J.Neurol.Sci.

[Turk]

Journal of Neurological Sciences [Turkish] 30:(1)# 34; 048-058, 2013

http://www.jns.dergisi.org/text.php3?id=645
Research Article

Clinical Features and Treatment Outcomes of Moyamoya Disease in 125 Patients of

Henan, China
Hong-Wei CUI, Yan-Ru LIU, Bo-Ai ZHANG
The First Affiliated Hospital of Zhengzhou University, Nöroloji, Zhengzhou, Çin
Summary
Objective: We aim to describe clinical features and treatment outcomes of patients with
Moyamoya disease (MMD) at a single center in China.
Methods: Clinical features of a total of 125 cases of MMD from Henan, a provincial capital
in China, were retrospectively analyzed. Follow-up studies were performed through telephone
or regular visits, and recurrent stroke risk was assessed by Kaplan-Meier analysis.
Results: The average age at onset of symptoms was 31.6 (range, 0.8-74) years, with the
female predominance (1.72:1). There is a bimodal age of onset. The initial symptoms
included ischemia (64%), hemorrhage (20%) and others (16%). 100 patients received
conservative management. The remaining 25 patients received surgical revascularization. The
median follow-up period was 28.8 (range, 1-192) months. 13 patients were withdrawn.
During the follow-up period, 7 of 25 patients experienced a second episode of bleeding with a
third in 1patient, none of which underwent revascularization. The mortality of rebleeding was
28.6% (2/7). Cerebral infarction appeared in 14 of 74 ischemic cases after the initial
symptom, with 2 patients dying of large area acute cerebral infarction. 2 of 25 cases who
underwent surgical revascularization had ischemic events within 30-day, and another 2
patients died resulting from recurrent infarction caused by surgery. The 5-year risk of
recurrent stroke was 42% after the initial symptom for all patients with conservative
treatment.
Conclusion: In the drug-treated group, there was a higher recurrent rate of stroke. These data
suggest no potential benefit from surgery in the short term, however, long-time outcome
requires a further investigation.
Key words: Moyamoya disease, Clinical features, Outcome, Kaplan-Meier

Çin'in Henan Eyaletindeki 125 Moyamoya Hastası Üzerinde Yapılan Klinik Özellik
Analizi ve Prognoz Takibi

Özet
Amaç: Çin’deki tek bir merkezdeki Moyamoya hastalığı klinik analizini ve farklı olan tedavi
yöntem prognozunu açıklamaktır.
Yöntemler: Çin Henan eyaletindeki Moyamoya hastalığı olan 125 hasta üzerinde klinik
özeliklerinin retrospektif olarak analizi yapıldı. Telefonla veya hastaları düzenli takip ederek
prognostik verileri toplandı. Hastalarda yineleyen inme riski değerlendirilmesi için Kaplan-
Meier analiz yöntemi kullanıldı.
Bulgular: Erkek ve Kadın hastaların oranı 1:1,72, hastalığın başlangıç ortalama yaşı 31,6
(0,8-74) olarak bulundu. Yaş dağılımında iki önemli zirve bulunmaktadır. İlk dönemde
görülen klinik semptomlar iskemi (%64), kanama (%20) ve diğerlerini (%16) içerir. Medikal
tedavi alan 100 hastadan sadece 25 hasta için cerrahi revaskülarizasyon tedavisi uygulandı.

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Yüzoniki hastanın uzun süreli takip edilmesi sağlandı ve ortalama takip zamanı 28,8 (1-192)
ay oldu. Kanaması olan 25 hastanın 7’sinde ikinci bir kanama görüldü; bunlardan bir olguda
üçüncü kez kanama görüldü, Tüm 7 hasta için konservatif tedavi yapıldı. İlk semptomu
iskemik olay olan hastalar arasındaki toplam 74 hasta üzerinde takip tam olup, bunların içinde
bulunan 14 hastada beyin infarktüsü görüldü; 2 hasta geniş alanda infarkt nedeniyle öldü.
Cerrahi revaskülarizasyon 25 hasta için yapıldı, Bunların içinde 2 hastada ameliyattan sonra
30 gün içinde reinfarktüs görüldü; diğer 2 hasta ameliyattan sonra infarktüs nedeniyle öldü.
İlaç tedavisi alan hastalarda 5 yıllık Kaplan-Meier inme tekrarlama riski olanlar ise yaklaşık
%42,0 olarak saptandı.
Sonuç: Medikal tedavide daha yüksek bir inme tekrarlama oranı olacağı için, cerrahi
revaskülarizasyon ameliyatında kısa vadeli kazanç olmayacaktır. Bu nedenle ameliyatın
tedavi etkinliğini değerlendirmek için daha uzun süreli bir takip gerektirmektedir.
Anahtar Kelimeler: Moyamoya hastalığı, klinik özellikler, prognoz, Kaplan-Meier

MATERIAL AND METHODS

INTRODUCTION
Moyamoya disease (MMD) is a rare 1 Patient Selection
chronic cerebrovascular disease with We identified 125 patients with bilateral or
unknown etiology characterized by unilateral MMD between January 2006 and
progressive stenosis of bilateral internal December 2011 at the First Affiliated
carotid arteries and their proximal branches Hospital of Zhengzhou University, Henan,
along with development of a collateral China. All the patients were diagnosed by
network of small vessels from pial arteries digital subtraction angiography (DSA)
and perforating artery at the base of the and/or magnetic resonance angiography
brain(22). The name "moyamoya" was (MRA) or magnetic resonance imaging
originally described by Suzuki and Takaku (MRI). The criteria for diagnosis of MMD
in Japan because of the characteristic was according to the guidelines set by the
appearance of abnormal fine vascular Research Committee on Moyamoya
network on angiography, like a puff of Disease (Spontaneous Occlusion of the
cigarette smoke(23). Circle of Willis)(5,6). Written informed
consent was obtained from each subject.
Since MMD was first reported in 1957 by
The patients were divided into the
Takeuchi and Shimizu(27), it has been
operation and drug treatment group.
increasingly reported throughout the world
in people of many ethnic backgrounds. 2 Method
Over the past few decades, many studies Clinical features, laboratory examinations,
have documented the epidemiological and and radiological studies were reviewed
clinical characteristics of the
(8,9,10,12,13) retrospectively. The follow-up data were
disease . These studies have obtained by a telephone interview or
indicated there is a higher prevalence in
clinical visits (Tab. 1). In living patients
Asians, especially in Japan, Korea and diagnosed with MMD <1 year before data
China. However, reviewing the literature, collection, the data were obtained from
we should realize that there is only very
recent clinical visits. In living patients
rare data about clinical features and long-
diagnosed >1 year before data collection,
time natural history of MMD in mainland
we obtained long-term follow-up data
China to date. Therefore, we aimed to through a telephone interview or clinical
describe the detailed clinical features and visits. Kaplan-Meier analysis was
long-time outcome of MMD in the present performed to determine the risk of
study. recurrent stroke of the different groups. In

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addition, the patients with surgery before statistical significance for differences
surgical intervention was considered to between proportions was assessed using χ2,
receive drug treatment. when appropriate. Student's t-test was used
for continuous data. A p value <0.05 was
3 Statistical method
considered to have statistical significance.
Statistical Package for the Social Sciences Kaplan-Meier methods were used to
(SPSS15.0) for Windows was used for estimate stroke recurrence risk.
statistical analysis. For univariate analyses,

Table 1. Diagram of patients with moyamoya disease included in present study.

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1). In men, there was a significantly higher

RESULTS
peak among patients aged 5-9 years,
1 General features however, for females, the biggest peak was
There were 46 men and 79 women with a seen in patients aged 40-44 years,
significant gender difference (Tab. 2). The suggesting the peak of the incidence varies
female-to-male ratio was significantly according to the gender.
higher other series in mainland China(3,18),
however, the result is similar to the study
reported from Japan and South Korea(8,12) ,
indicating that there is a women
predominance in sex distribution of MMD
in China. The age at onset of presentation
ranged from 0.8 to 74 years with a mean of
31.6 years. A bimodal age distribution has
been demonstrated in Asia, with children
primarily suffering from ischemic
symptoms and adults experiencing
intracranial hemorrhage(5,9,11,19). Our study
also revealed a bimodal age distribution
with the largest peak at age 5-9 years and a
second smaller peak at 40-44 years (Fig.

Tab 2: Comparison of moyamoya disease between the current study, Taiwan, and other series
in mainland China.

Clinical Features The research of our Duan et al Wei et al Hung et al (Tai

group(China ) (China) (China) Wan)
Female to male 1.72:1 1:1 1.15:1 1.3:1
Distribution of age Two-Peak Two-Peak Two-Peak One-peak
Age peak in child 5-9 5-9 5-9 Nil
Age peak in adult 40-44 35-39 35-39 31-40
Family history 0% 5.2% 1.48% Unmentioned
Hemorrhagic stroke 83.3% 95.6% 62% Unmentioned
in Patients with
≥10 years old
Patients < 10 years 20.8% 26.9% 8.47% 18.4%
old
Asymptomatic 0.8% 1.1% 3.3% Unmentioned
Unilateral lesion 4.8% 10.8% Unmentioned Unmentioned

posterior cerebral 12.0% 31.4% Unmentioned Unmentioned

artery
involved(stenosis or
occlusion)

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Fig 1: Bimodal pattern of age distribution in male and female patients.

2 Disease Type difference (P=0.012) in the percentage of

patients between ischemic group and
The initial symptoms include ischemia,
bleeding group (> 10 years old) was
hemorrhage, and others. The percentage of
significant. Headache as another frequent
ischemia was significantly higher than that
presenting symptom occurred in our 12
of haemorrhage (P < 0.01), and most of the
patients (9.6%), and the history of
affected adults and children presented with
headache was more frequently seen in
ischemic symptom onset in our cohort
hemorrhagic MMD patients (p=0.013,
(Fig. 2). Infarction was the most common
compared with the ischemic group),
initial clinical manifestation (41.6%),
suggesting the patient with a history of
transient ischemic attack (22.4%) was
headache is more likely to suffer from
second. Intraventricular hemorrhage (IVH)
hemorrhagic MMD. Furthermore, there
with or without intracerebral hemorrhage
was a significant difference (Tab. 3) in the
(ICH) was a dominant finding on
age between the two groups with an earlier
computerized tomography scans during the
age at onset in the ischemic group.
first bleeding episode in 25 cases (20%), 9
Unexpectedly, we observed choreiform
and 5 cases, respectively. Simple ICH was
revealed on CT scans in 5 cases (4%) and movements in 3 cases, which was rarely
subarachnoid hemorrhage in 5 cases reported in the literature to the best of our
(4.8%). In the 10 patients who suffered knowledge. It is thought that dilated
from ICH with or without IVH, the basal moyamoya-associated collateral vessels in
ganglia (6 cases) and the thalamus (2 the basal ganglia have also been implicated
cases) were the main sites of distribution. in the development of choreiform
And the other two in temporal lobe. One movements(22). Other symptoms included
patient presented with infarction firstly, dizziness in 2 patients, epilepsy in 1
then he suffered haemorrhaging in 3 and patients. Just one patient was
20 years after the initial symptom, which is asymptomatic in our series, being lower
quite infrequent with literature review(14). than document reports (Tab. 2).
ICH as an initial manifestation mostly 3 Supplemental studies
occurred in the 20-40 years old, which was Although MMD has long been considered
not in accordance with reports from Japan as a disease involving the anterior
and other groups in China, where circulation only, there were steno-
hemorrhage was seen mostly in patients in occlusive changes of the PCA in 15
the third and fourth decades. The statistical

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patients (12%) in our cohort. We also patient. 1 of 7 patients suffered from a

identified 6 unilateral MMD patients. The third episode of bleeding within one and a
antinuclear antibody test is positive in 11 half months from the second bleeding
cases with the weakly positive in 8 episode. All of 3 patients who underwent
patients. The positive anticardiolipin indirect bypass surgery after the first
antibody has been detected in the sera of 5 bleeding episode suffered no rebleeding
patients with MMD. Thyroid dysfunction during the follow-up period. 2 cases of
occurred in 4 female patients, with 3 cases hemorrhagic MMD with conservative
of hypothyroidism and 1 case of treatment died of the second bleeding
hyperthyroidism respectively. 2 patients episode and the third bleeding episode,
with hypothyroidism were complicated by respectively. During follow-up, infarction
Graves' disease and positive anticardiolipin took place in 14 patients from ischemic
antibody. Besides, 1 patient presented with group after the first ischemic events with 2
hyperthyroidism concurrent with Graves' patients dying of large area acute cerebral
disease and type 2 diabetes mellitus. These infarction. The median time to recurrent
findings show autoimmunity may play an infarction was 40.4 ( rang, 1-120 ) months.
especially significant role in the process of In 25 patients who received surgical
MMD. In our present study, we procedures at the last, the symptoms at
uncommonly identified 2 cases of MMD onset included ischemia in 19 patients,
with congenital anomalies, manifesting as haemorrhage in 3 patients and involuntary
cleft lip, bicuspid aortic valve and mitral movements in 1 patient, which was
deformity. significantly improved after surgery. 2
patients who received surgical procedures
4 Follow-Up
experienced a second episode of infarction
100 patients had been treated within the first 30 days after surgery; after
conservatively. The remaining 25 patients the first year, one of the two patients
received surgical revascularization suffered a third episode of infarction. The
procedures according to patients' requires, mortality of surgery is 8% resulting from
all of which underwent indirect bypass complicated infarction in our study. The
using EDAS and/or burr holes for the Kaplan-Meier estimate of recurrent stroke
treatment. The mean time during the risk after the first ischemic event was 17%
interval between diagnosis and surgical (95% CI, 16.5%-17.5%) in the first two
intervention was 2.2 months, ranging from year for the patients with conservative
0.5 to 12 months. 13 patients could not be treatment. The 5-year-Kaplan-Meier risk of
contacted by phone for data collection. The recurrent stroke was 42% (95% CI, 40.9%-
follow-up period averaged 28.8 (rang, 1- 42.1%) after the first ischemic event for
192) months in all patients. The average medically treated patients. As the period of
time of follow up were 14.2 months in the disease getting longer, the risk of
surgical patients and 30.2 months in recurrent stroke was increasing gradually
patients with medical treatment, (Fig. 3). In surgically treated patients, the
respectively. During the follow-up period, Kaplan-Meier risk for stroke after the first
7of 25 patients with hemorrhagic MMD stroke event was slightly more higher than
experienced a second episode of bleeding, that of the drug treatment group within two
which occurred 7 years or longer after the years. Because surgical revascularization
original hemorrhage in 4 cases ( 57.2%) or procedures were often performed on
within half a year after the first bleeding patients with a rather long history, long-
episode in 3 cases (42.8%). IVH was the term outcome of surgery remains to be
dominant types of rebleeding in 6 cases further studied.
(85.7%). ICH occurred in the other one

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Fig 2: Moyamoya disease pattern at onset by age distribution.

Table 3. Clinical features of 125 patients with Moyamoya disease. * Statistically significant
difference. SD = standard deviation.

Gender Age History of Cognitive Patients >

Clinical (male/female (years, mean headache deficits 10 years old
features ) ± SD)

Ischemia 31/49 28.2±19.4 23（ 28.6%） 34（ 42.5%） 57（ 71.3%）

Hemorrhage 9/16 36.6±12.7 14（ 56.0%） 8（ 32.0%） 24（ 96.0%）

P value 0.805 * 0.016 * 0.013 0.350 * 0.012

Fig 3: Kaplan-Meier plot for

recurrent stroke risk for patients
treated with surgical
revascularization or conservative
treatment.

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DISCUSSION et al, where the patients have much higher

rates of hemorrhage as a presenting
To the best of our knowledge, there were
symptom (56%). Hemorrhage as the
only two papers concerning the clinical
primary symptom mostly occurred in the
characteristic of MMD in mainland China,
20-40th decades. IVH with or without ICH
however, contradictory results were
was the most common type during the first
extremely confusing(3,18). Therefore, we
bleeding episode, and the incidence rate of
present data from a cohort of 125 Chinese
IVH was up to 85.7%. Previous studies
patients with idiopathic MMD with details
have indicated that IVH, associated with
about clinical manifestation, and long-term
excessive dilation and abnormal branching
natural history.
of the anterior choroidal artery, was the
There is a higher known prevalence of predominant subtype of hemorrhagic
MMD in Asian populations(5,9,11,19). lesions in adult MMD(20,27). Under
However, epidemiological features of enhanced hemodynamic stress, the
MMD in China are largely unknown. In exceedingly dilated and fragile branches of
the present study, be short of accurate the anterior choroidal or posterior
demographic data and limited to a single communicating artery may rupture and
center, we failed to gain epidemiological result in IVH, which most likely explains
features of MMD in Henan, China. the situation(22).
Recently, an epidemiological study in the
area of Nanjing, showed the prevalence at To date, the pathogenesis of moyamoya
3.92/100 000, which was lower than the disease remains unknown. It has been
prevalence of 6.03/100 000 in Japan(12,18). suggested that in some Japanese families
MMD may be transmitted through a
One of the well-known specific features of polygenic or autosomal dominant mode
MMD is bimodal age of onset. This study with low penetrance(28). Familial
also demonstrated a 2-peak pattern. The occurrence of MMD was to be reported
results are similar to that of the other approximately 10%-15% in Japan
Chinese series(3,18), whereas there are (1)
patients . Moreover, the concordance rate
differences between our data and reports of MMD in monozygotic twins is as high
from Japan(12). The higher peak observed as 80%(24). These findings, as well as racial
in patients age 5-9 years prior to 10s in differences in susceptibility to MMD(22),
Japan shows the prevalence peak is much indicate that genetic factors may play an
earlier in mainland China. For males, the important role in the incidence of MMD.
biggest peak was at ages 5-9 and a smaller We uncommonly identified two cases of
peak at 40-44 years. Unexpectedly, we MMD with congenital anomalies, which
found the highest prevalence for females at support a role for genetic predisposition
ages 40-44 and a smaller peak at ages 35- further. Whereas there was no evidence of
39, suggesting MMD occurs mostly in familial MMD in our patients; it is
adults for females. Although there was a probably because no family members with
significantly higher prevalence at 5-9 MMD were examined and eventually
years, but the percentage of patients (ages diagnosed by angiography or MRA in our
< 10 years old) account for only 19.2% of study. But we can conclude that familial
all patients in our cohort; MMD occurred occurrence rate of MMD in mainland
mainly in adults in mainland China with China was very low according to Tab. 2.
reviewing literature(3,18). Autoimmune factor has been reported to be
In the current study, the majority of associated with the pathogenesis of
patients presented with ischemic symptom MMD(21,25). Higher proportion of
onset. It is different from the results of Wei autoantibodies were also detected in our

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cohort, and we rarely identified 3 patients In medically treated patients, the Kaplan-
with coexistence of moyamoya disease and Meier risk for recurrent stroke after the
Graves' disease, which is very rare(25). first ischemic event was approximately
17% in the first two years. The 5-year-
Previous studies have described an
Kaplan-Meier risk of recurrent stroke was
inevitable disease progression without
42.0%. However, there is the lower risk of
surgery(15). It has been estimated that up to
recurrent stroke in another Chinese report,
two thirds of patients with MMD have
where the cumulative 5-year Kaplan-Meier
symptomatic progression over a 5-year
risk of stroke was only 12.7% in surgically
period; the outcome is poor without
treated patients(3), as well as North
treatment(4). However, there are no reports
American study (17%)(10) and the
on long-time natural history of patients
European study (27.3%)(13). All these data
with MMD in mainland China. The
show there is a good outcome with surgical
recurrence rate is 18.9% after the first
procedures, but the recurrent stroke rate
ischemic events in our study, which is
was slightly more higher than that of the
similar to the result reported before
(23.8%)(15). Infarction is often recurrent drug treatment group within two years in
with intervals of 1 month to 120 months. our patients, which was probably related to
The total rebleeding rate is 25%, however, recurrent infarctions caused by the surgery.
it is noteworthy that in four cases (57.2%) Up to now, although there has not been any
rebleeding occurred more than 7 years randomized controlled trial comparing
after the first hemorrhage. Recurrent surgical with medical treatment, surgical
bleeding within 30 days was not frequent revascularization has been accepted as a
with a poor prognosis; the second primary treatment for moyamoya(1). A
hemorrhage developed within one month meta-analysis suggested 87% patients
after the first bleeding episode in three gained benefit from surgical
revascularization, with indirect, direct, and
cases with 2 patients dying. These findings
have similarity of the report in EIICHI et al combined techniques showing equal
effectiveness(7). One study found that the
series. And the second bleeding episode
was characterized by a change in 5-year risk of ipsilateral stroke was
hemisphere and by the type of bleeding(14). reduced from 82% in conservatively
treated patients to 17% in surgically treated
It is presumed that the condition is
patients(10). But the recurrence rate of
associated with diffuse vulnerability of
stroke is highest within the first 30 days
collateral vessels adjacent to the lateral
after surgery, after which the risk reduces
ventricle. However, some authors have
significantly(26). In our patients, a
emphasized the relevance of a ruptured
subsequent infarction occurred in 2 cases
microaneurysm during the second
(16) within the first 30 days after surgery, and a
rebleeding . We identified 2 cases with
aneurysm, but no rebleeding was seen second infarction 1 year after the surgery
during follow-up. In the series reported by in 1 case. Because the mortality of surgery
Chiu(2) et al, no patient initially presenting is 8%, the further study to estimate the
safety of the operation is required.
with an ischemic stroke experienced a
subsequent hemorrhage and no patient In conclusion, this study expands the
initially presenting with a hemorrhage knowledge of MMD in mainland China.
experienced a subsequent ischemic stroke. There was a specific bimodal pattern of
In the present study, our findings are age distribution in Chinese people. The
basically consistent with the report by Chiu majority of patients presented with
et al; only 1 patient presenting with ischemic symptom. The patients with
hemorrhage suffered haemorrhaging in 3 medical treatment were at extremely high
and 20 years after the initial symptom. risk of recurrent stroke. Further
prospective studies are needed to estimate

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