Acta Neurochirurgica
9 Springer-Verlag 1997
Printed in Austria

Acta Neurochir (Wien) (1997) 139:82-85

Progression of Arteriovenous Malformation in Moyamoya Syndrome
M.-E. Halatsch 1, H.-H. Rustenbeck 2, and J. Jansen 1
Departments of 1Neurosurgery and 2 Neuroradiology, University of G6ttingen, Federal Republic of Germany

Summary

ture o f c e r e b r a l A V M a s s o c i a t e d w i t h o c c l u s i v e v a s -

We report a case of moyamoya disease (MMD) associated with
arteriovenous malformation (AVM). The 30-year-old female patient presented with left-hemispheric transient ischaemic attacks
(TIAs) involving dysphasia and right-sided hemiparesis. CT-scan
and lumbar puncture showed no evidence of intracranial haemorrhage. Cerebral angiography revealed typical moyamoya vessels
and occlusion of multiple cerebral arteries with consecutive collateral blood supply. Moreover, a left-parietal AVM with a diameter
of approximately 2 cm was detected. An extra-intracranial arterial
bypass (EIAB) connecting the left superficial temporal artery
(STA) with a cortical branch of the left middle cerebral artery
(MCA) was performed (STA-MCA anastomosis) and yielded subsequent resolution of the neurological deficit. Nine months postoperatively neurological deficits similar to those of the initial presentation recurred. Repeated angiography suggested comparatively
increased AVM blood flow, and successful extirpation of the AVM
gradually re-established almost full functional ability. However,
deterioration of the neurological condition developed again. We
herewith present the first European case of moyamoya disease
associated with arteriovenous malformation and report the clinical
course under an alternative neurosurgical treatment consisting of
STA-MCA anastomosis and delayed extirpation of the AVM.

c u l a r d i s e a s e in 13 p a t i e n t s , n i n e o f w h o m s h o w i n g

Keywords." Moyamoya disease; cerebral ischaemia; extra-intracranial arterial bypass; extirpation of arteriovenous malformation.
Introduction
M o y a m o y a d i s e a s e is r a r e l y f o u n d in c o n j u n c t i o n
with cerebral AVM, and few cases have been reported
in the l i t e r a t u r e [1, 4, 5, 10, 11, 15]. W h i l e A u s t r a l i a
[11], the U n i t e d S t a t e s [5, 12] and Japan [1, 4, 10, 15]
h a v e d e s c r i b e d o n e , f o u r a n d f o u r cases, r e s p e c t i v e l y ,
n o cases h a v e t h u s far b e e n r e p o r t e d f r o m o t h e r c o u n tries. I n e i g h t o f t h e s e c a s e s the A V M w a s m a n a g e d
c o n s e r v a t i v e l y [1, 4, 5, 11, 12, 15], w h e r e a s the nineth
p a t i e n t u n d e r w e n t s i m u l t a n e o u s e x t i r p a t i o n o f the
AVM and prophylactic encephalo-aponeurotic synang i o s i s [10]. A p a r t f r o m t h e s e cases, t h e r e has b e e n a
r a d i o l o g i c a l s t u d y [8] d e s c r i b i n g the angio-architec-

c o l l a t e r a l s o f v a r i o u s types.
T h e aim o f this r e p o r t is to c o n t r i b u t e to the c l i n i cal u n d e r s t a n d i n g o f this rare c o m b i n e d d i s e a s e a n d to
b r i e f l y r e v i e w p e r t i n e n t literature.

Case Report
A 30-year-old woman was admitted to our hospital on January
10, 1992 with sudden development of left-occipital cephalgia, nausea and hypaesthesia of the II. through V. finger on the right.
Dysaesthesia of the right-sided fingertips and cheek was also present. The past medical history was significant for episodes of leftsided visual disturbances, aphasia, and intermittent paresis of the
right arm. Physical and neurological examination was normal
except for mild hemiparesis and dysdiadochokinesis on the right.
A plain CT-scan revealed a hypodensity in the area of the left
caput nuclei candatus and narrow basal cisterns but was otherwise
unremarkable. While evoked potentials and electroencephalography detected no impressive functional abnormality, transcranial
Doppler (TCD) demonstrated severe bilateral flow acceleration
which was not clearly attributable to distinct arteries. However, the
abnormal signals were felt most likely related to the left MCA and
the right posterior cerebral artery (PCA). Increased flow velocity
was also present in the basilar and right vertebral artery. Flow accelerations evoked by acetazolamide (ACZ) challenge were abnormally low or absent, and the flow velocity even dropped about 15%
in the distribution of the left MCA. On January 20, 1992 detailed
cerebral angiography disclosed a large caliber right vertebral artery
with remarkably enlarged bilateral PCA and posterior choroid arteries. Anastomosis was present between the vertebro-basilar and
supratentorial circulation. Carotid angiography demonstrated an
extraordinarily large caliber of both external carotid arteries and
their branches as well as proximal occlusion of both anterior cerebral arteries and distal occlusion of both MCA. A cork-screw-like
altered vessel convolution mainly originating from the left MCA
also showed blood supply from extradurally located anastomosis.
Capillary network-like anastomoses involving both lentieulostriate
arteries were traceable in the basal ganglia regions bilaterally. Left
external carotid angiogram revealed a prominent transdural anastomosis between the left middle meningeal and left anterior cerebral

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83

Fig. 2. Tl-weighted cerebral MRI (January 24, 1992) showing the
left-parietal localization of the AVM

Fig. 1. (a) Left carotid angiogram (January 20, 1992)before left
STA-MCA anastomosis demonstrating the AVM in 12 o'clock
position and the cork-screw-like altered vessel convolution characteristic for MMD. (b) Left carotid angiogram (January 27, 1993)
after EIAB surgery and before extirpation of the AVM suggesting
comparatively increased blood flow despite a slight difference between the angiographical phases

artery; an additional transdural anastomosis between the left maxillary and left ophthalmic artery was also demonstrated. Moreover,
this study disclosed a left-sided AVM in parieto-paramedio-postcentral projection with a diameter of approximately 2 cm and enlarged venous drainers (Fig. 1 a). The site of this lesion was confirmed by cerebral MRI on January 24, 1992 (Fig. 2).
On February 25, 1992 the patient underwent EIAB surgery
establishing a left-sided STA-MCA anastomosis. Postoperatively,
the neurological deficits gradually resolved, and the patient remained tree of complaints over a period of nine months when the

symptoms recurred in a fashion similar to the initial presentation.
Repeated cerebral angiography on January 27, 1993 showed the
EIAB to be patent and suggested comparatively increased AVM
blood flow (Fig. 1 b). The AVM was further examined by dynamic
CT-scan study which demonstrated presence of intense steal effect
and considerable shunt volume, whereas the diameter of the AVM
had remained constant on MRI.
Successful extirpation of the AVM was performed on February
16, 1993. A right-sided hemiparesis occurred postoperatively and
was progressively improving when the patient was transferred to a
rehabilitation unit on March 23, 1993. However, after a period of
approximately two and a half years the neurological deficit worsened anew, and the patient was readmitted to our hospital on October 11, 1995. This time, in addition to recurrence of left-hemispheric TIAs, she had experienced transient left-sided motor weakness.
A CT-scan was performed on admission and remained inconclusive. On October 18, 1995 cerebral angiography showed no significant progression of MMD or presence of AVM, and the patient has
been treated conservatively.

Discussion

From the nine cases of moyamoya disease associated with arteriovenous malformation previously described in the literature, six initially presented with
symptoms of cerebral ischaemia [4, 5, 10-12] while a
haemorrhage had taken place in the remaining three
[1, 5, 15]. Distribution of gender was essentially
equal and age ranged from 11 to 79 years (mean 39
years). In five cases the AVM was located in the frontal region without definite preference of side [ 1, 4, 5,
10, 15]; the remaining locations were left-parietooccipital [12], in the corpus callosum and in the dis-

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M.-E. Halatsch et al.: Progression of Arteriovenous Malformation

tribution of the right MCA [5]. Particularities were
the description of dural AVM [15] and, in another
case, the occurrence of the cerebrovascular phenomena within the context of Sneddon's syndrome [ 11]. In
addition, a case of de novo development of a cerebral
AVM in the exact location of a previous infarct in a
child with MMD was very recently reported [12].
While operations for MMD such as encephaloduroarteriosynangiosis, encephalomyosynangiosis, encephaloaponeurotic synangiosis, omentum transplantation, perivascular sympathectomy and superior cervical ganglionectomy were carried out in four cases [1, 4, 5, 10],
only one patient underwent resection of the AVM
[10]. In that patient, the left MCA was occluded one
month after surgery.
In our case, the patient presented with clinical features of an ischaemic cerebral state and corresponding
findings on CT-scan. The TCD results on initial admission suggested either compensatorily increased
blood flow or long-distance stenosis. Given a constant vessel diameter, the relationship between blood
flow velocity and blood flow within a large artery is
linear. Acetazolamide is known to cause extracellular
acidosis in the brain by reversibly inhibiting carbonic
anhydrase; resulting from vasodilation at the arteriolar level, cerebral blood flow (CBF) is subsequently
increased as a normal response [14]. The vasomotor
reactivity may diminish if the vasodilatory mechanisms are impaired or the already maximally dilated
vessels are incapable of further response. In this patient, the paradoxical decrease of flow velocity in the
left MCA after ACZ infusion was therefore indicative
of a possible intracerebral steal phenomenon.
The patient's neurological condition clearly improved following EIAB bypass but unfortunately
deteriorated after nine months, leading to the extirpation of the left-parietal AVM. The fact that the operatively achieved improvement of the haemodynamic
condition was lost may either be due to the natural
course of MMD with progressive vascular narrowing
and insufficient collateral blood supply or to increasing steal effect by the AVM that overtaxed bypass
capacity. The latter consideration seemed more likely
since on the one hand repeated angiography had suggested comparatively increased AVM blood flow and
on the other hand the patient had regained almost full
functional ability after extirpation of the AVM.
Despite a constant diameter of the AVM on MRI one
may assume that a "functional" progression of the
AVM on the basis of vessel dilation not influencing
the diameter of the AVM had occurred, the mecha-

nism of which remains unclear. Noteworthy, the
hypercapnic vasoreactivity in moyamoya syndrome is
severely reduced [13], probably due to already maximal vasodilation and/or decreased visco-elastic capacity of the cerebral vessels [2, 3, 9], also indicating
highly impaired compensatory potential with regard
to haemodynamic steal caused by an AVM. Yet, the
recurrence of neurological deficits after extirpation of
the AVM proves MMD to be an advancing process,
which may be true on the level of microcirculation
even if not detectable by angiography.
Several hypotheses have been raised to explain the
genesis or coincidence of AVM in this disease [1, 4, 5,
10, 12, 15], and it was pointed out that in the presence
of a cerebral AVM there may be an increase of blood
flow and turbulence at the internal carotid bifurcation
producing focal intimal hyperplasia which may lead
to arterial mural thickening and progressing stenosis
[8]. In contrast, under ischaemic conditions some
cerebral AVM may result from hyperstimulated anglogenesis involving basic fibroblast growth factor, a
powerful mitogen for fibroblasts, vascular endotheliurn, and smooth muscle cells [7].
Surgical mortality and morbidity rates of small
AVM (less than 4 cm in diameter) are lower than the
projected natural risk [6], so that surgical excision is
almost always indicated. On the other hand, extirpation of the AVM does not seem to definitively improve the impaired haemodynamics in MMD as seen
in this case.
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Comments
It is the first European report on moyamoya disease associated
with arteriovenous malformation. This combination is very rare,
because moyamoya disease is thought to be an acquired disease,
whereas AVM is a congenital disease.
Y. gonekawa

Several cases of arteriovenous malformation associated with
moyamoya disease have been reported especially from Japan, but
the coincidence is rather rare. I think such a case presented in this
report is extremely rare in Europe. The photos demonstrate the condition well.
K. Takakura

Correspondence: Dr. Marc-Eric Halatsch, The Mount Sinai
School of Medicine, The City University of New York, Division of
Neoplastic Diseases, Box 1128, One Gustave L. Levy Place, New
York, N.Y. 10029-6574, U.S.A.