Elsevier

Pediatric Neurology

Volume 52, Issue 1, January 2015, Pages 65-72
Pediatric Neurology

Original Article
Patterns of Cerebral Ischemia in Children With Moyamoya

https://doi.org/10.1016/j.pediatrneurol.2014.10.007Get rights and content

Abstract

Background

Moyamoya disease is characterized by progressive cerebrovascular stenosis with recurrent cerebral ischemic events. Transient ischemic attacks are often associated with hyperventilation in children with moyamoya, suggesting hypoperfusion rather than thrombotic vaso-occlusion as a prominent mechanism. The patterns of ischemia and severity of steno-occlusive disease in such children may elucidate these mechanisms.

Methods

Children, 1 month to 18 years, with moyamoya, observed over 11 years were analyzed. A study neuroradiologist reviewed all presurgical neuroimaging. Ischemic injury was categorized into cortical, subcortical, and watershed infarction. Angiographic findings were staged using a standardized method.

Results

Twenty children, 15 girls, median age 6.4 years, were included. All children had magnetic resonance imaging and angiography, and in 16, conventional angiography was available. All 40 hemispheres, in 20 children, were evaluated. The initial clinical presentation included neurological deficits in 17, recurrent transient ischemic attacks in 7, headache in 8, seizures in 8, and alteration in consciousness in 4 children. Infarcts were bilateral in 13 (65%) children (ischemia alone in 14, ischemic stroke with hemorrhagic transformation in two, and primary hemorrhage in two). Infarcts were cortical and/or subcortical in 13 (65%), both deep and cortical watershed in 11 (55%), and cortical watershed alone in 5 (25%) children. The predominant vascular territory involved was the middle cerebral artery. The internal carotid arterial system was involved in all, with stage IV being the most frequent angiographic stage.

Conclusions

Ischemic injury in deep watershed zones is common in childhood moyamoya and may reflect non–vaso-occlusive ischemic mechanisms. Location and severity of vascular involvement may correlate with various patterns of ischemic infarction in moyamoya disease and requires further study.

Introduction

Moyamoya disease, common in Asian countries, is a rare progressive steno-occlusive cerebrovascular disorder of unknown etiology. It is characterized by stenosis and occlusion of the arteries of circle of Willis, with abnormal telangiectatic collateral circulation at the base of the brain. Moyamoya is categorized as moyamoya disease when there is no underlying etiology or association and as moyamoya syndrome if an underlying etiology or association is recognized.1, 2 Childhood moyamoya typically presents with recurrent bilateral ischemic events, often transient ischemic attacks (TIAs), in association with hyperventilation suggesting brain hypoperfusion as the likely mechanism in the already compromised stenotic and occluded vessels and newly formed telangiectatic collateral circulation. The clinical presentation is variable, with either focal neurological deficits (often transient) or nonspecific symptoms such as lethargy, headache, and vomiting, depending on the areas of ischemic involvement and severity of the steno-occlusive disease.1, 2, 3, 4, 5, 6, 7 The need for revascularization surgery in children with moyamoya is dependent on the extent and type of ischemic infarction (bilateral and multiple strokes), the presence of advanced vascular stage and poor cerebrovascular reserve (as indicated by the ivy sign on magnetic resonance imaging [MRI] brain fluid attenuated inversion recovery and contrast-enhanced T1-weighted sequences),8, 9 and cerebrovascular reserve mapping studies including single-photon emission computerized tomography and perfusion scans10, 11 and progression of the disease.12, 13, 14 In the Japanese population, where the moyamoya disease is prevalent, data regarding the severity of the disease have been well studied. However, the literature is limited regarding the patterns of cerebral ischemia in childhood moyamoya, particularly in the non-Japanese population. One recent study in a Korean cohort of patients with moyamoya studied the pattern of ischemic infarction based on diffusion-weighted neuroimaging. They compared the acute diffusion-weighted neuroimaging of 34 adult patients with moyamoya to 32 childhood moyamoya patients when they presented with acute stroke signs. They found that among all patterns of infarction, a gyral pattern was the most common (44%) and cortical border zone and deep lacunar patterns were infrequent, and among children with moyamoya, cortical and border zone patterns were more frequently observed, whereas a honeycomb pattern was common in adult patients and with advanced vascular stages.15 In their study, the border zone pattern only included the typical cortical watershed border zone that is present between two major cerebral arteries, and the honeycomb pattern was the patchy cortical and subcortical infarction. In addition, the study did not assess the patterns of infarction over a longitudinal period or the patterns of chronic or remote infarction using other neuroimaging sequences.15 We therefore sought to determine patterns of cerebral ischemic infarction in a non-Japanese population of children with moyamoya.

Section snippets

Study design

We retrospectively reviewed the records of a prospectively ascertained consecutive cohort of children, 1 month to 18 years, with both moyamoya disease and moyamoya syndrome, observed at the two Canadian Pediatric Ischemic Stroke Registry affiliated centers, The Hospital for Sick Children and the McMaster University Medical Centre. The study period was from January 1992 to June 2006. The study was approved by the institution's research ethics board.

Aims of the study

The primary aim of the study was to review the

Demographics

We identified 23 children, without sickle cell hemoglobinopathy, with a diagnosis of either moyamoya disease or syndrome. Three patients with unavailable radiology films were excluded from the analysis. Of the remaining 20 children, there were five boys and 15 girls, with median age 6.4 years (range, 2 months to 15.5 years).

Clinical presentation

The initial clinical presentation included persistent focal neurological deficits in 17, history consistent with preceding TIAs in seven, headache in eight, focal seizures

Discussion

The etiologic mechanisms and associations of moyamoya disease is extensively described and studied in the medical literature.1, 21, 22 There are scarce data with regards to patterns of ischemic injury in patients with this unique disorder. In addition, both embolic and hemodynamic factors have been implicated as the underlying mechanism of ischemia. Our study is the first to assess the patterns of both acute and chronic ischemic infarction in a North American cohort of children with moyamoya.

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