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Published in: Journal of Neuro-Oncology 2/2018

01-11-2018 | Clinical Study

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

Authors: Yuqi Han, Zhen Xie, Yali Zang, Shuaitong Zhang, Dongsheng Gu, Mu Zhou, Olivier Gevaert, Jingwei Wei, Chao Li, Hongyan Chen, Jiang Du, Zhenyu Liu, Di Dong, Jie Tian, Dabiao Zhou

Published in: Journal of Neuro-Oncology | Issue 2/2018

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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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Literature
1.
go back to reference Chen B, Liang T, Yang P et al (2016) Classifying lower grade glioma cases according to whole genome gene expression. Oncotarget 7(45):74031–74042PubMedPubMedCentral Chen B, Liang T, Yang P et al (2016) Classifying lower grade glioma cases according to whole genome gene expression. Oncotarget 7(45):74031–74042PubMedPubMedCentral
2.
go back to reference 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 131:803–820CrossRefPubMed 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 131:803–820CrossRefPubMed
3.
go back to reference Network CGAR (2015) Comprehensive, integrative genomic analysis of diffuse low-grade gliomas. N Engl J Med 372:2481–2498CrossRef Network CGAR (2015) Comprehensive, integrative genomic analysis of diffuse low-grade gliomas. N Engl J Med 372:2481–2498CrossRef
4.
go back to reference 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 18:636–636CrossRefPubMed 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 18:636–636CrossRefPubMed
5.
go back to reference 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):16805–16817CrossRef 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):16805–16817CrossRef
7.
go back to reference 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 48:825–830CrossRefPubMed 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 48:825–830CrossRefPubMed
8.
go back to reference Ino Y, Betensky RA, Zlatescu MC et al (2001) Molecular subtypes of anaplastic oligodendroglioma. Clin Cancer Res 7:839–845PubMed Ino Y, Betensky RA, Zlatescu MC et al (2001) Molecular subtypes of anaplastic oligodendroglioma. Clin Cancer Res 7:839–845PubMed
9.
go back to reference 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 68:1831–1836CrossRefPubMed 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 68:1831–1836CrossRefPubMed
10.
go back to reference 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 145:1175–1190PubMedPubMedCentral 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 145:1175–1190PubMedPubMedCentral
13.
go back to reference Sanai N, Martino J, Berger MS (2012) Morbidity profile following aggressive resection of parietal lobe gliomas: clinical article. J Neurosurg 116:1182–1186CrossRefPubMed Sanai N, Martino J, Berger MS (2012) Morbidity profile following aggressive resection of parietal lobe gliomas: clinical article. J Neurosurg 116:1182–1186CrossRefPubMed
14.
go back to reference Tate MC, Kim C-Y, Chang EF et al (2011) Assessment of morbidity following resection of cingulate gyrus gliomas: clinical article. J Neurosurg 114:640–647CrossRefPubMed Tate MC, Kim C-Y, Chang EF et al (2011) Assessment of morbidity following resection of cingulate gyrus gliomas: clinical article. J Neurosurg 114:640–647CrossRefPubMed
15.
go back to reference Ducray F, Idbaih A, Reyniès AD et al (2008) Anaplastic oligodendrogliomas with 1p19q codeletion have a proneural gene expression profile. Mol Cancer 7(1):41CrossRefPubMedPubMedCentral Ducray F, Idbaih A, Reyniès AD et al (2008) Anaplastic oligodendrogliomas with 1p19q codeletion have a proneural gene expression profile. Mol Cancer 7(1):41CrossRefPubMedPubMedCentral
16.
go back to reference 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):34–42CrossRef 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):34–42CrossRef
17.
go back to reference Van den Bent MJ, Smits M, Kros JM et al (2017) Diffuse infiltrating oligodendroglioma and astrocytoma. J Clin Oncol 35(21):JCO2017726737 Van den Bent MJ, Smits M, Kros JM et al (2017) Diffuse infiltrating oligodendroglioma and astrocytoma. J Clin Oncol 35(21):JCO2017726737
18.
go back to reference 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):1884CrossRefPubMed 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):1884CrossRefPubMed
19.
go back to reference Megyesi JF, Kachur E, Lee DH et al (2004) Imaging correlates of molecular signatures in oligodendrogliomas. Clin Cancer Res 10:4303–4306CrossRefPubMed Megyesi JF, Kachur E, Lee DH et al (2004) Imaging correlates of molecular signatures in oligodendrogliomas. Clin Cancer Res 10:4303–4306CrossRefPubMed
22.
go back to reference Lambin P, Rios-Velazquez E, Leijenaar R et al (2012) Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer 48:441–446CrossRefPubMedPubMedCentral Lambin P, Rios-Velazquez E, Leijenaar R et al (2012) Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer 48:441–446CrossRefPubMedPubMedCentral
24.
go back to reference Zhou M, Hall L, Goldgof D et al (2014) Radiologically defined ecological dynamics and clinical outcomes in glioblastoma multiforme: preliminary results. Transl Oncol 7:5–13CrossRefPubMedPubMedCentral Zhou M, Hall L, Goldgof D et al (2014) Radiologically defined ecological dynamics and clinical outcomes in glioblastoma multiforme: preliminary results. Transl Oncol 7:5–13CrossRefPubMedPubMedCentral
25.
go back to reference 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):208–216PubMed 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):208–216PubMed
26.
go back to reference 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):115–123CrossRefPubMed 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):115–123CrossRefPubMed
27.
go back to reference Aerts HJWL, Velazquez ER, Leijenaar RTH et al (2014) Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun 5:4006CrossRefPubMedPubMedCentral Aerts HJWL, Velazquez ER, Leijenaar RTH et al (2014) Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun 5:4006CrossRefPubMedPubMedCentral
28.
go back to reference 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):947CrossRefPubMed 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):947CrossRefPubMed
29.
go back to reference 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 34:2157–2164CrossRefPubMed 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 34:2157–2164CrossRefPubMed
30.
go back to reference Henson JW, Gaviani P, Gonzalez RG (2005) MRI in treatment of adult gliomas. Lancet Oncol 6:167–175CrossRefPubMed Henson JW, Gaviani P, Gonzalez RG (2005) MRI in treatment of adult gliomas. Lancet Oncol 6:167–175CrossRefPubMed
31.
go back to reference Yushkevich PA, Piven J, Hazlett HC et al (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31:1116–1128CrossRefPubMed Yushkevich PA, Piven J, Hazlett HC et al (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31:1116–1128CrossRefPubMed
32.
go back to reference Gebejes A, Huertas R (2013) Texture characterization based on grey-level co-occurrence matrix. Proc Conf Inf Manag Sci 2:375–378 Gebejes A, Huertas R (2013) Texture characterization based on grey-level co-occurrence matrix. Proc Conf Inf Manag Sci 2:375–378
33.
go back to reference Galloway MM (1975) Texture analysis using gray level run lengths. Comput Graph Image Process 4:172–179CrossRef Galloway MM (1975) Texture analysis using gray level run lengths. Comput Graph Image Process 4:172–179CrossRef
34.
go back to reference Chu A, Sehgal CM, Greenleaf JF (1990) Use of gray value distribution of run lengths for texture analysis. Pattern Recognit Lett 11:415–419CrossRef Chu A, Sehgal CM, Greenleaf JF (1990) Use of gray value distribution of run lengths for texture analysis. Pattern Recognit Lett 11:415–419CrossRef
35.
go back to reference Dasarathy BV, Holder EB (1991) Image characterizations based on joint gray level run length distributions. Pattern Recognit Lett 12:497–502CrossRef Dasarathy BV, Holder EB (1991) Image characterizations based on joint gray level run length distributions. Pattern Recognit Lett 12:497–502CrossRef
36.
go back to reference Thibault G, Fertil B, Navarro C et al (2013) Shape and texture indexes application to cell nuclei classification. Int J Pattern Recognit Artif Intell 27:1357002CrossRef Thibault G, Fertil B, Navarro C et al (2013) Shape and texture indexes application to cell nuclei classification. Int J Pattern Recognit Artif Intell 27:1357002CrossRef
37.
go back to reference Amadasun M, King R (1989) Textural features corresponding to textural properties. IEEE Trans Syst Man Cybern 19:1264–1274CrossRef Amadasun M, King R (1989) Textural features corresponding to textural properties. IEEE Trans Syst Man Cybern 19:1264–1274CrossRef
38.
go back to reference Kim SH, Kim H, Kim TS (2005) Clinical, histological, and immunohistochemical features predicting 1p/19q loss of heterozygosity in oligodendroglial tumors. Acta Neuropathol 110:27–38CrossRefPubMed Kim SH, Kim H, Kim TS (2005) Clinical, histological, and immunohistochemical features predicting 1p/19q loss of heterozygosity in oligodendroglial tumors. Acta Neuropathol 110:27–38CrossRefPubMed
39.
go back to reference DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845CrossRef DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845CrossRef
40.
go back to reference Louis BN, Jana P, Joachim B et al (2018) NCCN Guidelines Version 1.2018 Panel Members Central Nervous System Cancers. National Comprehensive Cancer Network 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.
go back to reference 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):340–351CrossRefPubMed 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):340–351CrossRefPubMed
42.
go back to reference Chahlavi A, Kanner A, Peereboom D et al (2003) Impact of chromosome 1p status in response of oligodendroglioma to temozolomide: preliminary results. J Neurooncol 61:267–273CrossRefPubMed Chahlavi A, Kanner A, Peereboom D et al (2003) Impact of chromosome 1p status in response of oligodendroglioma to temozolomide: preliminary results. J Neurooncol 61:267–273CrossRefPubMed
43.
go back to reference Alattar AA, Brandel MG, Hirshman BR et al (2017) Oligodendroglioma resection: a surveillance, epidemiology, and end results (SEER) analysis. J Neurosurg 128:1076–1083CrossRef Alattar AA, Brandel MG, Hirshman BR et al (2017) Oligodendroglioma resection: a surveillance, epidemiology, and end results (SEER) analysis. J Neurosurg 128:1076–1083CrossRef
44.
go back to reference 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):5732CrossRefPubMedPubMedCentral 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):5732CrossRefPubMedPubMedCentral
45.
go back to reference 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 14:2357–2362CrossRefPubMed 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 14:2357–2362CrossRefPubMed
46.
go back to reference Sanai N, Chang S, Berger MS (2011) Low-grade gliomas in adults: a review. J Neurosurg 115:1–18 Sanai N, Chang S, Berger MS (2011) Low-grade gliomas in adults: a review. J Neurosurg 115:1–18
Metadata
Title
Non-invasive genotype prediction of chromosome 1p/19q co-deletion by development and validation of an MRI-based radiomics signature in lower-grade gliomas
Authors
Yuqi Han
Zhen Xie
Yali Zang
Shuaitong Zhang
Dongsheng Gu
Mu Zhou
Olivier Gevaert
Jingwei Wei
Chao Li
Hongyan Chen
Jiang Du
Zhenyu Liu
Di Dong
Jie Tian
Dabiao Zhou
Publication date
01-11-2018
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 2/2018
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-018-2953-y

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