Key-words:
Development hypoplastic sinus - dural arteriovenous fistulae - postoperative outcome
Introduction
Intracranial dural arteriovenous fistulae (AVF) are defined as abnormal arteriovenous
shunts or connections that occur within the dura mater. Unlike arteriovenous malformations,
the development of dural AVF seems more similar to that of acquired lesions.[[1]] Sinus thrombosis after trauma, infection, and surgery can cause venous outflow
obstruction and venous hypertension and frequently arises in patients with dural AVF.[[1]],[[2]],[[3]],[[4]] However, the pathophysiology of dural AVF development has not been elucidated.
This report describes two patients who developed a dural AVF in the nondominant or
hypoplastic transverse (TS)-sigmoid (SS) sinuses after the sinus occlusion during
intracranial surgery. Both patients were evaluated by angiography just before the
original surgery and when a dural AVF was diagnosed. We discuss the pathogenesis of
dural AVF after the sinus occlusion during intracranial surgery in the posterior fossa
based on our experience with these patients.
Case Reports
Case 1
A benign meningioma was surgically resected from the left cerebellopontine angle of
a 63-year-old female using a left lateral suboccipital approach [[Figure 1]]a and [[Figure 1]]b. Preoperative DSA revealed that the ipsilateral left TS-SS was hypoplastic, and
the contralateral right TS-SS was dominant [[Figure 1]]c. The sinus occlusion was revealed after surgery and 6 months after craniotomy,
three-dimensional enhanced computed tomography angiography (3D-CTA) showed venous
reflux in the left TS-SS region [[Figure 1]]d and [[Figure 1]]e. Sixteen months after craniotomy, she presented with the progressive left retroauricular
pulse-synchronous bruit. Recurrent meningioma was not found using magnetic resonance
imaging (MRI) and angiography, but 3D-CTA showed worsening venous reflux [[Figure 1]]f. Dural AVF in the left TS-SS fed by the left ascending pharyngeal and occipital
(OA) arteries with retrograde drainage to the left inferior petrosal sinus with SS
occlusion was confirmed by DSA [[Figure 2]]a. She was treated with transvenous coil embolization through a transconfluence
approach, and she recovered without neurological deterioration [[Figure 2]]b,[[Figure 2]]c,[[Figure 2]]d. The patient has remained free of recurrent dural AVF for 5 years.
Figure 1: Surgical resection of a left cerebellar brain tumor in a 53-year-old female. Resection
of the left cerebellar brain tumor (a) proceeded via the lateral suboccipital approach
(b). Preoperative digital subtraction angiography shows hypoplastic left, compared
with the right transverse sinus (c). Preoperative three-dimensional-computed tomography
angiography shows no abnormalities (d). Slight cerebral venous reflux evident on a
three-dimensional-computed tomography angiography image at 6 months after surgery
(e; arrowhead) became symptomatic (left retro-auricular bruit) at 16 months after
surgery (f; arrowhead)
Figure 2: Postoperative arterio-venous shunt in the patient described in Figure 1. digital
subtraction angiography shows arterio-venous shunt, fed by the occipital artery and
stylomastoid branch, and drained into the left transverse (TS) and left superior petrosal
sinuses (a, left common carotid angiography lateral [Lat] view) of the transverse
sinus/sigmoid sinus dural arteriovenous fistula (Cognard type 2a + b). Under local
anesthesia, a 6 Fr Envoy MPD 90-cm sheath catheter (Cordis, Miami Lakes, FL, USA)
was inserted via the right femoral artery for digital subtraction angiography. An
Excelsior 1018 microcatheter was introduced with Cerulean G and 5 Fr ENVOY (Cordis)
catheters into the right jugular vein. A shunt point was transvenously coil embolized
using an Echelon-14 microcatheter (MicroTherapeutics, Natick, MA, USA) via the transconfluence
approach (b, left common carotid angiography Lat live image; c, left common carotid
angiography AP view; d, left common carotid angiography Lat view). Symptoms of left
retroauricular bruit immediately disappeared thereafter
Case 2
An epidermoid tumor in the right cerebellopontine angle of a 56-year-old female was
surgically resected through a right presigmoid, transpetrosal, and retrosigmoid approach
[[Figure 3]]a and [[Figure 3]]b. Preoperative 3D-CTA and DSA revealed severe ipsilateral right TS stenosis and
dominant contralateral left TS-SS, [[Figure 3]]c and [[Figure 3]]d and the sinus occlusion was revealed after surgery. Two years after intracranial
surgery, she presented with the progressive right retroauricular pulse-synchronous
bruit. Dural AVF in the right TS-SS region fed by the right OA was diagnosed by DSA,
and the isolated sinus appearance with retrograde drainage to the right vein of Labbe
and an inferior temporal vein was shown [[Figure 4]]a. She underwent transvenous coil embolization through a transconfluence approach,
without neurological deterioration [[Figure 4]]b,[[Figure 4]]c,[[Figure 4]]d. The patient has remained free of recurrent dural AVF for 5 years.
Figure 3: Brain tumor at the right cerebellopontine angle and temporal middle fossa of a 54-year-old
female. Constructive interference in steady state magnetic resonance image shows a
tumor at the right cerebellopontine angle and temporal middle fossa (a). Tumor resection
via the presigmoid transpetrosal and retrosigmoid approach on magnetic resonance image
constructive interference in steady state image (b). Preoperative three-dimensional
enhanced computed tomography angiography (c) and digital subtraction angiography (d)
images show right transverse sinus stenosis (arrowhead)
Figure 4: Postoperative arterio-venous shunt in the patient described in Figure 3. The patient
presented with right retroauricular bruit 2 years after surgery and digital subtraction
angiography revealed cerebral venous reflux and arterio-venous shunt in the right
transverse sinus region. The shunt was fed by occipital artery and drained by the
right vein of Labbe and inferior temporal vein (a, left common carotid angiography
Lat view). This was diagnosed as transverse sinus/sigmoid sinus dural arteriovenous
fistula (Cognard type 2a + b). Under local anesthesia, a 6 Fr Envoy MPD 90-cm sheath
catheter was inserted via the right femoral artery for digital subtraction angiography.
Then, an Excelsior 1018 microcatheter was introduced together with Tempo 4 and 5 Fr
ENVOY catheters into the left jugular vein. A shunt point was transvenously coil embolized
using a microcatheter via transconfluence approach (b, right common carotid angiography
Lat live view). Symptoms and arterio-venous shunt immediately disappeared (c, right
common carotid angiography Lat view arterial phase; d, right common carotid angiography
Lat view venophase)
Discussion
The etiology of dural AVF in the posterior fossa remains uncertain. Clinical observations
and serial angiographic findings have indicated that many dural AVF are acquired and
that sinus thrombosis,[[1]] sinus hypertension,[[1]] intracranial abscess,[[2]] and trauma[[3]] might contribute to their formation. The notion that this condition is acquired
is supported by the finding that they frequently develop after trauma, craniotomy,
and sinus thrombosis. Clinical observations indicate that pathological changes in
the intracranial sinus, including sinus thrombosis, can lead to dural AVF formation.[[4]] Notably, 39%–80% of dural AVF are associated with intracranial sinus thrombosis,
and 78% of patients without thrombosis have sinus dysplasia, stenosis, septation,
or distortion.[[5]],[[6]],[[7]],[[8]],[[9]],[[10]],[[11]]
[[Table 1]] shows published case series of dural AVF developing after intracranial surgery.[[12]],[[13]],[[14]],[[15]] Most of them occurred at the site of a prior intracranial surgery, regardless of
the dominance or stenosis of venous or occluded sinuses before intracranial surgery.
These authors speculated that venous thrombosis after sinus occlusion due to intracranial
surgery might cause a fistula by opening the physiological shunts in the dura mater,
which would consequently redirect arterial blood into the cortical veins, followed
by the eventual development of a dural AVF at the site of the original intracranial
surgery. On the other hand, experimental studies that have investigated the mechanisms
or pathogenesis of dural AVF have found that they can be induced by venous hypertension
without sinus or venous thrombosis.[[16]],[[17]] Therefore, an exposure of the vessels to venous hypertension and subsequent local
hypoperfusion might cause vessel dilation and the loss of sphincter control in arterioles.
Increased intraluminal pressure in the vessels stimulates angiogenesis, and the subsequent
formation of direct connections to a sinus or vein results in the development of dural
AVF. Shin et al. suggested that venous sinus hypertension increases the production
of vascular endothelial growth factor (VEGF),[[18]] which might help to increase the angiogenesis and lead to an AVF. Matrix metallopeptidase-9
(MMP-9) is closely associated with neovascularization and it might synergistically
work with VEGF.[[19]] Furthermore, cerebral venous sinus thrombosis induces MMP-9 upregulation and inflammatory
activation.[[19]] Dural AVF developed in our patients after posterior fossa craniotomy of the nondominant
or hypoplastic TS-SS side. We speculate that the nondominant or hypoplastic sinus
became occluded after posterior fossa craniotomy in our patients and that subsequent
local intrasinus hypertension and local hypoperfusion induced the opening of a physiological
shunt that stimulated angiogenesis, which subsequently resulted in a dural AVF.
Table 1: Summary of reports regarding dural arteriovenous fistula after intracranial surgery
The transverse and sigmoid sinuses are exposed and manipulated during presigmoid,
transpetrosal and retrosigmoid approaches to the skull base, but there are a scant
data available on the incidence of venous sinus occlusion after surgery. Jean et al.
reported that 10% of patients were discovered asymptomatic sinus occlusion after posterior
fossa craniotomy.[[20]],[[21]] The sigmoid and transverse sinuses can be occluded during presigmoid, transpetrosal
approaches to the skull base tumor.[[22]] It is important to follow-up MRI because there is a possibility of occurrence of
dural AVF if asymptomatic sinus occlusion is observed after posterior fossa surgery.
Transfemoral embolization of the feeding arteries, embolization of the affected sinus
or complete surgical excision is recommended to treat dural AVF.[[4]] We believe that all of these procedures, including surgical excision, are valuable
in the appropriate setting. Transvenous embolization of venous channels appears to
be the first choice because to penetrate a fistulous point using glue injected via
transarterial embolization is difficult.[[4]],[[5]],[[6]],[[7]],[[8]],[[9]],[[10]],[[11]],[[12]],[[13]],[[14]],[[15]],[[16]],[[17]],[[18]],[[19]],[[20]],[[21]],[[22]],[[23]] Shunts in our patients were completely occluded after transvenous sinus embolization
through a transconfluence approach because these affected sinuses were not associated
with normal cerebral venous drainage. Embolization using Onyx (eV3 Neurovascular,
Inc., Irvine, CA, USA), which penetrates better and allows for robust injections,
is a new and promising modality for treating dural AVF.[[24]],[[25]],[[26]],[[27]],[[28]] However, Onyx has the same disadvantage as other embolic materials in that its
ability to penetrate small dangerous anastomoses to cranial nerves or vessels supplying
the brain cannot be controlled.[[29]] Findings from long-term follow-up are awaited to establish the value of embolization
with Onyx for dural AVF.[[30]]
Conclusion
Sinus manipulation during intracranial surgery of the posterior fossa carries a risk
of sinus occlusion and developing postoperative dural AVF. This should be considered
even if the ipsilateral TS-SS is nondominant or appears hypoplastic.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms.
In the form, the patient has given her consent for her images and other clinical information
to be reported in the journal. The patient understands that name and initials will
not be published and due efforts will be made to conceal identity, but anonymity cannot
be guaranteed.