Journal Pre-proof

Differential semiology based on VEEG monitoring between psychogenic non-epileptic

seizures and temporal lobe epileptic seizures

Nicolás Lombardi, Laura Scévola, Mercedes Sarudiansky, Brenda Giagante, Angel

Gargiulo, Nicolás Alonso, Ernesto Gonzalez Stivala, Silvia Oddo, Mónica Fernandez-
Lima, Silvia Kochen, Korman Guido, Luciana D’Alessio
PII: S0033-3182(20)30212-7
DOI: https://doi.org/10.1016/j.psym.2020.07.003
Reference: PSYM 1154

To appear in: Psychosomatics

Received Date: 15 April 2020

Revised Date: 11 July 2020
Accepted Date: 13 July 2020

Please cite this article as: Lombardi N, Scévola L, Sarudiansky M, Giagante B, Gargiulo A, Alonso N,
Stivala EG, Oddo S, Fernandez-Lima M, Kochen S, Guido K, D’Alessio L, Differential semiology based
on VEEG monitoring between psychogenic non-epileptic seizures and temporal lobe epileptic seizures,
Psychosomatics (2020), doi: https://doi.org/10.1016/j.psym.2020.07.003.

This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition
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© 2020 Academy of Consultation-Liaison Psychiatry. Published by Elsevier Inc. All rights reserved.
Differential semiology based on VEEG monitoring between psychogenic non-
epileptic seizures and temporal lobe epileptic seizures

Nicolás Lombardi1, Laura Scévola1, Mercedes Sarudiansky 1,3, Brenda Giagante 1,4, Angel Gargiulo1, Nicolás
Alonso1, Ernesto Gonzalez Stivala1,2, Silvia Oddo 1,4, Mónica Fernandez-Lima1,4, Silvia Kochen1,4, Korman
Guido1,3 , Luciana D’Alessio 1,2.

1. Universidad de Buenos Aires, Hospital Ramos Mejía, Centro de Epilepsia, Buenos Aires, Argentina.

2. Universidad de Buenos Aires, IBCN-CONICET, Buenos Aires, Argentina.

3. Universidad de Buenos Aires, CAEA-CONICET, Buenos Aires, Argentina.

4. Hospital El Cruce Hospital, Centro de Epilepsia, ENyS-CONICET, Buenos Aires, Argentina.

Corresponding author:

Luciana D´Alessio

Universidad de Buenos Aires, IBCN-CONICET (Cell Biology and Neuroscience Institute-National Scientific and
Technical Research Council), Buenos Aires Argentina.
Paraguay 2155 (C1121ABG), 3th Floor. Phone Number: 0054-11-59509500. Email: luladalessio@gmail.com,
lucianad@conicet.gov.ar

Abstract

Introduction

Psychogenic non-epileptic seizures (PNES) are disruptive changes in behavior without ictal correlate of
epileptic activity and high prevalence of psychiatric morbidity. Differential diagnosis is difficult particularly
with TLE (temporal lobe epilepsy), which is also associated with high prevalence of psychiatric comorbidity.
Although Video-EEG (VEEG) is the gold standard for differential diagnosis, clinical semiology analysis may
help the clinician in general medical practice. In this study the differential semiology based on VEEG,
between PNES and TLE seizures was analysed.

Methods

The VEEG of patients with diagnosis of PNES and TLE were reviewed and compared between groups.
Clinical semiology of all episodes recorded by VEEG in each patient was analyzed and classified according to

1
the presence of: behavioral arrest, motor hyperkinetic activity, impaired awareness, aura and automatisms. Chi
square test and binary logistic regression were determined.

Results

Thirty-two patients with PNES (32 ±11 years) and 34 with TLE (32 ±12 years) were included. Female patients
were predominant in PNES group (p<0.05). Mean time duration of episodes was 6,8 ±10 minutes in PNES and
1,6±0,8 minutes in TLE (p<0.05). Impaired awareness (OR= 24.4, CI 95% 3.79-157.3, p<0.01), automatisms
(OR= 13.9 CI, 95% 2.1-90.5, p<0.01) and shorter duration of the events (OR = 2.261, CI 95% 1.149- 4.449,
p=0.018), were found as independent factors for detecting TLE seizures comparing PNES.

Conclusion

Clinical semiology analysis may orientate the differential diagnosis in general medical practice, between
PNES and TLE seizures. Further studies comparing PNES semiology with other subtypes of epilepsies may
complete these preliminary findings.

Key Words: clinical semiology, automatisms, impaired awareness, differential diagnosis, psychiatric
disorders.

1. Introduction

Psychogenic non-epileptic seizures (PNES) are diagnosed when disruptive changes in behavior, thinking or
emotion, that resemble epileptic seizures (ES), are present without any ictal correlate of epileptogenic brain
activity. Usually PNES represent an underlying psychiatric disorder, classified in Axis I of DSM-IV as
conversion disorder and/or dissociative disorder. More recently, DSM-5 categorized PNES as a functional
neurological disorder (1–5). Psychogenic factors like sexual abuse, trauma and posttraumatic stress disorder
(PTSD) have been associated with PNES occurrence (6,7).

PNES accounts for approximately 20-30% of patients referred to epilepsy centers with suspicion of resistant
epilepsy (1,5). Additionally, an important delay in the recognition of PNES, between seven to eleven years, has
been reported in the international literature and also in previous studies performed by our group (1,4,8,9). The
diagnostic delay could be in part accounted by difficulties in accessing VEEG (Video-
electroencephalography), the gold standard to achieve PNES diagnosis. This is possibly related to both
economic and availability factors; indeed, only a limited number of specialized centers have access to these
diagnostic tools. Diagnostic delay implies unnecessary exposure to antiepileptic drugs and, in turn, a
postponement of the appropriate treatment implementation (psychiatric treatment and psychotherapy) (8,10–12).

PNES are frequently confused with epileptic seizures, particularly with TLE (temporal lobe epilepsy), which
is the most frequent subtype of epilepsy and is also frequently associated with psychiatric comorbidity,
making differential diagnoses even more complex (4,13). Although VEEG is the gold standard method in
establishing differential diagnosis between PNES events and epileptic seizures (14,15), descriptive semiology

2
may help in patients with suspected PNES in general hospitals, in epilepsy units and/or in mental health
departments. Several studies analysed the clinical features of PNES semiology (16,17) but only a few studies
compared specifically the subtypes of epilepsies with PNES semiology (1,18,19). In a previous study performed
by our group, we analysed the presence of psychiatric disorders in patients with PNES and in patients with
drug resistant epilepsy, finding a high prevalence of depression in both groups while trauma and post-
traumatic stress disorder were more frequent in PNES patients (4). In the present study we aim to compare the
clinical semiology detected during VEEG monitoring between PNES and TLE.

2. Material and methods

2.1. Patient selection

The VEEG records of a selected subgroup of patients with a confirmed diagnosis of PNES or TLE, which
were, completed all the mental health protocol and signed the informed consent, were retrospectively
reviewed. Selected patients were admitted to the VEEG unit of Ramos Mejía Epilepsy Center. In the PNES
group patients were admitted to the VEEG from 2006 until 2016 and some of them (n=14) were included in a
previous study about psychiatric aspects of PNES (4). In the TLE group patients were admitted from 2012 until
2015 and some of them (n=16) were included in a previous study about the quality of life of patients with drug
resistant epilepsy (2). Thus, the number of patients included in this exploratory study does not reflect the
prevalence of PNES or TLE among the total population admitted to the VEEG unit. The approval of the Ethics
Committee of Ramos Mejía Hospital was obtained to conduct the study in accordance with the ethical
standards established in the 1964 Declaration of Helsinki.

2.2 Diagnosis of PNES events and TLE seizures: Inclusion and exclusion criteria

All patients included in this study underwent a medical assessment according to a standardized protocol
including clinical history, neurological evaluation, MRI and completed a psychiatric assessment protocol. The
diagnosis of PNES events and/or TLE was made by two epileptologists based on VEEG monitoring. The
diagnosis of PNES according to VEEG was complemented by the psychiatric evaluation to support the
psychogenic origin of PNES.
In this study two groups of patients were selected and grouped according the presence of PNES or TLE.
PNES events diagnostic criteria were: atypical paroxysmal behavioral episodes recorded by VEEG
monitoring, without any electroencephalographic ictal activity (at least one attack recorded) with no existing
clinical or electroencephalographic evidence suggestive of epilepsy; neither neurological nor medical disorder
that explains the atypical paroxysmal behavior (exclusion criteria). Patients were included in PNES group,
when at least one PNES event was recorded during VEEG. Exclusively patients with only PNES recorded
during VEEG in which the documented seizures were similar from their usual and current episodes were
included in this group.
Temporal lobe epileptic seizures diagnostic criteria were: characteristic clinical events recorded with
simultaneous ictal EEG abnormalities during VEEG localized in temporal lobe. The subtype of epileptic
syndrome was diagnosed according to ILAE nomenclature guidelines (20,21) and temporal lobe epilepsy was

3
diagnosed according to clinical semiology and ictal VEEG results (20,21). Patients were included in TLE group,
when at least one TLE event was recorded during VEEG. Exclusively patients with only TLE events recorded
in VEEG were included in this group.

Exclusion criteria were: Patients with both types of seizures (PNES and epileptic seizures) registered during
VEEG were excluded. Additionally, patients with doubts about epileptogenic zone or patients with other
subtype of epilepsy registered during VEEG were excluded of the group of TLE. Patients who did not
complete all diagnostic steps, paroxysmal events of other medical aetiology, (e.g., transient ischemic attacks,
vasovagal syncope, sleep disorders and non-epileptic myoclonus), and patients who did not sign the informed
consent were also excluded. If the documented seizures differed from their usual episodes, and patients with
purely subjective phenomena during the events were excluded from the study.

2.3 Video-Electroencephalography (VEEG)

For VEEG monitoring (5 days period), a Stellate-Bioscience EEG machine at a 200-Hz sample rate was used.
All ictal recordings were obtained using the international 10–20 system with the addition of temporal
electrodes of the 10–10 system. Referential montages as well as longitudinal–bipolar and transverse bipolar
montages were used for the analysis. VEEG is usually indicated in order to determine the possibility of
epilepsy surgery and/or to confirm the differential diagnosis between epilepsy and PNES. A routine practice
during the ictal and post-ictal period includes systematic patient assessment performed by qualified technical
staff and, at the same time, patients are instructed to promptly advise the staff whenever they experience an
aura. For the purpose of this study, all video-EEG recordings were retrospectively reviewed by three qualified
readers, trained and experienced in video-EEG interpretation. Seizure onset was defined as the first electrical
change seen in the EEG rhythm as compared to baseline or at any clinical sign or symptom indicating seizure
onset.

2.4 Psychiatric assessment

Psychiatric assessment protocol was performed by 2 trained psychiatrist based on a standardized protocol
previously applied in our population in other studies (1,). Psychiatric history was obtained. All patients
underwent the Structured Clinical Interview for DSM IV Axis I disorders (SCID I), a semi-structured
interview for major DSM IV Axis I diagnoses and the SCID II, which is a semis-structured interview for DSM
IV Axis II personality disorder diagnoses (Spanish Clinical Version of SCID I and SCID II). Patients with
mental disabilities were excluded from the psychiatric data analysis.

2.5 Magnetic Resonance Imaging

(22).
All patients had magnetic resonance imaging (MRI) 3T, with a temporal lobe epilepsy protocol The
sequences used were the following: Sagittal plane T1-weighted image for the purpose of detecting the
hippocampus in the parasagittal slices; inversion-recovery (IR) pulse sequence, fluid- attenuated IR (FLAIR),
and three-dimensional gradient echo sequence (volumetric), perpendicular to the long axis of the
hippocampus, and T2-weighted axial sequence parallel to the long axis of the hippocampus.

4
2.6 Semiological analysis of PNES events and TLE seizures recorded during VEEG

The VEEGs of patients included in this study were reviewed, and all the episodes of PNES and TLE recorded
in each group of patients were examined and classified depending on the presence of the following signs and
symptoms (1). 1- Behavioral arrest: detention of activities, immobility and/or freezing (20,23). 2-
Motor/Hyperkinetic activity: active movements of fluctuating intensity involving the limbs, head and trunk
(13,25-27). 3- Impaired awareness: this was considered when the patient did not contact (i.e eye contact), listen,
neither answer, nor remember during all the episode’s duration since the beginning of the seizure (after aura)
until the end. Fluctuations of awareness during the episode were not considered total impaired awareness
(1,20,23). 4- Presence of aura: we included subjective symptoms and/or sings when they were clearly
manifested before seizures started. We included somatic aura, presence of clinical symptoms (pain, autonomic
symptoms, headache, dizziness, etc.), sensorial aura (different types of hallucinations or illusions) and psychic
aura (psychological symptoms such as anxiety, fear, other emotions, etc.) (1,20,23). 5- Presence of
automatisms: a coordinated, repetitive and stereotyped motor activity, affecting facial and/or distal movements
(20,23).

2.7. Statistical analysis

All the variables studied were compared between groups. Chi-square test and binary logistic regression were
determined to compare clinical semiology between patients with TLE and PNES (p<0.05 was considered
significant). Two-tailed Student t test was used for continuous data. SPSS for Windows was used.

3. Results

In this study we included 32 patients with PNES (women n=26, men n=6; mean age= 32±11) and 34 patients
with TLE (women=16, men=18; mean age=32±12). Sociodemographic and clinical data is summarized in
Table 1. A higher prevalence of female sex and a higher age of onset were found in PNES group comparing to
TLE group (p<0.05).

The presence of aura, behavioral arrest, automatisms and impaired awareness, were significantly more
frequent in TLE group, compared to PNES (Chi Square test, p<0.05). On the contrary, hyperkinetic seizures
and the absence of impaired awareness were more frequently found in the PNES group (Chi Square test,
p<0.05 (Figure 1). Mean seizure duration of episodes was 1.72±0.9 minutes in TLE group and 3.98±3.1
minutes in PNES group (p<0.001)(Figure 2).

According to logistic regression analysis, impaired awareness (OR= 0.050, CI 95% 0.004-0.6343, p=0.021),
the presence of automatisms (OR= 0.032, CI 95% 0.003-0.306, p=0.003) and the shorter duration (OR =
2.261, CI 95% 1.149- 4.449, p=0.018), were found as independent factors for detecting TLE compared to
PNES (Table 2).

4. Discussion

5
In this study we examined and compared the frequency of presentation of the main semiological sings detected
during VEEG, between PNES and TLE seizures (1,9). The semiological classification used in this analysis was
restricted to a limited number of specific semiological signs, usually described in epileptic seizures and
previously reported by our group (1). However other broader semiological stereotyped classifications were
proposed in the literature to describe PNES in detail (26–29). Nevertheless, in this preliminary study we focused
on TLE (a very frequent syndrome among patients with resistant epilepsy admitted to epilepsy centres), which
is also frequently associated with psychiatric comorbidity, making differential diagnoses even more difficult
(26–28). In this analysis, we used common linguae to neurologists for describing seizures, with the aim to
improve the communication between neurologists and psychiatrists, enhancing a prompt diagnosis. This also
may provide standardization across future studies that compare epileptic seizures versus PNES.

According to the literature (1,8) the 20-30% of patients referred to epilepsy centers with suspicion of resistant
epilepsy, have PNES; so semiological data may be crucial to speed up the differential diagnosis. In the present
study we found differences in TLE semiology comparing with PNES events. The presence of automatisms
was found an independent factor for differentiating TLE from PNES. Although automatisms are widely
described phenomena in TLE, it is interesting to point out, that in this study the presence of automatisms
allowed us to strongly differentiate TLE from PNES. Other publications obtained a similar results, finding that
automatisms, referred as “focal signs”, “minor motor seizures”(26,27), are less frequent in PNES (1,17,30,31) and
predominate in TLE seizures (20,32). Nevertheless, these studies did not compare the clinical semiology of
PNES specifically with TLE.

Total impaired awareness during all the episode’s duration was also found as an independent factor, according
to logistic regression, and constitutes as a useful clinical manifestation for differentiating TLE seizures from
PNES. Similar to our results, consciousness alterations have been previously reported as a key clinical feature
for TLE diagnosis (20,32,33). Additionally, other publications and previous reports published by our group (1),
found that impaired awareness was less frequently in PNES compared to epileptic seizures (25,26). However, as
far as our knowledge, there is no data available about comparisons between PNES and TLE regarding
semiological aspects.

Other semiological signs such as hyperkinetic seizures were more frequently found among PNES patients.
Nevertheless, in this study we did not distinguished between different subtypes of hyperkinetic seizures.
Similar to our results, other studies found that hyperkinetic seizures, also named in the literature as “motor
seizures” or “hypermotor seizures”(27) are characteristic of PNES (1,3,17,19,27,31,34). Still, hyperkinetic seizures
are also frequently described among frontal epilepsies, which have been not analysed in this preliminary study
(35). On the other side, behavioral arrest, also described in the literature as “psychogenic atonic seizures”,
“dialeptic” or “pseudosyncope” (27), was more frequently found in TLE patients in this study. Similarly, other
reports described behavioral arrest as a common sing of epileptic seizures (20), especially TLE seizures (32).
This clinical manifestation seemed to be rarely found in PNES (1,3,17,19,31,34). Regarding aura, it was more
frequently found in TLE seizures. The presence of aura is classically described in TLE seizure semiology
(20,32,33), and not so frequently described in PNES (1,3,17,19,31,34).

6
A classical sign which has been considered an important semiology factor useful for differentiation PNES
versus epileptic seizures, is the time duration of the events (1,3,17,19,32,36). In agreement with the literature we
found a significant higher duration of seizures among PNES patients compared with TLE. We also found that
patients with TLE seizures presented a significantly younger seizures’ age of onset in comparison to PNES,
similarly to other studies (17,19,30,32–34). Additionally, we found an over representation of female in PNES group
(1,3,17,19,36,37).

In this study we found semiological signs that could help the clinicians to differential diagnosis between PNES
and TLE. PNES diagnostic delay in Latin America, particularly in Argentina, is very high, ranging between 7
to 11 years (1,4). Although, other international studies also reported a high diagnosis delay, similar to ours, but,
in our country we have to additionally consider the difficulties in accessing to VEEG (8,38,39). This is possibly
related to both economic and availability factors. Besides, only a limited number of specialized centers in the
whole country have access to this diagnostic tool. Additionally, the misdiagnosis in clinical practice is
bidirectional, PNES may be confused with epilepsy and epilepsy (i.e TLE), may be confused with PNES.
According to this study, the presence of impaired awareness, automatisms and a shorter duration, are
suggestive of TLE comparing PNES, reinforcing the idea of epileptic origin. On the contrary, longer duration
of the events may be considered as independent factor for diagnosis PNES.

Some limitations of this study must be mentioned; this is a small and exploratory study, which compared the
clinical semiology between PNES and TLE. We found differences on TLE patients useful to differentiate from
PNES but larger studies, using more detailed classifications and including other subtypes of epilepsies (i.e
frontal epilepsy), should be made in the future to find clinical differences in PNES to differentiate from
epilepsy. As well as VEEG is the gold standard for differential diagnosis, clinical semiology may help the
clinician (neurologists and psychiatrists) in differential diagnosis, may reduce the diagnosis delay time and
may accelerate a correct treatment instauration. In PNES patients psychiatric treatment and psychotherapy is
the treatment of choice, and an early differential diagnosis may help in reducing the risks of unnecessary
antiepileptic drugs use.

5. Conclusion

In this preliminary study we found semiological signs that may orientate the differential diagnosis between
PNES and TLE. The presence of automatisms, impaired awareness and a shorter duration of the events were
more frequently found in TLE, comparing to PNES. Clinical semiology information constitutes a useful tool
for differential diagnosis between TLE and PNES and may help neurologists and mental health professionals
(psychiatrists, psychologists), to differentiate PNES from TLE seizures, and also to consider an early request
of VEEG. Further studies comparing PNES semiology with other subtypes of epilepsies using large and
detailed classifications will complete these preliminary findings.

Disclosures

The authors do not declare any conflict of interest.

Acknowledgments
7
We thank all participants of the study and all the team of Epilepsy Center of Ramos Mejía Hospital and El
Cruce Hospital.

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10
Table 1. Demographic Data

TLE PNES p value

Female 16 26
0.004
Male 18 6

Age (years) 32(±12years) 32(±11years) 0.872

Age of Seizures’ Onset 13(±9years) 19(±11years) 0.012

Occupation

Unemployed 51.6% 27.3%

Underemployed 29.0% 45.5%

0.531
Active Work 9.7% 13.6%

Student 3.2% 4.5%

Disability Pension 6.5% 9.1%

Civil Status

Single 56.3% 44.4%

0.489
Married/Couple 40.6% 55.6%

Divorced 3.1% --

Location

Buenos Aires City 18.5% 38.1%

Great Buenos Aires 33.3% 33.3% 0.336

Buenos Aires Province 14.8% 14.3%

Rest of the Country 33.3% 35.0%

Education

Less than 12 years 44.4% 41.2% 0.831

More than 12 years 55.6% 58.8%

 Table 2. Logistic regression analysis of semiological symptoms recorded during VEEG

Odds Ratio 95% CI for Odds Ratio p value

Automatisms 0.050 0.004 - 0.634 0.021

Impaired Awareness 0.032 0.003 - 0.306 0.003

Mean time duration (minutes) 2.261 1.149 - 4.449 0.018

Aura 0.916 0.035-23.80 0.958

Hyperkinetic 2.571 0.169-39.00 0.496

Behavioral Arrest 0.224 0.027-1.857 0.166

Results of the logistic regression analysis, clinical semiology between TLE seizures and PNES events
were compared. The presence of automatisms, the impaired awareness ant the shorter time duration,
was found as independent factors for detecting TLE compared to PNES.