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Research ArticleAdult Brain
Open Access

Are Dynamic Arterial Spin-Labeling MRA and Time-Resolved Contrast-Enhanced MRA Suited for Confirmation of Obliteration following Gamma Knife Radiosurgery of Brain Arteriovenous Malformations?

A. Rojas-Villabona, F.B. Pizzini, T. Solbach, M. Sokolska, G. Ricciardi, C. Lemonis, E. DeVita, Y. Suzuki, M.J.P. van Osch, R.I. Foroni, M. Longhi, S. Montemezzi, D. Atkinson, N. Kitchen, A. Nicolato, X. Golay and H.R. Jäger
American Journal of Neuroradiology April 2021, 42 (4) 671-678; DOI: https://doi.org/10.3174/ajnr.A6990
A. Rojas-Villabona
aFrom The Gamma Knife Centre at Queen Square (A.R.-V.)
dDepartment of Neurosurgery (A.R.-V.), Royal Victoria Infirmary, Newcastle upon Tyne, UK
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  • ORCID record for A. Rojas-Villabona
F.B. Pizzini
eDepartment of Radiology (F.B.P., R.I.F.), Department of Diagnostic and Public Health, Verona University, Verona, Italy
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T. Solbach
bThe Lysholm Department of Neuroradiology (T.S., H.R.J.)
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M. Sokolska
fDepartment of Medical Physics and Bioengineering (M.S.)
gNeuroradiological Academic Unit (M.S., X.G., H.R.J.)
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G. Ricciardi
nNeuroradiology Unit (G.R., C.L.), Department of Diagnostic and Pathology, University Hospital of Verona, Verona, Italy
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C. Lemonis
nNeuroradiology Unit (G.R., C.L.), Department of Diagnostic and Pathology, University Hospital of Verona, Verona, Italy
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E. DeVita
iSchool of Biomedical Engineering and Imaging Sciences (E.D.V.), King’s College London, London, UK
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Y. Suzuki
jWellcome Centre for Integrative Neuroimaging (Y.S.), FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK
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M.J.P. van Osch
kC.J. Gorter Center for High Field MRI (M.J.P.v.O.), Department of Radiology, Leiden University Medical Center, Leiden, Netherlands
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R.I. Foroni
eDepartment of Radiology (F.B.P., R.I.F.), Department of Diagnostic and Public Health, Verona University, Verona, Italy
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M. Longhi
lDepartment of Neuroscience (M.L., A.N.)
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S. Montemezzi
mRadiology Unit (S.M.)
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D. Atkinson
hDepartment of Brain Repair and Rehabilitation, Institute of Neurology and Centre for Medical Imaging (D.A.), University College London, London, UK
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N. Kitchen
cDepartment of Neurosurgery (N.K.), National Hospital for Neurology and Neurosurgery, London, UK
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A. Nicolato
lDepartment of Neuroscience (M.L., A.N.)
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X. Golay
gNeuroradiological Academic Unit (M.S., X.G., H.R.J.)
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H.R. Jäger
bThe Lysholm Department of Neuroradiology (T.S., H.R.J.)
gNeuroradiological Academic Unit (M.S., X.G., H.R.J.)
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  • FIG 1.
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    FIG 1.

    Post-GKR DSA and MRA of a study case in which the residual AVM was not visualized on ASL-MRA (case 30). Post-GKR DSA (A and B) shows a residual AVM nidus (white arrow) fed by the left posterior cerebral artery. CE-MRA (E–F) shows slow filling of the AVM nidus (white arrow) lateral to the deep venous system. No residual AVM is noted on ASL-MRA (C and D).

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    FIG 2.

    Representative case of a residual AVM not visualized on CE-MRA (case 13). The pre-GKR DSA (A) shows 2 AVM nidi (white arrows) at the time of GKR in a patient with previous partial surgical excision of a ruptured AVM. The most lateral nidus is not identified in post-GKR imaging; however, a residual of the most medial nidus (arrowheads) is identified on post-GKR DSA (B) and ASL-MRA (C and D). The small size of the lesion renders it not identifiable on the CE-MRA (E–F).

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    FIG 3.

    Characterization of a residual AVM (case 19) using ASL (D–F) and CE-MRA (G–I) compared with DSA (A–C) . The feeding arteries of this AVM, which are branches of the anterior and middle cerebral arteries (white arrows), are clearly depicted on ASL-MRA and CE-MRA . The draining veins (arrowheads) seen on DSA can also be identified on ASL and CE-MRA, and they involve both the superficial venous system via the superior sagittal sinus and the deep system via the left internal cerebral vein.

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    Table 1:

    Demographic details and AVM characteristics of the study subjects

    Characteristics
    Age (mean) (range) (yr)37 (18–69)
    Female (%)66%
    AVM location (No.) (%)
     Temporal9 (30%)
     Frontal6 (20%)
     Parietal6 (20%)
     Occipital3 (10%)
     Basal ganglia/brain stem4 (13%)
     Posterior fossa2 (7%)
    Lateralization (%)
     Right30%
     Left70%
    AVM volume (mean) (range) (mL)7.01 (0.07–50.54)
    GKR (mean) (range)
     Dose (Gy)17  (11–22)
     Percentage isodose50%
    Mean time post-GKR (range) (mo)53 (22–168)
    • View popup
    Table 2:

    Scanning parameters of ASL-MRA and CE-MRA

    ParameterASL-MRACE-MRA
    MRA typeDynamic (4D)Dynamic (4D)
    Scan duration (min:sec)5:583:19
    Contrast
     AcquisitionT1-TFEPIT1-FFE
     TR (ms)123
     TE (ms)51
     Flip angle10°25°
    Resolution
     FOV (RL × AP × CC mm)210 × 210 × 90150 × 210 × 210
    AcquisitionTransversalSagittal
    Slabs11
    Acquisition matrix172 × 172 × 7050 × 248 × 248
    Acquired voxel size (mm)1.22 × 1.26 × 1.33 × 0.85 × 0.85
    Reconstruction matrix256 × 256288 × 288
    reconstructed voxel size (mm)0.82 × 0.82 × 0.651.5 × 0.73 × 0.73
    No. of slices140100
    SENSE factor2.5/14/2
    Dynamic acquisition
     Dynamic imaging modeTFEPICENTRA keyhole
     No. of dynamic phases824
     Phase interval (temporal resolution) (ms)200 608 
     Label delay (ms)200 –
     Contrast–Gadovist 0.1 mL/Kg; IV pump injection: 3.5 mL/s
    • Note:—indicates non-applicable; TFEPI, Turbo-field echo-planar imaging; FFE, fast-field echo; CENTRA, enhanced robust-timing angiography; RL, right-left; AP, anterior-posterior; CC, caudo-cranial; SENSE, sensitivity encoding.

    • View popup
    Table 3:

    Identification of residual AVM with DSA, ASL-MRA, and CE-MRA in cases with a residual lesion

    CaseResidual AVM
    DSAASL-MRACE-MRA
    3YesYesYes
    6YesYesYes
    9YesYesNoa
    10YesYesYes
    11YesYesYes
    13YesYesNoa
    19YesYesYes
    23YesYesYes
    30YesNoaYes
    • ↵a False-negative.

    • View popup
    Table 4:

    Sensitivity, specificity, PPV, and NPV of ASL-MRA, CE-MRA, and the combination of the 2 for detection of residual AVMs

    ASL-MRACE-MRABoth
    Sensitivity88%77%100%
    Specificity100%100%100%
    PPV100%100%100%
    NPV95%90%100%
    Diagnostic accuracy (ROC)0.94 (P < .001)a0.89 (P = .002)a1 (P < .001)a
    Agreement (κ)0.92 (P < .001)0.82 (P < .001)1 (P < .001)
    • ↵a Null hypothesis: true area = 0.5.

    • View popup
    Table 5:

    Characterization of residual AVMs using ASL-MRA and CE-MRA compared with DSA

    Observer 1Observer 2
    DSAMRADSAMRA
    SMS
     Size
      <3 cm7777
      3–6 cm2222
      >6 cm––––
     Drainage
      Superficial only5555
      Deep4444
     Eloquence
      Noneloquent5434
      Eloquent4565
    Feeding arteries14141715
    Draining veins13131512
    • Note:—indicates non-applicable; SMS, Spetzler-Martin Score.

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American Journal of Neuroradiology: 42 (4)
American Journal of Neuroradiology
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1 Apr 2021
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A. Rojas-Villabona, F.B. Pizzini, T. Solbach, M. Sokolska, G. Ricciardi, C. Lemonis, E. DeVita, Y. Suzuki, M.J.P. van Osch, R.I. Foroni, M. Longhi, S. Montemezzi, D. Atkinson, N. Kitchen, A. Nicolato, X. Golay, H.R. Jäger
Are Dynamic Arterial Spin-Labeling MRA and Time-Resolved Contrast-Enhanced MRA Suited for Confirmation of Obliteration following Gamma Knife Radiosurgery of Brain Arteriovenous Malformations?
American Journal of Neuroradiology Apr 2021, 42 (4) 671-678; DOI: 10.3174/ajnr.A6990

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Are Dynamic Arterial Spin-Labeling MRA and Time-Resolved Contrast-Enhanced MRA Suited for Confirmation of Obliteration following Gamma Knife Radiosurgery of Brain Arteriovenous Malformations?
A. Rojas-Villabona, F.B. Pizzini, T. Solbach, M. Sokolska, G. Ricciardi, C. Lemonis, E. DeVita, Y. Suzuki, M.J.P. van Osch, R.I. Foroni, M. Longhi, S. Montemezzi, D. Atkinson, N. Kitchen, A. Nicolato, X. Golay, H.R. Jäger
American Journal of Neuroradiology Apr 2021, 42 (4) 671-678; DOI: 10.3174/ajnr.A6990
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  • Diagnostic Performance of TOF, 4D MRA, Arterial Spin-Labeling, and Susceptibility-Weighted Angiography Sequences in the Post-Radiosurgery Monitoring of Brain AVMs
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