Keywords
caroticocavernous fistula - proptosis - embolization
Introduction
Caroticocavernous sinus fistulae (CCFs) result from abnormal communication between
the carotid system arteries and the cavernous sinus.[1]
[2] The resultant increase in cavernous sinus pressure is the main reason for the clinical
features and complications of this entity. Advances in endovascular techniques have
resulted in this approach to have become the mainstay of treatment for CCFs.
Classification and Etiology of CCFs
Classification and Etiology of CCFs
Caroticocavernous sinus fistulae can be categorized according to etiology (spontaneous
or posttraumatic), hemodynamic effects (high or low flow), and angiographic findings
(direct or indirect). It is the latter which forms the basis of classification proposed
by Barrow et al[3] and is the most helpful to plan a therapeutic treatment strategy.[1] According to this classification system the CCFs can be categorized into four distinct
types ([Table 1]).
Table 1
Angiographic classification of caroticocavernous fistulas
|
aTomsick[4] further subdivided type D into D1 (unilateral) and D2 (bilateral).
|
|
Type A
|
Direct communication between Internal carotid artery (ICA) and cavernous sinus leading
to a high-flow fistula ([Fig. 1])
|
|
Type B
|
Indirect dural arteriovenous fistulas centered on cavernous sinus being fed by branches
of ICA
|
|
Type C
|
Indirect dural arteriovenous fistulas centered on cavernous sinus being fed by branches
of external carotid artery (ECA)
|
|
Type Da
|
Indirect dural arteriovenous fistulas centered on cavernous sinus being fed by branches
of both ICA and ECA ([Fig. 2])
|
Fig. 1 Lateral ICA angiogram showing a direct CCF with a rent (white arrow) between the
distal horizontal ICA and cavernous sinus. Reflux is seen into the SOV (black arrow) and inferior petrosal sinus (red arrow).
Fig. 2 Type D2 CCF: Selective frontal angiograms of bilateral ICAs (a,b) and ECAs (c,d) show opacification of left cavernous sinus with feeders from dural branches of bilateral
cavernous ICAs and middle meningeal (red arrows), anterior meningeal (black arrows),
and ascending pharyngeal branches (black arrows) of bilateral ECAs. The right cavernous
sinus is opacified through the intercavernous communication.
Etiological Classification
Etiological Classification
-
Traumatic CCFs mostly demonstrate a single direct communication between internal carotid artery
(ICA) (most commonly the proximal horizontal cavernous segment) and cavernous sinus
and are hence type A.[1] Bilateral traumatic CCFs are extremely rare and mostly associated with extensive
head injury, and are commonly fatal.[5]
-
Spontaneous CCFs may be of any of the four types since a type A shunt can develop following a spontaneous
rupture of cavernous ICA aneurysm. More commonly, spontaneous CCF is an indirect CCF
and has low flow rates. The main arterial supply to indirect fistulas originates from
internal maxillary, ascending pharyngeal, accessory meningeal, and middle meningeal
branches of external carotid artery (ECA) and cavernous branches of ICA. They occur
more commonly in postmenopausal women and have an association with diabetes mellitus,
hypertension, pregnancy, and atherosclerosis.[6]
[7]
[8]Trauma is only very rarely associated with indirect CCF.[9]
Clinical Features
A CCF leads to transmission of high-pressure arterial blood into cavernous sinus and
its various tributaries, that is, superior and inferior ophthalmic veins anteriorly,
the superior petrosal and inferior petrosal sinuses and basilar plexus posteriorly,
the pterygoid plexus inferiorly, the sphenoparietal sinus laterally, and cavernous
sinus contralaterally.[10]
It is this redirection of high-pressure flow into the venous system that causes the
clinical symptomatology of CCF ([Fig. 1]).
The orbital diversion of flow leads to orbital venous congestion and transudation
of interstitial fluid into orbit with resultant proptosis and chemosis. Presence of
an orbital bruit on auscultation completes the Dandy’s triad[1]: exophthalmos, bruit, and conjunctival chemosis which, however, is not found in
most patients of CCF. Most patients present with proptosis (90%); chemosis (90%);
diplopia (50%); bruit (25%); orbital pain (25%); III, IV, V, and VI nerve palsies;
raised intraorbital pressure (IOP); and some form of visual loss (50%) due to impaired
drainage of aqueous humor.[1]
[11]
Raised venous pressure and IOP can compromise retinal perfusion, leading to severely
diminished visual acuity.[1]
Hence any visual loss warrants immediate treatment of a CCF. Whereas minor deficit
in visual acuity resolve completely in most cases post treatment, severe loss with
loss of perception of light rarely improves even with successful treatment.[12]
Incidence of intracranial hemorrhage is 5% and it occurs due to cortical venous hypertension
([Fig. 2]). Massive epistaxis due to formation of pseudoaneurysmal cavernous sinus varix can
manifest in 1 to 2% of the cases.[13] Similarly rupture of dilated veins draining the ear canal can lead to massive otorrhagia.[13]
[14]
It must be noted that indirect CCFs progress more insidiously and most cases present
with slowly progressive glaucoma and relatively moderate proptosis or conjunctival
injection[1]
[15]
[16] ([Fig. 3]).
Fig. 3 Myriad clinical presentations of direct CCF: (a,b) A 45-year-old man with complete ptosis and severe proptosis right eye with no chemosis.
(c,d) Two different patients having complete and partial ptosis. Patients having mild (e) and severe (f) chemosis and proptosis. (g) and (h) show a patient having bilateral proptosis and chemosis with left abducens palsy due
to right direct CCF.
Exacerbations and remissions are hallmark of CCF (both direct and indirect), likely
due to cavernous sinus thrombosis and rerouting of venous flow.[1] Incidence of spontaneous resolution of indirect CCFs ranges from 10 to 60% in literature[17] whereas symptomatic high flow direct CCFs rarely regress on their own.[18]
It is important to bear in mind that any change or improvement in symptoms of a CCF
should alert the treating physician to an alteration in venous drainage and a possible
switch to a higher risk central or spinal pial draining pattern predisposing to life-threatening
venous bleed and myelopathy, respectively ([Table 2]).[1]
Table 2
Dangerous signs which are indications for early/emergency treatment[1]
[14]
[18]
|
Clinical signs and symptoms
|
Angiographic signs
|
|
Abbreviations: CVR, central venous reflux; TIA, transient ischemic attack.
|
|
Severe headache (indicates central venous reflux and a high risk of bleeding)
Raised intracranial pressure
Rapid progression of proptosis
Diminished visual acuity
Hemorrhage (intracranial, subarachnoid, otorrhagia, epistaxis)
TIA (signifies significant steal)
|
CVR ([Fig. 2])
Varix of cavernous sinus ([Fig. 8])
Pseudoaneurysm of carotid artery
|
Imaging Evaluation
Doppler evaluation of affected eye shows a prominent superior ophthalmic vein with
arterialized flow ([Fig. 4]) consistent with an arteriovenous fistula.
Fig. 4 Frontal right ICA angiogram of a patient with right direct CCF shows significant
reflux into the right sylvian vein (black arrow), bilateral pial veins (white arrow),
and right cortical veins (red arrow).
Computed tomography (CT) and CT angiography (CTA) show proptosis of affected eye with
swelling of extraocular muscles (EOMs), dilatation, and tortuosity of superior opthalmic
vein ( SOV) and ipsilateral cavernous sinus ([Fig. 5a]). In addition, CTA can show location of the rent in many cases of direct CCFs ([Fig. 5b]) as well as size of cavernous sinus pouch, which helps to decide the selection of
coil size for treatment. The volume rendered (VR) images also help in locating the
SOV in cases where direct exposure of this vein is required for accessing the cavernous
sinus in indirect CCFs ([Fig. 5c]). In addition, CT is excellent to evaluate for any bony injuries of skull base especially
ones which may compress the carotid lumen.[1]
Fig. 5 A 63-year-old lady presented with 2 months history of gradually progressive chemosis
and ptosis right eye. Her DSA revealed a type D2 CCF (see [Fig. 2]).
Magnetic resonance imaging (MRI) shows the orbital edema and abnormal flow voids thereby
confirming high flow within the orbital veins. MRI may also show prominent cerebral
veins.
Digital subtraction angiography (DSA) of cerebral arteries remains the mainstay and
gold standard for diagnosis and treatment planning of CCFs.
All cases of CCF should undergo an angiogram with selective cannulation of bilateral
ECAs and ICAs.
The angiogram should be able to provide the following information:[1]
[2]
[5]
[15]
[16]
-
Size, location, and number of fistula(s) (since there may be multiple rents).
-
Differentiating direct versus indirect fistula ([Figs. 6]
[7]).
-
Assessment of cervical ICA for any associated injury such as dissection or pseudoaneurysm.
-
Any associated cavernous carotid aneurysm/venous varix ([Fig. 8]).
-
Quality of antegrade flow (presence/absence of steal phenomenon).
-
Collateral flow through circle of Willis (important in cases when parent artery occlusion
is being planned ([Fig. 9]).
-
Degree of central venous reflux(CVR):[Figure 2].
-
Balloon test occlusion should be performed in case ICA occlusion is being contemplated
as a means of treatment.
Fig. 6 Doppler of the orbit in a case of direct CCF shows reversed arterialized flow in
the superior ophthalmic vein (SOV).
Fig. 7 (a, b) Contrast-enhanced CT in a case of left-sided direct CCF shows prominent left cavernous
sinus (white arrow) and dilated left SOV (red arrow). (c) Volume-rendered image of CT angiography for an indirect CCF shows the dilated SOV
in relation to the superior margin of orbit. (d) Sagittal reconstruction of CT angiography maximal intensity projection shows the
rent in cavernous ICA (arrow).
Fig. 8 Lateral angiogram in a case of direct caroticocavernous fistula shows a large varix
of cavernous sinus (arrow).
Fig. 9 Right ICA angiogram with manual compression of left CCA in a case of left direct
caroticocavernous fistula shows good cross flow across the anterior communicating
artery.
Successful demonstration of fistula in a direct CCF depends on several factors such
as number, location, and size of rent in the ICA. The following methods help to improve
the diagnostic accuracy of the study ([Fig. 10]):
Fig. 10 Left ICA angiogram in a case of direct caroticocavernous fistula ([Fig. 1]) with manual compression of left CCA (Mehringer and Heishiema maneuver) leads to
excellent delineation of the rent in cavernous ICA (arrow).
-
Using a high frame rate (> 5 fps) during acquisition.[1]
[18]
-
Using pure contrast at high injection rate (7–8 mL/sec).[1]
[18]
-
Using Mehringer and Heishiema or Heuber maneuvers.[1]
[18]
[19]
In indirect CCFs it is important to note presence or absence of the draining venous
sinuses ([Fig. 11]), which would serve as pathways for access to the concerned cavernous sinus.
Fig. 11 Late arterial phase of lateral angiogram of right ICA in a case of indirect caroticocavernous
fistula shows absence of inferior petrosal sinuses thereby precluding a posterior
transvenous approach to enter the cavernous sinus.
Treatment Modalities
For cases with minor symptoms and absence of any dangerous features on angiography,
a conservative approach including follow up of intraocular pressures, visual acuity,
and cranial neuropathies can be followed. Medical treatment to decrease IOP, corneal
protection measures along with manual compression of carotid artery by the patient
(while in a sitting or lying down position using his/her contralateral hand) are part
of this treatment plan.[2]
Currently endovascular treatment is the primary mode of treatment for symptomatic
CCFs.
Microsurgical treatment of CCFs after frontotemporal cavernous sinus exposure is reserved
for symptomatic patients who fail endovascular therapy.[1]
[15]
Stereotactic radiosurgery has been described as a means to treat some indirect CCFs
but it has the disadvantage of having a significantly long lag time for its effects
to set in and having high recurrence rates.[20]
Endovascular Management for Direct CCF
Endovascular Management for Direct CCF
The aim is to occlude the tear between the ICA and sinus while protecting the ICA
and a transarterial approach is a favored one. Choice of the embolizing material varies
from detachable coils, liquid embolizing agents, and detachable balloons.
Coiling of the Cavernous Sinus Using Detachable Coils
This is currently the mainstay of treatment for direct CCF in India since one of the
other methods favored earlier, that is, detachable balloons have been of limited availability
for the past few years. The approach consists of selectively cannulating the rent
in the ICA using a microcatheter and subsequently deploying coils within the cavernous
sinus till it is no longer filled ([Figs. 12]
[13]
[14]).
Fig. 12 Balloon-assisted coiling for a case of left direct caroticocavernous fistula. (a) 18-year-old man presented with left proptosis and chemosis 2 weeks post trauma. (b–e) Complete closure of the fistula post coiling. (f,g) Pre- and 3-hour post procedure images showing significant resolution of chemosis.
(h) One week post procedure image showing complete resolution of proptosis.
Fig. 13 Balloon-assisted coiling for a case of right direct caroticocavernous fistula. (a,b) A 45-year-old man presented with right proptosis and ptosis ten days post trauma.
(c–e) Complete closure of the fistula and deep venous reflux post coiling. (f) One week post procedure image showing partial resolution of proptosis and ptosis
but more importantly he is now cured of venous reflux which had a high risk of leading
to venous hemorrhage.
Fig. 14 (a–d) Two patients with right direct caroticocavernous fistulas presenting with extensive
chemosis and conjunctival eversion (a) and complete ptosis (b) who were treated with coiling.
In our experience use of a balloon is extremely useful in ensuring dense packing of
cavernous sinus while ensuring no coil prolapse into the parent artery. Authors have
also described use of liquid embolic agents such as N-butyl cyanoacrylate (n-BCA)
and ethylene vinyl alcohol (EVOH) along with coils to cure CCF.[2]
Fistula Occlusion Using Detachable Balloon
Serbinenko described the first successful case of CCF treated by a detachable balloon
([Fig. 15]) while preserving the ICA.[21] The balloon catheter is advanced through a guiding catheter placed high in the cervical
ICA and is directed inside the cavernous sinus across the rent due to the flow. Once
in place it is inflated and detached. Complications of this procedure include early
deflation of the balloon,[1]
[2]
[15] unintended migration of the inflated balloon distal into the ICA, and venous side
migration of the balloon.[22]
[23]
Fig. 15 (a–c) A 17-year-old boy presented with proptosis and chemosis of right eye following road
traffic accident. Diagnostic angiogram revealed (a) a direct caroticocavernous fistula with rent located at the horizontal segment of
right cavernous ICA. The occlusion of the rent in this case was achieved with a detachable
balloon (b). Check angiogram revealed complete occlusion of the fistula and normal filling of
the intracranial circulation (c).
Parent Artery Occlusion (PAO) of ICA
It may be required in cases when the ICA is extensively damaged and the rent is too
big to allow the coils to be accommodated into the cavernous sinus without prolapsing
into the ICA. If PAO is planned assessment of collateral flow across the Circle of
Willis is essential which may require performing a Balloon test occlusion (BTO) prior
to the PAO. It is important to say that if a patient has complete steal through the
CCF on DSA and still does not have symptoms of TIA then this would suggest that the
collateral flow across the anterior and posterior communicating arteries is adequate
and a BTO may not be needed.[1]
[18]
Methods for PAO include coiling of the ipsilateral ICA ([Fig. 16]) in a distal to proximal fashion so as to prevent filling of the fistula in retrograde
manner from supraclinoid ICA.[1]
[2]
[15] PAO can also be done by placing two detachable balloons, proximal and distal to
the fistula.
Fig. 16 (a-f) A 26-year-old gentleman presented with right-sided direct caroticocavernous fistula
with venous drainage to bilateral superior ophthalmic veins and associated cortical
venous reflux (a,b). The rent was located at the posterior horizontal aspect of cavernous segment of
right ICA. Initial attempt to treat the caroticocavernous fistula with detachable
balloons (c) was not successful. The case was then managed with parent artery occlusion of right
ICA with use of detachable coils (d). Good cross-circulation via the anterior and posterior communicating artery was
evident (e,f) which perfused the right sided anterior circulation. The patient recovered without
any deficit.
Stent Graft Placement in the ICA
Though navigability of stent grafts into the cavernous ICA is an issue this method
has been described by some authors to treat direct CCFs in patients with favorable
anatomy.[1]
[15] However long-term patency issues preclude their use as a first line method to treat
CCFs.
Endovascular Management for Indirect CCF
Endovascular Management for Indirect CCF
Unlike a direct CCF which is approached through a transarterial approach an indirect
CCF is best treated by a transvenous approach into the affected cavernous sinus. The
aim is to occlude the fistula without disturbing venous drainage in the cortical veins[1]
[2]
[15]
Transvenous embolization requires access to the affected cavernous sinus through a
preferred posterior approach (through the IJV and subsequently IPS) or if it fails
via an anterior approach through the facial vein−SOV pathway.[1] The latter may require a direct SOV exposure in some cases ([Fig. 17]). Much less favored than these two routes are the ones through the cortical veins,
lateral pterygoid veins, superior petrosal veins, and inferior ophthalmic veins.[1] Once the concerned cavernous sinus is accessed embolization is completed using coils
and/or liquid agents.[1]
Fig. 17 A case of indirect caroticocavernous fistula (type D2) (a) centered on left cavernous sinus (angiogram shown in [Fig. 2]) treated by anterior approach to cavernous sinus by direct exposure of right SOV
(b,c). Post coiling and Onyx embolization of left cavernous sinus (d) the patient showed complete clinical improvement in 4 weeks (e).
Long-term Outcomes
The long-term follow-up results for endovascular treatment for CCFs are extremely
good with a success rate for closure of direct CCFs reported to be from 82 to 99%
and that of indirect CCFs to be from 70 to 78% without any major procedure related
complications.[24]
[25]
[26]
