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.

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., Mcevoy, A. W., Miserocchi, A., Duncan, J. S., Duncan, J. S., & 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: American Academy of Neurology
• 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.