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

BackgroundEfforts 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 functiona...

Full description

Bibliographic Details
Main Authors: Sanzhong Li, Yunfeng Mu, Yang Rao, Chuanzhu Sun, Xiang Li, Huan Liu, Xun Yu, Xiao Yan, Yunxia Ding, Yangtao Wang, Zhou Fei
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Oncology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fonc.2023.1089787/full
_version_ 1811173220284366848
author Sanzhong Li
Yunfeng Mu
Yang Rao
Chuanzhu Sun
Xiang Li
Xiang Li
Huan Liu
Xun Yu
Xiao Yan
Yunxia Ding
Yangtao Wang
Zhou Fei
author_facet Sanzhong Li
Yunfeng Mu
Yang Rao
Chuanzhu Sun
Xiang Li
Xiang Li
Huan Liu
Xun Yu
Xiao Yan
Yunxia Ding
Yangtao Wang
Zhou Fei
author_sort Sanzhong Li
collection DOAJ
description BackgroundEfforts 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.MethodsSixteen 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 (HSnTMS). Both groups then underwent awake surgery and intraoperative DES mapping. DES hotspots (HSDES) were also determined in a manner analogous to HSnTMS. The spatial distribution of HSnTMS and HSDES in the nTMS group was recorded, registered in a single brain template, and compared. The center of gravity (CoG) of HSnTMS (HSnTMS-CoG)-based and HSDES-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.ResultsHSnTMS and HSDES 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).ConclusionPreoperative IT-TMS provides data equally crucial to DES and thus facilitates precise brain mapping and the preservation of linguistic function.
first_indexed 2024-04-10T17:44:18Z
format Article
id doaj.art-787fecc5805748b28ebb5778da895c77
institution Directory Open Access Journal
issn 2234-943X
language English
last_indexed 2024-04-10T17:44:18Z
publishDate 2023-02-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Oncology
spelling doaj.art-787fecc5805748b28ebb5778da895c772023-02-03T06:07:08ZengFrontiers Media S.A.Frontiers in Oncology2234-943X2023-02-011310.3389/fonc.2023.10897871089787Preoperative 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 studySanzhong Li0Yunfeng Mu1Yang Rao2Chuanzhu Sun3Xiang Li4Xiang Li5Huan Liu6Xun Yu7Xiao Yan8Yunxia Ding9Yangtao Wang10Zhou Fei11Department of Neurosurgery, Xijing Hospital, Air Force Medical University, Xi’an, Shaanxi, ChinaDepartment of Gynecological Oncology, Shaanxi Provincial Cancer Hospital, Xi’an, ChinaShaanxi Brain Modulation and Scientific Research Center, Xi'an, Shaanxi, ChinaShaanxi Brain Modulation and Scientific Research Center, Xi'an, Shaanxi, ChinaShaanxi Brain Modulation and Scientific Research Center, Xi'an, Shaanxi, ChinaThe Key Laboratory of Biomedical Information Engineering of Ministry of Education, Institute of Health and Rehabilitation Science, School of Life Science and Technology, Xi’an Jiaotong University, Xi’an, Shaanxi, ChinaSchool of Mathematics and Statistics, Xi’an Jiaotong University, Xi’an, Shaanxi, ChinaProduct Department, Solide Brain Medical Technology, Ltd., Xi’an, Shaanxi, ChinaShaanxi Brain Modulation and Scientific Research Center, Xi'an, Shaanxi, ChinaShaanxi Brain Modulation and Scientific Research Center, Xi'an, Shaanxi, ChinaShaanxi Brain Modulation and Scientific Research Center, Xi'an, Shaanxi, ChinaDepartment of Neurosurgery, Xijing Hospital, Air Force Medical University, Xi’an, Shaanxi, ChinaBackgroundEfforts 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.MethodsSixteen 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 (HSnTMS). Both groups then underwent awake surgery and intraoperative DES mapping. DES hotspots (HSDES) were also determined in a manner analogous to HSnTMS. The spatial distribution of HSnTMS and HSDES in the nTMS group was recorded, registered in a single brain template, and compared. The center of gravity (CoG) of HSnTMS (HSnTMS-CoG)-based and HSDES-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.ResultsHSnTMS and HSDES 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).ConclusionPreoperative IT-TMS provides data equally crucial to DES and thus facilitates precise brain mapping and the preservation of linguistic function.https://www.frontiersin.org/articles/10.3389/fonc.2023.1089787/fulltranscranial magnetic stimulationlanguage mappingfiber-trackingelectromagnetic simulationdeep electrical stimulation
spellingShingle Sanzhong Li
Yunfeng Mu
Yang Rao
Chuanzhu Sun
Xiang Li
Xiang Li
Huan Liu
Xun Yu
Xiao Yan
Yunxia Ding
Yangtao Wang
Zhou Fei
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
Frontiers in Oncology
transcranial magnetic stimulation
language mapping
fiber-tracking
electromagnetic simulation
deep electrical stimulation
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 transcranial magnetic stimulation
language mapping
fiber-tracking
electromagnetic simulation
deep electrical stimulation
url https://www.frontiersin.org/articles/10.3389/fonc.2023.1089787/full
work_keys_str_mv AT sanzhongli preoperativeindividualtargettranscranialmagneticstimulationdemonstratesaneffectcomparabletointraoperativedirectelectricalstimulationinlanguageeloquentgliomamappingandimprovespostsurgicaloutcomearetrospectivefibertrackingandelectromagneticsimulationstudy
AT yunfengmu preoperativeindividualtargettranscranialmagneticstimulationdemonstratesaneffectcomparabletointraoperativedirectelectricalstimulationinlanguageeloquentgliomamappingandimprovespostsurgicaloutcomearetrospectivefibertrackingandelectromagneticsimulationstudy
AT yangrao preoperativeindividualtargettranscranialmagneticstimulationdemonstratesaneffectcomparabletointraoperativedirectelectricalstimulationinlanguageeloquentgliomamappingandimprovespostsurgicaloutcomearetrospectivefibertrackingandelectromagneticsimulationstudy
AT chuanzhusun preoperativeindividualtargettranscranialmagneticstimulationdemonstratesaneffectcomparabletointraoperativedirectelectricalstimulationinlanguageeloquentgliomamappingandimprovespostsurgicaloutcomearetrospectivefibertrackingandelectromagneticsimulationstudy
AT xiangli preoperativeindividualtargettranscranialmagneticstimulationdemonstratesaneffectcomparabletointraoperativedirectelectricalstimulationinlanguageeloquentgliomamappingandimprovespostsurgicaloutcomearetrospectivefibertrackingandelectromagneticsimulationstudy
AT xiangli preoperativeindividualtargettranscranialmagneticstimulationdemonstratesaneffectcomparabletointraoperativedirectelectricalstimulationinlanguageeloquentgliomamappingandimprovespostsurgicaloutcomearetrospectivefibertrackingandelectromagneticsimulationstudy
AT huanliu preoperativeindividualtargettranscranialmagneticstimulationdemonstratesaneffectcomparabletointraoperativedirectelectricalstimulationinlanguageeloquentgliomamappingandimprovespostsurgicaloutcomearetrospectivefibertrackingandelectromagneticsimulationstudy
AT xunyu preoperativeindividualtargettranscranialmagneticstimulationdemonstratesaneffectcomparabletointraoperativedirectelectricalstimulationinlanguageeloquentgliomamappingandimprovespostsurgicaloutcomearetrospectivefibertrackingandelectromagneticsimulationstudy
AT xiaoyan preoperativeindividualtargettranscranialmagneticstimulationdemonstratesaneffectcomparabletointraoperativedirectelectricalstimulationinlanguageeloquentgliomamappingandimprovespostsurgicaloutcomearetrospectivefibertrackingandelectromagneticsimulationstudy
AT yunxiading preoperativeindividualtargettranscranialmagneticstimulationdemonstratesaneffectcomparabletointraoperativedirectelectricalstimulationinlanguageeloquentgliomamappingandimprovespostsurgicaloutcomearetrospectivefibertrackingandelectromagneticsimulationstudy
AT yangtaowang preoperativeindividualtargettranscranialmagneticstimulationdemonstratesaneffectcomparabletointraoperativedirectelectricalstimulationinlanguageeloquentgliomamappingandimprovespostsurgicaloutcomearetrospectivefibertrackingandelectromagneticsimulationstudy
AT zhoufei preoperativeindividualtargettranscranialmagneticstimulationdemonstratesaneffectcomparabletointraoperativedirectelectricalstimulationinlanguageeloquentgliomamappingandimprovespostsurgicaloutcomearetrospectivefibertrackingandelectromagneticsimulationstudy