Neurol Med Chir (Tokyo) 50, 320¿323, 2010

Cerebral Vasospasms After Intraventricular Hemorrhage
From an Arteriovenous Malformation
—Case Report—
Shoji YOKOBORI, Akihiro WATANABE, Ryuta NAKAE, Hidetaka ONDA,
Akira FUSE, Shigeki KUSHIMOTO, and Hiroyuki YOKOTA
Department of Emergency and Critical Care Medicine, Nippon Medical School, Tokyo

Abstract
A 33-year-old female presented with a rare case of severe vasospasm following the rupture of an arteriovenous malformation (AVM) without subarachnoid hemorrhage. Initial computed tomography
(CT) revealed a subcutaneous hematoma and cast formation of intraventricular clots without the deposition of subarachnoid blood in any basal cistern. Cerebral angiography revealed a small AVM located
in the right parietal lobe without aneurysmal formations. Repeat CT demonstrated no evidence of
subarachnoid clots expected with the presence of intraventricular clots and she was transferred to a
general ward. She suffered sudden onset of motor aphasia and disturbance of consciousness on Day 17
after the hemorrhage. Magnetic resonance imaging indicated diffuse cortical infarction and subsequent
magnetic resonance angiography revealed severe narrowing of the bilateral internal carotid arteries.
Three-dimensional CT angiography on the same day indicated similar findings. She was transferred
back to the intensive care unit for critical treatment. However, she suffered persistent mild right
hemiparesis and motor aphasia. The characteristic features of vasospasm after intraventricular hemorrhage from AVMs are delayed onset, acute deterioration of consciousness, female predominance, and
localization to the bilateral internal carotid arteries. Treatment of patients with AVM rupture should
consider the risk of severe vasospasm, even if there is no subarachnoid clot.
Key words: vasospasm,
cerebral infarction

arteriovenous malformation,

Introduction

Initial computed tomography (CT) indicated a right occipital subcutaneous hematoma and cast formation of intraventricular clots without blood accumulation in the
basal cisterns (Fig. 1A). Her blood pressure was normalized with calcium antagonists to prevent deterioration of
the hemorrhage, and she was admitted to the intensive
care unit and observed closely.
The next day, her level of consciousness had slightly improved. Cerebral angiography performed on the following
day revealed a small AVM located in the right parietal
lobe, fed by the left anterior cerebral artery and drained by
the right parietal cerebral vein, but no aneurysmal formations (Fig. 1B). Repeat CT at intervals of several days
demonstrated no evidence of subarachnoid clots except
for the presence of intraventricular clots. She was transferred to a general ward without severe neurological deterioration on Day 13 after admission.
Her verbal response suddenly decreased, and she appeared to have motor aphasia on Day 17 after the hemorrhage. Emergent magnetic resonance (MR) imaging indicated diffuse cortical infarction (Fig. 2A) and subsequent
MR angiography revealed severe narrowing in the
supraclinoid portions of the bilateral internal carotid arteries (Fig. 2B). Three-dimensional CT angiography per-

Cerebral arterial vasospasm often occurs in patients
suffering from aneurysmal subarachnoid hemorrhage
(SAH). Cerebral vasospasm is an uncommon but critical
complication in patients with intraventricular hemorrhage (IVH) caused by arteriovenous malformation (AVM)
rupture. Ruptured AVM can induce vasospasm, but rarely
without SAH.14,15,17) We report a case of symptomatic
vasospasm following IVH related to AVM.

Case Report
A 33-year-old female suddenly suffered headache, nausea,
and loss of consciousness, and was transferred to our
hospital. On admission, she was comatose with a Glasgow
Coma Scale score of 13 and moderate left hemiparesis.
Her blood pressure was 178/84 mmHg. Initial blood examinations, including clotting factors, found no abnormalities. She had no history of illnesses such as hypertension, and was not taking any medications on a regular basis.
Received

May 28, 2009;

Accepted

intraventricular hemorrhage,

August 25, 2009

320

Vasospasms After IVH From an AVM

Fig. 1 A: Head computed tomography scans on admission
showing right occipital subcutaneous hematoma and intraventricular clots in the lateral and fourth ventricles without accumulation of blood in the basal cisterns as subarachnoid
hemorrhage. B: Left internal carotid angiograms performed
on the day after admission revealing a small arteriovenous malformation in the right parietal lobe, fed by the left anterior
cerebral artery and drained by the right parietal cerebral vein.
No aneurysmal formation was seen. This series of bilateral
carotid angiograms detected no spasm or occlusion of the
cerebral vessels.

321

Fig. 2 A: Axial diffusion-weighted magnetic resonance (MR)
image (repetition time/echo time 10,000/80 msec) on the 17th
day of hospitalization demonstrating high intensity areas
which indicated cerebral infarction in the bilateral
hemisphere. B: MR angiogram performed on the same day
revealing severe narrowing in the bilateral cerebral arteries, especially in the supraclinoid, A1, and distal portions of the anterior cerebral arteries (white arrows). C: MR angiogram on
the 24th day of admission revealing dramatic improvement of
the vasospasms (white arrows).

hemiparesis and was transferred to another institute for
rehabilitation on Day 40. She was discharged from the rehabilitation hospital and is planning to undergo gamma
knife radiosurgical treatment of the residual nidus.

Discussion
formed on the same day indicated similar findings. Her
level of consciousness gradually deteriorated, and motor
and sensory aphasia developed. She was treated with intravenous calcium antagonists, radical scavengers, and
volume expanders, and was transferred back to the intensive care unit.
Despite intensive therapies for vasospasm, CT performed on Day 20 demonstrated low density areas indicating cerebral infarction in the left frontal lobe, left insular
region, and right occipital lobe, according with the
``watershed'' area of the cerebrum. Her level of consciousness and aphasia improved during the 3rd week after the
neurological deterioration. MR angiography on Day 24
demonstrated improvement of the severe spasms of the
cerebral arteries (Fig. 2C).
Superselective embolization to the feeding artery and nidus was performed on Day 33. The size of the nidus was
decreased and the flow of venous drainage reduced after
embolization. However, she had persistent mild right

Neurol Med Chir (Tokyo) 50, April, 2010

Six cases of symptomatic vasospasm due to IVH following
AVM rupture have been reported (Table 1).8,11,12,15,17) Initial CT demonstrated obvious IVH in all cases. Most cases
had intraparenchymal hemorrhage as well but no cases
demonstrated subarachnoid blood in the basal cisterns.
The size and thickness of subarachnoid blood in the
basal cisterns are major predictors of vasospasm after
aneurysmal bleeding,6) but the predictive value of IVH is
not well known in patients with SAH. Several studies have
found no significant association between IVH and the risk
of vasospasm in the setting of aneurysm rupture,1,7) but
others have demonstrated that IVH is an independent
predictor of delayed vasospasm. Blood in the lateral ventricle might be a risk factor for delayed cerebral ischemia
due to vasospasm in patients with SAH.3) The IVH was
mainly distributed in the lateral ventricle in all previous
cases (Table 1). Intraventricular clot was present for
almost 2 weeks in our patient, so we suppose that such

lt ACA
lateral,
third,
fourth
rt occipital
17
＋

33
Japan
Present case

F

＋

－

rt PCA
lateral,
third
—
10
－
－
＋

41
United
States

F

—
17
－

26
Japan

Kobayashi et al.
(2002)11)
Gerard et al.
(2007)8)

M

＋

－

rt putaminal
17
－
＋
＋

14
Japan

F

rt thalamus
6
＋

40
Japan
Maeda et al.
(1997)15)

F

＋

－

rt caudate
nucleus
16
－
＋
＋

F
31
Switzerland
Kothbauer et al.
(1995)12)

rt occipital,
lt frontal,
lt temporal

rt temporooccipital
lt parietooccipital

bil MCAs,
bil ACAs
bil MCAs,
lt ICA,
bil PCAs
bil ICAs,
lt ACA
rt AchA

unknown
bil ICAs
rt MCA

lt parietal
bil ICAs

bil frontal
bil ICAs,
rt MCA

rt anterior
callosal
artery
rt AchA

lt parietooccipital
bil A1s,
bil M1s
lt MCA,
lt ACA

lt lateral,
third,
fourth
bil lateral,
third,
fourth
bil lateral,
third
bil lateral,
third
rt lateral
—
3
－
－
＋

F
11
Japan
Yanaka et al.
(1992)17)

Infarct
Location of
vasospasm
Location of
AVM
Location of
initial IVH
Location of
intraparenchymal
hemorrhage
Onset of
vasospasm
(days)
SAH
ICH
IVH
Sex
Age
(yrs)
Country
Author (Year)

Reported cases of symptomatic vasospasm due to intraventricular hemorrhage (IVH) following arteriovenous malformation (AVM) rupture
Table 1

A1: A1 segment of anterior cerebral artery, ACA: anterior cerebral artery, AchA: anterior choroidal artery, ICA: internal carotid artery, ICH: intracranial hemorrhage, M1: M1 segment of middle cerebral artery, MCA: middle cerebral artery, PCA: posterior cerebral artery, SAH: subarachnoidal hemorrhage.

S. Yokobori et al.

322

persistent clots in the lateral ventricles will stimulate the
cerebral vessels continuously due to the circulation of
bloody cerebrospinal fluid (CSF). Therefore, we also suggest that long-lasting clots are the main cause of
vasospasm.
Vasospasm is also uncommon in patients with primary
IVH. The first case of cerebral vasospasm associated with
primary IVH suggested several mechanisms.4) The main
cause of vasospasms in patients with primary IVH could
not be established, but subsequent hydrocephalus may
have been involved. Hypothalamic dysfunction with extension of intracranial hemorrhage was also proposed as
the cause of development of intracranial vasospasm.16)
Neither hypothalamic extension of intracranial bleeding
nor remarkable severe hydrocephalus was present in our
patient, so these mechanisms seemed unlikely causes of
the vasospasm in our patient.
Bilateral carotid involvement also appears to be a
characteristic feature of IVH-induced vasospasm after
AVM rupture. The mechanism of vasospasm following
IVH is unknown, but hypothetical mechanisms include
recirculation of heme products into the subarachnoid CSF
space with subsequent impairment of endothelium-dependent relaxation, decreased response to nitric oxide, increased sensitivity to the vasoconstrictor endothelin, and
inactivity of potassium channels.5)
Remarkably, in 3 of the previous 6 cases, the onset of
vasospasms occurred over 2 weeks after the hemorrhage
(16–17 days after onset of hemorrhage). Our patient
demonstrated late-phase vasospasm with onset on the 17th
day after the hemorrhage. Such delayed onset may be a
characteristic of vasospasm after only IVH is caused by
bleeding from AVMs.15) The cause of delayed vasospasm
following IVH is not known. However, a large amount of
IVH may delay CSF circulation and inhibit the washout of
bloody CSF, thus provoking continuous cerebrovascular
stimulation, resulting in delayed vasospasm.
The previous patients were almost all young females
(Table 1). The incidence of AVM rupture in females is
higher than in males.9) No female predisposition for IVH
has been described in patients with AVMs. However, female dominancy is known for the occurrence of
vasospasm in patients with SAH,2,10) but the mechanism is
not well known. The effect of estrogen on changing vascular tone in coronary artery diseases may be important.13)
In our case, hormonal examination was not performed, so
we cannot confirm any relationship between the hormonal balance and vasospasm. Analysis of the female hormones or sexual cycles is needed in patients with IVH
from AVMs.
We conclude that the characteristic features of
vasospasm after IVH from AVMs are delayed onset, acute
deterioration of consciousness, female predominance,
and localization to the bilateral internal carotid arteries.
Treatment of patients with AVM rupture should consider
the risk of severe vasospasm, even if there is no
subarachnoid clot.

Neurol Med Chir (Tokyo) 50, April, 2010

Vasospasms After IVH From an AVM

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Address reprint requests to: Shoji Yokobori, M.D., Department of
Emergency and Critical Care Medicine, Nippon Medical
School, 1–1–5 Sendagi, Bunkyo–ku, Tokyo 113–8603, Japan.
e-mail: shoji＠nms.ac.jp