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Research ArticleAdult Brain
Open Access

The Value of Preoperative Phase-Contrast MRI in Predicting the Clinical Outcome of Moyamoya Disease after Encephalo-Duro-Arterial Synangiosis Surgery

S. Liu, M. Lu, C. Han, F. Hao, F. Sheng, Y. Liu, L. Zhang, D. Liu, R. Xie, H. Zhang and J. Cai
American Journal of Neuroradiology November 2022, 43 (11) 1582-1588; DOI: https://doi.org/10.3174/ajnr.A7667
S. Liu
aFrom the Medical School of Chinese People’s Liberation Army (S.L., L.Z.), Beijing, China
bDepartment of Radiology (S.L., F.S., Y.L., L.Z., D.L., R.X., H.Z., J.C.), the fifth Medical Center
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M. Lu
dDepartment of Radiology (M.L.), Pingjin Hospital, Characteristic Medical Center of Chinese People’s Armed Police Force, Tianjin, China
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C. Han
cDepartment of Neurosurgery (C.H., F.H.), Chinese People’s Liberation Army General Hospital, Beijing, China
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F. Hao
cDepartment of Neurosurgery (C.H., F.H.), Chinese People’s Liberation Army General Hospital, Beijing, China
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F. Sheng
bDepartment of Radiology (S.L., F.S., Y.L., L.Z., D.L., R.X., H.Z., J.C.), the fifth Medical Center
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Y. Liu
bDepartment of Radiology (S.L., F.S., Y.L., L.Z., D.L., R.X., H.Z., J.C.), the fifth Medical Center
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L. Zhang
aFrom the Medical School of Chinese People’s Liberation Army (S.L., L.Z.), Beijing, China
bDepartment of Radiology (S.L., F.S., Y.L., L.Z., D.L., R.X., H.Z., J.C.), the fifth Medical Center
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D. Liu
bDepartment of Radiology (S.L., F.S., Y.L., L.Z., D.L., R.X., H.Z., J.C.), the fifth Medical Center
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R. Xie
bDepartment of Radiology (S.L., F.S., Y.L., L.Z., D.L., R.X., H.Z., J.C.), the fifth Medical Center
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H. Zhang
bDepartment of Radiology (S.L., F.S., Y.L., L.Z., D.L., R.X., H.Z., J.C.), the fifth Medical Center
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J. Cai
bDepartment of Radiology (S.L., F.S., Y.L., L.Z., D.L., R.X., H.Z., J.C.), the fifth Medical Center
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  • FIG 1.
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    FIG 1.

    PC-MR imaging and DSA examination in a patient with good collateral formation. Images in a female patient diagnosed with MMD who had right EDAS surgery. She underwent PC-MRI and DSA before and 6 months after the operation. A, Phase image shows the ROI of the right STA. A, the arrow represents the enlarged view of the small white square. Modulation of the Vmean (B), Vpeak (C), and BVF (D) of the right STA acquired by PC-MRI. Anterior-posterior and lateral projections of preoperative (E and F) and postoperative (G and H) DSAs of the right external carotid artery show large areas of revascularization (more than one-third but less than two-thirds of MCA territory).

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    FIG 2.

    PC-MR imaging and DSA examination in a patient with poor collateral formation. Images in a male patient diagnosed with MMD who had right EDAS surgery. He underwent PC-MRI and DSA before and 7 months after the operation. A, Phase image shows the ROI of the right STA. A, the arrow represents the enlarged view of the small white square. Modulation of Vmean (B), Vpeak (C), and BVF (D) of the right STA acquired by PC-MRI. Anterior-posterior and lateral projections of preoperative (E and F) and postoperative (G and H) DSAs of right external carotid artery show small areas of revascularization (less than one-third of the MCA territory).

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    FIG 3.

    Comparison of PC-MR imaging parameters between patients with good and poor collateral formation (A) and between patients with improved mRS and poor response (B). The asterisk indicates P < .05.

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    Table 1:

    Demographic and clinical characteristics

    Patients with MMD, Mean (SD) or No. (%)P
    Good Collateral Formation (n = 23)Poor Collateral Formation (n = 22)
    Sex, male10 (43%)12 (55%).458
    Age (yr)30.87 (SD, 18.36)37.05 (SD, 17.57).256
    Hypertension8 (35%)9 (41%).672
    Hyperlipidemia9 (39%)11 (50%).463
    CHD1 (4%)0 (0%)1.000
    Diabetes3 (13%)2 (10%)1.000
    Smoking0 (0%)3 (14%).217
    DSA interval (mo)7.11 (SD, 1.69)7.73 (SD, 1.91).256
    PCA involvement4 (17%)2 (9%).704
    Diameter of MMA (mm)
     Ipsilateral2.49 (SD, 0.51)2.42 (SD, 0.4).674
     Contralateral2.30 (SD, 0.45)2.19 (SD, 0.46).417
    Preoperative DSC
     Ipsilateral rTTP (sec)3.36 (SD, 2.07)1.40 (SD, 1.57).002
     Contralateral rTTP (sec)1.72 (SD, 2.10)1.07 (SD, 2.18).353
     Ipsilateral CBF (mL/100 g/min)1.04 (SD, 0.31)1.31 (SD, 0.44).021
     Contralateral CBF (mL/100 g/min)1.18 (SD, 0.34)1.24 (SD, 0.31).540
     Ipsilateral CBV (mL/100 g)1.77 (SD, 0.62)2.23 (SD, 0.65).019
     Contralateral CBV (mL/100 g)1.89 (SD, 0.48)2.12 (SD, 0.54).138
    Suzuki stage.775
     I–II42
     III– IV1317
     V–VI63
    • Note:—CHD indicates coronary heart disease; DSA interval, interval from surgery to DSA examination; PCA, posterior cerebral artery.

    • View popup
    Table 2:

    Comparison of measurements of the STA between participants with good and poor collateral formation

    Patients with MMD, Mean (SD) or No. (%)P
    Good Collateral Formation (n = 23)Poor Collateral Formation (n = 22)
    Morphologic features of ipsilateral STA
     Cross-sectional area (mm2)0.10 (SD, 0.03)0.09 (SD, 0.02).258
     Straightness11 (48%)13 (59%).449
     High bifurcation position10 (43%)10 (46%).894
    Morphologic features of contralateral STA
     Cross-sectional area (mm2)0.11 (SD, 0.02)0.12 (SD, 0.04).095
     Straightness12 (52%)2 (55%).873
     High bifurcation position14 (61%)9 (41%).181
    PC-MR imaging of ipsilateral STA
     Vmean (cm/s)6.69 (SD, 2.02)5.30 (SD, 1.41).011
     Vpeak (cm/s)22.62 (SD, 5.79)17.00 (SD, 6.62).004
     BVF (mL/s)0.70 (SD, 0.32)0.50 (SD, 0.17).013
    PC-MR imaging of contralateral STA
     Vmean (cm/s)7.08 (SD, 2.92)6.03 (SD, 1.53).141
     Vpeak (cm/s)23.06 (SD, 6.37)18.75 (SD, 6.07).025
     BVF (mL/s)0.74 (SD, 0.35)0.61 (SD, 0.26).166
    • Note:—Ipsilateral STA indicates superficial temporal artery on the operative side; Contralateral STA, superficial temporal artery on the nonoperative side.

    • View popup
    Table 3:

    Association of hemodynamic status of the ipsilateral STA and collateral formation using logistic regression analysisa

    Univariate RegressionMultivariate Regression
    OR95% CIPOR95% CIP
    Vmean1.661.08–2.53.0202.281.23–4.25.009
    Vpeak1.161.04–1.30.0091.181.04–1.34.010
    BVF1.041.01–1.07.0241.731.02–2.94.043
    • ↵a Multivariate regression was adjusted for age, sex, hypertension, hyperlipidemia, diabetes, smoking, interval from the operation to the latest DSA examination, cross-sectional area, straightness and high bifurcation position of the STA, preoperative rCBV, and the diameter of the MMA after EDAS.

    • View popup
    Table 4:

    Comparison of PC-MR imaging of STA between participants with improved mRS and those with poor response

    Patients with MMD, Mean (SD) or No. (%)P
    Improved mRS (n = 24)Poor Response mRS (n = 21)
    PC-MR imaging of ipsilateral STA
     Vmean (cm/s)6.43 (SD, 1.91)5.53 (SD, 1.73).106
     Vpeak (cm/s)22.13 (SD, 6.59)17.30 (SD, 6.13).015
     BVF (mL/s)0.65 (SD, 0.30)0.55 (SD, 0.24).268
    PC-MR imaging of contralateral STA
     Vmean (cm/s)6.92 (SD, 2.37)6.15 (SD, 2.50).295
     Vpeak (cm/s)21.97 (SD, 6.60)19.79 (SD, 6.22).263
     BVF (mL/s)0.71 (SD, 0.28)0.64 (SD, 0.34).453
    • View popup
    Table 5:

    Interactive effects of age, sex, and rCBV on collateral formation

    FP
    Age1.829.186
    Sex1.773.193
    rCBV1.839.185
    Age × sex1.781.192
    Age × rCBV1.832.186
    Sex × rCBV1.756.195
    Age × sex × rCBV1.77.193
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American Journal of Neuroradiology: 43 (11)
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S. Liu, M. Lu, C. Han, F. Hao, F. Sheng, Y. Liu, L. Zhang, D. Liu, R. Xie, H. Zhang, J. Cai
The Value of Preoperative Phase-Contrast MRI in Predicting the Clinical Outcome of Moyamoya Disease after Encephalo-Duro-Arterial Synangiosis Surgery
American Journal of Neuroradiology Nov 2022, 43 (11) 1582-1588; DOI: 10.3174/ajnr.A7667

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Preop Phase-Contrast MRI in Moyamoya Outcome
S. Liu, M. Lu, C. Han, F. Hao, F. Sheng, Y. Liu, L. Zhang, D. Liu, R. Xie, H. Zhang, J. Cai
American Journal of Neuroradiology Nov 2022, 43 (11) 1582-1588; DOI: 10.3174/ajnr.A7667
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