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Research ArticleAdult Brain
Open Access

Stable and Discriminatory Radiomic Features from the Tumor and Its Habitat Associated with Progression-Free Survival in Glioblastoma: A Multi-Institutional Study

R. Verma, V.B. Hill, V. Statsevych, K. Bera, R. Correa, P. Leo, M. Ahluwalia, A. Madabhushi and P. Tiwari
American Journal of Neuroradiology August 2022, 43 (8) 1115-1123; DOI: https://doi.org/10.3174/ajnr.A7591
R. Verma
aFrom the Department of Biomedical Engineering (R.V., K.B., R.C., P.L.), Case Western Reserve University, Cleveland, Ohio
dAlberta Machine Intelligence Institute (R.V.), Edmonton, Alberta
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V.B. Hill
bDepartment of Neuroradiology (V.B.H.), Feinberg School of Medicine, Northwestern University, Chicago, Illinois
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V. Statsevych
cBrain Tumor and Neuro-Oncology Center (V.S.), Cleveland Clinic, Cleveland, Ohio
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  • ORCID record for V. Statsevych
K. Bera
aFrom the Department of Biomedical Engineering (R.V., K.B., R.C., P.L.), Case Western Reserve University, Cleveland, Ohio
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R. Correa
aFrom the Department of Biomedical Engineering (R.V., K.B., R.C., P.L.), Case Western Reserve University, Cleveland, Ohio
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P. Leo
aFrom the Department of Biomedical Engineering (R.V., K.B., R.C., P.L.), Case Western Reserve University, Cleveland, Ohio
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M. Ahluwalia
eMiami Cancer Institute (M.A.), Miami, FL and Herbert Wertheim College of Medicine, Florida International University, Florida
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A. Madabhushi
fDepartment of Biomedical Engineering (A.M.), Emory University, Atlanta Veterans Administration Medical Center
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P. Tiwari
gDepartments of Radiology and Biomedical Engineering (P.T.), University of Wisconsin Madison, Wisconsin
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  • FIG 1.
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    FIG 1.

    Overview of the methodology and overall workflow. MR imaging scans (Gd-T1w, T2w, and FLAIR) were preprocessed and segmented into 3 tumor subcompartments (necrosis, enhancing tumor, and peritumoral edema). Next, a set of radiomic features was obtained for each of the MR imaging scans across the 3 tumor subcompartments. The most stable and discriminatory features were identified using the PI score and AUC measures across every subcompartment and every MR imaging protocol. The identified stable and discriminatory features were used for stability assessment across tumor subcompartments (with the associated habitat), individual imaging protocols (Gd-T1w, T2w, FLAIR), and MR imaging acquisition parameters (magnetic field strength, pixel resolution, and slice spacing).

  • FIG 2.
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    FIG 2.

    The strategy used for segregating our cohort into training (T̂ 1 –T̂ 4), validation (VS1–VS4), and TSs. The training and the validation sets were created using the LOSO scheme.

  • FIG 3.
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    FIG 3.

    2D plots of discriminability (average AUC, y-axis) versus instability (PI score, x-axis) for each tumor subcompartment (A, Necrosis. B, Enhancing tumor. C, T2/FLAIR hyperintensity). Each radiomic feature is shown as a bubble where its size represents the SD between the AUC values across different LOSO runs. D, The stacked barplot of the total number of extracted features, the features that were identified as stable (PI = 0) from across different feature families per MR imaging sequence (Gd-T1w, T2w, and FLAIR), and the overlapping stable features across multiparametric MR imaging sequences. Different colors represent different feature families.

  • FIG 4.
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    FIG 4.

    Barplots showing training and validation AUCs to distinguish patients with improved and poor outcomes using the top 5 stable and discriminatory radiomic versus discriminatory-only features. Blue barplots depict the AUC values using discriminatory features, while orange bars represent AUC values using stable and discriminatory radiomic features from the respective training and validation cohorts.

Tables

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    Table 1:

    Summary of patient demographics and the most commonly varying MR parameters across our cohort curated from 5 different sites (S1–S5)

    Imaging Source SiteS1, MD Anderson Cancer Center, Houston, TexasS2, Ivy Glioblastoma Atlas ProjectS3, Henry Ford Hospital, Detroit, MichiganS4, University of California, San Francisco, CaliforniaS5, Cleveland Clinic, Ohio
    No. of cases1733281557
    Magnetic field strength
     1.5T119161448
     3T6241219
    Sex
     Female7175623
     Male101623934
    Scanner
     GE Healthcare1730281557
     Siemens03000
    Slice thickness (range) (mm)6.50.9–6.51–61.5–60.9–7.5
    Pixel spacing (range) (mm)0.47–0.860.43–1.050.43–0.940.45–1.020.23–1
    • View popup
    Table 2:

    A list of the top 5 features identified to reliably differentiate poor from improved survival in patients with GBM from the training set for every tumor subcompartment (necrosis, enhancing tumor, peritumoral T2/FLAIR hyperintensity, and nonenhancing tumor)

    No.Feature FamilyDescriptorWindow SizeMRI SequenceStatistic
    Top 5 features selected from necrosis
     1LawsEdge-edge-level5T1Skewness
     2LawsLevel-level-level3T1Skewness
     3LawsWave-wave-level5FLAIRMedian
     4CoLIAGeSum variance3FLAIRSkewness
     5CoLIAGeSum variance3FLAIRKurtosis
    Top 5 features selected from enhancing tumor
     1CoLIAGeSum average3T2Median
     2CoLIAGeSum average5T2Median
     3CoLIAGeEnergy3FLAIRMedian
     4CoLIAGeSum average3FLAIRMedian
     5LawsSpot-level-ripple5T1Skewness
    Top 5 features selected from edema and nonenhancing tumor
     1LawsLevel-edge-level5T1Median
     2CoLIAGeSum variance5T2Variance
     3CoLIAGeSum variance5T2Skewness
     4HaralickSum entropy5FLAIRSkewness
     5Gabor–θ = 1.178, XZ –θ = 0, λ = 1.482, BW = 15T2Kurtosis
    • Note:—BW indicates bandwidth.

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American Journal of Neuroradiology: 43 (8)
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R. Verma, V.B. Hill, V. Statsevych, K. Bera, R. Correa, P. Leo, M. Ahluwalia, A. Madabhushi, P. Tiwari
Stable and Discriminatory Radiomic Features from the Tumor and Its Habitat Associated with Progression-Free Survival in Glioblastoma: A Multi-Institutional Study
American Journal of Neuroradiology Aug 2022, 43 (8) 1115-1123; DOI: 10.3174/ajnr.A7591

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Radiomic Features and Glioblastoma Survival
R. Verma, V.B. Hill, V. Statsevych, K. Bera, R. Correa, P. Leo, M. Ahluwalia, A. Madabhushi, P. Tiwari
American Journal of Neuroradiology Aug 2022, 43 (8) 1115-1123; DOI: 10.3174/ajnr.A7591
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