Carotid Cavernous Fistula

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Carotid Cavernous Fistula
Axial T1 MRI demonstrating left-sided proptosis and bilateral SOV enlargement


Disease Entity

A carotid-cavernous fistula (CCF) is the result of an abnormal vascular connection between the internal carotid artery (ICA) or external carotid artery (ECA) and the venous channels of the cavernous sinus. CCFs are classified based on the arterial system involved, hemodynamics, and etiology. The presentation can be varied and nonspecific; however, patients with CCFs commonly present with ophthalmic manifestations due to venous drainage of the orbit from the cavernous sinus. Early diagnosis and appropriate management is essential to avoid vision and life-threatening complications.

Disease

ICD-10-CM I77.0 Arteriovenous fistula, acquired

Epidemiology

CCFs are a rare entity that can occur spontaneously or secondary to trauma. Traumatic CCFs account for the majority of CCFs. They can occur following closed head injury, skull base fractures, penetrating head trauma, or iatrogenically after craniotomies, endoscopic transsphenoidal or sinus surgery, and endovascular procedures.[1][2] These CCFs typically correspond to Type A CCFs (see Classification section). The true incidence is not well-documented; however, studies have reported an incidence of 0.2% in patients with traumatic brain injury and up to 4% with skull base fractures.[3][4] Bilateral CCFs are rare but more commonly reported in traumatic CCFs, occurring in up to 1% of traumatic cases.[5]

Spontaneous CCFs account for up to 30% of all CCFs reported in the literature and are more common in the postmenopausal patients.[6][7] Spontaneous CCFs may result from the rupture of an aneurysm of the cavernous segment of the internal carotid artery (ICA). This can occur in up to 24% of individuals with such aneurysms, dependent on size and morphology.[6] Musculoskeletal and collagen related disorders including Ehler’s-Danlos syndrome, pseudoxanthoma elasticum, osteogenesis imperfecta, and fibromuscular dysplasia are also thought to predispose to CCF formation due to presumed arterial wall defects and risk of dissection.[8][9][10] CCF from an cavernous ICA aneurysm rupture or cavernous ICA dissection would commonly result in a Type A CCF (see Classification section).

Anatomy

Figure 1: MRI T2 sequence, axial (left) and coronal (right) views, shows the horizontal segment of the left cavernous ICA (blue arrow), lateral dural wall (red), anterior clinoid process (ACP, yellow) and optic nerve (green). Coronal view also shows the clinoid segment of the ICA in cross-section. Image courtesy of John D. Nerva, MD.

The cavernous sinus (CS) is a paired dural venous sinus centered around the sella turcica.[11] It contains multiple venous channels extending from the endosteal dural layer of the sphenoid bone inferiorly and medially to the meningeal dural layer of the floor of the middle cranial fossa. The CS extends from the superior orbital fissure (SOF) anteriorly to the petrous apex posteriorly, between the dorsum sellae medially and Meckel’s cave laterally. The CS serves as a confluence of venous systems draining the orbit (via superior and inferior ophthalmic veins, SOV, IOV), Sylvian fissure, anterior and middle cranial fossae (via sphenoparietal sinus) and posterior cranial fossa (via the basilar plexus and superior and inferior petrosal sinuses), and they are connected by intercavernous sinuses existing within the sella. The CS also drains inferiorly via emissary veins through the foramen ovale into the pterygoid venous plexus. The venous drainage patterns of the cavernous sinus are pertinent for the pathophysiology of CCFs.

The cavernous segment of the ICA courses through the cavernous sinus (Figure 1). This segment has also been referred to as both the intercavernous and intracavernous ICA. The ICA enters the cavernous sinus as it passes the petrolingual ligament and exits at the proximal dural ring becoming the clinoidal segment.[11] Although the course of the cavernous ICA is variable and dependent of patient specific factors, the typical segments include the proximal ascending, posterior genu, horizontal and anterior genu (Figure 2).[12][13] The anterior genu is at the posterior border of the optic strut, a region of bone between the anterior clinoid process and body of the sphenoid between the optic canal and SOF.[11] Branches of the cavernous ICA include the meningohypophyseal trunk (MHT), inferolateral trunk (ILT) and capsular arteries of McConnell.

The oculomotor (CN III), trochlear (CN IV), trigeminal (CN V) and abducens (CN VI) nerves are associated with the CS.[11] From superior to inferior, CNs III, IV, V1 (ophthalmic division) and V2 (maxillary division) course within the lateral wall of the CS. CNs III (superior and inferior divisions), IV, V1 (lacrimal nerve, frontal nerve, nasociliary branch) and VI exit the CS via the SOF along with the SOV and IOV.

Classification

Figure 2: Cerebral angiogram, ICA, lateral projection, shows the segments of the cavernous ICA including the proximal ascending segment, posterior genu, horizontal segment (blue arrow), anterior genu and distal ascending segment. Branches of the meningohypophyseal trunk (MHT, white) and inferolateral trunk (orange) are shown. The ophthalmic artery is also demonstrated (purple). Image courtesy of John D. Nerva, MD.

CCFs are primarily classified into 4 types based on the arterial system involved as described by Barrow et al (Table 1).[14] Type A are direct fistulas, whereas types B, C, and D are indirect fistulas. CCFs are further classified into traumatic or spontaneous etiology and high or low flow based on hemodynamic properties (Table 2). The flow rate is determined by angiography and largely influences clinical presentation.

Table 1: Barrow Classification[14]

Type Description
A Direct connection between the ICA and cavernous sinus
B Connection between meningeal branches of ICA and cavernous sinus
C Connection between meningeal branches of ECA and cavernous sinus
D Connection between meningeal branches of both ICA and ECA and the cavernous sinus

Table 2: CCF Classification[6]

Type Classification
Anatomical Direct vs Indirect
Hemodynamic High vs Low Flow
Etiology Traumatic vs Spontaneous

An updated classification system proposed by Thomas et al. is based on venous drainage and demonstrates a significant correlation with clinical symptoms, treatment planning, and outcome (Table 3).[15]

Table 3: Classification of CCF by Venous Drainage[15]

Type Description
1 Posterior/inferior venous drainage only
2 Posterior/inferior and anterior venous drainage
3 Anterior venous drainage only
4 Retrograde cortical venous drainage
5 Direct ICA-cavernous sinus fistulae corresponding to the type A Barrow classification

Pathophysiology

All types of CCFs lead to shunting of blood from a high-flow arterial system (ICA or ECA) into a low-flow venous system (cavernous sinus) without an intervening capillary bed. This produces increased vascular pressure and resistance which impedes venous drainage and leads to vascular congestion in areas that are drained by the cavernous sinus. Impaired drainage of the orbit in an anterior draining CCF is what leads to the common ophthalmic manifestations as a result of congestion, ischemia, and mass effect.[16]

Direct or Type A CCFs are the most common type and form a direct connection between the cavernous segment of the ICA and the cavernous sinus.[14] This high-flow variant of CCFs causes retrograde blood flow from the cavernous sinus into the superior ophthalmic vein (SOV) leading to dilation of the SOV and ophthalmic clinical manifestations. The majority of direct CCFs are caused by trauma, frequently involving a tear in the muscular wall of the ICA, a laceration of one of its branches, or complete transection of the ICA by shearing forces.[16] The cavernous segment of the ICA is particularly susceptible to injury in basilar skull fractures.[3][17] In a review of 91 cases with a direct CCF, Gupta et al. identified 85 trauma-related causes, while 6 were secondary to aneurysm rupture.[18] Less commonly, direct CCFs can occur spontaneously; particularly in patients with predisposing muscular and collagen disorders or cavernous ICA aneurysms.[8][9]

Type B, C, and D CCFs are dural, low-flow fistulae that result from an indirect connection between meningeal branches of the internal carotid artery (ICA) and/or external carotid artery (ECA) and the cavernous sinus.[14] Indirect CCFs are considered low-flow shunts because the originate from these dural arterial branches rather than the high-flow ICA. The majority of indirect CCFs occur spontaneously and are thought to be caused by a dural rupture in the arterial wall; however, the pathophysioloogy is poorly understood. Associations with hypertension, female gender, and older age have been reported.[14] An increased incidence is seen in pregnancy and is postulated to be related to a hormonally induced hypercoagulable state.[19] Indirect CCFs can also be seen in patients with sinusitis, recent trauma or surgery, hypercoagulable states, and cavernous sinus thrombosis.[20][21]

Diagnosis

The diagnosis of CCF is based on the combination of clinical presentation, physical and ophthalmic examination, and diagnostic procedures.

Clinical Presentation

Figure 3: Cerebral angiogram, left ICA, AP projection pre (left) and post (right) transarterial balloon-assisted coil embolization. The patient presented with pulsatile tinnitus and left abducens nerve palsy six weeks after trauma. Angiography shows the Type A CCF with reflux inferiorly and contralaterally involving bilateral cavernous sinuses (black arrows). There is also evidence of steal phenomenon with decreased flow into the middle cerebral artery (red) territory and no visualization of the anterior cerebral artery territory. Post-embolization angiography shows the coil mass and obliteration of the CCF with restoration of normal arterial flow distally.  Image courtesy of John D. Nerva, MD.

The clinical presentation is influenced by the etiology, classification, size, location within the cavernous sinus, the blood flow rate, and drainage route of the CFF.[22] Direct CCFs tend to have a more severe, acute onset presentation while indirect CCFs are associated with a more gradual onset and chronic course. The earliest clinical features typically involve the orbit, due to venous congestion and venous drainage through the superior and inferior ophthalmic vein into the cavernous sinus.

Direct CCFs often present with a classic triad of pulsatile exophthalmos, orbital bruit, and chemosis. Patients may report diplopia, ocular redness, orbital/retro-orbital pain, swelling, swishing or buzzing sounds, headache, or vision loss. Patients can also have pulsatile tinnitus as a result of turbulent flow through the venous system (Figure 3).[23] Symptoms are typically ipsilateral to the fistula but can occur bilaterally depending on the severity and chronicity of venous congestion.

Ophthalmic signs that can be seen in both direct and indirect CCFs include proptosis, eyelid edema, ptosis, conjunctival arterialization, elevated intraocular pressure, pulsatile exophthalmos, pupillary abnormalities, ocular misalignment, papilledema, dilated retinal veins, ischemic optic neuropathy, central retinal vein occlusion, or choroidal detachment.[14][24] The conjunctival hyperemia associated with CCFs is a result of the arterialization of conjunctival and episcleral veins, consisting of distinct tortuous corkscrew blood vessels that converge at the limbus.[22]

Cranial nerve deficits from ischemia to cranial nerves III, IV, and/or VI can occur and change over time. Ophthalmoplegia has been reported in up to 63% of patients.[25][26] A Horner's syndrome can also be seen with a CN VI palsy due to compression within the cavernous sinus. Compression of V1 and V2 can produce ipsilateral decreased facial sensation. CCFs can also present as an isolated oculomotor palsy without anterior orbital congestive signs and is referred to as a “white-eyed shunt.”[27] A history of trauma should always be elicited in young patients presenting with an isolated CN VI palsy.

In contrast to direct high-flow CCFs, indirect low-flow CCFs may be asymptomatic and insidious in onset. The most common presentation is conjunctival injection which may be initially treated as conjunctivitis causing a delay in diagnosis. With advanced indirect CCFs, increased arterial flow into the cavernous sinus creates venous congestion and retrograde drainage into the orbital veins. The most common findings include arterialization of the conjunctival veins, chemosis, proptosis, diplopia, bruit, retro-orbital headache, elevated intraocular pressure, and a decrease in vision.[28] The classic triad of ocular symptoms seen in direct CCFs are less commonly seen in indirect CCFs.

Diagnosis

A complete history and a detailed clinical exam with appropriate diagnostic testing can help identify and classify CCFs. In office modalities that can be performed include auscultation for an ocular bruit and pneumotonometry to assess for increased ocular pulse amplitude.[29] An ocular doppler ultrasound can identify SOV dilation, arterial flow within the SOV, or enlargement of the extraocular muscles.[24] While a specific diagnosis of direct CCFs is often made quickly, the majority of dural CCFs present insidiously and often go months without a diagnosis.[16] The workup may vary significantly given the clinical symptoms, potential etiologies and pathological states associated with CCFs.

Diagnostic Imaging

The goal of diagnostic procedures is for initial diagnosis of the CCF and then to evaluate the anatomy and physiology of the CCF as it relates to potential treatment options. This workup includes identifying the arterial supply, venous drainage, presence of intracranial or ophthalmic artery collaterals, and assessment of the carotid bifurcation before initiating treatment.[28]

Most patients initially undergo noninvasive imaging with computed tomography (CT), magnetic resonance imaging (MRI), CT angiography (CTA), or magnetic resonance angiography (MRA). The most common neuroimaging signs of anterior draining CCFs include proptosis, enlargement of the SOV, CS, and extraocular muscle enlargement.[30] Enlargement of the IOV and cerebral venous congestion can also seen. If there is a high degree of clinical suspicion or suggestion of a CCF on noninvasive imaging, diagnostic cerebral angiography (digital subtraction angiography, DSA) can confirm the diagnosis and guide treatment.

Figure 4: CTA, sagittal view, shows the course of the cavernous segment of the ICA including the anterior genu, horizontal segment (blue arrow), posterior genu and proximal ascending segment. The ACP (yellow) is also shown. Image courtesy of John D. Nerva, MD.

CTA/MRA: CTA and MRA are often used as first-line noninvasive imaging modalites to evaluate CCFs (Figure 4).[31] CTA and MRA will identify the majority of arterial dissections and cavernous ICA aneurysms causing a CCF as well as enlargement of the affected CS. These modalities can also detect abnormal flow voids, proptosis, enlargement of the SOV/IOV and enlargement of extraocular muscles.[32]

CT: CT without contrast is a useful screening modality to detect skull base fractures in the setting of trauma. Performed with contrast without CTA, a CT may reveal proptosis and engorgement of the SOV.

MRI: Compared to CT, MRI can better demonstrate fat stranding reflecting orbital edema and abnormal flow voids.[33]

Although non-invasive studies can demonstrate findings suggestive of CCF, they cannot definitively diagnosis a CCF which requires the presence of abnormal venous drainage due to the fistulous connection. Further, the absence of findings on non-invasive imaging does not exclude a diagnosis of CCF.

DSA: DSA remains the gold standard imaging modality in the diagnosis of direct and indirect CCFs. DSA is necessary to identify CCF location, arterial supply, flow rate, and venous drainage to classify the CCF and help plan for potential endovascular treatment strategies.[24][28]

Differential Diagnosis

Due to the significant variability in presentation of CCFs, the differential diagnosis will depend on clinical signs and symptoms. It is important to consider the other diagnoses below.

Management

General treatment

Figure 5: Cerebral angiogram, ICA, lateral projection pre (top) and post (bottom) transarterial coil embolization. The patient presented acutely after a motor vehicle accident with this Type A CCF with high flow into the cavernous sinus (black arrow) with reflux into the ophthalmic veins (double black) and pterygoid plexus (triple black). The horizontal segment of the ICA is labeled (blue). The dissection was located in the proximal ascending segment and the posterior genu of the cavernous ICA. After coil embolization of the cavernous sinus via a transarterial approach, the CCF has been obliterated with no evidence of abnormal venous flow.  Image courtesy of John D. Nerva, MD.

The management of CCFs depends on the etiology, clinical manifestations, radiographic findings, and risk for ophthalmic and neurological complications. Patients with asymptomatic, incidentally discovered indirect CCFs can often be safely observed with routine follow-up to assess for ophthalmologic symptoms and exam changes. Patients with mild ocular symptoms can be treated with appropriate topical medications and observed for visual acuity, intraocular pressure, or ophthalmoscopic changes. Indirect CCFs may also spontaneously resolve in some cases. Direct CCFs are rarely asymptomatic and are treated urgently.[34] For symptomatic CCFs, endovascular treatment is first line therapy with the approach to obliterate the fistulous connection (i.e. transarterial, transvenous or transorbital) dependent on arterial supply, venous drainage and pathophysiology. Despite treatment, symptoms may persist depending on severity and chronicity especially if presenting with blindness.

Direct CCFs

Direct CCFs are unlikely to close spontaneously, and upfront treatment is indicated due to the risk of neurological deficits and worsening of venous congestion. Signs for urgent treatment of direct CCFs include visual impairment, progressive paresis of extraocular muscles, intractable orbital pain, bruit, and progressive exophthalmos.[14][18] Because direct CCFs originate from a defect in the cavernous ICA either from an aneurysm rupture or dissection, the goal of treatment is to cease flow into the CS and reconstruct the cavernous ICA. There are numerous endovascular techniques utilized to achieve this end including coil embolization (Figure 5), coil embolization with balloon remodeling of the ICA and coil embolization with stent-assistance.[35][36][37] Combined transvenous and transarterial approaches can be used to preserve the ICA and pack the CS with coils to stop flow. Liquid embolics such as Onyx (ethylene vinyl alcohol copolymer, Medtronic, USA) and n-butyl cyanoacrylate glue (n-BCA, Trufill, Cerenovus, USA) are less commonly used for direct CCF due to the risk of distal embolization into cerebral arteries and stroke. A large cavernous ICA defect such as that from a traumatic transection may require ICA sacrifice as a life-sustaining treatment. Parent vessel sacrifice (endovascular occlusion) may also be option in cases of recurrence if the patient passes a balloon test occlusion. Less commonly used approaches include covered stents, packing the cavernous sinus via open microsurgery, and cavernous ICA trapping with bypass.

Indirect CCFs

Figure 6: Cerebral angiogram, ICA, lateral projection, shows an incidentally discovered Type B CCF supplied by branches of the MHT with inferior venous drainage via the basilar plexus (cavernous sinus, black arrow; horizontal segment of cavernous ICA, blue arrow). The patient presented with a ruptured brain arteriovenous malformation and was asymptomatic from the CCF. The CCF was observed with follow-up. Image courtesy of John D. Nerva, MD.

Indirect CCFs that fail conservative therapy or demonstrate progression of symptoms can be considered for endovascular treatment. Symptoms may include decreased vision, diplopia, intractable headache or bruit, or worsening proptosis with exposure keratitis can. Further, neurological deficits, intradural hemorrhage, and venous thrombosis indicate a need for more urgent treatment. While endovascular treatment is the mainstay of therapy, manual compression therapy via contralateral hand compresses has been reported to occlude indirect CCFs in up to 30% of cases.[38] Indirect CCFs may also spontaneously thrombose in up to 60% cases.[6][14]

Endovascular treatment of indirect CCFs is primarily via a transvenous route unlike treatment of direct CCF.[35][39] Transarterial embolization can be attempted if the primary fistulous connection is from branches of the ECA but fistulous connection from dural branches the ICA limits the transarterial approach due to the risk of stroke and arterial dissection with treatment. Transvenous embolization occurs via catheterization of the cavernous sinus commonly via the petrosal sinuses and pterygoid plexus and less commonly via a transorbital approach.[40][41] Embolization proceeds with detachable coils or liquid embolics (Onyx, n-BCA) to obliterate the fistula, restore normal orbital venous drainage and preserve intradural arterial flow. During transvenous embolization, the arterial circulation is monitored with intermittent angiography via the ipsilateral ICA to ensure the patency of normal cerebral vasculature.

Radiosurgery may be considered in patients with low-flow, indirect CCFs who cannot tolerate endovascular treatment or as salvage therapy for recurrent CCF with limited endovascular options.

Follow Up

A multi-disciplinary approach is often necessary under the care of neurosurgery, oculoplastic surgery and ophthalmology.

Complications

Cranial neuropathies can be seen secondary to compression secondary to mass or thrombogenic effect with coil and less commonly liquid embolization of CCFs.[42] These are typically transient with resolution within several months but can sometimes be permanent.[43] Cerebellar hemorrhage and venous infarction can also occur when liquid embolization is incomplete causing redirected flow to deeper cerebellar veins. Complications of the SOV approach for embolization include hemorrhage, superior oblique damage, CNIV damage, and infection.[44]

Prognosis

The results of embolization for direct CCFs and indirect CCFs are favorable with successful angiographic closure in up to 93% and 92%, respectively.[28][45] Direct or indirect CCFs carry a favorable visual prognosis unless there is evidence of retinal or optic nerve ischemia prior to treatment.[24] Mortality is possible with CCFs if retrograde cortical drainage is present due to the risk of intracerebral hemorrhage. Immediate improvement of intraocular pressure and resolution of an ocular bruit is often observed after successful embolization.[22] Improvement of proptosis, chemosis, and extraocular muscle enlargement is typically seen within weeks of treatment.[22][46][47] A transient “paradoxical worsening” after treatment due to an extension of cavernous sinus thrombosis to the SOV may occur and can be mitigated with corticosteroids prior to spontaneous resolution.[22] Recurrence is rare but more common in younger patients and should be suspected in a patient with recurrence of diplopia.[48]

Additional Resources

https://webeye.ophth.uiowa.edu/eyeforum/cases/111-Carotid-Cavernous-Fistula.htm

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