J Neurosurg
J Neurosurg
109:1049–1051,
109:000–000, 2008

Acute cerebral ischemia following intraventricular
hemorrhage in moyamoya disease: early perfusion
computed tomography findings
Case report
I-Chang Su, M.D.,1 Chi-Cheng Yang, Ph.D. Candidate,1,2 Wei-Han Wang, M.S., 2
Jing-Er Lee, M.D., 3 Yong-Kwang Tu, M.D., Ph.D.,1 and Kuo-Chuan Wang, M.D.1
Division of Neurosurgery, Department of Surgery, National Taiwan University Hospital;
Department of Psychology, National Taiwan University; and 3Department of Neurology,
Zhuchi Buddhist Hospital, Taipei, Taiwan
1
2

The authors present a rare case of an infarction complication 15 days following acute intraventricular bleeding
due to moyamoya disease. Before the infarction occurred, perfusion CT imaging disclosed early but reversible isch­
emic injury on the day of hemorrhage. Dehydration and hypotension are both possibly contributing factors of pro­
gressive injury from reversible ischemia due to infarction. Although the patient underwent successful bypass surgery,
1 month after the ictus the neurobehavior evaluation still showed marked executive dysfunction. The authors address
that, in hemorrhagic-type moyamoya disease, early perfusion CT scanning is not only a powerful tool to identify the
high-risk group of patients who could experience subacute infarction, but also alarms neurosurgeons to eliminate any
predisposing factors when it shows reversible ischemic injuries. (DOI: 10.3171.JNS.2008.109.12.1049)

Key Words
•
cerebral infarction
•
intraventricular hemorrhage
moyamoya disease
•
perfusion computed tomography

M

oyamoya disease is characterized by idiopathic

stenosis of bilateral supraclinoid ICAs and for­
mation of collateral arteries, known as moya­
moya vessels. The disease is classified as 1 of 2 types:
infarction or hemorrhagic. The former has been reported
to be frequently encountered in the pediatric or juvenile
population, whereas the latter seems to be more prevalent
in adults.4,11 Generally speaking, the prognosis of hem­
orrhagic-type is poorer than infarction-type moyamoya
disease.
Infarction following the acute presentation of hemor­
rhagic-type moyamoya disease has been rarely reported;
we identified 7 cases after reviewing the literature. Various
mechanisms have been proposed, but they remain contro­
versial.5–7,9 Herein, we report on a patient with moyamoya
disease who developed cerebral infarction 15 days after
suffering a hemorrhage. Before this irreversible in­jury, ev­
Abbreviations used in this paper: CBF = cerebral blood flow;
CBV = cerebral blood volume; ICA = internal carotid artery; ICP
= intracranial pressure; IVH = intraventricular hemorrhage; MTT =
mean transit time.

J. Neurosurg. / Volume 109 / December
October 2008
2008

•

i­dence of reversible cerebral ischemia had already been
noted on perfusion CT scanning on the day of bleeding.
Given that early radiological detection of this ischemic in­
jury following IVH in moyamoya disease has never been
described, the usefulness of perfusion CT is especially ad­
dressed.

Case Report
History and Examination. This 29-year-old wom­
an presented to our hospital with sudden headache and
decreased level of consciousness. There was no motor
weakness. Routine laboratory tests revealed normal find­
ings. An initial CT scan revealed primary IVH, mainly
in the left lateral ventricle (Fig. 1A). No evidence of ce­
rebral infarction was observed. Perfusion CT scanning
revealed increased CBV in bilateral frontal cortices. The
CBF was markedly reduced, and the MTT was abnor­
mally prolonged in these regions (Fig. 1B–D). Cerebral
angiography demonstrated occlusion of the bilateral su­
praclinoid ICA and the presence of a rich but tortuous
1049

I. C. Su et al.

Fig. 1. A: Admission CT scan showing primary IVH. B–D:
Perfusion CT scans obtained on the day of bleeding, revealing
decreased CBF (B), increased CBV (C), and prolonged MTT (D)
in the bifrontal areas.

vascular network in the lenticulostriatal regions, a typical
pattern of moyamoya disease. The anterior and middle
ce­rebral arteries were not demonstrated bilaterally.

Treatment. After admission, the patient underwent
conservative treatment with osmotic diuretic and isotonic
solutions. Her blood pressure was ~ 100/70 mm Hg, and
her urine output was adequate. However, her oral intake
was inadequate due to poor appetite and nausea. On pos­
tictal Day 12, the patient fainted suddenly while walking
around. Repeated head CT scanning revealed neither a
new hemorrhage nor an ischemic lesion. On Day 15, the
patient became obtunded. An emergency head CT scan
disclosed bilateral frontal infarction (Fig. 2C and D). The
patient then received hypervolemia and induced hyper­
tension in the intensive care unit. One month later, she
underwent successful superficial temporal artery–middle
cerebral artery anastomosis on the left side. Aspirin and
Persantin were prescribed after the operation.
Posttreatment Course. One week after the bypass sur­
gery, the patient’s higher cortical functions were evaluated
by a neuropsychological test battery.2,3,8,12 The test results
showed a moderate level of aspontaneity and logopenia,
whereas it revealed a remarkable executive dysfunction
and impairments of verbal episodic memory.

Discussion

Infarction Complications Following Bleeding From
Moyamoya Disease

Infarction complications secondary to hemorrhagictype moyamoya are rarely reported, and their pathogeneses
are largely undetermined. Only 7 cases have been de­scribed
1050

Fig. 2. Left (A) and right (B) carotid artery angiograms show­
ing occlusion of supraclinoid segments of ICA and their bifurca­
tions. Moyamoya vessels were prominent around the base of the
brain. Computed tomography scans (C and D) obtained 15 days
after acute bleeding, showing cerebral infarction at the bifrontal
regions.

in the English-language literature.5–7,9 Summarizing all
these cases, we found that infarction mainly occurs during
the subacute stage after bleeding, typically between pos­
tictal Days 7 and 16. Dehydration,5 unrelieved increased
ICP,9 shrinkage of the ruptured vessel,6 and vasospasm7 are
all proposed contributing factors of infarction complica­
tions. In our patient, bilateral frontal infarction developed
15 days after IVH, and the proposed precipitating factors
included dehydration and borderline hypotension. There­
fore, a powerful tool that helps define the high-risk group
of infarction complication becomes essential.
Usefulness of Perfusion CT Scanning in Predicting the
High-Risk Group for Infarction Complications

Perfusion CT scanning provides a rapid and noninva­
sive survey of cerebral hemodynamics. It produces a color
mapping of CBV, CBF, and MTT, and it is applied in the
evaluation of various disease entities. For instance, this
tool is commonly used to evaluate the evolution of acute
ischemic stroke.10,13 Three distinct patterns have been de­
scribed. The first consists of a cerebral hypoperfusion
without true ischemia. In response to autoregulatory ef­
fects, perfusion CT scanning usually shows a prolonged
MTT, but CBV and CBF remain undisturbed. When au­
toregulation is impaired, the second pattern, so-called re­
versible ischemia, occurs. At this stage, prolonged MTT
is associated with a reduction in CBF. The CBV remains
normal or slightly increased. As autoregulation is no lon­
ger maintained, irreversible ischemia develops, which is
now characterized by an increased MTT in association
with decreased CBF and CBV.
J. Neurosurg. / Volume 109 / December 2008

Early perfusion CT findings in hemorrhagic-type moyamoya disease
Some authors have suggested that, in hemorrhagictype moyamoya, the only hemodynamic change before
bleeding is cerebral hypoperfusion without ischemic in­
jury. It corresponds to the first pattern of acute ischemic
stroke. For patients with preexisting cerebral hypoperfu­
sion, increased ICP resulting from acute bleeding may
lead to development of reversible ischemia, the second
pattern of ischemic stroke. Perfusion CT scanning in our
patient demonstrated this pattern during the acute stage
of IVH. This injury is due neither to vasospasm because
of the acute onset,1,10 nor to shrinkage of the ruptured
moyamoya vessel because ischemia involves bifrontal re­
gions. Instead, this likely reflects the effects of general­
ized edema and early impairment of oxidative metabo­
lism after IVH.1,10
Without paying attention to this early ischemic insult,
further dehydration, unrelieved increased ICP, or even va­
sospasm during the subacute stage will possibly lead to
irreversible ischemia and subsequent infarction, the third
pattern of ischemic stroke. In the 8 reported cases, includ­
ing ours, the authors of 7 reported infarction complications
during the subacute stage of bleeding. We highly suspect
that, before infarction develops, all these patients may al­
ready have early but reversible ischemia immediately after
acute IVH.
Herein, we have proposed that the susceptibility to fur­
ther ischemic injury in hemorrhagic-type moyamoya can
be determined by perfusion CT scanning in the early stage
of bleeding. When perfusion CT scanning shows re­versible
ischemia, it alarms neurosurgeons to eliminate any predis­
posing factors. Aggressive control of increased ICP and
adequate hydration are mandatory to prevent the infarction
complications following hemorrhage in patients with moy­
amoya disease, especially when early but reversible isch­
emic pattern is documented by perfusion CT scanning at
the acute stage of bleeding.

Conclusions

Ischemic injury following IVH is rare, but patients
at high risk for subacute infarction can be predicted us­
ing perfusion CT scanning in the acute stage of bleeding.
These patients may further suffer from neurobehavioral
disturbances, which probably depend on lesion locations.
Elimination of any possible unfavorable factors, such as
in­creased ICP and dehydration, is essential to prevent in­
farction complications following hemorrhage in moyamoya
disease, especially for those with radiological evidence of
acute but reversible ischemic injury.

J. Neurosurg. / Volume 109 / December 2008

Disclaimer
The authors report no conflict of interest concerning the mate­
rials or methods used in this study or the findings specified in this
paper.
References
1. Binaghi S, Colleoni ML, Maeder P, Uske A, Regli L, Dehdash­
ti AR, et al: CT angiography and perfusion CT in cerebral va­
sospasm after subarachnoid hemorrhage. AJNR Am J Neu­
ro­radiol 28:750–758, 2007
2. Folstein MF, Folstein SE, McHugh PR: “Mini-mental state.” A
practical method for grading the cognitive state of patients for
the clinician. J Psychiatr Res 12:189–198, 1975
3. Hua MS, Chang SH, Chen ST: Factor structure and age effects
with an aphasia test battery in normal Taiwanese adults. Neu­
ropsychology 11:156–162, 1997
4. Hung CC, Tu YK, Su CF, Lin LS, Shih CJ: Epidemiological
study of moyamoya disease in Taiwan. Clin Neurol Neuro­
surg 99 (2 Suppl):S23–S25, 1997
5. Iwama T, Kotani Y, Yamakawa H, Nagata I, Hashimoto N,
Sakai N: Cerebral ischemic complications following intracra­
nial bleeding in patients with moyamoya disease–three case
reports. Neurol Med Chir (Tokyo) 41:450–453, 2001
6. Nagasaka T, Hayashi S, Naito T, Okamoto T, Ikeda H, Inao S:
Concomitant cerebral infarction and intraventricular hemor­
rhage in moyamoya disease. Case report. J Neurosurg 106:
388–390, 2007
7. Nakai Y, Hyodo A, Yanaka K, Nose T: Fatal cerebral infarction
after intraventricular hemorrhage in a pregnant patient with
moya­moya disease. J Clin Neurosci 9:456–458, 2002
8. Nelson HE: A modified card sorting test sensitive to frontal
lobe defects. Cortex 12:313–324, 1976
9. Rafay MF, Smith SE, Dirks P, Armstrong D, deVeber GA:
Hem­orrhage predisposing to cerebral infarction in children
with moyamoya disease. Pediatr Neurol 34:400–404, 2006
10. Sanelli PC, Ougorets I, Johnson CE, Riina HA, Biondi A: Us­
ing CT in the diagnosis and management of patients with ce­
rebral vasospasm. Semin Ultrasound CT MR 27:194–206,
2006
11. Suzuki J, Kodama N: Moyamoya disease–a review. Stroke 14:
104–109, 1983
12. Wechsler D: Wechesler Adult Intelligence Scale, ed 3. San
Antonio, Texas: Psychological Corp, 1997
13. Wintermark M, Reichhart M, Cuisenaire O, Maeder P, Thi­
ran JP, Schnyder P, et al: Comparison of admission perfusion
computed tomography and qualitative diffusion- and perfu­
sion-weighted magnetic resonance imaging in acute stroke
pa­tients. Stroke 33:2025–2031, 2002
Manuscript submitted August 22, 2007.
Accepted December 17, 2007.
Address correspondence to: Kuo-Chuan Wang, M.D., Division of
Neurosurgery, Department of Surgery, National Taiwan University
Hospital, No. 7, Chung San South Road, Taipei, Taiwan, China.
email: wang081466@yahoo.com.tw.

1051