European Radiology

, Volume 28, Issue 11, pp 4871–4881 | Cite as

4D ASL-based MR angiography for visualization of distal arteries and leptomeningeal collateral vessels in moyamoya disease: a comparison of techniques

  • Osamu Togao
  • Akio HiwatashiEmail author
  • Makoto Obara
  • Koji Yamashita
  • Daichi Momosaka
  • Ataru Nishimura
  • Koichi Arimura
  • Nobuhiro Hata
  • Koji Yoshimoto
  • Koji Iihara
  • Marc Van Cauteren
  • Hiroshi Honda



To evaluate the performance of four-dimensional pseudo-continuous arterial spin labeling (4D-pCASL)-based angiography using CENTRA-keyhole and view sharing (4D-PACK) in the visualization of flow dynamics in distal cerebral arteries and leptomeningeal anastomosis (LMA) collaterals in moyamoya disease in comparison with contrast inherent inflow-enhanced multiphase angiography (CINEMA), with reference to digital subtraction angiography (DSA).


Thirty-two cerebral hemispheres from 19 patients with moyamoya disease (mean age, 29.7 ± 19.6 years; five males, 14 females) underwent both 4D-MR angiography and DSA. Qualitative evaluations included the visualization of anterograde middle cerebral artery (MCA) flow and retrograde flow via LMA collaterals with reference to DSA. Quantitative evaluations included assessments of the contrast-to-noise ratio (CNR) on these vessels. The linear mixed-effect model was used to compare the 4D-PACK and CINEMA methods.


The vessel visualization scores were significantly higher with 4D-PACK than with CINEMA in the visualization of anterograde flow for both Observer 1 (CINEMA, 3.53 ± 1.39; 4D-PACK, 4.53 ± 0.80; p < 0.0001) and Observer 2 (CINEMA, 3.50±1.39; 4D-PACK, 4.31 ± 0.86; p = 0.0009). The scores were higher with 4D-PACK than with CINEMA in the visualization of retrograde flow for both Observer 1 (CINEMA, 3.44 ± 1.05; 4D-PACK, 4.47 ± 0.88; p < 0.0001) and Observer 2 (CINEMA, 3.19 ± 1.20; 4D-PACK, 4.38 ± 0.91; p < 0.0001). The maximum CNR in the anterograde flow was higher in 4D-PACK (40.1 ± 16.1, p = 0.0001) than in CINEMA (27.0 ± 16.6). The maximum CNR in the retrograde flow was higher in 4D-PACK (36.1 ± 10.0, p < 0.0001) than in CINEMA (15.4 ± 8.0).


The 4D-PACK provided better visualization and higher CNRs in distal cerebral arteries and LMA collaterals compared with CINEMA in patients with this disease.

Key Points

The 4D-PACK enables good visualization of distal cerebral arteries in moyamoya disease.

The 4D-PACK enables direct visualization of leptomeningeal collateral vessels in moyamoya disease.

Vessel visualization by 4D-PACK can be useful in assessing cerebral hemodynamics.


Magnetic resonance imaging Magnetic resonance angiography Moyamoya disease Collateral circulation Cerebrovascular disorders 



Four-dimensional pseudo-continuous arterial spin labeling-based angiography using CENTRA-keyhole and view sharing


Four dimensional


Acceleration-selective ASL


Cerebral blood flow


Contrast-enhanced timing-robust angiography


Contrast inherent inflow-enhanced multiphase angiography


Contrast-to-noise ratio


Digital subtraction angiography


Echo planer imaging


Internal carotid artery


Leptomeningeal anastomosis


Middle cerebral artery


Maximum intensity projection


Posterior cerebral artery


Pseudo-continuous arterial spin labeling




Region of interest


Stationary tissue


Time of flight



This study has received funding by JSPS KAKENHI grant no. JP 17K10410.

Compliance with ethical standards


The scientific guarantor of this publication is Hiroshi Honda.

Conflict of interest

The authors of this manuscript declare relationships with the following companies: Philips Japan.

Two authors (M.O., M.V.C.) were employees of Philips Japan and provided technical support in sequence development but were not involved in the study design or interpretation of the data.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.


• retrospective

• diagnostic study

• performed at one institution

Supplementary material

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Copyright information

© European Society of Radiology 2018

Authors and Affiliations

  • Osamu Togao
    • 1
  • Akio Hiwatashi
    • 1
    Email author
  • Makoto Obara
    • 2
  • Koji Yamashita
    • 1
  • Daichi Momosaka
    • 1
  • Ataru Nishimura
    • 3
  • Koichi Arimura
    • 3
  • Nobuhiro Hata
    • 3
  • Koji Yoshimoto
    • 3
  • Koji Iihara
    • 3
  • Marc Van Cauteren
    • 2
  • Hiroshi Honda
    • 1
  1. 1.Department of Clinical Radiology, Graduate School of Medical SciencesKyushu UniversityFukuokaJapan
  2. 2.Philips JapanTokyoJapan
  3. 3.Department of Neurosurgery, Graduate School of Medical SciencesKyushu UniversityFukuokaJapan

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