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Can histologically normal epileptogenic zone share common electrophysiological phenotypes with focal cortical dysplasia? SEEG-based study in MRI-negative epileptic patients

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Abstract

Objective

We aimed to assess stereoelectroencephalography (SEEG) seizure-onset and interictal patterns associated with MRI-negative epilepsy and investigate their possible links with histology, extent of the epileptogenic zone (EZ) and surgical outcome.

Methods

We retrospectively analysed a cohort of 59 consecutive MRI-negative surgical candidates, who underwent SEEG recordings followed by cortectomy between 2000 and 2016.

Results

Most of the eight distinct seizure-onset patterns could be encountered both in confirmed focal cortical dysplasia (FCD) and in histologically non-specific or normal cases. We found strong correlation (p = 0.008) between seizure-onset pattern and histology for: (1) slow-wave/DC-shift prior to low voltage fast activity (LVFA), associated with normal/non-specific histology, and (2) bursts of polyspikes prior to LVFA, exclusively observed in FCD. Three interictal patterns were identified: periodic slow-wave/gamma burst, sub-continuous rhythmic spiking and irregular spikes. Both “periodic” patterns were more frequent in but not specific to FCD. Surgical outcome depended on the EZ complete removal, regardless electrophysiological features.

Conclusions

Histologically normal and FCD-associated epileptogenic zones share distinct interictal and ictal electrophysiological phenotypes, with common patterns between FCD subtypes and between dysplastic and apparently normal brain.

Significance

Some specific seizure-onset patterns seem to be predictive of the underlying histology and may help to detect an MRI-invisible FCD.

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Acknowledgements

We thank Prof. Henry Dufour and Prof. Jean-Claude Peragut (Marseille), Prof. Pierre Kehrli (died May 28, 2014) and Dr. Alexander Timofeev (Strasbourg) for surgical procedures in some of the selected patients. We thank Prof. Patrick Chauvel, Prof Jean Régis, Prof. Martine Gavaret, Dr. Francesca Bonini, Dr. Lisa Vaugier, Dr. Sandrine Aubert, Dr. Geraldine Daquin, Dr. Constanza Dalvit, Dr. Nathalie Villeneuve and Dr. Anne Lepine (Marseille), Dr. Anne De Saint Martin, Dr. Clotilde Boulay, Dr Christel Dentel, Dr Charles Behr and Dr. Serge Chassagnon (Strasbourg) for the clinical management of some included patients.

Funding

This work has been carried out within the FHU EPINEXT with the support of the A*MIDEX project (ANR-11-IDEX-0001-02) funded by the "Investissements d'Avenir" French Governement program managed by the Agence Nationale de la Recherche (ANR) Part of this work was funded by a joint Agence Nationale de la Recherche (ANR) and Direction Génerale de l'Offre de Santé (DGOS) under Grant "VIBRATIONS" ANR-13-PRTS-0011-01.

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Author notes

  1. Stanislas Lagarde and Julia Scholly contributed equally to this work.

Authors and Affiliations

  1. Epileptology Department, Timone Hospital, Inst Neurosci Syst, Service d’Epileptologie, Aix Marseille University, APHM, INSERM, INS, 264 Rue St Pierre, 13005, Marseille, France

    Stanislas Lagarde, Julia Scholly, Agnès Trebuchon, Aileen McGonigal & Fabrice Bartolomei

  2. Medical and Surgical Epilepsy Unit, Hautepierre Hospital, Strasbourg, France

    Julia Scholly, Irina Popa, Maria Paola Valenti-Hirsch, François Proust, Mustapha Benmekhbi & Edouard Hirsch

  3. Paediatric Neurology, Timone Hospital, APHM, Marseille, France

    Mathieu Milh

  4. Kork Epilepsy Center, Kehl-Kork, Germany

    Anke M. Staack

  5. Department of Pathology, Hautepierre Hospital, Strasbourg, France

    Béatrice Lannes & Benoît Lhermitte

  6. Pediatric Neurosurgery, Timone Hospital, APHM, Marseille, France

    Didier Scavarda

  7. Functional and Stereotactic Neurosurgery, Timone Hospital, Inst Neurosci Syst, Aix Marseille University, APHM, INSERM, INS, Marseille, France

    Romain Carron

  8. Anatomopathology Department, Timone Hospital, Institut de Neurophysiopathologie, Aix-Marseille University, APHM, Marseille, France

    Dominique Figarella-Branger

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  1. Stanislas Lagarde
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  2. Julia Scholly
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  3. Irina Popa
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  4. Maria Paola Valenti-Hirsch
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  5. Agnès Trebuchon
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Corresponding author

Correspondence to Fabrice Bartolomei.

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This study has been approved by the hospital ethics committee and has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

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Lagarde, S., Scholly, J., Popa, I. et al. Can histologically normal epileptogenic zone share common electrophysiological phenotypes with focal cortical dysplasia? SEEG-based study in MRI-negative epileptic patients. J Neurol 266, 1907–1918 (2019). https://doi.org/10.1007/s00415-019-09339-4

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