Clinical Neurology and Neurosurgery 109 (2007) 125131

Surgical results in pediatric moyamoya disease: Angiographic

revascularization and the clinical results
Dal-Soo Kim, Seok-Gu Kang , Do-Sung Yoo, Pil-Woo Huh,
Kyoung Suok Cho, Chun Kun Park
Department of Neurosurgery, The Catholic University of Korea College of Medicine, Uijeongbu St. Marys Hospital,
65-1 Kumoh-dong, Uijeongbu, Gyeonggi 480-130, Republic of Korea
Received 26 January 2006; received in revised form 15 May 2006; accepted 18 June 2006

Abstract
Objecive: We retrospectively reviewed the pediatric patients with moyamoya disease (MMD) who underwent bypass surgery at our institution
to compare the surgical results according to the surgical procedures.
Patients and methods: There were 24 total patients (age range: 215 years; mean age: 8.2 years). Twelve patients underwent encephalo-duroarterio-synangiosis (EDAS) on 16 sides, 5 patients underwent encephalo-duro-arterio-myo-synangiosis (EDAMS) on 8 sides and 7 patients
underwent combined superficial temporal arterymiddle cerebral artery (STAMCA) anastomosis with EDAMS (STAMCAEDAMS) on 12
sides. The postoperative results were evaluated between 4 months and 5 years following surgery in terms of the angiographic revascularization
and the clinical outcome.
Results: EDAMS, regardless of the combined STAMCA anastomosis, was significantly effective for achieving a good extent of the postoperative angiographic revascularization as compared with simple EDAS (P < 0.05). STAMCAEDAMS tended to be better with respective to
the relief of preoperative ischemic symptoms as compared with simple EDAS, although there was no significant statistical difference.
Conclusion: These results suggest that EDAMS with or without the combination of STAMCA anastomosis was very useful for the formation
of collateral circulation in comparison with simple EDAS for treating the pediatric patients with MMD, although these findings were not well
correlated with the clinical outcomes.
2006 Elsevier B.V. All rights reserved.
Keywords: Bypass surgery; EDAMS; Moyamoya disease; Pediatric; Surgical results

1. Introduction
There are currently three different surgical treatments
for moyamoya disease (MMD). The first technique is
direct anastomotic bypass surgery such as superficial temporal arterymiddle cerebral artery (STAMCA) anastomosis [18]. Another one is indirect non-anastomotic bypass
surgery such as encephalo-duro-arterio-synangiosis (EDAS)
[914], encephalo-myo-synangiosis (EMS) [4,9,11,1518],
encephalo-galeo-myo-synangiosis (EGMS) [19,20], pial
synangiosis [21] and omentum transplantation [22]. The
other technique is combined direct and/or indirect bypass

Corresponding author. Tel.: +82 31 820 3067; fax: +82 31 847 2369.
E-mail address: seokgu9@kornet.net (S.-G. Kang).

0303-8467/$ see front matter 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.clineuro.2006.06.004

surgery such as encephalo-duro-arterio-myo-synangiosis

(EDAMS) with or without the combination of STAMCA
anastomosis (STAMCAEDAMS) [2327]. The final goal
of these surgical procedures is to minimize or prevent the
progression of ischemia in the brain that is due to MMD by
creating sufficient extracranial to intracranial collateral circulation.
We have operated on pediatric patients suffering with
MMD first using EDAS and later EDAMS with or without STAMCA anastomosis to utilize the source of a variety of donor arteries either directly or indirectly. To the
best of our knowledge, there have been no reports that
have compared the result of EDAS, EDAMS, and combined
STAMCA anastomosis with EDAMS for treating pediatric
MMD.

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Therefore the main purpose of this study is to compare the

surgical results according to the three surgical procedures
that were done by one neurosurgeon, for treating the pediatric patients suffering with MMD, and the results of surgery
were examined between 4 months and 5 years following the
surgery (mean follow-up: 1.5 years).

2. Materials and methods

This study consisted of 24 Korean children who suffered
with MMD and who underwent bypass surgery and were
followed up at our institute. The clinical characteristics of
our patients are presented in Table 1. They were 12 boys and
12 girls with age range of 215 years and their mean age was
8.2 years at the time of disease onset.
In this study, the patients who underwent only one of the
three different types of single or combined surgical procedures on either the unilateral or bilateral sides were selected:
EDAS on done on 16 sides in 12 patients, EDAMS was done
on 8 sides in 5 patients and combined STAMCA anastomosis and EDAMS was done on 12 sides in 7 patients.
The EDAS procedure described by Matsushima et al.
[10,14], was basically performed using a larger branch of
the superficial temporal artery (STA) on the bone flap that
was 67 cm in length and 34 cm in width. The dura mater
was incised along the longer diameter of the bone window
with taking care not to injure the large meningeal arteries and
the arachnoid membrane was not opened.
The EDAMS procedure reported by Kinugasa et al. [26]
was basically utilized. However, we used both branches of the
STA for encephalo-arterio-synangiosis (EAS) and we preserved the intact arachnoid membrane.

The third procedure was the combination of STAMCA

anastomosis using a larger branch of the STA and EDAMS
using another branch of the STA. The detailed surgical procedures are explained as follows. The scalp incision is made
directly above the posterior branch of the STA and extended
anteriorly at a blunt angle to the distal frontal branch of the
STA which resulted in a question-mark shaped incision. Both
branches of the STA are exposed as long as possible and the
galea and skin are widely divided to achieve the sufficient
galea attached and surrounded the STA. Then two lines of
incisions are placed in the galea 12 cm apart from each side
of both branches of the STA to the main trunk of the STA
in the shape of the letter Y. After retracting the Y-shaped
STA-galeal pedicle to either sides, the exposed temporal fascia and muscle are incised by means of an electric cautery
in a curvilinear fashion. After reflecting the muscle from the
skull, four burr holes are then made to perform craniotomy:
the first one is placed around the center of craniotomy site
to expose the middle meningeal artery (MMA), the second
and third one are placed at each of the two distal ends of
the STA, the last one is made at the frontal side. Then the
temporal base is removed additionally to make a space for
the inlaid STA pedicle and the temporal muscle to enter
underneath the frontal flap. The dura is incised into pedicles
based the bone window and rolled back on the brain surface
as described by Shirane et al. [19], while keeping the main
branches of the MMA and the arachnoid membrane intact.
The one of two branches of the STA is cut at its distal side
with the attached galea together create the STAMCA anastomosis. Another branch of the STA with its galea is laid on
the exposed brain surface. At this time, the distal end of the
STA is left intact in order to secure abundant and constant
blood flow through the STA. Thereafter the temporal mus-

Table 1
Clinical summary of the 24 patients with moyamoya disase
Number of patients (n = 24)
EDAS (n = 12)

EDAMS (n = 5)

STAMCAEDAMS (n = 7)

9.3 4.5

7.1 3.5

7.7 5.0

4 (33.3%)
8 (66.7%)

3 (60%)
2 (40%)

5 (71.4%)
2 (28.6%)

12 (50%)
12 (50%)

2 (16.7%)
8 (66.6%)
2 (16.7%)

1 (20%)
3 (60%)
1 (20%)

2 (28.6%)
0
5 (71.4%)

5 (20.8%)
11 (45.8%)
8 (33.4%)

Angiographic findingsa (Suzukis stage)c

II
2 (16.7%)
III
7 (58.3%)
IV
2 (16.7%)
V
1 (8.3%)

0
4 (80%)
1 (20%)
0

0
4 (57.1%)
2 (28.6%)
1 (14.3%)

2 (8.3%)
15 (62.6%)
5 (20.8%)
2 (8.3%)

Age (year) of

onseta

Total

Gendera
Male
Female
Clinical presentationb
TIA
TIAinfarction
Infarction

TIA: transient ischemic attack; EDAS: encephaloduroarteriosynangiosis; EDAMS: encephaloduroarteriomyosynangiosis; STAMCA: superficial temporal
arterymiddle cerebral artery.
a All preoperative factors between the groups were not significant.
b Significant difference only between the group EDAS and STAMCAEDAMS groups (P < 0.05).
c The angiographic findings were graded according to the criteria described by Suzuki and Kodama [38].

D.-S. Kim et al. / Clinical Neurology and Neurosurgery 109 (2007) 125131

cle is pulled over two branches of the STA and the exposed
brain surface and sutured along the opened dural edges. The
bone flap is replaced and the scalp wound is sutured in
layers.
For angiographic evaluation, selective digital subtraction
angiography of the external carotid artery was usually performed from 4 months to 5 years after the surgery for 24
patients. The extent of angiographic revascularization from
the implanted external carotid artery system was graded as
described by Matsushima et al. [13]: (1) good: the revascularization area was more than two-thirds of the MCA
distribution; (2) fair: the revascularization area was between
one-third and two-thirds of the MCA territory; (3) poor: the
revascularization area was less than one-third of the MCA
distribution.
The postoperative clinical outcomes were followed-up
from 4 months to 5 years after the surgery and they were
categorized into four grades, as described by Kim et al.
[28]: (1) excellent: the preoperative symptoms such as TIAs
or seizures completely disappeared; (2) good: the symptoms completely disappeared but the neurological deficits
remained; (3) fair: the symptoms persisted, albeit less frequently; (4) poor: the symptoms remained unchanged or
worsened.
The preoperative factors in between the three groups
of MMD patients (EDAS, EDAMS, STAMCAEDMAS)
were compared by using a Dunnett multiple comparison
test for continuous variables (age) and the 2 -test was used
for categorical variables (sex, clinical presentation and the
angiographic stage). The angiographic revascularization at
the operated sites and the clinical outcomes of the MMD children following the three different types of operations (EDAS,
EDAMS and, STAMCAEDAMS) were compared by 2 test. All the statistical units were the number of patients. Yet,

127

especially for the angiographic revascularization, the statistical unit was the number of surgical procedures.

3. Results
3.1. Angiographic revascularization
The angiographic results on the 36 operated sides are presented on Table 2. Among 36 sides that underwent surgery,
good revascularization was found in 6 of 16 sides that were
operated on by EDAS, in 6 of 8 sides that were operated
on by EDAMS (Fig. 1), and in 10 of 12 sides operated on
by STAMCAEDAMS (Fig. 2). Fair revascularization was
obtained in 8 of 16 sides with EDAS, in 1 of 8 sides with
EDAMS and in 2 of 12 sides with STAMCAEDAMS.
However, 2 of 16 sides with EDAS and 1 of 8 sides with
EDAMS resulted in poor revascularization.
There was a significant statistical difference between
EDAS and EDAMS (P < 0.05) as well as between EDAS
and STAMCAEDAMS (P < 0.05) in terms of angiographic neovascularization. It meant that EDAMS and
STAMCAEDAMS resulted in more revascularization than
did EDAS.
3.2. Clinical outcomes
Our results based on the 24 operated patients are presented in Table 2. An excellent to good result was obtained
in 8 (67%) of 12 patients treated with EDAS, in 4 (80%) of
5 patients treated with EDAMS, and in all patients treated
with STAMCAEDAMS. Fair results were found in 3 of 12
patients who underwent EDAS and a poor result was found in
one patient each who underwent EDAS and EDAMS, respec-

Table 2
Surgical outcomes of the 24 patients with moyamoya disease
Number of surgical procedures (n = 36)
EDAS (n = 16)a
Angiograohic revascularization
Good
6 (37.5%)
Fair
8 (50%)
Poor
2 (12.5%)

EDAMS (n = 8)

STAMCAEDAMS (n = 12)

Total

6 (75%)
1 (12.5%)
1 (12.5%)

10 (83.3%)
2 (16.7%)
0

22 (61.1%)
11 (30.6%)
3 (8.3%)

Number of patients (n = 24)

EDAS (n = 12)

EDAMS (n = 5)

STAMCAEDAMS (n = 7)

Total

7 (59%)
1 (8%)
3 (25%)
1 (8%)

4 (80%)
0
0
1 (20%)

4 (57%)
3 (43%)
0
0

15 (62.5%)
4 (16.7%)
3 (12.5%)
2 (8.3%)

outcomeb

Clinical
Excellent
Good
Fair
Poor

TIA: transient ischemic attack; EDAS: encephaloduroarteriosynangiosis; EDAMS: encephaloduroarteriomyosynangiosis; STAMCA: superficial temporal
arterymiddle cerebral artery.
a Significant difference between the groups that underwent EDAS and EDAMS (P < 0.05), and between the groups that underwent EDAS and
STAMCAEDAMS (P < 0.05).
b No significant difference between the groups (P > 0.05).

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D.-S. Kim et al. / Clinical Neurology and Neurosurgery 109 (2007) 125131

Fig. 1. A 7-year-old girl with moyamoya disease (angiographic stage II) (a) shows excellent revascularization through the dilated superficial temporal artery
and middle meningeal artery on the lateral view (b) of the right external carotid angiogram 6 months after the EDAMS, as compared with the preoperative
angiogram (c).

tively. These findings suggest that STAMCAEDAMS had

a tendency to show a more favorable clinical outcome when
compared with EDAS, although this difference was not statistically significant.

4. Discussion
Ikezaki et al. [29] have recently reported that single indirect bypass surgery is still the most frequently used technique
to treat MMD in Japan. EDAS has been described to be effective for the treatment of MMD in that the TIAs disappeared
within 1 year for more than 75% of the patients [12]. Further-

more, revascularization of more than one-third of the MCA

territory has been reported in 6284% of the cases after simple EDAS [1113,3032]. However, Miyamoto et al. [33]
have described that some patients were refractory to simple
indirect bypass surgery such as EDAS. Nakagawa et al. [34]
have also reported that this indirect revascularization cannot
halt the progression of cerebral ischemia in some cases.
Matsushima et al. [13] reported that a combination of
STAMCA anastomosis and EMS was superior to EDAS
for both the development of collateral circulation and the
postoperative clinical improvement at 1 year after surgery.
According to studies by Ischikawa et al. [35] or Takahashi
et al. [27], combined STAMCA bypass with EDAMS for

D.-S. Kim et al. / Clinical Neurology and Neurosurgery 109 (2007) 125131

129

Fig. 2. A 10-year-old boy with moyamoya disease (angiographic stage II) (a) shows extensive revascularization on the lateral view (b) of the right external
carotid angiogram 4 months after the combined STAMCA anastomosis with EDAMS (c).

treating pediatric MMD was effective in reducing the risk

of postoperative ischemic attacks as compared with indirect
surgery such as EDAMS [35] or EMAS [27].
Our study showed that EDAMS with or without the combination of STAMCA anastomosis seemed to be superior to
EDAS in the extent of achieving postoperative angiographic
revascularization (P < 0.05), although there was no statistical difference for the clinical outcome between EDAS and
EDAMS alone or EDAMS in combination with STAMCA
bypass.
For EDAS, the extent of the postoperative collateral circulation seemed to be limited because the operation field
was usually made along the course of the parietal branch
of the STA which was mainly used in our EDAS procedure.

Therefore these findings suggest that both branches of the

STA should be utilized as possible as not only for EDAS but
for EDAMS with or without STAMCA anastomosis in an
attempt to keep an extended area of postoperative revascularization.
The clinical symptoms such as TIA, RIND, and/or involuntary movements disappeared in the cases with a good
collateral formation but not in those cases with insufficient
development of the collateral circulation [11]. However other
reports [5,10,13,26,27,3537] have described that revascularization surgery for pediatric MMD has been consistently
effective in eliminating ischemic neurologic symptoms, and
this is irrespective of the use of direct or indirect bypass
surgery.

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D.-S. Kim et al. / Clinical Neurology and Neurosurgery 109 (2007) 125131

Ishikawa et al. [35] have recently observed that there

were no differences irrespective of the use of direct bypass
surgery for the final outcome after a certain period of time
when revascularization via indirect bypass had developed.
Even though STAMCA anastomosis provides an immediate increase in the blood supply to the brain and favorable results have been reported [2,3,5,38], this direct anastomosis alone did not promote long-lasting filling of the
MCA, which is presumably due to progression of the occlusive process with the involvement of the recipient artery in
MMD [38,39]. These findings supported the results of our
study, which did not show significant statistical differences
between the three surgical procedures with respect to the postoperative clinical outcome, although STAMCAEDAMS
tended to show a more favorable outcome as compared
with simple EDAS. We did not compare the time to clinical improvement after surgery between these two surgical
procedures.
Karasawa et al. [40] found that the STAMCA anastomosis became increasingly obstructed even though the cortical
branches of the MCA were opacified through the fine network produced in the region of the anastomosis. Furthermore,
Houkin et al. [24] have described that the deep temporal artery
and middle meningeal artery induced good neovascularization in the case of pediatric MMD. In contrast the induction
of neovascularization from the STA was not always good in
most pediatric cases. Therefore their main principle of the
surgery for pediatric MMD is to expose as much of the brain
surface as possible and to use the potential tissue as widely
as possible as a source of indirect revascularization, such as
the STA, temporal muscle, dura mater and MMA.
Our study had some drawbacks. We did not choose a
constant period of time after the bypass surgery to analyze the angiographic and clinical outcomes. This made our
results slightly difficult in comparison with different treatment modalities, although any new changes in the patients
conditions have not been found during the follow-up period.
Additionally, one preoperative factor (the clinical presentation) was not significantly the same between the different
treatment groups.
Based on our study, both EDAMS and STAMCA
EDAMS with using various sources of donor arteries might be
effective for achieving a good extent of postoperative revascularization, as compared with simple EDAS, in the pediatric
patients with MMD, although there were no significant differences according to surgical procedures in terms of the
postoperative clinical outcomes.

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