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Research ArticlePediatrics

Predictive Value of MRI in Diagnosing Brain AVM Recurrence after Angiographically Documented Exclusion in Children

A. Jhaveri, A. Amirabadi, P. Dirks, A.V. Kulkarni, M.M. Shroff, N. Shkumat, T. Krings, V.M. Pereira, V. Rea and P. Muthusami
American Journal of Neuroradiology July 2019, 40 (7) 1227-1235; DOI: https://doi.org/10.3174/ajnr.A6093
A. Jhaveri
aFrom Pediatric Neuroradiology and Image Guided Therapy (A.J., A.A., M.M.S., N.S., V.R., P.M.), Diagnostic Imaging
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A. Amirabadi
aFrom Pediatric Neuroradiology and Image Guided Therapy (A.J., A.A., M.M.S., N.S., V.R., P.M.), Diagnostic Imaging
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P. Dirks
bDivision of Neurosurgery (P.D., A.V.K.), Department of Surgery, The Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada
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A.V. Kulkarni
bDivision of Neurosurgery (P.D., A.V.K.), Department of Surgery, The Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada
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M.M. Shroff
aFrom Pediatric Neuroradiology and Image Guided Therapy (A.J., A.A., M.M.S., N.S., V.R., P.M.), Diagnostic Imaging
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N. Shkumat
aFrom Pediatric Neuroradiology and Image Guided Therapy (A.J., A.A., M.M.S., N.S., V.R., P.M.), Diagnostic Imaging
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T. Krings
cDivisions of Neuroradiology and Neurosurgery (T.K.,V.M.P.), Departments of Medical Imaging and Surgery, University of Toronto, and Toronto Western Hospital, University Health Network, Toronto, Ontario, Canada.
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V.M. Pereira
cDivisions of Neuroradiology and Neurosurgery (T.K.,V.M.P.), Departments of Medical Imaging and Surgery, University of Toronto, and Toronto Western Hospital, University Health Network, Toronto, Ontario, Canada.
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V. Rea
aFrom Pediatric Neuroradiology and Image Guided Therapy (A.J., A.A., M.M.S., N.S., V.R., P.M.), Diagnostic Imaging
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P. Muthusami
aFrom Pediatric Neuroradiology and Image Guided Therapy (A.J., A.A., M.M.S., N.S., V.R., P.M.), Diagnostic Imaging
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    Fig 1.

    MR imaging appearances of true-positive AVM recurrence. A, Recurrent nidus in a 7-year-old girl with a right choroidal AVM that was embolized with n-BCA through a posterolateral choroidal feeder, with postembolization digital subtraction angiography confirming exclusion. B, Axial section from TOF-MRA performed 6 months posttreatment showing a tuft of vessels (arrow) posterior to the right lateral ventricular choroid plexus. This was also seen on contrast-enhanced MR imaging (not shown here) as exuberant and asymmetric choroid enhancement. C, Conventional angiogram, obtained 3 weeks after MR imaging, confirms an AVM nidus. Left vertebral artery injection confirms a right choroidal nidus (arrow) with deep venous drainage. The patient subsequently underwent radiosurgery. D, Recurrent cerebellar AVM in a 11-year-old girl with hereditary hemorrhagic telengiectasia lateral angiogram with negative findings immediately following endovascular embolization through a cerebellar branch of the right posterior inferior cerebellar artery. E, Sagittal section from postgadolinium MR imaging 3 months after treatment shows a nodular juxtamural focus of enhancement (arrow), with a vein traceable to the torcular. F, Conventional angiogram performed 1 month after MR imaging confirms this to be a recurrent nidus with early venous drainage. The recurrent AVM was surgically removed.

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    Fig 2.

    False-negative MR imaging findings for brain AVM recurrence, confirmed by digital subtraction and 3D rotational angiography. A 16-year-old boy with a left occipital AVM treated by embolization with Onyx. A, Frontal projection, left internal carotid angiography, shows a hypertrophied temporo-occipital middle cerebral artery branch suppling a compact nidus, with superficial venous drainage. B, Postembolization frontal angiogram shows complete exclusion of the shunt. C, Axial postgadolinium MR imaging section obtained 1 year after angiographically documented cure shows the hematoma cavity with artifacts from the Onyx cast within, but no suggestion of recurrence. D, Volume-rendered reformat obtained from 3D rotational angiography in the left vertebral artery shows a nidus behind the Onyx cast, with a prominent feeder (thin arrow) and early draining vein (thick arrow), which was also confirmed on digital subtraction angiography (E).

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    Fig 3.

    False-positive MR imaging for brain AVM recurrence, confirmed by conventional angiography and 3DRA-MR imaging fusion. A 5-year-old boy with a left parietal AVM. A, Left internal carotid injection in the lateral projection during conventional angiography shows a postcentral diffuse AVM nidus with a deep white matter component, hypertrophied anterior and middle cerebral arterial feeders, and venous drainage into the superior sagittal sinus. B, Complete surgical resection was performed after partial embolization, with cure confirmed with postresection angiography. C, Axial postgadolinium section from MR imaging performed 1 year after cure shows central linear and nodular enhancement suspicious for recurrence. D, Digital subtraction angiographic image, left internal carotid injection, shows no AVM recurrence. This was also confirmed from injections into the posterior circulation. E, 3DRA-MR imaging fusion shows no vascularity within the encephalomalacic cavity, excluding recurrence. MR imaging enhancement is believed to be related to scar tissue or dural folds.

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    Fig 4.

    3DRA-MR imaging fusion for accurate depiction of a small AVM recurrence. A, Axial CTA section in an 8-year-old child who presented with sudden reduced level of consciousness, showing a right temporal hematoma and an anterior temporal AVM with an anterolaterally directed pseudoaneurysm (arrow). B, Microcatheter injection into the temporopolar branch of the right middle cerebral artery shows the AVM and rupture point (arrow). C, This was embolized with n-BCA in Lipiodol, achieving a complete angiographic cure. D, MR imaging performed 1 year after treatment shows a small juxtamural nodular enhancement (arrow) on this postgadolinium coronal section. E, Basal view from a right internal carotid injection on subsequent conventional angiography confirms recurrent arteriovenous shunting (arrow). F, 3DR-MR imaging coronal fused image confirms CEMRI findings, as well as providing exquisite delineation of feeding arteries and draining vein (not shown here). This sequence, providing all requisite information for surgical resection, was used for intraoperative neuronavigation.

Tables

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    Table 1:

    Patient demographics in our cohort of pediatric bAVMs (N = 39)a

    Demographics
    Age (mean) (range) (yr)10.8 ± 3.9, 2–17
    Male/female ratio19/20
    Presentation
        Hemorrhage28 (71.2)
        Seizures5 (12.8)
        HHT screening3 (7.7)
        Incidental (screening for headache)2 (5.1)
        Partially treated at outside institution1 (2.6)
    SM grade
        I10 (26)
        II24 (61.5)
        III4 (10.3)
        IV1 (2.6)
    Location
        Frontal5 (12.8)
        Parietal9 (23.1)
        Temporal11 (28.2)
        Occipital9 (23.1)
        Brain stem1 (2.6)
        Cerebellar3 (7.7)
        Choroidal1 (2.6)
    Arterial feeder type
        Terminal19 (48.7)
        En passant20 (51.3)
    Venous drainage
        Superficial only31 (79.5)
        Deep (±superficial drainage)8 (20.5)
    Venous stenosis
        Present3 (7.7)
        Absent36 (92.3)
    Compactness
        Compact30 (76.9)
        Diffuse9 (23.1)
    Treatment
        Surgery20 (51.3)
        Embolization11 (28.2)
        Radiosurgery3 (7.7)
        Multimodality5 (12.8)
    • Note:—HHT indicates hereditary hemorrhagic telengiectasia.

    • ↵a Data are numbers (%) unless otherwise indicated.

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    Table 2:

    Results of multivariable logistic regression model to predict bAVM recurrence

    Odds Ratio (95% CI)P Value
    Age at diagnosis (yr)0.9 (0.7–1.3).914
    Sex (M)3.3 (0.4–28.7).287
    SM grade0.2 (0.0–1.2).079
    Diffuse nidus (compact vs diffuse)0.2 (0.0–2.8).256
    Draining vein stenosis (yes vs no)1.6 (0.0–130.3).831
    Embolization only treatment (yes vs no)32.4 (2.7–386.3).006
    • View popup
    Table 3:

    Sensitivity, specificity, PPV, and NPV for CEMRI, TOF-MRA, and a combination of both to diagnose recurrent brain AVM after treatment in children

    CEMRITOF-MRACEMRI + TOF-MRA
    Sensitivity84.6%50.0%75.0%
    Specificity38.5%96.1%90.9%
    PPV40.7%85.7%85.7%
    NPV81.8%79.3%83.3%
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American Journal of Neuroradiology: 40 (7)
American Journal of Neuroradiology
Vol. 40, Issue 7
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A. Jhaveri, A. Amirabadi, P. Dirks, A.V. Kulkarni, M.M. Shroff, N. Shkumat, T. Krings, V.M. Pereira, V. Rea, P. Muthusami
Predictive Value of MRI in Diagnosing Brain AVM Recurrence after Angiographically Documented Exclusion in Children
American Journal of Neuroradiology Jul 2019, 40 (7) 1227-1235; DOI: 10.3174/ajnr.A6093

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Predictive Value of MRI in Diagnosing Brain AVM Recurrence after Angiographically Documented Exclusion in Children
A. Jhaveri, A. Amirabadi, P. Dirks, A.V. Kulkarni, M.M. Shroff, N. Shkumat, T. Krings, V.M. Pereira, V. Rea, P. Muthusami
American Journal of Neuroradiology Jul 2019, 40 (7) 1227-1235; DOI: 10.3174/ajnr.A6093
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