Resective surgery prevents progressive cortical thinning in temporal lobe epilepsy

Author:

Galovic Marian1234,de Tisi Jane3,McEvoy Andrew W3,Miserocchi Anna3,Vos Sjoerd B345,Borzi Giuseppe367,Cueva Rosillo Juana3,Vuong Khue Anh3,Nachev Parashkev3,Duncan John S34,Koepp Matthias J34

Affiliation:

1. Department of Neurology, University Hospital Zurich, Zurich, Switzerland

2. Clinical Neuroscience Center, University Hospital Zurich, Zurich, Switzerland

3. Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, London, UK

4. MRI Unit, Epilepsy Society, Chalfont St Peter, Buckinghamshire, UK

5. Centre for Medical Image Computing, University College London, London, UK

6. Institute of Neurology, University of Catanzaro, Italy

7. Neurology Unit, Ospedale Civile San’Agostino Estense, Azienda Ospedaliero-Universitaria Modena, Modena Italy

Abstract

Abstract Focal epilepsy in adults is associated with progressive atrophy of the cortex at a rate more than double that of normal ageing. We aimed to determine whether successful epilepsy surgery interrupts progressive cortical thinning. In this longitudinal case-control neuroimaging study, we included subjects with unilateral temporal lobe epilepsy (TLE) before (n = 29) or after (n = 56) anterior temporal lobe resection and healthy volunteers (n = 124) comparable regarding age and sex. We measured cortical thickness on paired structural MRI scans in all participants and compared progressive thinning between groups using linear mixed effects models. Compared to ageing-related cortical thinning in healthy subjects, we found progressive cortical atrophy on vertex-wise analysis in TLE before surgery that was bilateral and localized beyond the ipsilateral temporal lobe. In these regions, we observed accelerated annualized thinning in left (left TLE 0.0192 ± 0.0014 versus healthy volunteers 0.0032 ± 0.0013 mm/year, P < 0.0001) and right (right TLE 0.0198 ± 0.0016 versus healthy volunteers 0.0037 ± 0.0016 mm/year, P < 0.0001) presurgical TLE cases. Cortical thinning in these areas was reduced after surgical resection of the left (0.0074 ± 0.0016 mm/year, P = 0.0006) or right (0.0052 ± 0.0020 mm/year, P = 0.0006) anterior temporal lobe. Directly comparing the post- versus presurgical TLE groups on vertex-wise analysis, the areas of postoperatively reduced thinning were in both hemispheres, particularly, but not exclusively, in regions that were affected preoperatively. Participants who remained completely seizure-free after surgery had no more progressive thinning than that observed during normal ageing. Those with postoperative seizures had small areas of continued accelerated thinning after surgery. Thus, successful epilepsy surgery prevents progressive cortical atrophy that is observed in TLE and may be potentially neuroprotective. This effect was more pronounced in those who remained seizure-free after temporal lobe resection, normalizing the rate of atrophy to that of normal ageing. These results provide evidence of epilepsy surgery preventing further cerebral damage and provide incentives for offering early surgery in refractory TLE.

Funder

Medical Research Council

University College London

University College London Hospital

National Institute for Health Research

NIHR

Biomedical Research Centres

Wellcome Trust

National Institute for Mental Health

Publisher

Oxford University Press (OUP)

Subject

Clinical Neurology

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