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Early identification of seizure freedom with medical treatment in patients with mesial temporal lobe epilepsy and hippocampal sclerosis

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Abstract

Background

Mesial temporal lobe epilepsy with hippocampal sclerosis (MTLE-HS) is usually associated with a poor response to antiseizure medications. We focused on MTLE-HS patients who were seizure free on medication to: (1) determine the clinical factors associated with seizure freedom and (2) develop a machine-learning classifier to better earlier identify those patients.

Methods

We performed a retrospective, multicentric study comparing 64 medically treated seizure-free MTLE-HS patients with 200 surgically treated drug-resistant MTLE-HS patients. First, we collected medical history and seizure semiology data. Then, we developed a machine-learning classifier based on clinical data.

Results

Medically treated seizure-free MTLE-HS patients were seizure-free for at least 2 years, and for a median time of 7 years at last follow-up. Compared to drug-resistant MTLE-HS patients, they exhibited: an older age at epilepsy onset (22.5 vs 8.0 years, p < 0.001), a lesser rate of: febrile seizures (39.0% vs 57.5%, p = 0.035), focal aware seizures (previously referred to as aura)(56.7% vs 90.0%, p < 0.001), autonomic focal aware seizures in presence of focal aware seizure (17.6% vs 59.4%, p < 0.001), dystonic posturing of the limbs (9.8% vs 47.0%, p < 0.001), gestural (27.4% vs 94.0%, p < 0.001), oro-alimentary (32.3% vs 75.5%, p < 0.001) or verbal automatisms (12.9% vs 36.0%, p = 0.001). The classifier had a positive predictive value of 0.889, a sensitivity of 0.727, a specificity of 0.962, a negative predictive value of 0.893.

Conclusions

Medically treated seizure-free MTLE-HS patients exhibit a distinct clinical profile. A classifier built with readily available clinical data can identify them accurately with excellent positive predictive value. This may help to individualize the management of MTLE-HS patients according to their expected pharmacosensitivity.

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Data availability

The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.

Abbreviations

MTLE-HS:

Mesial temporal lobe epilepsy with hippocampal sclerosis

MTLE:

Mesial temporal lobe epilepsy

TLE:

Temporal lobe epilepsy

ASM:

Antiseizure medications

HS:

Hippocampal sclerosis

FTBS:

Focal to bilateral tonic–clonic seizures

SEEG:

Stereo-electroencephalography

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Acknowledgements

The authors thank Drs. J.P.Vignal, A.Gales, V.Frazzini, C.Adam and Pr P.Thomas for their contribution to the recruitment of this study

Funding

No funding to disclose.

Author information

Authors and Affiliations

  1. Reference Center for Rare Epilepsies, Department of Neurology, Epileptology Unit, AP-HP, Pitié-Salpêtrière Hospital, 47-83, boulevard de l’hôpital, 75651, Paris Cedex 13, France

    Margaux Cheval, Bastien Herlin & Sophie Dupont

  2. Rehabilitation Unit, AP-HP, Pitié-Salpêtrière Hospital, Paris, France

    Margaux Cheval, Bastien Herlin & Sophie Dupont

  3. Sorbonne Université, Paris, France

    Margaux Cheval, Bastien Herlin & Sophie Dupont

  4. Centre of Excellence of Neurodegenerative Disease (CoEN), AP-HP, Pitié-Salpêtrière Hospital, Paris, France

    Marion Houot

  5. Institute of Memory and Alzheimer’s Disease (IM2A), Department of Neurology, AP-HP, Pitié-Salpêtrière Hospital, Paris, France

    Marion Houot

  6. Clinical Investigation Centre, Institut du Cerveau et de la Moelle épinière (ICM), Pitié-Salpêtrière Hospital Paris, Paris, France

    Marion Houot

  7. Department of Neurophysiology, Rouen University Hospital, Rouen, France

    Nathalie Chastan

  8. Department of Clinical Neurophysiology, Amiens University Hospital, Amiens, France

    William Szurhaj

  9. Neurology-Epilepsy Unit, Bordeaux University Hospital, Bordeaux, France

    Cécile Marchal

  10. Department of Functional Neurology and Epileptology, Hospices Civils de Lyon, Lyon, France

    Hélène Catenoix

  11. INSERM U1028, CNRS 5292, Lyon, France

    Hélène Catenoix

  12. Department of Neurology, Toulouse University Hospital, Toulouse, France

    Luc Valton

  13. Centre de Recherche Cerveau et Cognition, CNRS, UMR5549, Toulouse, France

    Luc Valton

  14. Neurophysiology and Epileptology Department, GHU Paris Psychiatrie et Neurosciences, Université Paris Cité, INSERM UMR 1266, IPNP, Paris, France

    Martine Gavaret

  15. Neurology Department, Rennes University Hospital, Rennes, France

    Arnaud Biraben

  16. Epileptology and Cerebral Rythmology Department, Timone Hospital, APHM, Marseille, France

    Stanislas Lagarde

  17. Aix Marseille Univ, Inserm, INS, Inst Neurosci Syst, Marseille, France

    Stanislas Lagarde

  18. Department of Neurology, University Hospital of Saint-Étienne, Saint-Étienne, France

    Laure Mazzola

  19. Department of Neurology, Grenoble-Alpes University Hospital, Grenoble, France

    Lorella Minotti

  20. Inserm, U1216, Grenoble Institut Neurosciences, Grenoble, France

    Lorella Minotti

  21. Reference Center for Rare Epilepsies, Neurology Department, CHU de Nancy, Nancy, France

    Louis Maillard

  22. CRAN UMR 7039, Université de Lorraine, Nancy, France

    Louis Maillard

  23. Institut du Cerveau Et de La Moelle Épinière (ICM), Pitié-Salpêtrière Hospital Paris, Paris, France

    Sophie Dupont

Authors
  1. Margaux Cheval
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  2. Marion Houot
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  3. Nathalie Chastan
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  4. William Szurhaj
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  5. Cécile Marchal
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  6. Hélène Catenoix
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  7. Luc Valton
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  8. Martine Gavaret
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  9. Bastien Herlin
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  11. Stanislas Lagarde
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  12. Laure Mazzola
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  13. Lorella Minotti
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  14. Louis Maillard
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  15. Sophie Dupont
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Contributions

MC and SD had the idea for the study, included patients and wrote the initial protocol and analysis plan. MC collected the data. MC, MH and SD did the data analysis. MH did the statistical analysis and developed the machine-learning classifier. MC produced the table and wrote the first draft of the manuscript. MH and SD further reviewed the manuscript and contributed to the final version of the manuscript. All other authors (NC, WS, CM, HC, LV, MG, BH, AB, SL, L.Maz, L.Min, L.Mai) included in the study patients from their epilepsy centres and contributed to editing and commenting on the final version.

Corresponding authors

Correspondence to Margaux Cheval or Sophie Dupont.

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Conflicts of interest

None of the authors has any conflict of interest to disclose.

Ethical publication statement

We confirm that we have read the Journal’s position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. We used the STROBE reporting guidelines [44].

IRB statement

The study was approved by the local ethics committee of Sorbonne University (no CER-2021-089). The patients signed an informed consent form for the use of medical reports and data.

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Cheval, M., Houot, M., Chastan, N. et al. Early identification of seizure freedom with medical treatment in patients with mesial temporal lobe epilepsy and hippocampal sclerosis. J Neurol 270, 2715–2723 (2023). https://doi.org/10.1007/s00415-023-11603-7

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