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Research ArticleADULT BRAIN
Open Access

Antiangiogenic Effect of Bevacizumab: Application of Arterial Spin-Labeling Perfusion MR Imaging in a Rat Glioblastoma Model

T.J. Yun, H.R. Cho, S.H. Choi, H. Kim, J.-K. Won, S.-W. Park, J.-h. Kim, C.-H. Sohn and M.H. Han
American Journal of Neuroradiology September 2016, 37 (9) 1650-1656; DOI: https://doi.org/10.3174/ajnr.A4800
T.J. Yun
aFrom the Department of Radiology (T.J.Y., H.R.C., S.H.C., H.K., S.-W.P., J.-h.K., C.-H.S., M.H.H.), Seoul National University College of Medicine, Republic of Korea
bDepartments of Radiology (T.J.Y., H.R.C., S.H.C., H.K., J.-h.K., C.-H.S., M.H.H.)
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H.R. Cho
aFrom the Department of Radiology (T.J.Y., H.R.C., S.H.C., H.K., S.-W.P., J.-h.K., C.-H.S., M.H.H.), Seoul National University College of Medicine, Republic of Korea
bDepartments of Radiology (T.J.Y., H.R.C., S.H.C., H.K., J.-h.K., C.-H.S., M.H.H.)
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S.H. Choi
aFrom the Department of Radiology (T.J.Y., H.R.C., S.H.C., H.K., S.-W.P., J.-h.K., C.-H.S., M.H.H.), Seoul National University College of Medicine, Republic of Korea
bDepartments of Radiology (T.J.Y., H.R.C., S.H.C., H.K., J.-h.K., C.-H.S., M.H.H.)
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H. Kim
aFrom the Department of Radiology (T.J.Y., H.R.C., S.H.C., H.K., S.-W.P., J.-h.K., C.-H.S., M.H.H.), Seoul National University College of Medicine, Republic of Korea
bDepartments of Radiology (T.J.Y., H.R.C., S.H.C., H.K., J.-h.K., C.-H.S., M.H.H.)
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J.-K. Won
cPathology (J.-K.W.)
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S.-W. Park
aFrom the Department of Radiology (T.J.Y., H.R.C., S.H.C., H.K., S.-W.P., J.-h.K., C.-H.S., M.H.H.), Seoul National University College of Medicine, Republic of Korea
eDepartment of Radiology (S.-W.P.), Seoul National University Boramae Medical Center, Seoul, Republic of Korea.
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J.-h. Kim
aFrom the Department of Radiology (T.J.Y., H.R.C., S.H.C., H.K., S.-W.P., J.-h.K., C.-H.S., M.H.H.), Seoul National University College of Medicine, Republic of Korea
bDepartments of Radiology (T.J.Y., H.R.C., S.H.C., H.K., J.-h.K., C.-H.S., M.H.H.)
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C.-H. Sohn
aFrom the Department of Radiology (T.J.Y., H.R.C., S.H.C., H.K., S.-W.P., J.-h.K., C.-H.S., M.H.H.), Seoul National University College of Medicine, Republic of Korea
bDepartments of Radiology (T.J.Y., H.R.C., S.H.C., H.K., J.-h.K., C.-H.S., M.H.H.)
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M.H. Han
aFrom the Department of Radiology (T.J.Y., H.R.C., S.H.C., H.K., S.-W.P., J.-h.K., C.-H.S., M.H.H.), Seoul National University College of Medicine, Republic of Korea
bDepartments of Radiology (T.J.Y., H.R.C., S.H.C., H.K., J.-h.K., C.-H.S., M.H.H.)
dNeurosurgery (M.H.H.), Seoul National University Hospital, Seoul, Republic of Korea
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    Fig 1.

    Experimental design showing the timeline of each group for U87 glioma cell inoculation, bevacizumab therapy, MR imaging, and sacrifice for brain harvest.

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    Fig 2.

    Quantification of tumor volume and perfusion parameters in all tumors. T2WI and perfusion maps were acquired from a rat belonging to the 10-day treatment group. Serial reductions in rCBV and rCBF based on DSC and CBF based on ASL are shown. Graphs in the right column show serial changes of tumor volume and perfusion parameters in all tumors. Scale units of rCBVDSC, rCBFDSC, and CBFASL are milliliters × 100 g−1, milliliters × 100 g−1 × min−1, and milliliters × 100 g−1 × min−1, respectively. Data are mean results from paired t tests (unpaired t tests). One asterisk indicates P < .05; 2 asterisks, P < .001; NS, not significant; nCBVDSC, nCBV based on DSC; nCBFDSC, nCBF based on DSC; nCBFASL, nCBF based on ASL.

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    Fig 3.

    Quantification of tumor volume, perfusion parameters, and MVA in tumors with available histology. T2WI and perfusion maps were acquired from rats in the control group, 3-day treatment group, or 10-day treatment group. Differences in rCBV and rCBF based on DSC, CBF based on ASL, and MVA are shown. Graphs in the right column show differences in the tumor volume and hemodynamic parameters and MVA. In the lower images, the tumors stained immunohistochemically with anti-CD34 show positive brown cytoplasmic staining of the endothelial area and vessel lumen. Scale units of rCBVDSC, rCBFDSC, and CBFASL are milliliters × 100 g−1, milliliters × 100 g−1 × min−1, and milliliters × 100 g−1 × min−1, respectively. P values were based on 1-way analyses of variances. One asterisk indicates a significant (P < .05) difference from the Scheffe post hoc multiple comparisons.

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    Table 1:

    Comparison of volume and perfusion parameters based on DSC and ASL MR imaging in all tumorsa

    Variables0 Days (n = 14)3 Days (n = 10)10 Days (n = 4)Paired t TestUnpaired t Test
    P ValuebP ValuecP ValuedP ValuebP ValuecP Valued
    Volume (mm3)40.0 (32.3–61.8)91.9 (53.9–124.1)203.7 (103.0–301.3).015.200.117.002.090.086
    nCBVDSC5.9 (5.7–6.3)2.7 (2.4–2.9)0.8 (0.6–1.4)<.001.004<.001<.001.002.005
    nCBFDSC3.7 (3.2–4.0)1.8 (1.4–2.2)0.7 (0.6–1.0)<.001.020<.001<.001.075.004
    nCBFASL1.7 (1.2–2.0)0.3 (0.2–0.5)0.1 (0.1–0.1)<.001.041<.001.004.029.050
    • Note:—nCBVDSC indicates nCBV based on DSC; nCBFDSC, nCBF based on DSC; nCBFASL, nCBF based on ASL.

    • ↵a Values are presented as medians (interquartile range, range from the 25th to the 75th percentile).

    • ↵b Results between 0 and 3 days.

    • ↵c Results between 3 and 10 days.

    • ↵d Results between 0 and 10 days.

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    Table 2:

    Comparison and correlation of perfusion parameters based on DSC and ASL MR imaging with MVA in tumors with available histologya

    VariablesControl (n = 4)3-Day Treatment (n = 6)10-Day Treatment (n = 4)P ValuebDifferent Groupsc
    Volume (mm3)51.9 (40.8–72.1)99.7 (91.8–124.1)203.7 (103.0–301.3)0.066
    nCBVDSC6.0 (5.7–6.3)2.4 (2.2–2.7)0.8 (0.6–1.4)<.001(Control) (3 days) (3 days) (10 days) (Control) (10 days)
    nCBFDSC3.5 (3.3–3.7)1.8 (1.5–1.9)0.7 (0.6–1.0)<.001(Control) (3 days) (Control) (10 days)
    nCBFASL1.4 (1.0–1.7)0.3 (0.2–0.5)0.1 (0.1–0.1)0.005(Control) (3 days) (Control) (10 days)
    MVA (×10−2)7.5 (6.9–7.9)2.8 (2.3–3.3)2.4 (1.9–2.9)<.001(Control) (3 days) (Control) (10 days)
    • ↵a Values are presented as medians (interquartile range, range from the 25th to the 75th percentile).

    • ↵b Results from 1-way analyses of variances.

    • ↵c Results from Scheffe post hoc multiple comparisons.

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T.J. Yun, H.R. Cho, S.H. Choi, H. Kim, J.-K. Won, S.-W. Park, J.-h. Kim, C.-H. Sohn, M.H. Han
Antiangiogenic Effect of Bevacizumab: Application of Arterial Spin-Labeling Perfusion MR Imaging in a Rat Glioblastoma Model
American Journal of Neuroradiology Sep 2016, 37 (9) 1650-1656; DOI: 10.3174/ajnr.A4800

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Antiangiogenic Effect of Bevacizumab: Application of Arterial Spin-Labeling Perfusion MR Imaging in a Rat Glioblastoma Model
T.J. Yun, H.R. Cho, S.H. Choi, H. Kim, J.-K. Won, S.-W. Park, J.-h. Kim, C.-H. Sohn, M.H. Han
American Journal of Neuroradiology Sep 2016, 37 (9) 1650-1656; DOI: 10.3174/ajnr.A4800
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