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

BACKGROUND AND OBJECTIVES: In 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...

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Autores principales: 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.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Lippincott Williams & Wilkins 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10103113/
https://www.ncbi.nlm.nih.gov/pubmed/36750386
http://dx.doi.org/10.1212/WNL.0000000000206862
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author 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.
author_facet 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.
author_sort Binding, Lawrence Peter
collection PubMed
description BACKGROUND AND OBJECTIVES: In 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. METHODS: We 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. RESULTS: Language-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. 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.
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spelling pubmed-101031132023-04-15 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. Neurology Research Article BACKGROUND AND OBJECTIVES: In 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. METHODS: We 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. RESULTS: Language-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. 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. Lippincott Williams & Wilkins 2023-04-11 /pmc/articles/PMC10103113/ /pubmed/36750386 http://dx.doi.org/10.1212/WNL.0000000000206862 Text en Copyright © 2023 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology. https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
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.
Contribution of White Matter Fiber Bundle Damage to Language Change After Surgery for Temporal Lobe Epilepsy
title Contribution of White Matter Fiber Bundle Damage to Language Change After Surgery for Temporal Lobe Epilepsy
title_full Contribution of White Matter Fiber Bundle Damage to Language Change After Surgery for Temporal Lobe Epilepsy
title_fullStr Contribution of White Matter Fiber Bundle Damage to Language Change After Surgery for Temporal Lobe Epilepsy
title_full_unstemmed Contribution of White Matter Fiber Bundle Damage to Language Change After Surgery for Temporal Lobe Epilepsy
title_short Contribution of White Matter Fiber Bundle Damage to Language Change After Surgery for Temporal Lobe Epilepsy
title_sort contribution of white matter fiber bundle damage to language change after surgery for temporal lobe epilepsy
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10103113/
https://www.ncbi.nlm.nih.gov/pubmed/36750386
http://dx.doi.org/10.1212/WNL.0000000000206862
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