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; Winston, Gavin P; Duncan, John S; Vos, Sjoerd B

Abstract

Background and Objectives:

In medically refractory temporal lobe epilepsy (TLE), 30-50% of patients experience substantial language decline following resection in the language dominant hemisphere. Here, we investigate the contribution of white matter fiber bundle damage to language change at 3- and 12-months after surgery.

Methods:

We studied 127 patients who underwent TLE surgery from 2010–2019. Neuropsychological testing included picture naming, semantic, and phonemic verbal fluency, performed pre-operatively, 3- and 12-months post-operatively. Outcome was assessed using reliable change index (RCI; clinically significant decline) and change across timepoints (post- minus pre-operative scores).

Functional MRI was used to determine language lateralization. The arcuate (AF), inferior fronto-occipital (IFOF), inferior longitudinal, middle longitudinal (MLF), and uncinate fasciculi were mapped using diffusion MRI probabilistic tractography. Resection masks, drawn comparing co-registered pre- and post-operative T1 MRI scans, were used as exclusion regions on pre-operative tractography to estimate the percentage of pre-operative tracts transected in surgery. Chi-squared assessments evaluated the occurrence of RCI-determined language decline. Independent samples 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.

Results:

Language dominant and non-dominant resections were treated separately for picture naming, as post-operative 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 sub-fasciculus of the IFOF was related to change at 3 months. In language non-dominant hemisphere resections, increased MLF resection was associated with RCI-decline at 3 months, and damage to the anterior sub-fasciculus was related to change at 3 months.

Language dominant and non-dominant resections were treated as one cohort for semantic and phonemic fluency, as there were no significant differences in post-operative decline between these groups. Post-operative seizure freedom was associated with an absence of significant language decline 12 months after surgery for semantic fluency.

Discussion:

We 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, https://doi.org/10.1212/WNL.0000000000206862

• Journal Article Type: Article
• Acceptance Date: Dec 12, 2022
• Online Publication Date: Feb 7, 2023
• Publication Date: Feb 7, 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
• 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/early/2023/02/07/WNL.0000000000206862
• 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.