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Regional paroxysmal fast rhythms on scalp EEG: an
observational study
Reyhan Sürmeli1 , Hatice Kurucu2 , Seher Naz Yeni2 , Ahmet Veysi Demirbilek2
1Clinic of Neurology, University of Health Sciences, Ümraniye Training and Research Hospital, İstanbul, Turkey 2Department of Neurology, İstanbul University-Cerrahpaşa, Cerrahpaşa School of Medicine, İstanbul, Turkey
Corresponding Author: Reyhan Sürmeli E-mail: reyhansurmeli@gmail.com Submitted: 22 February 2019 Accepted: 27 June 2019
You may cite this article as: Sürmeli R, Kurucu H, Yeni SN, Demirbilek AV. Regional paroxysmal fast rhythms on scalp EEG: an observational study.
Neurol Sci Neurophysiol 2019; 36(3): 158-66.
Abstract
Objective: It is known that interictal regional paroxysmal fast activity (RPFA) on scalp electroencephalogram (EEG) is seen in
patients with focal cortical dysplasia. We aim to investigate these activities and to understand their correlation with structural lesions on magnetic resonance imaging (MRI) and other interictal epileptiform activities on scalp EEG.
Methods: We searched the prevalence of RPFA in video EEG monitorized epilepsy patients between 2012-2016 years. An
addi-tional group of patients were also added to the cohort from routine EEG recordings in order to make correlations of RPFA’s with the accompanying EEG features and structural lesions on MRI. RPFA was defined as frequencies above 10 Hz, on 2-5 consecutive electrodes and short lasting.
Results: A total of 250 patients were screened retrospectively. The prevalence of RPFA was 5.6% (14 patients). The total group
consisted of 19 patients. The frequencies of RPFA were between 35 Hz (mean 26.21) and the amplitudes were between 20-52 µV (mean 30.84). The duration of RPFA vary between 200-770 milisecond (mean 293.42). All patients but one had epilepsy. Nine patients had abnormal MRI. The MRI lesion and location of RPFA were concordant in three patients. Fifteen patients had also focal sharp/spike activities which were concordant with the localization of RPFA in 13 patients. Ictal activity was available in thirteen patients. The localization of the onset of ictal activities of these patients were found to be concordant with the location of RPFA in 5 patients.
Conclusion: The prevalence of RPFA was 5.6%. RPFA was observed not only in patients with developmental lesions but also
encephalomalacic lesions. The concordance of RPFA with interictal, ictal EEG features and MR lesions was found moderate.
Keywords: Developmental lesion, electroencephalogram, encephalomalacic lesion, focal fast activity
INTRODUCTION
Epileptiform activities on scalp electroencephalogram (EEG) are defined as spikes, sharps and waves, polyspike and wave activities and temporal intermittent rhythmic delta activities (1). However, short lasting low amplitude focal fast rhythms are also observed on scalp EEG in the standard recordings in patients with epilepsy but the significance of these patterns are needed to be clarified and defined further. Until recently, their relevance to seizures, lesion types were not studied adequately, their significance has not been documented sufficiently. There are some published studies that indicate that interictal regional rhythmic polyspikes may be specific to focal cortical dysplasia (2). But the fast rhythms are not always in the form of polyspikes and therefore may not be accepted as equivalent. A novel article discussing the issue named these patterns as regional paroxysmal fast activity (RPFA) (3).
In this data collection, we searched for RPFA retrospectively first to define these activities, to find the prevalence and to understand their correlation with structural lesions on magnetic resonance imaging (MRI) and other interic-tal epileptiform activities on scalp EEG.
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METHODSDrug resistant epilepsy patients who were video EEG moni-tored with the indications of differential diagnosis, epilepsy surgery, or neuro-stimulation between January 2012-Decem-ber 2016 were screened for RPFA. All patients were filled with informed consent form.
During the study period, any EEG (from the routine EEG and video EEG monitoring laboratory) showing RPFA was also in-cluded to the study but this additional group was not includ-ed in the prevalence ratios.
The EEGs were interpreted by RS, NY and VD interviewed in case of any conflict. RPFA was defined as frequencies above 10 Hz, location; 2-5 consecutive electrodes (focal, regional) and which were discontinuous and intermittent, and short lasting (Figure 1). The devices used for video EEG monitoring (Medelec Nicolet v32 program of 32 channels), and for routine EEG (Nihon Kohden with 32 channels). We used 10-20 electrode montage system with additional electrodes if necessary in selected cases such as, T1/T2 or F9/10. EEG samples were evaluated visually using bipo-lar longitudinal, transverse and referential montages.
If interictal epileptiform acitivities were on the same elec-trode(s) with RPFA this is accepted as concordant. If any
electrode is intersecting, even though the covered area is not equal it is still accepted as concordant. The same is also ap-plied to ictal onset zone.
Cranial MRI were at least 1.5 tesla and were compatible with epilepsy protocols. The concordance criteria of MRI lesions with regard to RPFA was individualized as written in results section. 2017 International League Against Epilepsy’s seizure classifi-cation was used (4).
Statistical Analysis
Statistical analyses were performed with Statistical Package for the Social Sciences version 20 (SPSS IBM Corp.; Armonk, NY, USA). Descriptive statistical analyses of the patients were performed.
RESULTS
A total of 250 patients were screened retrospectively. The prevalence of RPFA was 5.6% (14 patients). Also, 5 additional cases were identified during the study period.
The frequencies of these rhythms were between 20-35 Hz (mean ± std. deviation: 26.21±4.65) and the amplitudes were between 20-52 µV (mean ± std. deviation: 30.84±8.21). The duration of RPFA varied between 200-770 milisecond (mean ± std. deviation: 293.42±126.93). The distribution of the RPFA varied from two electrodes to 5 electrodes (median: 2).
Figure 1. Interictal EEG examples of the RPFA on right F4-C4-Cz-Pz electrodes on a bipolar montage during sleep (RPFA activitiy is indicated
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Patient Age/Gender MRI Seizure type Treatment
1 38/F Corpus callosum splenium agenesis Focal onset,loss of awareness AED + VNS 2 10/M L diffuse, R frontal lobe encephalomalacia Tonic postural seizure , AED + VNS +
gelastic seizure Surgery (hemispherectomy) 3 18/M R MTS Atypical absence, GTC AED + VNS
4 25/M Asymmetric enlargement of the right Focal AED lateral ventricular temporal horn to BTC
5 26/M Left hemisphere atrophic left parietal Focal onset,loss of awareness, AED encephalomalacia and hippocampal gelastic seizure, FBTC
atrophy,right frontal craniotomy
6 24/M Left temporal encephalomalacia Focal onset, loss of awareness AED 7 32/F Bilateral temporo-occipital heterotopia Focal onset, loss of awareness AED 8 32/F Bilateral perisylvian schizencephaly Focal motor, FBTC AED 9 48/F Normal Focal to BTC AED 10 13/F Left temporo-occipital infarct sequeale, Focal to BTC AED 11 26/M Bilateral occipital perinatal lesions Tonic Postural, FBTC AED
12 11/M Basal ganglia and subcortical calcifications Generalized tonic and atypical AED + Surgery absence (corpus callosotomy) 13 15/M Left lateral periventricular heterotopia Asymmetric Tonic postural, AED + Surgery
and Corpus callosum agenesis FBTC (resective surgery) 14 5/F Not available Focal sensorial AED
15 36/M The right hippocampus is polipoid variant Focal to BTC AED 16 5/M Not available ADHD, no known seizures None 17 24/M Normal Focal to BTC None 18 25/F Normal Focal sensorial AED 19 18/F Normal Focal to GTC AED
BTC; bilateral tonic clonic seizure; FBTC; focal to bilateral tonic clonic seizure; GTC; generalized onset tonic clonic seizure; ADHD; attention deficit hyperactivity disorder; L; left; R; right; VNS: vagal nerve stimulation
Table 1. Clinical and radiological features of the patients
Patients Concordance for
(as shown Focal sharp/ Concordance for hemispheric
on table 1) spike activities Location of RPFA localization lateralization
1 FP1-F3-F7 T3-T5-T4-P4 NO YES
2 FP1-P3-T3-T5-F4 F4-FP2 D* D*
3 Generalized spike and waves F3-C3-P3 NO NO
4 T4 F8-T4 YES YES 5 F3-F4 FP2-F4 D* D* 6 F4-T4 F4-T4 YES YES 7 F7 FP1-F7-F3-C3-P3 YES YES 8 F4-C4 F4-C4-Cz-Pz YES YES 9 F7-T3 F7-P3 YES YES
10 F3-C3 Fp1-F3-C3-P3-O1 YES YES
11 F4 F8-C4 YES YES
12 F7-T3-F8-T4 (synchronous) T5-O1-T6_O2 (synchronous)
Generalized spike and waves T3-T5 NO NO
13 F9-T7 C3-F3 NO YES
14 O1 T5-O1 YES YES
15 P4-T6-O2 P4-T6-O2 YES YES
18 O1-O2 O1-O2 YES YES
19 F4 FP2-F4 YES YES
*D: needs discussion, these two cases need to be discussed further for epileptogenic zone and the epileptiform activities and RPFA and their concordance RPFA: regional paroxysmal fast activity
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Figure 2.a, b. Interictal EEG examples of the patient 14 during NREM II and III sleep. Left O1 spike acitivities (a), Interictal EEG examples of thepatient 14 during NREM II and III sleep. RPFA on the same electrode position (b) (RPFA activitiy is indicated by arrows. Sweep speed: 10 seconds/ page, sensitivity: 7 µV/mm, high frequency: 70 Hz, low frequency: 1,00 Hz, notch fitler: 50 Hz)
a
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Clinical Data of Patients with RPFA
Overall, 19 patients were identified as having RPFA (Table 1). Mean age was 22.8 years (5-48), and 9 were females. All patients but one had epilepsy and the onset age of seizures was 12.45 (1-34) years. Seizures were classified as focal seizures with or without loss of awareness in 10, focal to bilateral tonic clonic in 10 patients (some patients presented with two types of sei-zures). Two had atypical absences with additional seizures and were classified as having epileptic encephalopathies. One had
no known history of epilepsy rather had language retardation, attention deficit with hyperactivity syndrome (ADHD) and trig-onocephaly in examination additionally (Figure 2a, b).
Neurologic examination revealed mild to moderate men-tal retardation in 6 patients, two had autism. Four patients showed pyramidal signs on neurologic examination while one had visual field deficit. Six had a history of febrile seizures. One patient had language retardation and ADHD.
Figure 3.a, b. MRI of patient 2 who had perinatal hematoma and
surgery in the history. There is a diffuse encephalomalacia on left hemisphere but there is focal hyperintensity on right frontal lobe also (a) The EEG example of the same patient, showing left frontal (F3, C3) sharps but right frontal (F4) RPFA during sleep (b) (RPFA ac-tivitiy is indicated by arrows. Sweep speed: 30 mm/seconds, sensitiv-ity: 7 µV/mm, high frequency: 70 Hz, low frequency: 1,00 Hz, notch fitler: 50 Hz)
a
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Treatment responses; two patients were seizure free. One had no history of epilepsy. All the rest of the patients were resis-tant to treatment. Three had epilepsy surgery as a result of in-tractable seizures and were followed seizure free after surgery (Patient 2, 12, 13) (hemispherectomy, corpus callosotomy and lesionectomy) (Figure 3a, b). Three patients were applied va-gal nerve stimulation (Table 1).
Radiologic Data of Patients with RPFA
Nine patients had abnormal MRI while four patients normal. Four patients had some MRI/computed tomography (CT) features which the relevance to epilepsy was not clear (hippocampus was polipoid variant, agenesis of corpus callosum, ventricular asymmetry, calcifications on basal ganglia as a result of radia-tion therapy for leukemia). Two patients had no cranial MRI/CT
images. One patient has no epilepsy but language retardation, ADHD and the primary doctor has not suggested an MRI. The other patients' parents refused any further investigation. Three patients had developmental malformations; one had bilateral perisylvian schizencephaly, two had nodular hetere-topia, one bilateral, the other unilateral. Five had encephalo-malacic lesions, one had mesial temporal sclerosis.
The anatomic distribution of lesions were; one had diffuse hemi-spheric lesions with additional frontal damage on the other side (Figure 3a), one patient had lobar lesion, one had mesial tempo-ral sclerosis, four patients had lesions in two neighboring lobes (temporo-parietal, bi-occipital), bilateral perisylvian in one pa-tient, one had a heteretopia on lateral ventricule (Table 1).
Patients
(as shown Onset of the Location of Hemisphere
on table 1) ictal activities RPFA EEG Concordance lateralization
1 Left hemisphere T3-T5-T4-P4 NO YES 2 Right frontal F4-Fp2 YES YES 3 Generalized F3-C3-P3
5 Right frontal Fp2-F4 YES YES 6 Left temporal enchephalomalacia F4-T4 NO NO 7 Left fronto-temporal, posterotemporal Fp1-F3-C3-P3-F7 YES YES 8 Right hemisphere F4-C4-Cz-Pz NO YES 10 FP1-F7-F3-C3-P3 Fp1-F3-C3-P3-O1 YES YES 11 Non-lateralized and non-localized F8-C4 NO NO 12 Right frontal region T3-T5 NO NO
13 F9-TP7 C3-F3 NO YES
15 Non-lateralized and non-localized P4-T6-O2 NO NO 18 Right occipital region O1-O2 YES YES
RPFA: regional paroxysmal fast activity
Table 3. Correlation ofonset of ictal activities and localization of RPFA
Patients
(as shown Location of Hemisphere
on table 1) MRI lesion RPFA Concordance lateralization
2 Left hemisphere encephalomalacia, right F4-Fp2 * mesial frontal encephalomalacia
3 Right mesial temporal sclerosis F3-C3-P3 NO NO 5 Left parietal enchephalomalacia, hippocampal Fp2-F4 *
atrophy, right frontal craniotomy
6 Left temporal enchephalomalacia F4-T4 NO NO 7 Bilateral temporo-occipital heteretopia Fp1-F3-C3-P3-F7 NO NO 8 Bilateral perisylvian schizencephaly F4-C4 YES YES 10 Left temporo-occipital enchephalomalacia Fp1-F3-C3-P3-O1 YES YES 11 Bilateral occipital perinatal lesions F8-C4 NO NO 13 Left periventricular nodular heteretopia C3-F3 YES YES
*These two patients are discussed separately
RPFA: regional paroxysmal fast activity; MRI: magnetic resonance imaging
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RPFA with Regard to Sleep to Wakefulness Stage
Most of the regional paroxysmal fast activities (in 15 patients) were observed only during sleep EEG. In one patient, they were observed during both sleep and awake period, in three patients they were observed only during awake EEG.
Correlations of RPFA with Interictal and Ictal EEG Interictal EEG features other than RPFA
Fifteen patients had also focal sharp/spike activities. Two pa-tients presented with generalized spike, sharp slow waves (Table 2, patients 3,12). Two patients showed no other activity on EEG (Table 1, patients 16,17, Figure 4).
The localization of focal interictal epileptiform activities were concordant with the localization of RPFA in 13 patients (Figure 5) but not concordant in two. Sixteen patients were concor-dant for hemispheric lateralization.
Ictal EEG features
Thirteen patients had ictal EEG recordings. Four patients had no localized/lateralized onset of ictal activities on scalp EEG
recordings (Table 3). The localization of the onset of ictal ac-tivities were found to be concordant with the localization of RPFA in 5 patients. In 4 patients, RPFA and the onset of ictal activities were lateralized to the same hemisphere, but not lo-calized to the same electrodes. Ictal onset were more diffuse than RPFA.
Correlations of RPFA with the MRI Lesion
Nine patients presenting epileptogenic MRI lesions were cor-related for the localization of RPFA.
The MRI lesion and location of RPFA were concordant in three patients (Table 4). Two patients need to be discussed sepa-rately. Patient 2, had a left hemispherectomy later with sei-zure freedom. As seen on Table 2 and 3, the RPFA and some of the interictal epileptiform activities were observed on the contrary (right) side and later after hemispherectomy they disappeared. Patient 5 has also some contradictory findings; he had a past right frontal cranial surgery of an unknown reason. He had left hemispheric atrophy with left parietal en-cephalomalacia and left hippocampal atrophy but RPFA were
Figure 4. Patient 17 showing RPFA on O1-P3 electrodes during NREM sleep. The patient had no other epileptiform activities (RPFA activitiy is
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observed on the right frontal electrodes. His seizures seemed to originate from right frontal electrodes but he refused inva-sive EEG recording. Because of these reasons, we could not evaluate concordance of the MRI lesion and the location of RPFA in these two patients. For the rest of the 4 patients, there was no concordance.
DISCUSSION
Although many additional techniques were developed, EEG is still an essential tool in epilepsy practice. Epileptiform activi-ties are defined as spike, sharp waves, temporal intermittent rhythmic delta activity (3). But RPFA rhythms are also observed on scalp EEG and under recognized until recently. In this study the prevalence of RPFA was found to be 5.6% in a group of medically intractable heterogenous epilepsy population. This ratio is very low with regard to recent literature which gave a ratio of 22% (5). However Noachtar et al. found a similar ratio but we have not used their criteria for these rhythms. So, the criteria for regional fast rhythms are not clear enough and this may be the reason of such a great discrepancy between stud-ies (2). In this study, we visually identified these rhythms using a criteria which was not very strict; Any frequencies above 10 Hz and not continuous without identifying a duration limit and no strict criteria for amplitudes. Delta brushes may be mistaken with these activities. The delta wave of a delta brush
is up to 1.5 Hz with a lower threshold variously stated as 0.3 Hz (6-9). Their amplitudes are between 50-300 µV (9, 10). The fre-quency of the superimposed set of fast varies 8-20 Hz, usually on a steeply ascending slope (11). The characteristic features of delta brushes are mostly described in the neonatal period (12). Delta waves are the distinctive feature of delta brush ac-tivities when compared to RPFA.
After identifying these rhythms we analyzed the results and found that the frequency of RPFA was generally between 20-35 Hz (mean 26.21), the amplitudes were between 20-52 µV (mean 30.84) and the duration varied between 200-770 mil-liseconds (mean 293.42). They usually cover 2 electrodes but this may be up to 5 electrodes.
In this study and the recent published study the significance of RPFA rhythms were not correlated only with focal cortical dysplasia but also gliosis or encephalomalacic lesions (5). So, we can speculate that these rhythms may not be specific to underlying etiology.
An interesting feature is that RPFA is sensitive to sleep. This is a similar feature as with most of the epileptiform activities. However RPFA was also observed in one patient without ep-ilepsy in this study. Previous studies included only patients
Figure 5. Patient 19 showing sharp activities on Fp2-F4 electrode during NREM II sleep. The patient had RPFA on the same electrode position
during sleep (RPFA activitiy is indicated by arrows. Sweep speed: 10 seconds/page, sensitivity: 7 µV/mm, high frequency: 70 Hz, low frequency: 1,00 Hz, notch fitler: 50 Hz)
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who were video EEG monitored or intracerebral EEG for med-ically intractable focal epilepsies (2, 13). We have studied the same group but also included patients who were caught ran-domly during daily EEG recordings. This finding may alarm us the necessity of discussing the significance of these rhythms. However we should keep in mind that one patient in this case series had language retardation, ADHD and we do not know if this patient will develop epilepsy in the future.
Regional paroxysmal fast activity localizing or lateralizing val-ue is an essential qval-uestion to answer. Most of the RPFA were observed in extratemporal lobe epilepsies (14). In our series, majority of the patients had lesions beyond the boundaries of one lobe, some had bilateral lesions. RPFA with regard to le-sion localization was challenging in patient 2 and patient 5. In patient 2 although there was a very limited lesion on the right mesial frontal area, he became seizure-free after left hemi-spherectomy and the RPFA was vanished in the following EEG recordings after surgery. Patient 5 could not be evaluated with intracranial electrodes, unfortunately. We can speculate out hemisphere hypothesis as in the case of burned-out hippocampus. In such patients, propagation pathways and connectivity may change causing rapid propagation to contralateral temporal lobe. After hemispherectomy, the first patient became seizure free and thus we can propose that the epileptogenic zone was the left hemisphere which was burned-out (15, 16). As this is the case, RPFA observed on the contralateral hemisphere may be as a result of rapid propaga-tion. This data needs clarificapropaga-tion.
In this retrospective analysis, RPFA rhythms were evaluated on scalp EEG. These rhythms were observed in different patient populations such as, patients with treatment-resistant focal ep-ilepsy, epileptic patients with benign form and even patients without epilepsy. Structural lesions were not always present in these patients, however both developmental and encephalo-malacic lesions may underlie these rhythms. The concordance of RPFA with interictal, ictal EEG features and location of lesions is heterogeneous. This should be further studied in bigger series.
Ethics Committee Approval: Ethics committee approval was
received from University of Health Sciences, Ümraniye Training and Research Hospital Ethics Committee (Num-ber: 40, Date: 20.02.2019).
Informed Consent: Written informed consent was obtained
from patients’ and the parents of the patients who partic-ipated in this study.
Peer-review: Externally peer-reviewed.
Author Contributions: Concept – R.S.; Design – S.N.Y.;
Super-vision – S.N.Y., A.V.D.; Resources – S.N.Y., A.V.D.; Materials – H.K.; Data Collection and/or Processing – H.K.; Analy-sis and/or Interpretation – R.S.; Literature Search – H.K.; Writing Manuscript – R.S.; Critical Review – S.N.Y.
Acknowledgements: We would like to thank Gülfem
SALBA-CAK for making EEG records.
Conflict of Interest: The authors have no conflicts of interest
to declare.
Financial Disclosure: The authors declared that this study
has received no financial support.
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