Skip to main content

Research Repository

Advanced Search

Contribution of White Matter Fiber Bundle Damage to Language Change After Surgery for Temporal Lobe Epilepsy

Binding, Lawrence Peter; Dasgupta, Debayan; Taylor, Peter Neal; Thompson, Pamela Jane; O'Keeffe, Aidan G; De Tisi, Jane; Mcevoy, Andrew William; Miserocchi, Anna; Duncan, John S.; Duncan, John S; Vos, Sjoerd B.

Authors

Lawrence Peter Binding

Debayan Dasgupta

Peter Neal Taylor

Pamela Jane Thompson

Jane De Tisi

Andrew William Mcevoy

Anna Miserocchi

John S. Duncan

John S Duncan

Sjoerd B. Vos



Abstract

Background and ObjectivesIn medically refractory temporal lobe epilepsy (TLE), 30%-50% of patients experience substantial language decline after resection in the language-dominant hemisphere. In this study, we investigated the contribution of white matter fiber bundle damage to language change at 3 and 12 months after surgery.MethodsWe studied 127 patients who underwent TLE surgery from 2010 to 2019. Neuropsychological testing included picture naming, semantic fluency, and phonemic verbal fluency, performed preoperatively and 3 and 12 months postoperatively. Outcome was assessed using reliable change index (RCI; clinically significant decline) and change across timepoints (postoperative scores minus preoperative scores). Functional MRI was used to determine language lateralization. The arcuate fasciculus (AF), inferior fronto-occipital fasciculus (IFOF), inferior longitudinal fasciculus, middle longitudinal fasciculus (MLF), and uncinate fasciculus were mapped using diffusion MRI probabilistic tractography. Resection masks, drawn comparing coregistered preoperative and postoperative T1 MRI scans, were used as exclusion regions on preoperative tractography to estimate the percentage of preoperative tracts transected in surgery. Chi-squared assessments evaluated the occurrence of RCI-determined language decline. Independent sample t tests and MM-estimator robust regressions were used to assess the impact of clinical factors and fiber transection on RCI and change outcomes, respectively.ResultsLanguage-dominant and language-nondominant resections were treated separately for picture naming because postoperative outcomes were significantly different between these groups. In language-dominant hemisphere resections, greater surgical damage to the AF and IFOF was related to RCI decline at 3 months. Damage to the inferior frontal subfasciculus of the IFOF was related to change at 3 months. In language-nondominant hemisphere resections, increased MLF resection was associated with RCI decline at 3 months, and damage to the anterior subfasciculus was related to change at 3 months. Language-dominant and language-nondominant resections were treated as 1 cohort for semantic and phonemic fluency because there were no significant differences in postoperative decline between these groups. Postoperative seizure freedom was associated with an absence of significant language decline 12 months after surgery for semantic fluency.DiscussionWe demonstrate a relationship between fiber transection and naming decline after temporal lobe resection. Individualized surgical planning to spare white matter fiber bundles could help to preserve language function after surgery.

Citation

Binding, L. P., Dasgupta, D., Taylor, P. N., Thompson, P. J., O'Keeffe, A. G., De Tisi, J., …Vos, S. B. (2023). Contribution of White Matter Fiber Bundle Damage to Language Change After Surgery for Temporal Lobe Epilepsy. Neurology, 100(15), e1621-e1633. https://doi.org/10.1212/WNL.0000000000206862

Journal Article Type Article
Acceptance Date Dec 12, 2022
Online Publication Date Feb 7, 2023
Publication Date Apr 11, 2023
Deposit Date Feb 24, 2023
Publicly Available Date Feb 24, 2023
Journal Neurology
Print ISSN 0028-3878
Electronic ISSN 1526-632X
Publisher Ovid Technologies (Wolters Kluwer Health)
Peer Reviewed Peer Reviewed
Volume 100
Issue 15
Pages e1621-e1633
DOI https://doi.org/10.1212/WNL.0000000000206862
Keywords Neurology (clinical)
Public URL https://nottingham-repository.worktribe.com/output/17664582
Publisher URL https://n.neurology.org/content/100/15/e1621
Additional Information This is an open access article distributed under the Creative Commons Attribution License 4.0 (CCBY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Files




You might also like



Downloadable Citations