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The development of a combined clinico-radiomics model for predicting post-operative recurrence in atypical meningiomas: a multicenter study

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Abstract

Purpose

Atypical meningiomas could manifest early recurrence after surgery and even adjuvant radiotherapy. We aimed to construct a clinico-radiomics model to predict post-operative recurrence of atypical meningiomas based on clinicopathological and radiomics features.

Materials and methods

The study cohort was comprised of 224 patients from two neurosurgical centers. 164 patients from center I were divided to the training cohort for model development and the testing cohort for internal validation. 60 patients from center II were used for external validation. Clinicopathological characteristics, radiological semantic, and radiomics features were collected. A radiomic signature was comprised of four radiomics features. A clinico-radiomics model combining the radiomics signature and clinical characteristics was constructed to predict the recurrence of atypical meningiomas.

Results

1920 radiomics features were extracted from the T1 Contrast and T2-FLAIR sequences of patients in center I. The radiomics signature was able to differentiate post-operative patients into low-risk and high-risk groups based on tumor recurrence (P < 0.001). A clinic-radiomics model was established by combining age, extent of resection, Ki-67 index, surgical history and the radiomics signature for recurrence prediction in atypical meningiomas. The model achieved a good prediction performance with the integrated AUC of 0.858 (0.802−0.915), 0.781 (0.649−0.912) and 0.840 (0.747−0.933) in the training, internal validation and external validation cohort, respectively.

Conclusions

The present study established a radiomics signature and a clinico-radiomics model with a favorable performance in predicting tumor recurrence for atypical meningiomas.

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Data availability

The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Ostrom QT, Cioffi G, Waite K, Kruchko C, Barnholtz-Sloan JS (2021) CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2014–2018. Neuro Oncol 23:31–2105. https://doi.org/10.1093/neuonc/noab200

    Article  Google Scholar 

  2. Louis DN, Perry A, Wesseling P, Brat DJ, Cree IA, Figarella-Branger D, Hawkins C, Ng HK, Pfister SM, Reifenberger G, Soffietti R, von Deimling A, Ellison DW (2021) The 2021 WHO classification of tumors of the central nervous system: a summary. Neuro Oncol 23:1231–1251. https://doi.org/10.1093/neuonc/noab106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Champeaux C, Houston D, Dunn L (2017) Atypical meningioma: a study on recurrence and disease-specific survival. Neurochirurgie 63:273–281. https://doi.org/10.1016/j.neuchi.2017.03.004

    Article  CAS  PubMed  Google Scholar 

  4. Apra C, Peyre M, Kalamarides M (2018) Current treatment options for meningioma. Expert Rev Neurother 18:241–249. https://doi.org/10.1080/14737175.2018.1429920

    Article  CAS  PubMed  Google Scholar 

  5. Ren L, Hua L, Deng J, Cheng H, Wang D, Chen J, Xie Q, Wakimoto H, Gong Y (2022) Favorable long-term outcomes of chordoid meningioma compared with the other WHO grade 2 meningioma subtypes. Neurosurgery. https://doi.org/10.1227/neu.0000000000002272

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ren L, Cheng H, Chen J, Deng J, Wang D, Xie Q, Wakimoto H, Hua L, Gong Y (2022) Progesterone receptor expression and prediction of benefits of adjuvant radiotherapy in de novo atypical meningiomas after gross-total resection. J Neurosurg. https://doi.org/10.3171/2022.9.JNS221530

    Article  PubMed  Google Scholar 

  7. Meta R, Boldt HB, Kristensen BW, Sahm F, Sjursen W, Torp SH (2021) The prognostic value of methylation signatures and NF2 mutations in atypical meningiomas. Cancers (Basel). https://doi.org/10.3390/cancers13061262

    Article  PubMed  Google Scholar 

  8. Bayoumi AB, Laviv Y, Karaali CN, Ertilav K, Kepoglu U, Toktas ZO, Konya D, Kasper EM (2020) Spinal meningiomas: 61 cases with predictors of early postoperative surgical outcomes. J Neurosurg Sci 64:446–451. https://doi.org/10.23736/S0390-5616.17.04102-9

    Article  PubMed  Google Scholar 

  9. Bodalal Z, Trebeschi S, Nguyen-Kim TDL, Schats W, Beets-Tan R (2019) Radiogenomics: bridging imaging and genomics. Abdom Radiol (NY) 44:1960–1984. https://doi.org/10.1007/s00261-019-02028-w

    Article  PubMed  Google Scholar 

  10. Lin BJ, Chou KN, Kao HW, Lin C, Tsai WC, Feng SW, Lee MS, Hueng DY (2014) Correlation between magnetic resonance imaging grading and pathological grading in meningioma. J Neurosurg 121:1201–1208. https://doi.org/10.3171/2014.7.JNS132359

    Article  PubMed  Google Scholar 

  11. Zhou M, Scott J, Chaudhury B, Hall L, Goldgof D, Yeom KW, Iv M, Ou Y, Kalpathy-Cramer J, Napel S, Gillies R, Gevaert O, Gatenby R (2018) Radiomics in brain tumor: image assessment, quantitative feature descriptors, and machine-learning approaches. AJNR Am J Neuroradiol 39:208–216. https://doi.org/10.3174/ajnr.A5391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hu J, Zhao Y, Li M, Liu J, Wang F, Weng Q, Wang X, Cao D (2020) Machine learning-based radiomics analysis in predicting the meningioma grade using multiparametric MRI. Eur J Radiol 131:109251. https://doi.org/10.1016/j.ejrad.2020.109251

    Article  PubMed  Google Scholar 

  13. Lambin P, Rios-Velazquez E, Leijenaar R, Carvalho S, van Stiphout RG, Granton P, Zegers CM, Gillies R, Boellard R, Dekker A, Aerts HJ (2012) Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer 48:441–446. https://doi.org/10.1016/j.ejca.2011.11.036

    Article  PubMed  PubMed Central  Google Scholar 

  14. Desseroit MC, Visvikis D, Tixier F, Majdoub M, Perdrisot R, Guillevin R, Cheze Le Rest C, Hatt M (2016) Development of a nomogram combining clinical staging with (18)F-FDG PET/CT image features in non-small-cell lung cancer stage I-III. Eur J Nucl Med Mol Imaging 43:1477–1485. https://doi.org/10.1007/s00259-016-3325-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Coroller TP, Agrawal V, Huynh E, Narayan V, Lee SW, Mak RH, Aerts H (2017) Radiomic-based pathological response prediction from primary tumors and lymph nodes in NSCLC. J Thorac Oncol 12:467–476. https://doi.org/10.1016/j.jtho.2016.11.2226

    Article  PubMed  Google Scholar 

  16. Jiang Y, Chen C, Xie J, Wang W, Zha X, Lv W, Chen H, Hu Y, Li T, Yu J, Zhou Z, Xu Y, Li G (2018) Radiomics signature of computed tomography imaging for prediction of survival and chemotherapeutic benefits in gastric cancer. EBioMedicine 36:171–182. https://doi.org/10.1016/j.ebiom.2018.09.007

    Article  PubMed  PubMed Central  Google Scholar 

  17. Yao Z, Dong Y, Wu G, Zhang Q, Yang D, Yu JH, Wang WP (2018) Preoperative diagnosis and prediction of hepatocellular carcinoma: Radiomics analysis based on multi-modal ultrasound images. BMC Cancer 18:1089. https://doi.org/10.1186/s12885-018-5003-4

    Article  PubMed  PubMed Central  Google Scholar 

  18. Xi IL, Zhao Y, Wang R, Chang M, Purkayastha S, Chang K, Huang RY, Silva AC, Vallieres M, Habibollahi P, Fan Y, Zou B, Gade TP, Zhang PJ, Soulen MC, Zhang Z, Bai HX, Stavropoulos SW (2020) Deep Learning to distinguish benign from malignant renal lesions based on routine MR imaging. Clin Cancer Res 26:1944–1952. https://doi.org/10.1158/1078-0432.CCR-19-0374

    Article  PubMed  Google Scholar 

  19. Niu L, Zhou X, Duan C, Zhao J, Sui Q, Liu X, Zhang X (2019) Differentiation researches on the meningioma subtypes by radiomics from contrast-enhanced magnetic resonance imaging: a preliminary study. World Neurosurg 126:e646–e652. https://doi.org/10.1016/j.wneu.2019.02.109

    Article  PubMed  Google Scholar 

  20. Hamerla G, Meyer HJ, Schob S, Ginat DT, Altman A, Lim T, Gihr GA, Horvath-Rizea D, Hoffmann KT, Surov A (2019) Comparison of machine learning classifiers for differentiation of grade 1 from higher gradings in meningioma: a multicenter radiomics study. Magn Reson Imaging 63:244–249. https://doi.org/10.1016/j.mri.2019.08.011

    Article  PubMed  Google Scholar 

  21. Zhang J, Yao K, Liu P, Liu Z, Han T, Zhao Z, Cao Y, Zhang G, Zhang J, Tian J, Zhou J (2020) A radiomics model for preoperative prediction of brain invasion in meningioma non-invasively based on MRI: a multicentre study. EBioMedicine 58:102933. https://doi.org/10.1016/j.ebiom.2020.102933

    Article  PubMed  PubMed Central  Google Scholar 

  22. Wolf I, Vetter M, Wegner I, Bottger T, Nolden M, Schobinger M, Hastenteufel M, Kunert T, Meinzer HP (2005) The medical imaging interaction toolkit. Med Image Anal 9:594–604. https://doi.org/10.1016/j.media.2005.04.005

    Article  PubMed  Google Scholar 

  23. Acharya UR, Dua S, Du X, Sree SV, Chua CK (2011) Automated diagnosis of glaucoma using texture and higher order spectra features. IEEE Trans Inf Technol Biomed 15:449–455. https://doi.org/10.1109/TITB.2011.2119322

    Article  PubMed  Google Scholar 

  24. Simon N, Friedman J, Hastie T, Tibshirani R (2011) Regularization paths for Cox’s proportional hazards model via coordinate descent. J Stat Softw 39:1–13. https://doi.org/10.18637/jss.v039.i05

    Article  PubMed  PubMed Central  Google Scholar 

  25. Harrell FE Jr, Lee KL, Mark DB (1996) Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med 15:361–387. https://doi.org/10.1002/(SICI)1097-0258(19960229)15:4%3c361::AID-SIM168%3e3.0.CO;2-4

    Article  PubMed  Google Scholar 

  26. Moons KG, Altman DG, Reitsma JB, Ioannidis JP, Macaskill P, Steyerberg EW, Vickers AJ, Ransohoff DF, Collins GS (2015) Transparent reporting of a multivariable prediction model for individual prognosis or diagnosis (TRIPOD): explanation and elaboration. Ann Intern Med 162:W1-73. https://doi.org/10.7326/M14-0698

    Article  PubMed  Google Scholar 

  27. Fitzgerald M, Saville BR, Lewis RJ (2015) Decision curve analysis. JAMA 313:409–410. https://doi.org/10.1001/jama.2015.37

    Article  CAS  PubMed  Google Scholar 

  28. Da Broi M, Borrelli P, Meling TR (2021) Predictors of survival in atypical meningiomas. Cancers (Basel). https://doi.org/10.3390/cancers13081970

    Article  PubMed  Google Scholar 

  29. Peeken JC, Hesse J, Haller B, Kessel KA, Nusslin F, Combs SE (2018) Semantic imaging features predict disease progression and survival in glioblastoma multiforme patients. Strahlenther Onkol 194:580–590. https://doi.org/10.1007/s00066-018-1276-4

    Article  PubMed  Google Scholar 

  30. Kim H, Lim DH, Kim TG, Lee JI, Nam DH, Seol HJ, Kong DS, Choi JW, Suh YL, Kim ST (2018) Leptomeningeal enhancement on preoperative brain MRI in patients with glioblastoma and its clinical impact. Asia Pac J Clin Oncol 14:e366–e373. https://doi.org/10.1111/ajco.12861

    Article  PubMed  Google Scholar 

  31. Chen XY, Chen JY, Huang YX, Xu JH, Sun WW, Chen Y, Ding CY, Wang SB, Wu XY, Kang DZ, You HH, Lin YX (2021) Establishment and validation of an integrated model to predict postoperative recurrence in patients with atypical meningioma. Front Oncol 11:754937. https://doi.org/10.3389/fonc.2021.754937

    Article  PubMed  PubMed Central  Google Scholar 

  32. Lin Y, Dai P, Lin Q, Chen J (2022) A predictive nomogram for atypical meningioma based on preoperative magnetic resonance imaging and routine blood tests. World Neurosurg 163:e610–e616. https://doi.org/10.1016/j.wneu.2022.04.034

    Article  PubMed  Google Scholar 

  33. Gu H, Zhang X, di Russo P, Zhao X, Xu T (2020) The current state of radiomics for meningiomas: promises and challenges. Front Oncol 10:567736. https://doi.org/10.3389/fonc.2020.567736

    Article  PubMed  PubMed Central  Google Scholar 

  34. Coroller TP, Bi WL, Huynh E, Abedalthagafi M, Aizer AA, Greenwald NF, Parmar C, Narayan V, Wu WW, Miranda de Moura S, Gupta S, Beroukhim R, Wen PY, Al-Mefty O, Dunn IF, Santagata S, Alexander BM, Huang RY, Aerts H (2017) Radiographic prediction of meningioma grade by semantic and radiomic features. PLoS ONE 12:e0187908. https://doi.org/10.1371/journal.pone.0187908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Park YW, Oh J, You SC, Han K, Ahn SS, Choi YS, Chang JH, Kim SH, Lee SK (2019) Radiomics and machine learning may accurately predict the grade and histological subtype in meningiomas using conventional and diffusion tensor imaging. Eur Radiol 29:4068–4076. https://doi.org/10.1007/s00330-018-5830-3

    Article  PubMed  Google Scholar 

  36. Zhu Y, Man C, Gong L, Dong D, Yu X, Wang S, Fang M, Wang S, Fang X, Chen X, Tian J (2019) A deep learning radiomics model for preoperative grading in meningioma. Eur J Radiol 116:128–134. https://doi.org/10.1016/j.ejrad.2019.04.022

    Article  PubMed  Google Scholar 

  37. Morin O, Chen WC, Nassiri F, Susko M, Magill ST, Vasudevan HN, Wu A, Vallieres M, Gennatas ED, Valdes G, Pekmezci M, Alcaide-Leon P, Choudhury A, Interian Y, Mortezavi S, Turgutlu K, Bush NAO, Solberg TD, Braunstein SE, Sneed PK, Perry A, Zadeh G, Mcdermott MW, Villanueva-Meyer JE, Raleigh DR (2019) Integrated models incorporating radiologic and radiomic features predict meningioma grade, local failure, and overall survival. Neurooncol Adv 1:11. https://doi.org/10.1093/noajnl/vdz011

    Article  Google Scholar 

  38. Zhang Y, Chen JH, Chen TY, Lim SW, Wu TC, Kuo YT, Ko CC, Su MY (2019) Radiomics approach for prediction of recurrence in skull base meningiomas. Neuroradiology 61:1355–1364. https://doi.org/10.1007/s00234-019-02259-0

    Article  PubMed  PubMed Central  Google Scholar 

  39. Li N, Mo Y, Huang C, Han K, He M, Wang X, Wen J, Yang S, Wu H, Dong F, Sun F, Li Y, Yu Y, Zhang M, Guan X, Xu X (2021) A clinical semantic and radiomics nomogram for predicting brain invasion in WHO grade II meningioma based on tumor and tumor-to-brain interface features. Front Oncol 11:752158. https://doi.org/10.3389/fonc.2021.752158

    Article  PubMed  PubMed Central  Google Scholar 

  40. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131:803–820. https://doi.org/10.1007/s00401-016-1545-1

    Article  PubMed  Google Scholar 

  41. Kalasauskas D, Kronfeld A, Renovanz M, Kurz E, Leukel P, Krenzlin H, Brockmann MA, Sommer CJ, Ringel F, Keric N (2020) Identification of high-risk atypical meningiomas according to semantic and radiomic features. Cancers (Basel). https://doi.org/10.3390/cancers12102942

    Article  PubMed  Google Scholar 

  42. Lohmann P, Galldiks N, Kocher M, Heinzel A, Filss CP, Stegmayr C, Mottaghy FM, Fink GR, Jon Shah N, Langen KJ (2021) Radiomics in neuro-oncology: basics, workflow, and applications. Methods 188:112–121. https://doi.org/10.1016/j.ymeth.2020.06.003

    Article  CAS  PubMed  Google Scholar 

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Acknowledements

We would like to express our gratitude to the Professor Ye gong, Doctor Lingyang Hua and Jiaojiao Deng for their financial support (National Natural Science Foundation of China: 82072788 to YG, 82203390 to LYH, 82203204 to JJD) and insightful discussions throughout the course of this study.

Funding

This work was supported by grants from the National Natural Science Foundation of China (82072788 to YG, 82203390 to LYH, 82203204 to JJD).

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Contributions

LR, JC, JD, XQ, HC, DW, JJ, HC, TAJ, HW, YG, LH contributed to the study conception and design. Material preparation, data collection and analysis were performed by [LR], [JC] and [LH]. The first draft of the manuscript was written by [LR] and all authors commented on previous versions of the manuscript. LR, JC, JD, XQ, HC, DW, JJ, HC, TAJ, HW, YG, LH read and approved the final manuscript.

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Correspondence to Ye Gong or Lingyang Hua.

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The authors have no relevant financial or non-financial interests to disclose.

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This clinical study was approved by the Human Subjects Institutional Review Board at Huashan Hospital, Fudan University.

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The consent process was omitted due to the retrospective nature of our study.

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The authors affirm that human research participants provided informed consent for publication of the images in Fig. 1.

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Ren, L., Chen, J., Deng, J. et al. The development of a combined clinico-radiomics model for predicting post-operative recurrence in atypical meningiomas: a multicenter study. J Neurooncol 166, 59–71 (2024). https://doi.org/10.1007/s11060-023-04511-3

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