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Rethinking extent of resection of contrast-enhancing and non-enhancing tumor: different survival impacts on adult-type diffuse gliomas in 2021 World Health Organization classification

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Abstract

Objectives

Extent of resection (EOR) of contrast-enhancing (CE) and non-enhancing (NE) tumors may have different impacts on survival according to types of adult-type diffuse gliomas in the molecular era. This study aimed to evaluate the impact of EOR of CE and NE tumors in glioma according to the 2021 World Health Organization classification.

Methods

This retrospective study included 1193 adult-type diffuse glioma patients diagnosed between 2001 and 2021 (183 oligodendroglioma, 211 isocitrate dehydrogenase [IDH]–mutant astrocytoma, and 799 IDH-wildtype glioblastoma patients) from a single institution. Patients had complete information on IDH mutation, 1p/19q codeletion, and O6-methylguanine-methyltransferase (MGMT) status. Cox survival analyses were performed within each glioma type to assess predictors of overall survival, including clinical, imaging data, histological grade, MGMT status, adjuvant treatment, and EOR of CE and NE tumors. Subgroup analyses were performed in patients with CE tumor.

Results

Among 1193 patients, 935 (78.4%) patients had CE tumors. In entire oligodendrogliomas, gross total resection (GTR) of NE tumor was not associated with survival (HR = 0.56, p = 0.223). In 86 (47.0%) oligodendroglioma patients with CE tumor, GTR of CE tumor was the only independent predictor of survival (HR = 0.16, p = 0.004) in multivariable analysis. GTR of CE and NE tumors was independently associated with better survival in IDH-mutant astrocytoma and IDH-wildtype glioblastoma (all ps < 0.05).

Conclusions

GTR of both CE and NE tumors may significantly improve survival within IDH-mutant astrocytomas and IDH-wildtype glioblastomas. In oligodendrogliomas, the EOR of CE tumor may be crucial in survival; aggressive GTR of NE tumor may be unnecessary, whereas GTR of the CE tumor is recommended.

Clinical relevance statement

Surgical strategies on contrast-enhancing (CE) and non-enhancing (NE) tumors should be reassessed considering the different survival outcomes after gross total resection depending on CE and NE tumors in the 2021 World Health Organization classification of adult-type diffuse gliomas.

Key Points

  • The survival impact of extent of resection of contrast-enhancing (CE) and non-enhancing (NE) tumors was evaluated in adult-type diffuse gliomas.

  • Gross total resection of both CE and NE tumors may improve survival in isocitrate dehydrogenase (IDH)–mutant astrocytomas and IDH-wildtype glioblastomas, while only gross total resection of the CE tumor improves survival in oligodendrogliomas.

  • Surgical strategies should be reconsidered according to types in adult-type diffuse gliomas.

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Abbreviations

CE:

Contrast-enhancing

CI:

Confidence interval

EGFR:

Epidermal growth factor receptor

EOR:

Extent of resection

GTR:

Gross total resection

HR:

Hazard ratio

IDH:

Isocitrate dehydrogenase

KPS:

Karnofsky performance status

MGMT:

O6-methylguanine-methyltransferase

NE:

Non-enhancing

OS:

Overall survival

TERTp:

Telomerase reverse transcriptase promoter

WHO:

World Health Organization

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Acknowledgements

This research was previously presented as a poster at the 2022 Annual Society for Neuro-Oncology (SNO) Conference (Nov 18, 2022), under the title “NCOG-11. EXTENT OF RESECTION OF CONTRAST-ENHANCING AND NON-ENHANCING TUMOR: DIFFERENT IMPACTS ON SURVIVAL ACCORDING TO TYPES OF ADULT-TYPE DIFFUSE GLIOMAS IN 2021 WHO CLASSIFICATION” at Tampa, FL (DOI: 10.1093/neuonc/noac209.764).

Funding

This research received funding from the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, Information and Communication Technologies & Future Planning (2020R1A2C1003886); Ministry of Education (2020R1I1A1A01071648); Ministry of Health & Welfare, Republic of Korea (HI21C1161).

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Authors and Affiliations

  1. Department of Radiology and Research Institute of Radiological Science and Center for Clinical Imaging Data Science, Yonsei University College of Medicine, 50-1 Yonsei-ro, Seodaemun-gu, Seoul, 120-752, Korea

    Yae Won Park, Kyunghwa Han, Sung Soo Ahn, Jinna Kim & Seung-Koo Lee

  2. Department of Statistics and Data Science, Yonsei University, Seoul, Korea

    Sooyon Kim

  3. Department of Neurosurgery, Yonsei University College of Medicine, 50-1 Yonsei-ro, Seodaemun-gu, Seoul, 120-752, Korea

    Ju Hyung Moon, Eui Hyun Kim, Seok-Gu Kang & Jong Hee Chang

  4. Department of Pathology, Yonsei University College of Medicine, Seoul, Korea

    Se Hoon Kim

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  1. Yae Won Park
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Correspondence to Sung Soo Ahn or Jong Hee Chang.

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Guarantor

The scientific guarantor of this publication is Professor Seung-Koo Lee, MD, PhD, from Yonsei University College of Medicine (slee@yuhs.ac).

Conflict of interest

The authors declare no competing interests.

Statistics and biometry

We consulted a PhD who has significant statistical expertise (K.H., a biostatistician with 11 years of experience in biostatistics).

Informed consent

The institutional review board of our university (Yonsei University College of Medicine) waived the requirement for informed patient consent for this retrospective study.

Ethical approval

This study was approved by the institutional review board (no. 4-2022-0320) and requirement for patient consent was waived owing to the retrospective study design.

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  • Retrospective study

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  • Performed at one institution

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Park, Y.W., Kim, S., Han, K. et al. Rethinking extent of resection of contrast-enhancing and non-enhancing tumor: different survival impacts on adult-type diffuse gliomas in 2021 World Health Organization classification. Eur Radiol 34, 1376–1387 (2024). https://doi.org/10.1007/s00330-023-10125-0

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