Case Report

Contralateral extensive cerebral hemorrhagic
venous infarction caused by retrograde venous
reflux into the opposite basal vein of Rosenthal in
posttraumatic carotid-cavernous fistula: A case
report and literature review

Interventional Neuroradiology
0(00) 1–13
! The Author(s) 2018
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DOI: 10.1177/1591019918776615
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Prasert Iampreechakul1 , Adisak Tanpun1, Punjama Lertbusayanukul2
and Somkiet Siriwimonmas3

Abstract
We describe a patient with traumatic carotid-cavernous fistula (CCF), subsequently developing contralateral extensive
hemorrhagic venous infarction from retrograde venous reflux into the opposite basal vein of Rosenthal. A 54-year-old
woman was involved in a motor vehicle accident and sustained severe traumatic brain injury. Two months later, she
developed bilateral proptosis and audible bruit. Magnetic resonance imaging (MRI) and magnetic resonance angiography
(MRA) of the brain demonstrated the right direct CCF. Fluid-attenuated inversion recovery (FLAIR) images showed a small
hyperintense area at the left basal ganglia. Ten days later, she developed right-sided grade 2/5 hemiparesis, facial upper
motor neuron weakness, and cognitive impairment. Follow-up MRI showed significant progression of hyperintensities
involving the left-sided centrum semiovale, basal ganglia, thalamus, midbrain, pons, cerebellum, basal frontal, temporal
lobes, especially subcortical white matter on FLAIR images, and multiple hypointense foci of hemorrhagic component on
T2*-weighted gradient-echo images, representing hemorrhagic venous infarction. While waiting for embolization, she
rapidly developed right hemiplegia and aphasia, and became somnolent. Under general anesthesia, emergency endovascular treatment was performed successfully to obliterate the fistula without surgical intervention. Five months after
endovascular treatment, MRI and MRA confirmed no residual fistula and revealed nearly complete resolution of abnormal
increased signal intensity. In the present case, the factors related to the presence of this rare condition were absence of the
ipsilateral basal vein of Rosenthal (BVR), occlusion of posterior segment of the contralateral superior petrosal sinus, and a
developed uncal vein with hypoplastic second and third segments of the contralateral BVR.

Keywords
Venous infarction, venous congestion, traumatic carotid-cavernous fistula, direct carotid-cavernous fistula, basal vein of
Rosenthal
Received 18 March 2018; accepted 22 April 2018

Introduction
A direct carotid-cavernous fistula (CCF), that is,
Barrow type A, is defined by direct high-flow connection between the cavernous segment of the internal carotid artery (ICA) and the cavernous sinus (CS).1 Direct
type A CCF has been classified into traumatic, including iatrogenic, or spontaneous fistula. The traumatic
CCF, the most common type, usually occurs from a
motor vehicle accident with closed traumatic brain
injury associated with a basilar skull fracture.2,3 The
spontaneous CCF usually results from rupture of a
pre-existing intracavernous carotid aneurysm, and
may rarely be associated with intrinsic weakness of

the vessel wall in some diseases, such as Ehlers–
Danlos type IV and fibromuscular dysplasia.4
1

Department of Neurosurgery, Prasat Neurological Institute, Bangkok,
Thailand
2
Department of Neuroradiology, Prasat Neurological Institute, Bangkok,
Thailand
3
Department of Radiology, Bumrungrad International Hospital, Bangkok,
Thailand
Corresponding author:
Prasert Iampreechakul, Department of Neurological Surgery, Prasat
Neurological Institute, 312 Ratchawithi Road, Khwaeng Thung Phaya Thai,
Bangkok 10400, Thailand.
Email: bangruad@hotmail.com

2
The most common clinical manifestations, that is,
pulsating proptosis, chemosis, and an audible bruit,
depend on the venous drainage. Due to drainage
through intercavernous sinuses across the midline, the
ocular symptoms may occur on the opposite side to the
fistula or bilaterally.5 Rarely, aggressive neurologic
symptoms, especially deterioration of consciousness,
may also develop due to cerebral ischemia and/or
hemorrhage.6,7
Cerebral ischemia in traumatic or direct CCF may
result from arterial or venous cause. The arterial infarction from stealing of blood flow by direct CCF usually
occurs in the ipsilateral carotid territory.8 The steal
phenomenon can cause life-threatening or fatal complications when collateral circulation from the circle of
Willis is insufficient.9 On the other hand, venous congestion from retrograde cortical or deep venous reflux
in the direct CCFs in the area of the venous territories,
resulting in cerebral hemorrhage or less common
venous infarction.10,11 Intracerebral hemorrhage from
direct CCF may be considered rare, with only 1% incidence from the study of Lewis et al.2 Intracerebral hemorrhagic venous infarction in direct CCF is much rarer
than spontaneous hemorrhage.12
We describe a case of traumatic CCF with contralateral extensive cerebral hemorrhagic venous infarction due to retrograde venous reflux into the opposite
basal vein of Rosenthal (BVR), which is an extremely
rare complication. We also review literature of abnormal appearance in computerized tomography (CT)
scan or magnetic resonance imaging (MRI) of brain
edema or venous congestion with or without hemorrhagic changes from direct CCFs.

Case report
A 54-year-old woman was involved in a motor vehicle
accident and sustained head trauma resulting in unconsciousness for a few hours. In the time after regaining
consciousness, she had bleeding from the nostrils and
ears without neurological deficits. A CT scan of the
head showed acute thin subdural hematomas along
both sides of the falx cerebri, skull fracture of the
right parietal bone and multiple fractures of the skull
base and facial bone, including bilateral zygomatic
arches, bilateral lateral orbital walls, superior and lateral wall of the right sphenoid sinus, and lateral wall of
the left maxillary sinus. Pedicle screws fixation was performed for correction of unstable thoracolumbar fractures. She gradually recovered without neurological
deficits and was discharged home 10 days later. Two
months later, she developed redness of both eyes, bilateral proptosis in association with chemosis in both eyes,
bilateral audible bruit, and binocular horizontal diplopia. She went back to check with the ophthalmologist
in the previous hospital, and was sent to our institute.
Ophthalmic examination revealed bilateral proptosis
more prominent on the right side, chemosis with conjunctival injection of both eyes, and normal findings on

Interventional Neuroradiology 0(00)
pupillary examination. Visual acuity was 20/50 in the
right eye and 20/40 in the left. There was a limitation to
abduction in the right eye. A bruit was audible over
both eyes and in the right temporal region. She had
no muscle weakness or sensory loss during physical
examination. Cerebral angiography and simultaneously
performing the endovascular treatment were scheduled
in the next three weeks. MRI and magnetic resonance
angiography (MRA) of the brain (Magnetom Skyra 3T;
Siemens, Erlangen, Germany) with a complete
sequence of images obtained before hospital discharge
demonstrated the right direct CCF located at the posterior genu of the cavernous carotid artery. Fluid-attenuated inversion recovery (FLAIR) images showed a
small hyperintense area at the left putamen, caudate
nucleus, and internal capsule, indicating edema, congestion, or early venous infarction (Figure 1(a)).
Time-of-flight (TOF) MRA indicated an enlarged left
BVR on the opposite side to the fistula (Figure 2(a)).
T2-weighted images also revealed the abnormal flow
void corresponded to venous anastomoses of the left
peduncular vein, BVR, and deep middle cerebral vein
(DMCV), respectively (Figure 3(a)). Susceptibilityweighted imaging (SWI) demonstrated hyperintensity
in the left BVR, representing arterialized blood flow
of this draining vein (Figure 3(b)). Ten days later
after staying at home, she developed right-sided grade
2/5 hemiparesis, facial upper motor neuron weakness,
and cognitive impairment. She went back again to the
local hospital and was sent to obtain MRI of the brain
(Magnetom Symphony 1.5T; Siemens, Erlangen,
Germany) for evaluation of these problems. The findings demonstrated significant progression of hyperintensities involving the left-sided centrum semiovale,
basal ganglia, thalamus, midbrain, pons, cerebellum,
basal frontal, temporal lobes, especially subcortical
white matter on FLAIR images (Figure 1(b) and
Figure 4(a)), an enlarged left BVR and perimesencephalic veins on TOF-MRA (Figure 2(b)), and multiple
hypointense foci of hemorrhagic component on T2*weighted gradient-echo images, representing hemorrhagic venous infarction. The disabled patient was
transferred to our institute 10 days later. While waiting
for embolization, she rapidly developed right hemiplegia and aphasia, and became somnolent. A CT scan of
the brain obtained before treatment showed progression of hemorrhagic venous infarction at the leftsided basal ganglia, thalamus, brainstem, cerebellum,
frontal, and temporal lobes with a small acute subcortical hemorrhage at the left temporal lobe, resulting in
diffuse brain swelling and midline shift (Figure 5(a)).
Emergency endovascular treatment was performed by
using a biplane flat panel detector angiographic system
(Axiom Artis dBA; Siemens, Erlangen, Germany)
under general anesthesia. Cerebral angiography
revealed direct CCF from the inferomedial aspect of
the posterior genu of the right cavernous carotid
artery. Multiple venous drainages included right superior ophthalmic vein (SOV), right inferior petrosal sinus

Iampreechakul et al.

3

Figure 1. Sequential axial fluid-attenuated inversion recovery (FLAIR) images at level of pons to basal ganglia (BG) obtained at two
months after the accident (a), ten days later (b), and five months after embolization (c) demonstrated rapid progression from a small
hyperdense area at left BG to extensive hyperintensity involving the left side of BG, thalamus, basal frontal lobe, temporal lobe, midbrain,
and pons, representing extensive venous infarction in a period of ten days. Five months after endovascular treatment, FLAIR images
confirmed nearly complete resolution of abnormal increased signal intensity.

(IPS), and basilar venous plexus, and posterior intercavernous sinus draining into the left CS. The subsequent
venous drainages from the left CS ran anteriorly into
the left SOV, posterolaterally into residual segment of
the proximal superior petrosal sinus (SPS) with subsequent draining into the left superior petrosal vein
(SPV) entering further into the veins of cerebellar
hemisphere, posteriorly into bridging vein with draining into the left transverse pontine vein (TPV) also
opening into left cerebellar veins, and superiorly into
the dilated left uncal vein connecting with the left
BVR. From anastomosis of the left uncal vein and
the BVR, the drainages then ran anteriorly into the
residual dilated vein of the first segment of the left
BVR, and posterosuperiorly to the great vein of
Galen through multiple hypoplastic portions of the

second and third segments of BVR. There was antegrade flow of the right ICA filling into the right anterior, and middle cerebral territories (Figure 4(b) and
Figure 6(a) to (d)). Another retrograde venous drainage detected by angiographic CT in maximum intensity projection (MIP) reformatted images revealed
venous reflux from the right SPS running into the
right TPV through the right SPV, and then turning
around anteromedially through the anterior and lateral pontomesencephalic veins up to the right peduncular vein crossing the midline via the interpeduncular
or posterior communicating vein to the left peduncular vein connecting posteriorly into the left perimesencephalic vein and terminating to the dilated left BVR
joining with the route from the left uncal vein (Figure
7). Transarterial embolization with one detachable

4

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Figure 2. Axial time-of-flight magnetic resonance angiography obtained at two months after the accident (a), ten days later before
embolization (b), and five months after embolization(c) confirmed the disappearance of an enlarged left basal vein of Rosenthal (arrow
heads) after obliteration of the fistula.

Figure 3. (a) Axial T2-weighted magnetic resonance imaging revealed the flow voids of venous anastomoses of the left peduncular vein
(white arrow head), the left basal vein of Rosenthal (BVR) (black arrow head), and the left deep middle cerebral vein (white arrow). (b)
Axial susceptibility-weighted imaging demonstrates hyperintensity in the left BVR (black arrow head), representing arterialized blood flow
of this draining vein.

balloon (Goldbal; Balt Extrusion, Montmorency,
France) was unable to complete obliteration of the
fistula. Thus, this balloon was placed to close only
posterior
drainage
(Figure
8(a)
and
(b)).
Unfortunately, occlusion of the right ICA occurred
after inflation of another balloon (Figure 8(c)). Even
though the left internal carotid and vertebral showed
collateral circulation of the right anterior cerebral
artery via anterior communicating artery from the
left ICA and the right middle cerebral artery via the
right posterior communicating artery from the right
posterior cerebral artery (Figure 6(e) and (f)), these
findings could not guarantee that the collateral circulation was adequate. Transvenous embolization was
subsequently performed via the left IPS by using the
fibered interlock detachable coils (Boston Scientific

Corporation, Natick, MA, USA) densely packing in
the proximal dilated right SOV and posterior part of
the right CS (Figure 8(f)). A control right ICA injection immediately after embolization confirmed complete obliteration of the fistula with preservation of
the flow in the parent artery (Figure 8(d) and (e)).
Following occlusion of the fistula, a bruit entirely disappeared, and ocular symptoms significantly
improved. Immediate assessment of the patient
revealed improvement of consciousness and muscle
power. We decided to use medication for reduction
brain swelling instead of performing decompressive
surgery.
Follow-up sequential CT scans of the brain demonstrated gradual resolution of extensive hemorrhagic
venous infarction until nearly complete disappearance

Iampreechakul et al.

5

Figure 4. Before embolization, axial fluid-attenuated inversion recovery (FLAIR) MR image (a) and axial maximum intensity projection
(MIP) reformatted image of angiographic CT (b) at the level of cerebellum revealed multiple left-sized dilated cerebellar veins and a small
hyperintensity (black arrow head) compatible with edema or venous congestion at left deep cerebellar white matter. Five months after
embolization, coronal T2*-weighted gradient-echo image (c) shows a small hypointense foci of previous hemorrhage (white arrow head).

Figure 5. Axial computerized tomography (CT) scan obtained before embolization (a) showed extensive parenchymal edema at the left
side of the basal ganglia, thalamus, frontal, and temporal lobes with a small acute subcortical hemorrhage at the left temporal lobe,
resulting in diffuse brain swelling and midline shift. Axial CT scans obtained at one day (b), four days (c), two weeks (d), three weeks (e),
and one month (f) following embolization revealed that extensive hemorrhagic venous infarction gradually resolved until nearly complete
resolution after obliteration of the fistula.

within one month (Figure 5(b) to (f)). MRI and MRA
of the brain obtained at five months after endovascular
treatment confirmed no evidence flow-related enhancement or early enhancement of the right CS on either
three-dimensional TOF-MRA or contrast-enhanced

MRA (Figure 9). FLAIR images revealed nearly complete resolution of abnormal increased signal intensity
of the left side of basal ganglia, thalamus, basal frontal
lobe, temporal lobe, midbrain, and pons (Figure 1(c)).
TOF-MRA also confirmed the disappearance of an

6

Interventional Neuroradiology 0(00)

Figure 6. Anteroposterior ((a) and (c)) and lateral ((b) and (d)) views in early ((a) and (b)) and late ((c) and (d)) arterial phases of the right
internal carotid artery (ICA) injection demonstrate antegrade flow in the right ICA distal to the direct carotid-cavernous fistula with retrograde
drainage into the right superior ophthalmic vein (SOV), the right inferior petrosal sinus, basilar venous plexus, and crossing to the left
cavernous sinus (CS) via the posterior intercavernous sinus. The left CS further drains into the left SOV and the left basal vein of Rosenthal
(BVR) via the left uncal vein (black arrow heads), running superiorly into the great vein of Galen and anteriorly to the residual dilated vein of
the first segment of the left BVR. There were hypoplastic portions (white arrow heads) at the second and third segments of the left BVR.
Another route of retrograde venous reflux opens into proximal part of the left superior petrosal sinus, where the residual part was occluded
(asterisks), then turns medially to the left superior petrosal vein draining into left cerebellar veins. Anteroposterior views of the left ICA (e) and
left vertebral artery (f) injections reveal collateral circulation of the right anterior cerebral artery via anterior communicating artery from the
left ICA and the right middle cerebral artery via the right posterior communicating artery from the right posterior cerebral artery.

enlarged left BVR after obliteration of the fistula
(Figure 2(c)). T2*-weighted gradient-echo images
showed multiple small hypointense foci of an old hemorrhage at the right parietal white matter and left deep
cerebellar white matter (Figure 4(c)). At six months’
follow-up, ophthalmic examination revealed complete
resolution of proptosis, chemosis, and diplopia without
secondary glaucoma. Visual acuity with correction was
20/25 in the right eye, and 20/20 in the left. Nine
months after embolization, the patient had recovered

completely from aphasia. The time to nearly complete
recovery of the right-sided weakness was two years. She
is able to independently perform activities of her
daily living. However, she still has mild cognitive
impairment.

Discussion
Since 1978, Ambler et al.13 demonstrated unusual serial
angiographic and neurological findings of right atypical

Iampreechakul et al.

7

Figure 7. Axial maximum intensity projection reformatted images of angiographic computerized tomography at the level of pons (a) and
(b) to midbrain; (c) and (d) reveal another retrograde venous reflux from the right superior petrosal sinus (thick white arrow) running into
the right transverse pontine vein (white asterisk) via the left superior petrosal vein (white arrow heads), and then turning around
anteromedially via the anterior pontomesencephalic veins (not shown) up to the right peduncular vein crossing the midline via the
interpeduncular or posterior communicating vein (thin white arrow) to the left peduncular vein (black arrow head) terminating at the
dilated left basal vein of Rosenthal (thick black arrows) on the opposite site.

Figure 8. Lateral views of the right internal carotid artery (ICA) injections (a) and (b) reveal incomplete closure of anterior and posterior
drainages of the traumatic carotid-cavernous fistula with only one detachable balloon via transarterial approach. Therefore, only the
posterior drainage was closed initially, and another balloon was delivered to close the residual drainage. Lateral view of the right
common carotid artery injection (c) shows sacrifice of the right ICA after inflation of another balloon. Then, transvenous approach was
performed using fibered coils for occlusion of anterior drainage. Anteroposterior (d) and lateral (e) views of the right ICA injections
confirm complete obliteration of the fistula with preservation of flow in the parent artery. Lateral radiograph of the skull (f) demonstrates
the balloon and pack of deposited coils.

traumatic CCF in middle-aged woman with bilateral
CCFs. There was progressive high pressure reflux into
the sphenoparietal sinus, middle cerebral vein, and
BVR, as well as diminished intracerebral arterial opacification. They believed that progressive intracranial
arterial insufficiency accompanied by simultaneous
venous hypertension may cause delayed clinical deterioration in four months and death. From gross and
microscopic examination, right parasylvian, orbital

gyri, and rostral pons, especially subcortical white
matter, were swollen and boggy with elliptical and
petechial hemorrhage associated with profoundly
hypertrophied pial veins. In our opinion, these findings
may correspond with extensive hemorrhagic venous
infarction as in the current case.
Five years later, Vaghi et al.14 reported unusual
appearances, that is, hyperdense lesion with perifocal
hypodensity and mass effect of frontoparietal area, on

8

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Figure 9. Anteroposterior view of three-dimensional time-of-flight magnetic resonance angiography obtained five months after
embolization confirmed no residual right carotid-cavernous fistula.

a CT scan in a case of traumatic CCF. They speculated that these findings could be hemorrhagic venous
infarction due to coincidence between the gradual
regressions of the CT findings with the angiographic
disappearance of the dilated veins after complete
occlusion of the direct fistula by the detachable
balloon.
We reviewed the literature of cerebral venous infarction or edema caused by venous congestion from direct
CCFs. The data, including the sex, age, cause and side
of fistula, location and side of brain edema, sinuses
and/or veins involved, presence of hemorrhage, methods of treatment, and outcome of patients are described
in Table 1.6,8,14–23 Including our one case, there were
14 cases (7 females and 7 males) with a median age of
48 years (range 24–88 years). Out of 14 fistulas, 8 were
the result of traumatic causes, 5 spontaneous, and
1 iatrogenic. In one case of spontaneous CCFs an
underlying connective tissue disorder was suspected.18
There were 6 fistulas located on the right side, and 8 on
the left. Brain edema occurred on the same side in
9 cases, bilateral or diffuse on brainstem in 4, and
contralateral in only 1 (i.e. our case). There were extensive edema (involving cerebral cortex, basal ganglia,
thalamus, brain stem, and/or cerebellum) in 3 cases,
including our case; only cerebral cortex in 2; brain
stem and thalamus in 2; only brain stem in 4; only
cerebellum in 1; brain stem, cerebellum and spinal
cord in 1; and brain stem and spinal cord in 1.
Venous infarction or edema presumably related to the
BVR occurred in 6 cases, DMCV and/or superficial
middle cerebral vein (SMCV) in 2, veins of brain stem
in 6, uncal vein in 4, veins of cerebellum in 4, and veins
of spinal cord in 3. Occlusion or stenosis of posterior
segment of the SPS was found in 6 cases, including our
case. Three of these 6 cases had no stenosis or occlusion
of the SPS on prior angiography.8,16 There was no filling of the SPS in 5 cases. No apparent anterior venous
drainage, that is, SOV, was observed in 2 cases.19,20

Hemorrhagic transformation occurred in 8 cases,
including our case.
After the onset of symptoms of direct CCFs, aggressive symptoms can develop within a few days, weeks,
months, or years. Aggressive symptoms included headache, dysarthria or aphasia, hemiparesis or hemiplegia,
hemiparesthesia, tetraparesis, cerebellar ataxia, cognitive impairment, respiratory insufficiency, and deterioration of consciousness. Three patients developed
aggressive symptoms after incomplete treatment by
embolization or surgical bypass. For almost all patients
the symptoms finally developed into life-threatening
conditions.
Hemorrhagic venous infarction is the infarction
accompanied by hemorrhagic transformation. It may
be secondary to increased venous pressure or venous
congestion from the redirection of the venous outflow
through the valveless veins or sinuses after some conditions, for example, sacrificing of some draining veins,
thrombosis of the CS or draining veins, or stenosis of
venous outlet.8,23,24
Kamio et al.23 demonstrated that cerebellar hemorrhage with surrounding edema resulted from direct
CCF after performing maxillary surgery involving sacrifice of ipsilateral facial vein and pterygoid plexus.
Sacrifice of these veins may alter the venous drainage
and increase venous pressure in infratentorial veins. In
addition, Aldea et al.20 reported spontaneous direct
CCF from a ruptured large cavernous carotid artery
aneurysm blocking ipsilateral anterior venous drainage,
producing rerouted retrograde flow into SPS, leading to
hemorrhagic venous infarction of brainstem and cerebellum. Similarly, Herrera et al.19 proposed that spontaneous thrombosis of the anterior drainage with
subsequent development of reflux into the peripontomesencephalic and perimedullary veins could explain
progressive tetraparesis and respiratory insufficiency.
From knowledge of the embryologic processes, the
SPS develops primarily as a drainage route from the

M/39

M/27

F/55

F/45
M/51
M24

F/63

F/54

Bussière, 2009 18

Herrera, 2011 19

Aldea, 2011 20

Ract, 2014 21
Yu, 2015 6
Ryu, 2017 22

Kamio, 2017 23

Present study, 2018

Trauma

Iatrogenic

Trauma
Trauma
Trauma

Spontaneous

Trauma

Spontaneouse

Spontaneous
Spontaneous

R

L

R
R
R

L

R

L

L
L

L

R
L
L

Fistula
side

L

R
R
R, L
(ventral)
L

R, L
(diffuse)
R, L
(dorsal)
L

R, L
(diffuse)
L
L

R
L
L

Edema side

FL, TL, BG, T,
MB, P, CE

CE

TL, BG, MB, P, CP
P
MB

P, CE, SC

MB, P, ME, SC

P
FL, TL, BG,
T, MB, P
P, ME

MB, T

FL, PL
TL
MB, T

Location

Yes
Yes

SPS,c PV, UV, DMCV, Ped.V,
IPed.V, BVR, ISV, CV

No
No
No

Yes

No

No

SPS,c PV, CV

SPS,a Ped.V, APMV,
AMV, CV, ASV
SPS,c PPMV, PMV
(No SOV)
SPS, CV, ASV
(No SOV)
SPS,a UV, BVR, ISV
SPS,a TPV, APMV, BVR
SPS,a BVR, UV, IPed.V

Yes
Yes

No

SPS,c IPS, UV, BVR
SPS,c ATPV
N/A

Yes
Yes
Yes (TL)

Hemorrhage

SPS,a SMCV, DMCV
N/A
SPS,c IPS, BVR

Involved sinuses/veins

Balloon (A)
Coils (V)

Sacrifice by
balloons (A) (1st)
Sacrifice by coils (A)
Balloon (A)
Coils (V) (1st)d
Proximal trapping (3rd)
Sacrifice (A) (V)

Coils (A)

Balloon

Coils (V) (1st)d
Sacrifice (2nd)
Coils (A)
N/A

Balloon
Balloon
Balloon (3rd)

Endovascular treatment

No

No
No
Bypass/ distal
trapping (2nd)
No

DC/EH (2nd)

No

No

No
N/A

No
No
Bypass (1st)d
DC/EH (2nd)
No

Surgery

GR
VL (L)
GR

GR
GR
GR

GR

PR

GR

GR
N/A

GR

GR
N/A
GR

Outcome

b

No filling of the SPS on angiography.
Details from only English abstract.
c
Stenosis or occlusion of posterior segment of the SPS.
d
Incomplete treatment.
e
Underlying connective tissue abnormality.
A: arterial approach; AMV: anterior medullary veins; APMV: anterior pontomesencephalic vein; ASV: anterior spinal vein; ATPV: anterior transpontine vein; BG: basal ganglia; BVR: basal vein of Rosenthal; CE: cerebellum;
CP: cerebellar peduncle; CV: cerebellar veins; DC: decompressive craniectomy; DMCV: deep middle cerebral vein; EH: evacuation of hematoma; F: female; FL: frontal lobe; GR: good recovery; IPed.V: interpeduncular vein;
IPS: inferior petrosal sinus; ISV: inferior striate veins; L: left; M: male; MB: midbrain; ME: medulla; N/A: data not available; P: pons; Ped.V: peduncular vein; PL: parietal lobe; PMV: perimedullary vein; PPMV: peripontomesencephalic vein; PR: partial recovery; PV: petrosal vein; R: right; SC: spinal cord; SMCV: superficial middle cerebral vein; SOV: superior ophthalmic vein; SPS: superior petrosal sinus; T: thalamus; TL: temporal lobe;
TPV: transverse pontine vein; UV: uncal vein; V: venous approach; VL: visual loss; 1st: first procedure; 2nd: second procedure; 3rd: third procedure.

a

F/41
F/88

Trauma

M/26

Murata, 2003 16
Ohshima,b 2006 17

Trauma
Spontaneous
Trauma

M/54
F/74
M/36

Vaghi, 1983 14
Kasama,b 1990 15
Teng, 1991 8

Cause

Sex/Age

Authors

Table 1. Literature review of cerebral venous infarction or edema caused by venous congestion from direct carotid-cavernous fistulas.

Iampreechakul et al.
9

10
petrosal vein, collecting blood from the anterior cerebellar and brainstem venous drainage systems.25
Therefore, the SPS provides an important route for
infratentorial venous drainage from the brainstem and
cerebellum via the petrosal vein.23 SPS was divided into
anterior and posterior segments.26 Hypoplasia or occlusion of this sinus may promote venous congestion of
the venous system in surrounding brainstem, leading to
edema and/or hemorrhage of brainstem and/or
cerebellum.8,16,19,23
Importantly, incomplete closure of direct CCF
should be avoided due to the possibility of the rerouting
of venous drainage into cortical or deep venous systems, leading to cerebral edema and/or hemorrhage,
rather than resolution of the fistula. Further complete
obliteration of the residual fistula or drainage should be
achieved when possible.8,22
To understand the possible mechanisms of cerebral
hemorrhagic venous infarction from the CCF, it is
important to know the essential anatomy of the BVR,
basal cerebral venous drainage of the CS, basal cranial
venous sinus, and bridging veins communicating
between the CS and the brain.
Based on a venous study by Huang,27 the BVR was
divided into three segments, that is, anterior, middle,
and posterior. The first segment (striate segment), passing posteromedially above the uncus to reach the
anterior part of the cerebral peduncle, is formed
mainly by the union of the DMCV and its insular tributaries, the inferior striate veins, the olfactory vein,
the orbitofrontal vein, and the anterior cerebral vein.
The second segment (peduncular segment), running further posterolaterally around the most lateral portion of
the cerebral peduncle and turning posteromedially to
the lateral mesencephalic sulcus, is formed mainly by
the union of the peduncular vein, the inferior thalamic
vein, the inferior ventricular veins, and the uncal vein.
Last, the third segment (posterior mesencephalic segment), joining the great vein of Galen or the posterior
portion of the internal cerebral vein by running posteromedially and superiorly, is formed mainly by the
union of the lateral mesencephalic vein (LMV), the lateral atrial vein, the medial occipitotemporal vein, the
posterior longitudinal hippocampal vein, and the posterior thalamic vein.
During late embryogenesis after regression of the
tentorial sinus, the BVR was formed by four groups
of afferent veins described by Terbrugge and
Lasjaunias.28 First, the telencephalic group receives
drainage from the olfactory vein, the inferior frontal
vein, the anterior communicating vein, inferior striate
veins, and the uncal vein. Second, the diencephalic
group carries blood from the hypothalamic vein, the
hippocampal vein, the inferior thalamic vein, the inferior ventricular vein, the inferior choroidal vein, the posterior communicating vein, the peduncular vein, the
anterior pontomesencephalic vein (APMV), and the
infratemporal vein. Third, the tegmental group drains
blood from the LMV, and the posterior mesencephalic

Interventional Neuroradiology 0(00)
vein. Last, the tectal group collects blood from the
tectal vein, the tectogeniculate vein, and the precentral
vein.
The venous drainage from the brain mainly drains
into the CS through bridging veins including the
SMCV, SPV, and bridging vein from the brainstem.29
The petrosal vein is a bridging vein connecting and
receiving venous blood from veins of cerebellum and
brainstem by connection with the third segment of the
BVR through the LMV and with the APMV through
the TPV. The bridging veins from the posterior part of
the CS may connect to the medial APMV or TPV.20,30–32
The inferior striate veins drain a large area above the
anterior perforated substance including the putamen,
caudate nucleus, and internal capsule.33 In the present
case, the presence of abnormal hyperintensity signal on
FLAIR images of the putamen, caudate nucleus, and
internal capsule represent radiographic evidence of
brain edema resulting from venous congestion of tributaries of the inferior striate veins draining into the
BVR.
To the best of our knowledge, our patient is the
first report of a posttraumatic CCF creating contralateral cerebral hemorrhagic venous infarction. Lau
et al.34 reported an atypical case of the left spontaneous
direct CCF causing venous hypertension in the
right SMCV from cross-flow through intercavernous
sinus, resulting in contralateral intracerebral hematoma. Interestingly, this fistula resolved spontaneously
without intervention. Similarly, hemorrhagic venous
infarction in the current case occurred opposite to the
direct fistula through posterior intercavernous sinus and
also the posterior communicating vein. An anastomotic
venous circle of veins was described by Cullen et al.35
This venous circle is formed by the anterior and posterior communicating veins, linking bilateral BVRs across
the midline, representing a route of contralateral venous
drainage. It may become an essential route for the
absence of segments of the BVR or high-flow arteriovenous shunts accessing the deep venous system. Our case
may be the suitable example of this speculation due to
the absence of the right BVR in high-flow traumatic
CCF, resulting in redirection of venous drainage to the
contralateral BVR.
Fortunately, our patient has regained almost a complete recovery, both clinically and radiologically, from
the life-threatening condition after performing endovascular treatment without surgical intervention, teaching us to know about the natural history of this very
rare consequence of traumatic CCF. However, it is
imperative to obliterate the fistula before hemorrhagic
transformation when brain edema caused by venous
congestion from direct traumatic CCF is early diagnosed. Early diagnosis can be achieved by FLAIR
and SWI images.
Abnormal hyperintensity within the venous structures on the SWI images represents arterialized blood
flow in the veins from arteriovenous shunting in vascular malformations of the brain or from cortical venous

Iampreechakul et al.
reflux in dural arteriovenous fistulas (DAVFs).36,37
However, we also found abnormal hyperintensity and
flow void of the left BVR on TOF and T2-weighted
images, respectively.
The BVR and veins around brainstem are often difficult to identify on routine angiography. Using angiographic CT with a flat panel detector, these small veins
can be visible in multiplanar reformations and MIP
reformatted images as shown in the present case.
Based on the secondary longitudinal anastomoses
between embryonic veins (i.e. the deep telencephalic
vein, ventral and dorsal diencephalic vein, and mesencephalic vein) by Padget,25 Suzuki et al.38 classified
variations of the BVR using three-dimensional CT
angiography into five drainage pathways including
draining to the great vein of Galen, to the CS or sphenoparietal sinus, to the SPS through the LMV, to the
SPV through the peduncular vein, and finally to the
transverse or straight sinus through the primitive tentorial sinus. In the present case, the BVR not only
drains into the great vein of Galen, but also connects
the CS through the dilated uncal vein. By the axial
angiographic CT in MIP reformatted images, we
found another anastomosis to the peduncular vein,
which was rarely seen in the study of Suzuki et al.38
Compared with low-flow fistulas, CS DAVFs
(CSDAVFs) may also rarely manifest as venous infarction and/or intracerebral hemorrhage.7,30 Miyamoto
et al.30 found that angiographic risk factors were cortical venous drainage only, ectasia of the draining vein,
agenesis of the second and third segment of the BVR,
and thrombosis of the SOV, distal segment of the SPS,
and distal cortical vein drainage. From study of anatomical variations of the uncal vein in normal and
CSDAVFs by Ide et al.,7 the uncal vein is a small cerebral vein communicated between the CS and BVR. It
may terminate into the CS or SMCV. The connection
between the first and second segments of the BVR is
usually hypoplastic when there is a well-developed
uncal vein. The results of our literature search found
that there was a dilated uncal vein in four cases, including our case.8,21,22 However, a hypoplastic segment of
the BVR was shown on angiography only in our case
and Ract et al.’s case.21 Shimada et al.26 studied visualization and hemodynamic features of the SPS in normal
and CSDAVFs. The SPS frequently has segmentally
hypoplastic features on angiography. A higher risk of
venous reflux into the cerebellopontine veins occurred
in CSDAVFs associated with hypoplastic posterior segment of the SPS. Similarly, our case and another five
cases from our review had occlusion or hypoplastic posterior segment of the SPS, resulting in edema of brainstem, cerebellum, and/or spinal cord.8,16,19,23 Three of
five cases were confirmed spontaneous thrombosis of
the SPS because prior angiography revealed the patent
SPS.8,16 The SPS was not identifiable in another five
cases, and probably thrombosed.6,8,14,21,22
Interestingly, Chan et al.12 reviewed brainstem dysfunction with venous congestion and/or hemorrhage

11
caused by CCF (i.e. 9 direct and 13 indirect fistulas).
Most direct CCFs had engorged veins in surrounding
brainstem on angiography, while most indirect fistulas
had venous congestion without engorged veins. Four
cases had brainstem hemorrhage caused by direct
fistulas.
Endovascular treatment currently has been the therapy of choice for traumatic CCFs, and consists of a
transarterial and transvenous approach. A venous
approach, via mainly IPS or ophthalmic vein, may be
used in case of unsuccessful transarterial embolization
or previous ligation of the ICA. Emergency treatment is
indicated in the setting of progressive visual loss, epistaxis from pseudoaneurysm extended into sphenoid
sinus, rapid aggravation of ophthalmic symptoms
from migration of a treated previous balloon, and
unconscious patients with exclusion of other intracranial lesions.5 Emergency treatment with balloon embolization followed by immediate removal of hematoma
has been recommended for a life-threatening condition
in traumatic CCF with intracerebral venous hemorrhage.10 Without previous closure of the high-flow
fistula, uncontrollable hemorrhage may occur and
lead to disastrous results.11,22 Therefore, cerebral
edema or infarction due to venous congestion in
direct CCF should be considered as urgency or emergency conditions, and requires prompt endovascular
treatment. From the present review, endovascular treatments were performed through arterial and/or venous
routes with balloon and/or coils in the majority of these
cases. Four CCFs needed to be sacrificed or trapped.
Only two cases required decompressive craniectomy
with removal of a blood clot. Most patients had good
recovery except two patients had no data available. One
case had partial recovery, and another case still has lost
vision of the left eye.19,23
Generally, the impairment of venous drainage from
thrombosis of the cerebral deep venous system located
within the core of the brain, that is, the internal cerebral
veins, the BVR, or the great vein of Galen, may lead to
irreversible hemorrhagic venous infarction, mainly in cerebral white matter.39 In contrast, most patients in the present review have returned to normal after obliteration of
the fistula, representing that hemorrhagic or non-hemorrhagic venous infarction caused by venous hypertension
from direct CCF was a more reversible process.
To the best of our knowledge, our case is probably
the most extensive venous infarction, involving frontal
lobe, temporal lobe, basal ganglia, thalamus, brainstem, and cerebellum. Only two cases of extensive cerebral edema and/or hemorrhagic transformation from
direct CCF have been previously reported. Ohshima
et al.17 reported extensive hemorrhagic venous infarction, involving left frontal lobe, temporal lobe, basal
ganglia, thalamus, midbrain, and pons, associated
with left spontaneous CCF. They speculated that
these finding possibly associated with hypovolemia
and perioperative infection during biopsy of the left
ethmoidal sinus. Ract et al.21 also reported a patient

12

Interventional Neuroradiology 0(00)

with a life-threatening traumatic CCF associated with
extensive edema of ipsilateral temporal lobe, basal
ganglia, and brainstem caused by venous congestion
of an anatomical variation of the BVR. They speculated that venous infarction-related factors included
large-sized fistula, a hypoplastic segment of the BVR
with developed uncal vein, and a hypoplastic or thrombosed SPS. Similarly, our case also had a hypoplastic
segment of the BVR, dilated uncal vein, and a hypoplastic or thrombosed SPS. However, the fistula in our
case was small, located opposite the side of the brain,
and developed more extensive venous infarction with
hemorrhagic transformation.
Aldea et al.20 suggested using anticoagulant drugs
in order to avoid massive thrombosis of the venous drainage, causing a progressive worsening of the neurological
status, after the occlusion of the high-flow CCF. Despite
no anticoagulation for prevention of the ongoing venous
thrombosis following the obliteration of the CCF, this
condition did not occur in our case. However, this management remains controversial, and there are still no evidence-based guidelines.

Conclusion
We reported an extremely rare case of contralateral
extensive hemorrhagic venous infarction caused by a
traumatic CCF related to retrograde venous reflux
into the opposite BVR. The cause of this condition
may relate to absence of the ipsilateral BVR, occlusion
of posterior segment of the contralateral SPS, and
a developed uncal vein with hypoplastic second
and third segments of the contralateral BVR.
Neurologically and radiologically, the extensive hemorrhagic venous infarction has nearly completely resolved
following obliteration of the fistula by endovascular
treatment without surgical intervention. Cerebral
edema or infarction due to venous congestion in
direct CCF should be considered as urgency or emergency conditions, and requires prompt endovascular
treatment with complete obliteration of the fistula.
Declaration of conflicting interests
The authors declared no potential conflicts of interest with
respect to the research, authorship, and/or publication of this
article.

Funding
The authors received no financial support for the research,
authorship, and/or publication of this article.

ORCID iD
Prasert Iampreechakul

http://orcid.org/0000-0002-8241-7955

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