A perfusion territory shift attributable solely to the secondary collaterals in moyamoya patients: a potential risk factor for preoperative hemorrhagic stroke revealed by t-ASL and 3D-TOF-MRA

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OBJECTIVE

The authors conducted a study to noninvasively and nonradioactively reveal moyamoya disease (MMD) intracerebral perfusion and perfusion territory supplied by the unilateral internal carotid artery (ICA) and external carotid artery (ECA) and bilateral vertebral arteries (VAs) before surgery and to further identify risk factors for preoperative hemorrhage in adult MMD.

METHODS

Forty-three consecutive adult patients with bilateral MMD underwent unenhanced T1-weighted MRI, territorial arterial spin labeling (t-ASL), and unenhanced 3D time-of-flight MRA (3D-TOF-MRA). Clinical factors, including age, sex, hypertension, diabetes mellitus, hyperlipidemia, current smoking status, and history of taking aspirin, were gathered and stratified. Univariate logistic regression analyses were used to examine the relationship between various risk factors and the occurrence of preoperative hemorrhage. Stepwise multivariate logistic regression analyses were used to determine independent risk factors of preoperative hemorrhage in MMD.

RESULTS

Among the 86 MMD hemispheres, t-ASL revealed 137 perfusion territory shifts in 79 hemispheres. Five distinct categories of perfusion territory shifts were observed on t-ASL maps. The subtypes of perfusion territory shift on t-ASL maps were further subdivided into 2 different categories, group A and group B, in combination with findings on 3D-TOF-MRA. A perfusion territory shift attributable solely to the secondary collaterals was a potential independent risk factor for preoperative hemorrhage (p = 0.026; 95% CI 1.201–18.615; OR 4.729). After eliminating the influence of the secondary collaterals, the primary collaterals had no significant effect on the risk of preoperative hemorrhage (p = 0.182).

CONCLUSIONS

t-ASL could reveal comprehensive MMD cerebral blood perfusion and the vivid perfusion territory shifts fed by the unilateral ICA and ECA and bilateral VAs in a noninvasive, straightforward, nonradioactive, and nonenhanced manner. 3D-TOF-MRA could subdivide t-ASL perfusion territory shifts according to their shunt arteries. A perfusion territory shift attributable to the secondary collaterals is a potential independent risk factor for preoperative hemorrhage in MMD patients. A perfusion territory shift fed by the primary collaterals may not have a strong effect on preoperative hemorrhage in MMD patients. These findings make the combined modalities of t-ASL and 3D-TOF-MRA a feasible tool for MMD disease assessment, management, and surgical strategy planning.

ABBREVIATIONS ACA = anterior cerebral artery; ASL = arterial spin labeling; CBF = cerebral blood flow; CTP = CT perfusion; ECA = external carotid artery; ICA = internal carotid artery; MCA = middle cerebral artery; MMD = moyamoya disease; MRP = MRI perfusion; PCASL = pseudocontinuous ASL; SS-PCASL = superselective PCASL; t-ASL = territorial ASL; VA = vertebral artery; VE-PCASL vessel-encoded PCASL; 3D-TOF-MRA = 3D time-of-flight MRA.

Article Information

Correspondence Zhen-Wei Yao: Huashan Hospital, Fudan University, Shanghai, China. zwyao@fudan.edu.cn.

INCLUDE WHEN CITING Published online August 9, 2019; DOI: 10.3171/2019.5.JNS19803.

X.Y.G., Q.L., and J.R.L. contributed equally to this work.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Flowchart of this study.

  • View in gallery

    t-ASL maps of a 45-year-old man with MMD (left hemisphere, Suzuki stage 4; right hemisphere, Suzuki stage 4). Right ICA labeled images (A–C) showed the following: 1) CBF being shifted from the right carotid artery to the left ACA territory; 2) CBF shifting from the right anterior circulation to the right posterior circulation. Bilateral VA labeled images (D and E) showing CBF being shifted from the posterior circulation to the anterior circulation. Left internal carotid artery labeled image (F) showing CBF being shifted from the left anterior circulation to the left posterior circulation. Figure is available in color online only.

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    Images obtained in a 27-year-old man with MMD (left hemisphere, Suzuki stage 5; right hemisphere, Suzuki stage 1). A and B: Right ICA labeled images showing CBF being shifted from the right carotid artery to the left ACA territory as well as the left MCA territory. Figure is available in color online only.

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    Images obtained in a 47-year-old man with MMD (left hemisphere, Suzuki stage 5; right hemisphere, Suzuki stage 4). A and B: Bilateral VA labeled images showing CBF being shifted from the posterior circulation to the anterior circulation. Figure is available in color online only.

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    Images obtained in a 41-year-old woman with MMD (left hemisphere, Suzuki stage 1; right hemisphere, Suzuki stage 5). A: 3D-TOF-MRA image demonstrating the branches of right ECA (arrow) inside brain. B: t-ASL map (ECA labeled) showing the blood supply from the right ECA inside the brain (arrow). Figure is available in color online only.

  • View in gallery

    Representative imaging examples from a patient in group A. A 20-year-old woman with MMD (left hemisphere, Suzuki stage 4; right hemisphere, Suzuki stage 1). A: 3D-TOF-MRA image showing the anterior communicating artery (arrow). B: Preoperative DSA image showing the anterior communicating artery (arrow). C and D: t-ASL maps (right ICA labeled) showing blood being shunted from the right ICA to the left ACA and left MCA territories. Figure is available in color online only.

  • View in gallery

    Representative imaging examples from a patient in group B. A 35-year-old woman with MMD (left hemisphere, Suzuki stage 2; right hemisphere, Suzuki stage 3) presented with preoperative hemorrhage. A: DSA echoed the absence of the posterior communicating artery. B: MRA demonstrating the absence of the posterior communicating artery. C and D: t-ASL map (VA labeled) showed blood being shunted from the posterior circulation to the anterior circulation. Figure is available in color online only.

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