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The sinuous, wave-like intratumoral-wall sign is a sensitive and specific radiological biomarker for oligodendrogliomas

  • Oncology
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Abstract

Objectives

The purpose of this study was to investigate the clinical utility of the sinuous, wave-like intratumoral-wall (SWITW) sign on T2WI in diagnosing isocitrate dehydrogenase (IDH) mutant and 1p/19q codeleted (IDHmut-Codel) oligodendrogliomas, for which a relatively conservative resection strategy might be sufficient due to a better response to chemoradiotherapy and favorable prognosis.

Methods

Imaging data from consecutive adult patients with diffuse lower-grade gliomas (LGGs, histological grades 2–3) in Beijing Tiantan Hospital (December 1, 2013, to October 31, 2021, BTH set, n = 711) and the Cancer Imaging Archive (TCIA) LGGs set (n = 117) were used to develop and validate our findings. Two independent observers assessed the SWITW sign and some well-reported discriminative radiological features to establish a practical diagnostic strategy.

Results

The SWITW sign showed satisfying sensitivity (0.684 and 0.722 for BTH and TCIA sets) and specificity (0.938 and 0.914 for BTH and TCIA sets) in defining IDHmut-Codels, and the interobserver agreement was substantial (κ 0.718 and 0.756 for BTH and TCIA sets). Compared to calcification, the SWITW sign improved the sensitivity by 0.28 (0.404 to 0.684) in the BTH set, and 81.0% (277/342) of IDHmut-Codel cases demonstrated SWITW and/ or calcification positivity. Combining the SWITW sign, calcification, low ADC values, and other discriminative features, we established a concise and reliable diagnostic protocol for IDHmut-Codels.

Conclusions

The SWITW sign was a sensitive and specific imaging biomarker for IDHmut-Codels. The integrated protocol provided an explicable, efficient, and reproducible method for precise preoperative diagnosis, which was essential to guide individualized surgical plan-making.

Key Points

• The SWITW sign was a sensitive and specific imaging biomarker for IDHmut-Codel oligodendrogliomas.

• The SWITW sign was more sensitive than calcification and an integrated strategy could improve diagnostic sensitivity for IDHmut-Codel oligodendrogliomas.

• Combining SWITW, calcification, low ADC values, and other discriminative features could make a precise preoperative diagnosis for IDHmut-Codel oligodendrogliomas.

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Abbreviations

ADC:

Apparent diffusion coefficient

AUC:

Area under the curve

BTH:

Beijing Tiantan Hospital

DT:

Decision tree

FLAIR:

Fluid-attenuated inversion-recovery

GBDT:

Gradient boosting decision tree

hyperFLAIRrim:

Hyperintense FLAIR rim

IDH:

Isocitrate dehydrogenase

LASSO:

Least absolute shrinkage and selection operator

LGG:

Lower-grade glioma

MGMT:

O6-methylguanine-DNA methyltransferase

NPV:

Negative predictive value

OS:

Overall survival

PFS:

Progression-free survival

PPV:

Positive predictive value

RF:

Random forests

ROC:

Receiver operating characteristic curve

SVM:

Support vector machine

SWITW:

Sinuous wave-like intratumoral-wall feature on T2WI

T2FM:

T2-FLAIR mismatch

VASARI:

Visually Accessible Rembrandt Images

VOI:

Volumes of interest

WHO:

World Health Organization

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Acknowledgments

The authors sincerely thank the patients and their families for their participation in the present study.

Funding sources

This study was supported by the Capital Funds for Health Improvement and Research (2020-2-1075 and 2022-2-1072) and the National Natural Science Foundation of China (81571632 and 81771309).

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Authors and Affiliations

  1. Department of Neurosurgical Oncology, Beijing Tiantan Hospital, Capital Medical University, China National Clinical Research Center for Neurological Diseases, Beijing Neurosurgical Institute, Beijing, 100070, China

    Mingxiao Li, Shaoping Shen, Chuanwei Yang, Xiaokang Zhang, Xuzhe Zhao, Qinghui Zhu, Ming Li, Yong Cui, Xiaohui Ren & Song Lin

  2. Department of Neurosurgery, Beijing Neurosurgical Institute, Capital Medical University, Beijing, China

    Mingxiao Li, Shaoping Shen, Chuanwei Yang, Xiaokang Zhang, Xuzhe Zhao, Qinghui Zhu, Ming Li, Yong Cui, Xiaohui Ren & Song Lin

  3. Department of Radiology, Peking University Cancer Hospital, Beijing, China

    Jincheng Wang

  4. Department of Radiology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

    Xuzhu Chen

  5. Department of Pathology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

    Gehong Dong & Weiwei Zhang

  6. Department of Neurosurgery, Peking University Third Hospital, Peking University, Beijing, China

    Haihui Jiang

  7. Department of Neurosurgery, Beijing Neurosurgical Institute, Capital Medical University, Center of Brain Tumor, Institute for Brain Disorders and Beijing Key Laboratory of Brain Tumor, Beijing, China

    Song Lin

  8. Department of Neurosurgical Oncology, Beijing Tiantan Hospital, Center of Brain Tumor, Beijing Institute for Brain Disorders, Beijing Key Laboratory of Brain Tumor, Capital Medical University, China National Clinical Research Center for Neurological Diseases, Beijing Neurosurgical Institute, Beijing, 100070, China

    Song Lin

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  1. Mingxiao Li
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The scientific guarantor of this publication is Xiaohui Ren, MD., PhD., and Song Lin, MD., PhD.

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Statistics and biometry

Mingxiao L and Jincheng W have significant statistical expertise.

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• Multicenter study

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Li, M., Wang, J., Chen, X. et al. The sinuous, wave-like intratumoral-wall sign is a sensitive and specific radiological biomarker for oligodendrogliomas. Eur Radiol 33, 4440–4452 (2023). https://doi.org/10.1007/s00330-022-09314-0

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