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Research ArticleAdult Brain

Visualization and Classification of Deeply Seated Collateral Networks in Moyamoya Angiopathy with 7T MRI

T. Matsushige, M. Kraemer, T. Sato, P. Berlit, M. Forsting, M.E. Ladd, R. Jabbarli, U. Sure, N. Khan, M. Schlamann and K.H. Wrede
American Journal of Neuroradiology July 2018, 39 (7) 1248-1254; DOI: https://doi.org/10.3174/ajnr.A5700
T. Matsushige
aFrom the Department of Neurosurgery (T.M., T.S., R.J., U.S., K.H.W.), University Hospital Essen, University Duisburg-Essen, Essen, Germany
bDepartment of Neurosurgery (T.M.), Graduate School of Biomedical and Health Sciences, Hiroshima University, Hiroshima, Japan
cErwin L. Hahn Institute for Magnetic Resonance Imaging (T.M., T.S., M.E.L., K.H.W.), University Duisburg-Essen, Essen, Germany
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M. Kraemer
dDepartment of Neurology (M.K., P.B.), Alfried Krupp Hospital, Essen, Germany
eDepartment of Neurology (M.K.), University Hospital Duesseldorf, Duesseldorf, Germany
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T. Sato
aFrom the Department of Neurosurgery (T.M., T.S., R.J., U.S., K.H.W.), University Hospital Essen, University Duisburg-Essen, Essen, Germany
cErwin L. Hahn Institute for Magnetic Resonance Imaging (T.M., T.S., M.E.L., K.H.W.), University Duisburg-Essen, Essen, Germany
fDepartment of Neurosurgery (T.S.), Fukushima Medical University, Fukushima, Japan
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P. Berlit
dDepartment of Neurology (M.K., P.B.), Alfried Krupp Hospital, Essen, Germany
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M. Forsting
gDepartment of Diagnostic and Interventional Radiology and Neuroradiology (M.F., M.S.), University Hospital Essen, Essen, Germany
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M.E. Ladd
cErwin L. Hahn Institute for Magnetic Resonance Imaging (T.M., T.S., M.E.L., K.H.W.), University Duisburg-Essen, Essen, Germany
hMedical Physics in Radiology (M.E.L.), German Cancer Research Center, Heidelberg, Germany
iFaculty of Physics and Astronomy and Faculty of Medicine (M.E.L.), University of Heidelberg, Heidelberg, Germany
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R. Jabbarli
aFrom the Department of Neurosurgery (T.M., T.S., R.J., U.S., K.H.W.), University Hospital Essen, University Duisburg-Essen, Essen, Germany
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U. Sure
aFrom the Department of Neurosurgery (T.M., T.S., R.J., U.S., K.H.W.), University Hospital Essen, University Duisburg-Essen, Essen, Germany
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N. Khan
jMoyamoya Center, Division of Pediatric Neurosurgery (N.K.), Department of Surgery, University Children's Hospital Zurich, Zurich, Switzerland
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M. Schlamann
gDepartment of Diagnostic and Interventional Radiology and Neuroradiology (M.F., M.S.), University Hospital Essen, Essen, Germany
kDepartment of Neuroradiology (M.S.), University Hospital Cologne, Cologne, Germany.
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K.H. Wrede
aFrom the Department of Neurosurgery (T.M., T.S., R.J., U.S., K.H.W.), University Hospital Essen, University Duisburg-Essen, Essen, Germany
cErwin L. Hahn Institute for Magnetic Resonance Imaging (T.M., T.S., M.E.L., K.H.W.), University Duisburg-Essen, Essen, Germany
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  • Fig 1.
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    Fig 1.

    Schematic illustrations of deeply seated collateral networks are shown in coronal (A) and sagittal (B) MR imaging views. Six pathways of collateral vessels according to perfusing territories can be divided into collateral networks to cortical vessels (remote, type a and b) and to major trunk vessels (local, types c–f). Anastomoses between striate arteries or choroidal arteries and cortical arteries directly or via medullary arteries (a); septal transcallosal anastomoses between choroidal arteries with pericallosal arteries (b); anastomoses between choroidal arteries or the posterior communicating artery and thalamostriate arteries (c); intrastriatal anastomosis among striatal arteries (d); intrathalamic anastomosis among thalamic arteries (e); and focal Moyamoya vessels in the basal cistern (f).

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    Fig 2.

    Case 1. Selective right internal carotid angiography (anteroposterior, A; lateral view, B) shows anastomotic connections to cortical arteries from the anterior choroidal artery (black arrowheads, type b) as well as from thalamostriate arteries (white arrows, type a). Collateral networks are excellently visualized in MIP from TOF-MRA with slab thickness of 20 mm (white arrows and black arrowheads) (C). Transcallosal connections to cortical arteries (white arrowheads) not detected by DSA are poorly visualized on MPRAGE (D).

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    Fig 3.

    Case 8. Selective right internal carotid angiography (anteroposterior, A; right 45°oblique view, B) shows anastomosis between the posterior communicating artery and the thalamostriate arteries (arrows, type c). MIP from TOF-MRA (C) demonstrates this anastomosis clearly as well as connection with the anterior choroidal artery (asterisk). The latter anastomosis could neither be detected in DSA nor visualized by MIP from MPRAGE (D).

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    Fig 4.

    Case 5. Selective right internal carotid angiography (right 45° oblique, A; left 45° oblique view, B) shows intrastriatal anastomoses among thalamostriate arteries running through the periventricular space (arrows, type d). MIP from TOF-MRA (C) excellently demonstrates these networks as well as focal connections among Moyamoya vessels in the basal cistern (asterisk, type f). MIP from MPRAGE (D) moderately depicts the network; however, basal Moyamoya vessels are poorly visualized.

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    Fig 5.

    Case 6. Selective left vertebral angiography (anteroposterior, A; lateral view, B) shows no marked anastomosis. The MIP from TOF-MRA (C) demonstrates excellent visualization of inner thalamic anastomosis among posterior thalamostriate arteries (white arrows, type e), whereas the visualization is only moderate on MIP from MPRAGE (D).

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    Fig 6.

    Case 10. Selective right vertebral angiography (anteroposterior, A; lateral view, B) shows a tiny, barely visible anastomosis (black arrows) between the posterior thalamostriate artery and a medullary-cortical artery. MIP from TOF-MRA (C) and MIP from MPRAGE (D) do not delineate the anastomosis. The white arrow (C) indicates the supposed anatomic location of the anastomosis.

Tables

  • Figures
  • Comparison of 7T MRA and DSA regarding the number of detected collateral networks and image quality for anastomoses to major trunk vessels and collateral pathways to cortical vessels

    TypeConnecting Vessels in Collateral NetworksDSATOF-MRAMPRAGE
    Collateral networks connecting to cortical arteries
        aStriate/choroidal arteries and medullary-cortical arteries11168
        bStriate/choroidal arteries and the pericallosal arteries794
    Total182512
    Image quality (n = 18)a (mean) (SEM) (range)4.0 (0.26, 3–5)4.8 (0.10, 3–5)2.4 (0.35, 1–5)
    Collateral networks connecting to major trunk vessels
        cChoroidal arteries or PcomA and thalamostriate arteries21199
        dIntrastriatal arteries212216
        eIntrathalamic arteries886
        fMoyamoya vessels in the basal cistern323230
    Total828161
    Image quality (n = 82)a (mean) (SEM) (range)4.6 (0.07, 2–5)4.4 (0.12, 3–5)2.7 (0.13, 1–5)
    • Note:—PcomA indicates posterior communicating artery.

    • ↵a Image quality was evaluated in collateral networks detected by DSA as a clinical standard using a 5-point scale.

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American Journal of Neuroradiology: 39 (7)
American Journal of Neuroradiology
Vol. 39, Issue 7
1 Jul 2018
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Cite this article
T. Matsushige, M. Kraemer, T. Sato, P. Berlit, M. Forsting, M.E. Ladd, R. Jabbarli, U. Sure, N. Khan, M. Schlamann, K.H. Wrede
Visualization and Classification of Deeply Seated Collateral Networks in Moyamoya Angiopathy with 7T MRI
American Journal of Neuroradiology Jul 2018, 39 (7) 1248-1254; DOI: 10.3174/ajnr.A5700

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Visualization and Classification of Deeply Seated Collateral Networks in Moyamoya Angiopathy with 7T MRI
T. Matsushige, M. Kraemer, T. Sato, P. Berlit, M. Forsting, M.E. Ladd, R. Jabbarli, U. Sure, N. Khan, M. Schlamann, K.H. Wrede
American Journal of Neuroradiology Jul 2018, 39 (7) 1248-1254; DOI: 10.3174/ajnr.A5700
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