|Year : 2022 | Volume
| Issue : 1 | Page : 30-37
Carotico-cavernous fistula - From the eye of an ophthalmologist
Deepsekhar Das1, Mandeep S Bajaj1, Sujeeth Modaboyina1, Pallavi Singh1, Saloni Gupta2, Sahil Agrawal1
1 Oculoplasty and Paediatric Ophthalmology Services, Dr Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, New Delhi, India
2 Department of Ophthalmology, Northern Railway Central Hospital, New Delhi, India
|Date of Submission||17-Jul-2021|
|Date of Decision||28-Jan-2022|
|Date of Acceptance||07-Feb-2022|
|Date of Web Publication||22-Mar-2022|
Dr. Sahil Agrawal
Oculoplastic and Ocular Oncology Services, Dr. R.P. Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, New Delhi - 110 029
Source of Support: None, Conflict of Interest: None
Carotid-cavernous fistulas (CCFs) are spontaneous or acquired abnormal connections between the cavernous sinus and the carotid arterial system. It can be a direct connection between the cavernous segment of the internal carotid artery and the cavernous sinus, or an indirect one between the cavernous sinus, and one or more meningeal branches of the internal carotid artery, external carotid artery, or both. Ophthalmologists are called to diagnose and manage the condition in cases that present with ocular features such as decreased vision, conjunctival chemosis, external ophthalmoplegia and proptosis. A high index of suspicion in a case without any history of trauma and collagen vascular disease is the key factor. Prompt diagnosis of intravascular malformations at initial presentation can prevent ophthalmological complications and vision loss. Conventional treatments include carotid ligation and embolization, with minimal significant morbidity or mortality. A team approach including neurosurgeons, emergency physicians and ophthalmologists is needed for the proper management of such patients. Ophthalmologists may be the primary attending physician; therefore, this review aims to help understand the diagnostic approach and possible modes of treatment with expected outcomes.
Keywords: Angiography, carotico-cavernous fistula, CCF, head trauma
|How to cite this article:|
Das D, Bajaj MS, Modaboyina S, Singh P, Gupta S, Agrawal S. Carotico-cavernous fistula - From the eye of an ophthalmologist. TNOA J Ophthalmic Sci Res 2022;60:30-7
|How to cite this URL:|
Das D, Bajaj MS, Modaboyina S, Singh P, Gupta S, Agrawal S. Carotico-cavernous fistula - From the eye of an ophthalmologist. TNOA J Ophthalmic Sci Res [serial online] 2022 [cited 2022 Jul 2];60:30-7. Available from: https://www.tnoajosr.com/text.asp?2022/60/1/30/340335
| Introduction|| |
Carotid cavernous fistula (CCF) is an abnormal communication between the cavernous sinus and the carotid arterial system, resulting most commonly due to head trauma from a basal skull fracture creating a tear in the internal carotid artery (ICA) within the cavernous sinus. James Winslow coined the term 'cavernous sinus' in 1734, and Benjamin Travers described the first case of pulsating exophthalmos in 1811. In 1835, an abnormal connection between the internal carotid artery (ICA) and the cavernous sinus in a patient with pulsating exophthalmos was first reported in an autopsy report by Baron. Edward Dandy's post-mortem reports on patients with pulsating exophthalmos showed the existence of an abnormal connection between the internal carotid artery and the cavernous sinus, which could be due to an opening, severing of the artery or weakening of the wall by arteriosclerosis.
Spontaneous rupture of an atherosclerotic ICA or an existing aneurysm or spontaneous rupture of small meningeal arteries supplying the cavernous sinus's dural wall are unusual causes of CCF. The former condition is usually seen in hypertensive females of the postmenopausal age group and is associated with classic features of CCF as compared to the latter causes where there are mild signs associated with minimal or no bruit. Though CCFs may progress with time, spontaneous resolution has also been reported. A careful history taking, meticulous clinical examination and in many instances, diagnostic imaging may lead to correct and timely diagnosis. This review aims to describe ophthalmological features, classification, differential diagnoses, management and complications related to CCF.
| Methods of Literature Search|| |
An electronic search of the PubMed and Google Scholar databases was performed for the years 1980–2020 with the keywords 'Carotico-cavernous fistula' and 'CCF'. Some articles that were not found by our PubMed search were taken from the references from other articles and books. English abstracts available on PubMed were included in certain important non-English language articles on carotico-cavernous fistula.
Ophthalmic manifestations of CCFs vary widely depending on underlying aetiology, type, size, location, blood flow rate and drainage route of the CCF. The classic triad of CCF includes pulsatile exophthalmos, chemosis and orbital bruit. Patients may also describe subjective ocular bruits as a swishing or buzzing sound. For instance, CCF can present with only conjunctival chemosis, which may be misdiagnosed as conjunctivitis, and the patient may be kept on topical antibiotics for a long time. A high possibility of CCF must be considered in patients who present with corkscrew episcleral blood vessels associated with pulsating proptosis, conjunctival chemosis, thrill and bruit around the orbit [Figure 1]. Arterialization of episcleral and conjunctival blood vessels is also seen. Sometimes, CCF can mimic myasthenia gravis as the patient presents with complaints of fluctuating ptosis and diplopia.
|Figure 1: (a) A 57-year old female presented with left eye proptosis, swelling and decreased vision. (b) Further examination revealed dilated episcleral vessels and elevated intraocular pressure|
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The occurrence of CCF in children is rare, and they mostly have spontaneous onset. Acute-onset esotropia associated with proptosis is seen in CCF, attributed to the close relation of the abducens nerve with the internal carotid artery. Isolated third nerve palsy with pupil involvement has also been reported in spontaneous-onset CCF patients. However, there can be complete or incomplete third-nerve palsy with or without the pupil's involvement. The clinical features vary based on the venous drainage pattern. The anterior drainage pattern, which drains into the superior ophthalmic vein or inferior ophthalmic vein, might cause chemosis, exophthalmos or ocular bruit. This is the so-called 'red-eye shunt'. In this pattern, the sixth nerve is involved along with the third cranial nerve, and the patient may have ophthalmoplegia. The posterior drainage pattern, which drains into the superior petrosal sinus or inferior petrosal sinus, might cause isolated ocular motor nerve palsy without congestive ocular signs. This is the so-called 'white-eye shunt', which commonly remains undiagnosed and untreated because of unapparent congestive signs. Therefore, in patients with isolated cranial nerve palsies without the classic triad of CCF, imaging plays a vital role in diagnosis and early intervention.
Elevated intraocular pressures (IOP) are noted in up to 50% of patients with CCF [Figure 2]. The most common cause is open-angle glaucoma caused by increased episcleral and vortex vein pressure. The mechanism behind angle-closure glaucoma is elevated venous pressure that causes congestion and oedema of the choroid and ciliary body, thereby producing a forward displacement of the lens-iris diaphragm and, ultimately, a shallow anterior chamber. It has been proposed that CCF may lead to the development of neovascular glaucoma due to ischemia by the obstruction of venous blood flow. IOP measurement, visual field testing and optic nerve head evaluation are of paramount importance, and the patient must be closely followed up in this manner. Closure of CCF can control IOP in most cases. Trabeculectomy may be needed in cases with secondary changes or neovascularisation of angles. One may also find blood in the Schelmm's canal.
|Figure 2: A 45-year-old female presented with right-sided proptosis, mid dilated pupil, elevated intraocular pressure and dilated episcleral vessels|
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As described earlier, an increase in venous pressure may obstruct blood flow, causing ischemic changes in the retina. Retinal and choroidal changes may include venous dilatation, flame-shaped or punctate haemorrhages, sub or pre-retinal haemorrhages, vitreous haemorrhage, central retinal vein occlusion, central retinal artery occlusion and cotton wool spots. Visual impairment in CRVO is due to ischemic maculopathy, macular oedema and epiretinal membrane. When proliferative retinopathy sets in, it can result in vitreous haemorrhage and tractional retinal detachment involving the macula, contributing to vision loss. Bilateral retinal detachment, serous retinal detachment and choroidal effusion or detachment are rare complications of CCF.,,
Elevated venous pressure also affects the perfusion along the visual pathway, thereby causing vision loss. In the early phases, anoxic injury of the optic nerve occurs due to stagnant blood flow or compression injury due to distended venous sinuses. High intraocular pressure can also cause mechanical and axonal conduction block of the optic nerve. In these settings, the retina appears normal and the visual impairment is reversible on immediate intervention. Visual impairment due to exposure keratopathy can also happen due to severe proptosis in patients if topical lubricants are not used.
Classification of CCFs
There are many ways in which CCFs can be classified. These have been enumerated in [Table 1] and [Table 2].
In 1985, Barrow et al., classified CCFs into four subtypes based on their arterial system's communication pattern [Table 3], [Table 4] and [Figure 3].
|Table 3: Barrows classification[8,28] (subtypes based on their communication pattern of the arterial system)|
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|Figure 3: Carotico-cavernous fistulas as classified by Barrow. Type A direct shunting from the ICA (1) into the cavernous sinus (2). Type B and C fistulas are shunts to the cavernous sinus (2) from branches of the ICA (3) and ECA (4), respectively. Type D shunts from both the ICA and ECA simultaneously (5)|
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There are two theories behind the origin of CCF following closed head injury.,
- Based on basilar skull fracture, the first theory states that tear in the carotid artery occurs directly as a result of a bony fracture or by shear forces during the traumatic incident.
- An alternative theory is a sudden increase in the ICA's intraluminal pressure with concurrent distal artery compression, which forces the rupture of the vessel wall. The projectile or slash injuries may cause high-flow communication with the cavernous sinus as a result of the laceration of the cavernous carotid artery and thereby cause traumatic CCFs.
Although rare, iatrogenic injury during craniotomy, carotid endarterectomy, trans-sphenoidal exploration, endovascular procedures, nasopharyngeal biopsy, viridian neurectomy and trigeminal rhizotomy has been reported to cause CCFs. Mechanical thrombectomy by stent retrieval in some patients has been shown to cause acute vessel wall injury, weakening the vessel wall and likely increasing the risk for subsequent perforation or CCF. In trans-sphenoidal pituitary surgeries, even blunt instruments such as curettes can cause injury to ICA. The anterior genu of the carotid is at particular risk during the bony opening during the sellar phase, while the horizontal intra-cavernous segment is more at risk during the intra-cavernous dissection in invasive adenomas.
CCF due to spontaneous rupture of the cavernous part of ICA is seen in nearly 30% of patients. Pre-existing collagen disorders such as fibromuscular dysplasia, Ehlers–Danlos syndrome type IV or pseudoxanthoma elasticum, infective or non-infective cavernous sinus thrombosis, and aneurysm on ICA or trigeminal artery can rupture into the cavernous sinus, causing CCF. There are two theories believed behind spontaneous CCF.
- First theory: An arterial wall defect in these patients predispose them to CCF formation after minor stress, such as coughing or Valsalva manoeuvre.
- Second theory: Microscopic breaks in dural vessels to the cavernous sinus may result in fistula formation because of microscopic venous thrombosis or increases in venous sinus pressure.
Common differential diagnoses for CCF include,, arteriovenous malformation, cavernous sinus thrombosis, cavernous sinus tumours, orbital tumours, skull base tumours and mucocele, infections such as orbital cellulitis, mucormycosis, and tuberculosis, thyroid eye disease (TED), orbital pseudotumor; and orbital vasculitis resulting from Wegener's granulomatosis, PAN, intracranial sarcoidosis and Tolosa–Hunt syndrome. Due to the extensive list of differentials and varied spectrum of presentation, CCF should be included in the differential diagnosis of 'atypical' red eye.
Orbital ultrasound is a useful non-invasive modality in diagnosing CCF. The presence of a dilated superior ophthalmic vein, which appears as a hollow tubular structure with no internal echo [Figure 4] and shows an increased velocity and dilatation on colour doppler arterialisation secondary to the reversal of blood flow, hints towards CCF. Ultrasound also helps differentiate the mimickers such as graves orbitopathy, non-specific orbital inflammatory disease, orbital tumours and scleritis. Boomerang sign has also been described on a B-scan of an orbit which is a boomerang-shaped hypoechoic area along its natural course from medial to lateral side intraconally. Carotid duplex sonography (CDS) and transcranial color-coded duplex sonography (TCD) aid in detecting indirect CCFs. Fistulas are diagnosed based on identifying asymmetry in the cluster of flow in the cavernous sinus on either side. Haemodynamic changes are better correlated clinically with duplex ultrasound than by direct imaging, challenging quantise. Besides the importance of CDS and TCD in investigating CCFs, they play crucial roles in long-term follow-ups after the intervention, especially in patients with indolent symptoms, negative findings on computed tomography (CT) or magnetic resonance imaging (MRI) from the beginning, or patients complicated with aneurysms. The shortcomings of ultrasound are precise localisation and size of the fistula for which further imaging is needed.
|Figure 4: Ultrasound imaging showing a dilated superior ophthalmic vein as a hollow tubular structure with no internal echo|
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The gold-standard imaging modality is cerebral angiography [Figure 5]; however, CT or MRI shows proptosis, cavernous sinus enlargement, extraocular muscle (EOM) enlargement, superior ophthalmic vein dilation, or dilation of cortical or leptomeningeal vessels, as well as associated skull fractures, which can be suggestive of CCF., A dilated superior ophthalmic vein is often the initial finding on imaging, which can be found in 86%–100% cases on contrast-enhanced CT and in 75%–100% on T1W or post-contrast MRI [Figure 6]. Moreover, CT allows easier identification of fractures and complications such as haemorrhage, whereas MRI allows detecting abnormal flow voids within the cavernous sinus (CS). In the event of subtle or absent findings on standard spin-echo MR sequences, the detection of flow-related hyperintensity within the affected CS on MR sequences such as three-dimensional Fast Imaging with Steady State Precession (FISP) and three-dimensional time-of-flight source images is of value. The absence of abnormalities in non-invasive imaging studies does not rule out the possibility of CCF.
|Figure 5: Angiograms of a 25-year-old female with enlarged superior ophthalmic vein|
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|Figure 6: MRI showing classic features of CCF on the right side manifested as evidence of the enlargement of the superior ophthalmic vein on the axial section of a T1-weighted image (SOV) (a). Dilated signal-void serpiginous structures are seen intraconally and extending to the right cavernous sinus seen on T2-weighted MRI (b). In addition, there were enlarged extraocular muscles on the right side, as evidenced by coronal and sagittal MRI (c and d)|
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In the presence of CCF, the patient should be referred for diagnostic catheter cerebral angiography, which is performed using transfemoral arterial catheterisation with imaging of the bilateral CCAs, ICAs and ECAs, as well as the vertebral arteries. Huber manoeuvre (compression of the ipsilateral carotid artery during vertebral injection) helps in demonstrating shunting to the distal aspect of the fistula from the posterior circulation vessels. In addition, Mehringer manoeuvre (ipsilateral common carotid artery compression during ICA injection) limits the concurrent amount of unopacified blood shunting through the fistula and thus helps visualise very-high-flow CCFs.
The treatment of CCFs should be tailored as per the nature of CCF, which differs from patient to patient. As most CCFs are not life-threatening, the organ at risk in most of them is the eye.
The therapeutic methods for CCF treatment include
- Conservative management
- Endovascular intervention
- Open surgery
All direct CCFs require intervention, while only a few selected symptomatic cases of the indirect types need to be surgically treated. The main indications for treatment include glaucoma, diplopia, intolerable bruit or headache, and severe proptosis causing exposure keratopathy.
Direct CCFs previously had limited treatment options of either observation or ligating the cervical ICA proximal to the fistula and the intracranial ICA distal to the fistula or occlusion of the common carotid artery or ICA, thereby trapping it. This could result in an embolic event or an induced low-flow state, causing cerebral ischaemic events., Today, with the advent of endovascular interventional techniques, ligation is no longer an open surgical procedure, thereby preserving the ICA. This includes fistula embolization with particles (polyvinyl alcohol particles or n-BCA n-Butyl cyano-acrylate mixed with lipiodol), glue, detachable balloons and thrombogenic micro coils, best of which is the detachable balloon through an end arterial route.,,, However, in complicated cases, transvenous embolization of cavernous sinus may be safe and efficient as discussed in a study by He et al. This technique is successful in over 90% of patients; however, in 30% of cases, there may be a transient ocular motor paresis.,,,,,
The ideal route to approach such a case depends on the vascular supply and drainage, the speed with which the blood flows through the fistula, and the patency of the circle of Willis., When possible, the best approach is through the inferior petrous sinus. If not accessible, the superior ophthalmic vein approach is adopted.
Retrograde cannulation of the SOV, first proposed by Hanneken et al. in 1989, enables direct access to embolise the cavernous sinus by using platinum micro coils. However, if the SOV is thrombosed or inaccessible, the inferior ophthalmic vein (IOV) may be used. In a study by Leibovitch et al., they described technically tricky cases in which isolating or cannulating SOV for embolization was not possible. The IOV can be accessed via the inferonasal orbital space. Michels et al. catheterised the IOV to deliver multiple platinum coils to the cavernous sinus fistula. In a case of cavernous dural fistula with an anteriorly narrowed and thrombosed SOV described by Badilla et al., cannulation was performed in the deep orbit through a lateral orbitotomy.
Direct CCFs rarely undergo spontaneous closure. Spontaneous closure of dural fistulas may happen, especially after diagnostic angiography.,,, The use of iodinated contrast medium kicks off the Virchow's triad by exaggerating leukocytic accumulation, promoting red blood cell aggregation and directly affecting vascular endothelium, thereby leading to thrombosis. Spontaneous closure of direct CCF may result from slow flow due to ICA dissection leading to venous stasis and damage to the vascular endothelium of cavernous sinus by venous hypertension. Another mechanism is the absence of posterior drainage of CCF through superior and inferior petrosal sinus which may also play a role in spontaneous closure of CCF.
In patients with dural CCF with low ocular or cerebral risk, a manual carotid-jugular manipulation/compression technique several times a day for 4–6 weeks has also been successful in the closure of 17% of direct and 30% of dural CCFs,, and 20%–60% of indirect CCFs. In cases with conservative management, a close follow-up with serial visual acuity, IOP, and fundoscopic examinations is the key.
Cranial neuropathy (typically transient with resolution within several months) can be seen secondary to compression secondary to mass or thrombogenic effect with coil and less commonly liquid embolization of CCFs., Cerebellar haemorrhage and venous infarction can also occur when liquid embolization is incomplete, causing a redirected flow to deeper cerebellar veins.
Embolization of CCF via SOV carries potential risks, including difficulty in finding SOV, difficulty in determining the direction of the flow, inadvertent SOV puncture resulting in orbital haemorrhage, orbital infection, possible injury to trochlea and acute orbital congestion secondary to thrombosis of the ophthalmic veins leading to loss of vision.
Arruabarrena et al., after an attempt to close a CCF, reported complete ophthalmoplegia and vision loss due to a CRVO. Among the 80 patients treated by Preechawat et al., intra-operative complications were found in three patients, including ophthalmic artery occlusion and cerebral infarction. Ophthalmic vein thrombosis resulting in CRVO developed in three patients and severe visual deficit. Few experienced a transient aggravation of symptoms, including increased proptosis, the elevation of IOP, a choroidal detachment that required suprachoroidal drainage, and venous stasis retinopathy. Deeper orbital dissections may be avoided in those with recently diagnosed high-flow fistulas or fragile veins as it carries a higher risk of uncontrolled bleeding.
Responsibility of ophthalmologist
He/she may be the primary contact of a patient with CCF visits and is therefore crucial in making a presumptive diagnosis and instituting early treatment and referral wherever required. A history of trauma occurs in the direct type, while a picture similar to chronic conjunctivitis, orbital pseudotumor, orbital cellulitis or thyroid disease may indicate indirect CCF. Vision loss or diplopia in such patients should raise suspicion of glaucoma, besides exposure keratopathy and optic neuropathy. The ophthalmologist should document extraocular changes, fundus changes and IOP measurements at the first visit itself and keep a serial track of the same in subsequent visits. Glaucoma may be caused by iris neovascularisation due to decreased retinal perfusion or vascular engorgement and oedema of the choroid and ciliary body, causing a forward movement of the iris/lens and resulting in pupil block glaucoma., Persistent diplopia can be managed with prism therapy or occlusion of one eye, and proptosis-related keratopathy can be relieved with ocular lubrication.
A proper and timely referral to a neurologist/neurosurgeon with assistance from a neuro-ophthalmologist is must. He can also help in selecting candidates for embolization treatment and possibly assist by helping isolate the ophthalmic vein at the time of surgery. In the post-operative period, a regular follow-up to manage glaucoma, exposure keratopathy and persistent diplopia is essential. Thinda et al. reported a case of worsening angle-closure glaucoma and choroidal detachment over an extended period of 2 months after the closure of the carotid-cavernous fistula. It is also known that embolization through fragile and clotted veins can increase the risk of thrombosis.
Arriving at a direct CCF diagnosis is relatively easy based on the history and clinical presentation, especially in post-traumatic cases. However, the same may not be true in spontaneous cases. The indirect variety may be mistaken for chronic conjunctivitis, orbital pseudotumor, orbital cellulitis or thyroid disease.
A multidisciplinary approach under the care of a neurosurgeon, an ophthalmologist, a neuro-ophthalmologist and an interventional radiologist is the key.
The embolization results for direct CCFs and indirect CCFs are favourable with successful angiographic closure in up to 93% and 92%, respectively., Visual acuity, unless with retinal or optic nerve ischemia prior to treatment, has a good prognosis. An immediate decrease in IOP and bruit after successful embolization is commonly seen. However, proptosis and chemosis may take weeks to go. Mortality due to the risk of intracerebral haemorrhage is possible with CCFs if retrograde cortical drainage is present. Recurrence is rare but should be suspected in patients with recurrence of diplopia.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form the patient (s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
[Table 1], [Table 2], [Table 3], [Table 4]