Neurol Med Chir (Tokyo) 48, 390¿393, 2008

Dramatic Disappearance of Moyamoya Disease-Induced
Chorea After Indirect Bypass Surgery
—Case Report—
Koji KAMIJO and Toru MATSUI
Department of Neurosurgery, Saitama Medical Center/Saitama
Medical University, Kawagoe, Saitama

Abstract
A 31-year-old woman with moyamoya disease presented with choreiform movements persisting for 4.5
years. Magnetic resonance imaging showed a fine vascular plexus in the base of the brain but no parenchymal brain damage. Cerebral angiography revealed intracranial vascular abnormalities compatible
with moyamoya disease. Single photon emission computed tomography with N-isopropyl-p-123I-iodoamphetamine showed definite reduction of the regional cerebral blood flow (rCBF) in the bilateral striata
and frontotemporoparietal cortex. rCBF study with acetazolamide administration indicated marked
decrease of rCBF reserve in those regions. She underwent indirect bypass surgery (encephalo-duro-arterio-myo-synangiosis) under a diagnosis of moyamoya disease. The choreic involuntary movements
disappeared shortly after surgery. Postoperative angiography showed neovascularization in the extracranial to intracranial direction, associated with dramatic increase in rCBF in the involved regions.
Key words:

moyamoya disease,

chorea,

regional cerebral blood flow,

Introduction

Moyamoya disease occurs predominantly in children and young adults of Asian ethnicity, who usually present with headache, ischemic or hemorrhagic stroke, and seizures.3) Involuntary movement is
relatively rare as a clinical symptom of moyamoya
disease. Analysis of 1500 moyamoya disease cases in
Japan showed that 2.6% of the initial symptoms, and

Moyamoya disease is defined as an idiopathic
cerebral vasculopathy characterized by steno-occlusive changes in the terminal portion of the bilateral
internal carotid arteries and the formation of aberrant arterial networks in the vicinity of this lesion.

Fig. 1

Received

indirect bypass surgery

Preoperative axial T1-weighted (A) and T2-weighted (B) magnetic resonance (MR) images, and
MR angiogram (C), showing the development of fine vascular plexus in the base of the brain,
but no infarction or hemorrhage associated with moyamoya disease.

October 12, 2007;

Accepted

May 23, 2008

390

Moyamoya Disease and Chorea

Fig. 2

Preoperative right (A) and left (B) carotid
angiograms showing bilateral carotid arterial occlusions and abnormal basal vascular
network typical of moyamoya disease.

Fig. 4

Fig. 3

391

Preoperative
N-isopropyl-p-123I-iodoamphetamine single photon emission computed tomography (123I-IMP SPECT) scans
prior to (A) and after (B) acetazolamide administration, and subtraction image (C),
demonstrating reduction in the regional
cerebral blood flow and decreased vascular
reserve in bilateral striata and the frontotemporoparietal cortex. Postoperative 123IIMP SPECT scans prior to (D) and after (E)
acetazolamide administration, and subtraction image (F), demonstrating remarkable
improvement of cerebral perfusion in the
left hemisphere and bilateral striata.

3.3% of the neurological symptoms on admission
comprised involuntary movements.3) Only 23 cases
have been reported with choreiform movements, occurring in 6 adults and 17 children.1,2,4–6,8–12,14–19)
Two adults and 14 children underwent either direct
or indirect bypass surgery, all resulting in favorable
outcomes.
We describe an adult patient with moyamoya dis-

Neurol Med Chir (Tokyo) 48, September, 2008

Preoperative left external carotid angiograms, anteroposterior (A) and lateral (B)
views, and left external carotid angiograms,
anteroposterior (C) and lateral (D) views, 2
months after surgery demonstrating the formation of neovascularization from the extracranial anastomosis.

ease initially presenting with persistent choreic
movement, who was successfully treated with
cerebral revascularization.

Case Report
A 31-year-old right-handed woman presented with
choreic involuntary movements beginning in her
right thumb and middle finger in 1998, which then
expanded to the right side of her face several months
later. Administration of haloperidol 0.75 mg/day by
a local physician resulted in temporary subsidence
of the choreic involuntary movements. However, 4
years later, choreic movements recurred in her right
upper and lower extremities, expanding to the left
upper extremity after several months. The choreic
movements were resistant to medication, and she
was referred to us.
Neurological examination found she was intact
except for the choreic involuntary movements and
slight hypotonicity in her extremities. The involuntary movements were bilateral, but more frequent on
the right. Laboratory examination found no abnormalities in blood count, urinalysis, liver and renal

K. Kamijo et al.

392

function, electrolytes, blood glucose, and thyroid
function. Prothrombin time and activated thromboplastin time were normal. Antinuclear antibody
and rheumatoid factor levels were all within normal
limits. Magnetic resonance (MR) imaging showed
development of fine vascular plexus in the base of
the brain, but no infarct or hemorrhage (Fig. 1).
Cerebral angiography showed occlusion of the
bilateral internal carotid arteries just after the
branching of the ophthalmic artery on the right, and
the posterior communicating artery on the left. The
bilateral anterior and middle cerebral arteries were
not well visualized and numerous fine collateral vessels were seen (Fig. 2). Single photon emission computed tomography scans with N-isopropyl-p-123Iiodoamphetamine (123I-IMP SPECT) before and
after administration of acetazolamide showed reduced regional cerebral blood flow (rCBF) in the bilateral striata and frontotemporoparietal cortex,
more prominent on the left (Fig. 3A, B). These findings implied a lack of vascular reserve in these regions, suggesting misery perfusion (Fig. 3C).
We initially planned superficial temporal artery-

Table 1

middle cerebral artery (STA-MCA) anastomosis plus
encephalo-duro-arterio-myo-synangiosis (EDAMS).
However, the recipient MCA was too thin (less than
0.4 mm in diameter) for direct revascularization.
Therefore, we performed EDAMS on the left.
Postoperative angiography taken 2 months after surgery showed abundant neovascularization from the
extracranial arteries, compared with the preoperative finding (Fig. 4). Postoperative 123I-IMP SPECT
demonstrated remarkable improvement of cerebral
perfusion in the left hemisphere and bilateral striata
(Fig. 3D–F). The choreic involuntary movements improved satisfactorily without medication within 2
months after surgery. She has remained symptomfree for 4 years without additional contralateral surgery.

Discussion
Choreiform movement has been reported in association with striatal lesions caused by either cerebral
stroke or degenerative diseases.7,13) Therefore,
moyamoya disease-induced chorea is likely to be

Cases of moyamoya disease-induced chorea examined by cerebral blood flow (CBF) studies
Age
(yrs),
Sex

Abnormal signal on
MR imaging

CBF studies (SPECT/PET)

Tsuchiyama et al.
(1992)17)
Hosoya (1997)5)

33, F

caudate nucleus

9, F

Unno et al.
(2000)18)

16, F

frontal, parietal,
and occipital
areas
deep in the frontal
white matter

hypoperfusion in the caudate nucleus
and the parietal lobe (SPECT)
hypoperfusion in these regions as well
as in the basal ganglia (SPECT)

Han et al.
(2000)2)

29, F

frontal white
matter

Lyoo et al.
(2000)9)

22, F

Miura et al.
(2002)10)
Hong et al.
(2002)4)

54, M

frontotemporoparietal white
matter
no infarcts

20, F

centrum semiovale

Im et al.
(2004)6)

7, F

frontal white
matter
frontoparietal
white matter

Author (Year)

13, F
Kim et al.
(2006)8)
Present case

8, F

no infarcts

31, F

no infarcts

hypoperfusion and decreased vascular
reserve in the frontal and parietal
lobes and the basal ganglia (SPECT)
decreased vascular reserve in the
frontal and temporal lobes and the
basal ganglia (SPECT)
hypoperfusion in the frontotemporoparietal lobe (SPECT)
misery perfusion in the temporoparietal
lobe and the striatum (PET)
perfusion defect in the basal ganglia
and decreased vascular reserve in the
frontal lobe (SPECT)
perfusion defect in the hemisphere
(SPECT)
perfusion defect and decreased vascular
reserve in the posterior border zone
(SPECT)
decreased vascular reserve in the
frontoparietal lobe (SPECT)
hypoperfusion and decreased vascular
reserve in the frontotemporoparietal
lobe and the striatum (SPECT)

Effective therapy
(Postoperative rCBF)
medical therapy (*)
STA-MCA anastomosis (increased
rCBF in the whole hemisphere
including the basal ganglia)
chorea during pregnancy,
completely subsided after
abortion (*)
EDAS (*)
spontaneous resolution (*)
haloperidol (*)
STA-MCA anastomosis (normal
perfusion in the basal
ganglia, no improvement in
the left frontal lobe)
EDAS (*)
EDAS and EGS (*)
EDAMS (*)
EDAMS (markedly increased rCBF
in these regions)

EDAMS: encephalo-duro-arterio-myo-synangiosis, EDAS: encephalo-duro-arterio-synangiosis, EGS: encephalo-galeosynangiosis, MR: magnetic resonance, PET: positron emission tomography, rCBF: regional CBF, SPECT: single photon emission computed tomography, STA-MCA: superficial temporal artery-middle cerebral artery, (*): not described.

Neurol Med Chir (Tokyo) 48, September, 2008

Moyamoya Disease and Chorea
caused by ischemia of the striatopallidum, or compression by the abnormal vascular network.4,6,8–10,14)
CBF studies have been performed in 11 moyamoya
disease patients with chorea including the present
case (Table 1).2,4–6,8–10,17,18) Even if MR imaging
showed no damage of the basal ganglia, basal blood
flow reduction or decreased vascular reserve in
basal ganglia was noted in almost all cases. Surgical
vascular reconstruction resulted in disappearance
of involuntary movement such as chorea in all 17
patients. Postoperative CBF study (SPECT) demonstrated marked improvement of rCBF in the basal
ganglia in all 3 patients investigated.4,5) One
moyamoya disease patient with involuntary movements showed postoperative improvement of perfusion in the basal ganglia on SPECT, whereas the
rCBF response to acetazolamide in the frontal lobe
was not improved.4) These results suggested that the
hypoperfusion in the basal ganglia, rather than the
cerebral cortex, was responsible for the generation
of hemichorea.
The present case showed dramatic improvement
of bilateral choreic movements after EDAMS on the
left, which corresponded with remarkable improvement of perfusion in bilateral striata on postoperative 123I-IMP SPECT. These findings strongly suggest that hemodynamic compromise in the striatum
is responsible for the manifestation of choreic movement in moyamoya disease patients.
Patients with choreic involuntary movements
caused by moyamoya disease with poor vascular
reserve in the relevant region may be candidates for
surgical intervention.

References
1)

2)

3)

4)

5)

Gonzalez-Alegre P, Ammache Z, Davis PH, Rodnitzky RL: Moyamoya-induced paroxysmal dyskinesia.
Mov Disord 18: 1051–1056, 2003
Han SH, Kim YG, Cha SH, Chung SY: Moyamoya disease presenting with singing induced chorea. J Neurol Neurosurg Psychiatry 69: 833–834, 2000
Handa H, Yonekawa Y, Goto Y, Hohshimaru M,
Komori Y, Minato K: [Filing of 1,500 cases of the occlusive disease of the circle of Willis. Appendix, a follow-up study of 5 years or more on 200 cases], in Handa H (ed): Annual Report of Research Group on the
Occlusive Disease of the Circle of Willis. Kyoto, Ministry of Health and Welfare, 1985, pp 14–22 (Jpn)
Hong YH, Ahn TB, Oh CW, Jeon BS: Hemichorea as
an initial manifestation of moyamoya disease: reversible striatal hypoperfusion demonstrated on single
photon emission computed tomography. Mov Disord
17: 1380–1383, 2002
Hosoya M: [Moyamoya disease presenting initially
with mental disturbance]. No To Hattatsu 29: 471–

Neurol Med Chir (Tokyo) 48, September, 2008

6)

7)

8)

9)

10)

11)

12)

13)
14)

15)

16)

17)

18)

19)

393

475, 1997 (Jpn, with Eng abstract)
Im SH, Oh CW, Kwon OK, Cho BK, Chung YS, Han
DH: Involuntary movement induced by cerebral
ischemia: pathogenesis and surgical outcome. J Neurosurg 100: 877–882, 2004
Kase CS, Maulsby GO, deJuan E, Mohr JP:
Hemichorea-hemiballism and lacunar infarction of
the basal ganglia. Neurology 31: 452–455, 1981
Kim YO, Kim TS, Woo YJ, Kim CJ, Oh AK:
Moyamoya disease-induced hemichorea corrected by
indirect bypass surgery. Pediatr Int 48: 504–506, 2006
Lyoo CH, Oh SH, Joo JY, Chung TS, Lee MS:
Hemidystonia and hemichoreoathetosis as an initial
manifestation of moyamoya disease. Arch Neurol 57:
1510–1512, 2000
Miura T, Kobayashi M, Sonoo M, Isii K, Shimizu T:
[An adult case of Moyamoya disease presenting with
transient hemichorea]. Rinsho Shinkeigaku 42: 45–47,
2002 (Jpn, with Eng abstract)
Parmar RC, Bavdekar SB, Muranjan MN, Limaye U:
Chorea: an unusual presenting feature in pediatric
Moyamoya disease. Indian Pediatr 37: 1005–1009,
2000
Pavlakis SG, Schneider S, Black K, Gould RJ: Steroidresponsive chorea in moyamoya disease. Mov Disord
6: 347–349, 1991
Saris S: Chorea caused by caudate infarction. Arch
Neurol 40: 590–591, 1983
Scott RM, Smith JL, Robertson RL, Madsen JR,
Soriano SG, Rockoff MA: Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg 100 (2
Suppl Pediatrics): 142–149, 2004
Sudo K, Tashiro K, Moriwaka F, Kamiyama H, Abe
H: [A case of cerebrovascular ``moyamoya'' disease
with bilateral choreo-athetotic involuntary movements]. No To Hattatsu 18: 513–518, 1986 (Jpn, with
Eng abstract)
Suzuki J, Takaku A, Kodama N, Sato S: An attempt to
treat cerebrovascular `Moyamoya' disease in children. Childs Brain 1: 193–206, 1975
Tsuchiyama M, Kawabata K, Uyama O, Tachibana
H, Sugita H: [Hemichorea induced by cerebrovascular disease]. Nippon Iji Shinpo 3534: 43–45, 1992 (Jpn)
Unno S, Iijima M, Osawa M, Uchiyama S, Iwata M:
[A case of chorea gravidarum with moyamoya disease]. Rinsho Shinkeigaku 40: 378–382, 2000 (Jpn,
with Eng abstract)
Watanabe K, Negoro T, Maehara M, Takahashi I,
Nomura K, Miura K: Moyamoya disease presenting
with chorea. Pediatr Neurol 6: 40–42, 1990

Address reprint requests to: Koji Kamijo, M.D., Department of Neurosurgery, Saitama Medical Center/Saitama Medical University, 1981 Kamodatsujido–machi, Kawagoe, Saitama 350–8550, Japan.
e-mail: kamijo＠saitama-med.ac.jp