C ase R eport

doi: 10.2176/nmc.cr2013-0025
Online November 20, 2013

Neurol Med Chir (Tokyo) 54, 227–230, 2014

Emerging Sylvian Subpial Hematoma after the Repair of
the Ruptured Anterior Cerebral Artery Aneurysm with
Interhemispheric Approach: Case Report
Noriaki Minami,1 Toshikazu Kimura,1 Yasumitsu Ichikawa,1 and Akio Morita1
1

Department of Neurosurgery, NTT Medical Center Tokyo Stroke Unit,
NTT Medical Center, Tokyo

Abstract
A 60-year-old woman was admitted to the hospital due to a sudden loss of consciousness. Computed
tomography (CT) revealed a thick subarachnoid hemorrhage in almost all of the parachiasmatic cisterns, including the sylvian cisterns, with mild hydrocephalus. Three dimensional (3D)-CT angiography
showed an irregularly shaped aneurysm at the bifurcation of the left A2 and the frontopolar artery. The
aneurysm was successfully obliterated by clipping through the interhemispheric approach. CT performed
immediately after the operation showed a newly formed left temporal subpial hematoma. The patient’s
neurological status improved gradually after surgery, but deteriorated again 2 days after the operation.
CT revealed an enlarging right sylviansubpial hematoma. The subpial hematoma was rapidly removed
surgically. Slight hemiparesis and impaired higher cognitive function remained after a shunt procedure
for subsequent hydrocephalus. Emerging sylvian hematoma associated with a distant site of a ruptured
aneurysm is extremely rare. However, adequate attention is required in cases with a thick subarachnoid
hemorrhage in distant fissures.
Key words:

sylvian hematoma, subpial hematoma, subarachnoid hemorrhage, late complication

Introduction

Coma Scale: E1V3M5), but she showed normal motion of the
extremities. Blood pressure was 172/82 mmHg, and electrocardiogram showed normal sinus rhythm with mild tachycardia.
Computed tomography (CT) scan of the brain revealed a thick
subarachnoid hemorrhage with intraventricular extension
(Fisher group III) and mild hydrocephalus (Fig. 1). A small
subpial hematoma was also identified in the left frontal lobe.
An irregularly shaped saccular aneurysm was also detected
at the bifurcation of the left A2 and the frontopolar artery on
three-dimensional computed tomography (3D-CT) angiography
(Fig. 2). Laboratory data indicated normal coagulation status
(platelets: 280,000/μL; activated partial thromboplastin time
(APTT): 26.9 s; prothrombin time-international normalized
ratio (PT-INR): 0.98; fibrinogen/fibrin degradation products
(FDPs): 9.6 μg/mL; D-dimer: 7.4 mg/L; bleeding time: 1.5
min), although the white blood cell count (WBC) and
C reactive protein (CRP) level were increased. After the
smooth induction of general anesthesia, the aneurysm was
successfully obliterated with a clip through the anterior
interhemispheric approach on the day of admission.
Blood pressure showed little fluctuation during the
preoperative and operative periods. During the operation,
a ventricular drain was placed before opening the dura,

Intracerebral hematoma complicated with rupture of
the anterior communicating artery (ACom) and anterior
cerebral artery aneurysms is generally localized in medial
structures, such as the frontal lobe and corpus callosum.
Subpial hematoma in the sylvian cistern, which is idiomatically called “sylvian hematoma,” is usually seen in
cases with ruptured middle cerebral artery aneurysms.
Sylvian hematoma often induces cerebral artery spasm,
and is associated with poor prognosis. Here, we present
a rare case of emerging sylvian subpial hematoma after
successful clipping of a proximal anterior cerebral artery
aneurysm through the interhemispheric approach without
opening of the sylvian cistern.

Case Report
A 60-year-old woman was admitted to hospital because of
sudden loss of consciousness after complaining of severe
headache. On admission, she was in a stupor state (Glasgow
Received January 28, 2013; Accepted April 4, 2013

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Fig. 1 Computed tomography on
admission revealing thick subarachnoid hemorrhage with intraventricular
extension and mild hydrocephalus. The
small subpial hematoma was identified in the left frontal lobe (arrows),
but not in the right temporal lobe.

Fig. 2 Three-dimensional computed tomography angiogram on admission revealed an irregularly shaped saccular aneurysm
at the bifurcation of left A2 and frontopolar artery (arrows). No apparent spasm of the right middle cerebral artery was seen.

and the interhemispheric fissure was opened meticulously
with irrigation with urokinase (60,000 international units
(IU)/500 mL of saline). The sylvian cistern was not
opened because it was distant from the callosal cistern
where the aneurysm was located. We also recognized
and attempted to remove a small subpial hematoma at
the medial side of the left frontal lobe. However, this
was difficult due to the severe damage and edema of the
rectal gyrus. CT performed immediately postoperatively
showed the subpial hematoma in the right temporal lobe,
which was distant from the surgical corridor, but it was
not removed because the patient’s neurological condition
was good and it would have required an extensive and
invasive surgical procedure. After the operation, systolic

blood pressure was controlled between 110 mmHg and
140 mmHg. No additional intrathecal urokinase injection
was given. CT performed 12 h after surgery showed no
change (Fig. 3).

Discussion
Intracerebral hemorrhage associated with subarachnoid
hemorrhage indicates poor prognosis, with mortality rate
ranging from 21% to 85% even following successfully
surgery.1) Sylvian hematoma has also been reported to
lead to a poor prognosis compared with other types of
hematoma with subarachnoid hemorrhage.2) It occurs more
often than temporal intraparenchymal hematoma, and has

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Emerging Sylvian Subpial Hematoma with Ruptured ACA Aneurysm

Fig. 3 A: Computed tomography (CT) scans immediately after
the first operation demonstrating the emerging right sylvian
subpial hematoma. B: CT scans 12 h after the first operation
showing no apparent changes in size or shape of the hematoma. C: CT scans 36 h after the first operation. The sylvian
hematoma was definitely enlarged compared with A and B.
There was also a left frontal subpial hematoma, which had
already been noted, on admission. D: Postoperative CT scans
immediately after removal of the hematoma.

a significantly higher risk of symptomatic cerebral vasospasm.3) Sylvian hematoma is usually associated with a
ruptured middle cerebral artery aneurysm and sometimes
shows enlargement, even after complete obliteration of
the affected aneurysm. It is assumed that when an aneurysm adhering to the pia mater bleeds, the hemorrhage
can spread beneath the pia mater, and as the hematoma
extends, the thin arteries running perpendicular to the pia
mater are damaged, thus provoking secondary bleeding.4)
As this bleeding could cause further injury to nearby
small arteries, this process could be self-propagating
and eventually results in expansion of the hematoma.
However, as in our case, the aneurysm and the surgical
corridor were distant from the sylvian fissure, and thus
the initial formation of the subpial hematoma should be
different. This seems to be an extremely rare occurrence.
A similar case of an ACom aneurysm was reported previously, in which the pterional approach was employed
and the contralateral sylvian hematoma was subsequently
enlarged.5) However, in that case, the contralateral M1
portion was exposed in the initial operation, and therefore the possibility of injury to the pial artery cannot be
excluded. In our case, the sylvian fissure, to which the
pia mater originally adhered tightly, was damaged abruptly

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by the surging subarachnoid hematoma from the ruptured
anterior cerebral artery aneurysm, and the pial vessels were
injured. Relaxation of the increased intracranial pressure
by ventricular drainage and opening of the cistern may
have caused rebleeding of the affected pial artery of the
sylvian fissure. If this was true, the same phenomenon
could occur even in patients with endovascular coiling
procedures.
Cisternal irrigation with urokinase during the initial operation may have been responsible for the observed expansion
of the hematoma. Intrathecal irrigation with urokinase or
tissue plasminogen activator (tPA) was reported to be effective to remove the subarachnoid clot and is regarded as
preventing vasospasm. A randomized trial of intraoperative
intracisternal tPA for prevention of vasospasm following
aneurysmal subarachnoid hemorrhage revealed no significant
difference in the incidence of hemorrhagic complications
between the placebo (16.3%; subarachnoid hemorrhage:
2.3%) and tPA group (18.8%; subarachnoid hemorrhage:
4.6%) (P = 0.54).6) According to a retrospective review
of the comparison of intrathecal thrombolytic therapies
consisting of a no-treatment group (29 patients), urokinase
group (60 patients), and tPA group (22 patients), there was
one patient who developed intraventricular hemorrhage in
the tPA group, and this was the only bleeding complication
encountered in this cohort.7) In another report, the rate of
hemorrhagic complications was dependent on the dose,
and intraoperative irrigation with tPA was safe as long
as the proper dose was applied.8) We applied urokinase
rather than tPA, and the intraoperative dose was at most
60,000 IU diluted in 500 mL of normal saline, which was
a lower dose compared to these previous studies. Thus,
we consider the risk of bleeding due to urokinase to be
quite low, although the possibility that it was responsible
for accelerated bleeding cannot be excluded. Indeed, the
urokinase may have been responsible for enlargement of
the hematoma; the most important observation was that
the subpial hematoma was newly formed around the
unopened fissure distant from the operative field.
It is also possible that severe brain ischemia on admission and subsequent reperfusion provoked hematoma
expansion, but postoperative magnetic resonance imaging
(MRI) showed no such severe ischemic infarction.
A subpial hematoma with subarachnoid hemorrhage
should be removed as soon as possible to prevent cortical
perfusion impairment and subsequent cerebral vasospasm;
however, it is usually difficult to completely remove subpial
hematoma without parenchymal damage.2,9,10) The policy
in our facility is to remove subpial hematoma, if possible.
In this case, the subpial hematoma was first recognized
soon after clipping surgery, but we chose close observation
because the patient was in good condition and additional
removal would have required an extensive and invasive
surgical procedure. The patient’s outcome may have been
better if the hematoma had been removed earlier, but the

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risk and benefit of evacuation of the hematoma should
always be assessed carefully.

Conclusion
A subpial hematoma, which is difficult to remove
surgically, may form and gradually expand even when
located distant from the site of a ruptured aneurysm.
Special attention should be paid to patients with subpial
hematoma with subarachnoid hemorrhage, even if they
are treated by endovascular coiling. Growing sylvian
hematoma should be removed as soon as possible.

Conflicts of Interest Disclosure
The authors have no personal, financial, or institutional
interest in any of the drugs, materials, or devices described
in the article. All authors who are members of the Japan
Neurological Society (JNS) have registered online selfreported COI Disclosure Statement Forms through the
website for JNS members.

References
1)

Mutoh T, Ishikawa T, Moroi J, Suzuki A, Yasui N: Impact of
early surgical evacuation of sylvian hematoma on clinical
course and outcome after subarachnoid hemorrhage. Neurol
Med Chir (Tokyo) 50: 200–208, 2010
2) Kazumata K, Kamiyama H, Yokoyama Y, Asaoka K, Terasaka S,
Itamoto, K, Osanai T: Poor-grade ruptured middle cerebral
artery aneurysm with intracerebral hematoma: bleeding
characteristics and management. Neurol Med Chir (Tokyo)
50: 884–892, 2010
3) Saito A, Akamatsu Y, Mikawa S, Sugawara T, Seki H:
Comparison of large intrasylvian and subpial hematomas
caused by rupture of middle cerebral artery aneurysm.
Neurol Med Chir (Tokyo) 50: 281–285, 2010
4)	Ishikawa T: Surgery of ruptured middle cerebral artery aneurysms complicated with intracerebral hematoma. Currently

Practical Neurosurgery 17: 1027–1037, 2007
Nakamura H, Onodera H, Matsumori T, Nakayama H, Sakakibara
Y, Taguchi Y: [A case of sylvian hematoma enlarging 3 days
after neck clipping for the ruptured anterior communicating
artery aneurysm, in the contralateral sylvian fissure to
the operative approach]. Surgery for Cerebral Stroke 38:
119–123, 2010 (Japanese)
6) Findlay JM, Kassell NF, Weir BK, Haley EC Jr, Kongable
G, Germanson T, Truskowski L, Alves WM, Holness RO,
Knuckey NW, Yonas H, Steinberg GK, West M, Winn HR,
Ferguson G: A randomized trial of intraoperative, intracisternal tissue plasminogen activator for the prevention
of vasospasm. Neurosurgery 37: 168–176, 1995
7)	Usui M, Saito N, Hoya K, Todo T: Vasospasm prevention
with postoperative intrathecal thrombolytic therapy: a
retrospective comparison of urokinase, tissue plasminogen
activator, and cisternal drainage alone. Neurosurgery 34:
235–244; discussion 244–245, 1994
8) Kinouchi H, Ogasawara K, Shimizu H, Mizoi K, Yoshimoto T:
Prevention of symptomatic vasospasm after aneurysmal subarachnoid hemorrhage by intraoperative cisternal fibrinolysis
using tissue-type plasminogen activator combined with
continuous cisternal drainage. Neurol Med Chir (Tokyo)
44: 569–575; discussion 576–577, 2004
9)	Ishikawa T, Kamiyama H, Kobayashi N: [Extensive removal
of subarachnoid clot and intracerebral hematoma for poorgrade subarachnoid hemorrhage]. Surgery for Cerebral
Stroke 29: 328–334, 2001 (Japanese)
10) Shimoda M, Oda S, Mamata Y, Tsugane R, Sato O: Surgical
indications in patients with an intracerebral hemorrhage due
to ruptured middle cerebral artery aneurysm. J Neurosurg
87: 170–175, 1997
5)

Address reprint requests to: Noriaki Minami, MD, Department
of Neurosurgery and Stroke Unit, NTT Medical Center,
Higashi-Gotanda 5-9-22, Shinagawa-ku, Tokyo 141-0022,
Japan.
		e-mail: minaminoriaki@gmail.com

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