Arterial wall contrast enhancement in progressive moyamoya disease

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OBJECTIVE

The purpose of this study was to evaluate chronological patterns of arterial wall contrast enhancement in contrast-enhanced high-resolution MRI (CE-HR-MRI) in patients with moyamoya disease (MMD).

METHODS

The authors performed a blinded analysis of clinical and imaging data from MMD patients. Data were analyzed chronologically for each patient and the intensity of arterial wall enhancement was correlated with the clinical and imaging-based progression status of the disease.

RESULTS

A total of 31 MMD patients and 61 imaging time points were included. CE-HR-MRI results were available for 56 time points, representing 112 hemispheric analyses. No arterial wall contrast enhancement (grade 1) was seen in 54 (48%) of the analyses, mild enhancement (grade 2) in 24 (21%), moderate enhancement (grade 3) in 15 (13%), and strong (grade 4) mainly concentric arterial wall contrast enhancement in 19 (17%). Grade 4 contrast enhancement was significantly (p < 0.001) associated with clinical disease progression within 6 months (before or after the MRI) compared to grades 1–3, with positive and negative predictive values of 0.8 and 0.88, respectively. Grades 1 and 2 (no contrast enhancement and only mild contrast enhancement) were highly predictive for stable disease (negative predictive value: 0.95).

CONCLUSIONS

A specific chronological increasing and decreasing pattern of arterial wall contrast enhancement associated with “beginning” as well as progression of angiopathy occurs in MMD patients. In clinical practice, CE-HR-MRI of the arterial wall may help to identify patients at risk of new strokes caused by disease progression and hence impel early treatment for future stroke prevention. Understanding of this temporary enhancement of the arterial wall might also bring new insights into the etiology of MMD.

ABBREVIATIONS ACA = anterior cerebral artery; ACoA = anterior communicating artery; CE-HR-MRI = contrast-enhanced high-resolution MRI; DSA = digital subtraction angiography; ICA = internal carotid artery; MCA = middle cerebral artery; MMD = moyamoya disease; RI = remodeling index; TIA = transient ischemic attack.

Article Information

Correspondence Nadia Khan: Center for Moyamoya and Cerebral Revascularization, Tübingen, Germany, and Moyamoya Center, Children’s Hospital, University of Zürich, Switzerland. moyamoya@neurochirurgie-tuebingen.de.

INCLUDE WHEN CITING Published online May 24, 2019; DOI: 10.3171/2019.2.JNS19106.

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 showing how patients and time points were selected.

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    Time points of imaging in relation to contrast enhancement and symptoms. Diagrams showing time points of imaging in months in relation to the first symptoms for the respective hemisphere (zero line) (x-axis) and MR vessel wall contrast enhancement (y-axis) (grades 1–4; see Table 1). Colors are specific for respective hemispheres in the respective patients. Panel A shows time points of all hemispheres of patients who had specific hemispheric symptoms at any time. Panel B only shows time points for patients/hemispheres examined with CE-HR-MRI at least twice, with a finding of strong contrast enhancement (grade 4) on at least one of the studies. In panel B, time points of individuals are connected with a line to depict the chronologically increasing and decreasing pattern of contrast enhancement. Figure is available in color online only.

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    Box plot of intervals between symptoms and intensity of contrast enhancement. The x-axis indicates grade of contrast enhancement (see Table 1). The values on the y-axis represent time between contrast enhancement and onset of symptoms after transformation to absolute values, with t = 0 defined by the first onset of symptoms for the respective hemisphere. (“Negative” time points, i.e., for imaging performed before symptom onset, were converted to positive values to facilitate statistical analysis.) Data are shown for 8, 13, 12, and 17 hemispheres with new symptoms of grade 1, 2, 3, and 4, respectively. Kruskal-Wallis testing showed a statistically significant difference (p < 0.005) between medians.

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    Representative case of increasing and decreasing contrast enhancement of the terminal ICA in correlation to angiography. This female patient initially presented at the age of 45 years with symptomatic MMD of the left hemisphere and was treated successfully with extracranial-intracranial (EC-IC) revascularization. Shown are angiograms and corresponding CE-HR-MR images obtained at the initial evaluation (A, 0 months) and 14 (B), 24 (C), and 38 (D) months later. The initial imaging of the right, not relevantly affected hemisphere, showed only minimal stenosis of the terminal ICA (A, black-outline arrow) with only weak concentric (grade 2) contrast enhancement (A, white-outline arrow). At 14 months’ follow-up angiography showed a progressive stenosis (B, black-outline arrow) and CE-HR-MRI showed an increase in concentric contrast enhancement to grade 3 (B, white-outline arrow). After a total of 24 months, the right hemisphere became symptomatic with new diffuse infarctions (not shown) caused by significantly progressive stenosis of the carotid T (C, black-outline arrow) with a strong (grade 4) concentric contrast enhancement of the vessel wall (C, white-outline arrow). The patient was then treated with EC-IC revascularization for the right side as well. After a total of 38 months the carotid T was occluded (D, black-outline arrow) and contrast enhancement (D, white-outline arrow) was no longer seen in the vessel wall.

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    Representative case of decreasing contrast enhancement of the MCA in correlation to angiography. This female patient initially presented at the age of 33 years with symptomatic unilateral right-sided moyamoya angiopathy with a newly symptomatic M1 stenosis. The concentric strong contrast enhancement (grade 4) of the vessel wall (A) corresponds precisely to the angiographic stenosis (B). The patient was then treated with direct EC-IC revascularization. The 13-month follow-up CE-HR-MRI study (C) showed a significant decrease in contrast enhancement (to an eccentric mild [grade 2] enhancement) while angiography showed progressive stenosis with new surrounding collaterals (D).

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