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Progressive remodeling of structural networks following surgery for operculo-insular epilepsy

Sami Obaid 1, 2, 3, 4
Guido I Guberman 5
Etienne St-Onge 6
Emma Campbell 7
Manon Edde 4
Layton Lamsam 8
Alain Bouthillier 3
Alexander G. Weil 1, 9
Alessandro Daducci 10
François Rheault 11
Dang K. Nguyen 1, 2, 12
Maxime Descoteaux 4
Publication typeJournal Article
Publication date2024-07-31
scimago Q2
wos Q2
SJR0.993
CiteScore5.2
Impact factor2.8
ISSN16642295
Abstract
Introduction

Operculo-insular epilepsy (OIE) is a rare condition amenable to surgery in well-selected cases. Despite the high rate of neurological complications associated with OIE surgery, most postoperative deficits recover fully and rapidly. We provide insights into this peculiar pattern of functional recovery by investigating the longitudinal reorganization of structural networks after surgery for OIE in 10 patients.

Methods

Structural T1 and diffusion-weighted MRIs were performed before surgery (t0) and at 6 months (t1) and 12 months (t2) postoperatively. These images were processed with an original, comprehensive structural connectivity pipeline. Using our method, we performed comparisons between the t0 and t1 timepoints and between the t1 and t2 timepoints to characterize the progressive structural remodeling.

Results

We found a widespread pattern of postoperative changes primarily in the surgical hemisphere, most of which consisted of reductions in connectivity strength (CS) and regional graph theoretic measures (rGTM) that reflect local connectivity. We also observed increases in CS and rGTMs predominantly in regions located near the resection cavity and in the contralateral healthy hemisphere. Finally, most structural changes arose in the first six months following surgery (i.e., between t0 and t1).

Discussion

To our knowledge, this study provides the first description of postoperative structural connectivity changes following surgery for OIE. The ipsilateral reductions in connectivity unveiled by our analysis may result from the reversal of seizure-related structural alterations following postoperative seizure control. Moreover, the strengthening of connections in peri-resection areas and in the contralateral hemisphere may be compatible with compensatory structural plasticity, a process that could contribute to the recovery of functions seen following operculo-insular resections for focal epilepsy.

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Journal of Clinical Neurophysiology
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Ovid Technologies (Wolters Kluwer Health)
1 publication, 100%
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Obaid S. et al. Progressive remodeling of structural networks following surgery for operculo-insular epilepsy // Frontiers in Neurology. 2024. Vol. 15.
GOST all authors (up to 50) Copy
Obaid S., Guberman G. I., St-Onge E., Campbell E., Edde M., Lamsam L., Bouthillier A., Weil A. G., Daducci A., Rheault F., Nguyen D. K., Descoteaux M. Progressive remodeling of structural networks following surgery for operculo-insular epilepsy // Frontiers in Neurology. 2024. Vol. 15.
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RIS Copy
TY - JOUR
DO - 10.3389/fneur.2024.1400601
UR - https://www.frontiersin.org/articles/10.3389/fneur.2024.1400601/full
TI - Progressive remodeling of structural networks following surgery for operculo-insular epilepsy
T2 - Frontiers in Neurology
AU - Obaid, Sami
AU - Guberman, Guido I
AU - St-Onge, Etienne
AU - Campbell, Emma
AU - Edde, Manon
AU - Lamsam, Layton
AU - Bouthillier, Alain
AU - Weil, Alexander G.
AU - Daducci, Alessandro
AU - Rheault, François
AU - Nguyen, Dang K.
AU - Descoteaux, Maxime
PY - 2024
DA - 2024/07/31
PB - Frontiers Media S.A.
VL - 15
PMID - 39144703
SN - 1664-2295
ER -
BibTex
Cite this
BibTex (up to 50 authors) Copy
@article{2024_Obaid,
author = {Sami Obaid and Guido I Guberman and Etienne St-Onge and Emma Campbell and Manon Edde and Layton Lamsam and Alain Bouthillier and Alexander G. Weil and Alessandro Daducci and François Rheault and Dang K. Nguyen and Maxime Descoteaux},
title = {Progressive remodeling of structural networks following surgery for operculo-insular epilepsy},
journal = {Frontiers in Neurology},
year = {2024},
volume = {15},
publisher = {Frontiers Media S.A.},
month = {jul},
url = {https://www.frontiersin.org/articles/10.3389/fneur.2024.1400601/full},
doi = {10.3389/fneur.2024.1400601}
}