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Research ArticleOriginal Article

Clinical management and survival outcomes of patients with different molecular subtypes of diffuse gliomas in China (2011–2017): a multicenter retrospective study from CGGA

Kenan Zhang, Xing Liu, Guanzhang Li, Xin Chang, Shouwei Li, Jing Chen, Zheng Zhao, Jiguang Wang, Tao Jiang and Ruichao Chai
Cancer Biology & Medicine October 2022, 19 (10) 1460-1476; DOI: https://doi.org/10.20892/j.issn.2095-3941.2022.0469
Kenan Zhang
1Department of Molecular Pathology, Beijing Neurosurgical Institute, Capital Medical University, Beijing 100070, China
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Xing Liu
2Department of Neuropathology, Beijing Neurosurgical Institute, Capital Medical University, Beijing 100070, China
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Guanzhang Li
1Department of Molecular Pathology, Beijing Neurosurgical Institute, Capital Medical University, Beijing 100070, China
3Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing 100070, China
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Xin Chang
4Department of Neurosurgery, Beijing Sanbo Brain Hospital, Capital Medical University, Beijing 100093, China
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Shouwei Li
4Department of Neurosurgery, Beijing Sanbo Brain Hospital, Capital Medical University, Beijing 100093, China
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Jing Chen
1Department of Molecular Pathology, Beijing Neurosurgical Institute, Capital Medical University, Beijing 100070, China
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Zheng Zhao
1Department of Molecular Pathology, Beijing Neurosurgical Institute, Capital Medical University, Beijing 100070, China
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Jiguang Wang
5Division of Life Science and State Key Laboratory of Molecular Neuroscience, Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong SAR 999077, China
6Hong Kong Center for Neurodegenerative Diseases, Hong Kong Science Park, Hong Kong SAR 999077, China
7HKUST Shenzhen-Hong Kong Collaborative Innovation Research Institute, Futian, Shenzhen 518057, China
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Tao Jiang
1Department of Molecular Pathology, Beijing Neurosurgical Institute, Capital Medical University, Beijing 100070, China
3Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing 100070, China
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  • For correspondence: [email protected] [email protected]
Ruichao Chai
1Department of Molecular Pathology, Beijing Neurosurgical Institute, Capital Medical University, Beijing 100070, China
2Department of Neuropathology, Beijing Neurosurgical Institute, Capital Medical University, Beijing 100070, China
5Division of Life Science and State Key Laboratory of Molecular Neuroscience, Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong SAR 999077, China
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  • For correspondence: [email protected] [email protected]
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  • Figure 1
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    Figure 1

    Flowchart of patients with eligible diffuse gliomas who were included in the study.

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    Figure 2
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    Figure 2

    Survival outcomes of patients with different molecular subtypes. Kaplan-Meier estimates of overall survival (A) and progression-free survival (B) of patients with primary DG classified according to molecular subtypes. Kaplan-Meier estimation of the overall survival (C) and progression-free survival (D) of patients with recurrent DG classified according to molecular subtypes.

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    Figure 3

    Survival outcomes of patients with primary GBM receiving different postsurgical treatments. (A–B) Kaplan-Meier curves estimating the overall survival of patients with primary GBM-IDHwt (A) and patients with primary GBM-IDHm (B). (C–D) Kaplan-Meier curves estimating the progression-free survival of patients with primary GBM-IDHwt (C) and patients with primary GBM-IDHm (D). *P < 0.05, ****P < 0.0001.

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    Figure 4

    Survival outcomes of patients with recurrent GBM receiving different postsurgical treatments. (A–B) Kaplan-Meier curves estimating overall survival of patients with recurrent GBM-IDHwt patients (A) and patients with recurrent GBM-IDHm (B). (C–D) Kaplan-Meier curves estimating progression-free survival of patients with recurrent GBM-IDHwt (C) and patients with recurrent GBM-IDHm (D). *P < 0.05, **P < 0.01, ***P < 0.001.

Tables

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    Table 1

    Distribution of 1418 cases of diffuse glioma according to clinicopathological information

    CharacteristicsDiffuse gliomaPrimary diffuse gliomaRecurrent diffuse gliomaP
    Sex
    Male8395412980.0339
    Female579405174
    Age
     ≥ 456594602000.0276
     < 45755486272
     Mean age, years (SD)43.55 (12.33)44.33 (12.95)42.00 (10.67)
    Symptom at onset (n = 1334)
     Headache555445110< 0.0001
     Seizure457331126
     Focal deficit393240153
     No clear symptoms17958121
    Karnofsky performance status (n = 1330)
     ≥ 801260857403< 0.0001
     < 80703040
    Lateral involvement (n = 1390)
     Right6564502060.6024
     Left659439220
     Both sides704327
     Midline532
    Cortex involvement (n = 1390)
     Frontal lobe9316073240.0017
     Temporal lobe586386200
     Insular lobe30923772
     Parietal lobe298183115
     Occipital lobe1207743
     Other lobes725022
    Histological grade
     II37630967< 0.0001
     III413290123
     IV629347282
    Molecular subtype
     LGG, IDH-mutant and 1p/19q-codeleted16713037< 0.0001
     LGG, IDH-mutant19513065
     LGG, IDH-wildtype14110338
     LGG, NOS28623650
     GBM, IDH-wildtype389248141
     GBM, IDH-mutant18563122
     GBM, NOS553619
    MGMT methylation (n = 1080)
     Unmethylated3742511230.4077
     Methylated706492214
    Types of surgery
     Total resection627475152< 0.0001
     Subtotal resection511333178
     Partial resection278138140
     Biopsy202
    Treatment (n = 1274)
     Radio chemotherapy643520123< 0.0001
     Radiotherapy17315122
     Chemotherapy26374189
     None19511184
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    Table 2

    Characteristics of primary diffuse gliomas

    nLGG, IDH-mutant and 1p/19q-codeletedLGG, IDH-mutantLGG, IDH-wildtypeGBM, IDH-wildtypeGBM, IDH-mutantPLGG NOSGBM NOS
    Sex946130130103248630.799523636
     Male541727559150400.799512322
     Female405585544982311314
    Age
     ≥ 4546056373419528< 0.00018327
     < 4548674936953351539
     Mean age, years44.3042.1539.1538.5552.8643.6741.1749.75
     SD of age12.739.898.5716.0412.5711.799.9811.57
    Karnofsky performance status
     ≥ 80857126123100233580.372218928
     < 803043214241
    Diagnostic symptom89013012710224762< 0.000119329
     Headache445495648156437716
     Seizure3316864403718959
     Neurofunction deficit24022192911412359
     No clear symptom58156851221
    Lateral involved935130129101244630.040823335
     Right4506666441102911421
     Left4395757461233211311
     Both sides4376811263
     Midline30030000
    Cortex involved (n)93513012910124463< 0.000123335
     Frontal lobe60710393511144318122
     Temporal lobe386405040118329214
     Insular lobe2373444214616733
     Parietal lobe18317212267113411
     Occipital lobe77157455131
     Other lobes50661019360
    • View popup
    Table 3

    Univariate and multivariate Cox proportional-hazards models for low grade gliomas

    VariableHazard ratio (95% CI)
    LGG, IDH-mutant and 1p/19q-codeletedLGG, IDH-mutantLGG, IDH-wildtype
    UnivariateMultivariateUnivariateMultivariateUnivariateMultivariate
    Age at diagnosis11.069 (0.998–1.144)†1.378 (1.08–1.759)*0.984 (0.948–1.021)1.026 (1.007–1.045)†
    Sex
     FemaleReferenceReferenceReference
     Male0.702 (0.175–2.811)1.331 (0.684–2.591)1.598 (0.867–2.944)
     Histological grade25.84 (0.713–47.86)†48.808 (1.193–1997.239)*3.902 (1.789–8.51)†2.659 (1.195–5.918)*3.776 (1.808–7.887)6.024 (2.311–15.702)*
    MGMT
     UnmethylatedReferenceReferenceReference
     Methylated2.657 (0.318–22.229)0.566 (0.284–1.125)0.376 (0.194–0.729)†
     KPS_PRE30.991 (0.885–1.109)0.98 (0.922–1.041)0.971 (0.931–1.013)
     KPS_POST40.925 (0.869–0.986)†0.933 (0.903–0.964)†0.956 (0.925–0.988)*0.944 (0.92–0.969)†0.949 (0.906–0.994)*
    Resection rate
     Total resectionReferenceReferenceReferenceReferenceReferenceReference
     Subtotal resection4.68 (0.424–51.663)24.532 (0.522–1153.043)2.083 (0.911–4.765)†1.707 (0.724–4.025)6.022 (1.368–26.507)†11.326 (1.407–91.164)*
     Major partial resection147.156 (13.035–1661.254)†4288.619 (17.419–1.056^106)*21.3 (8.518–53.262)†13.381 (5.079–35.251)*28.795 (6.524–127.102)†46.648 (5.71–381.063)*
     Partial resection251.105 (17.041–3700.168)†615281.86 (102.016–3.711^109)*253.199 (43.115–1486.938)†120.991 (17.383–842.133)*42.932 (9.598–192.039)†100.392 (11.692–861.985)*
    Radiotherapy
     Not receivedReferenceReferenceReference
     Received1.386 (0.279–6.894)1.1 (0.459–2.636)1.292 (0.616–2.708)
    Chemotherapy
     Not receivedReferenceReferenceReference
     Received1.585 (0.318–7.902)0.748 (0.373–1.503)2.011 (0.924–4.373)†

    1The hazard ratio is for each 1-yr increase in age. 2The hazard ratio is for each 1 grade increase in WHO grade. 3The hazard ratio is for each 1 point increase in KPS score. 4The hazard ratio is for each 1 point increase in KPS score. †The P value of the hazard ratio was less than 0.1 for the univariate Cox models and included in the multivariate Cox model. *The hazard ratio was significant (P < 0.05).

      • View popup
      Table 4

      Univariate and multivariate cox proportional-hazards models for glioblastomas

      VariableHazard ratio (95% CI)
      Glioblastoma, IDH-wildtypeGlioblastoma, IDH-mutant
      UnivariateMultivariateUnivariateMultivariate
      Age at diagnosis11.018 (1.007–1.03)†1.012 (0.999–1.025)1.012 (0.985–1.041)
      Sex
       FemaleReferenceReference
       Male1.052 (0.794–1.393)1.208 (0.584–2.499)
      MGMT
       UnmethylatedReferenceReference
       Methylated0.938 (0.706–1.246)0.858 (0.424–1.739)
       KPS_PRE20.987 (0.967–1.007)0.96 (0.908–1.015)
       KPS_POST30.962 (0.949–0.975)†0.975 (0.959–0.991)*0.965 (0.934–0.998)†
      Resection rate
       Total resectionReferenceReferenceReferenceReference
       Subtotal resection2.269 (1.646–3.127)†2.074 (1.468–2.929)*1.814 (0.804–4.093)1.771 (0.726–4.319)
       Major partial resection7.259 (4.677–11.267)†5.598 (3.469–9.033)*30.002 (6.037–149.107)†66.577 (9.7–456.942)*
       Partial resection84.175 (41.344–171.378)†76.094 (30.649–188.918)*99.335 (20.047–492.219)†361.066 (37.041–3519.607)*
      Radiotherapy
       Not receivedReferenceReference
       Received0.582 (0.396–0.854)†0.771 (0.315–1.888)
      Chemotherapy
       Not receivedReferenceReferenceReferenceReference
       Received0.297 (0.198–0.447)†0.42 (0.271–0.652)*0.279 (0.113–0.691)†0.309 (0.115–0.829)*

      1The hazard ratio is for each 1-yr increase in age. 2The hazard ratio is for each 1 point increase in KPS score. 3The hazard ratio is for each 1 point increase in KPS score. †The P value of the hazard ratio was less than 0.1 for the univariate Cox models and included in the multivariate Cox model.*The hazard ratio was significant (P < 0.05).

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      Clinical management and survival outcomes of patients with different molecular subtypes of diffuse gliomas in China (2011–2017): a multicenter retrospective study from CGGA
      Kenan Zhang, Xing Liu, Guanzhang Li, Xin Chang, Shouwei Li, Jing Chen, Zheng Zhao, Jiguang Wang, Tao Jiang, Ruichao Chai
      Cancer Biology & Medicine Oct 2022, 19 (10) 1460-1476; DOI: 10.20892/j.issn.2095-3941.2022.0469

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      Clinical management and survival outcomes of patients with different molecular subtypes of diffuse gliomas in China (2011–2017): a multicenter retrospective study from CGGA
      Kenan Zhang, Xing Liu, Guanzhang Li, Xin Chang, Shouwei Li, Jing Chen, Zheng Zhao, Jiguang Wang, Tao Jiang, Ruichao Chai
      Cancer Biology & Medicine Oct 2022, 19 (10) 1460-1476; DOI: 10.20892/j.issn.2095-3941.2022.0469
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      Keywords

      • Diffuse glioma
      • IDH
      • 1p/19q
      • molecular pathology
      • temozolomide

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