Case Report

Surgical Venous Drainage Disconnection from Cavernous Sinus Dural Arteriovenous
Fistula and Ruptured Varix
Yusuke Iki1, Yoichi Morofuji1, Chika Somagawa2, Susumu Yamaguchi2, Jumpei Hamabe3, Nobutaka Horie1,
Tsuyoshi Izumo1, Kazuhiko Suyama2, Takayuki Matsuo1

Key words
- Cavernous sinus dural arteriovenous fistula
- Deep middle cerebral vein
- Draining venous disconnection
- Repeat intracranial bleeding

Abbreviations and Acronyms
APhA: Ascending pharyngeal artery
CS: Cavernous sinus
CS dAVF: Cavernous sinus dural arteriovenous
fistula
CT: Computed tomography
DMCV: Deep middle cerebral vein
DSA: Digital subtraction angiography
IPS: Inferior petrosal sinus
MMA: Middle meningeal artery
From the 1Departments of Neurosurgery, Nagasaki University
Graduate School of Biomedical Sciences, Nagasaki;
2
Departments of Neurosurgery, Nagasaki Harbor Medical
Center, Nagasaki; and 3Department of Neurology and
Strokology, Nagasaki Harbor Medical Center, Nagasaki,
Japan
To whom correspondence should be addressed:
Yusuke Iki, M.D.
[E-mail: yusuke.nagasaki1119@gmail.com]
Citation: World Neurosurg. (2020) 137:18-23.
https://doi.org/10.1016/j.wneu.2020.01.058
Journal homepage: www.journals.elsevier.com/worldneurosurgery

- BACKGROUND: Cavernous

sinus dural arteriovenous fistulas (CS dAVFs)
occasionally behave aggressively (e.g., intracranial hemorrhage, venous
infarction, seizures) depending on the drainage flow and presence of a collateral
route of cortical or basal cerebral venous drainage. When a CS dAVF with
aggressive behavior is encountered, a radical cure is required to avoid catastrophic deficits. However, conventional transvenous cavernous sinus (CS)
embolization via the inferior petrosal sinus does not always achieve shunt
obliteration. We herein report a case of surgical venous drainage disconnection
in an 83-year-old woman with a CS dAVF.

- CASE DESCRIPTION: The patient presented with coma and anisocoria due to

intracranial hemorrhage. Because of the patient’s critical condition, we had no
choice but to perform emergency decompressive craniectomy and hematoma
evacuation without detailed preoperative hemodynamic information obtained by
digital subtraction angiography. Postoperative digital subtraction angiography
showed a CS dAVF with retrograde venous drainage of the deep middle cerebral
vein (DMCV) and varix formation in the affected DMCV, causing hemorrhagic
episodes. Five days after admission, the patient’s neurologic state worsened
because of rebleeding from the varix, which had increased in size. The percutaneous transvenous approach failed because of compartmentalization within
the CS. Open surgery was performed; the deep vasculature was exposed by the
transsylvian approach, and the arterialized DMCV was permanently clipped at
its proximal segment with disconnection from the venous varix and fistulous
point. Shunt obliteration was successfully achieved.

Available online: www.sciencedirect.com

- CONCLUSIONS: Surgical venous drainage disconnection from the fistulous

1878-8750/$ - see front matter ª 2020 Elsevier Inc. All
rights reserved.

point may be an alternative radical therapy for CS dAVFs with aggressive
behaviors.

INTRODUCTION
In general, cavernous sinus dural arteriovenous fistulas (CS dAVFs) are recognized
as benign arteriovenous malformations
that sometimes result in ocular neurologic
deficits. In rare cases, CS dAVFs exhibit
aggressive behaviors such as venous
infarction, intracranial bleeding, and seizures. CS dAVFs may have various drainage
routes, and their occasional aggressive
behavior is dependent on the drainage
route. The present report describes a
spontaneous CS dAVF with deep drainage
toward the basal vein of Rosenthal via the
uncal vein, which caused massive intracranial hemorrhage. The standard therapy

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for CS dAVF is currently femoral access
and transvenous cavernous sinus (CS)
embolization via the inferior petrosal sinus
(IPS),1 but this treatment does not apply to
every case. Several access routes have been
reported as alternatives. However, many of
these are advanced and time-consuming
techniques with a potential risk of unpredictable complications. A CS dAVF with
aggressive behavior should be treated by
radical obliteration.2 We herein report a
case of a CS dAVF with repeated
hemorrhagic episodes due to a deep
draining venous varix. The CS dAVF was
successfully obliterated by draining

venous disconnection
clipping.

with

surgical

CASE REPORT
An 83-year-old woman was transferred to
our hospital with a coma, anisocoria, and
left hemiparesis that had developed
immediately after a sudden-onset headache. She had no history of trauma. Head
computed tomography (CT) showed
transtentorial and cingulate herniation
due to subarachnoid hemorrhage, an
intraparenchymal hematoma in the right
temporal lobe, and an ipsilateral subdural

WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2020.01.058

CASE REPORT
YUSUKE IKI ET AL.

RUPTURED CAVERNOUS SINUS DAVF DISCONNECT

Figure 1. (A and B) Admission computed tomography (CT) showed subarachnoid hemorrhage, an
intraparenchymal hematoma in the right temporal lobe, and an ipsilateral subdural hematoma, which
had caused transtentorial and cingulate herniation. (C and D) Concurrent CT angiography revealed a
vascular malformation in which the dilated and tortuous vasculature passed a nearby temporal
hematoma from the right parasellar region to the ipsilateral parietal cortex, which drained into the
superior sagittal sinus. (E) On postoperative day 1, plain CT showed improvement of the cerebral
herniation after decompressive craniectomy and partial hematoma evacuation. (F) On postoperative
day 5, emergency CT showed intraparenchymal rebleeding around the initial temporal hematoma
because of the reruptured venous varix.

WORLD NEUROSURGERY 137: 18-23, MAY 2020

hematoma (Figure 1). The patient was
treated by emergency open surgery
involving hematoma evacuation and
decompressive craniectomy. Preoperative
CT angiography showed dilated and
tortuous vasculature passing near the
temporal hematoma from the right
parasellar region to the ipsilateral
parietal cortex and draining into the
superior sagittal sinus. Although these
findings indicated a vascular anomaly,
detailed hemodynamic information by
digital subtraction angiography (DSA)
was not available preoperatively because
of the patient’s critical condition.
The day after the operation, a CS dAVF
with deep drainage via the uncal vein was
detected by DSA (Figure 2). Right carotid
angiography demonstrated a CS dAVF
fed by the cavernous branch of the
middle
meningeal
artery
(MMA),
ascending pharyngeal artery (APhA),
artery of the foramen rotundum, and
meningohypophyseal trunk, as well as
the left meningohypophyseal trunk. The
early retrograde venous filling drainage
flowed into the superior sagittal sinus via
the right deep middle cerebral vein
(DMCV), forming a venous varix
associated with bleeding (Cognard
classification; type 4). According to Suh
et al,3 this CS dAVF was classified as
“the restricted type.” A microcatheter
(Excelsior SL1018; Stryker Neurovascular,
Fremont, California, USA) was delivered
to the distal segment of the affected
APhA and MMA, individually, and a
detachable coil (Target XL; Stryker
Neurovascular) was used for flow
reduction of feeders. Only transarterial
coil embolization of the APhA and MMA
was performed at that time, and elective
transvenous CS embolization by femoral
access was planned. Five days after
admission,
the
patient
suddenly
exhibited lowering of consciousness and
worsening of the left hemiparesis.
Emergency CT revealed intraparenchymal
rebleeding around the initial temporal
hematoma. Considering the repeated
hemorrhagic episodes associated with
the draining venous varix, we attempted
emergency transvenous CS embolization.
Right cerebral arteriography showed the
CS dAVF, which drained the retrograde
toward the superior sagittal sinus and
already-known draining venous varix,
which had increased in size. A

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CASE REPORT
YUSUKE IKI ET AL.

RUPTURED CAVERNOUS SINUS DAVF DISCONNECT

microcatheter (Marathon; Medtronic,
Minneapolis, Minnesota, USA) was
advanced to the CS via the ipsilateral IPS,
but it did not reach the fistulous point
because of restricted flexibility of the
microcatheter tip, indicating compartmentalization due to development of the
affected CS septum. To avoid further
catastrophic deficits, we altered the strategy by performing surgical disconnection
of the venous drainage from the fistulous
point. The patient was transferred to the
operating room and underwent a second
surgery, during which the hematoma was
evacuated and deep vasculature was
exposed using a transsylvian approach. A
wide opening of the sylvian fissure allowed
us to observe the dilated and arterialized
DMCV was visually recognized as a
subcortical lesion in the temporal lobe
(Figure 3). It flowed out deeply into the
temporal lobe. After subpial dissection
for exposure, surgical clipping was
applied at the exit of the draining vein
from the right CS. Intraoperative
indocyanine green videoangiography
confirmed complete occlusion of the
draining vein. One week after the
surgical
procedure,
DSA
showed
obliteration of the fistulous lesion and
venous varix. The patient gradually
recovered from her mild somnolence and
left hemiparesis (upper and lower limbs,
grade 4/5). Three weeks after the
operation, the patient was transferred to
a
rehabilitation
institute.
No
postoperative recurrence was confirmed
during a 2-year follow-up.

DISCUSSION

Figure 2. Right (A) anteroposterior and (B) lateral external carotid angiography showed a cavernous sinus
dural arteriovenous fistula fed by the cavernous branch of the middle meningeal artery (black small
arrowheads) and artery of the foramen rotundum (black arrows). Feeders were centered on the right
cavernous sinus (asterisk) in the arterial phase. In the late arterial phase, retrograde venous drainage passed
retrograde fashion through the right deep middle cerebral vein with caliber variation (white arrows) and varix
formation (white arrowheads), which drained into the superior sagittal sinus (large black arrowheads). (C) Left
anteroposterior angiography showed that the cavernous sinus dural arteriovenous fistula was fed by the left
meningohypophyseal trunk. (D) Right external carotid angiography immediately after intraparenchymal
rebleeding showed enlargement of the venous varix and constant severe stenosis of its distal segment.

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CS dAVFs with Aggressive Behavior and
Alternatives for Limited Transvenous
Access Route
CS dAVFs rarely present with aggressive
behaviors, most of which are accompanied
by conjunctival hyperemia and concomitant
ocular
dysfunction.4
Clinical
symptoms can vary depending on the
degree and direction of shunt flow5 and
whether the neighboring sinus is affected
by
thrombosis.
Transvenous
CS
embolization via the IPS by the femoral
approach has been described as a
standard therapy. AVFs with retrograde
cortical venous drainage reportedly have
a high risk of early rebleeding within

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CASE REPORT
YUSUKE IKI ET AL.

RUPTURED CAVERNOUS SINUS DAVF DISCONNECT

Figure 3. (A and C) Intraoperative view. (B and D) Intravenous
indocyanine green videoangiography. Black arrows, right internal
carotid artery; white arrow, inferior trunk of right middle cerebral
artery; asterisk, arterialized deep middle cerebral vein (DMCV).
(A) The transsylvian approach was performed. The arterialized
DMCV passed through the subpial layer in the right temporal
lobe. (B) Indocyanine green videoangiography showed an early

2 weeks, with the rebleeding episode
being worse and potentially fatal
compared with the first.2 In our patient,
a repeated hemorrhage episode within a
short duration occurred because of
rupture of the varix of the affected DMCV
of the CS dAVF, which was obliterated by
surgical venous drainage disconnection.
The increased varix size seemed to be a
suggestive finding.6 Severe cases showing
aggressive behavior require immediate
radical cure as soon as possible to avoid
catastrophic progression. However, we
sometimes encounter troublesome cases
with an obstructed route due to
secondary
sinus
thrombosis
or
compartmentation within the CS. Various
alternatives have been reported in
accordance
with
individual
hemodynamics and available venous
access (e.g., superior ophthalmic vein,7,8
foramen ovale,9 and intercavernous
sinus). However, these techniques are
advanced and time consuming and have
a potential risk of unpredictable
complications. Indeed, the percutaneous
approach of the superior ophthalmic
veins has been described, but this
technique has nonnegligible risks of

contrast effect of the DMCV in the arterial phase. (C) The
proximal aspect of the DMCV was exposed by subpial
dissection. (D) After clipping, venous drainage disconnection
was confirmed by the nonenhanced DMCV. (E) Digital
subtraction angiography confirmed the obliteration of fistulous
lesion and venous varix 1 week after surgical venous drainage
disconnection.

intraorbital hematoma and cutaneous
nerve
injuries.
Transarterial
Onyx
embolization of fistulas was recently
highlighted as an alternative treatment of
CS dAVFs.10,11 While Onyx has become
the preferred embolysate, its broad usage
is
limited
by
possible
embolic
complications related to numerous
dangerous anastomoses and occlusion of
the vasa nervorum. Transarterial feeder
occlusion for flow reduction and
radiosurgery have also been established,
but these remain only second-line
therapies.12
CS dAVF with Deep Drainage Toward
DMCV via Uncal Vein
Although the CS has many extracranial
drainage routes, CS dAVFs with aggressive
behavior result from a restricted drainage
route due to secondary thrombosis neighboring the affected CS.6 Arterial blood flow
running through the venous system induces
gradual thickening of the intima,13 leading
to secondary thrombosis and stenosis.
The fluid pressure of venous drainage
increases to a dangerous level as
thrombosis occurs at other sites
(particularly the IPS, superior petrosal

WORLD NEUROSURGERY 137: 18-23, MAY 2020

sinus, and ophthalmic veins). Intracranial
hemorrhagic onset of CS dAVFs with
drainage into the DMCV has rarely been
reported. We reviewed the literature in
PubMed and identified 3 reports6,14,15 (i.e.,
total of 4 cases including our patient). All
patients were women and experienced
onset at >68 years of age. In all patients
except ours, the prehospital prodromal
sign was chemosis. All patients also had
neighboring sinus thrombosis (Table 1).
Our patient exhibited varix formation
associated with the affected draining vein.
Sequential enlargement of a venous varix
with repeat rupture is extremely rare.
Conventional transvenous CS coil
embolization was performed in the other
3 cases; only our patient was treated with
surgical venous drainage disconnection
using a permanent titanium clip. Shunt
obliteration was successfully achieved in
all cases.
Surgical Direct Cannulation for
Retrograde Draining of CS dAVFs
With respect to the surgical treatment of
CS dAVFs, other reports have stated that
microsurgical direct cannulation for
retrograde draining of the superficial

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CASE REPORT
YUSUKE IKI ET AL.

RUPTURED CAVERNOUS SINUS DAVF DISCONNECT

Table 1. Hemorrhagic Onset of Cavernous Sinus Dural Arteriovenous Fistula (CS dAVF) With Retrograde Deep Middle Cerebral Vein
(DMCV) Drainage
First
Author

Age
(year)/ Prodromic
Year Sex
Sign

Types of
Symptoms of
Intracranial Hemorrhagic
Hematoma
Hemorrhage
Onset
Interval Evacuation

Venous
Drainage

Angiographic
Immediate
Features
Treatment Outcome Recurrence

Takazawa 2005 81/F

Chemosis, IPH (putamen)
exophthalmos

Seizure

N/A

No

SOV
(stagnation),
SMCV, DMCV,
BVR

CS coil
Incomplete
embolization obliteration

No

Kiura

Chemosis,
IPH (insular
exophthalmos cortex), SAH

Somnolence,
hemiparesis

1 week

No

SOV and SOV and DMCV CS coil
Complete
DMCV
(stagnation) embolization obliteration
(stagnation),
SMCV

No

2007 82/F

SOV
(stagnation),
agenesis of
BVR

Miyamoto 2009 68/F

Diplopia,
abducent
palsy

IPH (temporal
lobe)

Hemiparesis 1 month

No

DMCV
(stagnation),
BVR

DMCV
(stagnation)

CS coil
Complete
embolization obliteration

No

Present
case

None

IPH (temporal
lobe), SAH,
SDH

Coma,
hemiparesis

Yes

DMCV, IPS
(stagnation)

Varix formation

Surgical
extirpation

No

2019 83/F

N/A

N/A

Interval, interval between prodromic sign and hemorrhage; F, female.

Sylvian vein was a useful procedure of
transvenous CS coil embolization via the
sphenoparietal
sinus.16
With
a
microcatheter advanced into the affected
CS, sinus packing was performed until
shunt obliteration and draining venous
occlusion were obtained. Although the
risk of abducens palsy after sinus
packing
should
be
considered,
transcortical affected sinus packing may
be one of the most reliable alternatives
for a radical cure instead of a failed
conventional transfemoral approach.
Surgical Venous Drainage Disconnection
from CS dAVFs and Varix
In our patient, we performed surgical
clipping for venous drainage disconnection between the fistulous point and
ruptured varix. Even if draining DMCV was
surgically cannulated proximally for CS
packing, catheterization into the CS would
be a challenging procedure because of the
insecure catheter operating in a narrow
and deep space. A pendent access route
unlined with dura mater and complicated
anatomic variations of the uncal vein
result in an extraordinarily difficult catheter operation.17 Furthermore, retrograde
forcible catheterization of arterialized
veins is challenging and associated with
a risk of perforation, leading to
iatrogenic rebleeding. Fortunately, by

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surgical occlusion of the draining vein,
shunt obliteration was achieved in the
short-term DSA follow-up. As to
long-term outcome after endovascular
treatment of CS dAVFs, eliminating
cortical venous reflux and major retrograde shunt flow has been reported to be
equivalent to immediate shunt disappearance elicited by tight coil packing of the
CS.18 Some reports have stated that
drainer occlusion would trigger opening
of the sleeping channels, resulting in
dangerous drainage. Semiquantitative
flow analysis during indocyanine green
videoangiography may facilitate the
identification of arterialized veins and
shunt obliteration.19,20 In addition,
intraoperative cerebral angiography may
be useful for simple and repeatable
evaluation of hemodynamic alternations.

CONCLUSION
CS dAVFs with massive intracranial hemorrhage require immediate hematoma
evacuation and radical treatment for shunt
obliteration. CS dAVFs often present
unique treatment challenges depending
on the anatomy and pattern of venous
drainage. Our report illustrates that
surgical venous drainage disconnection as
a last resort can be a valuable radical

alternative for CS dAVFs with limited
venous access.
ACKNOWLEDGMENT
We thank Angela Morben, DVM, ELS,
from Edanz Group (https://en-authorservices.edanzgroup.com/) for editing a
draft of this manuscript.
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Conflict of interest statement: The authors declare that the
article content was composed in the absence of any
commercial or financial relationships that could be construed
as a potential conflict of interest.
Received 16 December 2019; accepted 8 January 2020
Citation: World Neurosurg. (2020) 137:18-23.
https://doi.org/10.1016/j.wneu.2020.01.058
Journal homepage: www.journals.elsevier.com/worldneurosurgery
Available online: www.sciencedirect.com
1878-8750/$ - see front matter ª 2020 Elsevier Inc. All
rights reserved.

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