Childs Nerv Syst
DOI 10.1007/s00381-016-3111-5

CASE REPORT

Reversible striatal hypermetabolism in chorea associated
with moyamoya disease: a report of two cases
Yoshito Sugita 1 & Takeshi Funaki 1 & Jun C. Takahashi 2 & Yasushi Takagi 1 &
Yasutaka Fushimi 3 & Takayuki Kikuchi 1 & Kazumichi Yoshida 1 & Taketo Hatano 4 &
Natsuhi Sasaki 1 & Susumu Miyamoto 1

Received: 10 January 2016 / Accepted: 6 May 2016
# Springer-Verlag Berlin Heidelberg 2016

Abstract
Background The pathophysiological mechanism of chorea as a
presentation of pediatric moyamoya disease remains unknown,
although ischemia is suspected as a likely cause. The authors
describe two cases of pediatric moyamoya disease, both of
which presented with hemichorea in the stable phase after successful bypass surgery.
Clinical Presentation Cerebral blood flow was almost normal
in one case and decreased in the basal ganglia and watershed
area in the other case due to infarcts occurring before surgery.
In both cases, 18F-fluorodeoxyglucose positron emission tomography revealed elevated glucose metabolism in the corresponding side of the striatum, which reverted to normal after
recovery from chorea. Magnetic resonance angiography revealed a dilated and extended lenticulostriate artery at the
exact site of the hypermetabolic lesion.
Keywords Moyamoya disease . Chorea . Direct bypass
Electronic supplementary material The online version of this article
(doi:10.1007/s00381-016-3111-5) contains supplementary material,
which is available to authorized users.
* Takeshi Funaki
tfunaki@kuhp.kyoto-u.ac.jp

Introduction
Moyamoya disease is characterized as chronic progressive
stenosis of the terminal portion of the bilateral internal carotid
arteries and development of abnormal collaterals [22]. The
various manifestations of the disease include transient ischemic attack, ischemic and hemorrhagic stroke, epileptic seizure, and headache. Movement disorders such as chorea are
an uncommon presentation of pediatric moyamoya disease [1,
2, 11, 15–18, 21, 23, 25]. Because such chorea typically improves after bypass surgery, some researchers have postulated
ischemia in certain parts of the brain, including the basal ganglia, as a cause of chorea in moyamoya disease [11, 14, 15, 21,
23]. Neither the pathophysiological mechanism nor the origin of such chorea has been clarified, however. We describe two cases with moyamoya disease presenting with
hemichorea in the stable phase after successful direct bypass in which marked elevation of glucose metabolism in
the corresponding side of the striatum was observed with
18
F-fluorodeoxyglucose positron emission tomography
(18F-FDG PET).

Case presentation
Case 1

1

Department of Neurosurgery, Kyoto University Graduate School of
Medicine, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto 606-8507,
Japan

2

Department of Neurosurgery, National Cerebral and Cardiovascular
Center, Suita, Osaka, Japan

3

Department of Diagnostic Imaging and Nuclear Medicine, Kyoto
University Graduate School of Medicine, Kyoto, Japan

4

Department of Neurosurgery, Fukui Red Cross Hospital,
Fukui, Japan

A 12-year-old girl experienced transient numbness and
weakness on the left side of the body during running and
was admitted to our hospital. Angiography revealed severe
stenosis in the terminal portion of the bilateral internal
carotid artery with extensive development of abnormal collateral vessel networks (Fig. 1) symptomatic of moyamoya
disease. She underwent superficial temporal artery-tomiddle cerebral artery anastomosis of the right hemisphere;

Childs Nerv Syst

continued on their own without conscious effort (video), leading to a diagnosis of hemichorea. Laboratory examinations
were normal, including the level of free thyroxine, the
thyroid-stimulating hormone. Single-photon emission
computed tomography (SPECT) revealed normal cerebral
blood flow. Magnetic resonance imaging (MRI) revealed a
small asymptomatic ischemic lesion in the right frontal
white matter. 18F-FDG PET revealed markedly elevated
glucose metabolism in the right striatum (Fig. 2). Coronal
section of MR angiography demonstrated a dilated and
extended lenticulostriate artery passing through the right
striatum and connecting to the medullary artery in the
periventricular area (Fig. 2). She was treated with oral intake of haloperidol, with the chorea gradually improving
thereafter. Elimination of the chorea was confirmed when
she visited our clinic 2 months after onset. 18F-FDG PET
performed at that time revealed normalized glucose metabolism in the right striatum (Fig. 2).
Fig. 1 Case 1 (left hemichorea). Anterior-posterior view of right (a) and
left (b) internal carotid artery angiography before surgery revealing
occlusion of the terminal portion of the internal carotid artery with
development of moyamoya vessels. Lateral view of right (c) and left (d)
external carotid artery angiography after surgery revealing good patency
of bypasses

this was repeated on the left side 1 month later. The surgery
eliminated the transient ischemic attacks. Angiography
3 months after surgery revealed good patency of the bypasses (Fig. 1). She remained symptom-free for 5 years
after surgery.
At the age of 17 years, she suddenly experienced continuous involuntary movement of the left arm. Her manifestation
was characterized as brief, involuntary, and irregular movements of her left forearm, shoulder, fingers, and face that
Fig. 2 Case 1 (left hemichorea).
Axial image of 18F-FDG PET
during the acute phase (a) and
during recovery from chorea (b).
Subtraction image generated by
registered acute and recovery
phase 18F-FDG PET images (c)
revealing marked
hypermetabolism in the right
stratum in the acute phase.
Coronal image of 18F-FDG PET
during the acute phase of (d) and
during recovery from chorea (e).
Coronal section of MR
angiography (f) revealing an
extensively dilated and extended
lenticulostriate artery in the right
striatum (arrow)

Case 2
A 10-year-old girl experienced transient motor weakness of
the left leg while playing and was admitted to our hospital.
Her father was diagnosed as neurofibromatosis type 1. She
had many café-au-lait spots on her skin, a finding symptomatic of neurofibromatosis. Angiography revealed severe stenosis in the terminal portion of the bilateral internal carotid
artery with extensive development of abnormal collateral vessel networks (Fig. 3) symptomatic of moyamoya syndrome.
She underwent superficial temporal artery-to-middle cerebral
artery anastomosis of the left hemisphere; this was repeated on
the right side 1 month later. Surgery eliminated the transient
ischemic attacks.
Three months after surgery, she experienced involuntary
movement of her right extremities. The involuntary

Childs Nerv Syst

striatum (Fig. 4). The chorea gradually improved after administration of haloperidol. 18F-FDG PET performed after
recovery revealed normalized glucose metabolism in the right
striatum (Fig. 4).

Discussion

movements, especially prominent in her fingers, were diagnosed as hemichorea. While angiography revealed good patency of bypasses (Fig. 3), SPECT revealed hypoperfusion in
the left basal ganglia and watershed area attributable to the
infarcts occurring before surgery. She underwent 18F-FDG
PET, revealing elevation of glucose metabolism in the left
striatum (Fig. 4). Coronal section of MR angiography revealed a dilated and extended lenticulostriate artery in the left

In the present cases, the striatal metabolism was elevated
and subsequently normalized, corresponding to the activity of chorea and suggesting a probable association between the two phenomena. Striatal hypermetabolism has
been reported in various types of chorea, including
chorea caused by group A streptococcal infection
(Sydenham’s chorea) [5, 10, 20], hyperthyroidism [3,
9], and hyperglycemia [12, 19, 24]. As of this writing,
however, no reports have surfaced in relation to
moyamoya disease. Although the prospect of a causal
relationship between chorea and striatal hypermetabolism
remains a subject of discussion [8, 10], striatal hypermetabolism could represent activation of a direct pathway—
an inhibitory signal pathway to the internal segment of
the globus pallidus and substantia nigra, both of which
negatively regulates thalamocortical projection [4]—
resulting in activation of the motor circuit. Several possible mechanisms have been suggested to explain striatal
hypermetabolism observed in chorea: immunological reaction in Sydenham’s chorea and hyperthyroidism [3, 8,
9, 13, 20], and the failure of vascular autoregulation in
hyperglycemia [12, 19, 24].
In moyamoya disease, ischemia or decreased cerebral
blood flow is a commonly hypothesized cause of chorea [2,

Fig. 4 Case 2 (right hemichorea). Axial image of 18F-FDG PET during
the acute phase (a) and during recovery from chorea (b). Subtraction
image generated by registered acute and recovery phase 18F-FDG PET
images (c) revealing marked hypermetabolism in the left stratum in the

acute phase. Coronal image of 18F-FDG PET during the acute phase (a)
and during recovery from chorea (b). Coronal section of MR angiography
(f) revealing an extensively dilated and extended lenticulostriate artery in
the left striatum (arrow)

Fig. 3 Case 2 (right hemichorea). Anterior-posterior view of right (a) and
left (b) internal carotid artery angiography before surgery revealing
occlusion of the terminal portion of the internal carotid artery with
extensive development of moyamoya vessels. Lateral view of right (c)
and left (d) external carotid artery angiography after surgery revealing
good patency of bypasses

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11, 15–18, 21, 23, 25]. The basal ganglia [2, 11, 15, 17, 23]
and the frontal cortical/subcortical region [14, 21] are candidates for the origin of chorea in moyamoya disease. The location where MRI revealed ischemic lesions in our cases is
compatible with those reported previously, and such ischemic
lesions occurring before surgery could cause delayed-onset
chorea. On the other hand, it might be a unique finding of
our cases that chorea occurred in the stable phase despite good
augmentation of blood flow from successful bypass.
Furthermore, the striatal hypermetabolism observed in our
cases is unlikely to be related to cerebral blood flow, as it
occurred regardless of the presence of the perfusion defect in
SPECT. A different pathological mechanism of chorea might
be involved in our cases.
Both of our cases had a specific vascular feature—a dilated
and extended lenticulostriate artery—at the exact site of the
hypermetabolic lesion. We have defined this type of collateral
as periventricular anastomosis, which is specific to moyamoya
disease [6, 7]. Ahn et al. reported that all their cases of
moyamoya disease-induced chorea had similar angiographic
features on the side corresponding to the chorea [1]. They
speculated that these vessels might contribute to the development of chorea through their physical disruption of normal striatal signaling. In our cases, these vessels might also
involve activation of the striatum through some mechanism, such as impairment of vascular autoregulation,
resulting in a hypermetabolic state in the striatum.
Further studies of both striatal metabolism and vascular
morphology might elucidate the pathophysiological mechanism of chorea in moyamoya disease.

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Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.

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