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Non-invasive genotype prediction of chromosome 1p/19q co-deletion by development and validation of an MRI-based radiomics signature in lower-grade gliomas

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Abstract

Purpose

To perform radiomics analysis for non-invasively predicting chromosome 1p/19q co-deletion in World Health Organization grade II and III (lower-grade) gliomas.

Methods

This retrospective study included 277 patients histopathologically diagnosed with lower-grade glioma. Clinical parameters were recorded for each patient. We performed a radiomics analysis by extracting 647 MRI-based features and applied the random forest algorithm to generate a radiomics signature for predicting 1p/19q co-deletion in the training cohort (n = 184). The clinical model consisted of pertinent clinical factors, and was built using a logistic regression algorithm. A combined model, incorporating both the radiomics signature and related clinical factors, was also constructed. The receiver operating characteristics curve was used to evaluate the predictive performance. We further validated the predictability of the three developed models using a time-independent validation cohort (n = 93).

Results

The radiomics signature was constructed as an independent predictor for differentiating 1p/19q co-deletion genotypes, which demonstrated superior performance on both the training and validation cohorts with areas under curve (AUCs) of 0.887 and 0.760, respectively. These results outperformed the clinical model (AUCs of 0.580 and 0.627 on training and validation cohorts). The AUCs of the combined model were 0.885 and 0.753 on training and validation cohorts, respectively, which indicated that clinical factors did not present additional improvement for the prediction.

Conclusion

Our study highlighted that an MRI-based radiomics signature can effectively identify the 1p/19q co-deletion in histopathologically diagnosed lower-grade gliomas, thereby offering the potential to facilitate non-invasive molecular subtype prediction of gliomas.

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References

  1. Chen B, Liang T, Yang P et al (2016) Classifying lower grade glioma cases according to whole genome gene expression. Oncotarget 7(45):74031–74042

    PubMed  PubMed Central  Google Scholar 

  2. 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  PubMed  Google Scholar 

  3. Network CGAR (2015) Comprehensive, integrative genomic analysis of diffuse low-grade gliomas. N Engl J Med 372:2481–2498

    Article  CAS  Google Scholar 

  4. Smith JS, Perry A, Borell TJ et al (2000) Alterations of chromosome arms 1p Fand 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol 18:636–636

    Article  CAS  PubMed  Google Scholar 

  5. Lindberg N, Jiang Y, Xie Y et al (2013) Oncogenic signaling is dominant to cell of origin and dictates astrocytic or oligodendroglial tumor development from oligodendrocyte precursor cells. J Neurosci 33(42):16805–16817

    Article  CAS  Google Scholar 

  6. Appin CL, Brat DJ (2014) Molecular genetics of gliomas. Cancer J 20(1):66

    Article  CAS  PubMed  Google Scholar 

  7. Bauman G, Ino Y, Ueki K et al (2000) Allelic loss of chromosome 1p and radiotherapy plus chemotherapy in patients with oligodendrogliomas. Int J Radiat Oncol Biol Phys 48:825–830

    Article  CAS  PubMed  Google Scholar 

  8. Ino Y, Betensky RA, Zlatescu MC et al (2001) Molecular subtypes of anaplastic oligodendroglioma. Clin Cancer Res 7:839–845

    CAS  PubMed  Google Scholar 

  9. Kaloshi G, Benouaich-Amiel A, Diakite F et al (2007) Temozolomide for low-grade gliomas predictive impact of 1p/19q loss on response and outcome. Neurology 68:1831–1836

    Article  CAS  PubMed  Google Scholar 

  10. Reifenberger J, Reifenberger G, Liu L et al (1994) Molecular genetic analysis of oligodendroglial tumors shows preferential allelic deletions on 19q and 1p. Am J Pathol 145:1175–1190

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Theeler BJ, Yung WA, Fuller GN et al (2012) Moving toward molecular classification of diffuse gliomas in adults. Neurology 79:1917–1926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Woehrer A, Hainfellner JA (2015) Molecular diagnostics: techniques and recommendations for 1p/19q assessment. CNS Oncol 4:295–306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Sanai N, Martino J, Berger MS (2012) Morbidity profile following aggressive resection of parietal lobe gliomas: clinical article. J Neurosurg 116:1182–1186

    Article  PubMed  Google Scholar 

  14. Tate MC, Kim C-Y, Chang EF et al (2011) Assessment of morbidity following resection of cingulate gyrus gliomas: clinical article. J Neurosurg 114:640–647

    Article  PubMed  Google Scholar 

  15. Ducray F, Idbaih A, Reyniès AD et al (2008) Anaplastic oligodendrogliomas with 1p19q codeletion have a proneural gene expression profile. Mol Cancer 7(1):41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Mukasa A, Ueki K, Ge X et al (2010) Selective expression of a subset of neuronal genes in oligodendroglioma with chromosome 1p loss. Brain Pathol 14(1):34–42

    Article  Google Scholar 

  17. Van den Bent MJ, Smits M, Kros JM et al (2017) Diffuse infiltrating oligodendroglioma and astrocytoma. J Clin Oncol 35(21):JCO2017726737

    Google Scholar 

  18. Jenkinson MD, Du PD, Smith TS et al (2006) Histological growth patterns and genotype in oligodendroglial tumours: correlation with MRI features. Brain 129(Pt 7):1884

    Article  PubMed  Google Scholar 

  19. Megyesi JF, Kachur E, Lee DH et al (2004) Imaging correlates of molecular signatures in oligodendrogliomas. Clin Cancer Res 10:4303–4306

    Article  PubMed  Google Scholar 

  20. Patel SH, Poisson LM, Brat DJ et al (2017) T2-FLAIR mismatch, an imaging biomarker for IDH and 1p/19q status in lower grade gliomas: a TCGA/TCIA project. Clin Cancer Res. https://doi.org/10.1158/1078-0432.CCR-17-0560

    Article  PubMed  PubMed Central  Google Scholar 

  21. Mpg B, Smits M, Mmj W et al (2018) The T2-FLAIR mismatch sign as an imaging marker for non-enhancing IDH-mutant, 1p/19q-intact lower grade glioma: a validation study. Neuro Oncol. https://doi.org/10.1093/neuonc/noy048

    Article  Google Scholar 

  22. Lambin P, Rios-Velazquez E, Leijenaar R et al (2012) Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer 48:441–446

    Article  PubMed  PubMed Central  Google Scholar 

  23. Kumar V, Gu Y, Basu S et al (2012) Radiomics: the process and the challenges. Magn Reson Imaging 30:1234–1248

    Article  PubMed  PubMed Central  Google Scholar 

  24. Zhou M, Hall L, Goldgof D et al (2014) Radiologically defined ecological dynamics and clinical outcomes in glioblastoma multiforme: preliminary results. Transl Oncol 7:5–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Zhou M, Scott J, Chaudhury B et al (2017) Radiomics in brain tumor: image assessment, quantitative feature descriptors, and machine-learning approaches. Am J Neuroradiol 39(12):208–216

    PubMed  Google Scholar 

  26. Zhou M, Chaudhury B, Hall LO et al (2017) Identifying spatial imaging biomarkers of glioblastoma multiforme for survival group prediction. J Magn Reson Imaging 46(1):115–123

    Article  PubMed  Google Scholar 

  27. Aerts HJWL, Velazquez ER, Leijenaar RTH et al (2014) Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun 5:4006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Huang YQ, Liu ZY et al (2016) Radiomics signature: a potential biomarker for the prediction of disease-free survival in early-stage (I or II) non-small cell lung cancer. Radiology 281(3):947

    Article  PubMed  Google Scholar 

  29. Huang YQ, Liang CH, He L et al (2016) Development and validation of a radiomics nomogram for preoperative prediction of lymph node metastasis in colorectal cancer. J Clin Oncol 34:2157–2164

    Article  PubMed  Google Scholar 

  30. Henson JW, Gaviani P, Gonzalez RG (2005) MRI in treatment of adult gliomas. Lancet Oncol 6:167–175

    Article  PubMed  Google Scholar 

  31. Yushkevich PA, Piven J, Hazlett HC et al (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31:1116–1128

    Article  PubMed  Google Scholar 

  32. Gebejes A, Huertas R (2013) Texture characterization based on grey-level co-occurrence matrix. Proc Conf Inf Manag Sci 2:375–378

    Google Scholar 

  33. Galloway MM (1975) Texture analysis using gray level run lengths. Comput Graph Image Process 4:172–179

    Article  Google Scholar 

  34. Chu A, Sehgal CM, Greenleaf JF (1990) Use of gray value distribution of run lengths for texture analysis. Pattern Recognit Lett 11:415–419

    Article  Google Scholar 

  35. Dasarathy BV, Holder EB (1991) Image characterizations based on joint gray level run length distributions. Pattern Recognit Lett 12:497–502

    Article  Google Scholar 

  36. Thibault G, Fertil B, Navarro C et al (2013) Shape and texture indexes application to cell nuclei classification. Int J Pattern Recognit Artif Intell 27:1357002

    Article  Google Scholar 

  37. Amadasun M, King R (1989) Textural features corresponding to textural properties. IEEE Trans Syst Man Cybern 19:1264–1274

    Article  Google Scholar 

  38. Kim SH, Kim H, Kim TS (2005) Clinical, histological, and immunohistochemical features predicting 1p/19q loss of heterozygosity in oligodendroglial tumors. Acta Neuropathol 110:27–38

    Article  CAS  PubMed  Google Scholar 

  39. DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845

    Article  CAS  Google Scholar 

  40. Louis BN, Jana P, Joachim B et al (2018) NCCN Guidelines Version 1.2018 Panel Members Central Nervous System Cancers. National Comprehensive Cancer Network

  41. Buckner J, Giannini C, Eckelpassow J et al (2017) Management of diffuse low-grade gliomas in adults - use of molecular diagnostics. Nat Rev Neurol 13(6):340–351

    Article  CAS  PubMed  Google Scholar 

  42. Chahlavi A, Kanner A, Peereboom D et al (2003) Impact of chromosome 1p status in response of oligodendroglioma to temozolomide: preliminary results. J Neurooncol 61:267–273

    Article  PubMed  Google Scholar 

  43. Alattar AA, Brandel MG, Hirshman BR et al (2017) Oligodendroglioma resection: a surveillance, epidemiology, and end results (SEER) analysis. J Neurosurg 128:1076–1083

    Article  Google Scholar 

  44. Yang XF et al (2012) Ultrasound GLCM texture analysis of radiation-induced parotid-gland injury in head-and-neck cancer radiotherapy: an in vivo study of late toxicity. Med Phys 39(9):5732

    Article  PubMed  PubMed Central  Google Scholar 

  45. Brown R, Zlatescu M, Sijben A et al (2008) The use of magnetic resonance imaging to noninvasively detect genetic signatures in oligodendroglioma. Clin Cancer Res 14:2357–2362

    Article  CAS  PubMed  Google Scholar 

  46. Sanai N, Chang S, Berger MS (2011) Low-grade gliomas in adults: a review. J Neurosurg 115:1–18

    Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China under Grant Numbers 81227901, 81527805, 81501616, and 81771924, the National Key Research and Development Program of China Grant under Grant Number 2106YFC0103702 and 2017YFA0205200. Olivier Gevaert is supported by the National Institute of Biomedical Imaging And Bioengineering of the National Institutes of Health under Award Number R01EB020527. The authors would like to express their deep appreciation to all anonymous reviewers for their kind comments.

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Correspondence to Di Dong, Jie Tian or Dabiao Zhou.

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Han, Y., Xie, Z., Zang, Y. et al. Non-invasive genotype prediction of chromosome 1p/19q co-deletion by development and validation of an MRI-based radiomics signature in lower-grade gliomas. J Neurooncol 140, 297–306 (2018). https://doi.org/10.1007/s11060-018-2953-y

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