recall test words, and a fluctuating course were significantly more common in the PNES group compared with the temporal and frontal groups, whereas foam and salivation coming from the mouth, and ictal Figure 4 sign findings were found to be significantly less frequent than in the frontal and temporal groups [Table 3]. It was detected that the findings of forced eye closure and subjective sensory symptoms, pelvic thrust, arrhythmic asynchronous extremity movement, ictal crying, and tremor in the extremities were significantly more frequent in the PNES group compared with the temporal group. Sudden-onset and postictal confusion findings were found to be significantly lower in the PNES group compared with the temporal, frontal, and PNES + epileptic groups [Table 3].

Table 3: Comparison of semiological characteristics by seizure type

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It was found in the forward conditional method analysis, which was established to estimate the risk of PNES by involving semiologic characteristics, that sudden-onset and gradual-onset variables contributed significantly to the model, whereas other semiologic characteristics did not contribute significantly to the model. Sudden onset of seizures reduces the risk of PNES by 29.4 times, whereas gradual onset increases the risk of PNES by 29.2 times [Table 4] and [Figure 1].

Table 4: Psychogenic nonepileptic seizures risk logistic regression analysis (forward conditional method)

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Figure 1: Risk factors for PNES. PNES: Psychogenic nonepileptic seizures

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Discussion

PNES is a self-limiting event characterized by abnormal movements or paroxysmal shifts in behavior. They may resemble epileptic seizures but do not have a neurobiologic origin like that of epileptic seizures. They are not associated with electrophysiologic epileptiform discharges, and they are often associated with psychological disorders.^[10]

In this study, in the interictal EEG, abnormal findings were found to be significantly more frequent in the temporal and frontal groups compared with the PNES group. It was found that the disease duration was significantly longer among those with frontal and temporal seizures compared with those with PNES, and the number of monthly seizures was significantly higher in the PNES group compared with the temporal group. It was determined that the number of PNES seizures was significantly higher in the PNES group compared with the frontal and temporal groups, whereas epileptic seizures were less frequent. It was found that being able to execute commands, recalling test words, and a fluctuating course was significantly more common in the PNES group compared with the temporal and frontal groups, whereas foam coming from the mouth and salivation, and ictal Figure 4 sign findings were significantly less frequent than in the frontal and temporal groups. It was detected that forced eye closure and subjective sensory symptoms, pelvic thrust, arrhythmic asynchronous extremity movement, ictal crying, and tremor in the extremities were significantly higher in the PNES group compared with the temporal group. Sudden-onset and postictal confusion findings were found to be significantly less common in the PNES group compared with the temporal, frontal, and PNES + epileptic groups. Sudden onset of seizures reduces the risk of PNES by 29.4 times, whereas gradual onset increases the risk of PNES by 29.2 times.

In the study of LaFrance and Benbadis in which the differentiation of frontal lobe epilepsy from psychogenic nonepileptic seizures was investigated, VEM images of PNES and frontal lobe epilepsy were analyzed and their semiologic characteristics were assessed. In the study, the significance of VEM in the differentiation of semiologic characteristics for seizures was underscored.^[11] In our study, temporal and frontal epileptic seizures and PNES were compared in terms of semiologic characteristics. It was found that disease duration was significantly longer in frontal and temporal seizures compared with PNES, and the number of monthly seizures was significantly higher in the PNES group compared with the temporal group. In the study of Myers et al., based on the VEM results, the number of monthly seizures was determined to be significantly higher in the PNES group compared with the frontal and temporal groups.^[12] Comorbid psychiatric disorder is common among patients with PNES. In the study of Turner et al., all patients with PNES had a comorbid psychiatric disorder, and this rate was found as 50% in patients with epilepsy.^[13] In the study of Myers et al., personal and familial psychiatric history rates were much lower among young people with epilepsy, and it was found that all 15 young people with PNES and more than half of their families had comorbid psychiatric disorders.^[12] In our study, a history of comorbid psychiatric disorder was found to be significantly higher among patients with PNES compared with the other groups.

In the study of Ozer et al., in which the semiologic characteristics of patients with PNES and epilepsy were compared, preictal pseudo sleep, facial motor activity, eye closure, resistance to opening eyes, fist posturing in both hands, postictal pseudo sleep, seizures longer than 2 min, asynchronous extremity movement, and opisthotonos symptoms were detected to be more common in the epilepsy group.^[14] On the other hand, in our study, the ability to perform commands, recall test words, fluctuating course, and pseudo sleep were found to be significantly more frequent in the PNES group than in all groups, and gradual onset increased the risk of PNES 29.2 times. Frontal lobe seizures and PNES were compared by Saygı et al., and the similarities of the semiologic characteristics of the seizures were highlighted. Returning to the prone position during the seizure was determined to be more frequent only in frontal seizures. Nocturnal seizures, short ictal duration, younger age of onset, stereotypical movement patterns, magnetic resonance imaging, and EEG abnormalities suggested more frontal seizures.^[15] In our study, a longer duration of disease, sudden-onset, interictal abnormality, and bipedal automatism findings were found to be significantly more common in frontal seizures compared with PNES. Pelvic thrust and asynchronous extremity movement are common in PNES and frontal lobe seizures, whereas they are rare in the temporal group.^[16],[17] In our study, it was found that the findings of forced eye closure and subjective sensory symptoms, pelvic thrust, arrhythmic asynchronous extremity movement, ictal crying, and tremor in the extremities were significantly more frequent in the PNES group compared with the temporal group. Forced eye deviation, right/left versive head movement, ictal screaming, respiratory and heart rate variations, dystonic posturing, cyanosis, and bimanual automatism were determined to be significantly less common in the PNES group compared with the temporal group.

For a long time, it was considered that physical injury during ictus occurred only in patients with epilepsy. However, research shows that more than 50% of patients with PNES are injured during seizures. The character of the injury helps differentiate epileptic seizures from PNES.^[18],[19] It was found in our study that lateral tongue biting occurred in epileptic seizures, whereas biting at the tip of the tongue occurred in PNES, supporting previous studies. In other studies, it has been revealed that patients with PNES may also exhibit geotropic eye movements, in which the eyes shift downward to the side of the head. The eyelids are typically closed for a longer period (20 s) in PNES compared with temporal lobe epilepsy or frontal lobe epilepsy. Crying is a common characteristic of PNES.^{[20],[21],[22],[23]} Ictal stuttering and postictal whispering voice are findings in PNES.^[24] In our study, no difference was found between patients with PNES and those with epilepsy in terms of ictal and postictal speech, whereas ictal crying was a more common semiologic characteristic in PNES. In the logistic regression analysis, which was established to estimate the risk of PNES by involving the semiologic characteristics, sudden onset of seizure reduced the risk of PNES by 29.4 times, whereas the gradual onset increased the risk of PNES by 29.2 times.

The limited sample size, retrospective nature of the study, and lack of follow-up or treatment data were considered limitations of the study.

Conclusion

Based on the results of this study, it was found that there were semiologic differences between PNES and epileptic seizures. It was determined that ictal semiologic characteristics varied depending on the seizure types. The presence of frequent semiologic changes, frequent visits to a physician, comorbid psychiatric disease, ability to execute commands, recall test words, forced eye closure, subjective sensory symptoms, ictal crying, tremor in extremities, gradual onset, fluctuating course, postictal pseudo sleep, pelvic thrusting movement, and arrhythmic asynchronous extremity movements were found to mostly favor PNES. Challenges in diagnosing PNES can be tackled with a thorough identification of semiologic characteristics. VEM is a significant diagnostic tool in differentiating PNES and epileptic seizures.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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