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The prognostic value of maximal surgical resection is attenuated in oligodendroglioma subgroups of adult diffuse glioma: a multicenter retrospective study

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Abstract

Purpose

Maximal surgical resection is associated with survival benefit in the majority of studies in adult diffuse glioma. This study aims to characterize the prognostic value of surgical resection in molecular subgroups of diffuse glioma.

Methods

1178 patients with diffuse glioma from our centers and 422 from TCGA dataset were collected. The Kaplan–Meier analysis and multivariable Cox regression models were conducted to identify the prognostic value of surgical resection through different histological and molecular stratifications.

Results

Firstly, we confirmed progression-free survival (PFS) benefit associated with gross total resection (GTR) over sub-total resection (STR) in lower-grade glioma (HR 1.49; 95% CI 1.17–1.90; P = 0.001). Intriguingly however, we were unable to detect a significant PFS or overall survival (OS) benefit in oligodendroglioma (N = 397; HR 1.36; 95% CI 0.86–2.14; P = 0.19 and HR 1.05; 95% CI 0.55–1.99; P = 0.89, respectively). Secondly, when analyzed in molecular subgroups, we were similarly unable to detect a significant PFS or OS benefit in IDH MT/codel subgroup (N = 269; HR 1.47; 95% CI 0.92–2.34; P = 0.11 and HR 1.54; 95% CI 0.78–3.05; P = 0.21, respectively), oligodendroglioma with IDH MT/codel subgroup (N = 233; HR 1.33; 95% CI 0.79–2.21; P = 0.28 and HR 1.16; 95% CI 0.53–2.54; P = 0.70, respectively) or other relevant subgroups. TCGA validation also showed a significant survival benefit in astrocytoma rather than oligodendroglioma. Exploratory RNAseq analysis displayed that fewer cell proliferation-related gene expression features were specific to oligodendroglioma.

Conclusion

These results suggest that the benefit of maximal surgery may be attenuated in patients within oligodendroglioma relevant subgroups because of the chemosensitive and indolent nature. The aggressive surgery accompanying with risk of neurologic morbidity may be unnecessary for these patients given the lack of survival benefit with gross total resection.

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Acknowledgements

This study is supported by the Research Special Fund for Public Welfare Industry of Health (No. 201402008) to Yu Yao; the National Key Research and Development Plan (No. 2016YFC0902500) to Tao Jiang.

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Author notes

  1. Xiaojie Ding, Zheng Wang and Di Chen have contributed equally to this work.

Authors and Affiliations

  1. Department of Neurosurgery, Huashan Hospital, Fudan University, 12# Mid Wulumuqi Road, Shanghai, China

    Xiaojie Ding, Di Chen, Dikang Chen, Chao Tang, Lingchao Chen, Yu Yao & Liangfu Zhou

  2. Beijing Neurosurgical Institute, Beijing Tiantan Hospital, Capital Medical University, 6# Tiantanxili, Beijing, China

    Zheng Wang, Zheng Zhao & Tao Jiang

  3. Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, 6# Tiantanxili, Beijing, China

    Yinyan Wang & Tao Jiang

  4. Department of Neurosurgery, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, Zhejiang, China

    Chongran Sun

  5. Neurosurgical Immunology Laboratory, Neurosurgical Institute of Fudan University, Shanghai, China

    Chao Tang, Lingchao Chen, Yu Yao & Liangfu Zhou

  6. Department of Pathology, Huashan Hospital, Fudan University, Shanghai, China

    Ji Xiong

  7. Department of Radiology, Huashan Hospital, Fudan University, Shanghai, China

    Zhenwei Yao

  8. Department of Pathology, Basic Medical Science, Fudan University, Shanghai, China

    Ying Liu

  9. Evidence Based Medicine Center, Fudan University, Shanghai, China

    Xiaoqin Wang

  10. Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA

    Daniel P. Cahill

  11. Department of Neuro-Oncology, MD Anderson Cancer Center, University of Texas, Houston, TX, USA

    John F. de Groot

Authors
  1. Xiaojie Ding
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  2. Zheng Wang
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  3. Di Chen
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  4. Yinyan Wang
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  5. Zheng Zhao
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  6. Chongran Sun
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  7. Dikang Chen
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  8. Chao Tang
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  9. Ji Xiong
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  10. Lingchao Chen
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  11. Zhenwei Yao
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  12. Ying Liu
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  13. Xiaoqin Wang
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  14. Daniel P. Cahill
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  15. John F. de Groot
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  16. Tao Jiang
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  17. Yu Yao
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  18. Liangfu Zhou
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Contributions

XD, TJ and YY designed the study. XD, ZW, DC, YW, ZZ, CS, DC, CT, JX, YL, XW, JFG, TJ and YY collected data. XD, ZW, DC, YW, ZZ, CS, DC, CT, JX, ZY, YL, JFG, TJ, YY and LZ provided materials. XD, ZW, DC, YW, ZZ, CS, DC, CT, JX, YL, XW, JFG, TJ and YY analyzed and interpreted the data. XD, ZW, DC, ZZ and XW did the statistical analyses. XD, ZW, DC, ZY, DPC, JFG, TJ, YY and LZ wrote and revised the manuscript. All authors approved the final report.

Corresponding authors

Correspondence to John F. de Groot, Tao Jiang or Yu Yao.

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Ding, X., Wang, Z., Chen, D. et al. The prognostic value of maximal surgical resection is attenuated in oligodendroglioma subgroups of adult diffuse glioma: a multicenter retrospective study. J Neurooncol 140, 591–603 (2018). https://doi.org/10.1007/s11060-018-2985-3

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