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Preoperative individual-target transcranial magnetic stimulation demonstrates an effect comparable to intraoperative direct electrical stimulation in language-eloquent glioma mapping and improves postsurgical outcome: A retrospective fiber-tracking and electromagnetic simulation study

BACKGROUND: Efforts to resection of glioma lesions located in brain-eloquent areas must balance the extent of resection (EOR) and functional preservation. Currently, intraoperative direct electrical stimulation (DES) is the gold standard for achieving the maximum EOR while preserving as much functio...

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Autores principales: Li, Sanzhong, Mu, Yunfeng, Rao, Yang, Sun, Chuanzhu, Li, Xiang, Liu, Huan, Yu, Xun, Yan, Xiao, Ding, Yunxia, Wang, Yangtao, Fei, Zhou
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9936080/
https://www.ncbi.nlm.nih.gov/pubmed/36816968
http://dx.doi.org/10.3389/fonc.2023.1089787
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author Li, Sanzhong
Mu, Yunfeng
Rao, Yang
Sun, Chuanzhu
Li, Xiang
Liu, Huan
Yu, Xun
Yan, Xiao
Ding, Yunxia
Wang, Yangtao
Fei, Zhou
author_facet Li, Sanzhong
Mu, Yunfeng
Rao, Yang
Sun, Chuanzhu
Li, Xiang
Liu, Huan
Yu, Xun
Yan, Xiao
Ding, Yunxia
Wang, Yangtao
Fei, Zhou
author_sort Li, Sanzhong
collection PubMed
description BACKGROUND: Efforts to resection of glioma lesions located in brain-eloquent areas must balance the extent of resection (EOR) and functional preservation. Currently, intraoperative direct electrical stimulation (DES) is the gold standard for achieving the maximum EOR while preserving as much functionality as possible. However, intraoperative DES inevitably involves risks of infection and epilepsy. The aim of this study was to verify the reliability of individual-target transcranial magnetic stimulation (IT-TMS) in preoperative mapping relative to DES and evaluate its effectiveness based on postsurgical outcomes. METHODS: Sixteen language-eloquent glioma patients were enrolled. Nine of them underwent preoperative nTMS mapping (n=9, nTMS group), and the other seven were assigned to the non-nTMS group and did not undergo preoperative nTMS mapping (n=7). Before surgery, online IT-TMS was performed during a language task in the nTMS group. Sites in the cortex at which this task was disturbed in three consecutive trials were recorded and regarded as positive and designated nTMS hotspots (HS(nTMS)). Both groups then underwent awake surgery and intraoperative DES mapping. DES hotspots (HS(DES)) were also determined in a manner analogous to HS(nTMS). The spatial distribution of HS(nTMS) and HS(DES) in the nTMS group was recorded, registered in a single brain template, and compared. The center of gravity (CoG) of HS(nTMS) (HS(nTMS-CoG))-based and HS(DES-CoG)-based diffusion tensor imaging-fiber tracking (DTI-FT) was performed. The electromagnetic simulation was conducted, and the values were then compared between the nTMS and DES groups, as were the Western Aphasia Battery (WAB) scale and fiber-tracking values. RESULTS: HS(nTMS) and HS(DES) showed similar distributions (mean distance 6.32 ± 2.6 mm, distance range 2.2-9.3 mm, 95% CI 3.9-8.7 mm). A higher fractional anisotropy (FA) value in nTMS mapping (P=0.0373) and an analogous fiber tract length (P=0.2290) were observed. A similar distribution of the electric field within the brain tissues induced by nTMS and DES was noted. Compared with the non-nTMS group, the integration of nTMS led to a significant improvement in language performance (WAB scores averaging 78.4 in the nTMS group compared with 59.5 in the non-nTMS group, P=0.0321 < 0.05) as well as in brain-structure preservation (FA value, P=0.0156; tract length, P=0.0166). CONCLUSION: Preoperative IT-TMS provides data equally crucial to DES and thus facilitates precise brain mapping and the preservation of linguistic function.
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spelling pubmed-99360802023-02-18 Preoperative individual-target transcranial magnetic stimulation demonstrates an effect comparable to intraoperative direct electrical stimulation in language-eloquent glioma mapping and improves postsurgical outcome: A retrospective fiber-tracking and electromagnetic simulation study Li, Sanzhong Mu, Yunfeng Rao, Yang Sun, Chuanzhu Li, Xiang Liu, Huan Yu, Xun Yan, Xiao Ding, Yunxia Wang, Yangtao Fei, Zhou Front Oncol Oncology BACKGROUND: Efforts to resection of glioma lesions located in brain-eloquent areas must balance the extent of resection (EOR) and functional preservation. Currently, intraoperative direct electrical stimulation (DES) is the gold standard for achieving the maximum EOR while preserving as much functionality as possible. However, intraoperative DES inevitably involves risks of infection and epilepsy. The aim of this study was to verify the reliability of individual-target transcranial magnetic stimulation (IT-TMS) in preoperative mapping relative to DES and evaluate its effectiveness based on postsurgical outcomes. METHODS: Sixteen language-eloquent glioma patients were enrolled. Nine of them underwent preoperative nTMS mapping (n=9, nTMS group), and the other seven were assigned to the non-nTMS group and did not undergo preoperative nTMS mapping (n=7). Before surgery, online IT-TMS was performed during a language task in the nTMS group. Sites in the cortex at which this task was disturbed in three consecutive trials were recorded and regarded as positive and designated nTMS hotspots (HS(nTMS)). Both groups then underwent awake surgery and intraoperative DES mapping. DES hotspots (HS(DES)) were also determined in a manner analogous to HS(nTMS). The spatial distribution of HS(nTMS) and HS(DES) in the nTMS group was recorded, registered in a single brain template, and compared. The center of gravity (CoG) of HS(nTMS) (HS(nTMS-CoG))-based and HS(DES-CoG)-based diffusion tensor imaging-fiber tracking (DTI-FT) was performed. The electromagnetic simulation was conducted, and the values were then compared between the nTMS and DES groups, as were the Western Aphasia Battery (WAB) scale and fiber-tracking values. RESULTS: HS(nTMS) and HS(DES) showed similar distributions (mean distance 6.32 ± 2.6 mm, distance range 2.2-9.3 mm, 95% CI 3.9-8.7 mm). A higher fractional anisotropy (FA) value in nTMS mapping (P=0.0373) and an analogous fiber tract length (P=0.2290) were observed. A similar distribution of the electric field within the brain tissues induced by nTMS and DES was noted. Compared with the non-nTMS group, the integration of nTMS led to a significant improvement in language performance (WAB scores averaging 78.4 in the nTMS group compared with 59.5 in the non-nTMS group, P=0.0321 < 0.05) as well as in brain-structure preservation (FA value, P=0.0156; tract length, P=0.0166). CONCLUSION: Preoperative IT-TMS provides data equally crucial to DES and thus facilitates precise brain mapping and the preservation of linguistic function. Frontiers Media S.A. 2023-02-03 /pmc/articles/PMC9936080/ /pubmed/36816968 http://dx.doi.org/10.3389/fonc.2023.1089787 Text en Copyright © 2023 Li, Mu, Rao, Sun, Li, Liu, Yu, Yan, Ding, Wang and Fei https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Oncology
Li, Sanzhong
Mu, Yunfeng
Rao, Yang
Sun, Chuanzhu
Li, Xiang
Liu, Huan
Yu, Xun
Yan, Xiao
Ding, Yunxia
Wang, Yangtao
Fei, Zhou
Preoperative individual-target transcranial magnetic stimulation demonstrates an effect comparable to intraoperative direct electrical stimulation in language-eloquent glioma mapping and improves postsurgical outcome: A retrospective fiber-tracking and electromagnetic simulation study
title Preoperative individual-target transcranial magnetic stimulation demonstrates an effect comparable to intraoperative direct electrical stimulation in language-eloquent glioma mapping and improves postsurgical outcome: A retrospective fiber-tracking and electromagnetic simulation study
title_full Preoperative individual-target transcranial magnetic stimulation demonstrates an effect comparable to intraoperative direct electrical stimulation in language-eloquent glioma mapping and improves postsurgical outcome: A retrospective fiber-tracking and electromagnetic simulation study
title_fullStr Preoperative individual-target transcranial magnetic stimulation demonstrates an effect comparable to intraoperative direct electrical stimulation in language-eloquent glioma mapping and improves postsurgical outcome: A retrospective fiber-tracking and electromagnetic simulation study
title_full_unstemmed Preoperative individual-target transcranial magnetic stimulation demonstrates an effect comparable to intraoperative direct electrical stimulation in language-eloquent glioma mapping and improves postsurgical outcome: A retrospective fiber-tracking and electromagnetic simulation study
title_short Preoperative individual-target transcranial magnetic stimulation demonstrates an effect comparable to intraoperative direct electrical stimulation in language-eloquent glioma mapping and improves postsurgical outcome: A retrospective fiber-tracking and electromagnetic simulation study
title_sort preoperative individual-target transcranial magnetic stimulation demonstrates an effect comparable to intraoperative direct electrical stimulation in language-eloquent glioma mapping and improves postsurgical outcome: a retrospective fiber-tracking and electromagnetic simulation study
topic Oncology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9936080/
https://www.ncbi.nlm.nih.gov/pubmed/36816968
http://dx.doi.org/10.3389/fonc.2023.1089787
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