Rapid diagnosis of adult-type diffuse glioma using a layered scheme

Abstract Background Molecular biomarkers have become an essential part of the diagnosis of adult-type diffuse glioma. Still, complex detection methods and long-term turnaround for these biomarkers hinder integrated diagnosis in clinical practice. We hypothesized that IDH and TERT promoter (TERTp) mu...

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Main Authors: Jinsong Wu, Shuai Wu, Dandan Cao, Zhang Xiong, Jianhua Zhang, Yourui Zou, Zanyi Wu, Yanli Nie, Chen Luo, Ye Yao, Yanyan Song, Yuchen Jiao, Hong Chen, Hui Ma, Dezhi Kang, Ying Mao, Hai Yan
Format: Article
Language:English
Published: BMC 2025-06-01
Series:BMC Medicine
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Online Access:https://doi.org/10.1186/s12916-025-04124-9
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author Jinsong Wu
Shuai Wu
Dandan Cao
Zhang Xiong
Jianhua Zhang
Yourui Zou
Zanyi Wu
Yanli Nie
Chen Luo
Ye Yao
Yanyan Song
Yuchen Jiao
Hong Chen
Hui Ma
Dezhi Kang
Ying Mao
Hai Yan
author_facet Jinsong Wu
Shuai Wu
Dandan Cao
Zhang Xiong
Jianhua Zhang
Yourui Zou
Zanyi Wu
Yanli Nie
Chen Luo
Ye Yao
Yanyan Song
Yuchen Jiao
Hong Chen
Hui Ma
Dezhi Kang
Ying Mao
Hai Yan
author_sort Jinsong Wu
collection DOAJ
description Abstract Background Molecular biomarkers have become an essential part of the diagnosis of adult-type diffuse glioma. Still, complex detection methods and long-term turnaround for these biomarkers hinder integrated diagnosis in clinical practice. We hypothesized that IDH and TERT promoter (TERTp) mutations play similar roles in accurately classifying adult-type diffuse glioma compared to the complicated WHO CNS5-recommended biomarkers, and the detection of IDH and TERTp mutations should be the first layer in clinical practice. Methods We propose a novel layered diagnostic scheme for adult-type diffuse gliomas, with IDH and TERTp mutation detection as the initial layer. We also developed a rapid intraoperative testing technology capable of detecting TERTp and IDH mutations within 35 min. This study involved both a retrospective cohort and a prospective multicenter diagnostic test. The diagnostic accuracy of the layered approach was evaluated using sensitivity, specificity, and the area under the receiver operating characteristic curve (AUC), with a 95% confidence interval. Results In retrospective cohort, the TERTp mutation demonstrated comparable statistical power to 1p/19q codeletion in distinguishing oligodendrogliomas from astrocytomas (κ = 0.96, P < 0.001). Additionally, 91.8% of glioblastomas with either EGFR amplification or + 7/-10 exhibited TERTp mutations. In the prospective application of the layered diagnostic scheme and rapid testing, 223 gliomas and 2 non-gliomas (76.5%) were accurately classified intraoperatively. With the addition of postoperative permanent section analysis, 249 gliomas and 24 non-gliomas (92.9%) were correctly classified following the detection of the first-layer biomarkers. Conclusions The proposed layered diagnostic scheme offers a rapid and accurate means of classifying adult-type diffuse gliomas, facilitating the broader use of molecular classification. It expands its applicability from postoperative to intraoperative settings for the majority of patients, enhancing diagnostic efficiency and accuracy. Trial registration ClinicalTrials.gov NCT04924127, NCT04904419.
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spelling doaj-art-07e2a7547f944fe693d933a0ccc4952e2025-08-20T03:10:37ZengBMCBMC Medicine1741-70152025-06-0123111210.1186/s12916-025-04124-9Rapid diagnosis of adult-type diffuse glioma using a layered schemeJinsong Wu0Shuai Wu1Dandan Cao2Zhang Xiong3Jianhua Zhang4Yourui Zou5Zanyi Wu6Yanli Nie7Chen Luo8Ye Yao9Yanyan Song10Yuchen Jiao11Hong Chen12Hui Ma13Dezhi Kang14Ying Mao15Hai Yan16Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan UniversityDepartment of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan UniversityGenetron Health (Beijing) Co. Ltd.Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan UniversityGenetron Health (Beijing) Co. Ltd.Department of Neurosurgery, General Hospital of Ningxia Medical UniversityDepartment of Neurosurgery, Neurosurgery Research Institute, The First Affiliated Hospital, Fujian Medical UniversityGenetron Health (Beijing) Co. Ltd.Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan UniversitySchool of Public Health, Fudan UniversityDepartment of Biostatistics, Clinical Research Institute, Shanghai Jiaotong University School of MedicineState Key Laboratory of Molecular Oncology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeDepartment of Pathology, Huashan Hospital, Shanghai Medical College, Fudan UniversityDepartment of Neurosurgery, General Hospital of Ningxia Medical UniversityDepartment of Neurosurgery, Neurosurgery Research Institute, The First Affiliated Hospital, Fujian Medical UniversityDepartment of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan UniversityGenetron Health (Beijing) Co. Ltd.Abstract Background Molecular biomarkers have become an essential part of the diagnosis of adult-type diffuse glioma. Still, complex detection methods and long-term turnaround for these biomarkers hinder integrated diagnosis in clinical practice. We hypothesized that IDH and TERT promoter (TERTp) mutations play similar roles in accurately classifying adult-type diffuse glioma compared to the complicated WHO CNS5-recommended biomarkers, and the detection of IDH and TERTp mutations should be the first layer in clinical practice. Methods We propose a novel layered diagnostic scheme for adult-type diffuse gliomas, with IDH and TERTp mutation detection as the initial layer. We also developed a rapid intraoperative testing technology capable of detecting TERTp and IDH mutations within 35 min. This study involved both a retrospective cohort and a prospective multicenter diagnostic test. The diagnostic accuracy of the layered approach was evaluated using sensitivity, specificity, and the area under the receiver operating characteristic curve (AUC), with a 95% confidence interval. Results In retrospective cohort, the TERTp mutation demonstrated comparable statistical power to 1p/19q codeletion in distinguishing oligodendrogliomas from astrocytomas (κ = 0.96, P < 0.001). Additionally, 91.8% of glioblastomas with either EGFR amplification or + 7/-10 exhibited TERTp mutations. In the prospective application of the layered diagnostic scheme and rapid testing, 223 gliomas and 2 non-gliomas (76.5%) were accurately classified intraoperatively. With the addition of postoperative permanent section analysis, 249 gliomas and 24 non-gliomas (92.9%) were correctly classified following the detection of the first-layer biomarkers. Conclusions The proposed layered diagnostic scheme offers a rapid and accurate means of classifying adult-type diffuse gliomas, facilitating the broader use of molecular classification. It expands its applicability from postoperative to intraoperative settings for the majority of patients, enhancing diagnostic efficiency and accuracy. Trial registration ClinicalTrials.gov NCT04924127, NCT04904419.https://doi.org/10.1186/s12916-025-04124-9Layered diagnostic schemeAdult-type diffuse gliomasIDH mutationTERT promoter mutationIntraoperative integrated diagnosis
spellingShingle Jinsong Wu
Shuai Wu
Dandan Cao
Zhang Xiong
Jianhua Zhang
Yourui Zou
Zanyi Wu
Yanli Nie
Chen Luo
Ye Yao
Yanyan Song
Yuchen Jiao
Hong Chen
Hui Ma
Dezhi Kang
Ying Mao
Hai Yan
Rapid diagnosis of adult-type diffuse glioma using a layered scheme
BMC Medicine
Layered diagnostic scheme
Adult-type diffuse gliomas
IDH mutation
TERT promoter mutation
Intraoperative integrated diagnosis
title Rapid diagnosis of adult-type diffuse glioma using a layered scheme
title_full Rapid diagnosis of adult-type diffuse glioma using a layered scheme
title_fullStr Rapid diagnosis of adult-type diffuse glioma using a layered scheme
title_full_unstemmed Rapid diagnosis of adult-type diffuse glioma using a layered scheme
title_short Rapid diagnosis of adult-type diffuse glioma using a layered scheme
title_sort rapid diagnosis of adult type diffuse glioma using a layered scheme
topic Layered diagnostic scheme
Adult-type diffuse gliomas
IDH mutation
TERT promoter mutation
Intraoperative integrated diagnosis
url https://doi.org/10.1186/s12916-025-04124-9
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