(1)
Nuffield Department of Surgical Sciences, Oxford University, Oxford, UK
Preamble
In the past, students would confuse this condition with dural arteriovenous fistulas of the cavernous sinus. Happily that no longer happens because it has become obvious to nearly all that the carotid cavernous fistula is the result of the circumstance of the cavernous sinus, i.e. that a large artery runs within a venous sinus. If the artery ruptures, an arteriovenous fistula is caused. It is that simple. Why the past confusion? I assume it arose because of the similarities in symptoms and abnormal clinical findings of parients with these two types of arteriovenous shunts.
Before continuing, it is worth considering the purpose of the arrangement where an artery passes through a defined space substantially filled with venous blood. You might conclude that it is ‘asking for trouble’. The answer probably lies in comparative anatomy. The English expert in this field was the late George Du Boulay who told me that the mammalian cavernous sinus was probably a heat exchange mechanism to protect the brain, hence the panting dog cooling the upper airways and the adjacent cavernous sinuses, but then he mused on the rete mirabile of ungulates. These are found in animals that spend much of their lives grazing with their head near the ground and below the level of the heart. He thought rete help to maintain an even cerebral blood pressure. When he started to consider the situation in the giraffe, I am afraid I lost him. So, I don’t know, but please leave this tutorial recognising that the carotid cavernous fistula (CCF) is caused by a breakdown in the wall of the internal carotid artery, which normally separates its blood flow from the sinus.
11.1 Definition
A carotid cavernous fistula (CCF) consists of an abnormal connection between the cavernous segment of the internal carotid artery (ICA) and the cavernous sinus. The resulting high-flow shunt raises pressure to arterial levels, increases blood flow and dilates the sinus and its drainage pathways. Secondary venous stenosis may occur due to endothelial (mural) hyperplasia and further increase local venous pressure. Increased blood flow and venous hypertension occurs in veins of the orbit, skull base and rarely cortical veins. The cavernous sinus is the most frequent location of direct intracranial arteriovenous fistulas and they are usually caused by trauma. The fistula is primarily a direct communication between the ICA and sinus but after trauma, abnormal dural arteries of the ICA vessels may be torn in the injury or recruited as part of healing [1]. Spontaneous fistulas (i.e. no history of trauma) are caused by rupture of an aneurysm or other arterial diseases that weakens the wall of the cavernous ICA. The connection is usually a single hole or a small number of individual holes. The point of rupture in the arterial wall is often large (1–10 mm) and spontaneous cure is therefore rare.
The classification of spontaneous arteriovenous fistulas involving the cavernous sinus proposed by Barrow et al. [2], in my opinion, inappropriately includes CCF. It thus confuses them with DAVFs of the cavernous sinus region. The CCF discussed in this tutorial is a direct fistula and not a DAVF since involvement of any dural arteries is rare and due to collateral injury [1].
11.1.1 Aetiology
CCFs are traumatic (80%) or spontaneous (20%). The incidence of CCFs is difficult to quantify from the literature. An often-quoted estimate that they comprised 1/20,000 hospital admissions was made in 1956 [3], and is now irrelevant since the introduction of car seat belts and air bags has led to a dramatic fall in traumatic CCFs in European hospitals.
- (a)
Trauma
Accidental blunt trauma due to motor vehicle accidents (MVA) with direct deceleration injury to the face and cranium is the commonest history followed by falling from ladders, buildings, horses, etc. Arterial injury may occur due to penetrating injury, gunshot and other missile wounds.
Iatrogenic trauma: Iatrogenic injuries to the ICA can occur during trans-sphenoidal hypophysectomy, paranasal and other types of intracranial surgery. Endovascular treatment involving angioplasty or Fogarty catheters for endarterectomy has in the distant past been blamed for causing arterial injury and fistulas [4].
The passage of the ICA through the skull base creates bends with fixed sections below the cavernous sinus where it runs through its canal in the petrous temporal bone and foramen lacerum, and above at the dural ring where it is tightly adherent to dural. Though held within the arachnoid reflections and dura of the cavernous sinus, this ICA section is less supported and particularly prone to injury following craniofacial deceleration trauma. It is also vulnerable to trauma causing fractures (e.g. facial bones, skull base) or penetration wounds. The mechanism of arterial wall injury is thus either direct traumatic penetration, tearing of the wall or avulsion of branch arteries [5].
If the injured patient is comatose, the diagnosis of CCF may be delayed because objective signs take time to become evident or because they are initially attributed to direct traumatic soft tissue damage. Furthermore, the onset of the fistula may not necessarily occur at the time of trauma, since a traumatic pseudoaneurysm of the ICA may be caused, which later ruptures to cause a delayed fistula.
- (b)
Spontaneous
The CCF is caused by breakdown in the wall of a diseased ICA. The arterial diseases that may be responsible are:
Intracavernous aneurysm. The incidence of intracranial aneurysms in the cavernous ICA was only 1.5% in a single centre study and CCF was found in a quarter of symptomatic patients [6], and in a recent review of 316 cases of cavernous ICA aneurysms, 55 patients presented after subarachnoid haemorrhage (SAH) and 6.6% with CCFs [7]. This is probably an underestimate since it is usually difficult to demonstrate the remnants of an aneurysm without prior imaging. The presumed cause is atherosclerosis.
Ehlers–Danlos syndrome. CCF is the most common intracranial complication of this autosomal dominant abnormality of collagen metabolism. It is associated with defects in arterial media and bleeding due to increased vessel fragility. As discussed in Tutorial 8, affected people may develop intracranial aneurysms, and CCFs may be due to rupture of an intracavernous aneurysm, but when it occurs, a section of arterial wall is affected in a series of fistulas, consistent with a diseased (and weak) arterial wall [8, 9] (see Fig. 11.4).
Pseudoxanthoma elasticum. Autosomal recessive and dominant forms cause disruption of elastic fibres in the skin, arteries and eyes. It is a rare cause of G1 bleeding and CCFs [10].
Fibromuscular dysplasia. An association between fibromuscular dysplasia and CCF was first reported by Zimmerman et al [11] in 1977. They attributed it to rupture of microaneurysms. It is rare because there have only been a few case reports since.
11.1.2 Anatomy of the Cavernous Sinus
The cavernous sinus lies lateral to the pituitary gland and the body of the sphenoid bone. It extends from the superior orbital fissure to the apex of the petrous temporal bone. It is portioned by numerous fibrous strands and traversed by the cavernous portion of the ICA. The lateral wall is thicker than the medial wall (which separates it from the pituitary gland) and is formed by a double layer of dura. The oculomotor (IIIrd), trochlear (IVth) and the ophthalmic division (V1) of the trigeminal (Vth) cranial nerve run within the layers of the lateral wall. The abducens (VIth) cranial nerve runs within the sinus. Sympathetic fibres on the surface of the ICA in the sinus run with the VIth nerve in the sinus before joining V1 and passing forward into the orbit to supply ciliary muscles [12].
Anteriorly the sinus receives the superior and inferior ophthalmic veins, cerebral (uncal) veins and the sphenoparietal sinus. It communicates with the opposite cavernous sinus via a series of intercavernous sinuses, anterior and posterior to the pituitary gland. The normal outflow is to the superior and inferior petrosal sinuses, the pterygomaxillary venous plexus via emissary veins, the contralateral cavernous sinus and, depending on head position, to the superior and inferior ophthalmic veins. The VIth cranial nerve lies closest to the ICA within the inferior portion of the sinus [13] (Fig. 11.1a, b).
Fig. 11.1
Coronal illustration of the cavernous sinus in the coronal plane showing the cranial nerves and the intercavernous sinus (a). (Published with kind permission of © Henry Byrne, 2012. All rights reserved.) (b) The same view of a patient with a cavernous carotid fistula of the left side after internal carotid injection. On the left side, contrast is seen in orbital veins (white arrows) and the pterygoid plexus (short arrows). The intercavernous sinus (arrowheads) drains to the right cavernous sinus and then to the right inferior petrosal sinus
11.2 Diagnosis
11.2.1 Clinical Symptoms and Signs
The commonest presentation of a CCF is visual dysfunction and orbital congestion because the fistula is draining to orbital veins. The typical signs on examination are chemosis, exophthalmos, ocular pulsation and orbital bruit. Patients complain of bruit, diplopia, ocular pain or hypalgesia in the V1 territory. CCF may be difficult to distinguish from direct injury after trauma on ophthalmic and neurologic examinations.
Unilateral fistulas may cause bilateral orbital congestion (about 20% of cases). Localisation to the side of the fistula is usually obvious by asymmetry of proptosis or bruit (unless the SOV is thrombosed). Only 1% of traumatic fistulas are bilateral.
Occasionally, if the superior ophthalmic vein (SOV) is thrombosed or absent, orbital signs may be minimal or evident only in the contralateral eye (because venous flow is directed through intercavernous connections). Less often, sinus drainage occurs posteriorly (via the inferior petrosal sinus), laterally (via the superior petrosal sinus), inferiorly (via emissary veins of the foramen rotundum and foramen ovale to the pterygoid plexus) or superiorly (via the sphenoparietal sinus).
It is unusual for leptomeningeal and cortical veins to be involved by cortical venous reflux (CVR) but since the cavernous sinus connects to the sphenoparietal sinus, uncal veins and the petrosal sinuses, this may occur and venous pressure raised in either the superficial or deep cerebral venous systems.
The relative frequencies of common symptoms at presentation are [14]:
Subjective bruit | 80% |
Visual blurring | 59% |
Diplopia | 53% |
Headache | 53% |
Pain (ocular or orbital) | 35% |
- (a)
Bruit
The most consistent complaint in the conscious patient is bruit, which may be heard on auscultation. The site at which it is loudest gives a clue to the direction of blood flow from the cavernous sinus. Thus if the bruit is loudest over the orbit, flow is anterior and if loudest over the mastoid bone, flow is predominantly posterior. Other causes of bruit on auscultation over the orbit are dural arteriovenous fistula (DAVF), absence or hypoplasia of the sphenoid wing and transmitted sound from turbulent blood flow in carotid stenosis.
- (b)
Visual disturbance and diplopia
Visual loss caused by damage to the optic nerve at the time of trauma should be distinguished from secondary visual disturbance due to CCF. Permanent post-traumatic monocular blindness is caused by irreparable damage to the IInd cranial nerve. Otherwise, visual acuity is rarely severely affected by CCF alone. The signs are an afferent papillary defect, mild constriction of the visual fields and rarely central scotoma. The mechanism is probably a combination of compression by the enlarged SOV, and ischaemia due to the reduced arteriovenous gradient. Venous hypertension within the orbital veins causes functional changes that lead to symptoms. Most serious is secondary glaucoma caused by reduced drainage of aqueous humour and a rise in intraocular pressure (IOP) [14].
Orbital venous congestion causes:
Raised IOP: It is due to elevated pressure in episcleral veins, causing back pressure on drainage through the canals of Schlemm.1 Venous congestion of iris, ciliary muscle and ciliary body reduces the angle of the anterior chamber so narrowing the inlet to the trabecular network. About 20% of patients develop glaucoma-like visual loss and 2% severe visual failure if the IOP rises to levels that obstruct blood flow in the central artery of the retina [15].
Venous retinopathy: On fundoscopy, the veins are dilated and only rarely are disc blurring and haemorrhages evident.
Proptosis: The globe is usually displaced down and laterally by a dilated superior orbital vein (SOV). Palpable pulsation of the globe occurs in 30% and is more evident on ophthalmodynamometry.
Chemosis: Oedema of the eyelids and dilated conjunctival vessel occurs secondary to orbital venous hypertension and engorgement.
Ophthalmoplegia: This symptom is common and usually difficult to ascribe to a specific cranial nerve (see below). It may be due to swelling and ‘stiffness’ of the extraocular muscles secondary to the venous engorgement. Ophthalmoplegia caused by orbital congestion may be distinguished from cranial palsy by the forced duction test, but this is rarely indicated and contraindicated if the conjunctiva is swollen.
- (c)
Cranial nerve palsies
Damage to the orbital cranial nerves at the time of trauma can be distinguished from secondary palsies by the history and findings on initial examination. Early complete cranial nerve palsy has a poor prognosis and is usually caused by direct trauma. Palsies of the cranial nerves in the cavernous sinus are common secondary effects of CCF. The findings on examination are isolated IIIth or VIth or combined IIIth + IVth + VIth cranial nerve palsies. An isolated IVth palsy is said never to occur [14] and palsies of V1 and V2 are seen, but less often. Muscle weakness due to palsy of the trigeminal motor division is never caused by CCF alone [14]. The mechanism of palsies affecting the cavernous cranial nerves is thought to be due to interference with their blood supply in the sinus either by a steal effect or compression of their vasa nervorum by the enlarged sinus.
- (d)
Epistaxis
This is usually associated with traumatic CCF and is attributed to acute vessel injury which may or may not progress to cause a CCF [16]. The exact mechanism is often difficult to demonstrate though delayed epistaxis can be due to rupture of a traumatic pseudoaneurysm into the sphenoid or ethmoid air sinuses.
- (e)
Cerebral dysfunction
Cerebral ischaemia or infarction occurs if the CCF reduces perfusion to the hemisphere. Cerebral hypoperfusion may be seen on carotid angiography (DSA) when all the injected contrast flows to the cavernous sinus and none reaches the arteries of the circle of Willis. The ipsilateral hemisphere then depends on collateral blood flow via anterior and posterior communicating arteries. Symptoms of cerebral ischaemia or infarction occur if the collateral support is inadequate. Alternatively, venous reflux to cortical veins, i.e. cortical venous reflux (CVR), affects cerebral function and cause symptoms due to cerebral ischaemia. In this situation, CVR is evident on DSA and hyperintense signal changes may be seen on MRI. Reflux to posterior fossa veins causes brain stem symptoms [17] but symptomatic CVR is less frequent than in DAVFs of the cavernous sinus [18].
- (f)
Spontaneous intracranial haemorrhage
Intracerebral haemorrhage is rare and caused by raised venous pressure within subarachnoid or cortical veins [19]. Retrograde drainage to dural veins and the sphenoparietal sinus are relatively common, but spontaneous intracerebral haemorrhage has only been described in case reports. These have involved different sites, including the brain stem [19].
11.2.2 Imaging Diagnosis
Orbital ultrasound: This may show a dilated superior orbital vein (SOV) and disc swelling suggesting the diagnosis.
CT and CTA: Cranial CT is useful for demonstrating the extent of injury after trauma. It will demonstrate fractures around the orbit, paranasal sinuses, skull base and intra- or extra-axial haematomas or small cerebral contusions. A dilated SOV is usually well demonstrated after contrast enhancement, and the ipsilateral cavernous sinus may be enlarged (Fig. 11.2). CTA is useful in diagnosis and fistula localisation. One report found it comparable with DSA for diagnosis and superior to MRA in fistula localisation [20].
Fig. 11.2
Axial CT (a) and MRI (b) of a patient with left side proptosis due to enlarged orbital veins and soft tissue swelling. The T2W MRI shows an aneurysm in the left cavernous sinus. The fistula is the result of its rupture
MRI: It is generally not better than CT for diagnosis and is inferior for pre-operative fistula localisation. However, it will show cerebral signal changes due to CVR and is the best modality for follow-up imaging after treatment. MRA with high-frequency imaging techniques are being developed and may improve localisation of fistulas [21].
DSA: It is required to evaluate the fistula prior to endovascular treatment. Its benefit is the additional temporal resolution needed for pre-operative fistula localisation, which will be discussed below (Fig. 11.3).
