Abstract
Introduction
Being the most common primary brain tumor, glioblastoma presents as an extremely challenging malignancy to treat with dismal outcomes despite treatment. Varying molecular epidemiology of glioblastoma between patients and intra-tumoral heterogeneity explains the failure of current one-size-fits-all treatment modalities. Radiomics uses machine learning to identify salient features of the tumor on brain imaging and promises patient-specific management in glioblastoma patients.
Methods
We performed a comprehensive review of the available literature on studies investigating the role of radiomics and radiogenomics models for the diagnosis, stratification, prognostication as well as treatment planning and monitoring of glioblastoma.
Results
Classifiers based on a combination of various MRI sequences, genetic information and clinical data can predict non-invasive tumor diagnosis, overall survival and treatment response with reasonable accuracy. However, the use of radiomics for glioblastoma treatment remains in infancy as larger sample sizes, standardized image acquisition and data extraction techniques are needed to develop machine learning models that can be translated effectively into clinical practice.
Conclusion
Radiomics has the potential to transform the scope of glioblastoma management through personalized medicine.
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Data availability
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Code availability
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References
Tykocki T, Eltayeb M (2018) Ten-year survival in glioblastoma. A systematic Review. J Clin Neurosci 54:7–13
Hobbs SK, Shi G, Homer R, Harsh G, Atlas SW, Bednarski MD (2003) Magnetic resonance image-guided proteomics of human glioblastoma multiforme. J MagnReson Imaging 18(5):530–536
Ellingson BM (2015) Radiogenomics and imaging phenotypes in glioblastoma: novel observations and correlation with molecular characteristics. CurrNeurolNeurosci Rep 15(1):506
ElBanan MG, Amer AM, Zinn PO, Colen RR (2015) Imaging genomics of Glioblastoma: state of the art bridge between genomics and neuroradiology. Neuroimaging Clin N Am 25(1):141–153
Verduin M, Compter I, Steijvers D, Postma AA, Eekers DBP, Anten MM et al (2018) Noninvasive glioblastoma testing: multimodal approach to monitoring and predicting treatment response. Dis Markers 2018:2908609
Olar A, Aldape KD (2014) Using the molecular classification of glioblastoma to inform personalized treatment. J Pathol 232(2):165–177
Sotoudeh H, Shafaat O, Bernstock JD, Brooks MD, Elsayed GA, Chen JA et al (2019) Artificial intelligence in the management of glioma: era of personalized medicine. Front Oncol 9:768
Chaddad A, Kucharczyk MJ, Daniel P, Sabri S, Jean-Claude BJ, Niazi T, Abdulkarim B (2019) Radiomics in glioblastoma: current status and challenges facing clinical implementation. Front Oncol 21(9):374
Lambin P, Leijenaar RTH, Deist TM, Peerlings J, de Jong EEC, van Timmeren J et al (2017) Radiomics: the bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol 14(12):749–762
Pinker K, Shitano F, Sala E, Do RK, Young RJ, Wibmer AG et al (2018) Background, current role, and potential applications of radiogenomics. J MagnReson Imaging 47(3):604–620
Artzi M, Bressler I, Bashat DB (2019) Differentiation between glioblastoma, brain metastasis and subtypes using radiomics analysis. J Magn Reson Imaging 50(2):519–528
Bae S, An C, Ahn SS, Kim H, Han K, Kim SW et al (2020) Robust performance of deep learning for distinguishing glioblastoma from single brain metastasis using radiomic features: model development and validation. Sci Rep 21:10
Barajas RF, Phillips JJ, Parvataneni R, Molinaro A, Essock-Burns E, Bourne G et al (2012) Regional variation in histopathologic features of tumor specimens from treatment-naive glioblastoma correlates with anatomic and physiologic MR Imaging. Neuro Oncol 14(7):942–954
Cho HH, Lee SH, Kim J, Park H (2018) Classification of the glioma grading using radiomics analysis. PeerJ. 22(6):e5982
Colen RR, Vangel M, Wang J, Gutman DA, Hwang SN, Wintermark M et al (2014) Imaging genomic mapping of an invasive MRI phenotype predicts patient outcome and metabolic dysfunction: a TCGA glioma phenotype research group project. BMC Med Genomics 2(7):30
Drabycz S, Roldán G, de Robles P, Adler D, McIntyre JB, Magliocco AM et al (2010) An analysis of image texture, tumor location, and MGMT promoter methylation in glioblastoma using magnetic resonance imaging. Neuroimage 49(2):1398–1405
Ellingson BM, Lai A, Harris RJ, Selfridge JM, Yong WH, Das K et al (2013) Probabilistic radiographic atlas of glioblastoma phenotypes. AJNR Am J Neuroradiol 34(3):533–540
Gutman DA, Dunn WD, Grossmann P, Cooper LAD, Holder CA, Ligon KL et al (2015) Somatic mutations associated with MRI-derived volumetric features in glioblastoma. Neuroradiology 57(12):1227–1237
Jeong J, Wang L, Ji B, Lei Y, Ali A, Liu T et al (2019) Machine-learning based classification of glioblastoma using delta-radiomic features derived from dynamic susceptibility contrast enhanced magnetic resonance images: Introduction. Quant Imaging Med Surg 9(7):1201–1213
Hajianfar G, Shiri I, Maleki H, Oveisi N, Haghparast A, Abdollahi H et al (2019) Noninvasive O6 methylguanine-DNA methyltransferase status prediction in glioblastoma multiforme cancer using magnetic resonance imaging radiomics features: univariate and multivariate radiogenomics analysis. World Neurosurg 1(132):e140–e161
Korfiatis P, Kline TL, Coufalova L, Lachance DH, Parney IF, Carter RE et al (2016) MRI texture features as biomarkers to predict MGMT methylation status in glioblastomas. Med Phys 43(6):2835–2844
Kong D-S, Kim J, Lee I-H, Kim ST, Seol HJ, Lee J-I et al (2016) Integrative radiogenomic analysis for multicentric radiophenotype in glioblastoma. Oncotarget 7(10):11526–11538
Lee MH, Kim J, Kim S-T, Shin H-M, You H-J, Choi JW et al (2019) Prediction of IDH1 mutation status in glioblastoma using machine learning technique based on quantitative radiomic data. World Neurosurg 125:e688–e696
Li Z-C, Bai H, Sun Q, Li Q, Liu L, Zou Y et al (2018) Multiregional radiomics features from multiparametric MRI for prediction of MGMT methylation status in glioblastoma multiforme: a multicentre study. EurRadiol 28(9):3640–3650
Lin X, Lee M, Buck O, Woo KM, Zhang Z, Hatzoglou V et al (2017) Diagnostic accuracy of T1-weighted DCE-MRI and DWI-ADC for differentiation of glioblastoma and primary CNS lymphoma. AJNR Am J Neuroradiol 38(3):485–491
Suh HB, Choi YS, Bae S, Ahn SS, Chang JH, Kang S-G et al (2018) Primary central nervous system lymphoma and atypical glioblastoma: differentiation using radiomics approach. EurRadiol 28(9):3832–3839
Naeini KM, Pope WB, Cloughesy TF, Harris RJ, Lai A, Eskin A et al (2013) Identifying the mesenchymal molecular subtype of glioblastoma using quantitative volumetric analysis of anatomic magnetic resonance images. Neuro Oncol 15(5):626–634
Nakamoto T, Takahashi W, Haga A, Takahashi S, Kiryu S, Nawa K et al (2019) Prediction of malignant glioma grades using contrast-enhanced T1-weighted and T2-weighted magnetic resonance images based on a radiomic analysis. Sci Rep 9(1):19411
Pope WB, Mirsadraei L, Lai A, Eskin A, Qiao J, Kim HJ et al (2012) Differential gene expression in glioblastoma defined by ADC histogram analysis: relationship to extracellular matrix molecules and survival. AJNR Am J Neuroradiol 33(6):1059–1064
Rathore S, Akbari H, Rozycki M, Abdullah KG, Nasrallah MP, Binder ZA et al (2018) Radiomic MRI signature reveals three distinct subtypes of glioblastoma with different clinical and molecular characteristics, offering prognostic value beyond IDH1. Sci Rep 8(1):5087
Sasaki T, Kinoshita M, Fujita K, Fukai J, Hayashi N, Uematsu Y et al (2019) Radiomics and MGMT promoter methylation for prognostication of newly diagnosed glioblastoma. Sci Rep 9(1):14435
Tian Q, Yan L-F, Zhang X, Zhang X, Hu Y-C, Han Y et al (2018) Radiomics strategy for glioma grading using texture features from multiparametric MRI. J MagnReson Imaging 48(6):1518–1528
Xi Y, Guo F, Xu Z, Li C, Wei W, Tian P et al (2018) Radiomics signature: A potential biomarker for the prediction of MGMT promoter methylation in glioblastoma. J Magn Reson Imaging 47(5):1380–1387
Zhang X, Yan L-F, Hu Y-C, Li G, Yang Y, Han Y et al (2017) Optimizing a machine learning based glioma grading system using multi-parametric MRI histogram and texture features. Oncotarget 8(29):47816–47830
Zinn PO, Sathyan P, Mahajan B, Bruyere J, Hegi M, Majumder S et al (2012) A novel volume-age-KPS (VAK) glioblastoma classification identifies a prognostic cognate microRNA-gene signature. PLoS One. 7(8):e41522
Zinn PO, Mahajan B, Majadan B, Sathyan P, Singh SK, Majumder S et al (2011) Radiogenomic mapping of edema/cellular invasion MRI-phenotypes in glioblastoma multiforme. PLoS One. 6(10):e25451
Shin I, Kim H, Ahn SS, Sohn B, Bae S, Park JE, Kim HS, Lee SK (2021) Development and validation of a deep learning-based model to distinguish glioblastoma from solitary brain metastasis using conventional MR images. Am J Neuroradiol 42(5):838–844
Lim DA, Cha S, Mayo MC, Chen M-H, Keles E, VandenBerg S, Berger MS (2007) Relationship of glioblastoma multiforme to neural stem cell regions predicts invasive and multifocal tumor phenotype. Neuro Oncol 9(4):424–429
Gutman DA, Cooper LAD, Hwang SN, Holder CA, Gao J, Aurora TD et al (2013) MR imaging predictors of molecular profile and survival: multi-institutional study of the TCGA glioblastoma data set. Radiology 267(2):560–569
Diehn M, Nardini C, Wang DS, McGovern S, Jayaraman M, Liang Y et al (2008) Identification of noninvasive imaging surrogates for brain tumor gene-expression modules. Proc Natl AcadSci U S A 105(13):5213–5218
Chaddad A, Tanougast C (2016) Extracted magnetic resonance texture features discriminate between phenotypes and are associated with overall survival in glioblastoma multiforme patients. Med BiolEngComput 54(11):1707–1718
Abrigo JM, Fountain DM, Provenzale JM, Law EK, Kwong JS, Hart MG et al (2018) Magnetic resonance perfusion for differentiating low-grade from high-grade gliomas at first presentation. Cochrane Database Syst Rev. 1:CD011551
Beig N, Patel J, Prasanna P, Hill V, Gupta A, Correa R et al (2018) Radiogenomic analysis of hypoxia pathway is predictive of overall survival in Glioblastoma. Sci Rep 8(1):7
Choi Y, Nam Y, Jang J, Shin N-Y, Lee YS, Ahn K-J, et al (2020) Radiomics may increase the prognostic value for survival in glioblastoma patients when combined with conventional clinical and genetic prognostic models. EurRadiol.
Fuster-Garcia E, LorenteEstellés D, Álvarez-Torres M, Juan-Albarracín J, Chelebian E, Rovira A et al (2021) MGMT methylation may benefit overall survival in patients with moderately vascularized glioblastomas. EurRadiol 31(3):1738–47
Hsu JB-K, Lee GA, Chang T-H, Huang S-W, Le NQK, Chen Y-C, et al (2020) Radiomic immunophenotyping of GSEA-assessed immunophenotypes of glioblastoma and its implications for prognosis: a feasibility study. Cancers (Basel);12(10).
Kickingereder P, Götz M, Muschelli J, Wick A, Neuberger U, Shinohara RT et al (2016) Large-scale radiomic profiling of recurrent glioblastoma identifies an imaging predictor for stratifying anti-angiogenic treatment response. Clin Cancer Res 22(23):5765–5771
Jain R, Poisson LM, Gutman D, Scarpace L, Hwang SN, Holder CA et al (2014) Outcome prediction in patients with glioblastoma by using imaging, clinical, and genomic biomarkers: focus on the nonenhancing component of the tumor. Radiology 272(2):484–493
Lao J, Chen Y, Li Z-C, Li Q, Zhang J, Liu J et al (2017) A deep learning-based radiomics model for prediction of survival in glioblastoma multiforme. Sci Rep 4:7
Liao X, Cai B, Tian B, Luo Y, Song W, Li Y (2019) Machine-learning based radiogenomics analysis of MRI features and metagenes in glioblastoma multiforme patients with different survival time. J Cell Mol Med 23(6):4375–4385
Molitoris JK, Rao YJ, Patel RA, Kane LT, Badiyan SN, Gittleman H et al (2017) Multi-institutional external validation of a novel glioblastoma prognostic nomogram incorporating MGMT methylation. J Neurooncol 134(2):331–338
Park JE, Kim HS, Jo Y, Yoo R-E, Choi SH, Nam SJ et al (2020) Radiomics prognostication model in glioblastoma using diffusion- and perfusion-weighted MRI. Sci Rep 10(1):4250
Sanghani P, Ang BT, King NKK, Ren H (2018) Overall survival prediction in glioblastoma multiforme patients from volumetric, shape and texture features using machine learning. SurgOncol 27(4):709–714
Tixier F, Um H, Bermudez D, Iyer A, Apte A, Graham MS et al (2019) Preoperative MRI-radiomics features improve prediction of survival in glioblastoma patients over MGMT methylation status alone. Oncotarget 10(6):660–672
Yang D, Rao G, Martinez J, Veeraraghavan A, Rao A (2015) Evaluation of tumor-derived MRI-texture features for discrimination of molecular subtypes and prediction of 12-month survival status in glioblastoma. Med Phys 42(11):6725–6735
Zhang X, Lu H, Tian Q, Feng N, Yin L, Xu X et al (2019) A radiomics nomogram based on multiparametric MRI might stratify glioblastoma patients according to survival. EurRadiol 29(10):5528–5538
Zhou M, Chaudhury B, Hall LO, Goldgof DB, Gillies RJ, Gatenby RA (2017) Identifying spatial imaging biomarkers of glioblastoma multiforme for survival group prediction. J MagnReson Imaging 46(1):115–123
Soltani M, Bonakdar A, Shakourifar N, Babaie R, Raahemifar K (2021) Efficacy of location-based features for survival prediction of patients with glioblastoma depending on resection status. Front Oncol 6(11):2509
Verma R, Correa R, Hill VB, Statsevych V, Bera K, Beig N, Mahammedi A, Madabhushi A, Ahluwalia M, Tiwari P (2020) Tumor habitat–derived radiomic features at pretreatment MRI that are prognostic for progression-free survival in glioblastoma are associated with key morphologic attributes at histopathologic examination: a feasibility study. Radiol Artificial Intelligence. 2(6):e190168
Pope WB, Lai A, Mehta R, Kim HJ, Qiao J, Young JR et al (2011) Apparent diffusion coefficient histogram analysis stratifies progression-free survival in newly diagnosed bevacizumab-treated glioblastoma. AJNR Am J Neuroradiol 32(5):882–889
Chaddad A, Daniel P, Sabri S, Desrosiers C, Abdulkarim B (2019) Integration of radiomic and multi-omic analyses predicts survival of newly diagnosed IDH1 wild-type glioblastoma. Cancers 11(8):1148
Pérez-Beteta J, Molina-García D, Ortiz-Alhambra JA, Fernández-Romero A, Luque B, Arregui E et al (2018) Tumor surface regularity at MR imaging predicts survival and response to surgery in patients with glioblastoma. Radiology 288(1):218–225
Akbari H, Macyszyn L, Da X, Bilello M, Wolf RL, Martinez-Lage M et al (2016) Imaging surrogates of infiltration obtained via multiparametric imaging pattern analysis predict subsequent location of recurrence of glioblastoma. Neurosurgery 78(4):572–580
Baine M, Burr J, Du Q, Zhang C, Liang X, Krajewski L et al (2021) The potential use of radiomics with pre-radiation therapy MR imaging in predicting risk of pseudoprogression in glioblastoma patients. J Imaging 7(2):17
Bani-Sadr A, Eker OF, Berner L-P, Ameli R, Hermier M, Barritault M, et al (2019) Conventional MRI radiomics in patients with suspected early- or pseudo-progression. Neuro-Oncol Adv;1(vdz019).
Cai J, Zheng J, Shen J, Yuan Z, Xie M, Gao M et al (2020) A Radiomics model for predicting the response to bevacizumab in brain necrosis after radiotherapy. Clin Cancer Res 26(20):5438–5447
Elshafeey N, Kotrotsou A, Hassan A, Elshafei N, Hassan I, Ahmed S et al (2019) Multicenter study demonstrates radiomic features derived from magnetic resonance perfusion images identify pseudoprogression in glioblastoma. Nat Commun 10(1):3170
Gaw N, Hawkins-Daarud A, Hu LS, Yoon H, Wang L, Xu Y et al (2019) Integration of machine learning and mechanistic models accurately predicts variation in cell density of glioblastoma using multiparametric MRI. Sci Rep 9(1):10063
Grossmann P, Narayan V, Chang K, Rahman R, Abrey L, Reardon DA et al (2017) Quantitative imaging biomarkers for risk stratification of patients with recurrent glioblastoma treated with bevacizumab. Neuro Oncol 19(12):1688–1697
Kim JY, Park JE, Jo Y, Shim WH, Nam SJ, Kim JH et al (2019) Incorporating diffusion- and perfusion-weighted MRI into a radiomics model improves diagnostic performance for pseudoprogression in glioblastoma patients. Neuro Oncol 21(3):404–414
Petrova L, Korfiatis P, Petr O, LaChance DH, Parney I, Buckner JC et al (2019) Cerebral blood volume and apparent diffusion coefficient - Valuable predictors of non-response to bevacizumab treatment in patients with recurrent glioblastoma. J Neurol Sci. 405:116433
Yan J-L, Li C, van der Hoorn A, Boonzaier NR, Matys T, Price SJ (2020) A Neural network approach to identify the peritumoral invasive areas in glioblastoma patients by using MR radiomics. Sci Rep 10(1):9748
Yoon HG, Cheon W, Jeong SW, Kim HS, Kim K, Nam H, et al (2020) Multi-Parametric Deep Learning Model for Prediction of Overall Survival after Postoperative Concurrent Chemoradiotherapy in Glioblastoma Patients. Cancers (Basel) [Internet];12(8)
Zhang Z, Yang J, Ho A, Jiang W, Logan J, Wang X et al (2018) A predictive model for distinguishing radiation necrosis from tumour progression after gamma knife radiosurgery based on radiomic features from MR images. EurRadiol 28(6):2255–2263
Patel M, Zhan J, Natarajan K, Flintham R, Davies N, Sanghera P, Grist J, Duddalwar V, Peet A, Sawlani V (2021) Machine learning-based radiomic evaluation of treatment response prediction in glioblastoma. Clin Radiol.
Rathore S, Akbari H, Doshi J, Shukla G, Rozycki M, Bilello M, Lustig RA, Davatzikos CA (2018) Radiomic signature of infiltration in peritumoral edema predicts subsequent recurrence in glioblastoma: implications for personalized radiotherapy planning. J Med Imaging. 5(2):021219
De Ruysscher D, Niedermann G, Burnet NG, Siva S, Lee AWM, Hegi-Johnson F (2019) Radiotherapy toxicity. Nat Rev Dis Primers 5(1):1–20
Lee SY (2016) Temozolomide resistance in glioblastoma multiforme. Genes Dis 3(3):198–210
Patel MD, Zhan J, Natarajan K, Flintham R, Davies N, Sanghera P, et al (2019) Radiomic evaluation of treatment response in patients with glioblastoma: a preliminary study. ECR 2019 EPOS. Eur Cong Radiol ECR; 2019
Elshafeey N, Kotrotsou A, GiniebraCamejo D, Abrol S, Hassan I, El Salek K, et al (2017) Multicenter study to demonstrate radiomic texture features derived from MR perfusion images of pseudoprogression compared to true progression in glioblastoma patients. JCO. ;35(15_suppl):2016–2016.
About the Quantitative Imaging Network (QIN) | Quantitative Imaging Network (QIN) | CIP Grant-supported Networks | Programs & Resources | Cancer Imaging Program (CIP) [Internet]. [cited 2021 Feb 20]. Available from: https://imaging.cancer.gov/programs_resources/specialized_initiatives/qin/about/teams.htm
Shukla-Dave A, Obuchowski NA, Chenevert TL, Jambawalikar S, Schwartz LH, Malyarenko D et al (2019) Quantitative imaging biomarkers alliance (QIBA) recommendations for improved precision of DWI and DCE-MRI derived biomarkers in multicenter oncology trials. J MagnReson Imaging 49(7):e101–e121
Medical Image Artificial Intelligence Cloud Platform - Huiyihuiying-Medical Image Artificial Intelligence Cloud Platform [Internet]. [cited 2021 Feb 22]. Available from: http://en.huiyihuiying.com/
Menze BH, Jakab A, Bauer S, Kalpathy-Cramer J, Farahani K, Kirby J et al (2015) The multimodal brain tumor image segmentation benchmark (BRATS). IEEE Trans Med Imaging 34(10):1993–2024
The Cancer Genome Atlas Program - National Cancer Institute [Internet]. 2018 [cited 2021 Feb 22]. Available from: https://www.cancer.gov/about-nci/organization/ccg/research/structural-genomics/tcga
Narang S, Lehrer M, Yang D, Lee J, Rao A (2016) Radiomics in glioblastoma: current status, challenges and potential opportunities. Transl Cancer Res 5(4):383–397
Avanzo M, Stancanello J, El Naqa I (2017) Beyond imaging: the promise of radiomics. Phys Med 38:122–139
Bidgood WD, Horii SC, Prior FW et al (1997) Understanding and using DICOM, the data interchange standard for biomedical imaging. J Am Med Inform Assoc 4:199–212
Hoebel KV, Patel JB, Beers AL, Chang K, Singh P, Brown JM et al (2020) Radiomics repeatability pitfalls in a scan-rescan MRI study of glioblastoma. Radiol Artificial Intelligence. 3(1):e190199
Zaidi H, El Naqa I (2010) PET-guided delineation of radiation therapy treatment volumes: a survey of image segmentation techniques. Eur J Nucl Med Mol Imaging 37:2165–2187
Mishra D, Dash R, Rath AK et al (2011) Feature selection in gene expression data using principal component analysis and rough set theory. AdvExp Med Biol 696:91–100
Kumar D, Wong A, Clausi D (2015) Lung nodule classification using deep features in CT images. Computer & Robot Vision 327:110–116
Chawla NV, Bowyer KW, Hall LO, Kegelmeyer WP (2002) SMOTE: synthetic minority over-sampling technique. J Artificial Intelligence Res 1(16):321–357
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KA—conceptualization, drafting, revising, reviewing, supervision, FBA—drafting, revising, SM—drafting, revising, FM—revising, reviewing, supervision, SAE—conceptualization, revising, reviewing, supervision, WBP—revising, reviewing, TM—revising, reviewing, JPR—revising, reviewing.
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Aftab, K., Aamir, F.B., Mallick, S. et al. Radiomics for precision medicine in glioblastoma. J Neurooncol 156, 217–231 (2022). https://doi.org/10.1007/s11060-021-03933-1
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DOI: https://doi.org/10.1007/s11060-021-03933-1