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Adult Moyamoya Syndromes: Update on Diagnosis and Treatment

Article  in  Practical Neurology · September 2009

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Adult Moyamoya Syndromes:
Update on Diagnosis and Treatment
Aggressive interventions are indicated for this condition,
which is associated with significant morbidity.
By David A. Decker, MD and Reza Behrouz, DO
M
oyamoya, also known as Spontaneous
Occlusion of the Circle of Willis, is an
uncommon cerebral vasculopathy. It is
associated with progressive occlusion of
the terminal internal carotid arteries and the for-
mation of a fine network of neovascularization
referred to as moyamoya vessels. The disorder
takes its name from the Japanese word for the
angiographic appearance, which resembles a waft-
ing puff of smoke. This condition was first
described in 1957 in Japanese children.1 The Asian
form of moyamoya disease is an idiopathic condi-
tion with a well defined phenotype that occurs
predominately in children of Japanese ancestry.
However, a clinically distinct and less well
described secondary form of moyamoya occurs in
adults of all ethnic backgrounds and is termed
moyamoya syndrome. While relatively rare, this
condition is potentially treatable and, with increas-
ing awareness, will likely be discovered more fre-
quently.
Adult moyamoya syndrome is strongly associat-
ed with cranial radiation exposure, typically occur-
ring two or more years after treatment.2,3 Several
genetic diseases have been reported as risk factors,
including Down syndrome,4 sickle cell disease,5,6
and neurofibromatosis type 1.7-9 Severe intracranial
atheromatous disease may also lead to the forma-
tion of moyamoya vessels.10,11 In addition, fibro-
muscular dysplasia,12,13 hyperthyroidism,14 bacterial
meningitis,15 combined cigarette smoking and oral
contraceptive use,16 Sjogren syndrome,16,17 and
cocaine abuse18-20 have all been implicated.
Vascular Clinic
Diagnosis and Management
Diagnosis of moyamoya requires the presence of
the characteristic angiographic findings. The termi-
nal internal carotid arteries initially demonstrate
narrowed lumens that progress to complete occlu-
sion in later stages. The occlusive disease is almost
always bilateral but may be asymmetric and
spread to involve the anterior or middle cerebral
and posterior communicating arteries.21 In
response to the reduced blood flow, innumerable
tiny penetrating vessels sprout from the affected
vessels and act as collateral channels. Branches of
the external carotid may also be recruited for col-
lateral circulation. A grading system illustrating
the six stages devised by Suzuki and Takaku is
shown in Table 1.22
This compensatory vascular network, however,
is fragile and ultimately unable to sustain the
ischemic tissue. The friable moyamoya vessels may
rupture leading to hemorrhage. Hemodynamic
changes that increase flow through collateral ves-
sels may lead to the formation of aneurysms, most
Table 1 - Suzuki Stages of Moyamoya Disease 22
Suzuki Stage Angiographic Finding
I Narrowing of carotid arteries
II Initial appearance of moyamoya vessels
III Intensification of moyamoya vessels
IV Minimization of moyamoya vessels
V Reduction of moyamoya vessels
VI Disappearance of moyamoya vessels
September 2009 | Practical Neurology | 17
 Vascular Clinic
Figure 1. Progression of moyamoya: (A) Normal intracranial
internal carotid artery (ICA). (B) Progressive steno-occlusion
of the ICA terminus with development of small-caliber collat-
erals. (C) Complete occlusion of the intracranial ICA with
organization and increase in number of fragile (moyamoya)
collaterals, giving the typical “puff of smoke” appearance on
the cerebral angiogram (D). (E) Progressive degeneration of
moyamoya collateral arteries. (F) Disappearance of moyamoya
arteries with development of extracranial collateralization.
(Artwork by Reza Behrouz, DO)
commonly in the posterior circulation.21 The vascu-
lar territories supplied by the neovasculature are
chronically oligemic, which often leads to ischemic
infarction.
The typical clinical presentation in the United
States is a young woman with either recurrent
ischemic or hemorrhagic events, which may coex-
ist in the same patient. The adult syndrome occurs
in women two to four times more often than in
men and has a peak incidence between 30 and 50
years of age.23,24 Ischemic stroke in the vulnerable
territory occurs in approximately three-quarters of
patients. Approximately one quarter of patients
present with hemorrhage, yet a small number of
patients are asymptomatic at the time angiographic
findings are incidentally discovered.
18 | Practical Neurology | September 2009
While the natural history of this syndrome is
largely unknown and likely dependent in part on
the associated underlying condition, the risk of
recurrent events is high: as high as 65 percent in
those treated conservatively.23 In contrast, the rate
of progression in surgically treated patients is sub-
stantially lower at 2.6 percent, as estimated by a
meta-analysis of 1,156 patients.25 Revascularization
may be accomplished surgically through direct or
indirect techniques.26
In the majority of direct revascularization proce-
dures, the superficial temporal artery is anasto-
mosed to the middle cerebral artery or another
large intracranial artery. When the diameter of the
STA is too small for direct anastomosis, the occipi-
tal artery can be considered as a donor artery.27
The result is immediate restoration of blood flow
with a high rate of long-term patency26,28 and nor-
malization of cerebral hemodynamics.29 But the
procedure is not without significant complications.
Perioperative ischemia may occur due to clamping
of the recipient artery during anastomosis, and one
recent study of adult moyamoya patients found the
perioperative morbidity and mortality was 12.3
percent and 4.6 percent, respectively.29 The imme-
diate increase in cerebral blood flow also places
the patient at risk for symptomatic hyperperfusion
and transient neurologic deterioration.30,31
Indirect techniques involve a wide craniotomy
and placement of a vascularized tissue supplied by
the external carotid in direct contact with the cor-
tical surface. Collateral vessels then sprout from
the graft. These techniques are less invasive, do
not require clamping of a recipient vessel, and are
technically simpler. A number of indirect proce-
dures have been described.
Encephalomyosynangiosis (EMS), first described
in 1977,32 involves placing a section of temporalis
muscle directly over the underlying cerebral cortex
after the arachnoid layer has been removed.
Encephaloduroarteriosynangiosis (EDAS),
described in 1980,33 entails suturing a galeal cuff
with an intact STA onto the cortical surface once
the dura has been removed. These procedures or
other variations may be used singly or in combina-
 Vascular Clinic

tion and are tailored to the patient’s anatomy. The

Images courtesy of James E. Lefler, MD, Tampa General Hospital Department of Radiology
main disadvantage of indirect techniques is the
extended time period required for neovasculariza-
tion to occur, which is usually several months.34
While indirect techniques have been shown supe-
rior in the pediatric population,26 the success rate
in adults is significantly less. In 40-50 percent of
adults receiving indirect revascularization, collater-
al vessels fail to grow.26,35

Aggressive Intervention Warranted

It is important to note that the majority of Figure 2. A CT angiogram from a 49-year-old woman present-
research published on the treatment of moyamoya ing with intraventricular hemorrhage demonstrating Suzuki
in adults relates to the Asian form (moyamoya dis- Stage II moyamoya syndrome. The right internal carotid artery
ease) and not the secondary moyamoya syndromes is nearly occluded. The anterior and middle cerebral arteries
more commonly encountered in the United States. demonstrate moyamoya vessels.
One fact, however, is indisputable: moyamoya syn-
drome and disease are associated with consider-
able morbidity. Aggressive treatment appears to
yield the best outcomes. ■
David A. Decker, M.D. is Assistant Professor of
Neurology at the University of South Florida College
of Medicine and an Attending Physician in the
Neurosciences Intensive Care Unit at Tampa General
Hospital. He can be reached at
ddecker@health.usf.edu.
Figure 3. A CT perfusion study from the same patient in Figure 2
Reza Behrouz, D.O. is Assistant Professor of demonstrating impaired perfusion in the right hemisphere.
Neurology & Internal Medicine at the University of
South Florida College of Medicine and Co-Director of
the Neurosciences Intensive Care Unit at Tampa
General Hospital.
The authors report no conflict of interest.
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20 | Practical Neurology | September 2009

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