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Research ArticleAdult Brain

Prognostic Value of Preoperative MRI Metrics for Diffuse Lower-Grade Glioma Molecular Subtypes

P. Darvishi, P.P. Batchala, J.T. Patrie, L.M. Poisson, M.-B. Lopes, R. Jain, C.E. Fadul, D. Schiff and S.H. Patel
American Journal of Neuroradiology May 2020, 41 (5) 815-821; DOI: https://doi.org/10.3174/ajnr.A6511
P. Darvishi
aFrom the Departments of Radiology and Medical Imaging (P.D., P.P.B., S.H.P.)
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P.P. Batchala
aFrom the Departments of Radiology and Medical Imaging (P.D., P.P.B., S.H.P.)
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J.T. Patrie
bPublic Health Sciences (J.T.P.)
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L.M. Poisson
eDepartment of Public Health (L.M.P.), Henry Ford Health System, Detroit, Michigan
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M.-B. Lopes
cPathology, Divisions of Neuropathology and Molecular Diagnostics (M.-B.L.)
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R. Jain
fDepartments of Radiology (R.J.) and Neurosurgery (R.J.), New York University School of Medicine, New York, New York.
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C.E. Fadul
dDivision of Neuro-Oncology (C.E.F., D.S.), University of Virginia Health System, Charlottesville, Virginia
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D. Schiff
dDivision of Neuro-Oncology (C.E.F., D.S.), University of Virginia Health System, Charlottesville, Virginia
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S.H. Patel
aFrom the Departments of Radiology and Medical Imaging (P.D., P.P.B., S.H.P.)
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  • Fig 1.
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    Fig 1.

    Kaplan-Meier survival curves based on the LGG molecular subtype. Vertical tick marks identify right-censored survival times. The survival curves differed among all 3 LGG molecular subtypes (IDH-mutant 1p/19q-codeleted molecular subtype versus IDH-mutant 1p/19q-noncodeleted molecular subtype: P = .021; IDH-mutant 1p/19q-codeleted molecular subtype versus IDH wild-type molecular subtype: P < .001; and IDH-mutant 1p/19q-noncodeleted molecular subtype versus IDH-wild type molecular subtype: P < .001). Survival curves for patients who composed a subset of the current patient cohort are shown in Patel et al,46 in 2019.

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    Fig 2.

    Representative cases of IDHwt LGGs. A 51-year-old man with an IDH wild-type diffuse astrocytoma. FLAIR (A) shows a 6-cm mass in the right temporal lobe with ill-defined margins. Contrast-enhanced T1WI (B) shows no contrast enhancement of the mass. This patient is deceased, with a survival time of 262 days. Further molecular testing in this case was positive for TERT promoter (−124 C > T) mutation. A 26-year-old woman with an IDH wild-type diffuse astrocytoma. FLAIR (C) and contrast-enhanced T1WI (D) show a 1.6-cm left frontal lobe mass with fairly well-circumscribed margins and contrast enhancement. This patient was alive at last follow-up, with a survival time of 2757 days. Further molecular testing in this case was positive for the BRAF V600E mutation.

Tables

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    Table 1:

    Patient characteristics for each molecular subtype

    IDHmut-CodelIDHmut-NoncodelIDHwt
    Total patientsa104 (34.0%)129 (42.2%)73 (23.9%)
    Female sex58 (55.8%)61 (47.3%)35 (47.9%)
    Ageb48 (17–74)35 (17–70)57 (19–76)
    WHO grade
     II72 (69.2%)83 (64.3%)34 (46.6%)
     III32 (30.8%)46 (35.7%)39 (53.3%)
    • ↵a Data are listed as count (percentage of total cohort).

    • ↵b Data are listed as median (range). Other data are listed as count (percentage of cases within given molecular subtype).

    • View popup
    Table 2:

    Empiric distribution summaries for the preoperative MR imaging metrics according to LGG molecular subtype

    MR Imaging MetricIDHmut-CodelIDHmut-NoncodelIDHwt
    Tumor size (cm)
     Median6.66.96.2
     IQR (1st to 3rd quartile)(5.2–8.6)(5.3–9.3)(4.6–8.4)
     Range (minimum–maximum)(1.9–14.2)(1.7–15.3)(1.1–15.0)
    Location
     Central26 (25.0%)43 (33.3%)29 (39.7%)
     Peripheral78 (75.0%)86 (66.7%)44 (60.3%)
    No. of involved lobes
     Median2.02.02.0
     IQR (1st to 3rd quartile)(1.0–3.0)(1.0–3.0)(1.0–3.0)
     Range (minimum–maximum)(1.0–6.0)(1.0–9.0)(1.0–8.0)
    Corpus callosum extension44 (42.3%)46 (35.7%)18 (24.2%)
    Hydrocephalus12 (11.5%)27 (20.9%)7 (9.6%)
    Midline shift (cm)
     Median0.000.300.00
     IQR (1st to 3rd quartile)(0.00–0.43)(0.00–0.80)(0.00–0.10)
     Range (minimum–maximum)(0.00–2.70)(0.00–1.90)(0.00–1.40)
    Eloquent cortex33 (31.7%)45 (34.9%)24 (32.9%)
    Ependymal extension65 (62.5%)80 (62.0%)58 (79.5%)
    Margin
     <33% sharp/circumscribed32 (30.8%)31 (24.0%)28 (38.4%)
     33%–66% sharp/circumscribed55 (52.9%)38 (29.5%)31 (42.5%)
     >66% sharp/circumscribed17 (16.3%)60 (46.5%)14 (19.2%)
    Contrast enhancement21 (31.8%)51 (39.5%)30 (41.1%)
    Necrosis17 (16.3%)14 (10.9%)18 (24.7%)
    • View popup
    Table 3:

    Associations between preoperative MR imaging metrics and overall survival per LGG molecular subtype, after adjustment for patient age, sex, tumor grade, and surgical resection statusa

    Relative Comparison (Non-Reference:Reference)bIDHmut-CodelIDHmut-NoncodelIDHwt
    Tumor size (3rd to 1st quartile)2.85 (1.06–7.70) (P = .039)2.90 (1.54–5.48) (P < .001)3.82 (1.94–7.75) (P < .001)
    Location (central:peripheral)0.59 (0.16–2.18) (P = .430)0.50 (0.22–1.17) (P = .101)0.78 (0.36–1.70) (P = .534)
    No. of involved lobes (X + 1:X)1.37 (0.84–2.23) (P = .211)1.25 (0.99–1.58) (P = .065)1.70 (1.28–2.27) (P = .001)
    Corpus callosum extension (yes:no)2.60 (0.69–9.84) (P = .160)1.42 (0.59–3.41) (P = .433)1.89 (0.78–4.58) (P = .160)
    Hydrocephalus (yes:no)2.57 (0.42–15.81) (P = .308)0.63 (0.19–2.11) (P = .457)4.43 (1.12–17.54) (P = .034)
    Midline shift (3rd to 1st quartile)1.32 (0.77–2.26) (P = .320)1.14 (0.54–2.41) (P = .730)1.16 (1.03–1.30) (P = .013)
    Eloquent cortex (yes:no)1.00 (0.29–3.43) (P = .740)1.91 (0.77–4.78) (P = .165)2.01 (0.90–4.49) (P = .087)
    Ependymal extension (yes:no)6.34 (1.07–37.59) (P = .042)1.72 (0.64–4.64) (P = .289)1.51 (0.52–4.35) (P = .447)
    Margins (global test P value)c(P = .775)(P = .190)(P = .031)
     33%–66%:<33%d1.57 (0.42–5.97) (P = .505)0.51 (0.19–1.33) (P = .166)0.39 (0.17–0.90) (P = .027)
     >66%:<33%d0.98 (0.09–10.85) (P = .985)0.39 (0.13–1.19) (P = .098)0.24 (0.06–1.05) (P = .057)
     >66%:33%–66%d0.62 (0.06–6.40) (P = .688)0.77 (0.24–2.38) (P = .646)0.63 (0.14–2.87) (P = .554)
    Contrast enhancement (yes:no)3.11 (0.71–13.68) (P = .132)1.67 (0.62–4.51) (P = .313)0.34 (0.13–0.90) (P = .030)
    Necrosis (yes:no)1.84 (0.32–10.78) (P = .498)0.28 (0.03–2.42) (P = .247)1.93 (0.82–4.58) (P = .134)
    • ↵a Data are listed as adjusted hazard ratios (95% confidence interval) and corresponding P values.

    • ↵b Relative comparison (nonreference:reference) identifies the nonreference predictor variable value/level and the reference predictor variable value/level at which the adjusted instantaneous risk of death ratio (ie, hazard ratio) was evaluated. For example (3rd:1st quartile) represents a comparison of the adjusted instantaneous risk of death (ie, hazard) between 2 patients, 1 patient whose predictor variable value is at the 3rd quartile of the predictor variable empiric distribution (nonreference) and 1 patient whose predictor variable value is at the 1st quartile of the predictor variable empiric distribution (reference). A relative comparison denoted as (X + 1:1) represents a comparison of the adjusted instantaneous risk of death (ie, hazard) between 2 patients, 1 patient whose predictor variable value is X + 1 units (nonreference) and 1 patient whose predictor variable value is X units (reference). A relative comparison, denoted as (yes:no), represents a comparison of the adjusted instantaneous risk of death (ie, hazard) between 2 patients, 1 patient who has the factor of interest (nonreference = yes) and 1 patient who does not have the factor of interest (reference = no). Note, if the adjusted hazard ratio is >1 (<1), it indicates that the estimate for the instantaneous risk of death is greater (less) for the patient who has the nonreference predictor value/level.

    • ↵c Global test P value is the P value for testing the null hypothesis that the instantaneous risk of death is same for all “margin” categories.

    • ↵d Percentage of LGGs displaying sharp/circumscribed margin.

    • View popup
    Table 4:

    Associations between preoperative MR imaging metrics and WHO grade III per molecular subtypea

    Relative Comparison (Non-Reference:Reference)bIDHmut-CodelIDHmut-NoncodelIDHwt
    Tumor size (3rd to 1st quartile)0.97 (0.18–5.26) (P = .975)1.24 (0.34–4.57) (P = .742)1.60 (0.31–8.17) (P = .573)
    Location (central:peripheral)1.55 (0.22–10.49) (P = .654)0.21 (0.05–0.80) (P = .035)0.42 (0.10–1.84) (P = .252)
    No. of involved lobes (X + 1:X)1.45 (0.64–3.30) (P = .370)1.12 (0.65–1.94) (P = .673)0.96 (0.48–1.92) (P = .906)
    Corpus callosum extension (yes:no)1.88 (0.39–9.05) (P = .430)2.51 (0.72–8.76) (P = .149)1.46 (0.25–8.35) (P = .672)
    Hydrocephalus (yes:no)8.55 (0.33–223.32) (P = .197)2.07 (0.50–8.54) (P = .313)0.26 (0.01–5. 09) (P = .372)
    Midline shift (3rd to 1st quartile)0.88 (0.37–2.10) (P = .774)0.55 (0.16–1.85) (P = .331)1.31 (0.91–1.89) (P = .148)
    Eloquent cortex (yes:no)1.71 (0.49–5.99) (P = .402)1.87 (0.69–5.09) (P = .220)0.35 (0.08–1.54) (P = .165)
    Ependymal extension (yes:no)1.68 (0.28–10.07) (P = .570)0.65 (0.15–2.86) (P = .571)0.09 (0.01–0.59) (P = .012)
    Margins (global test)cP = .970P = .360P = .221
     33%–66%:<33%d1.20 (0.28–5.23) (P = .804)1.47 (0.37–5.79) (P = .583)1.62 (0.24–10.84) (P = .619)
     >66%:<33%d1.16 (0.15–9.17) (P = .888)0.64 (0.12–3.56) (P = .614)0.27 (0.02–3.35) (P = .305)
     >66%:33%–66%d0.96 (0.17–5.56) (P = .967)0.44 (0.13–1.42) (P = .170)0.16 (0.02–1.28) (P = .084)
    Contrast enhancement (yes:no)1.73 (0.47–6.43) (P = .411)6.08 (2.12–17.41) (P = .001)16.75 (3.47–80.86) (P < .001)
    Necrosis (yes:no)9.68 (0.83–112.49) (P = .070)0.61 (0.08–4.67) (P = .632)0.67 (0.13–3.36) (P = .630)
    • ↵a Note that for the multivariate logistic regression analysis, WHO grade III tumors were assigned the value 1 and WHO grade II tumors were assigned the value 0. Data are listed as adjusted odds ratios, (95% confidence interval) and corresponding P value determined by a Wald type III χ2 test.

    • ↵b Relative comparison (nonreference:reference) identifies the nonreference predictor variable value/level and the reference predictor variable value/level at which the adjusted odds ratio was evaluated. For example (3rd:1st Quartile) represents a comparison of the adjusted odds for tumor grade III between 2 patients, 1 patient whose predictor variable value is at the 3rd quartile of the predictor variable empiric distribution (nonreference) and 1 patient whose predictor variable value is at the 1st quartile of the predictor variable empiric distribution (reference). A relative comparison denoted as (X + 1:1) represents a comparison of the adjusted odds for tumor grade III between 2 patients, 1 patient whose predictor variable value equals X + 1 (nonreference) and 1 patient whose predictor variable value equals X (reference). A relative comparison denoted as (yes:no) represents a comparison of the adjusted odds for a tumor grade III between 2 patients, 1 patient who has the factor of interest (nonreference = yes) and 1 patient who does not have the factor of interest (reference = no). Note, if the adjusted odds ratio is >1 (<1), it indicates that the estimate for the adjusted odds for a tumor grade III is greater (less) for the patient who has the nonreference predictor value/level.

    • ↵c Global test P value is the P value for testing the null hypothesis that the adjusted odds ratio is same for all “margin” categories.

    • ↵d Percentage of LGG displaying sharp/circumscribed margin.

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American Journal of Neuroradiology: 41 (5)
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P. Darvishi, P.P. Batchala, J.T. Patrie, L.M. Poisson, M.-B. Lopes, R. Jain, C.E. Fadul, D. Schiff, S.H. Patel
Prognostic Value of Preoperative MRI Metrics for Diffuse Lower-Grade Glioma Molecular Subtypes
American Journal of Neuroradiology May 2020, 41 (5) 815-821; DOI: 10.3174/ajnr.A6511

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Prognostic Value of Preoperative MRI Metrics for Diffuse Lower-Grade Glioma Molecular Subtypes
P. Darvishi, P.P. Batchala, J.T. Patrie, L.M. Poisson, M.-B. Lopes, R. Jain, C.E. Fadul, D. Schiff, S.H. Patel
American Journal of Neuroradiology May 2020, 41 (5) 815-821; DOI: 10.3174/ajnr.A6511
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