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Research ArticleAdult Brain

Diagnostic Accuracy of Arterial Spin-Labeling, Dynamic Contrast-Enhanced, and DSC Perfusion Imaging in the Diagnosis of Recurrent High-Grade Gliomas: A Prospective Study

T.B. Nguyen, N. Zakhari, S. Velasco Sandoval, A. Guarnizo-Capera, M. Alexios Gulak, J. Woulfe, G. Jansen, R. Thornhill, N. Majtenyi and G.O. Cron
American Journal of Neuroradiology February 2023, 44 (2) 134-142; DOI: https://doi.org/10.3174/ajnr.A7771
T.B. Nguyen
aFrom the Department of Radiology (T.B.N., N.Z., R.T.), Radiation Oncology and Medical Physics
cUniversity of Ottawa (T.B.N., N.Z., J.W., G.J., R.T.), Ottawa, Ontario, Canada
dThe Ottawa Hospital Research Institute (T.B.N., J.W., G.J., R.T.), Ottawa, Ontario, Canada
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N. Zakhari
aFrom the Department of Radiology (T.B.N., N.Z., R.T.), Radiation Oncology and Medical Physics
cUniversity of Ottawa (T.B.N., N.Z., J.W., G.J., R.T.), Ottawa, Ontario, Canada
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S. Velasco Sandoval
eDivision of Neuroradiology (S.V.S., A.G.-C.), Department of Radiology, Hospital Universitario Fundación Santa Fe de Bogotá, Bogotá, D.C., Colombia
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A. Guarnizo-Capera
eDivision of Neuroradiology (S.V.S., A.G.-C.), Department of Radiology, Hospital Universitario Fundación Santa Fe de Bogotá, Bogotá, D.C., Colombia
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M. Alexios Gulak
fDepartment of Anesthesiology and Pain Medicine (M.A.G.), University of Toronto, Toronto, Ontario, Canada
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J. Woulfe
bDepartment of Pathology and Laboratory Medicine (J.W., G.J.), The Ottawa Hospital, Ottawa, Ontario, Canada
cUniversity of Ottawa (T.B.N., N.Z., J.W., G.J., R.T.), Ottawa, Ontario, Canada
dThe Ottawa Hospital Research Institute (T.B.N., J.W., G.J., R.T.), Ottawa, Ontario, Canada
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G. Jansen
bDepartment of Pathology and Laboratory Medicine (J.W., G.J.), The Ottawa Hospital, Ottawa, Ontario, Canada
cUniversity of Ottawa (T.B.N., N.Z., J.W., G.J., R.T.), Ottawa, Ontario, Canada
dThe Ottawa Hospital Research Institute (T.B.N., J.W., G.J., R.T.), Ottawa, Ontario, Canada
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R. Thornhill
aFrom the Department of Radiology (T.B.N., N.Z., R.T.), Radiation Oncology and Medical Physics
cUniversity of Ottawa (T.B.N., N.Z., J.W., G.J., R.T.), Ottawa, Ontario, Canada
dThe Ottawa Hospital Research Institute (T.B.N., J.W., G.J., R.T.), Ottawa, Ontario, Canada
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N. Majtenyi
gDepartment of Medical Physics (N.M.), Grand River Regional Cancer Centre, Kitchener, Ontario, Canada
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G.O. Cron
hStanford University (G.O.C.), Stanford, California
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    FIG 1.

    Flow chart of patients included and excluded in the study. Among the 26 patients included in the study, 6 patients had 2 lesions, 2 patients had 1 lesion with tumor recurrence (TR) and 1 lesion with radiation necrosis (RN), both confirmed with clinical/radiologic follow-up; 1 patient with 2 lesions with RN confirmed with surgery; 1 patient had 1 lesion with TR and 1 lesion with RN confirmed with surgery; 1 patient with 1 lesion with TR confirmed by surgery and 1 lesion with RN confirmed with clinical/radiology follow-up; 1 patient had 1 lesion with TR confirmed with surgery and 1 lesion with TR confirmed with clinical/radiologic follow-up.

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    FIG 2.

    Sample of a case of recurrent glioblastoma multiforme with a false-negative ASL study due to probable ineffective labeling. Patient had a history of a right frontal grade IV glioma and had undergone resection and chemoradiation 3 years earlier. A, Axial T1-weighted image shows a newly enhancing lesion in the right anterior thalamus. B, ASL-derived CBF reveals a low CBF value in the enhancing lesion (arrow). The CBF in the right hemispheric cortex is lower than on the left side, presumably due to ineffective labeling from dental hardware. DSC MR imaging demonstrates a high, uncorrected rCBV value (C) and leakage-corrected rCBV value (D) at the rim of the enhancing lesion (arrow). DCE MR imaging using MOLLI T1 mapping shows high Vp (E) and Ktrans (F) values in the lesion (arrows). Pathology confirmed glioblastoma recurrence.

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    FIG 3.

    Example of a case of recurrent glioblastoma multiforme with a false-negative DSC study due to susceptibility artifacts. A, Axial T1-weighted image shows a newly enhancing lesion in the right mesial temporal lobe. B, ASL-derived CBF map demonstrates a marked increase in CBF in the lesion (arrow). C, Corrected CBV map is unreliable in the tumoral region due to susceptibility artifacts (arrow). DCE MR imaging performed without T1 mapping reveals high Vp (D) and Ktrans (E) values in the lesion (arrow), which correlate with the high CBF value.

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    Table 1:

    Clinical and characteristics of patient populationa

    Radiation NecrosisTumor RecurrenceP Value
    Median age (yr) (95% CI)54 (44–63.2)59 (50.9–65.3).34
    Female/male13% (1/12)21% (4/15).35
    Initial tumor grade: grade 3, grade 40, 134, 15.098
    Median duration from radiation treatment to study MR imaging (days), (95% CI)179 (142–462)275 (191–915).066
    % Lesions with reresection30% (5/13)68% (13/19).27
    Median duration from imaging to reresection (days) (95% CI)2015 (13.5–26).96
    Median Karfnosky score (range)80 (75.3–90)80 (70–90).43
    • ↵a Patients with 2 lesions are entered as 2 separate entries for the purpose of this table.

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    Table 2:

    Comparison of perfusion parameters for lesions diagnosed as tumor recurrence versus radiation necrosis

     Radiation NecrosisTumor Recurrence
     No.Median95% CINo.Median95% CIP Value
    CBF_ASL (mL/100 g/min)1324.117.8–38.31936.033.9–62.2.003a
    rCBV131.811.55–3.18193.692.02–5.03.058
    Corrected rCBV131.240.83–2.89192.501.60–3.15.048
    Ktrans_SI (min−1)130.0130.0062–0.039190.0190.011–0.048.28
    Vp_SI130.160.12–0.29190.270.21–0.39.063
    Ktrans_MOLLI (min−1)110.0520.024–0.094140.0550.047–0.11.44
    Vp_MOLLI110.170.13–0.28140.280.20–0.41.012
    Ktrans_SMART (min−1)110.0420.020–0.075140.0460.037–0.071.48
    Vp_SMART110.120.082–0.23140.210.15–0.33.080
    • ↵a Significance following Holm Bonferroni correction.

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    Table 3:

    Correlogram between different perfusion parameters using the Spearman rank correlation coefficienta

    • ↵a Color coding is red for a very strong correlation (rs >0.8); orange for a strong correlation (0.6 ≤ rs ≤ 0.79), yellow for a moderate correlation (0.4 ≤ rs ≤ 0.59), and green for a weak correlation (rs <0.4).

    • View popup
    Table 4:

    Diagnostic accuracy of various parameters in the differentiation between tumor recurrence and radiation necrosis for all lesions (n = 32 lesions) and for subgroup analysis of patients with DCE T1 mapping (n = 25 lesions)a

    ParametersNo.AUC (95% CI)P ValueOptimal ThresholdSensitivity (%)Specificity (%)
    ASL_CBF320.81 (0.63–0.93)<.001>30 mL/100 g/min84 (60–97)77 (46–95)
    rCBV320.70 (0.52–0.89).033>2.4369 (43–87)77 (46–95)
    Corrected rCBV320.71 (0.51–0.90).037>1.5479 (54–94)69 (39–91)
    Ktrans_SI320.61 (0.41–0.82).27>0.0093 (min-1)84 (60–97)46 (19–75)
    Vp_SI320.69 (0.51–0.88).038>0.1879 (54–94)62 (32–86)
    Ktrans_SI250.66 (0.43–0.88).17>0.0092 (min-1)86 (57–98)55 (23–83)
    Vp_SI250.68 (0.46–0.90).10>0.1879 (49–95)64 (31–89)
    Ktrans_MOLLI250.59 (0.36-0.82).44>0.045 (min-1)78 (49–95)45 (17–77)
    Vp_MOLLI250.80 (0.62–0.98)<.001>0.1986 (57–98)63 (31–89)
    Ktrans_SMART250.58 (0.34–0.83).49>0.024 (min-1)92 (66–1)27 (6–61)
    Vp_SMART250.71 (0.49–0.88).057>0.1293 (66-1)54 (23–83)
    • ↵a Statistics are listed with their 95% CI.

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American Journal of Neuroradiology: 44 (2)
American Journal of Neuroradiology
Vol. 44, Issue 2
1 Feb 2023
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T.B. Nguyen, N. Zakhari, S. Velasco Sandoval, A. Guarnizo-Capera, M. Alexios Gulak, J. Woulfe, G. Jansen, R. Thornhill, N. Majtenyi, G.O. Cron
Diagnostic Accuracy of Arterial Spin-Labeling, Dynamic Contrast-Enhanced, and DSC Perfusion Imaging in the Diagnosis of Recurrent High-Grade Gliomas: A Prospective Study
American Journal of Neuroradiology Feb 2023, 44 (2) 134-142; DOI: 10.3174/ajnr.A7771

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MRI for Recurrent High-Grade Gliomas Diagnosis
T.B. Nguyen, N. Zakhari, S. Velasco Sandoval, A. Guarnizo-Capera, M. Alexios Gulak, J. Woulfe, G. Jansen, R. Thornhill, N. Majtenyi, G.O. Cron
American Journal of Neuroradiology Feb 2023, 44 (2) 134-142; DOI: 10.3174/ajnr.A7771
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