Skip to main content
Log in

Machine learning and radiomic phenotyping of lower grade gliomas: improving survival prediction

  • Neuro
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Background and purpose

Recent studies have highlighted the importance of isocitrate dehydrogenase (IDH) mutational status in stratifying biologically distinct subgroups of gliomas. This study aimed to evaluate whether MRI-based radiomic features could improve the accuracy of survival predictions for lower grade gliomas over clinical and IDH status.

Materials and methods

Radiomic features (n = 250) were extracted from preoperative MRI data of 296 lower grade glioma patients from databases at our institutional (n = 205) and The Cancer Genome Atlas (TCGA)/The Cancer Imaging Archive (TCIA) (n = 91) datasets. For predicting overall survival, random survival forest models were trained with radiomic features; non-imaging prognostic factors including age, resection extent, WHO grade, and IDH status on the institutional dataset, and validated on the TCGA/TCIA dataset. The performance of the random survival forest (RSF) model and incremental value of radiomic features were assessed by time-dependent receiver operating characteristics.

Results

The radiomics RSF model identified 71 radiomic features to predict overall survival, which were successfully validated on TCGA/TCIA dataset (iAUC, 0.620; 95% CI, 0.501–0.756). Relative to the RSF model from the non-imaging prognostic parameters, the addition of radiomic features significantly improved the overall survival prediction accuracy of the random survival forest model (iAUC, 0.627 vs. 0.709; difference, 0.097; 95% CI, 0.003–0.209).

Conclusion

Radiomic phenotyping with machine learning can improve survival prediction over clinical profile and genomic data for lower grade gliomas.

Key Points

• Radiomics analysis with machine learning can improve survival prediction over the non-imaging factors (clinical and molecular profiles) for lower grade gliomas, across different institutions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

FLAIR:

Fluid-attenuated inversion recovery

iAUC:

Integrated area under the ROC curve

IDH:

Isocitrate dehydrogenase

IRB:

Institutional research board

LGG:

Lower grade glioma

OS:

Overall survival

RF:

Random forest

ROC:

Receiver operating characteristics

RSF:

Random survival forest

T1C:

T1-weighted contrast-enhanced

T2:

T2-weighted

TCGA:

The Cancer Genome Atlas

TCIA:

The Cancer Imaging Archive

TE:

Echo time

TR:

Repetition time

References

  1. Hess KR, Broglio KR, Bondy ML (2004) Adult glioma incidence trends in the United States, 1977–2000. Cancer 101:2293–2299

    Article  Google Scholar 

  2. Cancer Genome Atlas Research N, Brat DJ, Verhaak RG et al (2015) Comprehensive, integrative genomic analysis of diffuse lower-grade Gliomas. N Engl J Med 372:2481–2498

    Article  Google Scholar 

  3. Pignatti F, van den Bent M, Curran D et al (2002) Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 20:2076–2084

    Article  Google Scholar 

  4. Schomas DA, Laack NN, Rao RD et al (2009) Intracranial low-grade gliomas in adults: 30-year experience with long-term follow-up at Mayo Clinic. Neuro-Oncol 11:437–445

    Article  Google Scholar 

  5. Zhao S, Lin Y, Xu W et al (2009) Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1α. Science 324:261–265

    Article  CAS  Google Scholar 

  6. Yan H, Parsons DW, Jin G et al (2009) IDH1 and IDH2 mutations in gliomas. N Engl J Med 360:765–773

    Article  CAS  Google Scholar 

  7. Parsons DW, Jones S, Zhang X et al (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321:1807–1812

    Article  CAS  Google Scholar 

  8. Wang Y, Wang K, Wang J et al (2016) Identifying the association between contrast enhancement pattern, surgical resection, and prognosis in anaplastic glioma patients. Neuroradiology 58:367–374

    Article  Google Scholar 

  9. Pope WB, Sayre J, Perlina A, Villablanca JP, Mischel PS, Cloughesy TF (2005) MR imaging correlates of survival in patients with high-grade Gliomas. AJNR Am J Neuroradiol 26:2466–2474

    PubMed  Google Scholar 

  10. Wang YY, Wang K, Li SW et al (2015) Patterns of tumor contrast enhancement predict the prognosis of anaplastic Gliomas with IDH1 mutation. Am J Neuroradiol 36:2023–2029

    Article  CAS  Google Scholar 

  11. Gillies RJ, Kinahan PE, Hricak H (2015) Radiomics: images are more than pictures, they are data. Radiology 278:563–577

    Article  Google Scholar 

  12. Kickingereder P, Burth S, Wick A et al (2016) Radiomic profiling of glioblastoma: identifying an imaging predictor of patient survival with improved performance over established clinical and radiologic risk models. Radiology 280:880–889

    Article  Google Scholar 

  13. Macyszyn L, Akbari H, Pisapia JM et al (2015) Imaging patterns predict patient survival and molecular subtype in glioblastoma via machine learning techniques. Neuro-oncology 18:417–425

    Article  Google Scholar 

  14. Zhang B, Chang K, Ramkissoon S et al (2017) Multimodal MRI features predict isocitrate dehydrogenase genotype in high-grade gliomas. Neuro-Oncology 19:109–117

    Article  CAS  Google Scholar 

  15. Ceccarelli M, Barthel FP, Malta TM et al (2016) Molecular profiling reveals biologically discrete subsets and pathways of progression in diffuse Glioma. Cell 164:550–563

    Article  CAS  Google Scholar 

  16. Shinohara RT, Sweeney EM, Goldsmith J et al (2014) Statistical normalization techniques for magnetic resonance imaging. Neuroimage Clin 6:9–19

    Article  Google Scholar 

  17. van Griethuysen JJM, Fedorov A, Parmar C et al (2017) Computational Radiomics system to decode the radiographic phenotype. Cancer Res 77:e104–e107

    Article  Google Scholar 

  18. Ishwaran H, Kogalur UB, Blackstone EH, Lauer MS (2008) Random survival forests. Ann Appl Stat 2:841–860

    Article  Google Scholar 

  19. Ishwaran H, Kogalur UB, Chen X, Minn AJ (2011) Random survival forests for highdimensional data. Stat Anal Data Min 4:115–132

    Article  Google Scholar 

  20. Carpenter J, Bithell J (2000) Bootstrap confidence intervals: when, which, what? A practical guide for medical statisticians. Stat Med 19:1141–1164

    Article  CAS  Google Scholar 

  21. Heagerty PJ, Zheng Y (2005) Survival model predictive accuracy and ROC curves. Biometrics 61:92–105

    Article  Google Scholar 

  22. Wasserstein RL, Lazar NA (2016) The ASA’s statement on p-values: context, process, and purpose. Am Stat 70:129–133

    Article  Google Scholar 

  23. Zhou H, Vallieres M, Bai HX et al (2017) MRI features predict survival and molecular markers in diffuse lower-grade gliomas. Neuro-Oncology 19:862–870

    Article  CAS  Google Scholar 

  24. Kickingereder P, Neuberger U, Bonekamp D et al (2017) Radiomic subtyping improves disease stratification beyond key molecular, clinical, and standard imaging characteristics in patients with glioblastoma. Neuro-oncology 20:848–857

    Article  Google Scholar 

  25. Liu X, Li Y, Qian Z et al (2018) A radiomic signature as a non-invasive predictor of progression-free survival in patients with lower-grade gliomas. NeuroImage: Clinical 20:1070–1077

    Article  Google Scholar 

  26. Louis DN, Perry A, Reifenberger G et al (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131:803–820

    Article  Google Scholar 

  27. Yan H, Parsons DW, Jin G et al (2009) IDH1 and IDH2 mutations in gliomas. N Engl J Med 360:765–773

    Article  CAS  Google Scholar 

  28. Bae S, Choi YS, Ahn SS et al (2018) Radiomic MRI phenotyping of glioblastoma: improving survival prediction. Radiology 289:797–806

    Article  Google Scholar 

  29. Chaddad A, Desrosiers C, Hassan L, Tanougast C (2016) A quantitative study of shape descriptors from glioblastoma multiforme phenotypes for predicting survival outcome. Br J Radiol 89:20160575

    Article  Google Scholar 

  30. Pérez-Beteta J, Molina-García D, Ortiz-Alhambra JA et al (2018) Tumor surface regularity at MR imaging predicts survival and response to surgery in patients with glioblastoma. Radiology 288:218–225

    Article  Google Scholar 

  31. Ellingson BM, Lai A, Harris RJ et al (2013) Probabilistic radiographic atlas of glioblastoma phenotypes. Am J Neuroradiol 34:533–540

    Article  CAS  Google Scholar 

Download references

Funding

This research received funding from the Basic Science Research Program through the National Research Foundation of Korea which is funded by the Ministry of Science, ICT & Future Planning (2017R1D1A1B03030440). This study was also supported by a faculty research grant from the Yonsei University College of Medicine (6-2016-0121) and by DongKook Life Science. Co., Ltd., Republic of Korea.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sung Soo Ahn.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Sung Soo Ahn.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

The statistical methodology of this study was reviewed by Kyunghwa Han, Yonsei University College of Medicine.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• Retrospective

• Cross-sectional study

• Multi-center study

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 34 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Choi, Y.S., Ahn, S.S., Chang, J.H. et al. Machine learning and radiomic phenotyping of lower grade gliomas: improving survival prediction. Eur Radiol 30, 3834–3842 (2020). https://doi.org/10.1007/s00330-020-06737-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-020-06737-5

Keywords

Navigation